Weekly Publications

WashU weekly Neuroscience publications: July 28, 2024

Reconciling shared versus context-specific information in a neural network model of latent causes” (2024) Scientific Reports

Reconciling shared versus context-specific information in a neural network model of latent causes
(2024) Scientific Reports, 14 (1), art. no. 16782, . 

Lu, Q.a , Nguyen, T.T.b , Zhang, Q.c , Hasson, U.a , Griffiths, T.L.a d , Zacks, J.M.b , Gershman, S.J.e , Norman, K.A.a

a Department of Psychology and Princeton Neuroscience Institute, Princeton University, Princeton, United States
b Department of Psychological and Brain Sciences, Washington University in St. Louis, St. Louis, United States
c Department of Psychology and Department of Computer Science, Rutgers University, New Brunswick, United States
d Department of Computer Science, Princeton University, Princeton, United States
e Department of Psychology and Center for Brain Science, Harvard University, Cambridge, United States

Abstract
It has been proposed that, when processing a stream of events, humans divide their experiences in terms of inferred latent causes (LCs) to support context-dependent learning. However, when shared structure is present across contexts, it is still unclear how the “splitting” of LCs and learning of shared structure can be simultaneously achieved. Here, we present the Latent Cause Network (LCNet), a neural network model of LC inference. Through learning, it naturally stores structure that is shared across tasks in the network weights. Additionally, it represents context-specific structure using a context module, controlled by a Bayesian nonparametric inference algorithm, which assigns a unique context vector for each inferred LC. Across three simulations, we found that LCNet could (1) extract shared structure across LCs in a function learning task while avoiding catastrophic interference, (2) capture human data on curriculum effects in schema learning, and (3) infer the underlying event structure when processing naturalistic videos of daily events. Overall, these results demonstrate a computationally feasible approach to reconciling shared structure and context-specific structure in a model of LCs that is scalable from laboratory experiment settings to naturalistic settings. © The Author(s) 2024.

Document Type: Article
Publication Stage: Final
Source: Scopus

Targeted co-expression networks for the study of traits” (2024) Scientific Reports

Targeted co-expression networks for the study of traits
(2024) Scientific Reports, 14 (1), art. no. 16675, . 

Gómez-Pascual, A.a , Rocamora-Pérez, G.b , Ibanez, L.c d , Botía, J.A.a

a Communications Engineering and Information Department, University of Murcia, Murcia, 30100, Spain
b Department of Genetics and Genomic Medicine Research and Teaching, UCL GOS Institute of Child Health, London, WC1N 1EH, United Kingdom
c Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO 63110, United States
d Department of Neurology, Washington University School of Medicine, Saint Louis, MO 63110, United States

Abstract
Weighted Gene Co-expression Network Analysis (WGCNA) is a widely used approach for the generation of gene co-expression networks. However, networks generated with this tool usually create large modules with a large set of functional annotations hard to decipher. We have developed TGCN, a new method to create Targeted Gene Co-expression Networks. This method identifies the transcripts that best predict the trait of interest based on gene expression using a refinement of the LASSO regression. Then, it builds the co-expression modules around those transcripts. Algorithm properties were characterized using the expression of 13 brain regions from the Genotype-Tissue Expression project. When comparing our method with WGCNA, TGCN networks lead to more precise modules that have more specific and yet rich biological meaning. Then, we illustrate its applicability by creating an APP-TGCN on The Religious Orders Study and Memory and Aging Project dataset, aiming to identify the molecular pathways specifically associated with APP role in Alzheimer’s disease. Main biological findings were further validated in two independent cohorts. In conclusion, we provide a new framework that serves to create targeted networks that are smaller, biologically relevant and useful in high throughput hypothesis driven research. The TGCN R package is available on Github: https://github.com/aliciagp/TGCN. © The Author(s) 2024.

Author Keywords
Co-expression;  Genes;  LASSO;  Trait;  WGCNA

Funding details
Mayo Foundation for Medical Education and ResearchMFMER
Illinois Department of Public HealthIDPH
Translational Genomics Research InstituteTGEN
Icahn School of Medicine at Mount SinaiISMMS
Michael J. Fox Foundation for Parkinson’s ResearchMJFF
National Institute on AgingNIA
Mayo ClinicR01 AG017216, U01 AG006786, R01 AG025711, U01 AG046139, R01 AG003949, R01 AG018023, U01 AG006576, R01 AG032990, P50 AG016574
21259/FPI/19
Arizona Department of Health ServicesADHS211002
RC2AG036547, U01AG46152, R01AG36836, U01AG46161, U01AG32984, U01AG61356, RF1AG57473, R01AG48015
PID2022-136306OB-I00
R01AG15819, P30AG10161, R01AG17917, R01AG36042, R01AG30146
Arizona Biomedical Research CommissionABRC1001, 0011, 05-901, 4001
R01 NS080820
National Institute of Neurological Disorders and StrokeNINDSU24 NS072026

Document Type: Article
Publication Stage: Final
Source: Scopus

Cerebrospinal fluid-based spatial statistics: towards quantitative analysis of cerebrospinal fluid pseudodiffusivity” (2024) Fluids and Barriers of the CNS

Cerebrospinal fluid-based spatial statistics: towards quantitative analysis of cerebrospinal fluid pseudodiffusivity
(2024) Fluids and Barriers of the CNS, 21 (1), art. no. 59, . 

Chen, Y.a , Hong, H.a b , Nazeri, A.c , Markus, H.S.a , Luo, X.b

a Department of Clinical Neuroscience, University of Cambridge, Cambridge, United Kingdom
b Department of Radiology, The Second Affiliated Hospital of Zhejiang University School of Medicine, Zhejiang, Hangzhou, 310009, China
c Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, MO, United States

Abstract
Background: Cerebrospinal fluid (CSF) circulation is essential in removing metabolic wastes from the brain and is an integral component of the glymphatic system. Abnormal CSF circulation is implicated in neurodegenerative diseases. Low b-value magnetic resonance imaging quantifies the variance of CSF motion, or pseudodiffusivity. However, few studies have investigated the relationship between the spatial patterns of CSF pseudodiffusivity and cognition. Methods: We introduced a novel technique, CSF-based spatial statistics (CBSS), to automatically quantify CSF pseudodiffusivity in each sulcus, cistern and ventricle. Using cortical regions as landmarks, we segmented each CSF region. We retrospectively analyzed a cohort of 93 participants with varying degrees of cognitive impairment. Results: We identified two groups of CSF regions whose pseudodiffusivity profiles were correlated with each other: one group displaying higher pseudodiffusivity and near large arteries and the other group displaying lower pseudodiffusivity and away from the large arteries. The pseudodiffusivity in the third ventricle positively correlated with short-term memory (standardized slope of linear regression = 0.38, adjusted p < 0.001) and long-term memory (slope = 0.37, adjusted p = 0.005). Fine mapping along the ventricles revealed that the pseudodiffusivity in the region closest to the start of the third ventricle demonstrated the highest correlation with cognitive performance. Conclusions: CBSS enabled quantitative spatial analysis of CSF pseudodiffusivity and suggested the third ventricle pseudodiffusivity as a potential biomarker of cognitive impairment. © The Author(s) 2024.

Author Keywords
Cerebrospinal fluid;  Dementia;  Glymphatic system;  Intravoxel incoherent motion;  Pseudodiffusivity

Funding details
National Natural Science Foundation of ChinaNSFC82271936

Document Type: Article
Publication Stage: Final
Source: Scopus

Involvement of the choroid plexus in Alzheimer’s disease pathophysiology: findings from mouse and human proteomic studies” (2024) Fluids and Barriers of the CNS

Involvement of the choroid plexus in Alzheimer’s disease pathophysiology: findings from mouse and human proteomic studies
(2024) Fluids and Barriers of the CNS, 21 (1), art. no. 58, . 

Delvenne, A.a , Vandendriessche, C.b c , Gobom, J.d e , Burgelman, M.b c , Dujardin, P.b c , De Nolf, C.c f , Tijms, B.M.g , Teunissen, C.E.h , Schindler, S.E.i j , Verhey, F.a , Ramakers, I.a , Martinez-Lage, P.k , Tainta, M.k , Vandenberghe, R.l m , Schaeverbeke, J.l m , Engelborghs, S.n o p , De Roeck, E.n q , Popp, J.r s , Peyratout, G.r , Tsolaki, M.t , Freund-Levi, Y.u v w , Lovestone, S.x y , Streffer, J.n z , Bertram, L.aa , Blennow, K.d e ab ac , Zetterberg, H.d e ad ae af ag , Visser, P.J.a g ah , Vandenbroucke, R.E.b c , Vos, S.J.B.a

a Department of Psychiatry and Neuropsychology, Alzheimer Centrum Limburg, School for Mental Health and Neuroscience, Maastricht University, P.O. Box 616, Maastricht, 6200 MD, Netherlands
b VIB Center for Inflammation Research, VIB, Ghent, Belgium
c Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium
d Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden
e Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden
f Department of Internal Medicine and Pediatrics, Ghent University, Ghent, Belgium
g Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, Netherlands
h Neurochemistry Laboratory, Department of Clinical Chemistry, Amsterdam University Medical Centers (AUMC), Amsterdam Neuroscience, Amsterdam, Netherlands
i Department of Neurology, Washington University School of Medicine, St. Louis, United States
j Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, United States
k Fundación CITA-Alzhéimer Fundazioa, San Sebastian, Spain
l Neurology Service, University Hospitals Leuven, Louvain, Belgium
m Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Louvain, Belgium
n Reference Center for Biological Markers of Dementia (BIODEM), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium
o Department of Neurology and Bru-BRAIN, Universitair Ziekenhuis Brussel, Brussels, Belgium
p NEUR Research Group, Center for Neurosciences (C4N), Vrije Universiteit Brussel, Brussels, Belgium
q Department of Neurology and Memory Clinic, Hospital Network Antwerp (ZNA) Middelheim and Hoge Beuken, Antwerp, Belgium
r Old Age Psychiatry, University Hospital Lausanne, Lausanne, Switzerland
s Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatry University Hospital Zürich, Zurich, Switzerland
t 1st Department of Neurology, AHEPA University Hospital, Medical School, Faculty of Health Sciences, Aristotle University of Thessaloniki, Makedonia, Thessaloniki, Greece
u Department of Neurobiology, Caring Sciences and Society (NVS), Division of Clinical Geriatrics, Karolinska Institutet, Stockholm, Sweden
v Department of Psychiatry in Region Örebro County and School of Medical Sciences, Faculty of Medicine and Health, Örebro University, Örebro, Sweden
w Department of Old Age Psychiatry, Psychology & amp; Neuroscience, King’s College, London, United Kingdom
x University of Oxford, Oxford, United Kingdom
y Johnson and Johnson Medical Ltd., Wokingham, United Kingdom
z H. Lundbeck A/S, Valby, Denmark
aa Lübeck Interdisciplinary Platform for Genome Analytics, University of Lübeck, Lübeck, Germany
ab Paris Brain Institute, ICM, Pitié-Salpêtrière Hospital, Sorbonne University, Paris, France
ac Neurodegenerative Disorder Research Center, Division of Life Sciences and Medicine, and Department of Neurology, Institute on Aging and Brain Disorders, University of Science and Technology of China and First Affiliated Hospital of USTC, Hefei, China
ad Department of Neurodegenerative Disease, UCL Institute of Neurology, London, United Kingdom
ae UK Dementia Research Institute at UCL, London, United Kingdom
af Hong Kong Center for Neurodegenerative Diseases, Clear Water Bay, Hong Kong
ag Wisconsin Alzheimer’s Disease Research Center, University of Wisconsin School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53792, United States
ah Department of Neurobiology, Care Sciences and Society, Division of Neurogeriatrics, Karolinska Institutet, Stockholm, Sweden

Abstract
Background: Structural and functional changes of the choroid plexus (ChP) have been reported in Alzheimer’s disease (AD). Nonetheless, the role of the ChP in the pathogenesis of AD remains largely unknown. We aim to unravel the relation between ChP functioning and core AD pathogenesis using a unique proteomic approach in mice and humans. Methods: We used an APP knock-in mouse model, APPNL-G-F, exhibiting amyloid pathology, to study the association between AD brain pathology and protein changes in mouse ChP tissue and CSF using liquid chromatography mass spectrometry. Mouse proteomes were investigated at the age of 7 weeks (n = 5) and 40 weeks (n = 5). Results were compared with previously published human AD CSF proteomic data (n = 496) to identify key proteins and pathways associated with ChP changes in AD. Results: ChP tissue proteome was dysregulated in APPNL-G-F mice relative to wild-type mice at both 7 and 40 weeks. At both ages, ChP tissue proteomic changes were associated with epithelial cells, mitochondria, protein modification, extracellular matrix and lipids. Nonetheless, some ChP tissue proteomic changes were different across the disease trajectory; pathways related to lysosomal function, endocytosis, protein formation, actin and complement were uniquely dysregulated at 7 weeks, while pathways associated with nervous system, immune system, protein degradation and vascular system were uniquely dysregulated at 40 weeks. CSF proteomics in both mice and humans showed similar ChP-related dysregulated pathways. Conclusions: Together, our findings support the hypothesis of ChP dysfunction in AD. These ChP changes were related to amyloid pathology. Therefore, the ChP could become a novel promising therapeutic target for AD. © The Author(s) 2024.

