Early-Life Adversity Interacts with FKBP5 Genotypes: Altered Working Memory and Cardiac Stress Reactivity in the Oklahoma Family Health Patterns Project

Neuropsychopharmacology

Volumn 41, Issue 7, 2016, Pages 1724-1732

  Lovallo, William R ^a,b   Enoch, Mary Anne ^c   Acheson, Ashley ^d   Cohoon, Andrew J ^a   Sorocco, Kristen H ^a,e   Hodgkinson, Colin A ^c   Vincent, Andrea S ^f   Goldman, David ^c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^e UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^f UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FKBP5 PROTEIN; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN; UNCLASSIFIED DRUG; FK 506 BINDING PROTEIN; HYDROCORTISONE; TACROLIMUS BINDING PROTEIN 5;

ADULT; ALCOHOLISM; ALLELE; ARTICLE; CONTROLLED STUDY; EARLY LIFE ADVERSITY; FAMILY HEALTH; FEMALE; FUNCTIONAL STATUS; GENE EXPRESSION; GENOTYPE ENVIRONMENT INTERACTION; HEALTH BEHAVIOR; HEART RATE; HEART STRESS; HOMOZYGOTE; HUMAN; HUMAN ACTIVITIES; MAJOR CLINICAL STUDY; MALE; MENTAL STRESS; MORBIDITY; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; STROOP TEST; SUBSTANCE ABUSE; UPREGULATION; WORKING MEMORY; ADOLESCENT; BLOOD; CHILD ABUSE SURVIVOR; GENETICS; GENOTYPE; IMPULSIVENESS; OKLAHOMA; PATHOPHYSIOLOGY; PERSONALITY TEST; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; PSYCHOLOGY; SHORT TERM MEMORY; TEMPERAMENT; YOUNG ADULT;

ADOLESCENT; ADULT; ADULT SURVIVORS OF CHILD ABUSE; FAMILY HEALTH; FEMALE; GENE-ENVIRONMENT INTERACTION; GENOTYPE; HEART RATE; HUMANS; HYDROCORTISONE; IMPULSIVE BEHAVIOR; MALE; MEMORY, SHORT-TERM; OKLAHOMA; PERSONALITY INVENTORY; POLYMORPHISM, SINGLE NUCLEOTIDE; PSYCHIATRIC STATUS RATING SCALES; STRESS, PSYCHOLOGICAL; TACROLIMUS BINDING PROTEINS; TEMPERAMENT; YOUNG ADULT;

EID: 84959287999     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.347     Document Type: Article

References (91)

1. Acheson A, Franklin C, Cohoon AJ, Glahn DC, Fox PT, Lovallo WR (2014). Anomalous temporoparietal activity in individuals with a family history of alcoholism: studies from the Oklahoma Family Health Patterns Project. Alcohol Clin Exp Res 38: 1639-1645.
2. Acheson A, Vincent AS, Sorocco KH, Lovallo WR (2011). Greater discounting of delayed rewards in young adults with family histories of alcohol and drug use disorders: studies from the Oklahoma family health patterns project. Alcohol Clin Exp Res 35: 1607-1613.
3. Al'Absi M, Bongard S, Buchanan T, Pincomb GA, Licinio J, Lovallo WR (1997). Cardiovascular and neuroendocrine adjustment to public speaking and mental arithmetic stressors. Psychophysiology 34: 266-275.
4. Al'Absi M, Hugdahl K, Lovallo WR (2002). Adrenocortical stress responses and altered working memory performance. Psychophysiology 39: 95-99.
5. American-Psychiatric-Association (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th (text rev.) edn. American Psychiatric Association: Washington, DC, USA.
6. Andreasen NC, Endicott J, Spitzer RL, Winokur G (1977). The family history method using diagnostic criteria. Reliability and validity. Arch Gen Psychiatry 34: 1229-1235.
7. Anglin RE, Rosebush PI, Mazurek MF (2006). The neuropsychiatric profile of Addison's disease: revisiting a forgotten phenomenon. J Neuropsychiatry Clin Neurosci 18: 450-459.
