Publications

Hope Center Member Publications: December 15, 2024

Decreased voluntary alcohol intake and ventral striatal epigenetic and transcriptional remodeling in male Acss2 KO mice” (2025) Neuropharmacology

Decreased voluntary alcohol intake and ventral striatal epigenetic and transcriptional remodeling in male Acss2 KO mice
(2025) Neuropharmacology, 265, art. no. 110258, . 

Egervari, G.a b , Donahue, G.c d , Cardé, N.A.Q.e , Alexander, D.C.c d , Hogan, C.c d , Shaw, J.K.e , Periandri, E.M.a b , Fleites, V.e , De Biasi, M.e , Berger, S.L.c d

a Department of Genetics, Washington University School of Medicine, St. Louis, MO, United States
b Department of Biochemistry and Molecular Biophysics, Washington University, School of Medicine, St. Louis, MO, United States
c Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States
d Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States
e Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States

Abstract
Metabolic-epigenetic interactions are emerging as key pathways in regulating alcohol-related transcriptional changes in the brain. Recently, we have shown that this is mediated by the metabolic enzyme Acetyl-CoA synthetase 2 (Acss2), which is nuclear and chromatin-bound in neurons. Mice lacking ACSS2 fail to deposit alcohol-derived acetate onto histones in the brain and show no conditioned place preference for ethanol reward. Here, we further explored the role of this pathway during voluntary alcohol intake. We found that Acss2 KO mice consume significantly less alcohol in a model of binge drinking, an effect primarily driven by males. Genome-wide transcriptional profiling of 7 key brain regions implicated in alcohol and drug use revealed that, following drinking, Acss2 KO mice exhibit blunted gene expression in the ventral striatum. Similarly to the behavioral differences, transcriptional dysregulation was more pronounced in male mice. Further, we found that the gene expression changes were associated with depletion of ventral striatal histone acetylation (H3K27ac) in Acss2 KO mice compared to WT. Taken together, our data suggest that ACSS2 plays an important role in orchestrating ventral striatal epigenetic and transcriptional changes during voluntary alcohol drinking, especially in males. Consequently, targeting this pathway could be a promising new therapeutic avenue. © 2024 The Authors

Funding details
Brain and Behavior Research FoundationBBRF
National Institutes of HealthNIHR01AA027202, R00AA028577
National Institutes of HealthNIH
YIG31527

Document Type: Article
Publication Stage: Final
Source: Scopus

Early Young Adult Death Underscores the Need for Adolescent and Young Adult Transition Programs in Neurofibromatosis Type 1” (2025) Journal of Pediatrics

Early Young Adult Death Underscores the Need for Adolescent and Young Adult Transition Programs in Neurofibromatosis Type 1
(2025) Journal of Pediatrics, 277, art. no. 114413, . 

Tarnawsky, T.a , Oh, I.Y.b , Hillis, E.b , Gupta, A.b , Gutmann, D.H.a

a Department of Neurology, Washington University School of Medicine, St. Louis, MO, United States
b Institute for Informatics, Data Science, and Biostatistics, Washington University School of Medicine, St. Louis, MO, United States

Abstract
There are few centers with combined pediatric and adult neurofibromatosis 1 practices and transition of care programming. Using an electronic health records-based approach, we found an early death peak in the fourth decade of life largely owing to malignancy, underscoring the need for integrated neurological training and practice across the lifespan. © 2024 Elsevier Inc.

Funding details
National Institute of Neurological Disorders and StrokeNINDS1R01NS131112
National Institute of Neurological Disorders and StrokeNINDS

Document Type: Article
Publication Stage: Final
Source: Scopus

Prenatal social disadvantage is associated with alterations in functional networks at birth” (2024) Proceedings of the National Academy of Sciences of the United States of America

Prenatal social disadvantage is associated with alterations in functional networks at birth
(2024) Proceedings of the National Academy of Sciences of the United States of America, 121 (50), pp. e2405448121. 

