Psychoneuroendocrinology
Volume 34, Issue 9 , Pages 1294-1303 , October 2009

Gene–environment interactions predict cortisol responses after acute stress: Implications for the etiology of depression

Received 27 October 2008 ,Revised 10 February 2009 ,Accepted 26 March 2009.

References 

  1. Anand A, Li Y, Wang Y, Wu J, Gao S, Bukhari L, et al. Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biol. Psychiatry. 2005;57:1079–1788
  2. Barr CS, Newman TK, Schwandt M, Shannon C, Dvoskin RL, Lindell SG. Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proc. Natl. Acad. Sci. 2004;101:12358–12363
  3. Beck AT, Steer RA. Beck Depression Inventory. San Antonio, TX: Psychological Corporation; 1987;
  4. Bennett AJ, Lesch KP, Heils A, Long JC, Lorenz JG, Shoaf SE. Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol. Psychiatry. 2002;7:118–122
  5. Biondi M, Picardi A. Psychological stress and neuroendocrine function in humans: the last two decades of research. Psychother. Psychosom. 1999;68:114–150
  6. Borkenau P, Ostendorf F. NEO-Fuenf-Faktoren-Inventar (NEO-FFI) nach Costa and McCrae. Goettingen: Hogrefe; 1994;
  7. Brown ES, Woolston DJ, Frol AB. Amygdala volume in patients receiving chronic corticosteroid therapy. Biol. Psychiatry. 2008;63:705–709
  8. Burke HM, Davis MC, Otte C, Mohr DC. Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology. 2005;30:846–856
  9. Canli T, Omura K, Haas BW, Fallgatter A, Constable RT, Lesch KP. Beyond affect: a role for genetic variation of the serotonin transporter in neural activation during a cognitive attention task. Proc. Natl. Acad. Sci. U.S.A. 2005;102:12224–12229
  10. Canli T, Qiu M, Omura K, Congdon E, Haas BW, Amin Z. Neural correlates of epigenesis. Proc. Natl. Acad. Sci. U.S.A. 2006;103:16033–16038
  11. Carpenter LL, Carvalho JP, Tyrka AR, Wier LM, Mello AF, Mello MF. Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol. Psychiatry. 2006;62:1080–1087
  12. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science. 2003;18:386–389
  13. Collier DA, Stöber G, Li T, Heils A, Catalano M, Di Bella D, et al. A novel functional polymorphism within the promoter of the serotonin transporter gene: possible role in susceptibility to affective disorders. Mol. Psychiatry. 1996;1:453–460
  14. Costa PT, McCrae RR. NEO PI/FFI Manual Supplement. Odessa, FL: Psychological Assessment; 1989;
  15. Covault J, Tennen H, Armeli S, Conner TS, Herman AI, Cillessen AH, et al. Interactive effects of the serotonin transporter 5-HTTLPR polymorphism and stressful life events on college student drinking and drug use. Biol. Psychiatry. 2007;61:609–616
  16. De Kloet CS, Vermetten E, Geuze E, Kavelaars A, Heijnen CJ, Westenberg HG. Assessment of HPA-axis function in posttraumatic stress disorder: pharmacological and non-pharmacological challenge tests. A review. J. Psychiatr. Res. 2006;40:550–567
  17. Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 2004;130:355–391
  18. Elzinga BM, Roelofs K, Tollenaar MS, Bakvis P, van Pelt J, Spinhoven P. Diminished cortisol responses to psychosocial stress associated with lifetime adverse events a study among healthy young subjects. Psychoneuroendocrinology. 2008;33:227–237
  19. Federenko IS, Nagamine M, Hellhammer DH, Wadhwa PD, Wüst S. The heritability of hypothalamus pituitary adrenal axis responses to psychosocial stress is context dependent. J. Clin. Endocrinol. Metab. 2004;89:6244–6250
  20. Fries E, Hesse J, Hellhammer J, Hellhammer DH. A new view on hypocortisolism. Psychoneuroendocrinology. 2005;30:1010–1016
  21. Frodl T, Möller HJ, Meisenzahl E. Neuroimaging genetics: new perspectives in research on major depression?. Acta Psychiatr. Scand. 2008;118:363–372
  22. Fu CH, Williams SC, Cleare AJ, Brammer MJ, Walsh ND, Kim J. Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. Arch. Gen. Psychiatry. 2004;61:877–889
