Interaction between early-life stress and FKBP5 gene variants in major depressive disorder and post-traumatic stress disorder: A systematic review and meta-analysis

Journal of Affective Disorders

Volumn 225, Issue , 2018, Pages 422-428

  Wang, Qingzhong ^a   Shelton, Richard C ^a   Dwivedi, Yogesh ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

FKBP5; Gene environment interaction; Meta analysis; Risk alleles; Systematic review

Indexed keywords

PROTEIN; PROTEIN FKBP5; UNCLASSIFIED DRUG; FK 506 BINDING PROTEIN; TACROLIMUS BINDING PROTEIN 5;

ALLELE; ARTICLE; EARLY LIFE STRESS; ETHNICITY; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; MAJOR DEPRESSION; MEDLINE; META ANALYSIS; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PSYCINFO; SENSITIVITY ANALYSIS; SYSTEMATIC REVIEW; ADULT; CHILD; CHILD ABUSE; CHILD ABUSE SURVIVOR; DEPRESSION; FEMALE; GENETICS; GENOTYPE; MALE; MENTAL STRESS; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICS AND NUMERICAL DATA;

ADULT; ADULT SURVIVORS OF CHILD ABUSE; ALLELES; CHILD; CHILD ABUSE; DEPRESSION; DEPRESSIVE DISORDER, MAJOR; FEMALE; GENE-ENVIRONMENT INTERACTION; GENOTYPE; HUMANS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK FACTORS; STRESS DISORDERS, POST-TRAUMATIC; STRESS, PSYCHOLOGICAL; TACROLIMUS BINDING PROTEINS;

EID: 85028035144     PISSN: 01650327     EISSN: 15732517     Source Type: Journal    
DOI: 10.1016/j.jad.2017.08.066     Document Type: Article

References (65)