Nielsen, A.N.a , Triplett, R.L.a , Bernardez, L.M.a , Tooley, U.A.b , Herzberg, M.P.b , Lean, R.E.b , Kaplan, S.a , Meyer, D.a , Kenley, J.K.a , Alexopoulos, D.a , Losielle, D.a , Latham, A.a , Smyser, T.A.b , Agrawal, A.b , Shimony, J.S.c , Jackson, J.J.d , Miller, J.P.e , Raichle, M.E.a c d f g , Warner, B.B.h , Rogers, C.E.b h , Sylvester, C.M.b , Barch, D.M.b c d , Luby, J.L.b , Smyser, C.D.a c h

a Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, United States
b Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63110, United States
c Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, United States
d Department of Psychological and Brain Sciences, Washington University in St. Louis, St. Louis, MO 63110, United States
e Department of Biostatistics, Washington University in St. Louis, St. Louis, MO 63110, United States
f Department of Neuroscience, Washington University in St. Louis, St. Louis, MO 63110, United States
g Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63110, United States
h Department of Pediatrics, Washington University School of Medicine, St. Louis, MO 63110, United States

Abstract
Childhood exposure to social disadvantage is a major risk factor for psychiatric disorders and poor developmental, educational, and occupational outcomes, presumably because adverse exposures alter the neurodevelopmental processes that contribute to risk trajectories. Yet, given the limited social mobility in the United States and other countries, childhood social disadvantage is frequently preceded by maternal social disadvantage during pregnancy, potentially altering fetal brain development during a period of high neuroplasticity through hormonal, microbiome, epigenetic, and immune factors that cross the placenta and fetal blood-brain barrier. The current study examines prenatal social disadvantage to determine whether these exposures in utero are associated with alterations in functional brain networks as early as birth. As part of the Early Life Adversity and Biological Embedding study, mothers were recruited during pregnancy, prenatal social disadvantage was assessed across trimesters, and their healthy, full-term offspring were imaged using resting-state functional magnetic resonance imaging during the first weeks of life. Multivariate machine learning methods revealed that neonatal functional connectivity (FC) varied as a function of prenatal exposure to social disadvantage (n = 261, R = 0.43, R2 = 0.18), with validation in an independent sample. Alterations in FC associated with prenatal social disadvantage occurred brain-wide and were most pronounced in association networks (fronto-parietal, ventral attention, dorsal attention) and the somatomotor network. Amygdala FC was altered at birth, with a pattern shared across subcortical structures. These findings provide critical insights into how early in development functional networks begin to diverge in the context of social disadvantage and elucidate the functional networks that are most impacted.

Author Keywords
functional connectivity;  infant;  prenatal exposure;  social disadvantage;  socieconomic status

Document Type: Article
Publication Stage: Final
Source: Scopus

Cellular trafficking and fate mapping of cells within the nervous system after in utero hematopoietic cell transplantation” (2024) Communications Biology

Cellular trafficking and fate mapping of cells within the nervous system after in utero hematopoietic cell transplantation
(2024) Communications Biology, 7 (1), art. no. 1624, . 

Grant, M.T.a , Nelvagal, H.R.b c , Tecos, M.a , Hamed, A.a , Swanson, K.a , Cooper, J.D.b , Vrecenak, J.D.a

a Washington University in St. Louis School of Medicine, Department of Surgery, Division of Pediatric Surgery, St. Louis, MO, United States
b Washington University in St. Louis School of Medicine, Department of Pediatrics, Division of Genetics and Genomics, St. Louis, MO, United States
c University College London, School of Pharmacy, Department of Pharmacology, London, United Kingdom

Abstract
In utero hematopoietic cell transplantation (IUHCT) utilizes fetal immune tolerance to achieve durable chimerism without conditioning or immunosuppression during a unique window in fetal development. Though donor cells have been observed within the nervous system following in utero injection, the timeline and distribution of cellular trafficking across the blood-brain barrier following IUHCT is not well understood. We injected 20 × 106 adult bone marrow mononuclear cells intravenously at gestational age (GA) 12–17 days and found that donor cells were maximally concentrated in the brain with treatment between GA 13–14. Donor cell engraftment persisted within the brain at every timepoint analyzed and concentrated within the hindbrain with significantly more grafted cells than in the forebrain. Additionally, transplanted cells terminally differentiated into various nervous system cellular morphologies and also populated the enteric nervous system. This study is the first to document the timeline and distribution of donor cell trafficking into the immune-protected nervous system and serves as a foundation for the application of IUHCT to treat neurogenetic diseases. © The Author(s) 2024.

