Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohorts
Abstract Background The occurrence of post-traumatic stress disorder (PTSD) following a traumatic event is associated with biological differences that can represent the susceptibility to PTSD, the impact of trauma, or the sequelae of PTSD itself. These effects include differences in DNA methylation...
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| author | Seyma Katrinli Agaz H. Wani Adam X. Maihofer Andrew Ratanatharathorn Nikolaos P. Daskalakis Janitza Montalvo-Ortiz Diana L. Núñez-Ríos Anthony S. Zannas Xiang Zhao Allison E. Aiello Allison E. Ashley-Koch Diana Avetyan Dewleen G. Baker Jean C. Beckham Marco P. Boks Leslie A. Brick Evelyn Bromet Frances A. Champagne Chia-Yen Chen Shareefa Dalvie Michelle F. Dennis Segun Fatumo Catherine Fortier Sandro Galea Melanie E. Garrett Elbert Geuze Gerald Grant Michael A. Hauser Jasmeet P. Hayes Sian M. J. Hemmings Bertrand Russel Huber Aarti Jajoo Stefan Jansen Ronald C. Kessler Nathan A. Kimbrel Anthony P. King Joel E. Kleinman Nastassja Koen Karestan C. Koenen Pei-Fen Kuan Israel Liberzon Sarah D. Linnstaedt Adriana Lori Benjamin J. Luft Jurjen J. Luykx Christine E. Marx Samuel A. McLean Divya Mehta William Milberg Mark W. Miller Mary S. Mufford Clarisse Musanabaganwa Jean Mutabaruka Leon Mutesa Charles B. Nemeroff Nicole R. Nugent Holly K. Orcutt Xue-Jun Qin Sheila A. M. Rauch Kerry J. Ressler Victoria B. Risbrough Eugène Rutembesa Bart P. F. Rutten Soraya Seedat Dan J. Stein Murray B. Stein Sylvanus Toikumo Robert J. Ursano Annette Uwineza Mieke H. Verfaellie Eric Vermetten Christiaan H. Vinkers Erin B. Ware Derek E. Wildman Erika J. Wolf Ross McD Young Ying Zhao Leigh L. van den Heuvel PGC-PTSD Epigenetics Workgroup PsychENCODE PTSD Brainomics Project Traumatic Stress Brain Research Group Monica Uddin Caroline M. Nievergelt Alicia K. Smith Mark W. Logue |
| author_facet | Seyma Katrinli Agaz H. Wani Adam X. Maihofer Andrew Ratanatharathorn Nikolaos P. Daskalakis Janitza Montalvo-Ortiz Diana L. Núñez-Ríos Anthony S. Zannas Xiang Zhao Allison E. Aiello Allison E. Ashley-Koch Diana Avetyan Dewleen G. Baker Jean C. Beckham Marco P. Boks Leslie A. Brick Evelyn Bromet Frances A. Champagne Chia-Yen Chen Shareefa Dalvie Michelle F. Dennis Segun Fatumo Catherine Fortier Sandro Galea Melanie E. Garrett Elbert Geuze Gerald Grant Michael A. Hauser Jasmeet P. Hayes Sian M. J. Hemmings Bertrand Russel Huber Aarti Jajoo Stefan Jansen Ronald C. Kessler Nathan A. Kimbrel Anthony P. King Joel E. Kleinman Nastassja Koen Karestan C. Koenen Pei-Fen Kuan Israel Liberzon Sarah D. Linnstaedt Adriana Lori Benjamin J. Luft Jurjen J. Luykx Christine E. Marx Samuel A. McLean Divya Mehta William Milberg Mark W. Miller Mary S. Mufford Clarisse Musanabaganwa Jean Mutabaruka Leon Mutesa Charles B. Nemeroff Nicole R. Nugent Holly K. Orcutt Xue-Jun Qin Sheila A. M. Rauch Kerry J. Ressler Victoria B. Risbrough Eugène Rutembesa Bart P. F. Rutten Soraya Seedat Dan J. Stein Murray B. Stein Sylvanus Toikumo Robert J. Ursano Annette Uwineza Mieke H. Verfaellie Eric Vermetten Christiaan H. Vinkers Erin B. Ware Derek E. Wildman Erika J. Wolf Ross McD Young Ying Zhao Leigh L. van den Heuvel PGC-PTSD Epigenetics Workgroup PsychENCODE PTSD Brainomics Project Traumatic Stress Brain Research Group Monica Uddin Caroline M. Nievergelt Alicia K. Smith Mark W. Logue |
| author_sort | Seyma Katrinli |
| collection | DOAJ |