8. Babor TF, De La Fuente JR, Saunders J, Grant M (1992). AUDIT: The Alcohol Use Disorders Identification Test: Guidelines for Use in Primary Health Care. World Health Organization: Geneva, Switzerland.
9. Baxter JD, Rousseau GG, Benson MC, Garcea RL, Ito J, Tomkins GM (1972). Role of DNA and specific cytoplasmic receptors in glucocorticoid action. Proc Natl Acad Sci USA 69: 1892-1896.
10. Bechara A, Damasio AR, Damasio H, Anderson SW (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50: 7-15.
11. Beck AT, Beamesderfer A (1974). Assessment of depression: the depression inventory. Mod Probl Pharmacopsychiatry 7: 151-169.
12. Bet PM, Penninx BW, Bochdanovits Z, Uitterlinden AG, Beekman AT, van Schoor NM et al (2009). Glucocorticoid receptor gene polymorphisms and childhood adversity are associated with depression: New evidence for a gene-environment interaction. Am J Med Genet B Neuropsychiatr Genet 150B: 660-669.
13. Binder EB (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.
14. Binder EB, Bradley RG, Liu W, Epstein MP, Deveau TC, Mercer KB et al (2008). Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA 299: 1291-1305.
15. Binder EB, Salyakina D, Lichtner P, Wochnik GM, Ising M, Putz B et al (2004). Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat Genet 36: 1319-1325.
16. Blouin AG, Perez EL, Blouin JH (1988). Computerized administration of the Diagnostic Interview Schedule. Psychiatry Res 23: 335-344.
17. Bogdan R, Pagliaccio D, Baranger DA, Hariri AR (2016). Genetic moderation of stress effects on corticolimbic circuitry. Neuropsychopharmacology 41: 275-296.
18. Buchanan TW, Lovallo WR (2001). Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26: 307-317.
19. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW et al (2002). Role of genotype in the cycle of violence in maltreated children. Science 297: 851-854.
20. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H et al (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301: 386-389.
21. Champagne F, Meaney MJ (2001). Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133: 287-302.
22. Cloninger CR (1987). Neurogenetic adaptive mechanisms in alcoholism. Science 236: 410-416.
23. Cloninger CR, Przybeck TR, Svrakic DM (1991). The tridimensional personality questionnaire: US normative data. Psychol Rep 69(3 Pt 1): 1047-1057.
24. Cservenka A, Herting MM, Nagel BJ (2012). Atypical frontal lobe activity during verbal working memory in youth with a family history of alcoholism. Drug Alcohol Depend 123: 98-104.
25. Davies TH, Ning YM, Sanchez ER (2002). A new first step in activation of steroid receptors: hormone-induced switching of FKBP51 and FKBP52 immunophilins. J Biol Chem 277: 4597-4600.
26. Derijk RH, de Kloet ER (2008). Corticosteroid receptor polymorphisms: determinants of vulnerability and resilience. Eur J Pharmacol 583: 303-311.
27. Desmond JE, Chen SH, DeRosa E, Pryor MR, Pfefferbaum A, Sullivan EV (2003). Increased frontocerebellar activation in alcoholics during verbal working memory: an fMRI study. Neuroimage 19: 1510-1520.
28. Dube SR, Felitti VJ, Dong M, Giles WH, Anda RF (2003). The impact of adverse childhood experiences on health problems: evidence from four birth cohorts dating back to 1900. Prev Med 37: 268-277.
29. Eysenck SB, Eysenck HJ (1964). An improved short questionnaire for the measurement of extraversion and neuroticism. Life Sci 305: 1103-1109.
30. Fani N, Gutman D, Tone EB, Almli L, Mercer KB, Davis J et al (2013). FKBP5 and attention bias for threat: associations with hippocampal function and shape. JAMA Psychiatry 70: 392-400.
31. Finn PR, Mazas CA, Justus AN, Steinmetz J (2002). Early-onset alcoholism with conduct disorder: go/no go learning deficits, working memory capacity, and personality. Alcohol Clin Exp Res 26: 186-206.
