Posttraumatic psychopathology and the pace of the epigenetic clock: A longitudinal investigation

Psychological Medicine

Volumn 49, Issue 5, 2019, Pages 791-800

  Wolf, Erika J ^a,b   Logue, Mark W ^a,b   Morrison, Filomene G ^a,b   Wilcox, Elizabeth S ^a   Stone, Annjanette ^c   Schichman, Steven A ^c   McGlinchey, Regina E ^a,d   Milberg, William P ^a,d   Miller, Mark W ^a,b  

^a VA BOSTON HEALTHCARE SYSTEM   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Alcohol use disorders; DNA methylation age; Epigenetic age; Longitudinal; PTSD

Indexed keywords

ADULT; CELL AGING; CROSS-SECTIONAL STUDY; DNA METHYLATION; FEMALE; GENETIC EPIGENESIS; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GOVERNMENT; HUMAN; INJURY SCALE; LONGITUDINAL STUDY; MALE; MENTAL DISEASE; POSTTRAUMATIC STRESS DISORDER; PSYCHOLOGY; REGRESSION ANALYSIS; UNITED STATES; YOUNG ADULT;

ADULT; CELLULAR SENESCENCE; CROSS-SECTIONAL STUDIES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LONGITUDINAL STUDIES; MALE; PSYCHOPATHOLOGY; REGRESSION ANALYSIS; STRESS DISORDERS, POST-TRAUMATIC; TRAUMA SEVERITY INDICES; UNITED STATES; UNITED STATES DEPARTMENT OF VETERANS AFFAIRS; YOUNG ADULT;

EID: 85048747707     PISSN: 00332917     EISSN: 14698978     Source Type: Journal    
DOI: 10.1017/S0033291718001411     Document Type: Article

References (59)

