Affective and neuroendocrine stress reactivity to an academic examination: Influence of the 5-HTTLPR genotype and trait neuroticism

Biological Psychology

Volumn 87, Issue 3, 2011, Pages 439-449

  Verschoor, Ellen ^a   Markus, C Rob ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

5 HTTLPR genotype; Cortisol; Examination stress; Mood; Neuroticism; Serotonin

Indexed keywords

HYDROCORTISONE;

5 HTTLPR GENE; ADULT; AFFECT; ARTICLE; CONTROLLED STUDY; DEPRESSION; EXAMINATION STRESS; FEMALE; GENE; GENOTYPE; HOMOZYGOSITY; HUMAN; HYDROCORTISONE SALIVA LEVEL; MALE; MOOD; NEUROENDOCRINE SYSTEM; NEUROSIS; NORMAL HUMAN; PHYSIOLOGICAL STRESS; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIORITY JOURNAL; PROFILE OF MOOD STATES; SALIVA LEVEL; UNIVERSITY STUDENT;

AFFECT; ALLELES; ANXIETY; FEMALE; GENOTYPE; HUMANS; HYDROCORTISONE; MALE; NEUROTIC DISORDERS; PERSONALITY; POLYMORPHISM, GENETIC; PSYCHIATRIC STATUS RATING SCALES; SALIVA; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 79960099773     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2011.06.001     Document Type: Article

References (99)