1. Alexander, N., Kuepper, Y., Schmitz, A., Osinsky, R., Kozyra, E., Hennig, J., Gene–environment interactions predict cortisol responses after acute stress: implications for the etiology of depression. Psychoneuroendocrinology 34 (2009), 1294–1303.
2. Anda, R.F., Felitti, V.J., Bremner, J.D., Walker, J.D., Whitfield, C., Perry, B.D., Dube, S.R., Giles, W.H., The enduring effects of abuse and related adverse experiences in childhood. Eur. Arch. Psychiatry Clin. Neurosci. 256 (2006), 174–186.
3. Appel, K., Schwahn, C., Mahler, J., Schulz, A., Spitzer, C., Fenske, K., Stender, J., Barnow, S., John, U., Teumer, A., Moderation of adult depression by a polymorphism in the FKBP5 gene and childhood physical abuse in the general population. Neuropsychopharmacology 36 (2011), 1982–1991.
4. Bandoli, G., Campbell-Sills, L., Kessler, R., Heeringa, S., Nock, M., Rosellini, A., Sampson, N., Schoenbaum, M., Ursano, R., Stein, M., Childhood adversity, adult stress, and the risk of major depression or generalized anxiety disorder in US soldiers: a test of the stress sensitization hypothesis. Psychol. Med. 26 (2017), 1–14.
5. Baughman, G., Wiederrecht, G.J., Chang, F., Martin, M.M., Bourgeois, S., Tissue distribution and abundance of human FKBP51, an FK506-binding protein that can mediate calcineurin inhibition. Biochem. Biophys. Res. Commun. 232 (1997), 437–443.
6. Begg, C.B., Mazumdar, M., Operating characteristics of a rank correlation test for publication bias. Biometrics, 1994, 1088–1101.
7. Bevilacqua, L., Carli, V., Sarchiapone, M., George, D.K., Goldman, D., Roy, A., Enoch, M.-A., Interaction between FKBP5 and childhood trauma and risk of aggressive behavior. Arch. Gen. Psychiatry 69 (2012), 62–70.
8. Binder, E.B., Understanding gene × early adversity interactions: possibilities for insight in the biology of psychiatric disorders. Eur. Arch. Psychiatry Clin. Neurosci. 267 (2017), 183–185.
9. Binder, E.B., Salyakina, D., Lichtner, P., Wochnik, G.M., Ising, M., Pütz, B., Papiol, S., Seaman, S., Lucae, S., Kohli, M.A., Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat. Genet. 36 (2004), 1319–1325.
10. Binder, E.B., Bradley, R.G., Liu, W., Epstein, M.P., Deveau, T.C., Mercer, K.B., Tang, Y., Gillespie, C.F., Heim, C.M., Nemeroff, C.B., Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. J. Am. Med. Assoc. 299 (2008), 1291–1305.
11. Boscarino, J.A., Erlich, P.M., Hoffman, S.N., Zhang, X., Higher FKBP5, COMT, CHRNA5, and CRHR1 allele burdens are associated with PTSD and interact with trauma exposure: implications for neuropsychiatric research and treatment. Neuropsychiatr. Dis. Treat. 8 (2012), 131–139.
12. Bremner, J.D., Southwick, S.M., Johnson, D.R., Yehuda, R., Charney, D.S., Childhood physical abuse and combat-related posttraumatic stress disorder in Vietnam veterans. Am. J. Psychiatry, 150, 1993, 235.
13. Breslau, N., Chilcoat, H.D., Kessler, R.C., Davis, G.C., Previous exposure to trauma and PTSD effects of subsequent trauma: results from the detroit area survey of trauma. Am. J. Psychiatry 156 (1999), 902–907.
14. Chapman, D.P., Whitfield, C.L., Felitti, V.J., Dube, S.R., Edwards, V.J., Anda, R.F., Adverse childhood experiences and the risk of depressive disorders in adulthood. J. Affect. Disord. 82 (2004), 217–225.
15. Cochran, W.G., The combination of estimates from different experiments. Biometrics 10 (1954), 101–129.
16. Collip, D., Myin-Germeys, I., Wichers, M., Jacobs, N., Derom, C., Thiery, E., Lataster, T., Simons, C., Delespaul, P., Marcelis, M., FKBP5 as a possible moderator of the psychosis-inducing effects of childhood trauma. Br. J. Psychiatry 202 (2013), 261–268.
17. Cougle, J.R., Timpano, K.R., Sachs-Ericsson, N., Keough, M.E., Riccardi, C.J., Examining the unique relationships between anxiety disorders and childhood physical and sexual abuse in the National Comorbidity Survey-Replication. Psychiatry Res. 177 (2010), 150–155.
18. Dackis, M.N., Rogosch, F.A., Oshri, A., Cicchetti, D., The role of limbic system irritability in linking history of childhood maltreatment and psychiatric outcomes in low-income, high-risk women: moderation by FK506 binding protein 5 haplotype. Dev. Psychopathol. 24 (2012), 1237–1252.
19. De Bellis, M.D., Chrousos, G.P., Dorn, L.D., Burke, L., Helmers, K., Kling, M.A., Trickett, P.K., Putnam, F.W., Hypothalamic-pituitary-adrenal axis dysregulation in sexually abused girls. J. Clin. Endocrinol. Metab. 78 (1994), 249–255.
20. Dube, S.R., Anda, R.F., Felitti, V.J., Chapman, D.P., Williamson, D.F., Giles, W.H., Childhood abuse, household dysfunction, and the risk of attempted suicide throughout the life span: findings from the Adverse Childhood Experiences Study. J. Am. Med. Assoc. 286 (2001), 3089–3096.