Funding details
Children’s Discovery InstituteCDIMI-II-2019-777
Children’s Discovery InstituteCDI
PR 2017281

Document Type: Article
Publication Stage: Final
Source: Scopus

MYT1L deficiency impairs excitatory neuron trajectory during cortical development” (2024) Nature Communications

MYT1L deficiency impairs excitatory neuron trajectory during cortical development
(2024) Nature Communications, 15 (1), art. no. 10308, . 

Yen, A.a b , Sarafinovska, S.a b , Chen, X.a c , Skinner, D.D.d , Leti, F.d , Crosby, M.c e , Hoisington-Lopez, J.c e , Wu, Y.a b , Chen, J.a b , Li, Z.A.a b , Noguchi, K.K.b , Mitra, R.D.a c , Dougherty, J.D.a b f

a Department of Genetics, Washington University School of Medicine, Saint Louis, MO, United States
b Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO, United States
c Edison Family Center for Genome Sciences and Systems Biology, Washington University School of Medicine, Saint Louis, MO, United States
d Scale Biosciences, San Diego, CA, United States
e DNA Sequencing and Innovation Lab, Washington University School of Medicine, Saint Louis, MO, United States
f Intellectual and Developmental Disabilities Research Center, Washington University School of Medicine, Saint Louis, MO, United States

Abstract
Mutations reducing the function of MYT1L, a neuron-specific transcription factor, are associated with a syndromic neurodevelopmental disorder. MYT1L is used as a pro-neural factor in fibroblast-to-neuron transdifferentiation and is hypothesized to influence neuronal specification and maturation, but it is not clear which neuron types are most impacted by MYT1L loss. In this study, we profile 412,132 nuclei from the forebrains of wild-type and MYT1L-deficient mice at three developmental stages: E14 at the peak of neurogenesis, P1 when cortical neurons have been born, and P21 when neurons are maturing, to examine the role of MYT1L levels on neuronal development. MYT1L deficiency disrupts cortical neuron proportions and gene expression, primarily affecting neuronal maturation programs. Effects are mostly cell autonomous and persistent through development. While MYT1L can both activate and repress gene expression, the repressive effects are most sensitive to haploinsufficiency, likely mediating MYT1L syndrome. These findings illuminate MYT1L’s role in orchestrating gene expression during neuronal development, providing insights into the molecular underpinnings of MYT1L syndrome. © The Author(s) 2024.

Funding details
Eunice Kennedy Shriver National Institute of Child Health and Human DevelopmentNICHD
Genome Technology Access CenterGTAC
University of WashingtonUW
St. Louis Children’s HospitalSLCHCDI-CORE-2019-813, CDI-CORE-2015-505
St. Louis Children’s HospitalSLCH
National Human Genome Research InstituteNHGRIT32HG000045
National Human Genome Research InstituteNHGRI
National Institute of Mental HealthNIMHR01MH124808, RF1MH126723, RF1MH117070
National Institute of Mental HealthNIMH
Autism Science FoundationASF22-007
Autism Science FoundationASF
Foundation for Barnes-Jewish HospitalFBJH4642, 3770
Foundation for Barnes-Jewish HospitalFBJH
National Institutes of HealthNIHP50 HD103525
National Institutes of HealthNIH

Document Type: Article
Publication Stage: Final
Source: Scopus

Correlation Between Visual Acuity and Foveal Threshold by Automated Perimetry With Size V Stimulus” (2024) Journal of Neuro-Ophthalmology

Correlation Between Visual Acuity and Foveal Threshold by Automated Perimetry With Size V Stimulus
(2024) Journal of Neuro-Ophthalmology, 44 (4), pp. 507-510. 

