Childhood maltreatment and methylation of FK506 binding protein 5 gene (FKBP5)

Development and Psychopathology

Volumn 27, Issue , 2015, Pages 1637-1645

  Tyrka, Audrey R ^a,b   Ridout, Kathryn K ^a,b   Parade, Stephanie H ^b,c   Paquette, Alison ^d   Marsit, Carmen J ^d   Seifer, Ronald ^b,c  

^a BUTLER HOSPITAL   (United States)

^b BROWN UNIVERSITY   (United States)

^c E P BRADLEY HOSPITAL   (United States)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FK 506 BINDING PROTEIN; TACROLIMUS BINDING PROTEIN 5;

CHILD ABUSE; DNA METHYLATION; FEMALE; GENETIC POLYMORPHISM; GENETICS; HUMAN; MALE; MENTAL STRESS; METABOLISM; POVERTY; PRESCHOOL CHILD; PSYCHOLOGY; RISK;

CHILD ABUSE; CHILD, PRESCHOOL; DNA METHYLATION; FEMALE; HUMANS; MALE; POLYMORPHISM, GENETIC; POVERTY; RISK; STRESS, PSYCHOLOGICAL; TACROLIMUS BINDING PROTEINS;

EID: 84963542655     PISSN: 09545794     EISSN: 14692198     Source Type: Journal    
DOI: 10.1017/S0954579415000991     Document Type: Article

References (118)

1. Barnett, D., Manly, J. T., & Cicchetti, D. (1993). Defining child maltreatment: The interface between policy and research. In D. Cicchetti & S. L. Toth (Eds.), Child abuse, child development, and social policy (pp. 7-73). Norwood, NJ: Ablex.
2. Bauer, M. E., Jeckel, C. M., & Luz, C. (2009). The role of stress factors during aging of the immune system. Annals of the New York Academy of Sciences, 1153, 139-152.
3. Beauchaine, T. P., Crowell, S. E., & Hsiao, R. C. (2015). Post-dexamethasone cortisol, self-inflicted injury, and suicidal ideation among depressed adolescent girls. Journal of Abnormal Child Psychology, 43, 619-632.
4. Binder, E. B. (2009). The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology, 34(Suppl. 1), S186-S195.
5. Booij, L., Wang, D., Levesque, M. L., Tremblay, R. E., & Szyf, M. (2013). Looking beyond the DNA sequence: The relevance of DNA methylation processes for the stress-diathesis model of depression. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences. Advance online publication.
6. Briggs-Gowan, M. J., Carter, A. S., Bosson-Heenan, J., Guyer, A. E., & Horwitz, S. M. (2006). Are infant-toddler social-emotional and behavioral problems transient? Journal of the American Academy of Child& Adolescent Psychiatry, 45, 849-858.
7. Brown, G. R., & Anderson, B. (1991). Psychiatric morbidity in adult inpatients with childhood histories of sexual and physical abuse. American Journal of Psychiatry, 148, 55-61.
8. Bryer, J. B., Nelson, B. A., Miller, J. B.,& Krol, P. A. (1987). Childhood sexual and physical abuse as factors in adult psychiatric illness. American Journal of Psychiatry, 144, 1426-1430.
9. Cameron, H. A., & Gould, E. (1994). Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience, 61, 203-209.
10. Carpenter, L. L., Carvalho, J. P., Tyrka, A. R., Wier, L. M., Mello, A. F., Mello, M. F., et al. (2007). Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biological Psychiatry, 62, 1080-1087.
11. Carpenter, L. L., Shattuck, T. T., Tyrka, A. R., Geracioti, T. D.,& Price, L. H. (2011). Effect of childhood physical abuse on cortisol stress response. Psychopharmacology (Berl), 214, 367-375.
12. Carpenter, L. L., Tyrka, A. R., Ross, N. S., Khoury, L., Anderson, G. M., & Price, L. H. (2009). Effect of childhood emotional abuse and age on cortisol responsivity in adulthood. Biological Psychiatry, 66, 69-75.