32. Friedman HR, Goldman-Rakic PS (1994). Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey. J Neurosci 14(5 Pt 1): 2775-2788.
33. Gao Y, Raine A, Venables PH, Dawson ME, Mednick SA (2010). Association of poor childhood fear conditioning and adult crime. Am J Psychiatry 167: 56-60.
34. Goldman-Rakic PS (1998). Topography of cognition: Parallel distributed networks in primate association cortex. Annu Rev Neurosci 11: 137-156.
35. Gough HG (1994). Theory, development, and interpretation of the CPI socialization scale. Psychol Rep 75(1 Pt 2): 651-700.
36. Holz NE, Buchmann AF, Boecker R, Blomeyer D, Baumeister S, Wolf I et al (2015). Role of FKBP5 in emotion processing: results on amygdala activity, connectivity and volume. Brain Struct Funct 220: 1355-1368.
37. Hubler TR, Scammell JG (2004). Intronic hormone response elements mediate regulation of FKBP5 by progestins and glucocorticoids. Cell Stress Chaperones 9: 243-252.
38. Jaaskelainen T, Makkonen H, Palvimo JJ (2011). Steroid upregulation of FKBP51 and its role in hormone signaling. Curr Opin Pharmacol 11: 326-331.
39. John KR, Rattan G (1992). Test Critiques. In: Keyser DJ, Sweetland RC (eds). Shipley Institute of Living Scale-Revised, Vol IX. Pro-Ed: Austin, TX, pp 490-495.
40. Klengel T, Binder EB (2015). FKBP5 allele-specific epigenetic modification in gene by environment interaction. Neuropsychopharmacology 40: 244-246.
41. Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC, Pariante CM et al (2013). Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nature neuroscience 16: 33-41.
42. Kumsta R, Entringer S, Koper JW, van Rossum EF, Hellhammer DH, Wust S (2010). Working memory performance is associated with common glucocorticoid receptor gene polymorphisms. Neuropsychobiology 61: 49-56.
43. Kumsta R, Moser D, Streit F, Koper JW, Meyer J, Wust S (2009). Characterization of a glucocorticoid receptor gene (GR, NR3C1) promoter polymorphism reveals functionality and extends a haplotype with putative clinical relevance. Am J Med Genet B Neuropsychiatr Genet 150B: 476-482.
44. Lee RS, Tamashiro KL, Yang X, Purcell RH, Harvey A, Willour VL et al (2010). Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinology 151: 4332-4343.
45. Lejuez CW, Read JP, Kahler CW, Richards JB, Ramsey SE, Stuart GL et al (2002). Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART). J Exp Psychol Appl 8: 75-84.
46. Lovallo WR (2013). Early life adversity reduces stress reactivity and enhances impulsive behavior: implications for health behaviors. Int J Psychophysiol 90: 8-16.
47. Lovallo WR, Farag NH, Sorocco KH, Acheson A, Cohoon AJ, Vincent AS (2013). Early life adversity contributes to impaired cognition and impulsive behavior: studies from the Oklahoma Family Health Patterns Project. Alcohol Clin Exp Res 37: 616-623.
48. Lovallo WR, Farag NH, Sorocco KH, Cohoon AJ, Vincent AS (2012a). Lifetime adversity leads to blunted stress axis reactivity: studies from the Oklahoma family health patterns project. Biol Psychiatry 71: 344-349.
49. Lovallo WR, Farag NH, Sorocco KH, Cohoon AJ, Vincent AS (2012b). Lifetime adversity leads to blunted stress axis reactivity: studies from the Oklahoma Family Health Patterns Project. Biol Psychiatry 71: 344-349.
50. Lovallo WR, Farag NH, Vincent AS (2010a). Use of a resting control day in measuring the cortisol response to mental stress: diurnal patterns, time of day, and gender effects. Psychoneuroendocrinology 35: 1253-1258.
51. Lovallo WR, Robinson JL, Glahn DC, Fox PT (2010b). Acute effects of hydrocortisone on the human brain: an fMRI study. Psychoneuroendocrinology 35: 15-20.