Bohm, P.E.a , Stunkel, L.a b , Van Stavern, G.P.a b

a Departments of Ophthalmology and Visual Sciences, Washington University in St. Louis, St. Louis, MO, United States
b Departments of Neurology, Washington University in St. Louis, St. Louis, MO, United States

Abstract
Background:Visual acuity has been shown to correlate with foveal threshold as determined by automated perimetry. Although automated perimetry with size V stimulus is commonly used in neuro-ophthalmology practice, the relationship between the visual acuity and the foveal threshold with this larger stimulus is not well known.Methods:Retrospective study of patients who had undergone neuro-ophthalmology evaluation and visual field testing with automated perimetry using size V stimulus. Healthy controls were also recruited. Using visual acuity and foveal threshold, Pearson correlation coefficients were calculated, and basic foveal threshold statistics were stratified by visual acuity. Prediction intervals for visual acuities by various foveal threshold were also calculated.Results:A total of 106 unique eyes were included. The final Pearson correlation coefficient between visual acuities was -0.795 for the right eye and -0.578 for the left eye, with a pooled correlation coefficient of -0.751 (P < 0.001). A foveal threshold of at least 34 dB was present in 94.4% of eyes with 20/20 visual acuity, and a foveal threshold of greater than 35 dB was not observed in eyes with visual acuity of 20/40 or worse.Conclusions:Foveal threshold as determined by automated perimetry using size V stimulus has moderate-to-strong correlation with visual acuity in patients undergoing neuro-ophthalmology evaluation. © 2023 by North American Neuro-Ophthalmology Society.

Document Type: Article
Publication Stage: Final
Source: Scopus

Difficult to Treat Depression: Focus on Approach, Algorithms, and Access” (2024) The Journal of Clinical Psychiatry

Difficult to Treat Depression: Focus on Approach, Algorithms, and Access
(2024) The Journal of Clinical Psychiatry, 85 (4), . 

Karp, J.F.a , Brinton, R.D.b , Fournier, J.C.c , Harding, L.d , Jha, M.K.e , Lenze, E.J.f , Mathew, S.J.g , Meltzer-Brody, S.h , Mohr, D.C.i , Riva-Posse, P.j , Wiechers, I.k l , Williams, N.R.m

a Department of Psychiatry, College of Medicine, University of Arizona, Tucson, United States
b Center for Innovation in Brain Science, University of Arizona, Tucson, AZ, United States
c Department of Psychiatry and Behavioral Health, Ohio State University, Columbus, OH, United States
d Yale University School of Medicine, New Haven, Connecticut, and Depression MD, Milford, Connecticut
e Department of Psychiatry and Center for Depression Research and Clinical Care, University of Texas Southwestern Medical Center, Dallas, TX, United States
f Department of Psychiatry, Washington University, St. Louis, MO, United States
g Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, United States
h Department of Psychiatry, School of Medicine, University of North Carolina at Chapel Hill
i Department of Preventive Medicine and the Center for Behavioral Intervention Technologies, Northwestern University Feinberg School of Medicine, Chicago, IL, United States
j Department of Psychiatry, Emory University, Atlanta, Georgia
k Office of Mental Health, Veterans Health AdministrationWA, United States
l Department of Psychiatry and Behavioral Sciences, San Francisco School of Medicine, University of California, San Francisco, CA, United States
m Department of Psychiatry, Stanford University, Palo Alto, CA, United States