13. Carr, C. P., Martins, C. M., Stingel, A.M., Lemgruber,V. B., & Juruena, M. F. (2013). The role of early life stress in adult psychiatric disorders: A systematic review according to childhood trauma subtypes. Journal of Nervous and Mental Disease, 201, 1007-1020.
14. Cicchetti, D. (2015). Neural plasticity, sensitive periods, and psychopathology. Development and Psychopathology, 27, 319-320.
15. Cicchetti, D., Handley, E. D., & Rogosch, F. A. (2015). Child maltreatment, inflammation, and internalizing symptoms: Investigating the roles of Creactive protein, gene variation, and neuroendocrine regulation. Development and Psychopathology, 27, 553-566.
16. Cioffi, D. L., Hubler, T. R., & Scammell, J. G. (2011). Organization and function of the FKBP52 and FKBP51 genes. Current Opinion in Pharmacology, 11, 308-313.
17. Ciufolini, S., Dazzan, P., Kempton, M. J., Pariante, C., & Mondelli, V. (2014). HPA axis response to social stress is attenuated in schizophrenia but normal in depression: Evidence from a meta-analysis of existing studies. Neuroscience & Biobehavioral Reviews, 47, 359-368.
18. Colich, N. L., Kircanski, K., Foland-Ross, L. C., & Gotlib, I. H. (2015). HPA-axis reactivity interacts with stage of pubertal development to predict the onset of depression. Psychoneuroendocrinology, 55, 94-101.
19. Dachir, S., Kadar, T., Robinzon, B., & Levy, A. (1993). Cognitive deficits induced in young rats by long-term corticosterone administration. Behavioral and Neural Biology, 60, 103-109.
20. Daskalakis, N. P., Lehrner, A., & Yehuda, R. (2013). Endocrine aspects of post-traumatic stress disorder and implications for diagnosis and treatment. Endocrinology and Metabolism Clinics, 42, 503-513.
21. de Kloet, C. S., Vermetten, E., Geuze, E., Kavelaars, A., Heijnen, C. J., & Westenberg, H. G. (2006). Assessment of HPA-axis function in posttraumatic stress disorder: Pharmacological and non-pharmacological challenge tests, a review. Journal of Psychiatric Research, 40, 550-567.
22. de Kloet, C. S., Vermetten, E., Lentjes, E., Geuze, E., van Pelt, J., Manuel, R., et al. (2008). Differences in the response to the combined DEX-CRH test between PTSD patients with and without co-morbid depressive disorder. Psychoneuroendocrinology, 33, 313-320.
23. de Kloet, E. R., Joels, M., & Holsboer, F. (2005). Stress and the brain: From adaptation to disease. Nature Reviews: Neuroscience, 6, 463-475.
24. Doom, J. R., Cicchetti, D.,& Rogosch, F. A. (2014). Longitudinal patterns of cortisol regulation differ in maltreated and nonmaltreated children. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 1206-1215.
25. Dozier, M., Manni, M., Gordon, M. K., Peloso, E., Gunnar, M. R., Stovall-McClough, K. C., et al. (2006). Foster children's diurnal production of cortisol: An exploratory study. Child Maltreatment, 11, 189-197.
26. Elzinga, B. M., Roelofs, K., Tollenaar, M. S., Bakvis, P., van Pelt, J., & Spinhoven, P. (2008). Diminished cortisol responses to psychosocial stress associated with lifetime adverse events a study among healthy young subjects. Psychoneuroendocrinology, 33, 227-237.
27. Endler, G., Greinix, H., Winkler, K., Mitterbauer, G., & Mannhalter, C. (1999). Genetic fingerprinting in mouthwashes of patients after allogeneic bone marrow transplantation. Bone Marrow Transplantation, 24, 95-98.
28. Ewald, E. R.,Wand, G. S., Seifuddin, F., Yang, X., Tamashiro, K. L., Potash, J. B., et al. (2014). Alterations in DNA methylation of Fkbp5 as a determinant of blood-brain correlation of glucocorticoid exposure. Psychoneuroendocrinology, 44, 112-122.
29. Fries, E., Hesse, J., Hellhammer, J., & Hellhammer, D. H. (2005). A new view on hypocortisolism. Psychoneuroendocrinology, 30, 1010-1016.