52. Lovallo WR, Yechiam E, Sorocco KH, Vincent AS, Collins FL (2006). Working memory and decision-making biases in young adults with a family history of alcoholism: studies from the Oklahoma family health patterns project. Alcohol Clin Exp Res 30: 763-773.
53. Lupien SJ, Wilkinson CW, Briere S, Menard C, Ng Ying Kin NM, Nair NP (2002). The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology 27: 401-416.
54. McEwen BS, Weiss JM, Schwartz LS (1968). Selective retention of corticosterone by limbic structures in rat brain. Nature 220: 911-912.
55. McEwen BS, Weiss JM, Schwartz LS (1969). Uptake of corticosterone by rat brain and its concentration by certain limbic structures. Brain Res 16: 227-241.
56. Meaney MJ (2010). Epigenetics and the biological definition of gene x environment interactions. Child Dev 81: 41-79.
57. Meaney MJ, Aitken DH, Bodnoff SR, Iny LJ, Sapolsky RM (1985). The effects of postnatal handling on the development of the glucocorticoid receptor systems and stress recovery in the rat. Prog Neuropsychopharmacol Biol Psychiatry 9: 731-734.
58. Meaney MJ, Aitken DH, Bodnoff SR, Iny LJ, Tatarewicz JE, Sapolsky RM (2013). Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behav Neurosci 127: 637-641.
59. 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 Behav 12: 289-296.
60. Moffitt TE, Caspi A, Rutter M (2006). Measured gene-environment interactions in psychopathology. Perspect Psychol Sci 1: 5-27.
61. Oei NY, Tollenaar MS, Spinhoven P, Elzinga BM (2009). Hydrocortisone reduces emotional distracter interference in working memory. Psychoneuroendocrinology 34: 1284-1293.
62. Pagliaccio D, Luby JL, Bogdan R, Agrawal A, Gaffrey MS, Belden AC et al (2014). Stress-system genes and life stress predict cortisol levels and amygdala and hippocampal volumes in children. Neuropsychopharmacology 39: 1245-1253.
63. Panknin TL, Dickensheets SL, Nixon SJ, Lovallo WR (2002). Attenuated heart rate responses to public speaking in individuals with alcohol dependence. Alcohol Clin Exp Res 26: 841-847.
64. Pariante CM (2004). Glucocorticoid receptor function in vitro in patients with major depression. Stress 7: 209-219.
65. Pratt WB, Toft DO (1997). Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18: 306-360.
66. Rousseau GG, Higgins SJ, Baxter JD, Gelfand D, Tomkins GM (1975). Binding of glucocorticoid receptors to DNA. J Biol Chem 250: 6015-6021.
67. Roy A, Gorodetsky E, Yuan Q, Goldman D, Enoch MA (2010). Interaction of FKBP5, a stress-related gene, with childhood trauma increases the risk for attempting suicide. Neuropsychopharmacology 35: 1674-1683.
68. Salimetrics (2015). High sensitivity salivary cortisol enzyme immunoassay kit. https://www.salimetrics.com/assay-kit/cortisol-salivary-elisa-eia-kit.
69. SalinskyMC, Binder LM, Oken BS, Storzbach D, Aron CR, Dodrill CB (2002). Effects of gabapentin and carbamazepine on the EEG and cognition in healthy volunteers. Epilepsia 43: 482-490.
70. Sanchez MM, Young LJ, Plotsky PM, Insel TR (2000). Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. J Neurosci 20: 4657-4668.
71. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD (2003). The neural basis of economic decision-making in the Ultimatum Game. Science 300: 1755-1758.
72. Saunders B, Farag N, Vincent AS, Collins FL Jr, Sorocco KH, Lovallo WR (2008). Impulsive errors on a Go-NoGo reaction time task: disinhibitory traits in relation to a family history of alcoholism. Alcohol Clin Exp Res 32: 888-894.