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 2009, 34:1294-1303.
2. Bale T.L. Stress sensitivity and the development of affective disorders. Hormones and Behavior 2006, 50:529-533.
3. Barelds P.H., Luteijn F. Measuring personality: a comparison of three personality questionnaires in the Netherlands. Personality and Individual Differences 2002, 33:499-510.
4. Barr C.S., Newman T.K., Shannon C., Parker C., Dvoskin R.L., Becker M.L., Schwandt M., Champoux M., Lesch K.P., Goldman D., Suomi S.J., Highley J.D. Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biological Psychiatry 2004, 55:733-738.
5. Beck A.T., Ward C.H., Mendelson M., Mock J., Erbaugh J. An inventory for measuring depression. Archives of General Psychiatry 1961, 4:561-571.
6. Beevers C.G., Gibb B.E., McGeary J.E., Miller I.W. Serotonin transporter genetic variation and biased attention for emotional word stimuli among psychiatric inpatients. Journal of Abnormal Psychology 2007, 116:208-212.
7. Belsky J., Bakermans-Kranenburg M.J., Van IJzendoorn M.H. For better and worse. Differential susceptibility to environmental influences. Current Directions in Psychological Science 2007, 16:300-304.
8. Belsky J., Jonassaint C., Pluess M., Stanton M., Brummett B., Williams R. Vulnerability genes or plasticity genes?. Molecular Psychiatry 2009, 14:746-754.
9. Belsky J., Pluess M. Beyond diathesis stress: differential susceptibility to environmental influences. Psychological Bulletin 2009, 135:885-908.
10. Bolger N., Schilling E.A. Personality and the problems of everyday life: the role of neuroticism in exposure and reactivity to daily stressors. Journal of Personality 1991, 59:355-386.
11. Boyce W.T., Ellis B.J. Biological sensitivity to context: I. An evolutionary-developmental theory of origins and functions of stress reactivity. Developmental Psychopathology 2005, 17:271-301.
12. Brummett B.H., Muller C.L., Collins A.L., Boyle S.H., Kuhn C.M., Siegler I.C., et al. 5-HTTLPR and gender moderate changes in negative affect responses to tryptophan infusion. Behavior Genetics 2008, 38:476-483.
13. Brummett B.H., Siegler I.C., McQuoid D.R., Svenson I.K., Marchuk D.A., Steffens D.C. Associations among the NEO personality inventory, revised and the serotonin transporter gene-linked polymorphic region in elders: effects of depression and gender. Psychiatric Genetics 2003, 13:13-18.
14. Budde H., Voelcker-Rehage C., Pietrassyk-Kendziorra S., Machado S., Ribeiro P., Arafat A.M. Steroid hormones in the saliva of adolescents after different exercise intensities and their influence on working memory in a school setting. Psychoneuroendocrinology 2010, 35:382-391.
15. Canli T., Zhao Z., Desmond J.E., Kang E., Gross J., Gabrieli J.D. An fMRI study of personality influences on brain reactivity to emotional stimuli. Behavioral Neuroscience 2001, 115:33-42.
16. Caspi A., Hariri A.R., Holmes A., Uher R., Moffit T. Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. American Journal of Psychiatry 2010, 167:509-527.
17. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., McClayF J., Mill J., Martin J., Braithwaite A., Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
18. Champoux M., Bennett A., Shannon C., Higley J.D., Lesch K.P., Suomi S.J. Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Molecular Psychiatry 2002, 7:1058-1063.
19. Chan S.W.Y., Norbury R., Goodwin G.M., Harmer C.J. Risk for depression and neural responses to fearful facial expressions of emotion. British Journal of Psychiatry 2009, 194:139-145.
20. Costa P.T., McCrae R.R. Influence of extraversion and neuroticism on subjective well-being: happy and unhappy people. Journal of Personality and Social Psychology 1980, 38:668-678.
21. Dannlowski U., Ohrmann P., Konrad C., Domschke K., Bauer J., Kugel H., Hohoff C., Schoning S., Kersting A., Baune B.T., Mortensen L.S., Arolt V., Zwisterlood P., Deckert J., Heindel W., Suslow T. Reduced amygdala-prefrontal coupling in major depression: association with MAOA genotype and illness severity. International Journal of Neuropsychopharmacology 2009, 12:11-22.
22. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin 2004, 130:355-391.
23. Dougherty L.R., Klein D.N., Congdon E., Canli T., Hayden E.P. Interaction between 5-HTTLPR and BDNF Val66Met polymorphisms on HPA axis reactivity in preschoolers. Biological Psychology 2010, 83:93-100.
24. Du L., Bakish D., Hrdina P.D. Gender differences in association between serotonin transporter gene polymorphism and personality traits. Psychiatric Genetics 2000, 10:159-164.
25. Eley T.C., Sugden K., Corsico A., Gregory A.M., Sham P., McGuffin P., et al. Gene-environment interaction analysis of serotonin system markers with adolescent depression. Molecular Psychiatry 2004, 9:908-915.
