Systems biology dissection of PTSD and MDD across brain regions, cell types, and blood
The molecular pathology of stress-related disorders remains elusive. Our brain multiregion, multiomic study of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) included the central nucleus of the amygdala, hippocampal dentate gyrus, and medial prefrontal cortex (mPFC). Genes...
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| Published in | Science (American Association for the Advancement of Science) Vol. 384; no. 6698; p. eadh3707 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
24.05.2024
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The molecular pathology of stress-related disorders remains elusive. Our brain multiregion, multiomic study of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) included the central nucleus of the amygdala, hippocampal dentate gyrus, and medial prefrontal cortex (mPFC). Genes and exons within the mPFC carried most disease signals replicated across two independent cohorts. Pathways pointed to immune function, neuronal and synaptic regulation, and stress hormones. Multiomic factor and gene network analyses provided the underlying genomic structure. Single nucleus RNA sequencing in dorsolateral PFC revealed dysregulated (stress-related) signals in neuronal and non-neuronal cell types. Analyses of brain-blood intersections in >50,000 UK Biobank participants were conducted along with fine-mapping of the results of PTSD and MDD genome-wide association studies to distinguish risk from disease processes. Our data suggest shared and distinct molecular pathology in both disorders and propose potential therapeutic targets and biomarkers. |
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| AbstractList | The molecular pathology of stress-related disorders remains elusive. Our brain multiregion, multiomic study of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) included the central nucleus of the amygdala, hippocampal dentate gyrus, and medial prefrontal cortex (mPFC). Genes and exons within the mPFC carried most disease signals replicated across two independent cohorts. Pathways pointed to immune function, neuronal and synaptic regulation, and stress hormones. Multiomic factor and gene network analyses provided the underlying genomic structure. Single nucleus RNA sequencing in dorsolateral PFC revealed dysregulated (stress-related) signals in neuronal and non-neuronal cell types. Analyses of brain-blood intersections in >50,000 UK Biobank participants were conducted along with fine-mapping of the results of PTSD and MDD genome-wide association studies to distinguish risk from disease processes. Our data suggest shared and distinct molecular pathology in both disorders and propose potential therapeutic targets and biomarkers. The molecular pathology of stress-related disorders remains elusive. Our brain multiregion, multiomic study of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) included the central nucleus of the amygdala, hippocampal dentate gyrus, and medial prefrontal cortex (mPFC). Genes and exons within the mPFC carried most disease signals replicated across two independent cohorts. Pathways pointed to immune function, neuronal and synaptic regulation, and stress hormones. Multiomic factor and gene network analyses provided the underlying genomic structure. Single nucleus RNA sequencing in dorsolateral PFC revealed dysregulated (stress-related) signals in neuronal and non-neuronal cell types. Analyses of brain-blood intersections in >50,000 UK Biobank participants were conducted along with fine-mapping of the results of PTSD and MDD genome-wide association studies to distinguish risk from disease processes. Our data suggest shared and distinct molecular pathology in both disorders and propose potential therapeutic targets and biomarkers.The molecular pathology of stress-related disorders remains elusive. Our brain multiregion, multiomic study of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) included the central nucleus of the amygdala, hippocampal dentate gyrus, and medial prefrontal