1. Achur RN, Freeman WM and Vrana KE (2010) Circulating cytokines as biomarkers of alcohol abuse and alcoholism. Journal of Neuroimmune Pharmacology 5, 83-91.
2. Aiello AE, Dowd JB, Jayabalasingham B, Feinstein L, Uddin M, Simanek AM, Cheng CK, Galea S, Wildman DE and Koenen K (2016) PTSD is associated with an increase in aged T cell phenotypes in adults living in Detroit. Psychoneuroendocrinology 67, 133-141.
3. Antoni FA, Hunter EF, Lowry PJ, Noble JM and Seckl JR (1992) Atriopeptin: An endogenous corticotropin-release inhibiting hormone. Endocrinology 130, 1753-1755.
4. Beech RD, Qu J, Leffert JJ, Lin A, Hong KA, Hansen J, Umlauf S, Mane S, Zhao H and Sinha R (2012) Altered expression of cytokine signaling pathway genes in peripheral blood cells of alcohol dependent subjects: Preliminary findings. Alcoholism: Clinical and Experimental Research 36, 1487-1496.
5. Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS and Keane TM (1995) The development of a clinician-administered PTSD scale. Journal of Traumatic Stress 8, 75-90.
6. Boks MP, van Mierlo HC, Rutten BP, Radstake TR, De Witte L, Geuze E, Horvath S, Schalkwyk LC, Vinkers CH, Broen JC and Vermetten E (2015) Longitudinal changes of telomere length and epigenetic age related to traumatic stress and post-traumatic stress disorder. Psychoneuroendocrinology 51, 506-512.
7. Breen MS, Maihofer AX, Glatt SJ, Tylee DS, Chandler SD, Tsuang MT, Risbrough VB, Baker DG, OConnor DT, Nievergelt CM and Woelk CH (2015) Gene networks specific for innate immunity define posttraumatic stress disorder. Molecular Psychiatry 20, 1538-1545.
8. Breton CV, Marsit CJ, Faustman E, Nadeau K, Goodrich JM, Dolinoy DC, Herbstman J, Holland N, LaSalle JM, Schmidt R, Yousefi P, Perera F, Joubert BR, Wiemels J, Taylor M, Yang IV, Chen R, Hew KM, Freeland DM, Miller R and Murphy SK (2017) Small-magnitude effect sizes in epigenetic end points are important in childrens environmental health studies: The Childrens Environmental Health and Disease Prevention Research Centers Epigenetics Working Group. Environmental Health Perspectives 125, 511-526.
9. Carroll JE, Irwin MR, Levine M, Seeman TE, Absher D, Assimes T and Horvath S (2017) Epigenetic aging and immune senescence in women with insomnia symptoms: Findings from the womens health initiative study. Biological Psychiatry 81, 136-144.
10. Chen BH, Marioni RE, Colicino E, Peters MJ, Ward-Caviness CK, Tsai PC, Roetker NS, Just AC, Demerath EW, Guan W, Bressler J, Fornage M, Studenski S, Vandiver AR, Moore AZ, Tanaka T, Kiel DP, Liang L, Vokonas P, Schwartz J, Lunetta KL, Murabito JM, Bandinelli S, Hernandez DG, Melzer D, Nalls M, Pilling LC, Price TR, Singleton AB, Gieger C, Holle R, Kretschmer A, Kronenberg F, Kunze S, Linseisen J, Meisinger C, Rathmann W, Waldenberger M, Visscher PM, Shah S, Wray NR, McRae AF, Franco OH, Hofman A, Uitterlinden AG, Absher D, Assimes T, Levine ME, Lu AT, Tsao PS, Hou L, Manson JE, Carty CL, LaCroix AZ, Reiner AP, Spector TD, Feinberg AP, Levy D, Baccarelli A, van Meurs J, Bell JT, Peters A, Deary IJ, Pankow JS, Ferrucci L and Horvath S (2016) DNA methylationbased measures of biological age: Meta-analysis predicting time to death. Aging (Albany NY) 8, 1844-1865.
11. Cook RT, Ballas ZK, Waldschmidt TJ, Vandersteen D, LaBrecque DR and Cook BL (1995) Modulation of T-cell adhesion markers, and the CD45R and CD57 antigens in human alcoholics. Alcoholism: Clinical and Experimental Research 19, 555-563.
12. Cook RT, Waldschmidt TJ, Ballas ZK, Cook BL, Booth BM, Stewart BC and Garvey MJ (1994) Fine T-cell subsets in alcoholics as determined by the expression of l-selectin, leukocyte common antigen, and-integrin. Alcoholism: Clinical and Experimental Research 18, 71-80.
13. Darrow SM, Verhoeven JE, Revesz D, Lindqvist D, Penninx BW, Delucchi KL, Wolkowitz OM and Mathews CA (2016) The association between psychiatric disorders and telomere length: A meta-analysis involving 14, 827 persons. Psychosomatic Medicine 78, 776-787.