  23. Fuller RW. Serotonin receptors and neuroendocrine responses. Neuropsychopharmacology. 1990;3:495–502
  24. Glatz K, Mössner R, Heils A, Lesch KP. Glucocorticoid-regulated human serotonin transporter (5-HTT) expression is modulated by the 5-HTT gene-promotor-linked polymorphic region. J. Neurochem. 2003;86:1072–1078
  25. Gotlib IH, Joormann J, Minor KL, Hallmayer J. HPA axis reactivity: a mechanism underlying the associations among 5-HTTLPR, stress, and depression. Biol. Psychiatry. 2008;63:847–851
  26. Gray MJ, Litz BT, Hsu JL, Lombardo TW. Psychometric properties of the life events checklist. Assessment. 2004;11:330–341
  27. Greenberg BD, Tolliver TJ, Huang SJ, Li Q, Bengel D, Murphy DL. Genetic variation in the serotonin transporter promoter region affects serotonin uptake in human blood platelets. Am. J. Med. Genet. 1999;88:83–87
  28. Hamilton JP, Siemer M, Gotlib IH. Amygdala volume in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Mol. Psychiatry. 2008;
  29. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D. Serotonin transporter genetic variation and the response of the human amygdala. Science. 2002;297:400–403
  30. Hautzinger M, Bailer M, Worall H, Keller F. Beck-Depressions-Inventary (BDI). Bern: Huber; 1994;
  31. Heim C, Newport DJ, Wagner D, Wilcox MM, Miller AH, Nemeroff CB. The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: a multiple regression analysis. Depress. Anxiety. 2002;15:117–125
  32. Heim C, Plotsky PM, Nemeroff CB. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology. 2004;29:641–648
  33. Heinz A, Jones DW, Mazzanti C, Goldman D, Ragan P, Hommer D, et al. A relationship between serotonin transporter genotype and in vivo protein expression and alcohol neurotoxicity. Biol. Psychiatry. 2000;47:643–649
  34. Heinz A, Smolka MN, Braus DF, Wrase J, Beck A, Flor H. Serotonin transporter genotype (5-HTTLPR): effects of neutral and undefined conditions on amygdala activation. Biol. Psychiatry. 2007;61:1011–1014
  35. Herman JP, Ostrander MM, Mueller NK, Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2005;29:1201–1213
  36. Het S, Wolf OT. Mood changes in response to psychosocial stress in healthy young women: effects of pretreatment with cortisol. Behav. Neurosci. 2007;121:11–20
  37. Holsboer F. Stress, hypercortisolism and corticosteroid receptors in depression: implications for therapy. J. Affect. Disord. 2001;62:77–91
  38. Holsboer F, Ising M. Central CRH system in depression and anxiety—evidence from clinical studies with CRH1 receptor antagonists. Eur. J. Pharmacol. 2008;583:350–357
  39. Hu XZ, Lipsky RH, Zhu G, Akhtar LA, Taubman J, Greenberg BD, et al. Serotonin transporter promoter gain-of-function genotypes are linked to obsessive–compulsive disorder. Am. J. Hum. Genet. 2006;78:815–826
  40. Ising M, Holsboer F. CRH-sub-1 receptor antagonists for the treatment of depression and anxiety. Exp. Clin. Psychopharmacol. 2007;15:519–528
  41. Kalin NH, Shelton SE, Fox AS, Rogers J, Oakes TR, Davidson RJ. The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor. Mol. Psychiatry. 2008;13:1021–1027
  42. Kaufman J, Yang BZ, Douglas-Palumberi H, Houshyar S, Lipschitz D, Krystal JH. Social supports and serotonin transporter gene moderate depression in maltreated children. Proc. Natl. Acad. Sci. U.S.A. 2004;101:17316–17321
  43. Kaufman J, Yang BZ, Douglas-Palumberi H, Crouse-Artus M, Lipschitz D, Krystal JH, et al. Genetic and environmental predictors of early alcohol use. Biol. Psychiatry. 2007;61:1228–1234
  44. Kendler KS, Karkowski LM, Prescott CA. Causal relationship between stressful life events and the onset of major depression. Am. J. Psychiatry. 1999;156:837–841
  45. Kendler KS, Kuhn JW, Vittum J, Prescott CA, Riley B. The interaction of stressful life events and a serotonin transporter polymorphism in the prediction of episodes of major depression: a replication. Arch. Gen. Psychiatry. 2005;62:529–535