30. Fujii, T., Hori, H., Ota, M., Hattori, K., Teraishi, T., Sasayama, D., et al. (2014). Effect of the common functional FKBP5 variant (rs1360780) on the hypothalamic-pituitary-adrenal axis and peripheral blood gene expression. Psychoneuroendocrinology, 42, 89-97.
31. Gillespie, C. F., Phifer, J., Bradley, B., & Ressler, K. J. (2009). Risk and resilience: Genetic and environmental influences on development of the stress response. Depression and Anxiety, 26, 984-992.
32. Golier, J. A., Caramanica, K., Makotkine, I., Sher, L., & Yehuda, R. (2014). Cortisol response to cosyntropin administration in military veterans with or without posttraumatic stress disorder. Psychoneuroendocrinology, 40, 151-158.
33. Gonzalez, A. (2013). The impact of childhood maltreatment on biological systems: Implications for clinical interventions. Paediatrics & Child Health, 18, 415-418.
34. Gould, E., Woolley, C. S., & McEwen, B. S. (1991). Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. Journal of Comparative Neurology, 313, 479-485.
35. Guintivano, J., & Kaminsky, Z. A. (2014). Role of epigenetic factors in the development of mental illness throughout life. Neuroscience Research. Advance online publication.
36. Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology, 13, 515-538.
37. Hart, H.,& Rubia, K. (2012). Neuroimaging of child abuse: A critical review. Frontiers of Human Neuroscience, 6, 52.
38. Hartman, C. A., Hermanns, V.W., de Jong, P. J., & Ormel, J. (2013). Self-or parent report of (co-occurring) internalizing and externalizing problems, and basal or reactivity measures of HPA-axis functioning: A systematic evaluation of the internalizing-hyperresponsivity versus externalizinghyporesponsivity HPA-axis hypothesis. Biological Psychology, 94, 175-184.
39. Heim, C., Ehlert, U., & Hellhammer, D. H. (2000). The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology, 25, 1-35.
40. Heim, C., Newport, D. J., Bonsall, R., Miller, A. H., & Nemeroff, C. B. (2001). Altered pituitary-adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. American Journal of Psychiatry, 158, 575-581.
41. Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., et al. (2000). Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the Americans Medical Association, 284, 592-597.
42. Herman, J. P., McKlveen, J. M., Solomon, M. B., Carvalho-Netto, E., & Myers, B. (2012). Neural regulation of the stress response: Glucocorticoid feedback mechanisms. Brazilian Journal of Medical and Biological Research, 45, 292-298.
43. Hickman, L. J., Jaycox, L. H., Setodji, C. M., Kofner, A., Schultz, D., Barnes-Proby, D., et al. (2013). How much does "how much" matter? Assessing the relationship between children's lifetime exposure to violence and trauma symptoms, behavior problems, and parenting stress. Journal of Interpersonal Violence, 28, 1338-1362.
44. Hohne, N., Poidinger, M., Merz, F., Pfister, H., Bruckl, T., Zimmermann, P., et al. (2015). FKBP5 genotype-dependent DNA methylation and mRNA regulation after psychosocial stress in remitted depression and healthy controls. International Journal of Neuropsychopharmacology. Advance online publication.
45. Ising, M., Depping, A. M., Siebertz, A., Lucae, S., Unschuld, P. G., Kloiber, S., et al. (2008). Polymorphisms in the FKBP5 gene region modulate recovery from psychosocial stress in healthy controls. European Journal Neuroscience, 28, 389-398.
46. Januar, V., Saffery, R., & Ryan, J. (2015). Epigenetics and depressive disorders: A review of current progress and future directions. International Journal of Epidemiology. Advance online publication.
47. Kadmiel, M.,& Cidlowski, J. A. (2013). Glucocorticoid receptor signaling in health and disease. Trends in Pharmacological Sciences, 34, 518-530.
48. Kendler, K. S., Kessler, R. C., Neale, M. C., Heath, A. C., & Eaves, L. J. (1993). The prediction of major depression in women: Toward an integrated etiologic model. American Journal of Psychiatry, 150, 1139-1148.