21. Dunn, E.C., Solovieff, N., Lowe, S.R., Gallagher, P.J., Chaponis, J., Rosand, J., Koenen, K.C., Waters, M.C., Rhodes, J.E., Smoller, J.W., Interaction between genetic variants and exposure to Hurricane Katrina on post-traumatic stress and post-traumatic growth: a prospective analysis of low income adults. J. Affect. Disord. 152 (2014), 243–249.
22. Dunn, E.C., Nishimi, K., Powers, A., Bradley, B., Is developmental timing of trauma exposure associated with depressive and post-traumatic stress disorder symptoms in adulthood?. J. Psychiatr. Res. 84 (2017), 119–127.
23. Ellsworth, K.A., Eckloff, B.W., Li, L., Moon, I., Fridley, B.L., Jenkins, G.D., Carlson, E., Brisbin, A., Abo, R., Bamlet, W., Contribution of FKBP5 genetic variation to gemcitabine treatment and survival in pancreatic adenocarcinoma. PLoS One, 8, 2013, e70216.
24. Ellsworth, K.A., Moon, I., Eckloff, B.W., Fridley, B.L., Jenkins, G.D., Batzler, A., Biernacka, J.M., Abo, R., Brisbin, A., Ji, Y., FKBP5 genetic variation: association with selective serotonin reuptake inhibitor treatment outcomes in major depressive disorder. Pharm. Genom., 23, 2013, 156.
25. Felitti, V.J., Anda, R.F., Nordenberg, D., Williamson, D.F., Spitz, A.M., Edwards, V., Koss, M.P., Marks, J.S., Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults: the Adverse Childhood Experiences (ACE) Study. Am. J. Prev. Med. 14 (1998), 245–258.
26. Heim, C., Nemeroff, C.B., The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49 (2001), 1023–1039.
27. Heim, C., Newport, D.J., Heit, S., Graham, Y.P., Wilcox, M., Bonsall, R., Miller, A.H., Nemeroff, C.B., Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. J. Am. Med. Assoc. 284 (2000), 592–597.
28. Heim, C., Newport, D.J., Mletzko, T., Miller, A.H., Nemeroff, C.B., The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33 (2008), 693–710.
29. Higgins, J.P., Thompson, S.G., Deeks, J.J., Altman, D.G., Measuring inconsistency in meta-analyses. Br. Med. J. 327 (2003), 557–560.
30. Karg, K., Burmeister, M., Shedden, K., Sen, S., The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch. Gen. Psychiatry 68 (2011), 444–454.
31. Kim, J.S., Lee, S.-H., Influence of interactions between genes and childhood trauma on refractoriness in psychiatric disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 70 (2016), 162–169.
32. Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J.C., Pariante, C.M., Pace, T.W., Mercer, K.B., Mayberg, H.S., Bradley, B., Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat. Neurosci. 16 (2013), 33–41.
33. Koenen, K., Saxe, G., Purcell, S., Smoller, J., Bartholomew, D., Miller, A., Hall, E., Kaplow, J., Bosquet, M., Moulton, S., Polymorphisms in FKBP5 are associated with peritraumatic dissociation in medically injured children. Mol. Psychiatry 10 (2005), 1058–1059.
34. Kohrt, B.A., Worthman, C.M., Ressler, K.J., Mercer, K.B., Upadhaya, N., Koirala, S., Nepal, M.K., Sharma, V.D., Binder, E.B., Cross-cultural gene- environment interactions in depression, post-traumatic stress disorder, and the cortisol awakening response: FKBP5 polymorphisms and childhood trauma in South Asia: gxe interactions in South Asia. Int. Rev. Psychiatry 27 (2015), 180–196.
35. Lahti, J., Ala-Mikkula, H., Kajantie, E., Haljas, K., Eriksson, J.G., Räikkönen, K., Associations between self-reported and objectively recorded early life stress, FKBP5 polymorphisms, and depressive symptoms in midlife. Biol. Psychiatry 80 (2016), 869–877.
36. Lavebratt, C., Åberg, E., Sjöholm, L.K., Forsell, Y., Variations in FKBP5 and BDNF genes are suggestively associated with depression in a Swedish population-based cohort. J. Affect. Disord. 125 (2010), 249–255.
37. Lesch, K.P., Gene-environment interaction and the genetics of depression. J. Psychiatry Neurosci., 29, 2004, 174.
38. Lohoff, F.W., Overview of the genetics of major depressive disorder. Curr. Psychiatry Rep. 12 (2010), 539–546.
39. Meaney, M.J., Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24 (2001), 1161–1192.
40. Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Br. Med. J, 339, 2009, b2535.
41. Nanni, V., Uher, R., Danese, A., Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: a meta-analysis. Am. J. Psychiatry, 2012.
42. Nemeroff, C.B., Owens, M.J., Pharmacologic differences among the SSRIs: focus on monoamine transporters and the HPA axis. CNS Spectr. 9 (2004), 23–31.
43. Rein, T., FK506 binding protein 51 integrates pathways of adaptation. BioEssays 38 (2016), 894–902.