| description | Abstract Background The occurrence of post-traumatic stress disorder (PTSD) following a traumatic event is associated with biological differences that can represent the susceptibility to PTSD, the impact of trauma, or the sequelae of PTSD itself. These effects include differences in DNA methylation (DNAm), an important form of epigenetic gene regulation, at multiple CpG loci across the genome. Moreover, these effects can be shared or specific to both central and peripheral tissues. Here, we aim to identify blood DNAm differences associated with PTSD and characterize the underlying biological mechanisms by examining the extent to which they mirror associations across multiple brain regions. Methods As the Psychiatric Genomics Consortium (PGC) PTSD Epigenetics Workgroup, we conducted the largest cross-sectional meta-analysis of epigenome-wide association studies (EWASs) of PTSD to date, involving 5077 participants (2156 PTSD cases and 2921 trauma-exposed controls) from 23 civilian and military studies. PTSD diagnosis assessments were harmonized following the standardized guidelines established by the PGC-PTSD Workgroup. DNAm was assayed from blood using Illumina HumanMethylation450 or MethylationEPIC (850 K) BeadChips. Within each cohort, DNA methylation was regressed on PTSD, sex (if applicable), age, blood cell proportions, and ancestry. An inverse variance-weighted meta-analysis was performed. We conducted replication analyses in tissue from multiple brain regions, neuronal nuclei, and a cellular model of prolonged stress. Results We identified 11 CpG sites associated with PTSD in the overall meta-analysis (1.44e − 09 < p < 5.30e − 08), as well as 14 associated in analyses of specific strata (military vs civilian cohort, sex, and ancestry), including CpGs in AHRR and CDC42BPB. Many of these loci exhibit blood–brain correlation in methylation levels and cross-tissue associations with PTSD in multiple brain regions. Out of 9 CpGs annotated to a gene expressed in blood, methylation levels at 5 CpGs showed significant correlations with the expression levels of their respective annotated genes. Conclusions This study identifies 11 PTSD-associated CpGs and leverages data from postmortem brain samples, GWAS, and genome-wide expression data to interpret the biology underlying these associations and prioritize genes whose regulation differs in those with PTSD. |
| format | Article |
| id | doaj-art-e7c75d3d1d50416e99e94207e5bfc3e1 |
| institution | Kabale University |
| issn | 1756-994X |
| language | English |
| publishDate | 2024-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Medicine |
| spelling | doaj-art-e7c75d3d1d50416e99e94207e5bfc3e12024-12-22T12:39:16ZengBMCGenome Medicine1756-994X2024-12-0116111710.1186/s13073-024-01417-1Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohortsSeyma Katrinli0Agaz H. Wani1Adam X. Maihofer2Andrew Ratanatharathorn3Nikolaos P. Daskalakis4Janitza Montalvo-Ortiz5Diana L. Núñez-Ríos6Anthony S. Zannas7Xiang Zhao8Allison E. Aiello9Allison E. Ashley-Koch10Diana Avetyan11Dewleen G. Baker12Jean C. Beckham13Marco P. Boks14Leslie A. Brick15Evelyn Bromet16Frances A. Champagne17Chia-Yen Chen18Shareefa Dalvie19Michelle F. Dennis20Segun Fatumo21Catherine Fortier22Sandro Galea23Melanie E. Garrett24Elbert Geuze25Gerald Grant26Michael A. Hauser27Jasmeet P. Hayes28Sian M. J. Hemmings29Bertrand Russel Huber30Aarti Jajoo31Stefan Jansen32Ronald C. Kessler33Nathan A. Kimbrel34Anthony P. King35Joel E. Kleinman36Nastassja Koen37Karestan C. Koenen38Pei-Fen Kuan39Israel Liberzon40Sarah D. Linnstaedt41Adriana Lori42Benjamin J. Luft43Jurjen J. Luykx44Christine E. Marx45Samuel A. McLean46Divya Mehta47William Milberg48Mark W. Miller49Mary S. Mufford50Clarisse Musanabaganwa51Jean Mutabaruka52Leon Mutesa53Charles B. Nemeroff54Nicole R. Nugent55Holly K. Orcutt56Xue-Jun Qin57Sheila A. M. Rauch58Kerry J. Ressler59Victoria B. Risbrough60Eugène Rutembesa61Bart P. F. Rutten62Soraya Seedat63Dan J. Stein64Murray B. Stein65Sylvanus Toikumo66Robert J. Ursano67Annette Uwineza68Mieke H. Verfaellie69Eric Vermetten70Christiaan