Healthy young women with serotonin transporter SS polymorphism show a pro-inflammatory bias under resting and stress conditions

Brain, Behavior, and Immunity

Volumn 24, Issue 3, 2010, Pages 350-357

  Fredericks, Carolyn A ^a   Drabant, Emily M ^a   Edge, Michael D ^a   Tillie, Jean M ^a   Hallmayer, Joachim ^a   Ramel, Wiveka ^a   Kuo, Janice R ^a   Mackey, Sean ^a   Gross, James J ^a   Dhabhar, Firdaus S ^a,b,c  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STANFORD CANCER INSTITUTE   (United States)

Author keywords

5 HTTLPR; Cytokine; Depression; IL 10; IL 6; Immunomodulation; Inflammation; Psychosocial stress; Risk factors for depression; Serotonin transporter promoter polymorphism

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 6; SEROTONIN TRANSPORTER;

ACUTE STRESS; ADULT; ARTICLE; BEHAVIOR GENETICS; CONTROLLED STUDY; DEPRESSION; EMOTIONAL STRESS; FEMALE; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HUMAN; HUMAN EXPERIMENT; INFLAMMATION; LIFE STRESS; NORMAL HUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; SOCIAL STRESS;

ADOLESCENT; AFFECT; DNA; FEMALE; GENOTYPE; HUMANS; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-6; POLYMORPHISM, GENETIC; REST; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 77951622489     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.10.014     Document Type: Article

References (76)