Abstract
The pandemic refocused interest on the burden of depression across the lifespan; the increased efforts to prevent and treat depression are now a priority of health care systems, insurers, patient advocates, digital therapeutic engineers, telemedicine platforms, and community health agencies. However, the challenges of treating depression to remission in adult patients who do not respond to first, second, or third levels of oral pharmacotherapy remain. The increased prevalence of these conditions is at odds with the shrinking psychiatric workforce. Since addressing difficult to treat depression is situated in a rapidly evolving treatment landscape, The University of Arizona College of Medicine-Tucson Department of Psychiatry organized and hosted the Southwest Forum on Difficult to Treat Depression: Focus on Approach, Algorithms, and Access in July 2024. The Forum convened 11 internationally renowned experts in the science and treatment of depression, in particular difficult to treat depression, for a day of teaching and discussion. Based on their expertise, participants were asked to address one of the following three themes: (1) Novel Mechanism Approaches for Difficult to Treat Depression, (2) What Do I Do Next? Evidence-Informed Algorithms to Get Patients Better Faster, and (3) Access: Providing Comprehensive Depression Care Across the Spectrum of Clinical Severity. © Copyright 2024 Physicians Postgraduate Press, Inc.

Document Type: Article
Publication Stage: Final
Source: Scopus

Endogenous self-peptides guard immune privilege of the central nervous system” (2024) Nature

Endogenous self-peptides guard immune privilege of the central nervous system
(2024) Nature, . Cited 2 times.

Kim, M.W.a b c d , Gao, W.a b , Lichti, C.F.a b e , Gu, X.a b , Dykstra, T.a b , Cao, J.a b , Smirnov, I.a b , Boskovic, P.a b , Kleverov, D.b f , Salvador, A.F.M.a b , Drieu, A.a b , Kim, K.a b , Blackburn, S.a b , Crewe, C.g , Artyomov, M.N.b e , Unanue, E.R.a b e , Kipnis, J.a b e

a Brain Immunology and Glia (BIG) Center, School of Medicine, Washington University in St Louis, St Louis, MO, United States
b Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, United States
c Immunology Graduate Program, School of Medicine, Washington University in St Louis, St Louis, MO, United States
d Medical Scientist Training Program, School of Medicine, Washington University in St Louis, St Louis, MO, United States
e Bursky Center for Human Immunology and Immunotherapy Programs, School of Medicine, Washington University in St Louis, St Louis, MO, United States
f Computer Technologies Laboratory, ITMO University, Saint Petersburg, Russian Federation
g Department of Cell Biology and Physiology, School of Medicine, Washington University in St Louis, St Louis, MO, United States

Abstract
Despite the presence of strategically positioned anatomical barriers designed to protect the central nervous system (CNS), it is not entirely isolated from the immune system1,2. In fact, it remains physically connected to, and can be influenced by, the peripheral immune system1. How the CNS retains such responsiveness while maintaining an immunologically unique status remains an outstanding question. Here, in searching for molecular cues that derive from the CNS and enable its direct communication with the immune system, we identified an endogenous repertoire of CNS-derived regulatory self-peptides presented on major histocompatibility complex class II (MHC-II) molecules in the CNS and at its borders. During homeostasis, these regulatory self-peptides were found to be bound to MHC-II molecules throughout the path of lymphatic drainage from the brain to its surrounding meninges and its draining cervical lymph nodes. However, in neuroinflammatory disease, the presentation of regulatory self-peptides diminished. After boosting the presentation of these regulatory self-peptides, a population of suppressor CD4+ T cells was expanded, controlling CNS autoimmunity in a CTLA-4- and TGFβ-dependent manner. CNS-derived regulatory self-peptides may be the molecular key to ensuring a continuous dialogue between the CNS and the immune system while balancing overt autoreactivity. This sheds light on how we conceptually think about and therapeutically target neuroinflammatory and neurodegenerative diseases. © The Author(s) 2024.

Funding details
National Institutes of HealthNIHDPI AT010416
National Institutes of HealthNIH

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

Neutrophil CRACR2A Promotes Neutrophil Recruitment in Sterile Inflammation and Ischemic Stroke” (2024) Circulation

Neutrophil CRACR2A Promotes Neutrophil Recruitment in Sterile Inflammation and Ischemic Stroke
(2024) Circulation, . 