14. Davis EG, Humphreys KL, McEwen LM, Sacchet MD, Camacho MC, MacIsaac JL, Lin DTS, Kobor MS and Gotlib IH (2017) Accelerated DNA methylation age in adolescent girls: Associations with elevated diurnal cortisol and reduced hippocampal volume. Translational Psychiatry 7, e1223.
15. Durso DF, Bacalini MG, Sala C, Pirazzini C, Marasco E, Bonafé M, do Valle IF, Gentilini D, Castellani G and Faria AMC (2017) Acceleration of leukocytes epigenetic age as an early tumor and sex-specific marker of breast and colorectal cancer. Oncotarget 8, 23237.
16. First MB, Gibbon M, Spitzer RL and Benjamin LS (1997). Users Guide for the Structured Clinical Interview for DSM-IV Axis II Personality Disorders: SCID-II. Washington, DC: American Psychiatric Association Publishing.
17. Fülöp T, Dupuis G, Witkowski JM and Larbi A (2016) The role of immunosenescence in the development of age-related diseases. Revista de Investigación Clínica 68, 84-91.
18. Glahn A, Riera Knorrenschild R, Rhein M, Haschemi Nassab M, Groschl M, Heberlein A, Muschler M, Frieling H, Bleich S and Hillemacher T (2014) Alcohol-induced changes in methylation status of individual CpG sites, and serum levels of vasopressin and atrial natriuretic peptide in alcohol-dependent patients during detoxification treatment. European Addiction Research 20, 143-150.
19. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, Klotzle B, Bibikova M, Fan JB, Gao Y, Deconde R, Chen M, Rajapakse I, Friend S, Ideker T and Zhang K (2013) Genome-wide methylation profiles reveal quantitative views of human aging rates. Molecular Cell 49, 359-367.
20. Harlaar N, Bryan AD, Thayer RE, Karoly HC, Oien N and Hutchison KE (2014) Methylation of a CpG site near the ALDH1A2 gene is associated with loss of control over drinking and related phenotypes. Alcoholism: Clinical and Experimental Research 38, 713-721.
21. Horvath S (2013) DNA methylation age of human tissues and cell types. Genome Biology 14, R115.
22. Horvath S, Gurven M, Levine ME, Trumble BC, Kaplan H, Allayee H, Ritz BR, Chen B, Lu AT, Rickabaugh TM, Jamieson BD, Sun D, Li S, Chen W, Quintana-Murci L, Fagny M, Kobor MS, Tsao PS, Reiner AP, Edlefsen KL, Absher D and Assimes TL (2016) An epigenetic clock analysis of race/ethnicity, sex, and coronary heart disease. Genome Biology 17, 171.
23. Jovanovic T, Vance LA, Cross D, Knight AK, Kilaru V, Michopoulos V, Klengel T and Smith AK (2017) Exposure to violence accelerates epigenetic aging in children. Scientific Reports 7, 8962.
24. Kananen L, Marttila S, Nevalainen T, Kummola L, Junttila I, Mononen N, Kähönen M, Raitakari O, Hervonen A and Jylhä M (2016) The trajectory of the blood DNA methylome ageing rate is largely set before adulthood: Evidence from two longitudinal studies. Age 38, 65.
25. Kessler RC, Sonnega A, Bromet E, Hughes M and Nelson CB (1995) Posttraumatic stress disorder in the National Comorbidity Survey. Archives of General Psychiatry 52, 1048-1060.
26. Kozlenkov A, Jaffe AE, Timashpolsky A, Apontes P, Rudchenko S, Barbu M, Byne W, Hurd YL, Horvath S and Dracheva S (2017) DNA methylation profiling of human prefrontal cortex neurons in heroin users shows significant difference between genomic contexts of hyper-and hypomethylation and a younger epigenetic age. Genes 8, 152.
27. Kubany ES, Haynes SN, Leisen MB, Owens JA, Kaplan AS, Watson SB and Burns K (2000) Development and preliminary validation of a brief broadspectrum measure of trauma exposure: The Traumatic Life Events Questionnaire. Psychological Assessment 12, 210-224.
28. Leclercq S, Cani PD, Neyrinck AM, Starkel P, Jamar F, Mikolajczak M, Delzenne NM and de Timary P (2012) Role of intestinal permeability and inflammation in the biological and behavioral control of alcoholdependent subjects. Brain, Behavior, and Immunity 26, 911-918.
29. LevineME, Lu AT, Bennett DA and Horvath S (2015) Epigenetic age of the prefrontal cortex is associatedwith neuritic plaques, amyloid load, and Alzheimers disease related cognitive functioning. Aging (Albany NY) 7, 1198-1211.