Author Keywords
Alzheimer’s disease;  Amyloid-β (Aβ);  APP knock-in mice;  Cerebrospinal fluid;  Choroid plexus;  Proteomics

Funding details
Alzheimer’s AssociationAA
Biogen
Horizon 2020 Framework ProgrammeH2020
European CommissionEC
Seventh Framework ProgrammeFP7
ZonMw
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen ForschungSNF
Innovative Medicines InitiativeIMI
7330505021
124/16
QLRT-2001-2455, 37670
1295223N, 1195019N, 1157621N
320030_204886, P30AG06644, P01AG003991, P01AG026276, 320030_141179
733050502
115952, 806999, IMI 2 JU
101034344
115372
SAO-FRA 2021/0022
Stiftung Synapsis – Alzheimer Forschung Schweiz AFS2017-PI01
733050824736
Instituto de Salud Carlos IIIISCIIIPI15/00919
2022-01018, 2019-02397, 2023-00356
-71320, 101053962
Alzheimer NederlandWE.15-2022-01
Seventh Framework ProgrammeFP7FP7/2007-2013

Document Type: Article
Publication Stage: Final
Source: Scopus

Exploring lipin1 as a promising therapeutic target for the treatment of Duchenne muscular dystrophy” (2024) Journal of Translational Medicine

Exploring lipin1 as a promising therapeutic target for the treatment of Duchenne muscular dystrophy
(2024) Journal of Translational Medicine, 22 (1), art. no. 664, . 

Jama, A.a , Alshudukhi, A.A.a d , Burke, S.b , Dong, L.c , Kamau, J.K.a , Morris, B.a , Alkhomsi, I.A.a , Finck, B.N.e , Voss, A.A.b , Ren, H.a

a Department of Biochemistry and Molecular Biology, Wright State University, 3640 Colonel Glenn Hwy., Dayton, OH 45435-0001, United States
b Department of Biological Sciences, Wright State University, Dayton, OH, United States
c Mumetel LLC, University Technology Park at IIT, Chicago, IL, United States
d Department of Medical Laboratories, College of Applied Medical Sciences, Qassim University, Buraydah, Saudi Arabia
e Division of Geriatrics & amp; Nutritional Science, Washington University School of Medicine, St. Louis, United States

Abstract
Background: Duchenne muscular dystrophy (DMD) is a progressive and devastating muscle disease, resulting from the absence of dystrophin. This leads to cell membrane instability, susceptibility to contraction-induced muscle damage, subsequent muscle degeneration, and eventually disability and early death of patients. Currently, there is no cure for DMD. Our recent studies identified that lipin1 plays a critical role in maintaining myofiber stability and integrity. However, lipin1 gene expression levels are dramatically reduced in the skeletal muscles of DMD patients and mdx mice. Methods: To identify whether increased lipin1 expression could prevent dystrophic pathology, we employed unique muscle-specific mdx:lipin1 transgenic (mdx:lipin1Tg/0) mice in which lipin1 was restored in the dystrophic muscle of mdx mice, intramuscular gene delivery, as well as cell culture system. Results: We found that increased lipin1 expression suppressed muscle degeneration and inflammation, reduced fibrosis, strengthened membrane integrity, and resulted in improved muscle contractile and lengthening force, and muscle performance in mdx:lipin1Tg/0 compared to mdx mice. To confirm the role of lipin1 in dystrophic muscle, we then administered AAV1-lipin1 via intramuscular injection in mdx mice. Consistently, lipin1 restoration inhibited myofiber necroptosis and lessened muscle degeneration. Using a cell culture system, we further found that differentiated primary mdx myoblasts had elevated expression levels of necroptotic markers and medium creatine kinase (CK), which could be a result of sarcolemmal damage. Most importantly, increased lipin1 expression levels in differentiated myoblasts from mdx:lipin1Tg/0 mice substantially inhibited the elevation of necroptotic markers and medium CK levels. Conclusions: Overall, our data suggest that lipin1 is a promising therapeutic target for the treatment of dystrophic muscles. © The Author(s) 2024.

Author Keywords
DMD;  Dystrophin;  lipin1;  Membrane integrity;  Muscular dystrophy;  Phosphatidic acid phosphatase;  Skeletal muscle;  Therapeutic target

Funding details
5R01 AR077574, W81XWH2110679
R15 NS099850, R01 HL119225

Document Type: Article
Publication Stage: Final
Source: Scopus

Practice Variations for Therapeutic Hypothermia in Neonates with Hypoxic-ischemic Encephalopathy: An International Survey” (2024) Journal of Pediatrics

Practice Variations for Therapeutic Hypothermia in Neonates with Hypoxic-ischemic Encephalopathy: An International Survey
(2024) Journal of Pediatrics, 274, art. no. 114181, . 

Lee, K.-S.a , Massaro, A.b , Wintermark, P.c , Soul, J.d , Natarajan, G.e , Dizon, M.L.V.f , Mietzsch, U.g , Mohammad, K.h , Wu, T.-W.i , Chandel, A.j , Shenberger, J.k , DiGeronimo, R.l , Peeples, E.S.m , Hamrick, S.n , Cardona, V.Q.o , Rao, R.p , Children’s Hospitals Neonatal Consortium, the Canadian Neonatal Network, and the Newborn Brain Societyq

a Division of Neonatology, the Hospital for Sick Children, Department of Paediatrics, University of Toronto, Canada
b Division of Neonatology, Children’s National Hospital, Department of Pediatrics, The George Washington School of Medicine, Washington, DC, United States
c Division of Newborn Medicine, Department of Pediatrics, Montreal Children’s Hospital, Research Institute of the McGill University Health Centre, McGill University, Montreal, Canada
d Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, MA, United States
e Children’s Hospital of Michigan/Wayne State University, Detroit, MI, United States
f Division of Neonatology, Department of Pediatrics, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL, United States
g Division of Neonatology, Department of Pediatrics, University of Washington/Seattle Children’s Hospital, Seattle, WA, United States
h Department of Pediatrics, Section of Newborn Critical Care, University of Calgary, Cumming School of Medicine, Alberta Children’s Hospital, Calgary, Canada
i Fetal and Neonatal Institute, Division of Neonatology, Children’s Hospital Los Angeles, Department of Pediatrics, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States
j Atrium Health Wake Forest Baptist, Winston-Salem, NC, United States
k Connecticut Children’s, Hartford, CT, United States
l Division of Neonatology, Seattle Children’s Hospital, University of Washington, Seattle, WA, United States
m Division of Neonatology, Department of Pediatrics, Children’s Nebraska, University of Nebraska Medical Center, Omaha, NE, United States
n Emory University and Children’s Healthcare of Atlanta, Atlanta, GA, United States
o St Christopher’s Hospital for Children, Drexel University College of Medicine, Philadelphia, PA, United States
p Division of Newborn Medicine, Department of Pediatrics, Washington University in St. Louis, St. Louis, MO, United States

Abstract
Objective: To evaluate variations in management of therapeutic hypothermia (TH) for neonatal hypoxic-ischemic encephalopathy (HIE) among international clinical sites and to identify areas for harmonization. Study design: An electronic survey was sent to Children’s Hospitals Neonatal Consortium site sponsors, Canadian Neonatal Network site investigators, members of the Newborn Brain Society, and American Academy of Pediatrics Neonatology chiefs. Results: One hundred five sites responded, with most from high-income regions (n = 95). Groupings were adapted from the United Nations regional groups: US (n = 52 sites); Canada (n = 20); Western Europe and other states excluding Canada and US Group (WEOG, n = 18); and non-WEOG (central and eastern Europe, Asia, Africa, Latin America, and Caribbean, n = 15). Regional variations were seen in the eligibility criteria for TH, such as the minimum gestational age, grading of HIE severity, use of electroencephalography, and the frequency of providing TH for mild HIE. Active TH during transport varied among regions and was less likely in smaller volume sites. Amplitude-integrated electroencephalogram and/or continuous electroencephalogram to determine eligibility for TH was used by most sites in WEOG and non-WEOG but infrequently by the US and Canada Groups. For sedation during TH, morphine was most frequently used as first choice but there was relatively high (33%) use of dexmedetomidine in the US Group. Timing of brain magnetic resonance imaging and neurodevelopmental follow-up were variable. Neurodevelopmental follow occurred earlier and more frequently, although for a shorter duration, in the non-WEOG. Conclusions: We found significant variations in practices for TH for HIE across regions internationally. Future guidelines should incorporate resource availability in a global perspective. © 2024 Elsevier Inc.

Author Keywords
hypoxic-ischemic encephalopathy;  neonate;  therapeutic hypothermia;  variation

Document Type: Article
Publication Stage: Final
Source: Scopus

iPSC-induced neurons with the V337M MAPT mutation are selectively vulnerable to caspase-mediated cleavage of tau and apoptotic cell death” (2024) Molecular and Cellular Neuroscience

iPSC-induced neurons with the V337M MAPT mutation are selectively vulnerable to caspase-mediated cleavage of tau and apoptotic cell death
(2024) Molecular and Cellular Neuroscience, 130, art. no. 103954, . 

Theofilas, P.a , Wang, C.b , Butler, D.c , Morales, D.O.a , Petersen, C.a , Ambrose, A.j , Chin, B.d , Yang, T.d , Khan, S.e , Ng, R.e , Kayed, R.f , Karch, C.M.g , Miller, B.L.a , Gestwicki, J.E.h , Gan, L.b i , Temple, S.c , Arkin, M.R.j , Grinberg, L.T.a k

a Memory and Aging Center, Department of Neurology, UCSF, San Francisco, CA, United States
b Gladstone Institute of Neurological Disease, San Francisco, CA, United States
c Neural Stem Cell Institute, Rensselaer, NY, United States
d Shanghai ChemPartner, Shanghai, China
e ChemPartner San Francisco, South San Francisco, CA, United States
f Department of Neurology, University of Texas Medical Branch, Galveston, TX, United States
g Washington University School of Medicine, St Louis, MO, United States
h Department of Pharmaceutical Chemistry, UCSF, San Francisco, CA, United States
i Helen and Robert Appel Alzheimer’s Disease Research Institute, Brain and Mind Research Institute, Weill Cornell Medicine, New York, NY, United States
j Department of Pharmaceutical Chemistry and Small Molecule Discovery Center, UCSF, San Francisco, CA, United States
k Department of Pathology, University of Sao Paulo Medical School, Brazil