1. Altemus M., Rao B., Dhabhar F.S., Ding W., Granstein R.D. Stress-induced changes in skin barrier function in healthy women. J. Invest. Dermatol. 2001, 117:309-317.
2. American Psychiatric Association, 1994. Diagnostic and statistical manual of mental disorders, fourth ed. American Psychiatric Association, Washington, DC.
3. 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., Higley J.D. Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biol. Psychiatry 2004, 55:733-738.
4. Beck A.T., Steer R.A., Brown G.K. Manual for the Beck Depression Inventory-II 1996, Psychological Corporation, San Antonio, TX.
5. Bernstein D.P., Stein J.A., Newcomb M.D., Walker E., Pogge D., Ahluvalia T., Stokes J., Handelsman L., Medrano M., Desmond D., Zule W. Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse Negl. 2003, 27:169-190.
6. Bob, P., Raboch, J., Maes, M., Susta, M., Pavlat, J., Jasova, D., Vevera, J., Uhrova, J., Benakova, H., Zima, T., 2009. Depression, traumatic stress and interleukin-6. J. Affect. Disord., doi:10.1016/j.jad.2009.03.017.
7. Brody G.H., Beach S.R., Philibert R.A., Chen Y.F., Lei M.K., Murry V.M., Brown A.C. Parenting moderates a genetic vulnerability factor in longitudinal increases in youths' substance use. J. Consult. Clin. Psychol. 2009, 77:1-11.
8. Brown G.W., Harris T.O. Social Origins of Depression: A Study of Psychiatric Disorder in Women 1978, Tavistock, London.
9. Bull S.J., Huezo-Diaz P., Binder E.B., Cubells J.F., Ranjith G., Maddock C., Miyazaki C., Alexander N., Hotopf M., Cleare A.J., Norris S., Cassidy E., Aitchison K.J., Miller A.H., Pariante C.M. Functional polymorphisms in the interleukin-6 and serotonin transporter genes, and depression and fatigue induced by interferon-alpha and ribavirin treatment. Mol. Psychiatry 2008, 13:1-10.
10. Capuron L., Ravaud A., Dantzer R. Early depressive symptoms in cancer patients receiving interleukin 2 and/or interferon alfa-2b therapy. J. Clin. Oncol. 2000, 18:2143-2151.
11. Capuron L., Gumnick J.F., Musselman D.L., Lawson D.H., Reemsnyder A., Nemeroff C.B., Miller A.H. Neurobehavioral effects of interferon-alpha in cancer patients: phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology 2002, 26:643-652.
12. Capuron L., Ravaud A., Neveu P.J., Miller A.H., Maes M., Dantzer R. Association between decreased serum tryptophan concentrations and depressive symptoms in cancer patients undergoing cytokine therapy. Mol. Psychiatry 2002, 7:468-473.
13. Capuron L., Su S., Miller A.H., Bremner J.D., Goldberg J., Vogt G.J., Maisano C., Jones L., Murrah N.V., Vaccarino V. Depressive symptoms and metabolic syndrome: is inflammation the underlying link?. Biol. Psychiatry 2008, 64:896-900.
14. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., McClay 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.
15. 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. Mol. Psychiatry 2002, 7:1058-1063.
16. Chen M.C., Joormann J., Hallmayer J., Gotlib I.H. Serotonin transporter polymorphism predicts waking cortisol in young girls. Psychoneuroendocrinology 2009, 34:681-686.
17. Cizza G., Marques A.H., Eskandari F., Christie I.C., Torvik S., Silverman M.N., Phillips T.M., Sternberg E.M. Elevated neuroimmune biomarkers in sweat patches and plasma of premenopausal women with major depressive disorder in remission: the POWER study. Biol. Psychiatry 2008, 64:907-911.
18. Cohen S., Doyle W.J., Skoner D.P. Psychological stress, cytokine production, and severity of upper respiratory illness. Psychosom. Med. 1999, 61:175-180.
19. Creswell J.D., Welch W.T., Taylor S.E., Sherman D.K., Gruenewald T.L., Mann T. Affirmation of personal values buffers neuroendocrine and psychological stress responses. Psychol. Sci. 2005, 16:846-851.
20. Daftarian P.M., Kumar A., Kryworuchko M., Diaz-Mitoma F. IL-10 production is enhanced in human T cells by IL-12 and IL-6 and in monocytes by tumor necrosis factor-alpha. J. Immunol. 1996, 157:12-20.
21. Danese A., Pariante C.M., Caspi A., Taylor A., Poulton R. Childhood maltreatment predicts adult inflammation in a life-course study. Proc. Natl. Acad. Sci. 2007, 104:1319-1324.
22. Danese A., Moffitt T.E., Pariante C.M., Ambler A., Poulton R., Caspi A. Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Arch. Gen. Psychiatry 2008, 65:409-415.
23. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
24. Dhabhar F.S. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. Neuroimmunomodulation. 2009, 16:300-317.