44. Riggs, D.L., Roberts, P.J., Chirillo, S.C., Cheung‐Flynn, J., Prapapanich, V., Ratajczak, T., Gaber, R., Picard, D., Smith, D.F., The Hsp90‐binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. EMBO J. 22 (2003), 1158–1167.
45. Roy, A., Gorodetsky, E., Yuan, Q., Goldman, D., Enoch, M.-A., Interaction of FKBP5, a stress-related gene, with childhood trauma increases the risk for attempting suicide. Neuropsychopharmacology 35 (2010), 1674–1683.
46. Roy, A., Hodgkinson, C.A., DeLuca, V., Goldman, D., Enoch, M.-A., Two HPA axis genes, CRHBP and FKBP5, interact with childhood trauma to increase the risk for suicidal behavior. J. Psychiatr. Res. 46 (2012), 72–79.
47. Sanchez, M., Lyon, C., Noble, P., Crawford, J., Boudreau, M., Higley, J., Nemeroff, C., Plotsky, P., Newman, T., Winslow, J., Maternal separation alters hypothalamic-pituitary-adrenal (HPA) axis function in rhesus macaques: effects of sex and serotonin transporter gene variation. Biol. Psychiatry, 2005, 57S–58S (ELSEVIER SCIENCE INC 360 PARK AVE SOUTH, NEW YORK, NY 10010-1710 USA).
48. Saveanu, R.V., Nemeroff, C.B., Etiology of depression: genetic and environmental factors. Psychiatr. Clin. N. Am. 35 (2012), 51–71.
49. Scharf, S.H., Liebl, C., Binder, E.B., Schmidt, M.V., Müller, M.B., Expression and regulation of the Fkbp5 gene in the adult mouse brain. PLoS One, 6, 2011, e16883.
50. Schmidt, F.L., Hunter, J.E., Methods of Meta-Analysis: Correcting Error and Bias in Research Findings. 2014, Sage publications, London.
51. Taylor, A., Kim-Cohen, J., Meta-analysis of gene–environment interactions in developmental psychopathology. Dev. Psychopathol. 19 (2007), 1029–1037.
52. Thapar, A., McGuffin, P., Genetic influences on life events in childhood. Psychol. Med. 26 (1996), 813–820.
53. Thapar, A., Harold, G., McGuffin, P., Life events and depressive symptoms in childhood—shared genes or shared adversity? A research note. J. Child Psychol. Psychiatry 39 (1998), 1153–1158.
54. Tozzi, L., Carballedo, A., Wetterling, F., McCarthy, H., O'Keane, V., Gill, M., Morris, D., Fahey, C., Meaney, J., Frodl, T., Single-Nucleotide Polymorphism of the FKBP5 Gene and Childhood Maltreatment as Predictors of Structural Changes in Brain Areas Involved in Emotional Processing in Depression. Neuropsychopharmacology 41 (2016), 487–497.
55. van Bodegom, M., Homberg, J.R., Henckens, M.J., Modulation of the hypothalamic-pituitary-adrenal axis by early life stress exposure. Front. Cell Neurosci., 11, 2017.
56. VanZomeren-Dohm, A.A., Pitula, C.E., Koss, K.J., Thomas, K., Gunnar, M.R., FKBP5 moderation of depressive symptoms in peer victimized, post-institutionalized children. Psychoneuroendocrinology 51 (2015), 426–430.
57. Weaver, I.C., Champagne, F.A., Brown, S.E., Dymov, S., Sharma, S., Meaney, M.J., Szyf, M., Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 25 (2005), 11045–11054.
58. Watkins, L.E., Han, S., Harpaz-Rotem, I, Mota, N.P., Southwick, S.M., Krystal, J.H., Gelernter, J., Pietrzak, R.H., FKBP5 polymorphisms, childhood abuse, and PTSD symptoms: Results from the National Health and Resilience in Veterans Study. Psychoneuroendocrinology 69 (2016), 98–105.
59. Widom, C.S., Posttraumatic stress disorder in abused and neglected children grown up. Am. J. Psychiatry 156 (1999), 1223–1229.
60. Wochnik, G.M., Rüegg, J., Abel, G.A., Schmidt, U., Holsboer, F., Rein, T., FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J. Biol. Chem. 280 (2005), 4609–4616.
61. Xie, P., Kranzler, H.R., Poling, J., Stein, M.B., Anton, R.F., Farrer, L.A., Gelernter, J., Interaction of FKBP5 with childhood adversity on risk for post-traumatic stress disorder. Neuropsychopharmacology 35 (2010), 1684–1692.
62. Yehuda, R., Daskalakis, N.P., Desarnaud, F., Makotkine, I., Lehrner, A., Koch, E., Flory, J.D., Buxbaum, J.D., Meaney, M.J., Bierer, L.M., Epigenetic biomarkers as predictors and correlates of symptom improvement following psychotherapy in combat veterans with PTSD. Front. Psychiatry, 4, 2013, 118.
63. Zannas, A., Binder, E., Gene–environment interactions at the FKBP5 locus: sensitive periods, mechanisms and pleiotropism. Genes Brain Behav. 13 (2014), 25–37.
64. Zannas, A.S., Wiechmann, T., Gassen, N.C., Binder, E.B., Gene–stress–epigenetic regulation of FKBP5: clinical and translational implications. Neuropsychopharmacology, 2015.
65. Zimmermann, P., Brückl, T., Nocon, A., Pfister, H., Binder, E.B., Uhr, M., Lieb, R., Moffitt, T.E., Caspi, A., Holsboer, F., Interaction of FKBP5 gene variants and adverse life events in predicting depression onset: results from a 10-year prospective community study. Am. J. Psychiatry 168 (2011), 1107–1116.