Abstract
Background: Tau post-translational modifications (PTMs) result in the gradual build-up of abnormal tau and neuronal degeneration in tauopathies, encompassing variants of frontotemporal lobar degeneration (FTLD) and Alzheimer’s disease (AD). Tau proteolytically cleaved by active caspases, including caspase-6, may be neurotoxic and prone to self-aggregation. Also, our recent findings show that caspase-6 truncated tau represents a frequent and understudied aspect of tau pathology in AD in addition to phospho-tau pathology. In AD and Pick’s disease, a large percentage of caspase-6 associated cleaved-tau positive neurons lack phospho-tau, suggesting that many vulnerable neurons to tau pathology go undetected when using conventional phospho-tau antibodies and possibly will not respond to phospho-tau based therapies. Therefore, therapeutic strategies against caspase cleaved-tau pathology could be necessary to modulate the extent of tau abnormalities in AD and other tauopathies. Methods: To understand the timing and progression of caspase activation, tau cleavage, and neuronal death, we created two mAbs targeting caspase-6 tau cleavage sites and probed postmortem brain tissue from an individual with FTLD due to the V337M MAPT mutation. We then assessed tau cleavage and apoptotic stress response in cortical neurons derived from induced pluripotent stem cells (iPSCs) carrying the FTD-related V337M MAPT mutation. Finally, we evaluated the neuroprotective effects of caspase inhibitors in these iPSC-derived neurons. Results: FTLD V337M MAPT postmortem brain showed positivity for both cleaved tau mAbs and active caspase-6. Relative to isogenic wild-type MAPT controls, V337M MAPT neurons cultured for 3 months post-differentiation showed a time-dependent increase in pathogenic tau in the form of caspase-cleaved tau, phospho-tau, and higher levels of tau oligomers. Accumulation of toxic tau species in V337M MAPT neurons was correlated with increased vulnerability to pro-apoptotic stress. Notably, this mutation-associated cell death was pharmacologically rescued by the inhibition of effector caspases. Conclusions: Our results suggest an upstream, time-dependent accumulation of caspase-6 cleaved tau in V337M MAPT neurons promoting neurotoxicity. These processes can be reversed by caspase inhibition. These results underscore the potential of developing caspase-6 inhibitors as therapeutic agents for FTLD and other tauopathies. Additionally, they highlight the promise of using caspase-cleaved tau as biomarkers for these conditions. © 2024

Author Keywords
Active caspase-6;  FTLD;  iPSCs;  Neoepitope antibody;  Postmortem;  Tau cleavage;  Tauopathies;  V337M MAPT mutation

Document Type: Article
Publication Stage: Final
Source: Scopus

Loss of function of FAM177A1, a Golgi complex localized protein, causes a novel neurodevelopmental disorder” (2024) Genetics in Medicine

Loss of function of FAM177A1, a Golgi complex localized protein, causes a novel neurodevelopmental disorder
(2024) Genetics in Medicine, 26 (9), art. no. 101166, . 

Kohler, J.N.a b r , Legro, N.R.c , Baldridge, D.d r , Shin, J.d r , Bowman, A.d , Ugur, B.e , Jackstadt, M.M.f g h , Shriver, L.P.f g h , Patti, G.J.f g h , Zhang, B.d , Feng, W.d , McAdow, A.R.d , Goddard, P.i , Ungar, R.A.i r , Jensen, T.i , Smith, K.S.j r , Fresard, L.k , Alvarez, R.a l , Bonner, D.a b r , Reuter, C.M.a b r , McCormack, C.a , Kravets, E.a r , Marwaha, S.a r , Holt, J.M.m , Acosta, M.T.r , Adam, M.r , Adams, D.R.r , Alvarez, R.L.r , Alvey, J.r , Amendola, L.r , Andrews, A.r , Ashley, E.A.a l r , Bacino, C.A.r , Bademci, G.r , Balasubramanyam, A.r , Bale, J.r , Bamshad, M.r , Barbouth, D.r , Bayrak-Toydemir, P.r , Beck, A.r , Beggs, A.H.r , Behrens, E.r , Bejerano, G.r , Bellen, H.J.r , Bennett, J.r , Berg-Rood, B.r , Bernstein, J.A.a b r , Berry, G.T.r , Bican, A.r , Bivona, S.r , Blue, E.r , Bohnsack, J.r , Botto, L.r , Boyd, B.r , Briere, L.C.r , Burke, E.A.r , Burrage, L.C.r , Butte, M.J.r , Byers, P.r , Byrd, W.E.r , Carey, J.r , Carrasquillo, O.r , Cassini, T.r , Chang, T.C.P.r , Chanprasert, S.r , Chao, H.-T.r , Chinn, I.r , Clark, G.D.r , Coakley, T.R.r , Cobban, L.A.r , Cogan, J.D.r , Coggins, M.r , Sessions Cole, F.r , Colley, H.A.r , Cope, H.r , Corner, B.r , Corona, R.r , Craigen, W.J.r , Crouse, A.B.r , Cunningham, M.r , D’Souza, P.r , Dai, H.r , Dasari, S.r , Davis, J.r , Dayal, J.G.r , Dell’Angelica, E.C.r , Dickson, P.r , Dipple, K.r , Doherty, D.r , Dorrani, N.r , Doss, A.L.r , Douine, E.D.r , Earl, D.r , Eckstein, D.J.r , Emrick, L.T.r , Eng, C.M.r , Ezell, K.r , Falk, M.r , Fieg, E.L.r , Fisher, P.G.a o r , Fogel, B.L.r , Forghani, I.r , Gahl, W.A.r , Glass, I.r , Gochuico, B.r , Goddard, P.C.r , Godfrey, R.A.r , Golden-Grant, K.r , Grajewski, A.r , Hadley, D.r , Hahn, S.r , Halley, M.C.r , Hamid, R.r , Hassey, K.r , Hayes, N.r , High, F.r , Hing, A.r , Hisama, F.M.r , Holm, I.A.r , Hom, J.r , Horike-Pyne, M.r , Huang, A.r , Hutchison, S.r , Introne, W.r , Isasi, R.r , Izumi, K.r , Jamal, F.r , Jarvik, G.P.r , Jarvik, J.r , Jayadev, S.r , Jean-Marie, O.r , Jobanputra, V.r , Karaviti, L.r , Ketkar, S.r , Kiley, D.r , Kilich, G.r , Kobren, S.N.r , Kohane, I.S.r , Korrick, S.r , Kozuira, M.r , Krakow, D.r , Krasnewich, D.M.r , Lalani, S.R.r , Lam, B.r , Lam, C.r , Lanpher, B.C.r , Lanza, I.R.r , LeBlanc, K.r , Lee, B.H.r , Levitt, R.r , Lewis, R.A.r , Liu, P.r , Liu, X.Z.r , Longo, N.r , Loo, S.K.r , Loscalzo, J.r , Maas, R.L.r , Macnamara, E.F.r , MacRae, C.A.r , Maduro, V.V.r , Maghiro, A.r , Mahoney, R.r , Malicdan, M.C.V.r , Mamounas, L.A.r , Manolio, T.A.r , Mao, R.r , Maravilla, K.r , Marom, R.r , Marth, G.r , Martin, B.A.r , Martin, M.G.r , Martínez-Agosto, J.A.r , McCauley, J.r , McConkie-Rosell, A.r , McCray, A.T.r , McGee, E.r , Mefford, H.r , Lawrence Merritt, J.r , Might, M.r , Mirzaa, G.r , Morava, E.r , Moretti, P.r , Mulvihill, J.r , Nakano-Okuno, M.r , Nelson, S.F.r , Neumann, S.r , Newman, J.H.r , Nicholas, S.K.r , Nickerson, D.r , Nieves-Rodriguez, S.r , Novacic, D.r , Oglesbee, D.r , Orengo, J.P.r , Pace, L.r , Pak, S.r , Carl Pallais, J.r , Palmer, C.G.S.r , Papp, J.C.r , Parker, N.H.r , Phillips, J.A., IIIr , Posey, J.E.r , Potocki, L.r , Pusey Swerdzewski, B.N.r , Quinlan, A.r , Rao, D.A.r , Raper, A.r , Raskind, W.r , Renteria, G.r , Rives, L.r , Robertson, A.K.r , Rodan, L.H.r , Rosenfeld, J.A.r , Rosenwasser, N.r , Rossignol, F.r , Ruzhnikov, M.r , Sacco, R.r , Sampson, J.B.r , Saporta, M.r , Schaechter, J.r , Schedl, T.r , Schoch, K.r , Scott, D.A.r , Ron Scott, C.r , Seto, E.r , Shashi, V.r , Silverman, E.K.r , Sinsheimer, J.S.r , Sisco, K.r , Smith, E.C.r , Solnica-Krezel, L.r , Solomon, B.r , Spillmann, R.C.r , Stoler, J.M.r , Sullivan, K.r , Sullivan, J.A.r , Sun, A.r , Sutton, S.r , Sweetser, D.A.r , Sybert, V.r , Tabor, H.K.r , Tan, Q.K.-G.r , Tan, A.L.M.r , Tarakad, A.r , Tekin, M.r , Telischi, F.r , Thorson, W.r , Tifft, C.J.r , Toro, C.r , Tran, A.A.r , Urv, T.K.r , Vanderver, A.r , Velinder, M.r , Viskochil, D.r , Vogel, T.P.r , Wahl, C.E.r , Walker, M.r , Wallace, S.r , Walley, N.M.r , Wambach, J.r , Wan, J.r , Wangler, M.F.r , Ward, P.A.r , Wegner, D.r , Hubshman, M.W.r , Wener, M.r , Wenger, T.r , Westerfield, M.r , Wheeler, M.T.a l r , Whitlock, J.r , Wolfe, L.A.r , Worley, K.r , Xiao, C.r , Yamamoto, S.r , Yang, J.r , Zhang, Z.r , Zuchner, S.r , Worthey, E.A.n , Montgomery, S.B.i j , Postlethwait, J.p , De Camilli, P.q , Solnica-Krezel, L.d , Undiagnosed Diseases Networks

a Stanford Center for Undiagnosed Diseases, Stanford University, Stanford, CA, United States
b Department of Pediatrics, Division of Medical Genetics, Stanford University School of Medicine, Stanford, CA, United States
c Department of Obstetrics and Gynecology, MedStar Washington Hospital Center and Georgetown University Hospital, Washington, DC, United States
d Model Organism Screening Center, Department of Developmental Biology, Washington University School of Medicine in St. Louis, St. Louis, MO, United States
e Departments of Neuroscience and of Cell Biology, Yale University School of Medicine, New Haven, CT, United States
f Department of Chemistry, Washington University in St. Louis, St. Louis, MO, United States
g Department of Medicine, Washington University in St. Louis, St. Louis, MO, United States
h Center for Proteomics, Metabolomics, Isotope Tracing, Washington University in St. Louis, St. Louis, MO, United States
i Department of Genetics, Stanford University School of Medicine, Stanford, CA, United States
j Department of Pathology, Stanford University School of Medicine, Stanford, CA, United States
k Invitae, San Francisco, CA, United States
l Division of Cardiovascular Medicine, Stanford University School of Medicine, Stanford, CA, United States
m PacBio, 1305 O’Brien Drive Menlo ParkCA, United States
n Center for Computational Genomics and Data Science, Department of Genetics, University of Alabama, Birmingham, AL, United States
o Department of Pediatrics, Division of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA, United States
p Institute of Neuroscience, University of Oregon, Eugene, OR, United States
q Departments of Neuroscience and of Cell Biology, Howard Hughes Medical Institute, Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale University School of Medicine, New Haven, CT, United States

Abstract
Purpose: The function of FAM177A1 and its relationship to human disease is largely unknown. Recent studies have demonstrated FAM177A1 to be a critical immune-associated gene. One previous case study has linked FAM177A1 to a neurodevelopmental disorder in 4 siblings. Methods: We identified 5 individuals from 3 unrelated families with biallelic variants in FAM177A1. The physiological function of FAM177A1 was studied in a zebrafish model organism and human cell lines with loss-of-function variants similar to the affected cohort. Results: These individuals share a characteristic phenotype defined by macrocephaly, global developmental delay, intellectual disability, seizures, behavioral abnormalities, hypotonia, and gait disturbance. We show that FAM177A1 localizes to the Golgi complex in mammalian and zebrafish cells. Intersection of the RNA sequencing and metabolomic data sets from FAM177A1-deficient human fibroblasts and whole zebrafish larvae demonstrated dysregulation of pathways associated with apoptosis, inflammation, and negative regulation of cell proliferation. Conclusion: Our data shed light on the emerging function of FAM177A1 and defines FAM177A1-related neurodevelopmental disorder as a new clinical entity. © 2024 American College of Medical Genetics and Genomics

Author Keywords
Developmental Delay;  FAM177A1;  Macrocephaly;  Neurodevelopment;  Zebrafish

Document Type: Article
Publication Stage: Final
Source: Scopus

Dominant missense variants in SREBF2 are associated with complex dermatological, neurological, and skeletal abnormalities” (2024) Genetics in Medicine

Dominant missense variants in SREBF2 are associated with complex dermatological, neurological, and skeletal abnormalities
(2024) Genetics in Medicine, 26 (9), art. no. 101174, . 