30. Liu C, Marioni RE, Hedman AK, Pfeiffer L, Tsai PC, Reynolds LM, Just AC, Duan Q, Boer CG, Tanaka T, Elks CE, Aslibekyan S, Brody JA, Kuhnel B, Herder C, Almli LM, Zhi D, Wang Y, Huan T, Yao C, Mendelson MM, Joehanes R, Liang L, Love SA, Guan W, Shah S, McRae AF, Kretschmer A, Prokisch H, Strauch K, Peters A, Visscher PM, Wray NR, Guo X, Wiggins KL, Smith AK, Binder EB, Ressler KJ, Irvin MR, Absher DM, Hernandez D, Ferrucci L, Bandinelli S, Lohman K, Ding J, Trevisi L, Gustafsson S, Sandling JH, Stolk L, Uitterlinden AG, Yet I, Castillo-Fernandez JE, Spector TD, Schwartz JD, Vokonas P, Lind L, Li Y, Fornage M, Arnett DK, Wareham NJ, Sotoodehnia N, Ong KK, van Meurs JB, Conneely KN, Baccarelli AA, Deary IJ, Bell JT, North KE, Liu Y, Waldenberger M, London SJ, Ingelsson E and Levy D (2016) A DNA methylation biomarker of alcohol consumption. Molecular Psychiatry 23, 422-433.
31. Logue MW, Smith AK, Wolf EJ, Maniates H, Stone A, Schichman SA, McGlinchey RE, Milberg W and Miller MW (2017) The correlation of methylation levels measured using Illumina 450 K and EPIC BeadChips in blood samples. Epigenomics 9, 1363-1371.
32. Macaulay R, Akbar AN and Henson SM (2013) The role of the T cell in age-related inflammation. Age 35, 563-572.
33. Marioni RE, Shah S, McRae AF, Chen BH, Colicino E, Harris SE, Gibson J, Henders AK, Redmond P, Cox SR, Pattie A, Corley J, Murphy L, Martin NG, Montgomery GW, Feinberg AP, Fallin MD, Multhaup ML, Jaffe AE, Joehanes R, Schwartz J, Just AC, Lunetta KL, Murabito JM, Starr JM, Horvath S, Baccarelli AA, Levy D, Visscher PM, Wray NR and Deary IJ (2015) DNA methylation age of blood predicts all-cause mortality in later life. Genome Biology 16, 25.
34. McGlinchey RE, Milberg WP, Fonda JR and Fortier CB (2017). A methodology for assessing deployment trauma and its consequences in OEF/OIF/OND veterans: The TRACTS longitudinal prospective cohort study. International Journal of Methods in Psychiatric Research 26, e1556.
35. McKinney BC, Lin H, Ding Y, Lewis DA and Sweet RA (2017) DNA methylation evidence against the accelerated aging hypothesis of schizophrenia. NPJ Schizophrenia 3, 13.
36. MillerMW, Lin AP, Wolf EJ and Miller DR (2017) Oxidative stress, inflammation, and neuroprogression in chronic PTSD. Harvard Review of Psychiatry 26, 57-69.
37. Miller MW, Wolf EJ, Reardon A, Greene A, Ofrat S and McInerney S (2012) Personality and the latent structure of PTSD comorbidity. Journal of Anxiety Disorders 26, 599-607.
38. Muschler MA, Hillemacher T, Kraus C, Kornhuber J, Bleich S and Frieling H (2010) DNA methylation of the POMC gene promoter is associated with craving in alcohol dependence. Journal of Neural Transmission (Vienna) 117, 513-519.
39. Passos IC, Vasconcelos-MorenoMP, Costa LG, Kunz M, Brietzke E, Quevedo J, Salum G, Magalhães PV, Kapczinski F and Kauer-SantAnna M (2015) Inflammatory markers in post-traumatic stress disorder: A systematic review, meta-analysis, and meta-regression. The Lancet Psychiatry 2, 1002-1012.
40. Perna L, Zhang Y, Mons U, Holleczek B, Saum KU and Brenner H (2016) Epigenetic age acceleration predicts cancer, cardiovascular, and all-cause mortality in a German case cohort. Clinical Epigenetics 8, 64.
41. Philibert RA, Penaluna B, White T, Shires S, Gunter T, Liesveld J, Erwin C, Hollenbeck N and Osborn T (2014) A pilot examination of the genome-wide DNA methylation signatures of subjects entering and exiting short-term alcohol dependence treatment programs. Epigenetics 9, 1212-1219.
42. Quach A, Levine ME, Tanaka T, Lu AT, Chen BH, Ferrucci L, Ritz B, Bandinelli S, Neuhouser ML and Beasley JM (2017) Epigenetic clock analysis of diet, exercise, education, and lifestyle factors. Aging (Albany NY) 9, 419.