H. Vinkers71Erin B. Ware72Derek E. Wildman73Erika J. Wolf74Ross McD Young75Ying Zhao76Leigh L. van den Heuvel77PGC-PTSD Epigenetics WorkgroupPsychENCODE PTSD Brainomics ProjectTraumatic Stress Brain Research GroupMonica Uddin78Caroline M. Nievergelt79Alicia K. Smith80Mark W. Logue81Department of Gynecology and Obstetrics, Emory UniversityGenomics Program, College of Public Health, University of South FloridaDepartment of Psychiatry, University of California San DiegoDepartment of Epidemiology, Columbia University Mailmain School of Public HealthStanley Center for Psychiatric Research, Broad Institute of MIT and HarvardU.S. Department of Veterans Affairs National Center of Posttraumatic Stress Disorder, Clinical Neurosciences DivisionU.S. Department of Veterans Affairs National Center of Posttraumatic Stress Disorder, Clinical Neurosciences DivisionCarolina Stress Initiative, University of North Carolina at Chapel HillDepartment of Biostatistics, Boston University School of Public HealthRobert N. Butler Columbia Aging Center, Department of Epidemiology, Columbia UniversityDuke Molecular Physiology Institute, Duke University Medical CenterDepartment of Psychiatry, University of California San DiegoDepartment of Psychiatry, University of California San DiegoDepartment of Psychiatry and Behavioral Sciences, Duke University School of MedicineDepartment of Psychiatry, Brain Center University Medical Center UtrechtDepartment of Psychiatry and Human Behavior, Alpert Medical School of Brown UniversityEpidemiology Research Group, State University of New York at Stony BrookDepartment of Psychology, The University of Texas at AustinBiogen Inc, Translational SciencesDepartment of Pathology, University of Cape TownDepartment of Psychiatry and Behavioral Sciences, Duke University School of MedicineMRC/UVRI and London School of Hygiene and Tropical Medicine, The African Computational Genomics (TACG) Research GroupDepartment of Psychiatry, Harvard Medical SchoolSchool of Public Health, Boston UniversityDuke Molecular Physiology Institute, Duke University Medical CenterBrain Research and Innovation Centre, Netherlands Ministry of DefenceDepartment of Neurosurgery, Duke University School of MedicineDepartment of Medicine, Duke University School of MedicineDepartment of Psychology, The Ohio State UniversityDepartment of Psychiatry, Faculty of Medicine and Health Sciences, Stellenbosch UniversityDepartment of Neurology, Boston University School of MedicineStanley Center for Psychiatric Research, Broad Institute of MIT and HarvardCollege of Medicine and Health Sciences, University of RwandaDepartment of Health Care Policy, Harvard Medical SchoolDepartment of Psychiatry and Behavioral Sciences, Duke University School of MedicineInstitute for Behavioral Medicine Research, The Ohio State University College of MedicineDepartment of Psychiatry and Behavioral Sciences, Johns Hopkins University School of MedicineDepartment of Psychiatry & Mental Health, University of Cape TownDepartment of Epidemiology, Harvard T.H. Chan School of Public HealthDepartment of Applied Mathematics and Statistics, Stony Brook UniversityDepartment of Psychiatry and Behavioral Sciences, Texas A&M University College of MedicineDepartment of Anesthesiology, University of North Carolina at Chapel HillDepartment of Psychiatry and Behavioral Sciences, Emory UniversityDepartment of Medicine, Stony Brook UniversityAmsterdam Neuroscience Research Institute Stress & Sleep Program, Amsterdam University Medical CenterDepartment of Psychiatry and Behavioral Sciences, Duke University School of MedicineDepartment of Psychiatry, UNC Institute for Trauma RecoveryCentre for Genomics and Personalised Health, Queensland University of TechnologyGRECC/TRACTS, VA Boston Healthcare System