Moulton, M.J.a b , Atala, K.c , Zheng, Y.a b d , Dutta, D.a b , Grange, D.K.e , Lin, W.-W.a b , Wegner, D.J.e , Wambach, J.A.e , Duker, A.L.f , Bober, M.B.f , Kratz, L.g , Wise, C.A.c h i j , Oxendine, I.c , Khanshour, A.c , Bacino, C.A.k , Balasubramanyam, A.k , Burrage, L.C.k , Chao, H.-T.k , Chinn, I.k , Clark, G.D.k , Craigen, W.J.k , Dai, H.k , Emrick, L.T.k , Ketkar, S.k , Lalani, S.R.k , Lee, B.H.k , Lewis, R.A.k , Marom, R.k , Orengo, J.P.k , Posey, J.E.k , Potocki, L.k , Rosenfeld, J.A.k , Seto, E.k , Scott, D.A.k , Tarakad, A.k , Tran, A.A.k , Vogel, T.P.k , Hubshman, M.W.k , Worley, K.k , Bellen, H.J.a b k , Wangler, M.F.a b k , Yamamoto, S.a b k , Kanca, O.k , Eng, C.M.k , Liu, P.k , Ward, P.A.k , Behrens, E.k , Falk, M.k , Hassey, K.k , Izumi, K.k , Kilich, G.k , Sullivan, K.k , Vanderver, A.k , Zhang, Z.k , Raper, A.k , Jobanputra, V.k , Mikati, M.k , McConkie-Rosell, A.k , Schoch, K.k , Shashi, V.k , Spillmann, R.C.k , Tan, Q.K.-G.k , Walley, N.M.k , Beggs, A.H.k , Berry, G.T.k , Briere, L.C.k , Cobban, L.A.k , Coggins, M.k , Fieg, E.L.k , High, F.k , Holm, I.A.k , Korrick, S.k , Loscalzo, J.k , Maas, R.L.k , MacRae, C.A.k , Pallais, J.C.k , Rao, D.A.k , Rodan, L.H.k , Silverman, E.K.k , Stoler, J.M.k , Sweetser, D.A.k , Walker, M.k , Douglas, J.k , Glanton, E.k , Kobren, S.N.k , Kohane, I.S.k , LeBlanc, K.k , Maghiro, A.S.C.k , Mahoney, R.k , McCray, A.T.k , Tan, A.L.M.k , Dasari, S.k , Lanpher, B.C.k , Lanza, I.R.k , Morava, E.k , Oglesbee, D.k , Bademci, G.k , Barbouth, D.k , Bivona, S.k , Borja, N.k , Gonzalez, J.M.k , Latchman, K.k , Peart, L.S.k , Rebelo, A.k , Smith, C.A.k , Tekin, M.k , Thorson, W.k , Zuchner, S.k , Taylor, H.k , Colley, H.A.k , Dayal, J.G.k , Doss, A.L.k , Eckstein, D.J.k , Hutchison, S.k , Krasnewich, D.M.k , Mamounas, L.A.k , Manolio, T.A.k , Urv, T.K.k , Acosta, M.T.k , D’Souza, P.k , Gropman, A.k , Macnamara, E.F.k , Maduro, V.V.k , Mulvihill, J.J.k , Novacic, D.k , Pusey Swerdzewski, B.N.k , Toro, C.k , Wahl, C.E.k , Adams, D.R.k , Afzali, B.k , Burke, E.A.k , Davis, J.k , Delgado, M.k , Fu, J.k , Gahl, W.A.k , Hanchard, N.k , Huang, Y.k , Introne, W.k , Jean-Marie, O.k , Malicdan, M.C.V.k , Morimoto, M.k , Petcharet, L.k , Rossignol, F.k , Sabaii, M.k , Solomon, B.k , Tifft, C.J.k , Wolfe, L.A.k , Wood, H.k , Allworth, A.k , Bamshad, M.k , Beck, A.k , Bennett, J.k , Blue, E.k , Byers, P.k , Chanprasert, S.k , Cunningham, M.k , Dipple, K.k , Doherty, D.k , Earl, D.k , Glass, I.k , Hing, A.k , Hisama, F.M.k , Horike-Pyne, M.k , Jarvik, G.P.k , Jarvik, J.k , Jayadev, S.k , Kaitryn, E.k , Lam, C.k , Miller, D.k , Mirzaa, G.k , Raskind, W.k , Rosenthal, E.k , Shelkowitz, E.k , Sheppeard, S.k , Stergachis, A.k , Sybert, V.k , Wener, M.k , Wenger, T.k , Alvarez, R.L.k , Bejerano, G.k , Bernstein, J.A.k , Bonner, D.k , Coakley, T.R.k , Fisher, P.G.k , Goddard, P.C.k , Halley, M.C.k , Hom, J.k , Kohler, J.N.k , Kravets, E.k , Martin, B.A.k , Marwaha, S.k , Reuter, C.M.k , Ruzhnikov, M.k , Sampson, J.B.k , Smith, K.S.k , Sutton, S.k , Tabor, H.K.k , Ungar, R.A.k , Wheeler, M.T.k , Ashley, E.A.k , Byrd, W.E.k , Crouse, A.B.k , Might, M.k , Nakano-Okuno, M.k , Whitlock, J.k , Butte, M.J.k , Corona, R.k , Dell’Angelica, E.C.k , Dorrani, N.k , Douine, E.D.k , Fogel, B.L.k , Huang, A.k , Krakow, D.k , Loo, S.K.k , Martin, M.G.k , Martínez-Agosto, J.A.k , McGee, E.k , Nelson, S.F.k , Nieves-Rodriguez, S.k , Papp, J.C.k , Parker, N.H.k , Renteria, G.k , Sinsheimer, J.S.k , Wan, J.k , Alvey, J.k , Andrews, A.k , Bale, J.k , Bohnsack, J.k , Botto, L.k , Carey, J.k , Longo, N.k , Moretti, P.k , Pace, L.k , Quinlan, A.k , Velinder, M.k , Viskochil, D.k , Marth, G.k , Bayrak-Toydemir, P.k , Mao, R.k , Westerfield, M.k , Bican, A.k , Cassini, T.k , Corner, B.k , Hamid, R.k , Neumann, S.k , Phillips, J.A., IIIk , Rives, L.k , Robertson, A.K.k , Ezell, K.k , Cogan, J.D.k , Hayes, N.k , Kiley, D.k , Sisco, K.k , Wambach, J.k , Wegner, D.k , Baldridge, D.k , Cole, F.S.e k , Pak, S.k , Schedl, T.k , Shin, J.k , Solnica-Krezel, L.k , Rios, J.c h i j , Undiagnosed Diseases Networkl


a Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, United States
b Jan and Dan Duncan Neurological Research Institute, Texas Children’s Hospital, Houston, TX, United States
c Center for Translational Research, Scottish Rite for Children, Dallas, TX, United States
d Current address: State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen University, Xiamen, China
e Edward Mallinckrodt Department of Pediatrics, Washington University in St. Louis School of Medicine and St. Louis Children’s Hospital, St. Louis, MO, United States
f Skeletal Dysplasia Program, Orthogenetics, Nemours Children’s Hospital, Wilmington, DE, United States
g Kennedy Krieger Institute, Department of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, United States
h Eugene McDermott Center for Human Growth and Development, University of Texas Southwestern Medical Center, Dallas, TX, United States
i Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, United States
j Department of Orthopedic Surgery, University of Texas Southwestern Medical Center, Dallas, TX, United States

Abstract
Purpose: We identified 2 individuals with de novo variants in SREBF2 that disrupt a conserved site 1 protease (S1P) cleavage motif required for processing SREBP2 into its mature transcription factor. These individuals exhibit complex phenotypic manifestations that partially overlap with sterol regulatory element binding proteins (SREBP) pathway-related disease phenotypes, but SREBF2-related disease has not been previously reported. Thus, we set out to assess the effects of SREBF2 variants on SREBP pathway activation. Methods: We undertook ultrastructure and gene expression analyses using fibroblasts from an affected individual and utilized a fly model of lipid droplet (LD) formation to investigate the consequences of SREBF2 variants on SREBP pathway function. Results: We observed reduced LD formation, endoplasmic reticulum expansion, accumulation of aberrant lysosomes, and deficits in SREBP2 target gene expression in fibroblasts from an affected individual, indicating that the SREBF2 variant inhibits SREBP pathway activation. Using our fly model, we discovered that SREBF2 variants fail to induce LD production and act in a dominant-negative manner, which can be rescued by overexpression of S1P. Conclusion: Taken together, these data reveal a mechanism by which SREBF2 pathogenic variants that disrupt the S1P cleavage motif cause disease via dominant-negative antagonism of S1P, limiting the cleavage of S1P targets, including SREBP1 and SREBP2. © 2024 American College of Medical Genetics and Genomics

Author Keywords
Drosophila;  Lipid droplet;  S1P;  SREBF1;  SREBF2

Funding details
University of Texas Southwestern Medical CenterUTSW
Baylor College of Medicine
National Institutes of HealthNIHU54D083092
National Institutes of HealthNIH
U01 HG010215, U01 NS13454, T32 NS043124-19
OD R24 OD022005, U54 NS093793
R01 AG073260, U01 AG072439

Document Type: Article
Publication Stage: Final
Source: Scopus

Temporal Trends and Racial Disparities in Long-Term Survival After Stroke” (2024) Neurology

Temporal Trends and Racial Disparities in Long-Term Survival After Stroke
(2024) Neurology, 103 (3), p. e209653. Cited 1 time.

Robinson, D.J., Ding, L., Howard, G., Stanton, R.J., Khoury, J., Sucharew, H., Haverbusch, M., Nobel, L., Khatri, P., Adeoye, O., Broderick, J.P., Ferioli, S., Mackey, J., Woo, D., Rios La Rosa, F.L., Flaherty, M., Slavin, S., Star, M., Martini, S.R., Demel, S., Walsh, K.B., Coleman, E., Jasne, A.S., Mistry, E.A., Kleindorfer, D., Kissela, B.