49. Kim-Spoon, J., Cicchetti, D., & Rogosch, F. A. (2013). A longitudinal study of emotion regulation, emotion lability-negativity, and internalizing symptomatology in maltreated and nonmaltreated children. Child Development, 84, 512-527.
50. Klaassens, E. R., van Noorden, M. S., Giltay, E. J., van Pelt, J., van Veen, T., & Zitman, F. G. (2009). Effects of childhood trauma on HPA-axis reactivity in women free of lifetime psychopathology. Progress in Neuropsychopharmacology & Biological Psychiatry, 33, 889-894.
51. Klengel, T., & Binder, E. B. (2015a). Epigenetics of stress-related psychiatric disorders and gene x environment interactions. Neuron, 86, 1343-1357.
52. Klengel, T., & Binder, E. B. (2015b). FKBP5 allele-specific epigenetic modification in gene by environment interaction. Neuropsychopharmacology, 40, 244-246.
53. Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J. C., Pariante, C. M., et al. (2013). Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nature Neuroscience, 16, 33-41.
54. Klengel, T., Pape, J., Binder, E. B., & Mehta, D. (2014). The role of DNA methylation in stress-related psychiatric disorders. Neuropharmacology, 80, 115-132.
55. Laryea, G., Muglia, L., Arnett, M., & Muglia, L. J. (2015). Dissection of glucocorticoid receptor-mediated inhibition of the hypothalamic-pituitaryadrenal axis by gene targeting in mice. Frontiers in Neuroendocrinology, 36, 150-164.
56. Lee, R. S., Tamashiro, K. L., Yang, X., Purcell, R. H., Huo, Y., Rongione, M., et al. (2011). A measure of glucocorticoid load provided by DNA methylation of Fkbp5 in mice. Psychopharmacology (Berlin), 218, 303-312.
57. Leszczynska-Rodziewicz, A., Szczepankiewicz, A., Narozna, B., Skibinska, M., Pawlak, J., Dmitrzak-Weglarz, M., et al. (2014). Possible association between haplotypes of the FKBP5 gene and suicidal bipolar disorder, but not with melancholic depression and psychotic features, in the course of bipolar disorder. Neuropsychiatric Disease and Treatment, 10, 243-248.
58. Lewinsohn, P. M., Hoberman, H. M., & Rosenbaum, M. (1988). A prospective study of risk factors for unipolar depression. Journal of Abnormal Psychology, 97, 251-264.
59. Lutz, P. E., Almeida, D., Fiori, L. M., & Turecki, G. (2015). Childhood maltreatment and stress-related psychopathology: The epigenetic memory hypothesis. Current Pharmaceutical Design, 21, 1413-1417.
60. Lutz, P. E., & Turecki, G. (2014). DNA methylation and childhood maltreatment: Fromanimalmodels to human studies. Neuroscience, 264, 142-156.
61. Magarinos, A. M., Orchinik, M., & McEwen, B. S. (1998). Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: A paradox. Brain Research, 809, 314-318.
62. Magee, J. A., Chang, L. W., Stormo, G. D., & Milbrandt, J. (2006). Direct, androgen receptor-mediated regulation of the FKBP5 gene via a distal enhancer element. Endocrinology, 147, 590-598.
63. Marsman, R., Swinkels, S. H., Rosmalen, J. G., Oldehinkel, A. J., Ormel, J., & Buitelaar, J. K. (2008). HPA-axis activity and externalizing behavior problems in early adolescents from the general population: The role of comorbidity and gender the TRAILS study. Psychoneuroendocrinology, 33, 789-798.
64. McCrory, E., De Brito, S. A.,& Viding, E. (2010). Research review: The neurobiology and genetics of maltreatment and adversity. Journal of Child Psychology and Psychiatry, 51, 1079-1095.
65. McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews, 87, 873-904.
66. Menke, A., Klengel, T., Rubel, J., Bruckl, T., Pfister, H., Lucae, S., et al. (2013). Genetic variation in FKBP5 associated with the extent of stress hormone dysregulation in major depression. Genes, Brain, and Behavior, 12, 289-296.
67. Mesman, J., & Koot, H. M. (2001). Early preschool predictors of preadolescent internalizing and externalizing DSM-IV diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 1029-1036.
