Psychoneuroendocrinology
Volume 33, Issue 8 , Pages 1102-1110 , September 2008

Higher body mass index (BMI) is associated with reduced glucocorticoid inhibition of inflammatory cytokine production following acute psychosocial stress in men

  • Petra H. Wirtz

      Affiliations

    • Department of Clinical Psychology and Psychotherapy, University of Zurich, Switzerland
    • Corresponding Author InformationCorresponding author. Department of Clinical Psychology and Psychotherapy, University of Zurich, Binzmühlestrasse 14/Box 26, CH-8050 Zurich, Switzerland. Tel.: +41 44 635 7367; fax: +41 44 635 7359.
  • ,
  • Ulrike Ehlert

      Affiliations

    • Department of Clinical Psychology and Psychotherapy, University of Zurich, Switzerland
  • ,
  • Luljeta Emini

      Affiliations

    • Department of Clinical Psychology and Psychotherapy, University of Zurich, Switzerland
  • ,
  • Tobias Suter

      Affiliations

    • Clinical Immunology, Department of Internal Medicine, University Hospital, Zurich, Switzerland

Received 11 January 2008 ,Revised 21 April 2008 ,Accepted 23 May 2008.

References 

  1. Auphan N, DiDonato JA, Rosette C, Helmberg A, Karin M. Immunosuppression by glucocorticoids: inhibition of NF-kappa B activity through induction of I kappa B synthesis. Science. 1995;270:286–290
  2. Babyak MA. What you see may not be what you get: a brief, nontechnical introduction to overfitting in regression-type models. Psychosom. Med. 2004;66:411–421
  3. Bamberger CM, Schulte HM, Chrousos GP. Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocr. Rev. 1996;17:245–261
  4. Bhattacharyya MR, Steptoe A. Emotional triggers of acute coronary syndromes: strength of evidence, biological processes, and clinical implications. Prog. Cardiovasc. Dis. 2007;49:353–365
  5. Bierhaus A, Wolf J, Andrassy M, Rohleder N, Humpert PM, Petrov D, et al. A mechanism converting psychosocial stress into mononuclear cell activation. Proc. Natl. Acad. Sci. U.S.A. 2003;100:1920–1925
  6. Bjorntorp P. Do stress reactions cause abdominal obesity and comorbidities?. Obes. Rev. 2001;2:73–86
  7. Black PH. The inflammatory consequences of psychologic stress: relationship to insulin resistance, obesity, atherosclerosis and diabetes mellitus, type II. Med. Hypotheses. 2006;67:879–891
  8. Bray GA. Medical consequences of obesity. J. Clin. Endocrinol. Metab. 2004;89:2583–2589
  9. Brueckmann M, Bertsch T, Lang S, Sueselbeck T, Wolpert C, Kaden JJ, et al. Time course of systemic markers of inflammation in patients presenting with acute coronary syndromes. Clin. Chem. Lab. Med. 2004;42:1132–1139
  10. Brunner EJ, Chandola T, Marmot MG. Prospective effect of job strain on general and central obesity in the Whitehall II Study. Am. J. Epidemiol. 2007;165:828–837
  11. Brunner EJ, Marmot MG, Nanchahal K, Shipley MJ, Stansfeld SA, Juneja M, et al. Social inequality in coronary risk: central obesity and the metabolic syndrome. Evidence from the Whitehall II study. Diabetologia. 1997;40:1341–1349
  12. Buemann B, Black E, Holst C, Toubro S, Echwald S, Pedersen O, et al. The N363S polymorphism of the glucocorticoid receptor and metabolic syndrome factors in men. Obes. Res. 2005;13:862–867
  13. Burnstein KL, Bellingham DL, Jewell CM, Powell-Oliver FE, Cidlowski JA. Autoregulation of glucocorticoid receptor gene expression. Steroids. 1991;56:52–58
  14. Cawthorn WP, Sethi JK. TNF-alpha and adipocyte biology. FEBS Lett. 2008;582:117–131
  15. Creely SJ, McTernan PG, Kusminski CM, Fisher M, Da Silva NF, Khanolkar M, et al. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am. J. Physiol. Endocrinol. Metab. 2007;292:E740–E747
  16. Di Blasio AM, van Rossum EF, Maestrini S, Berselli ME, Tagliaferri M, Podesta F, et al. The relation between two polymorphisms in the glucocorticoid receptor gene and body mass index, blood pressure and cholesterol in obese patients. Clin. Endocrinol. (Oxf.). 2003;59:68–74
  17. Ebrecht M, Buske-Kirschbaum A, Hellhammer D, Kern S, Rohleder N, Walker B, et al. Tissue specificity of glucocorticoid sensitivity in healthy adults. J. Clin. Endocrinol. Metab. 2000;85:3733–3779
  18. Elkind MS, Cheng J, Boden-Albala B, Rundek T, Thomas J, Chen H, et al. Tumor necrosis factor receptor levels are associated with carotid atherosclerosis. Stroke. 2002;33:31–37
  19. Epel EE, Moyer AE, Martin CD, Macary S, Cummings N, Rodin J, et al. Stress-induced cortisol, mood, and fat distribution in men. Obes. Res. 1999;7:9–15
  20. Esteve E, Villuendas G, Mallolas J, Vendrell J, Lopez-Bermejo A, Rodriguez M, et al. Polymorphisms in the interleukin-6 receptor gene are associated with body mass index and with characteristics of the metabolic syndrome. Clin. Endocrinol. (Oxf.). 2006;65:88–91
  21. Gaab J, Baumann S, Budnoik A, Gmunder H, Hottinger N, Ehlert U. Reduced reactivity and enhanced negative feedback sensitivity of the hypothalamus-pituitary-adrenal axis in chronic whiplash-associated disorder. Pain. 2005;119:219–224