From the Department of Neurology and Rehabilitation Medicine (D.R., R.J.S., M.H., L.N., P.K., J.P.B., S.F., D.W., M.L.F., S.D., E.A.M., B.K.), University of Cincinnati, OH; Department of Biostatistics (L.D., J.C.K.), Cincinnati Children’s Medical Center, OH; Department of Biostatistics (G.H.), University of Alabama at Birmingham School of Public Health, AL; Department of Emergency Medicine (H.S., K.B.W.), University of Cincinnati, OH; Department of Emergency Medicine (O.A.), Washington University, St. Louis, MO; Department of Neurology (J.M.), Indiana University School of Medicine, Indianapolis; Miami Neuroscience Institute (F.D.L.R.L.R.), Baptist Health South Florida, Miami; Department of Neurology (S.S.), University of Kansas Medical Center, Kansas City; Department of Neurology (M.S.), Soroka Medical Center, Beersheva, Israel; VA National TeleStroke Program (S.R.M.), Veterans Health Administration, Houston, TX; Department of Neurology (E.C.), University of Chicago, IL; Department of Neurology (A.S.J.), Yale University, New Haven, CT; and Department of Neurology (D.K.), University of Michigan, Ann Arbor

Abstract
BACKGROUND AND OBJECTIVES: Few studies have examined trends and disparities in long-term outcome after stroke in a representative US population. We used a population-based stroke study in the Greater Cincinnati Northern Kentucky region to examine trends and racial disparities in poststroke 5-year mortality. METHODS: All patients with acute ischemic strokes (AISs) and intracerebral hemorrhages (ICHs) among residents ≥20 years old were ascertained using ICD codes and physician-adjudicated using a consistent case definition during 5 periods: July 1993-June 1994 and calendar years 1999, 2005, 2010, and 2015. Race was obtained from the medical record; only those identified as White or Black were included. Premorbid functional status was assessed using the modified Rankin Scale, with a score of 0-1 being considered “good.” Mortality was assessed with the National Death Index. Trends and racial disparities for each subtype were analyzed with logistic regression. RESULTS: We identified 8,428 AIS cases (19.3% Black, 56.3% female, median age 72) and 1,501 ICH cases (23.5% Black, 54.8% female, median age 72). Among patients with AIS, 5-year mortality improved after adjustment for age, race, and sex (53% in 1993/94 to 48.3% in 2015, overall effect of study year p = 0.009). The absolute decline in 5-year mortality in patients with AIS was larger than what would be expected in the general population (5.1% vs 2.8%). Black individuals were at a higher risk of death after AIS (odds ratio [OR] 1.23, 95% CI 1.08-1.39) even after adjustment for age and sex, and this effect was consistent across study years. When premorbid functional status and comorbidities were included in the model, the primary effect of Black race was attenuated but race interacted with sex and premorbid functional status. Among male patients with a good baseline functional status, Black race remained associated with 5-year mortality (OR 1.4, 95% CI 1.1-1.7, p = 0.002). There were no changes in 5-year mortality after ICH over time (64.4% in 1993/94 to 69.2% in 2015, overall effect of study year p = 0.32). DISCUSSION: Long-term survival improved after AIS but not after ICH. Black individuals, particularly Black male patients with good premorbid function, have a higher mortality after AIS, and this disparity did not change over time.

Document Type: Article
Publication Stage: Final
Source: Scopus

Multicenter Registry of Adenomas of the Pituitary and Related Disorders: Initial Description of Cushing Disease Cohort, Surgical Outcomes, and Surgeon Characteristics” (2024) Neurosurgery

Multicenter Registry of Adenomas of the Pituitary and Related Disorders: Initial Description of Cushing Disease Cohort, Surgical Outcomes, and Surgeon Characteristics
(2024) Neurosurgery, 95 (2), pp. 372-379. 

Little, A.S.a , Karsy, M.b , Evans, J.J.c , Kim, W.d , Pacione, D.R.e , Kim, A.H.f , Gardner, P.A.g , Hendricks, B.K.a , Sarris, C.E.a , Torok, I.E.a , Low, T.M.a , Crocker, T.A.a , Valappil, B.g , Kanga, M.f , Abdallah, H.g , Collopy, S.c , Fernandez-Miranda, J.C.h , Vigo, V.h , Ljubimov, V.A.h , Zada, G.i , Garrett, N.E., 3rdi , Delery, W.d , Yuen, K.C.J.a , Rennert, R.C.j , Couldwell, W.T.j , Silverstein, J.M.k , Kshettry, V.R.l , Chicoine, M.R.m , RAPID Consortiumn

a Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, AZ, United States
b Department of Neurosurgery, Drexel University College of Medicine, Drexel University, Philadelphia, PA, United States
c Department of Neurosurgery, Jefferson University, Philadelphia, PA, United States
d Department of Neurosurgery, University of California, Los Angeles, CA, United States
e Department of Neurosurgery, New York UniversityNY, United States
f Department of Neurosurgery, Washington University School of Medicine, St Louis, MO, United States
g Department of Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, PA, United States
h Department of Neurosurgery, Stanford University, Palo Alto, CA, United States
i Department of Neurosurgery, University of Southern California, Los Angeles, CA, United States
j Department of Neurosurgery, University of Utah, Salt Lake City, UT, United States
k Division of Endocrinology, Metabolism and Lipid Research, Washington University School of Medicine, St Louis, MO, United States
l Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, OH, United States
m Department of Neurosurgery, University of Missouri, Columbia, MO, United States

Abstract
BACKGROUND AND OBJECTIVES: To address the lack of a multicenter pituitary surgery research consortium in the United States, we established the Registry of Adenomas of the Pituitary and Related Disorders (RAPID). The goals of RAPID are to examine surgical outcomes, improve patient care, disseminate best practices, and facilitate multicenter surgery research at scale. Our initial focus is Cushing disease (CD). This study aims to describe the current RAPID patient cohort, explore surgical outcomes, and lay the foundation for future studies addressing the limitations of previous studies. METHODS: Prospectively and retrospectively obtained data from participating sites were aggregated using a cloud-based registry and analyzed retrospectively. Standard preoperative variables and outcome measures included length of stay, unplanned readmission, and remission. RESULTS: By July 2023, 528 patients with CD had been treated by 26 neurosurgeons with varying levels of experience at 9 academic pituitary centers. No surgeon treated more than 81 of 528 (15.3%) patients. The mean ± SD patient age was 43.8 ± 13.9 years, and most patients were female (82.2%, 433/527). The mean tumor diameter was 0.8 ± 2.7 cm. Most patients (76.6%, 354/462) had no prior treatment. The most common pathology was corticotroph tumor (76.8%, 381/496). The mean length of stay was 3.8 ± 2.5 days. The most common discharge destination was home (97.2%, 513/528). Two patients (0.4%, 2/528) died perioperatively. A total of 57 patients (11.0%, 57/519) required an unplanned hospital readmission within 90 days of surgery. The median actuarial disease-free survival after index surgery was 8.5 years. CONCLUSION: This study examined an evolving multicenter collaboration on patient outcomes after surgery for CD. Our results provide novel insights on surgical outcomes not possible in prior single-center studies or with national administrative data sets. This collaboration will power future studies to better advance the standard of care for patients with CD. Copyright © Congress of Neurological Surgeons 2024. All rights reserved.

Document Type: Article
Publication Stage: Final
Source: Scopus

A Reinterpretation of the Relationship between Persistent and Resurgent Sodium Currents” (2024) Journal of Neuroscience

A Reinterpretation of the Relationship between Persistent and Resurgent Sodium Currents
(2024) Journal of Neuroscience, 44 (29), art. no. e2396232024, . 

Brown, S.P.a , Lawson, R.J.a , Moreno, J.D.b , Ransdell, J.L.a

a Department of Biology, Miami University, Oxford, OH 45056, United States
b Division of Cardiology, Department of Medicine, Washington University in St. Louis, St. Louis, MO 63130, United States

Abstract
The resurgent sodium current (INaR) activates on membrane repolarization, such as during the downstroke of neuronal action potentials. Due to its unique activation properties, INaR is thought to drive high rates of repetitive neuronal firing. However, INaR is often studied in combination with the persistent or noninactivating portion of sodium currents (INaP). We used dynamic clamp to test how INaR and INaP individually affect repetitive firing in adult cerebellar Purkinje neurons from male and female mice. We learned INaR does not scale repetitive firing rates due to its rapid decay at subthreshold voltages and that subthreshold INaP is critical in regulating neuronal firing rate. Adjustments to the voltage-gated sodium conductance model used in these studies revealed INaP and INaR can be inversely scaled by adjusting occupancy in the slow-inactivated kinetic state. Together with additional dynamic clamp experiments, these data suggest the regulation of sodium channel slow inactivation can fine-tune INaP and Purkinje neuron repetitive firing rates. Copyright © 2024 the authors.

Author Keywords
dynamic clamp;  intrinsic excitability;  membrane excitability;  persistent sodium;  resurgent sodium;  sodium channel

Funding details
University of Memphis – College of Arts and Sciences
National Institutes of HealthNIH1R15NS125560

Document Type: Article
Publication Stage: Final
Source: Scopus

Endoscopic endonasal optic nerve decompression in children younger than 2 years old with congenital optic canal stenosis: illustrative cases” (2024) Journal of Neurosurgery: Case Lessons

Endoscopic endonasal optic nerve decompression in children younger than 2 years old with congenital optic canal stenosis: illustrative cases
(2024) Journal of Neurosurgery: Case Lessons, 8 (2), art. no. CASE23559, . 

Yang, P.H.a , Schneider, J.S.b , Chicoine, M.R.c , Kim, A.H.a , Limbrick, D.D., Jr.d

a Departments of Neurological Surgery, Washington University in St. Louis, St. Louis, MO, United States
b Departments of Otolaryngology, Washington University in St. Louis, St. Louis, MO, United States
c Department of Neurological Surgery, University of Missouri, Columbia, MO, United States
d Department of Neurological Surgery, Virginia Commonwealth University, Richmond, VA, United States

Abstract
BACKGROUND Congenital optic canal stenosis causing compressive optic neuropathy is a rare disorder that presents unique diagnostic and treatment challenges. Endoscopic endonasal optic nerve decompression (EOND) has been described for optic nerve compression in adults and adolescents but has never been reported for young children without pneumatized sphenoid sinuses. The authors describe preoperative and intraoperative considerations for three patients younger than 2 years of age with congenital optic canal stenosis due to genetically confirmed osteopetrosis or chondrodysplasia. OBSERVATIONS Serial ophthalmological examinations, with a particular focus on object tracking ability, fundoscopic examination, and visual evoked potential trends in preverbal children, are important for detecting progressive optic neuropathy. The lack of pneumatization of the sphenoid sinus presents unique challenges and requires the surgical creation of a sphenoid sinus with the use of neuronavigation to determine the limits of bony exposure given the lack of easily identifiable anatomical landmarks such as the opticocarotid recess. There were no perioperative complications. LESSONS EOND for congenital optic canal stenosis is safe and technically feasible even given the lack of pneumatization of the sphenoid sinus in young patients. The key operative step is surgically creating the sphenoid sinus through careful bony removal with the aid of neuronavigation. © 2024 The authors.

Author Keywords
case report;  endoscopic endonasal transsphenoidal approach;  optic canal;  optic nerve decompression;  pediatric

Document Type: Article
Publication Stage: Final
Source: Scopus

Dural Arteriovenous Fistulas With Cognitive Impairment: Angiographic Characteristics and Treatment Outcomes” (2024) Neurosurgery

Dural Arteriovenous Fistulas With Cognitive Impairment: Angiographic Characteristics and Treatment Outcomes
(2024) Neurosurgery, 94 (5), pp. 1035-1043. 

Sanchez, S.a , Wendt, L.b , Hayakawa, M.c , Chen, C.-J.e , Sheehan, J.P.f , Kim, L.J.g , Abecassis, I.J.g , Levitt, M.R.g , Meyer, R.M.g , Guniganti, R.h , Kansagra, A.P.i , Lanzino, G.j , Giordan, E.j , Brinjikji, W.k , Bulters, D.O.l , Durnford, A.l , Fox, W.C.m , Smith, J.n , Polifka, A.J.n , Gross, B.o , Amin-Hanjani, S.p v , Alaraj, A.p , Kwasnicki, A.p , Starke, R.M.q , Chen, S.H.q , Van Dijk, J.M.C.r , Potgieser, A.R.E.r , Satomi, J.s , Tada, Y.s , Phelps, R.t , Abla, A.t , Winkler, E.t , Du, R.u , Rosalind Lai, P.M.u , Ortega-Gutierrez, S.a c d , Zipfel, G.J.h , Derdeyn, C.b , Samaniego, E.A.a c d

a Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
b Institute for Clinical and Translational Science, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
c Department of Radiology, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
d Department of Neurosurgery, University of Iowa Hospitals and Clinics, Iowa City, IA, United States
e Department of Neurosurgery, The University of Texas Health Science Center at Houston, Houston, TX, United States
f Department of Neurosurgery, University of Virginia Health System, Charlottesville, VA, United States
g Department of Neurosurgery, University of Washington, Seattle, WA, United States
h Department of Neurosurgery, Washington University School of Medicine in Saint Louis, St. Louis, MO, United States
i Mallinckrodt Institute of Radiology, Washington University School of Medicine in Saint Louis, St. Louis, MO, United States
j Department of Neurosurgery, Mayo Clinic Hospital, Rochester, MN, United States
k Department of Radiology, Mayo Clinic Hospital, Rochester, MN, United States
l Department of Neurosurgery, University Hospital Southampton, Nhs Foundation Trust, Southampton, United Kingdom
m Department of Neurosurgery, Mayo Clinic, Jacksonville, FL, United States
n Department of Neurosurgery, University of Florida, Gainesville, FL, United States
o Department of Neurosurgery, University of Pittsburgh Medical Center Health System, Pittsburgh, PA, United States
p Department of Neurosurgery, University of Illinois Chicago, Chicago, IL, United States
q Department of Neurosurgery, University of Miami, Coral Gables, FL, United States
r Department of Neurosurgery, University of Groningen, Groningen, Netherlands
s Department of Neurosurgery, Tokushima University Hospital, Tokushima, Japan
t Department of Neurosurgery, University of California San Francisco, San Francisco, CA, United States
u Department of Neurosurgery, Brigham and Women’s Hospital, Boston, MA, United States
v Department of Neurosurgery, University Hospitals Cleveland Medical Center, Case Western Reserve University School of Medicine, Cleveland, OH, United States