43. Ratanatharathorn A, Boks MP, Maihofer AX, Aiello AE, Amstadter AB, Ashley-Koch AE, Baker DG, Beckham JC, Bromet E, Dennis M, Garrett ME, Geuze E, Guffanti G, Hauser MA, Kilaru V, Kimbrel NA, Koenen KC, Kuan PF, Logue MW, Luft BJ, Miller MW, Mitchell C, Nugent NR, Ressler KJ, Rutten BPF, Stein MB, Vermetten E, Vinkers CH, Youssef NA, Workgroup VAM-AM, Workgroup PPE, Uddin M, Nievergelt CM and Smith AK (2017) Epigenome-wide association of PTSD from heterogeneous cohorts with a common multi-site analysis pipeline. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics 174, 619-630.
44. Sommershof A, Aichinger H, Engler H, Adenauer H, Catani C, Boneberg E-M, Elbert T, Groettrup M and Kolassa I-T (2009) Substantial reduction of naive and regulatory T cells following traumatic stress. Brain, Behavior, and Immunity 23, 1117-1124.
45. Spitzer R, Gibbon M and Williams J (1998) Structured Clinical Interview for DSM-IV Axis I Disorders: Patient Edition (February 1996 Final). New York, NY: Biometrics Research Department, New York State Psychiatric Institute.
46. Strohle A, Feller C, Strasburger CJ, Heinz A and Dimeo F (2006) Anxiety modulation by the heart Aerobic exercise and atrial natriuretic peptide. Psychoneuroendocrinology 31, 1127-1130.
47. Szabo G and Mandrekar P (2009) A recent perspective on alcohol, immunity, and host defense. Alcoholism: Clinical and Experimental Research 33, 220-232.
48. Voisey J, Lawford BR, Morris CP, Wockner LF, Noble EP, Young RM and Mehta D (2017) Epigenetic analysis confirms no accelerated brain aging in schizophrenia. NPJ Schizophrenia 3, 26.
49. Weidner CI and Wagner W (2014) The epigenetic tracks of aging. Biological Chemistry 395, 1307-1314.
50. WiedemannK, JahnH, YassouridisAandKellnerM(2001)Anxiolyticlike effects of atrial natriuretic peptide on cholecystokinin tetrapeptide-induced panic attacks: Preliminary findings. Archives of General Psychiatry 58, 371-377.
51. Wolf EJ and Morrison FM (2017) Traumatic stress and accelerated cellular aging: From epigenetics to cardiometabolic disease. Current Psychiatry Reports 19, 75.
52. Wolf EJ, Logue MW, Hayes JP, Sadeh N, Schichman SA, Stone A, Salat DH, MilbergW, McGlinchey R andMillerMW(2016) Accelerated DNAmethylationage: Associationswith PTSDand neural integrity. Psychoneuroendocrinology 63, 155-162.
53. Wolf EJ, Logue MW, Stoop TB, Schichman SA, Stone A, Sadeh N, Hayes JP and Miller MW (2017). Accelerated DNA methylation age: Associations with PTSD and mortality. Psychosomatic Medicine 80, 42-48.
54. Wolf EJ, Maniates H, Nugent N, Maihofer AX, Armstrong D, Ratanatharathorn A, Ashley-Koch AE, Garrett M, Kimbrel NA, Lori A, Va Aiello AE, Baker DG, Beckham JC, Boks MP, Galea S, Geuze E, Hauser MA, Kessler RC, Koenen KC, Miller MW, Ressler KJ, Risbrough V, Rutten BPF, Stein MB, Ursano RJ, Vermetten E, Vinkers CH, Uddin M, Smith AK, Nievergelt CM and LogueMW(2018) Traumatic stress and accelerated DNA methylation age: A meta-analysis. Psychoneuroendocrinology 92, 123-134.
55. Zannas AS, Arloth J, Carrillo-Roa T, Iurato S, Roh S, Ressler KJ, Nemeroff CB, Smith AK, Bradley B, Heim C, Menke A, Lange JF, Bruckl T, Ising M, Wray NR, Erhardt A, Binder EB and Mehta D (2015) Lifetime stress accelerates epigenetic aging in an urban, African American cohort: Relevance of glucocorticoid signaling. Genome Biology 16, 266.
56. Zhang H and Gelernter J (2017) DNA methylation and alcohol use disorders: Progress and challenges. The American Journal on Addictions 26, 502-515.
57. Zhang R, Miao Q, Wang C, Zhao R, Li W, Haile CN, HaoWand Zhang XY (2013) Genome-wide DNA methylation analysis in alcohol dependence. Addiction Biology 18, 392-403.
58. Zhao R, Zhang R, Li W, Liao Y, Tang J, Miao Q and Hao W (2013) Genome-wide DNA methylation patterns in discordant sib pairs with alcohol dependence. Asia-Pacific Psychiatry 5, 39-50.
59. Zheng Y, Joyce BT, Colicino E, Liu L, Zhang W, Dai Q, Shrubsole MJ, Kibbe WA, Gao T, Zhang Z, Jafari N, Vokonas P, Schwartz J, Baccarelli AA and Hou L (2016) Blood epigenetic age may predict cancer incidence and mortality. EBioMedicine 5, 68-73.