73. Schultebraucks K, Wingenfeld K, Heimes J, Quinkler M, Otte C (2015). Cognitive function in patients with primary adrenal insufficiency (Addison's disease). Psychoneuroendocrinology 55: 1-7.
74. Silveri MM, Rogowska J, McCaffrey A, Yurgelun-Todd DA (2011). Adolescents at risk for alcohol abuse demonstrate altered frontal lobe activation during Stroop performance. Alcohol Clin Exp Res 35: 218-228.
75. Smith EE, Jonides J (1997). Working memory: a view from neuroimaging. Cognit Psychol 33: 5-42.
76. Smith EE, Jonides J (1999). Storage and executive processes in the frontal lobes. Science 283: 1657-1661.
77. Sorocco KH, Carnes NC, Cohoon AJ, Vincent AS, Lovallo WR (2015). Risk factors for alcoholism in the Oklahoma Family Health Patterns project: impact of early life adversity and family history on affect regulation and personality. Drug Alcohol Depend 150: 38-45.
78. Sorocco KH, Lovallo WR, Vincent AS, Collins FL (2006). Blunted hypothalamic-pituitary-adrenocortical axis responsivity to stress in persons with a family history of alcoholism. Int J Psychophysiol 59: 210-217.
79. Starkman MN, Gebarski SS, Berent S, Schteingart DE (1992). Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol Psychiatry 32: 756-765.
80. Starkman MN, Giordani B, Gebarski SS, Berent S, Schork MA, Schteingart DE (1999). Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol Psychiatry 46: 1595-1602.
81. Starkman MN, Schteingart DE, Schork MA (1981). Depressed mood and other psychiatric manifestations of Cushing's syndrome: relationship to hormone levels. Psychosom Med 43: 3-18.
82. Stroop JR (1935). Studies of interference in serial verbal reactions. J Exp Psychol 18: 643-662.
83. Terfehr K, Wolf OT, Schlosser N, Fernando SC, Otte C, Muhtz C et al (2011a). Effects of acute hydrocortisone administration on declarative memory in patients with major depressive disorder: a placebo-controlled, double-blind crossover study. J Clin Psychiatry 72: 1644-1650.
84. Terfehr K, Wolf OT, Schlosser N, Fernando SC, Otte C, Muhtz C et al (2011b). Hydrocortisone impairs working memory in healthy humans, but not in patients with major depressive disorder. Psychopharmacology (Berl) 215: 71-79.
85. Tytherleigh MY, Vedhara K, Lightman SL (2004). Mineralocorticoid and glucocorticoid receptors and their differential effects on memory performance in people with Addison's disease. Psychoneuroendocrinology 29: 712-723.
86. van Rossum EF, Binder EB, Majer M, Koper JW, Ising M, Modell S et al (2006). Polymorphisms of the glucocorticoid receptor gene and major depression. Biol Psychiatry 59: 681-688.
87. van West D, Van Den Eede F, Del-Favero J, Souery D, Norrback KF, Van Duijn C et al (2006). Glucocorticoid receptor gene-based SNP analysis in patients with recurrent major depression. Neuropsychopharmacology 31: 620-627.
88. White MG, Bogdan R, Fisher PM, Munoz KE, Williamson DE, Hariri AR (2012). FKBP5 and emotional neglect interact to predict individual differences in amygdala reactivity. Genes Brain Behav 11: 869-878.
89. Yang X, Ewald ER, Huo Y, Tamashiro KL, Salvatori R, Sawa A et al (2012). Glucocorticoid-induced loss of DNA methylation in non-neuronal cells and potential involvement of DNMT1 in epigenetic regulation of Fkbp5. Biochem Biophys Res Commun 420: 570-575.
90. Zaharia MD, Kulczycki J, Shanks N, Meaney MJ, Anisman H (1996). The effects of early postnatal stimulation on Morris watermaze acquisition in adult mice: genetic and maternal factors. Psychopharmacology (Berl) 128: 227-239.
91. Zannas AS, Binder EB (2014). Gene-environment interactions at the FKBP5 locus: sensitive periods, mechanisms and pleiotropism. Genes Brain Behav 13: 25-37.