Abstract
BACKGROUND AND OBJECTIVES: Anecdotal cases of rapidly progressing dementia in patients with dural arteriovenous fistulas (dAVFs) have been reported in small series. However, large series have not characterized these dAVFs. We conducted an analysis of the largest cohort of dAVFs presenting with cognitive impairment (dAVFs-CI), aiming to provide a detailed characterization of this subset of dAVFs. METHODS: Patients with dAVFs-CI were analyzed from the CONDOR Consortium, a multicenter repository comprising 1077 dAVFs. A propensity score matching analysis was conducted to compare dAVFs-CI with Borden type II and type III dAVFs without cognitive impairment (controls). Logistic regression was used to identify angiographic characteristics specific to dAVFs-CI. Furthermore, post-treatment outcomes were analyzed. RESULTS: A total of 60 patients with dAVFs-CI and 60 control dAVFs were included. Outflow obstruction leading to venous hypertension was observed in all dAVFs-CI. Sinus stenosis was significantly associated with dAVFs-CI (OR 2.85, 95% CI: 1.16-7.55, P =.027). dAVFs-CI were more likely to have a higher number of arterial feeders (OR 1.56, 95% CI 1.22-2.05, P <.001) and draining veins (OR 2.05, 95% CI 1.05-4.46, P =.004). Venous ectasia increased the risk of dAVFs-CI (OR 2.38, 95% CI 1.13-5.11, P =.024). A trend toward achieving asymptomatic status at follow-up was observed in patients with successful closure of dAVFs (OR 2.86, 95% CI 0.85-9.56, P =.09) CONCLUSION: Venous hypertension is a key angiographic feature of dAVFs-CI. Moreover, these fistulas present at a mean age of 58 years-old, and exhibit a complex angioarchitecture characterized by an increased number of arteriovenous connections and stenosed sinuses. The presence of venous ectasia further exacerbates the impaired drainage and contributes to the development of dAVFs-CI. Notably, in certain cases, closure of the dAVF has the potential to reverse symptoms. © 2024 Wolters Kluwer Medknow Publications. All rights reserved.

Author Keywords
Dementia;  Fistula;  Intervention

Document Type: Article
Publication Stage: Final
Source: Scopus

The involvement of the piriform cortex in non-lesional temporal lobe epilepsy: An uncommon component of the epileptogenic network” (2024) Brain Communications

The involvement of the piriform cortex in non-lesional temporal lobe epilepsy: an uncommon component of the epileptogenic network
(2024) Brain Communications, 6 (4), art. no. fcae179, . 

Pedersen, N.P.a b , Raghu, A.c , Shivamurthy, V.K.N.d , Chern, J.J.c e , Gross, R.E.c , Willie, J.T.f , Dingledine, R.J.g , Kheder, A.b e

a Department of Neurology, UC Davis Comprehensive Epilepsy Center, University of California, Davis School of Medicine, Center for Neuroscience, Davis, CA 95618, United States
b Department of Neurology, Emory University, School of Medicine, Atlanta, GA 30322, United States
c Department of Neurosurgery, Emory University, School of Medicine, Atlanta, GA 30322, United States
d Department of Neurology, Saint Francis Hospital and Medical Center, Trinity Health of New England, Hartford, CT 06105, United States
e Epilepsy Center, Children’s Healthcare of Atlanta, Atlanta, GA 30342, United States
f Department of Neurological Surgery, Washington University, School of Medicine, St. Louis, MO 63110, United States
g Department of Pharmacology and Chemical Biology, Emory University, School of Medicine, Atlanta, GA 30322, United States

Abstract
The piriform cortex is recognized as highly epileptogenic in rodents, yet its electrophysiological role in human epilepsy remains understudied. Recent surgical outcomes have suggested potential benefits in resecting the piriform cortex for cases of medial temporal lobe epilepsy. However, little is known about its electrophysiological activity in human epilepsy. This case-series study aimed to explore the electrophysiological role of the piriform cortex within the epileptogenic network among patients with suspected temporal lobe epilepsy. Participants were recruited from Emory University Hospital or Children’s Healthcare of Atlanta, with non-lesional frontotemporal or temporal lobe hypotheses, undergoing stereoelectroencephalographic studies. Specifically, focus was placed on patients with one or more electrode contacts in the piriform cortex. Primary objectives included determining piriform cortex involvement within the electrophysiologically defined epileptogenic network and assessing the effects of electrical stimulation. Twenty-two patients were included in the study. Notably, only one patient exhibited piriform cortex involvement at seizure onset, associated with an olfactory aura. Two patients showed early piriform cortex involvement, while others displayed late or no involvement. Electrical stimulation of the piriform cortex induced after-discharges in three patients and replicated a habitual seizure in one. These findings present a contrast to surgical outcome studies, suggesting that the piriform cortex may not typically play a significant role in the epileptogenic network among patients with non-lesional temporal lobe epilepsy. © 2024 The Author(s).

Author Keywords
olfactory aura;  piriform cortex;  SEEG;  stereo-electroencephalography;  temporal lobe epilepsy

Document Type: Article
Publication Stage: Final
Source: Scopus

Predicting continuous amyloid PET values with CSF tau phosphorylation occupancies” (2024) Alzheimer’s and Dementia

Predicting continuous amyloid PET values with CSF tau phosphorylation occupancies
(2024) Alzheimer’s and Dementia, . 

Wisch, J.K.a , Gordon, B.A.b c , Barthélemy, N.R.a d , Horie, K.a d , Henson, R.L.e , He, Y.a d , Flores, S.b , Benzinger, T.L.S.b c , Morris, J.C.a c , Bateman, R.J.a c d e , Ances, B.M.a c , Schindler, S.E.a c e

a Department of Neurology, Washington University in St. Louis, St. Louis, MO, United States
b Department of Radiology, Washington University in St. Louis, St. Louis, MO, United States
c Knight Alzheimer Disease Research Center, Washington University School of Medicine, St Louis, MO, United States
d SILQ Center for Neurodegenerative Biology, St. Louis, MO, United States
e Hope Center, Washington University in Saint Louis, St. Louis, MO, United States

Abstract
INTRODUCTION: Cerebrospinal fluid (CSF) tau phosphorylation at multiple sites is associated with cortical amyloid and other pathologic changes in Alzheimer’s disease. These relationships can be non-linear. We used an artificial neural network to assess the ability of 10 different CSF tau phosphorylation sites to predict continuous amyloid positron emission tomography (PET) values. METHODS: CSF tau phosphorylation occupancies at 10 sites (including pT181/T181, pT217/T217, pT231/T231 and pT205/T205) were measured by mass spectrometry in 346 individuals (57 cognitively impaired, 289 cognitively unimpaired). We generated synthetic amyloid PET scans using biomarkers and evaluated their performance. RESULTS: Concentration of CSF pT217/T217 had low predictive error (average error: 13%), but also a low predictive range (ceiling 63 Centiloids). CSF pT231/T231 has slightly higher error (average error: 19%) but predicted through a greater range (87 Centiloids). DISCUSSION: Tradeoffs exist in biomarker selection. Some phosphorylation sites offer greater concordance with amyloid PET at lower levels, while others perform better over a greater range. Highlights: Novel pTau isoforms can predict cortical amyloid burden. pT217/T217 accurately predicts cortical amyloid burden in low-amyloid individuals. Traditional CSF biomarkers correspond with higher levels of amyloid. © 2024 The Author(s). Alzheimer’s & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer’s Association.

Author Keywords
biomarker concordance;  CSF tau occupancy;  machine learning;  novel biomarkers;  PET

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Insufficient evidence for an association between iatrogenic Alzheimer’s disease and cadaveric pituitary-derived growth hormone” (2024) Alzheimer’s and Dementia

Insufficient evidence for an association between iatrogenic Alzheimer’s disease and cadaveric pituitary-derived growth hormone
(2024) Alzheimer’s and Dementia, . 

Nath, A.a , Holtzman, D.M.b , Miller, B.L.c , Grinberg, L.T.c , Leschek, E.W.d

a National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, United States
b Department of Neurology, Hope Center for Neurological Disorders, Knight Alzheimer’s Disease Research Center, Washington University School of Medicine, St. Louis, MO, United States
c UCSF Weill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United States
d National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, United States

Abstract
A Nature Medicine paper published in January 2024 describes eight cases of iatrogenic Alzheimer’s disease in individuals who received cadaveric pituitary-derived human growth hormone. The paper’s conclusions argue for the transmissibility of Alzheimer’s disease, which, if true, would create a significant public health crisis. For example, neurosurgical practices would require substantial revision, and many individuals who have undergone neurosurgical procedures would now be at considerable risk of Alzheimer’s disease. A detailed review of the presented cases reveals that they do not have Alzheimer’s disease, and there are alternative explanations for the cognitive decline described. In people with progressive cognitive decline, the diagnosis of Alzheimer’s disease requires a demonstration of amyloid and tau pathology or amyloid and tau biomarkers. Extensive tau pathology is not demonstrated, and some also lack amyloid beta pathology. The cases described in this paper do not meet the criteria for dementia due to Alzheimer’s disease by clinical and pathological standards. Highlights: Creutzfeldt-Jakob disease has been transmitted by cadaveric growth hormone. There is no evidence for the transmission of Alzheimer’s disease by cadaveric growth hormone. There is no evidence that Alzheimer’s disease is transmissible. Published 2024. This article is a U.S. Government work and is in the public domain in the USA. Alzheimer’s & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer’s Association.

Author Keywords
Alzheimer’s disease;  amyloid-beta;  cadaveric pituitary-derived human growth hormone;  cerebral amyloid angiopathy;  Creutzfeldt-Jakob disease;  dementia;  tau

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Low-Dose Interleukin-2 Reverses Traumatic Brain Injury-Induced Cognitive Deficit and Pain” (2024) Annals of Neurology

Low-Dose Interleukin-2 Reverses Traumatic Brain Injury-Induced Cognitive Deficit and Pain
(2024) Annals of Neurology, . 

Czerpaniak, K., do Nascimento, L.F., Guo, T., Zhang, J., Liu, X., Sarzaeim, M., Fine, Z.D., Cao, Y.-Q.

Department of Anesthesiology and Washington University Pain Center, Washington University in St Louis School of Medicine, St Louis, MO, United States

Abstract
Objective: Despite the high prevalence, mild traumatic brain injury (mTBI)-induced chronic headache and cognitive deficits are poorly understood and lack effective treatments. Low-dose interleukin-2 (LD-IL-2) treatment soon after mTBI or overexpressing IL-2 in brain astrocytes prior to injury protects mice from developing post-traumatic headache (PTH)-related behaviors and cognitive decline. The present study addresses a clinically relevant knowledge gap: whether LD-IL-2 treatment long after the initial injury is still effective for chronic PTH and cognitive deficits. Methods: mTBI was induced by a noninvasive closed-head weight drop method. LD-IL-2 was administered 4–6 weeks post-mTBI to assess its effects on chronic PTH-related facial mechanical hypersensitivity as well as mTBI-induced impairment in novel object recognition and object location tests. Endogenous regulatory T (Treg) cells were depleted to investigate the mechanism of action of LD-IL-2. Results: Delayed LD-IL-2 treatment abolished chronic PTH-related behaviors. It also completely reversed mTBI-induced cognitive impairment in both male and female mice. Treg cell depletion not only prolonged PTH-related behaviors but also abolished the effects of LD-IL-2. Interestingly, LD-IL-2 treatment significantly increased the number of Treg cells in dura but not in brain tissues. Interpretation: These results suggest that the beneficial effects of LD-IL-2 treatment are mediated through the expansion of meningeal Treg cells. Collectively, our study identifies Treg as a cellular target and LD-IL-2 as a promising therapy for both chronic PTH and mTBI-induced cognitive impairment for both males and females, with a wide therapeutic time window and the potential of reducing polypharmacy in mTBI treatment. ANN NEUROL 2024. © 2024 American Neurological Association.