25. Dhabhar F.S., Burke H.M., Epel E.S., Mellon S.H., Rosser R., Reus V.I., Wolkowitz O.M. Low serum IL-10 concentrations and loss of regulatory association between IL-6 and IL-10 in adults with major depression. J. Psychiatr. Res. 2009, 43:962-969.
26. Dohrenwend B.P. Inventorying stressful life events as risk factors for psychopathology: toward resolution of the problem of intracategory variability. Psychol. Bull. 2006, 132:477-495.
27. First M.B., Gibbon M., Spitzer R.L., Williams J.B.W. User's Guide for the Structured Clinical Interview for DSM-IV Axis I Disorders - Research Version (SCID-1, Version 2.0, February 1996 Final Version) 1996, New York State Psychiatric Institute, New York.
28. Fothergill, A. (Director), 2006. " Jungles" , Planet Earth (television series). BBC, United Kingdom.
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. Biol. Psychiatry 2008, 63:847-851.
30. Hariri A.R., Drabant E.M., Munoz K.E., Kolachana B.S., Mattay V.S., Egan M.F., Weinberger D.R. A susceptibility gene for affective disorders and the response of the human amygdala. Arch. Gen. Psychiatry 2005, 62:146-152.
31. Heinrichs M., Baumgartner T., Kirschbaum C., Ehlert U. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol. Psychiatry 2003, 54:1389-1398.
32. Hu X.-Z., Lipsky R.H., Zhu G., Akhtar L.A., Taubman J., Greenberg B.D., Xu K., Arnold P.D., Richter M.A., Kennedy J.L., Murphy D.L., Goldman D. Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. Am. J. Hum. Genet. 2006, 78:815-826.
33. Kelly M.M., Tyrka A.R., Anderson G.M., Price L.H., Carpenter L.L. Sex differences in emotional and physiological responses to the Trier Social Stress Test. J. Behav. Ther. Exp. Psychiatry 2008, 39:87-98.
34. Kendler K.S., Kuhn J.W., Vittum J., Prescott C.A., 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.
35. Kenis G., Maes M. Effects of antidepressants on the production of cytokines. Int. J. Neuropsychopharmacol. 2002, 5:401-412.
36. Kilpatrick D.G., Koenen K.C., Ruggiero K.J., Acierno R., Galea S., Resnick H.S., Roitzsch J., Boyle J., Gelernter J. The serotonin transporter genotype and social support and moderation of posttraumatic stress disorder and depression in hurricane-exposed adults. Am. J. Psychiatry 2007, 164:1693-1699.
37. Kirschbaum C., Pirke K.M., Hellhammer D.H. The 'Trier Social Stress Test' - a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 1993, 28:76-81.
38. Kirschbaum C., Kudielka B.M., Gaab J., Schommer N.C., Hellhammer D.H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 1999, 61:154-162.
39. Kubera M., Kenis G., Bosmans E., Scharpé S., Maes M. Effects of serotonin and serotonergic agonists and antagonists on the production of interferon-γ and interleukin-10. Neuropsychopharmacology 2000, 23:89-98.
40. 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.L. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
41. Linden W. Development and initial validation of a life event scale for students. Can. Counsellor 1984, 18:106-110.
42. Lotrich F.E., Ferrell R.E., Rabinovitz M., Pollock B.G. Risk for depression during interferon-alpha treatment is affected by the serotonin transporter polymorphism. Biol. Psychiatry 2009, 65:344-348.
43. Maes M., Bosmans E., De Jongh R., Kenis G., Vandoolaeghe E., Neels H. Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment resistant depression. Cytokine 1997, 9:853-858.
44. Marschall D.E., Sanftner J., Tangney J.P. The State Shame and Guilt Scale 1994, George Mason University, Fairfax, VA.
45. Menard G., Turmel V., Bissonnette E.Y. Serotonin modulates the cytokine network in the lung: involvement of prostaglandin E2. Clin. Exp. Immunol. 2007, 150:340-348.
46. Mesquita A.R., Correla-Neves M., Roque S., Castro A.G., Vieira P., Pedrosa J., Palha J.A., Sousa N. IL-10 modulates depressive-like behavior. J. Psychiatr. Res. 2008, 43:89-97.
47. Miller A.H. Norman Cousins Lecture. Mechanisms of cytokine-induced behavioral changes: psychoneuroimmunology at the translational interface. Brain Behav. Immun. 2009, 23:149-158.
48. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65:732-741.
49. Monroe S.M., Reid M.W. Gene-environment interactions in depression research: genetic polymorphisms and life-stress polyprocedures. Psychol. Sci. 2008, 19:947-956.
50. Munafo M.R., Brown S.M., Hariri A.R. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol. Psychiatry 2008, 63:852-857.
51. Munafo M.R., Durrant C., Lewis G., Flint J. Gene×environment interactions at the serotonin transporter locus. Biol. Psychiatry 2009, 65:211-219.