cortex (mPFC). Genes and exons within the mPFC carried most disease signals replicated across two independent cohorts. Pathways pointed to immune function, neuronal and synaptic regulation, and stress hormones. Multiomic factor and gene network analyses provided the underlying genomic structure. Single nucleus RNA sequencing in dorsolateral PFC revealed dysregulated (stress-related) signals in neuronal and non-neuronal cell types. Analyses of brain-blood intersections in >50,000 UK Biobank participants were conducted along with fine-mapping of the results of PTSD and MDD genome-wide association studies to distinguish risk from disease processes. Our data suggest shared and distinct molecular pathology in both disorders and propose potential therapeutic targets and biomarkers. INTRODUCTIONStress-related disorders arise from the interplay between genetic susceptibility and stress exposure, occurring throughout the lifespan. Progressively, these interactions lead to epigenetic modifications in the human genome, shaping the expression of genes and proteins. Prior postmortem brain studies have attempted to elucidate the molecular pathology of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) compared with neurotypical controls (NCs) in a single-omic manner, revealing genomic overlap, sex differences, and immune and interneuron signaling involvement. However, without integrative systems approaches, progress in understanding the molecular underpinnings of these prevalent and debilitating disorders is hindered.RATIONALETo tackle this roadblock, we have created a brain multiregion, multiomic database of individuals with PTSD and MDD and NCs (77 per group, n = 231) to describe molecular alterations across three brain regions: the central nucleus of the amygdala (CeA), medial prefrontal cortex (mPFC), and hippocampal dentate gyrus (DG) at the transcriptomic, methylomic, and proteomic levels. By using this multiomic strategy that merges information across biological layers and organizational strata and complementing it with single-nucleus RNA sequencing (snRNA-seq), genetics, and blood plasma proteomics analyses, we sought to reveal an integrated-systems perspective of PTSD and MDD.RESULTSWe found molecular differences primarily in the mPFC, with differentially expressed genes (DEGs) and exons carrying the most disease signals. However, altered methylation was seen mainly in the DG in PTSD subjects, in contrast to the CeA in MDD subjects. Replication analysis substantiated these findings with multiomic data from two cohorts (n = 114). Moreover, we found a moderate overlap between the disorders, with childhood trauma and suicide being primary drivers of molecular variations in both disorders, and sex specificity being more notable in MDD. Pathway analyses linked disease-associated molecular signatures to immune mechanisms, metabolism, mitochondria function, neuronal or synaptic regulation, and stress hormone signaling with low concordance across omics. Top upstream regulators and transcription factors included IL1B, GR, STAT3, and TNF. Multiomic factor and gene network analyses provided an underlying genomic structure of the disorders, suggesting latent factors and modules related to aging, inflammation, vascular processes, and stress. To complement the multiomics analyses, our snRNA-seq analyses in the dorsolateral PFC (n = 118) revealed DEGs, dysregulated pathways, and upstream regulators in neuronal and non-neuronal cell-types, including stress-related gene signals. Examining the intersection of brain multiomics with blood proteins (in >50,000 UK Biobank participants) revealed significant correlation, overlap, and directional similarity between brain-to-blood markers. Fine-mapping of PTSD and MDD genome-wide association studies’ (GWASs’) results showed a limited overlap between risk and disease processes at the gene and pathway levels.Ultimately, prioritized genes with multiregion, multiomic, or multitrait disease associations were members of pathways or networks, showed cell-type specificity, had blood biomarker potential, or were involved in genetic