Funding details
U.S. Department of DefenseDODW81XWH2110597
National Institute of Neurological Disorders and StrokeNINDSNS128080

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Mental Health Diagnoses and Suicidality Among Transgender Youth in Hospital Settings” (2024) LGBT Health

Mental Health Diagnoses and Suicidality Among Transgender Youth in Hospital Settings
(2024) LGBT Health, . Cited 1 time.

Nunes-Moreno, M.a , Furniss, A.b , Cortez, S.c , Davis, S.M.d , Dowshen, N.e , Kazak, A.E.f , Nahata, L.g h , Pyle, L.d , Reirden, D.H.a , Schwartz, B.i , Sequeira, G.M.j , Nokoff, N.J.d

a Department of Psychiatry, University of Colorado, Anschutz Medical Campus, Aurora, CO, United States
b Adult & Child Center for Outcomes Research & Delivery Science, University of Colorado, Anschutz Medical Campus, Aurora, CO, United States
c Department of Pediatrics, Washington University School of Medicine, St. Louis, MO, United States
d Department of Pediatrics, University of Colorado, Anschutz Medical Campus, Aurora, CO, United States
e Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States
f Center for Healthcare Delivery Science, Nemours Children’s Health, Wilmington, DE, United States
g Department of Pediatrics, The Ohio State University College of Medicine, Columbus, OH, United States
h Center for Biobehavioral Health, Division of Endocrinology, Nationwide Children’s Hospital, Columbus, OH, United States
i Adolescent Medicine and Pediatric Gynecology, Nemours Children’s Health, Wilmington, DE, United States
j Department of Pediatrics, University of Washington, Seattle, WA, United States

Abstract
Purpose: The purpose of this analysis is to: 1) describe the most common mental health diagnoses in the emergency department (ED) and inpatient hospital settings among transgender and gender diverse (TGD) youth vs. matched controls and 2) evaluate if a gender-affirming hormone therapy (GAHT) or gonadotropin-releasing hormone agonist (GnRHa) prescription decreased the risk of suicidality within these settings. Methods: Using the PEDSnet dataset (years 2009–2019), TGD youth aged 8–18 (n = 3414, with a median age at last visit of 16.2 [14.4, 17.7] years, were propensity-score matched to controls (n = 13,628, age 16.6 [14.2, 18.3] years). Relative risks of the most common mental health diagnoses within ED and inpatient settings were calculated for TGD youth compared with controls. Recurrent time-to-event analysis was used to examine whether GAHT or GnRHa attenuated the risk of suicidality among subsamples of TGD youth. Results: TGD youth had a higher relative risk (95% confidence interval [CI]) of mental health diagnoses and suicidality in the ED (5.46 [4.71–6.33]) and inpatient settings (6.61 [5.28–8.28]) than matched controls. TGD youth prescribed GAHT had a 43.6% lower risk of suicidality (hazard ratio [HR] = 0.564 [95% CI 0.36–0.89]) compared with those never prescribed GAHT during our study period or before GAHT initiation. TGD youth who were prescribed GnRHa therapy had a nonstatistically significant reduction in ED or inpatient suicidality diagnoses compared with those never prescribed GnRHa (HR = 0.79 [0.47–1.31]). Conclusion: Although risk of mental health diagnoses and suicidality in ED and inpatient settings was high among TGD youth, a GAHT prescription was associated with a significant reduction in suicidality risk. © Mary Ann Liebert, Inc.

Author Keywords
gender-affirming hormone therapy;  gonadotropin-releasing hormone agonist;  suicidality;  transgender

Funding details
Stoneleigh Foundation
Doris Duke Charitable FoundationDDCF
K23HD092588, R03HD102773
K23 HL151868

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

A novel ABCC9 variant in a Greek family with Cantu syndrome affecting multiple generations highlights the functional role of the SUR2B NBD1” (2024) American Journal of Medical Genetics, Part A

A novel ABCC9 variant in a Greek family with Cantu syndrome affecting multiple generations highlights the functional role of the SUR2B NBD1
(2024) American Journal of Medical Genetics, Part A, . 

Gao, J.a b , Ververi, A.c , Thompson, E.a b , Tryon, R.a b , Sotiriadis, A.d , Rouvalis, F.e , Grange, D.K.b f , Giannios, C.g , Nichols, C.G.a b


a Department of Cell Biology and Physiology, Washington University in St. Louis, St. Louis, MO, United States
b Center for the Investigation of Membrane Excitability Diseases, Washington University in St. Louis, St. Louis, MO, United States
c Department for Genetics of Rare Diseases, Papageorgiou General Hospital, Thessaloniki, Greece
d Second Department of Obstetrics and Gynecology, Aristotle University of Thessaloniki, Ippokrateio Hospital, Thessaloniki, Greece
e Paediatric Cardiology Practice, Thessaloniki, Greece
f Department of Pediatrics, Division of Genetics and Genomic Medicine, Washington University in St. Louis, St. Louis, MO, United States
g Department of Developmental Paediatrics, Naval Hospital of Athens, Athens, Greece

Abstract
Cantu syndrome (CS) (OMIM #239850) is an autosomal dominant multiorgan system condition, associated with a characteristic facial phenotype, hypertrichosis, and multiple cardiovascular complications. CS is caused by gain-of-function (GOF) variants in KCNJ8 or ABCC9 that encode pore-forming Kir6.1 and regulatory SUR2 subunits of ATP-sensitive potassium (KATP) channels. A novel heterozygous ABCC9 variant, c.2440G&gt;T; p.Gly814Trp, was identified in three individuals from a four generation Greek family. The membrane potential in cells stably expressing hKir6.1 and hSUR2B with p.Gly814Trp was hyperpolarized compared to cells expressing WT channels, and inside-out patch-clamp assays of KATP channels formed with hSUR2B p.Gly814Trp demonstrated a decreased sensitivity to ATP inhibition, confirming a relatively mild GOF effect of this variant. The specific location of the variant reveals an unrecognized functional role of the first glycine in the signature motif of the nucleotide binding domains in ATP-binding cassette (ABC) protein ion channels. © 2024 The Author(s). American Journal of Medical Genetics Part A published by Wiley Periodicals LLC.

Author Keywords
Cantu syndrome;  DiBAC;  KATP channel;  nucleotide binding domain;  signature motif;  SUR2B

Funding details
National Institutes of HealthNIH

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Multimerization of TREM2 is impaired by Alzheimer’s disease–associated variants” (2024) Alzheimer’s and Dementia

Multimerization of TREM2 is impaired by Alzheimer’s disease–associated variants
(2024) Alzheimer’s and Dementia, . 

Dean, H.B.a b c , Greer, R.A.a , Yang, S.-Z.a , Elston, D.S.b , Brett, T.J.d , Roberson, E.D.b , Song, Y.a

a Department of Biomedical Engineering, School of Engineering, University of Alabama at Birmingham, Birmingham, AL, United States
b Alzheimer’s Disease Center, Center for Neurodegeneration and Experimental Therapeutics, & Departments of Neurology and Neurobiology, Marnix E. Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United States
c Medical Scientist Training Program, Marnix E. Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United States
d Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Department of Biochemistry and Molecular Biophysics, Hope Center for Neurological Disorders, & Department of Cell Biology and Physiology, Washington University School of Medicine, Washington University in St Louis, St. Louis, MO, United States

Abstract
INTRODUCTION: The immune receptor triggering receptor expressed on myeloid cells 2 (TREM2) is among the strongest genetic risk factors for Alzheimer’s disease (AD) and is a therapeutic target. TREM2 multimers have been identified in crystallography and implicated in the efficacy of antibody therapeutics; however, the molecular basis for TREM2 multimerization remains poorly understood. METHODS: We used molecular dynamics simulations and binding energy analysis to determine the effects of AD-associated variants on TREM2 multimerization and validated with experimental results. RESULTS: TREM2 trimers remained stably bound, driven primarily by salt bridge between residues D87 and R76 at the interface of TREM2 units. This salt bridge was disrupted by the AD-associated variants R47H and R98W and nearly ablated by the D87N variant. This decreased binding among TREM2 multimers was validated with co-immunoprecipitation assays. DISCUSSION: This study uncovers a molecular basis for TREM2 forming stable trimers and unveils a novel mechanism by which TREM2 variants may increase AD risk by disrupting TREM2 oligomerization to impair TREM2 normal function. Highlights: Triggering receptor expressed on myeloid cells 2 (TREM2) multimerization could regulate TREM2 activation and function. D87–R76 salt bridges at the interface of TREM2 units drive the formation of stable TREM2 dimers and trimers. Alzheimer’s disease (AD)–associated R47H and R98W variants disrupt the D87–R76 salt bridge. The AD-associated D87N variant leads to complete loss of the D87–R76 salt bridge. © 2024 The Author(s). Alzheimer’s & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer’s Association.

Author Keywords
Alzheimer’s disease–associated variants;  binding free energy analyses;  experimental validation;  molecular dynamics simulations;  oligomerization;  TREM2

Funding details
University of Alabama at BirminghamUAB
Alzheimer’s Drug Discovery FoundationADDF
National Institutes of HealthNIHT32GM008361, R01AG068395, T32NS095775, T32EB023872, R01AG081228, P20AG068024
National Science FoundationNSFOAC‐1541310

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Signaling Modulation Mediated by Ligand Water Interactions with the Sodium Site at μOR” (2024) ACS Central Science

Signaling Modulation Mediated by Ligand Water Interactions with the Sodium Site at μOR
(2024) ACS Central Science, . 

Ople, R.S.a b , Ramos-Gonzalez, N.a b , Li, Q.c , Sobecks, B.L.d e g , Aydin, D.d e g , Powers, A.S.d e g , Faouzi, A.a b , Polacco, B.J.d e , Bernhard, S.M.a b , Appourchaux, K.a b , Sribhashyam, S.a b , Eans, S.O.f , Tsai, B.A.f , Dror, R.O.d e g , Varga, B.R.a b , Wang, H.g , Hüttenhain, R.g , McLaughlin, J.P.f , Majumdar, S.a b

a Center for Clinical Pharmacology, University of Health Sciences & Pharmacy at St. Louis and Washington University School of Medicine, St. Louis, MO 63110, United States
b Department of Anesthesiology and Washington University Pain Center, Washington University School of Medicine, St. Louis, MO 63110, United States
c Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, United States
d Department of Computer Science, Stanford University, Stanford, CA 94305, United States
e Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305, United States
f Department of Pharmacodynamics, University of Florida, Gainesville, FL 032610, United States
g Department of Molecular & Cellular Physiology, Stanford University School of Medicine, Stanford, CA 94305, United States

Abstract
The mu opioid receptor (μOR) is a target for clinically used analgesics. However, adverse effects, such as respiratory depression and physical dependence, necessitate the development of alternative treatments. Recently we reported a novel strategy to design functionally selective opioids by targeting the sodium binding allosteric site in μOR with a supraspinally active analgesic named C6guano. Presently, to improve systemic activity of this ligand, we used structure-based design, identifying a new ligand named RO76 where the flexible alkyl linker and polar guanidine guano group is swapped with a benzyl alcohol, and the sodium site is targeted indirectly through waters. A cryoEM structure of RO76 bound to the μOR-Gi complex confirmed that RO76 interacts with the sodium site residues through a water molecule, unlike C6guano which engages the sodium site directly. Signaling assays coupled with APEX based proximity labeling show binding in the sodium pocket modulates receptor efficacy and trafficking. In mice, RO76 was systemically active in tail withdrawal assays and showed reduced liabilities compared to those of morphine. In summary, we show that targeting water molecules in the sodium binding pocket may be an avenue to modulate signaling properties of opioids, and which may potentially be extended to other G-protein coupled receptors where this site is conserved. © 2024 The Authors. Published by American Chemical Society.