  46. Kim JM, Stewart R, Kim SW, Yang SJ, Shin IS, Kim YH. Interactions between life stressors and susceptibility genes (5-HTTLPR and BDNF) on depression in Korean elders. Biol. Psychiatry. 2007;62:423–428
  47. Kinnally EL, Lyons LA, Abel K, Mendoza S, Capitanio JP. Effects of early experience and genotype on serotonin transporter regulation in infant rhesus macaques. Genes Brain Behav. 2008;7:481–486
  48. Kirschbaum C, Hellhammer DH. Salivary cortisol in psychobiological research: an overview. Neuropsychobiology. 1989;22:150–169
  49. Kirschbaum C, Wüst S, Faig HG, Hellhammer DH. Heritability of cortisol responses to human corticotropin-releasing hormone, ergometry, and psychological stress in humans. J. Clin. Endocrinol. Metab. 1992;75:1526–1530
  50. Lasky-Su JA, Faraone SV, Glatt SJ, Tsuang MT. Meta-analysis of the association between two polymorphisms in the serotonin transporter gene and affective disorders. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2005;133:110–115
  51. Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science. 1996;274:1527–1531
  52. Lesch KP. Gene–environment interaction and the genetics of depression. J. Psychiatry Neurosci. 2004;29:174–184
  53. Li Q, Wichems C, Heils A, Van De Kar LD, Lesch KP, Murphy DL. Reduction of 5-hydroxytryptamine (5-HT)(1A)-mediated temperature and neuroendocrine responses and 5-HT(1A) binding sites in 5-HT transporter knockout mice. J. Pharmacol. Exp. Ther. 1999;291:999–1007
  54. Lotrich FE, Pollock BG. Meta-analysis of serotonin transporter polymorphisms and affective disorders. Psychiatr. Genet. 2004;14:121–129
  55. McEwen BS. Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N.Y. Acad. Sci. 1998;840:33–44
  56. McEwen BS. The neurobiology of stress: from serendipity to clinical relevance. Brain Res. 2000;886:172–189
  57. Munafò MR, Brown SM, Hariri AR. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol. Psychiatry. 2007;63:852–857
  58. Munafò MR, Freimer NB, Ng W, Ophoff R, Veijola J, Miettunen J, et al. 5-HTTLPR genotype and anxiety-related personality traits: a meta-analysis and new data. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008;
  59. Nakamura M, Ueno S, Sano A, Tanabe H. The human serotonin transporter gene linked polymorphism (5-HTTLPR) shows ten novel allelic variants. Mol. Psychiatry. 2000;5:32–38
  60. Nemeroff CB. Recent advances in the neurobiology of depression. Psychopharmacol. Bull. 2002;36:6–23
  61. Nemeroff CB, Owens MJ. Pharmacologic differences among the SSRIs: focus on monoamine transporters and the HPA axis. CNS Spectr. 2004;9:23–31
  62. Newport DJ, Stowe ZN, Nemeroff CB. Parental depression: animal models of an adverse life event. Am. J. Psychiatry. 2002;159:1265–1283
  63. Newport DJ, Wilcox MM, Stowe ZN. Maternal depression: a child's first adverse life event. Semin. Clin. Neuropsychiatry. 2002;7:113–119
  64. Pauli-Pott U, Friedl S, Hinney A, Hebebrand J. Serotonin transporter gene polymorphism (5-HTTLPR), environmental conditions, and developing negative emotionality and fear in early childhood. J. Neural. Transm. 2009;
  65. Parsey RV, Hastings RS, Oquendo MA, Hu X, Goldman D, Huang YY, et al. Effect of a triallelic functional polymorphism of the serotonin-transporter-linked promoter region on expression of serotonin transporter in the human brain. Am. J. Psychiatry. 2006;163:48–51
  66. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, et al. 5-HTTLPR polymorphism impacts human cingulated–amygdala interactions: a genetic susceptibility mechanism for depression. Nat. Neurosci. 2005;8:828–834
  67. Plotsky PM, Owens MJ, Nemeroff CB. Psychoneuroendocrinology of depression. Hypothalamic–pituitary–adrenal axis. Psychiatr. Clin. North Am. 1998;21:293–307