68. Mills, R., Scott, J., Alati, R., O'Callaghan, M., Najman, J. M., & Strathearn, L. (2013). Child maltreatment and adolescent mental health problems in a large birth cohort. Child Abuse & Neglect, 37, 292-302.
69. Morris, M. C., Compas, B. E.,& Garber, J. (2012). Relations among posttraumatic stress disorder, comorbid major depression, and HPA function: A systematic review and meta-analysis. Clinical Psychology Review, 32, 301-315.
70. Nanni, V., Uher, R., & Danese, A. (2012). Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: A meta-analysis. American Journal of Psychiatry, 169, 141-151.
71. Norman, R. E., Byambaa, M., De, R., Butchart, A., Scott, J., & Vos, T. (2012). The long-term health consequences of child physical abuse, emotional abuse, and neglect: A systematic review and meta-analysis. PLOS Medicine, 9, e1001349.
72. Nugent, N. R., Tyrka, A. R., Carpenter, L. L., & Price, L. H. (2011). Geneenvironment interactions: Early life stress and risk for depressive and anxiety disorders. Psychopharmacology (Berlin), 214, 175-196.
73. Paquette, A. G., Lester, B. M., Koestler, D. C., Lesseur, C., Armstrong, D. A., & Marsit, C. J. (2014). Placental FKBP5 genetic and epigenetic variation is associated with infant neurobehavioral outcomes in the RICHS cohort. PLOS ONE, 9, e104913.
74. Philip, N. S., Sweet, L. H., Tyrka, A. R., Carpenter, S. L., Albright, S. E., Price, L. H., et al. (2015). Exposure to childhood trauma is associated with altered n-back activation and performance in healthy adults: Implications for a commonly used working memory task. Brain Imaging and Behavior. Advance online publication.
75. Pryce, C. R., Ruedi-Bettschen, D., Dettling, A. C., Weston, A., Russig, H., Ferger, B., et al. (2005). Long-term effects of early-life environmental manipulations in rodents and primates: Potential animal models in depression research. Neuroscience & Biobehavioral Reviews, 29, 649-674.
76. Radtke, K. M., Schauer, M., Gunter, H. M., Ruf-Leuschner, M., Sill, J., Meyer, A., et al. (2015). Epigenetic modifications of the glucocorticoid receptor gene are associated with the vulnerability to psychopathology in childhood maltreatment. Translational Psychiatry, 5, e571.
77. Reik, W. (2007). Stability and flexibility of epigenetic gene regulation in mammalian development. Nature, 447, 425-432.
78. Ridout, K. K., Parade, S. H., Seifer, R., Price, L. H., Gelernter, J., Feliz, P., et al. (2014). Interleukin 1B gene (IL1B) variation and internalizing symptoms in maltreated preschoolers. Development and Psychopathology, 26(4, Part 2), 1277-1287.
79. Ridout, S. J., Ridout, K. K., Kao, H. T., Carpenter, L. L., Philip, N. S., Tyrka, A. R., et al. (2015). Telomeres, early-life stress and mental illness. Advances in Psychosomatic Medicine, 34, 92-108.
80. Rohleder, N., Joksimovic, L., Wolf, J. M., & Kirschbaum, C. (2004). Hypocortisolism and increased glucocorticoid sensitivity of pro-Inflammatory cytokine production in Bosnian war refugees with posttraumatic stress disorder. Biological Psychiatry, 55, 745-751.
81. Roza, S. J., Hofstra, M. B., van der Ende, J., & Verhulst, F. C. (2003). Stable prediction of mood and anxiety disorders based on behavioral and emotional problems in childhood: A 14-year follow-up during childhood, adolescence, and young adulthood. American Journal of Psychiatry, 160, 2116-2121.
82. Sarapas, C., Cai, G., Bierer, L. M., Golier, J. A., Galea, S., Ising, M., et al. (2011). Genetic markers for PTSD risk and resilience among survivors of the World Trade Center attacks. Disease Markers, 30, 101-110.
83. Sasaki, A., de Vega, W. C., & McGowan, P. O. (2013). Biological embedding in mental health: An epigenomic perspective. Biochemistry and Cell Biology, 91, 14-21.