Biomedical Genetics & Psychiatry, Boston University Chobanian & Avedisian School of MedicineDepartment of Psychiatry and Mental Health, University of Cape TownResearch Innovation and Data Science Division, Rwanda Biomedical CenterDepartment of Clinical Psychology, University of RwandaCollege of Medicine and Health Sciences, University of RwandaDepartment of Psychology, The University of Texas at AustinDepartment of Emergency Medicine, Alpert Brown Medical SchoolDepartment of Psychology, Northern Illinois UniversityDuke Molecular Physiology Institute, Duke UniversityDepartment of Psychiatry & Behavioral Sciences, Emory UniversityDepartment of Psychiatry, Harvard Medical SchoolDepartment of Psychiatry, University of California San DiegoClinical Psychology, University of RwandaDepartment of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Maastricht Universitair Medisch CentrumDepartment of Psychiatry, Faculty of Medicine and Health Sciences, Stellenbosch UniversityDepartment of Psychiatry & Mental Health, University of Cape TownDepartment of Psychiatry, University of California San DiegoDepartment of Psychiatry, Faculty of Medicine and Health Sciences, Stellenbosch UniversityDepartment of Psychiatry, Center for the Study of Traumatic Stress, Uniformed Services UniversityCollege of Medicine and Health Sciences, University of RwandaDepartment of Psychiatry, Boston University School of MedicineDepartment of Psychiatry, Leiden University Medical CenterDepartment of Anatomy and Neurosciences, Amsterdam UMC Location Vrije Universiteit AmsterdamSurvey Research Center, University of MichiganCollege of Public Health, University of South FloridaNational Center for PTSD, VA Boston Healthcare SystemSchool of Clinical Sciences, Queensland University of TechnologyInstitute for Trauma Recovery, University of North Carolina at Chapel HillDepartment of Psychiatry, Faculty of Medicine and Health Sciences, Stellenbosch UniversityUniversity of South Florida College of Public Health, Genomics ProgramDepartment of Psychiatry, University of California San DiegoDepartment of Gynecology and Obstetrics, Emory UniversityDepartment of Biostatistics, Boston University School of Public HealthAbstract Background The occurrence of post-traumatic stress disorder (PTSD) following a traumatic event is associated with biological differences that can represent the susceptibility to PTSD, the impact of trauma, or the sequelae of PTSD itself. These effects include differences in DNA methylation (DNAm), an important form of epigenetic gene regulation, at multiple CpG loci across the genome. Moreover, these effects can be shared or specific to both central and peripheral tissues. Here, we aim to identify blood DNAm differences associated with PTSD and characterize the underlying biological mechanisms by examining the extent to which they mirror associations across multiple brain regions. Methods As the Psychiatric Genomics Consortium (PGC) PTSD Epigenetics Workgroup, we conducted the largest cross-sectional meta-analysis of epigenome-wide association studies (EWASs) of PTSD to date, involving 5077 participants (2156 PTSD cases and 2921 trauma-exposed controls) from 23 civilian and military studies. PTSD diagnosis assessments were harmonized following the standardized guidelines established by the PGC-PTSD Workgroup. DNAm was assayed from blood using Illumina HumanMethylation450 or MethylationEPIC (850 K) BeadChips. Within each cohort, DNA methylation was regressed on PTSD, sex (if applicable), age, blood cell proportions, and ancestry. An inverse variance-weighted meta-analysis was performed. We conducted replication analyses in tissue from multiple brain regions, neuronal nuclei, and a cellular model of prolonged stress. Results We identified 11 CpG