26. Fanous A.H., Gardner C.O., Prescott C.A., Cancro R., Kendler K.S. Neuroticism, major depression and gender: a population-based twin study. Psychological Medicine 2002, 32:719-728.
27. Firk C., Markus C.R. Differential effects of 5-HTTLPR genotypes on mood, memory and attention bias following acute tryptophan depletion and stress exposure. Psychopharmacology 2009, 203:805-818.
28. Foley P., Kirschbaum C. Human hypothalamus-pituitary-adrenal axis responses to acute psychosocial stress in laboratory settings. Neuroscience and Biobehavioral Reviews 2010, 35:91-96.
29. Gotlib I.H., Joormann J., Minor K.L., Hallmayer J. HPA axis reactivity: a mechanism underlying the associations among 5-HTTLPR, stress and depression. Biological Psychiatry 2008, 63:847-851.
30. Gottesman I.I., Gould T.D. The endophenotype concept in psychiatry: etymology and strategic intentions. American Journal of Psychiatry 2003, 160:636-645.
31. Greenberg B.D., Li Q., Lucas F.R., Hu S., Sirota L.A., Benjamin J., Lesch K.P., Hamer D., Murphy D.L. Association between the serotonin transporter promoter polymorphism and personality traits in a primarily female population sample. American Journal of Medical Genetics. Part B: Neuropsychiatric Genetics 2000, 96:202-216.
32. Hariri A.R., Holmes A. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends in Cognitive Sciences 2006, 10:182-191.
33. Heils A., Teufel A., Petri S., Stober G., Riederer P., Bengel D., Lesch K.P. Allelic variation of human serotonin transporter gene expression. Journal of Neurochemistry 1996, 66:2621-2624.
34. Hennig J., Possel P., Netter P. Sensitivity to disgust as an indicator of neuroticism: a psychobiological approach. Personality and Individual Differences 1996, 20:589-596.
35. Hill E.E., Zack E., Battaglini C., Viru M., Viru A., Hackney A.C. Exercise and circulating cortisol levels: the intensity threshold effect. Journal of Endocrinological Investigation 2008, 31:587-591.
36. Houtman I.L., Bakker F.C. Individual differences in reactivity to and coping with the stress of lecturing. Journal of Psychosomatic Research 1991, 35:11-24.
37. Hutchinson J.G., Williams P.G. Neuroticism, daily hassles, and depressive symptoms: an examination of moderating and mediating effects. Personality and Individual Differences 2007, 42:1367-1378.
38. Karg K., Burmeister M., Shedden K., Sen S. The serotonin transporter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Archives of General Psychiatry 2011, 68:444-454.
39. Kendler K.S., Gardner C.O., Prescott C.A. Personality and the experience of environmental adversity. Psychological Medicine 2003, 33:1193-1202.
40. Kendler K.S., Kuhn J., Prescott C.A. The interrelationship of neuroticism, sex, and stressful life events in the prediction of episodes of major depression. American Journal of Psychiatry 2004, 161:631-636.
41. Kraemer G.W., Moore C.F., Newman T.K., Barr C.S., Schneider M.L. Moderate level of fetal alcohol exposure and serotonin transporter gene promoter polymorphism affect neonatal temperament and LHPA axis regulation in monkeys. Biological Psychiatry 2008, 63:317-324.
42. Kudielka B.M., Hellhammer D.H., Wüst S. Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology 2009, 34:2-18.
43. Kunz-Ebrecht S.R., Kirschbaum C., Steptoe A. Work stress, socioeconomic status and neuroendocrine activation over the working day. Social Science & Medicine 2004, 58:1523-1530.
44. Lahey B.B. Public health significance of neuroticism. American Journal of Psychology 2009, 64:241-256.
45. Lesch K.P., Bengel D., Heils A., Sabol S.Z., Greenberg B.D., Petri S., Benjamin J., Muller C.R., Hamer D.H., Murphy D.I. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
46. Luteijn F., Starren J., Van Dijk H. Nederlandse Persoonlijkheids Vragenlijst [Dutch Personality Questionnaire] 1975, Swetz en Zeitlinger, Lisse.
47. Luteijn F., Starren J., Van Dijk H. NPV: Handleiding, herziene versie uitgave 2000 [NPV: Manual, Revised Version Issue 2000] 2000, Swets & Zeitlinger B.V., Lisse.
48. Malouff J.M., Thorsteinsson E.B., Schutte N.S. The relationship between the five-factor model of personality and symptoms of clinical disorders: a meta-analysis. Journal of Psychopathology and Behavioral Assessment 2005, 27:101-114.
49. Markus C.R., Firk C. Differential effects of tri-allelic 5-HTTLPR polymorphisms in healthy subjects on mood and stress performance after tryptophan challenge. Neuropsychopharmacology 2009, 34:2667-2674.
50. Markus, C.R., De Raedt, R., 2011. Differential effects of 5-HTTLPR genotypes on inhibition of negative emotional information following acute stress exposure and tryptophan challenge. Neuropsychopharmacology 36, 819-826.
51. McChargue D.E., Cohen L.M., Werth-Cook J. The influence of personality and affect on nicotine dependence among male college students. Nicotine & Tobacco Research 2004, 6:287-294.