84. Scheeringa, M. S., & Haslett, N. (2010). The reliability and criterion validity of the Diagnostic Infant and Preschool Assessment: A new diagnostic instrument for young children. Child Psychiatry and Human Development, 41, 299-312.
85. Schmidt, U., Buell, D. R., Ionescu, I. A., Gassen, N. C., Holsboer, F., Cox, M. B., et al. (2015). A role for synapse in in FKBP51 modulation of stress responsiveness: Convergent evidence from animal and human studies. Psychoneuroendocrinology, 52, 43-58.
86. Smith, A. K., Kilaru, V., Klengel, T., Mercer, K. B., Bradley, B., Conneely, K. N., et al. (2015). DNA extracted from saliva for methylation studies of psychiatric traits: Evidence tissue specificity and relatedness to brain. American Journal of Medical Genetics, 168B, 36-44.
87. Spijker, A. T., & van Rossum, E. F. (2012). Glucocorticoid sensitivity in mood disorders. Neuroendocrinology, 95, 179-186.
88. Stankiewicz, A. M., Swiergiel, A. H., & Lisowski, P. (2013). Epigenetics of stress adaptations in the brain. Brain Research Bulletin, 98, 76-92.
89. Suzuki, A., Matsumoto, Y., Sadahiro, R., Enokido, M., Goto, K.,& Otani, K. (2014). Relationship of the FKBP5 C/T polymorphism with dysfunctional attitudes predisposing to depression. Comprehensive Psychiatry, 55, 1422-1425.
90. Suzuki, H., Belden, A. C., Spitznagel, E., Dietrich, R., & Luby, J. L. (2013). Blunted stress cortisol reactivity and failure to acclimate to familiar stress in depressed and sub-syndromal children. Psychiatry Research, 210, 575-583.
91. Szczepankiewicz, A., Leszczynska-Rodziewicz, A., Pawlak, J., Narozna, B., Rajewska-Rager, A.,Wilkosc, M., et al. (2014). FKBP5 polymorphism is associated with major depression but not with bipolar disorder. Journal of Affective Disorders, 164, 33-37.
92. Szyf, M. (2011). The early life social environment and DNA methylation: DNA methylation mediating the long-term impact of social environments early in life. Epigenetics, 6, 971-978.
93. Szyf, M. (2015). Nongenetic inheritance and transgenerational epigenetics. Trends in Molecular Medicine, 21, 134-144.
94. Tatro, E. T., Everall, I. P., Kaul, M., & Achim, C. L. (2009). Modulation of glucocorticoid receptor nuclear translocation in neurons by immunophilins FKBP51 and FKBP52: Implications for major depressive disorder. Brain Research, 1286, 1-12.
95. Thiede, C., Prange-Krex, G., Freiberg-Richter, J., Bornhauser, M., & Ehninger, G. (2000). Buccal swabs but not mouthwash samples can be used to obtain pretransplant DNA fingerprints from recipients of allogeneic bone marrow transplants. Bone Marrow Transplantation, 25, 575-577.
96. Toth, S. L., Gravener-Davis, J. A., Guild, D. J., & Cicchetti, D. (2013). Relational interventions for child maltreatment: Past, present, and future perspectives. Development Psychopathology, 25(4, Part 2), 1601-1617.
97. Turecki, G., & Meaney, M. J. (2014). Effects of the social environment and stress on glucocorticoid receptor gene methylation: A systematic review. Biological Psychiatry. Advance online publication.
98. Tyrka, A. R., Burgers, D. E., Philip, N. S., Price, L. H., & Carpenter, L. L. (2013). The neurobiological correlates of childhood adversity and implications for treatment. Acta Psychiatrica Scandinavica, 128, 434-447.
99. Tyrka, A. R., Parade, S. H., Eslinger, N. M., Marsit, C. J., Lesseur, C., Armstrong, D. A., et al. (2015). Methylation of exons 1D, 1F, and 1H of the glucocorticoid receptor gene promoter and exposure to adversity in preschool-aged children. Development and Psychopathology, 27, 577-585.