risk for PTSD and MDD. CONCLUSIONOur findings unveil shared and distinct brain multiomic molecular dysregulations in PTSD and MDD, elucidate the involvement of specific cell types, pave the way for the development of blood-based biomarkers, and distinguish risk from disease processes. These insights not only implicate established stress-related pathways but also reveal potential therapeutic avenues. The molecular pathology of stress-related disorders remains elusive. Our brain multi-omic, multi-region study of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) included the central nucleus of the amygdala, hippocampal dentate gyrus, and medial prefrontal cortex (mPFC). Genes and exons within the mPFC carried most disease signals replicated across two independent cohorts. Pathways pointed to immune function, neuronal/synaptic regulation and stress hormones. Multi-omic factor and gene network analyses provided the underlying genomic structure. Single nucleus RNA-sequencing in dorsolateral PFC revealed dysregulated (stress-related) signals. Analyses of brain-blood intersections in >50,000 UK Biobank participants were conducted along with fine-mapping of PTSD and MDD genome-wide association studies’ results. Our data suggest shared and distinct molecular pathology in both disorders and propose potential therapeutic targets and biomarkers. |
| Author | Daskalakis, Nikolaos P. Bergner, Carisa Breen, Gerome Beckham, Jean C. Nievergelt, Caroline M. Dammer, Eric B. Wuchty, Stefan Ashley-Koch, Allison E. Seyfried, Nicholas T. Berretta, Sabina Bybjerg-Grauholm, Jonas Cruz-Fuentes, Carlos S. Tsatsani, Ioulia Boks, Marco P. Huuki, Louise Aaronson, Cindy Polimanti, Renato Atkinson, Elizabeth G. Duncan, Laramie E. Cheema, Sheraz Choi, Karmel W. Dalvie, Shareefa Bacanu, Silviu-Alin Davis, Lea K. Sun, Benjamin B. Bharadwaj, Rahul A. Andersen, Soren B. Wylie, Dennis Batzler, Anthony Nemeroff, Charles B. Snijders, Clara Andreassen, Ole A. Bækvad-Hansen, Marie Bolger, Elizabeth A. Børglum, Anders D. Caldas-de-Almeida, Jose Miguel Sendi, Mohammad S. E. Collado-Torres, Leonardo Huber, Bertrand R. Amstadter, Ananda B. Wolf, Erika J. Maihofer, Adam X. Baker, Dewleen G. Arbisi, Paul A. Biernacka, Joanna M. Ross, Deanna Iatrou, Artemis Ressler, Kerry J. Austin, S. Bryn Holstein, Vincent L. Tooke, James Miller, Mark W. Børte, Sigrid Pernia, Cameron D. Arasappan, Dhivya Chatzinakos, Chris Soliva-Estruch, Marina |
| AuthorAffiliation | 7 Department of Psychiatry and Neuropsychology, School for Mental Health, and Neuroscience (MHeNs), Maastricht University, Maastricht, 6229 ER, The Netherlands 21 Center for Excellence in Stress and Mental Health, Veterans Affairs San Diego Healthcare System; San Diego, CA, 92161, USA 28 Department of Neuroscience, Johns Hopkins University School of Medicine; Baltimore, MD, 21205, USA 4 Department of Psychiatry and Behavioral Sciences, SUNY Downstate Health Sciences University, Brooklyn, NY, 11203, USA 1 McLean Hospital; Belmont, MA, 02478, USA 18 Department of Biomedical Genetics, Boston University Chobanian & Avedisian School of Medicine, Boston, MA, 02118, USA 30 Department of Psychiatry and Behavioral Sciences, University of Texas at Austin; Austin, TX, 78712, USA 2 Department of Psychiatry, Harvard Medical School; Boston, MA, 02115, USA 5 VA New York Harbor Healthcare System, Brooklyn, NY, 11209, USA 26 Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Me |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38781393$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Contributor | Domschke, Katharina Bierut, Laura J Nievergelt, Caroline M Dennis, Michelle F Bybjerg-Grauholm, Jonas Hogan, Kelleigh Aaronson, Cindy Polimanti, Renato Dalvie, Shareefa Hveem, Kristian Javanbakht, Arash Bacanu, Silviu-Alin Baker, Dewleen G Jakovljević, Miro Batzler, Anthony Davis, Lea K Ashley-Koch, Allison E Hemmings, Sian M J Forbes, David Delahanty, Douglas L Atkinson, Elizabeth G Hickie, Ian B Clouston, Sean A P Andreassen, Ole A Calabrese, Joseph R Edenberg, Howard J Daskalakis, Nikolaos P Bolger, Elizabeth A Bisson, Jonathan I Maihofer, Adam X Beckham, Jean C Belangero, Sintia Bryant, Richard A Guindalini, Camila Feeny, Norah C Coombes, Brandon J Austin, S Bryn Geuze, Elbert Cruz-Fuentes, Carlos S Kulenović, Alma Džubur Hesselbrock, Victor Hougaard, David Michael Feder, Adriana Cahn, Leah Bierer, Linda M Boks, Marco P Biernacka, Joanna M Deckert, Jürgen Benjet, Corina Desarnaud, Frank DiPietro, Christopher P Bergner, Carisa Breen, Gerome Johnson, Jessica Gillespie, Charles F Garrett, Melanie E Coleman, Jonathan R I Goleva, Slavina B Hua |