52. McCormack K., Newman T.K., Higley J.D., Maestripieri D., Sanchez M.M. Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Hormones and Behavior 2009, 55:538-547.
53. Middeldorp C.M., De Geus E.J.C., Beem A.L., Lakenberg N., Hottenga J.J., Slagboom P.E., Boomsma D.I. Family based association analyses between the serotonin transporter gene polymorphism (5-HTTLPR) and neuroticism, anxiety and depression. Behavioral Genetics 2007, 37:294-301.
54. Mueller A., Brocke B., Fries E., Lesch K.P., Kirschbaum C. The role of the serotonin transporter polymorphism for the endocrine stress response in newborns. Psychoneuroendocrinology 2010, 35:289-296.
55. Munafo M.R., Clark T., Flint J. Does measurement instrument moderate the association between the serotonin transporter gene and anxiety-related personality traits? A meta-analysis. Molecular Psychiatry 2005, 10:415-419.
56. Munafo M.R., Clark T.G., Moore L.R., Payne E., Walton R., Flint J. Genetic polymorphisms and personality in healthy adults: a systematic review and meta-analysis. Molecular Psychiatry 2003, 8:471-484.
57. Munafo M.R., Durrant C., Lewis G., Flint J. Gene X environment interactions at the serotonin transporter locus. Biological Psychiatry 2009, 65:211-219.
58. Munafo M.R., Freimer N.B., Ophoff R., Veijola J., Miettunen J., Järvelin M.R., Taanila A., Flint J. 5-HTTLPR genotype and anxiety-related personality traits: a meta-analysis and new data. American Journal of Medical Genetics. Part B: Neuropsychiatric Genetics 2009, 150B:271-281.
59. Munafo M.R., Brown S.M., Hariri A.R. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biological Psychiatry 2008, 63:852-857.
60. Neumeister A., Xian-Zhang H., Luckenbaugh D.A., Schwarz M., Nugent A.C., Bonne O., Hercovitch P., Goldman D., Drevets W.C., Charney D.S. Differential effects of 5-HTTLPR genotypes on the behavioral and neural responses to tryptophan depletion in patients with major depression and controls. Archives of General Psychiatry 2006, 63:978-986.
61. O'Connor P.J., Corrigan D.L. Influence of short-term cycling on salivary cortisol levels. Medicine & Science in Sports & Exercise 1987, 19:224-228.
62. Ormel J., Wolfarth T. How neuroticism, long-term difficulties, and life situation change influence psychological distress: a longitudinal model. Journal of Personality and Social Psychology 1991, 60:744-755.
63. Oswald L.M, Zandi P., Nestadth G., Potash J.B., Kalaydjian A.E., Wand G.S. Relationship between cortisol responses to stress and personality. Neuropsychopharmacology 2006, 31:1583-1591.
64. Parslow R.A., Jorm A.F., Christensen H. Associations of pre-trauma attributes and trauma exposure with screening positive for PTSD: analysis of a community-based study of 2085 young adults. Psychological Medicine 2006, 36:387-395.
65. Peeters F.P.M.L., Ponds R.W.H.M., Vermeeren M.T.G. Affectivity and self-report of depression and anxiety. Tijdschrift van de Psychologie [Magazine of Psychology] 1996, 38:240-250. (Dutch).
66. Phillips A.C., Carroll D., Burns V.E., Drayson M. Neuroticism, cortisol reactivity, and antibody response to vaccination. Psychophysiology 2005, 42:232-238.
67. Rijsdijk F.V., Sham P.C., Sterne A., Purcell S., McGuffin P., Farmer A., Goldberg D., Mann A., Cherny S.S., Webster M., Ball D., Eley T.C., Plomin R. Life events and depression in a community sample of siblings. Psychological Medicine 2001, 29:1055-1067.
68. Risch N., Herrell R., Lehner T., Liang K.Y., Eaves L., Hoh J., et al. Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: a meta-analysis. JAMA 2009, 301:2462-2471.
69. Rutter M. Biological implications of gene-environment interaction. Journal of Abnormal Child Psychology 2008, 36:969-975.
70. Rutter M. Gene-environment interplay. Depression and Anxiety 2010, 27:1-4.
71. Schneider T.R. The role of neuroticism on psychological and physiological stress responses. Journal of Experimental Social Psychology 2004, 40:795-804.
72. Schinka J.A., Busch R.M., Robichaux-Keene N. A meta-analysis of the association between the serotonin transporter gene polymorphism (5-HTTLPR) and trait anxiety. Molecular Psychiatry 2004, 9:197-202.
73. Schommer N.C., Kudielka B.M., Hellhammer D.H., Kirschbaum C. No evidence for a close relationship between personality traits and circadian cortisol rhythm or a single cortisol stress response. Psychological Research 1999, 84:840-842.
74. Schoofs D., Hartmann R., Wolf O.T. Neuroendocrine stress responses to an oral academic examination: no strong influence of sex, repeated participation and personality traits. Stress 2008, 11:52-61.
75. Sen S., Burmeister M., Ghosh D. Meta-analysis of the association between a serotonin transporter polymorphism (5-HTTLPR) and anxiety-related personality traits. American Journal of Medical Genetics. Part B: Neuropsychiatric Genetics 2004, 127B:85-89.