sites associated with PTSD in the overall meta-analysis (1.44e − 09 < p < 5.30e − 08), as well as 14 associated in analyses of specific strata (military vs civilian cohort, sex, and ancestry), including CpGs in AHRR and CDC42BPB. Many of these loci exhibit blood–brain correlation in methylation levels and cross-tissue associations with PTSD in multiple brain regions. Out of 9 CpGs annotated to a gene expressed in blood, methylation levels at 5 CpGs showed significant correlations with the expression levels of their respective annotated genes. Conclusions This study identifies 11 PTSD-associated CpGs and leverages data from postmortem brain samples, GWAS, and genome-wide expression data to interpret the biology underlying these associations and prioritize genes whose regulation differs in those with PTSD.https://doi.org/10.1186/s13073-024-01417-1PTSDTraumaDNA methylationPostmortem brainGWASGene expression |
| spellingShingle | Seyma Katrinli Agaz H. Wani Adam X. Maihofer Andrew Ratanatharathorn Nikolaos P. Daskalakis Janitza Montalvo-Ortiz Diana L. Núñez-Ríos Anthony S. Zannas Xiang Zhao Allison E. Aiello Allison E. Ashley-Koch Diana Avetyan Dewleen G. Baker Jean C. Beckham Marco P. Boks Leslie A. Brick Evelyn Bromet Frances A. Champagne Chia-Yen Chen Shareefa Dalvie Michelle F. Dennis Segun Fatumo Catherine Fortier Sandro Galea Melanie E. Garrett Elbert Geuze Gerald Grant Michael A. Hauser Jasmeet P. Hayes Sian M. J. Hemmings Bertrand Russel Huber Aarti Jajoo Stefan Jansen Ronald C. Kessler Nathan A. Kimbrel Anthony P. King Joel E. Kleinman Nastassja Koen Karestan C. Koenen Pei-Fen Kuan Israel Liberzon Sarah D. Linnstaedt Adriana Lori Benjamin J. Luft Jurjen J. Luykx Christine E. Marx Samuel A. McLean Divya Mehta William Milberg Mark W. Miller Mary S. Mufford Clarisse Musanabaganwa Jean Mutabaruka Leon Mutesa Charles B. Nemeroff Nicole R. Nugent Holly K. Orcutt Xue-Jun Qin Sheila A. M. Rauch Kerry J. Ressler Victoria B. Risbrough Eugène Rutembesa Bart P. F. Rutten Soraya Seedat Dan J. Stein Murray B. Stein Sylvanus Toikumo Robert J. Ursano Annette Uwineza Mieke H. Verfaellie Eric Vermetten Christiaan H. Vinkers Erin B. Ware Derek E. Wildman Erika J. Wolf Ross McD Young Ying Zhao Leigh L. van den Heuvel PGC-PTSD Epigenetics Workgroup PsychENCODE PTSD Brainomics Project Traumatic Stress Brain Research Group Monica Uddin Caroline M. Nievergelt Alicia K. Smith Mark W. Logue Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohorts Genome Medicine PTSD Trauma DNA methylation Postmortem brain GWAS Gene expression |
| title | Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohorts |
| title_full | Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohorts |
| title_fullStr | Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohorts |
| title_full_unstemmed | Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohorts |
| title_short | Epigenome-wide association studies identify novel DNA methylation sites associated with PTSD: a meta-analysis of 23 military and civilian cohorts |
| title_sort | epigenome wide association studies identify novel dna methylation sites associated with ptsd a meta analysis of 23 military and civilian cohorts |
| topic | PTSD Trauma DNA methylation Postmortem brain GWAS Gene expression |
| url | https://doi.org/10.1186/s13073-024-01417-1 |
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epigenomewideassociationstudiesidentifynoveldnamethylationsitesassociatedwithptsdametaanalysisof23militaryandciviliancohorts AT aliciaksmith epigenomewideassociationstudiesidentifynoveldnamethylationsitesassociatedwithptsdametaanalysisof23militaryandciviliancohorts AT markwlogue epigenomewideassociationstudiesidentifynoveldnamethylationsitesassociatedwithptsdametaanalysisof23militaryandciviliancohorts |