Lee, J.a , Balzraine, B.a , Schweizer, A.a , Kuzmanova, V.a , Gwack, Y.g , Razani, B.e h i , Lee, J.-M.b c d , Mosher, D.F.j k , Cho, J.a f

a Division of Hematology, Department of Medicine, Washington University, School of Medicine, St Louis, MO, United States
b Department of Neurology, Washington University, School of Medicine, St Louis, MO, United States
c Hope Center for Neurological Disorders, 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 Biomedical Engineering, Washington University, School of Medicine, St Louis, MO, United States
f Department of Pathology and Immunology, Washington University, School of Medicine, St Louis, MO, United States
g Department of Physiology, David Geffen School of Medicine, University of California, Los Angeles, United States
h Vascular Medicine Institute, Department of Medicine, University of Pittsburgh, School of Medicine, UPMCPA, United States
i Pittsburgh VA Medical CenterPA, United States
j Department of Biomolecular Chemistry, University of Wisconsin-Madison, United States
k Department of Medicine, University of Wisconsin-Madison, United States

Abstract
BACKGROUND: Ca2+ release-activated Ca2+ channel regulator 2A (CRACR2A) has been linked to immunodeficiency attributable to T-cell dysfunction in humans. We discovered that neutrophil CRACR2A promotes neutrophil adhesive and migratory functions by facilitating Ca2+ mobilization and β2 integrin activation. METHODS: Myeloid-specific cracr2a conditional knockout mice and intravital microscopy were used to investigate the physiologic role of neutrophil cracr2a in neutrophil recruitment in vascular inflammation. Cracr2a-deficient neutrophils or dHL-60 (differentiated human neutrophil-like) cells and CRACR2A-derived peptides were used in flow cytometry, immunoprecipitation, cytosolic Ca2+ mobilization, and flow chamber assays to elucidate the molecular mechanism. Four-dimensional confocal intravital microscopy of mice after focal brain ischemia and single neutrophil behavioral analysis demonstrated the pathologic role of neutrophil cracr2a in brain damage. RESULTS: Compared with wild-type control mice, cracr2a conditional knockout mice exhibited significantly reduced adhesion, crawling, and transmigration of neutrophils on ear and cremaster venules in tumor necrosis factor-α-induced sterile inflammation. Neutrophil cracr2a rapidly interacts with STIM1 (stromal interaction molecule 1) after agonist stimulation and facilitates Ca2+ mobilization, increasing the ligand-binding function of β2 integrin. Our findings in cracr2a-deficient mouse neutrophils are recapitulated in dHL-60 cells, in which CRACR2A is deleted by CRISPR/Cas9. Furthermore, overexpression of CRACR2A in CRACR2A KO dHL-60 cells restores normal function. Using a series of peptides covering the coiled-coil region of CRACR2A, we identified a palmitoylated 20-mer that blocks STIM1-CRACR2A interaction. Treating neutrophils with this 20-mer inhibits Ca2+ mobilization and β2 integrin activation after agonist stimulation, reducing neutrophil recruitment to an activated endothelial cell monolayer under venous shear stress and to ear venules in tumor necrosis factor-α-challenged mice. Cerebral 4-dimensional intravital microscopy of mice after focal brain ischemia revealed that neutrophil cracr2a enhances the emergence of highly migratory neutrophils by increasing the surface level of αMβ2 integrin, thereby facilitating neutrophil infiltration into brain tissue and exacerbating brain injury. CONCLUSIONS: Our results demonstrate that neutrophil CRACR2A promotes neutrophil recruitment to sites of sterile inflammation, such as ischemic stroke. Blocking the STIM1-CRACR2A interaction may be a novel therapeutic strategy to mitigate inflammation and consequent tissue injury. © 2024 American Heart Association, Inc.

Author Keywords
inflammation;  integrins;  ischemic stroke;  neutrophil infiltration;  neutrophils

Funding details
National Institutes of HealthNIHR01HL148280, R01HL146559, R01HL153047, R01HL130028
National Institutes of HealthNIH
American Heart AssociationAHA24POST1189050, 23TPA1070903
American Heart AssociationAHA

Document Type: Article
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