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| Copyright | Copyright © 2024 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Writing – review & editing: N.P.D., A.I., A.J., C.S., K.J.R. with contributions from D.W., I.T., C.D.P., M.S.E., and critical input from all authors. These authors contributed equally to this work in alphabetic order collaborators and affiliations are listed in the supplementary materials. Resources and Data curation: N.P.D., C.S., L.C-T., A.D-S., A.X.M., C.M.N., B.B.S. Methodology N.P.D., A.I., A.J., D.W. Supervision: N.P.D., FAC, NTS, JHS, C.B.N., J.E.K., K.J.R. Conceptualization: N.P.D., C.B.N., J.E.K., K.J.R. Project administration: N.P.D., C.B.N., J.E.K., K.J.R. Investigation: N.P.D., C.C., B.A.B., D.A., A.D-S., D.M.D., R.T., J.T., S.B., F.A.C., T.H., N.T.S., J.H.S., D.R.W., C.B.N., J.E.K., K.J.R. Writing – original draft preparation: N.P.D., A.I., A.J., C.S., K.J.R. with contributions from D.W., I.T., C.D.P., M.S-E., J.F.L. and critical input from all authors. Project funding acquisition: N.P.D., C.B.N., J.E.K., K.J.R. Data Preprocessing: N.P.D., A.I., C.C., A.J., C.P.D., I.T., D.A., L.C-T., E.B.D., D.M.D., N.E., G.P., Formal Analysis and Software was performed by N.P.D., A.I., C.C., A.J., D.W., C.P.D., I.T., C-Y.C. with contributions by C.S., C.D.P., M.S.E., V.H., M.S.E.S. and critical input from D.A., B.A.B., L.C-T., S.W., D.R.W., C.B.N., J.E.K., Visualization: N.P.D., A.I., C.C., A.J., C.S., D.W., with contributions C.P.D., I.T., C.D.P., M.S.E., L.C-T., L.H., J.F.L. These authors contributed equally to this work These authors contributed equally to this work in alphabetic order Print summary – original draft: N.P.D., and AI with input from K.J.R. Author Contributions |
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| Snippet | The molecular pathology of stress-related disorders remains elusive. Our brain multiregion, multiomic study of posttraumatic stress disorder (PTSD) and major... INTRODUCTIONStress-related disorders arise from the interplay between genetic susceptibility and stress exposure, occurring throughout the lifespan.... The molecular pathology of stress-related disorders remains elusive. Our brain multi-omic, multi-region study of posttraumatic stress disorder (PTSD) and major... |
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| SubjectTerms | Amygdala Amygdala - metabolism Biomarkers Biomarkers - metabolism Blood Blood plasma Brain Brain - metabolism Brain mapping Children Chromosome Mapping Dentate gyrus Depressive Disorder, Major - genetics DNA methylation Epigenetics Exons Female Gene expression Gene mapping Gene Regulatory Networks Gene sequencing Genes Genetic Loci Genetics Genome-wide association studies Genome-Wide Association Study Genomes Genomics Health risk assessment Hippocampus Humans Life span Male Mental depression Mental disorders Network analysis Neurons - metabolism Nuclei (cytology) Post traumatic stress disorder Posttraumatic Stress Disorder Prefrontal cortex Prefrontal Cortex - metabolism Proteins Proteomics Psychological stress Risk Sex differences Signal transduction Single-Cell Gene Expression Analysis snRNA Stat3 protein Stress Disorders, Post-Traumatic - genetics Suicide Systems Biology Transcription factors Transcriptomics |
| Title | Systems biology dissection of PTSD and MDD across brain regions, cell types, and blood |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/38781393 https://www.proquest.com/docview/3058761764 https://www.proquest.com/docview/3060375936 https://pubmed.ncbi.nlm.nih.gov/PMC11203158 |
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