  68. Porter RJ, Gallagher P, Watson S, Young AH. Corticosteroid–serotonin interactions in depression: a review of the human evidence. Psychopharmacology. 2004;173:1–17
  69. Praschak-Rieder N, Kennedy J, Wilson AA, Hussey D, Boovariwala A, Willeit M, et al. Novel 5-HTTLPR allele associates with higher serotonin transporter binding in putamen: a [(11)C] DASB positron emission tomography study. Biol. Psychiatry. 2007;62:231–327
  70. Pryce CR, Ruedi-Bettschen D, Dettling AC, Weston A, Russig H, Ferger B. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci. Biobehav. Rev. 2005;29:649–674
  71. Rao U, Hammen C, Ortiz LR, Chen LA, Poland RE. Effects of early and recent adverse experiences on adrenal response to psychosocial stress in depressed adolescents. Biol. Psychiatry. 2008;64:521–526
  72. Reif A, Rösler M, Freitag CM, Schneider M, Eujen A, Kissling C, et al. Nature and nurture predispose to violent behavior: serotonergic genes and adverse childhood environment. Neuropsychopharmacology. 2007;32:2375–2383
  73. Reimold M, Smolka MN, Schumann G, Zimmer A, Wrase J, Mann K, et al. Midbrain serotonin transporter binding potential measured with [11C]DASB is affected by serotonin transporter genotype. J. Neural. Transm. 2006;114:635–639
  74. Reuter M. Impact of cortisol on emotions under stress and nonstress conditions: a pharmacopsychological approach. Neuropsychobiology. 2002;46:41–48
  75. Roelofs K, Bakvis P, Hermans EJ, van Pelt J, van Honk J. The effects of social stress and cortisol responses on the preconscious selective attention to social threat. Biol. Psychol. 2007;75:1–7
  76. Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch. Gen. Psychiatry. 2000;57:925–935
  77. Schinka JA, Busch RM, Robichaux-Keene N. A meta-analysis of the association between the serotonin transporter gene polymorphism (5-HTTLPR) and trait anxiety. Mol. Psychiatry. 2004;9:197–202
  78. Schmidt NB, Zvolensky MJ, Maner JK. Anxiety sensitivity: prospective prediction of panic attacks and Axis I pathology. J. Psychiatr. Res. 2006;40:691–699
  79. Sen S, Burmeister M, Ghosh D. Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2004;127:85–89
  80. Serretti A, Lilli R, Lorenzi C, Lattuada E, Cusin C, Smeraldi E. Serotonin transporter gene (5-HTTLPR) and major psychoses. Mol. Psychiatry. 2002;7:95–99
  81. Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA. Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol. Psychiatry. 2001;50:651–658
  82. Stein MB, Schork NJ, Gelernter J. Gene-by-environment (serotonin transporter and childhood maltreatment) interaction for anxiety sensitivity, an intermediate phenotype for anxiety disorders. Neuropsychopharmacology. 2008;33:312–319
  83. Stoltenberg SF, Twitchell GR, Hanna GL, Cook EH, Fitzgerald HE, Zucker RA, et al. Serotonin transporter promoter polymorphism, peripheral indexes of serotonin function, and personality measures in families with alcoholism. Am. J. Med. Genet. 2002;114:230–234
  84. Uher R, McGuffin P. The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: review and methodological analysis. Mol. Psychiatry. 2008;13:131–146
  85. van Dyck CH, Malison RT, Staley JK, Jacobsen LK, Seibyl JP, Laruelle M, et al. Central serotonin transporter availability measured with [123I]beta-CIT SPECT in relation to serotonin transporter genotype. Am. J. Psychiatry. 2004;161:525–531
  86. Wilhelm K, Siegel JE, Finch AW, Hadzi-Pavlovic D, Mitchell PB, Parker G, et al. The long and the short of it: associations between 5-HTT genotypes and coping with stress. Psychosom. Med. 2007;69:614–620
  87. Yang RJ, Mozhui K, Karlsson RM, Cameron HA, Williams RW, Holmes A. Variation in mouse basolateral amygdala volume is associated with differences in stress reactivity and fear learning. Neuropsychopharmacology. 2008;33:2595–2604

PII: S0306-4530(09)00114-0

doi: 10.1016/j.psyneuen.2009.03.017

Psychoneuroendocrinology
Volume 34, Issue 9 , Pages 1294-1303 , October 2009