Funding details
100001797, 0000 0000 9959 8153
R01DA056354, R01GM127359, RO1DA057790

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Genetic Variation and Stroke Recovery: The STRONG Study” (2024) Stroke

Genetic Variation and Stroke Recovery: The STRONG Study
(2024) Stroke, . 

Cramer, S.C.a b t , Parodi, L.c k , Moslemi, Z.d t , Braun, R.G.f , Aldridge, C.M.g , Shahbaba, B.d t , Rosand, J.c k , Holman, E.A.e t , Shah, S.h , Griessenauer, C.J.i , Patel, N.j , Anderson, C.k , Henry, J.k , Kourkoulis, C.k , Lin, D.J.k , Zaba, N.k , Gee, J.l , Moon, J.m , Schwertfeger, J.n , Jayaraman, A.o , Lee, R.p , Lansberg, M.G.q , Kemp, S.q , Huang, E.q , Bingham, E.q , Lugo, L.q , Kim, D.E.q , Payne, J.r , Patten, C.s , Ng, K.s , Cao, M.t , Jubb, A.t , McGee, B.t , Shahbaba, R.t , Agrawal, K.u , Kissela, B.v , DeJong, S.w , Cole, J.x , Braun, R.x , Silver, B.y , Manxhari, C.y , Cucchiara, B.z , Busza, A.aa , Hepple, J.P.aa , Liew, S.-L.ab , Alderman, S.ac , Beauchamp, J.ac , Mathew, N.J.ac , Hayes, H.ad , Majersik, J.J.ad , Aldridge, C.ae , Worrall, B.B.ae , Tirschwell, D.af , Bushnell, C.ag , El Husseini, N.ag , Lee, J.-M.ah , Falcone, G.J.ai , STRONG Study Investigatorsaj

a Department of Neurology, UCLA, Los Angeles, CA, United States
b California Rehabilitation Institute, Los Angeles, United States
c Department of Neurology, Center for Genomic Medicine, McCance Center for Brain Health, MGH, Boston, MA, United States
d Department of Statistics, UC IrvineCA, United States
e Sue & Bill Gross School of Nursing, Department of Psychological Science, UC IrvineCA, United States
f Department of Neurology, University of Maryland, Baltimore, United States
g Department of Neurology, University of Virginia, Charlottesville, United States
h Duke University, United States
i CGeisinger Health, Geisinger Commonwealth School of Medicine, United States
j Los Alamitos Medical Center, United States
k Massachusetts General Hospital, United States
l Providence Mission Hospital Mission Viejo, United States
m Providence St. Jude Medical Center, United States
n Rosalind Franklin University of Medicine and Science, United States
o Shirley Ryan AbilityLab, United States
p St. David’s Medical Center, United States
q Stanford University, United States
r University of Arizona, United States
s University of California, Davis School of Medicine, United States
t University of California, Irvine, United States
u University of California, San Diego, United States
v University of Cincinnati, United States
w University of Iowa, United States
x University of Maryland, United States
y UMass Chan, United States
z University of Pennsylvania, United States
aa University of Rochester, United States
ab University of Southern California, United States
ac University of Texas, Houston, United States
ad University of Utah, United States
ae University of Virginia, United States
af University of Washington, United States
ag Wake Forest School of Medicine, United States
ah Washington University, St. Louis, United States
ai Yale University, United States

Abstract
BACKGROUND: Genetic association studies can reveal biology and treatment targets but have received limited attention for stroke recovery. STRONG (Stroke, Stress, Rehabilitation, and Genetics) was a prospective, longitudinal (1-year), genetic study in adults with stroke at 28 US stroke centers. The primary aim was to examine the association that candidate genetic variants have with (1) motor/functional outcomes and (2) stress-related outcomes. METHODS: For motor/functional end points, 3 candidate gene variants (ApoE ϵ4, BDNF [brain-derived neurotrophic factor], and a dopamine polygenic score) were analyzed for associations with change in grip strength (3 months-baseline), function (3-month Stroke Impact Scale-Activities of Daily Living), mood (3-month Patient Health Questionnaire-8), and cognition (12-month telephone-Montreal Cognitive Assessment). For stress-related outcomes, 7 variants (serotonin transporter gene-linked promoter region, ACE [angiotensin-converting enzyme], oxytocin receptor, FKBP5 [FKBP prolyl isomerase 5], FAAH [fatty acid amide hydrolase], BDNF, and COMT [catechol-O-methyltransferase]) were assessed for associations with posttraumatic stress disorder ([PTSD]; PTSD Primary Care Scale) and depression (Patient Health Questionnaire-8) at 6 and 12 months; stress-related genes were examined as a function of poststroke stress level. Statistical models (linear, negative binomial, or Poisson regression) were based on response variable distribution; all included stroke severity, age, sex, and ancestry as covariates. Stroke subtype was explored secondarily. Data were Holm-Bonferroni corrected. A secondary replication analysis tested whether the rs1842681 polymorphism (identified in the GISCOME study [Genetics of Ischaemic Stroke Functional Outcome]) was related to 3-month modified Rankin Scale score in STRONG. RESULTS: The 763 enrollees were 63.1±14.9 (mean±SD) years of age, with a median initial National Institutes of Health Stroke Scale score of 4 (interquartile range, 2-9); outcome data were available in n=515 at 3 months, n=500 at 6 months, and n=489 at 12 months. At 1 year poststroke, the rs6265 (BDNF) variant was associated with poorer cognition (0.9-point lower telephone-Montreal Cognitive Assessment score, P=1×10-5). For stress-related outcomes, rs4291 (ACE) and rs324420 (FAAH) were risk factors linking increased poststroke stress with higher 1-year depression and PTSD symptoms (P&lt;0.05), while rs4680 (COMT) linked poststroke stress with lower 1-year depression and PTSD. Findings were unchanged when considering stroke subtype. STRONG replicated GISCOME: rs1842681 was associated with lower 3-month modified Rankin Scale score (P=3.2×10-5). CONCLUSIONS: This study identified genetic associations with cognitive function, depression, and PTSD 1 year poststroke. Genetic susceptibility to PTSD and depressive symptoms varied according to the amount of poststroke stress, underscoring the critical role of lived experiences in recovery. Together, the results suggest that genetic association studies provide insights into the biology of stroke recovery in humans. © 2024 American Heart Association, Inc.

Author Keywords
depression;  genetic polymorphism;  genetics;  hand strength;  paresis;  posttraumatic stress disorder;  stroke

Funding details
American Heart AssociationAHA
Eunice Kennedy Shriver National Institute of Child Health and Human DevelopmentNICHD
National Institute of Neurological Disorders and StrokeNINDS
National Center for Advancing Translational SciencesNCATS
National Institutes of HealthNIHR01NR015591

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Psilocybin desynchronizes the human brain” (2024) Nature

Psilocybin desynchronizes the human brain
(2024) Nature, . Cited 1 time.

Siegel, J.S.a , Subramanian, S.b , Perry, D.a , Kay, B.P.c , Gordon, E.M.d , Laumann, T.O.a , Reneau, T.R.d , Metcalf, N.V.c , Chacko, R.V.e , Gratton, C.f , Horan, C.g , Krimmel, S.R.c , Shimony, J.S.d , Schweiger, J.A.a , Wong, D.F.d , Bender, D.A.a , Scheidter, K.M.c , Whiting, F.I.c , Padawer-Curry, J.A.h , Shinohara, R.T.i j k , Chen, Y.k , Moser, J.l m , Yacoub, E.n , Nelson, S.M.l o , Vizioli, L.n , Fair, D.A.l m n o , Lenze, E.J.a , Carhart-Harris, R.p q , Raison, C.L.r s , Raichle, M.E.c d h t u , Snyder, A.Z.c d , Nicol, G.E.a , Dosenbach, N.U.F.c d h t v

a Department of Psychiatry, Washington University School of Medicine, St Louis, MO, United States
b Department of Psychiatry, Beth Israel Deaconess Medical Center, Boston, MA, United States
c Department of Neurology, Washington University School of Medicine, St Louis, MO, United States
d Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, MO, United States
e Department of Emergency Medicine, Advocate Christ Health Care, Oak Lawn, IL, United States
f Department of Psychology, Florida State University, Tallahassee, FL, United States
g Miami VA Medical Center, Miami, FL, United States
h Department of Biomedical Engineering, Washington University in St Louis, St Louis, MO, United States
i Center for Biomedical Image Computing and Analytics, University of Pennsylvania, Philadelphia, PA, United States
j Penn Statistics in Imaging and Visualization Endeavor, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States
k Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States
l Masonic Institute for the Developing Brain, University of Minnesota, Minneapolis, MN, United States
m Institute of Child Development, University of Minnesota, Minneapolis, MN, United States
n Center for Magnetic Resonance Research (CMRR), University of Minnesota, Minneapolis, MN, United States
o Department of Pediatrics, University of Minnesota, Minneapolis, MN, United States
p Department of Neurology, University of California, San Francisco, CA, United States
q Centre for Psychedelic Research, Imperial College London, London, United Kingdom
r Usona Institute, Fitchburg, WI, United States
s Department of Psychiatry, University of Wisconsin School of Medicine & amp; Public Health, Madison, WI, United States
t Department of Psychological and Brain Sciences, Washington University in St Louis, St Louis, MO, United States
u Department of Neuroscience, Washington University School of Medicine, St Louis, MO, United States
v Department of Pediatrics, Washington University School of Medicine, St Louis, MO, United States

Abstract
A single dose of psilocybin, a psychedelic that acutely causes distortions of space–time perception and ego dissolution, produces rapid and persistent therapeutic effects in human clinical trials1–4. In animal models, psilocybin induces neuroplasticity in cortex and hippocampus5–8. It remains unclear how human brain network changes relate to subjective and lasting effects of psychedelics. Here we tracked individual-specific brain changes with longitudinal precision functional mapping (roughly 18 magnetic resonance imaging visits per participant). Healthy adults were tracked before, during and for 3 weeks after high-dose psilocybin (25 mg) and methylphenidate (40 mg), and brought back for an additional psilocybin dose 6–12 months later. Psilocybin massively disrupted functional connectivity (FC) in cortex and subcortex, acutely causing more than threefold greater change than methylphenidate. These FC changes were driven by brain desynchronization across spatial scales (areal, global), which dissolved network distinctions by reducing correlations within and anticorrelations between networks. Psilocybin-driven FC changes were strongest in the default mode network, which is connected to the anterior hippocampus and is thought to create our sense of space, time and self. Individual differences in FC changes were strongly linked to the subjective psychedelic experience. Performing a perceptual task reduced psilocybin-driven FC changes. Psilocybin caused persistent decrease in FC between the anterior hippocampus and default mode network, lasting for weeks. Persistent reduction of hippocampal-default mode network connectivity may represent a neuroanatomical and mechanistic correlate of the proplasticity and therapeutic effects of psychedelics. © The Author(s) 2024.

Funding details
Intellectual and Developmental Disabilities Research CenterIDDRC
Tiny Blue Dot FoundationTBDF
Institute of Clinical and Translational SciencesICTS
Hope Center for Neurological Disorders, Washington University in St. Louis
McDonnell Center for Systems Neuroscience
U01DA041028, U01DA041093, U01DA041148, U01DA041022, U01DA041120, U01DA041106, U01DA051018, U24DA041123, U01DA050987, U01DA051016, U01DA041025, U01DA041048, U24DA041147, U01DA041156, U01DA051038, U01DA050989, U01DA041134, U01DA041117, U01DA050988, U01DA041089, U01DA041174, U01DA051039, U01DA051037
National Institutes of HealthNIHMH096773, MH124567, MH118370, NS124738, NS129521, MH112473, T32 DA007261, MH121276, NS088590, MH129616, NS123345, MH122066

Document Type: Article
Publication Stage: Article in Press
Source: Scopus