52. Murphy D.L., Fox M.A., Timpano K.R., Moya P.R., Ren-Patterson R., Andrews A.M., Holmes A., Lesch K.P., Wendland J.R. How the serotonin story is being rewritten by new gene-based discoveries principally related to SLC6A4, the serotonin transporter gene, which functions to influence all cellular serotonin systems. Neuropharmacology 2008, 55:932-960.
53. O'Connor J.C., Lawson M.A., Andre C., Moreau M., Lestage J., Castanon N., Kelley K.W., Dantzer R. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol. Psychiatry 2009, 14:511-522.
54. Ogawa Y., Duru E.A., Ameredes B.T. Role of IL-10 in the resolution of airway inflammation. Curr. Mol. Med. 2008, 8:437-445.
55. Otte C., McCaffery J., Ali S., Whooley M.A. Association of a serotonin transporter polymorphism (5-HTTLPR) with depression, perceived stress, and norepinephrine in patients with coronary disease: the heart and soul study. Am. J. Psychiatry 2007, 164:1379-1384.
56. Pace T.W., Mletzko T.C., Alagbe O., Musselman D.L., Nemeroff C.B., Miller A.H., Heim C.M. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am. J. Psychiatry 2006, 163:1630-1633.
57. Pace T.W., Negi L.T., Adame D.D., Cole S.P., Sivilli T.I., Brown T.D., Issa M.J., Raison C.L. Effect of compassion meditation on neuroendocrine, innate immune and behavioral responses to psychosocial stress. Psychoneuroendocrinology 2009, 34:87-98.
58. Pezawas L., Meyer-Lindenberg A., Drabant E.M., Verchinski B.A., Munoz K.E., Kolachana B.S., Egan M.F., Mattay V.S., Hariri A.R., Weinberger D.R. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat. Neurosci. 2005, 8:828-834.
59. Pollak Y., Yirmiya R. Cytokine-induced changes in mood and behaviour: implications for 'depression due to a general medical condition', immunotherapy and antidepressive treatment. Int. J. Neuropsychopharmacol. 2002, 5:389-399.
60. Pruessner J.C., Kirschbaum C., Meinlschmid G., Hellhammer D.H. Two formulas for computation of area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 2003, 28:916-931.
61. Raison C.L., Borisov A.S., Majer M., Drake D.F., Pagnoni G., Woolwine B.J., Vogt G.J., Massung B., Miller A.H. Activation of central nervous system inflammatory pathways by interferon-alpha: relationship to monoamines and depression. Biol. Psychiatry 2009, 65:296-303.
62. Reichenberg A., Yirmiya R., Schuld A., Kraus T., Haack M., Morag A., Pollmacher T. Cytokine-associated emotional and cognitive disturbances in humans. Arch. Gen. Psychiatry 2001, 58:445-452.
63. Risch N., Herrell R., Lehner T., Liang K.-Y., Eaves L., Hoh J., Griem A., Kovacs M., Ott J., Merikangas K.R. Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: a meta-analysis. JAMA 2009, 301:2462-2471.
64. Richell R.A., Deakin J.F., Anderson I.M. Effect of acute tryptophan depletion on the response to controllable and uncontrollable noise stress. Biol. Psychiatry 2005, 57:295-300.
65. Roy A., Hu X.Z., Janal M.N., Goldman D. Interaction between childhood trauma and serotonin transporter gene variation in suicide. Neuropsychopharmacology 2007, 32:2046-2052.
66. Russell J.A., Weiss A., Mendelsohn G.A. Affect grid: a single-item scale of pleasure and arousal. J. Pers. Soc. Psychol. 1989, 57:493-502.
67. Schatzberg A. Recent studies of the biology and treatment of depression. Focus 2005, 3:14-24.
68. Schiepers O.J., Wichers M.C., Maes M. Cytokines and major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:201-217.
69. Song C., Halbreich U., Han C., Leonard B.E., Luo H. Imbalance between pro- and anti-inflammatory cytokines, and between Th1 and Th2 cytokines in depressed patients: the effect of electroacupuncture or fluoxetine treatment. Pharmacopsychiatry 2009, 42:182-188.
70. Sookoian S., Gemma C., Garcia S.I., Gianotti T.F., Dieuzeide G., Roussos A., Tonietti M., Trifone L., Kanevsky D., Gonzalez C.D., Pirola C.J. Short allele of serotonin transporter gene promoter is a risk factor for obesity in adolescents. Obesity 2007, 15:271-276.
71. Steptoe A., Hamer M., Chida Y. The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav. Immun. 2007, 21:901-912.
72. Tsao C.W., Lin Y.S., Chen C.C., Bai C.H., Wu S.R. Cytokines and serotonin transporter in patients with major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:899-905.
73. Uher R., McGuffin P. The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: review and methological analysis. Mol. Psychiatry 2008, 13:131-146.
74. 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. Mol. Psychiatry 2006, 11:224-226.
75. Wolpe J. The Practice of Behavior Therapy 1969, New York, Pergamon Press. second ed.
76. Wust 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.