76. Shoji K., Harrigan J.A., Woll S.B., Miller S.A. Interactions among situations, neuroticism, and appraisals in coping strategy choice. Personality and Individual Differences 2009, 48:270-276.
77. Siegle G.J., Thompson W., Carter C.S., Steinhauer S.R., Thase M.E. Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biological Psychiatry 2007, 61:198-209.
78. Stress - From Molecules to Behavior. A Comprehensive Analysis of the Neurobiology of Stress Responses 2010, Wiley-Blackwell, Weinheim. H. Soreq, A. Friedman, D. Kaufer (Eds.).
79. Spinelli S., Schwandt M.L., Lindell S.G., Newman T.K., Heilig M., Suomi S.J., Higley J.D., Goldman D., Barr C. Association between the recombinant human serotonin transporter linked promoter region polymorphism and behavior in rhesus macaques during a separation paradigm. Developmental Psychopathology 2007, 19:977-987.
80. Stein M.B., Simmons A.N., Feinstein J.S., Paulus M.P. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. American Journal of Psychiatry 2007, 164:318-327.
81. Stowell J.R. Use and abuse of academic examinations in stress research. Psychosomatic Medicine 2003, 65:1055-1057.
82. Uher R., McGuffin P. The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: review and methodological analysis. Molecular Psychiatry 2008, 13:131-146.
83. Uher R., McGuffin P. The moderation by the serotonin transporter gene of environmental adversity in the etiology of depression: 2009 update. Molecular Psychiatry 2010, 15:18-22.
84. Van Eck M.M.M., Nicolson N.A., Berkhof H., Sulon J. Individual differences in cortisol responses to a laboratory speech task and their relationship to responses to stressful daily events. Biological Psychology 1996, 43:69-84.
85. Van Os J., Jones P.B. Early risk factors and adult person-environment relationships in affective disorders. Psychological Medicine 1999, 29:1055-1067.
86. Wald F.D.M., Mellenbergh G.J. De verkorte versie van de Nederlandse vertaling van de profile of mood states (POMS) [The shortened version of the Dutch translation of the profile of mood states (POMS)]. Nederlands Tijdschrift voor de Psychologie 1990, 45:86-90.
87. Walderhaug E., Magnusson A., Neumeister A., Lappalainen J., Lunde H., Refsum H., Landro N.I. Interactive effects of sex and 5-HTTLPR on mood and impulsivity during tryptophan depletion in healthy people. Biological Psychiatry 2007, 62:593-599.
88. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. Journal of Personality and Social Psychology 1988, 54:1063-1070.
89. Watson D., Tellegen A. Toward a consensual structure of mood. Psychological Bulletin 1985, 98:219-235.
90. Way B.M., Taylor S.E. The serotonin transporter promoter polymorphism is associated with cortisol response to psychosocial stress. Biological Psychiatry 2010, 67:487-492.
91. Weekes N., Lewis R., Patel F., Garrison-Jakel J., Berger D.E., Lupien S.J. Examination stress as an ecological inducer of cortisol and psychological responses to stress in undergraduate students. Stress 2006, 9:199-206.
92. Wendland J.R., Martin B.J., Kruse M.R., Lesch K.P., Murphy D.L. Simultaneous genotyping of four functional loci of human SLC6A4, with a reappraisal of 5-HTTLPR and rs25531. Molecular Psychiatry 2006, 11:224-226.
93. Wilhelm K., Mitchell P.B., Niven H., Finch A., Wedgwood L., Scimone A., Blair I.P., Parker G., Schofield P.R. Life events, first depression onset and the serotonin transporter gene. British Journal of Psychiatry 2006, 188:210-215.
94. Williams D.G. Personality effects in current mood: pervasive or reactive?. Personality and Individual Differences 1989, 10:948-1948.
95. Williams D.G. Effects of psychoticism, extraversion, and neuroticism in current mood: a statistical review of six studies. Personality and Individual Differences 1990, 6:615-630.
96. Willis-Owen S.A.G., Turri M.G., Munafo M.R., Surtees P.G., Wainwright N.W.J., Brixey R.D., Flint J. The serotonin transporter length polymorphism, neuroticism, and depression: a comprehensive assessment of association. Biological Psychiatry 2005, 58:451-456.
97. Wüst S., Kumsta R., Treutlein J., Frank J., Entringer S., Schulze T.G., Rietschel M. Sex-specific association between the 5-HTT gene-linked polymorphic region and basal cortisol secretion. Psychoneuroendocrinology 2009, 34:972-982.
98. Zalsman G., Huang Y.Y., Oquendo M.A., Burke A.K., Hu X.Z., Brent D.A., Ellis S.P., Goldman D., Mann J.J. Association of a triallelic serotonin transporter gene promoter region (5-HTTLPR) polymorphism with stressful life events and severity of depression. American Journal of Psychiatry 2006, 163:1588-1593.
99. Zobel A., Barkow K., Schulze-Rauschenbach S., Von Widdern O., Metten M., Pfeiffer U., Schnell S., Wagner M., Maier W. High neuroticism and depressive temperament are associated with dysfunctional regulation of the hypothalamic-pituitary-adrenocortical system in healthy volunteers. Acta Psychiatrica Scandinavia 2004, 109:392-399.