100. Tyrka, A. R., Parade, S. H., Price, L. H., Kao, H. T., Porton, B., Philip, N. S., et al. (2015). Alterations of mitochondrial DNA copy number and telomere length with early adversity and psychopathology. Biological Psychiatry. Advance online publication.
101. Tyrka, A. R., Price, L. H., Gelernter, J., Schepker, C., Anderson, G. M., & Carpenter, L. L. (2009). Interaction of childhood maltreatment with the corticotropin-releasing hormone receptor gene: Effects on hypothalamic-pituitary-adrenal axis reactivity. Biological Psychiatry, 66, 681-685.
102. Tyrka, A. R., Price, L. H., Kao, H. T., Porton, B., Marsella, S. A., & Carpenter, L. L. (2010). Childhood maltreatment and telomere shortening: Preliminary support for an effect of early stress on cellular aging. Biological Psychiatry, 67, 531-534.
103. Tyrka, A. R., Price, L. H., Marsit, C., Walters, O. C., & Carpenter, L. L. (2012). Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: Preliminary findings in healthy adults. PLOS ONE, 7, e30148.
104. Tyrka, A. R.,Wier, L., Price, L. H., Ross, N., Anderson, G. M.,Wilkinson, C. W., et al. (2008). Childhood parental loss and adult hypothalamic-pituitary-adrenal function. Biological Psychiatry, 63, 1147-1154.
105. van der Knaap, L. J., Oldehinkel, A. J., Verhulst, F. C., van Oort, F. V., & Riese, H. (2015). Glucocorticoid receptor gene methylation and HPAaxis regulation in adolescents: The TRAILS study. Psychoneuroendocrinology, 58, 46-50.
106. van der Knaap, L. J., van Oort, F. V., Verhulst, F. C., Oldehinkel, A. J., & Riese, H. (2015). Methylation of NR3C1 and SLC6A4 and internalizing problems: The TRAILS study. Journal of Affective Disorders, 180, 97-103.
107. Vandevyver, S., Dejager, L., & Libert, C. (2014). Comprehensive overview of the structure and regulation of the glucocorticoid receptor. Endocrine Reviews, 35, 671-693.
108. Van Zomeren-Dohm, A. A., Pitula, C. E., Koss, K. J., Thomas, K., & Gunnar, M. R. (2015). FKBP5 moderation of depressive symptoms in peer victimized, post-institutionalized children. Psychoneuroendocrinology, 51, 426-430.
109. Wagner, J. R., Busche, S., Ge, B., Kwan, T., Pastinen, T., & Blanchette, M. (2014). The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biology, 15, R37.
110. Watanabe, Y., Gould, E., & McEwen, B. S. (1992). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Research, 588, 341-345.
111. Weder, N., Zhang, H., Jensen, K., Yang, B. Z., Simen, A., Jackowski, A., et al. (2014). Child abuse, depression, and methylation in genes involved with stress, neural plasticity, and brain circuitry. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 417-424.
112. Widom, C. S., DuMont, K.,& Czaja, S. J. (2007).A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Archives of General Psychiatry, 64, 49-56.
113. Wolkowitz, O. M., Epel, E. S., Reus, V. I., & Mellon, S. H. (2010). Depression gets old fast: Do stress and depression accelerate cell aging? Depression and Anxiety, 27, 327-338.
114. Woolley, C. S., Gould, E., & McEwen, B. S. (1990). Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Research, 531, 225-231.
115. Yang, X., Han, H., De Carvalho, D. D., Lay, F. D., Jones, P. A., & Liang, G. (2014). Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell, 26, 577-590.
116. Yehuda, R., Cai, G., Golier, J. A., Sarapas, C., Galea, S., Ising, M., et al. (2009). Gene expression patterns associated with posttraumatic stress disorder following exposure to the World Trade Center attacks. Biological Psychiatry, 66, 708-711.
117. Zannas, A. S., & Binder, E. B. (2014). Gene-environment interactions at the FKBP5 locus: Sensitive periods, mechanisms and pleiotropism. Genes, Brain, and Behavior, 13, 25-37.
118. Zhang, T. Y., Labonte, B.,Wen, X. L., Turecki, G., & Meaney, M. J. (2013). Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology, 38, 111-123.