  22. Gidron Y, Gilutz H, Berger R, Huleihel M. Molecular and cellular interface between behavior and acute coronary syndromes. Cardiovasc. Res. 2002;56:15–21
  23. Gonzalez F, Minium J, Rote NS, Kirwan JP. Altered tumor necrosis factor alpha release from mononuclear cells of obese reproductive-age women during hyperglycemia. Metabolism. 2006;55:271–276
  24. Hardy MP, Sottas CM, Ge R, McKittrick CR, Tamashiro KL, McEwen BS, et al. Trends of reproductive hormones in male rats during psychosocial stress: role of glucocorticoid metabolism in behavioral dominance. Biol. Reprod. 2002;67:1750–1755
  25. Hemingway H, Marmot M. Evidence based cardiology: psychosocial factors in the aetiology and prognosis of coronary heart disease. Systematic review of prospective cohort studies. BMJ. 1999;318:1460–1467
  26. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J. Clin. Invest. 1995;95:2409–2415
  27. Jee SH, Sull JW, Park J, Lee SY, Ohrr H, Guallar E, et al. Body-mass index and mortality in Korean men and women. N. Engl. J. Med. 2006;355:779–787
  28. Kenchaiah S, Evans JC, Levy D, Wilson PW, Benjamin EJ, Larson MG, et al. Obesity and the risk of heart failure. N. Engl. J. Med. 2002;347:305–313
  29. Kirschbaum C, Pirke KM, Hellhammer DH. The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology. 1993;28:76–81
  30. Kloiber S, Ising M, Reppermund S, Horstmann S, Dose T, Majer M, et al. Overweight and obesity affect treatment response in major depression. Biol. Psychiatry. 2007;62:321–326
  31. Laimer M, Ebenbichler CF, Kaser S, Sandhofer A, Weiss H, Nehoda H, et al. Markers of chronic inflammation and obesity: a prospective study on the reversibility of this association in middle-aged women undergoing weight loss by surgical intervention. Int. J. Obes. Relat. Metab. Disord. 2002;26:659–662
  32. Liuzzo G, Baisucci LM, Gallimore JR, Caligiuri G, Buffon A, Rebuzzi AG, et al. Enhanced inflammatory response in patients with preinfarction unstable angina. J. Am. Coll. Cardiol. 1999;34:1696–1703
  33. Ljung T, Andersson B, Bengtsson BA, Bjorntorp P, Marin P. Inhibition of cortisol secretion by dexamethasone in relation to body fat distribution: a dose-response study. Obes. Res. 1996;4:277–282
  34. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR, et al. A transgenic model of visceral obesity and the metabolic syndrome. Science. 2001;294:2166–2170
  35. Pai JK, Pischon T, Ma J, Manson JE, Hankinson SE, Joshipura K, et al. Inflammatory markers and the risk of coronary heart disease in men and women. N. Engl. J. Med. 2004;351:2599–2610
  36. Pasquali R, Vicennati V, Cacciari M, Pagotto U. The hypothalamic-pituitary-adrenal axis activity in obesity and the metabolic syndrome. Ann. N. Y. Acad. Sci. 2006;1083:111–128
  37. Pasqui AL, Di Renzo M, Auteri A, Puccetti L. Cytokines in acute coronary syndromes. Int. J. Cardiol. 2005;105:355–356
  38. Pickup JC. Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes. Diab. Care. 2004;27:813–823
  39. Piestrzeniewicz K, Luczak K, Komorowski J, Jankiewicz-Wika J, Goch JH. Relation of C-reactive protein to obesity, adipose tissue hormones and cardiovascular risk factors in men treated with early percutaneous intervention in course of acute myocardial infarction. Neuro Endocrinol. Lett. 2007;28:427–432
  40. Plutzky J. Inflammatory pathways in atherosclerosis and acute coronary syndromes. Am. J. Cardiol. 2001;88:10K–15K
  41. Pober JS, Cotran RS. Immunologic interactions of T lymphocytes with vascular endothelium. Adv. Immunol. 1991;50:261–302
  42. Pruessner JC, Kirschbaum C, Meinlschmid G, Hellhammer DH. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology. 2003;28:916–931
  43. Ridker PM, Rifai N, Stampfer MJ, Hennekens CH. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation. 2000;101:1767–1772
  44. Rohleder N. Dynamic regulation of glucocorticoid sensitivity of pro-inflammatory cytokine production by psychosocial stress. Göttingen: Cuvillier; 2003;
  45. Rohleder N, Kudielka BM, Hellhammer DH, Wolf JM, Kirschbaum C. Age and sex steroid-related changes in glucocorticoid sensitivity of pro-inflammatory cytokine production after psychosocial stress. J. Neuroimmunol. 2002;126:69–77
  46. Rohleder N, Wolf JM, Kirschbaum C. Glucocorticoid sensitivity in humans-interindividual differences and acute stress effects. Stress. 2003;6:207–222
  47. Rosmond R, Dallman MF, Bjorntorp P. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J. Clin. Endocrinol. Metab. 1998;83:1853–1859
  48. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801–809
  49. Ross R. Atherosclerosis—an inflammatory disease. N. Engl. J. Med. 1999;340:115–126
  50. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000;21:55–89
  51. 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
  52. Steptoe A, Strike PC, Perkins-Porras L, McEwan JR, Whitehead DL. Acute depressed mood as a trigger of acute coronary syndromes. Biol. Psychiatry. 2006;60:837–842
  53. Strike PC, Magid K, Whitehead DL, Brydon L, Bhattacharyya MR, Steptoe A. Pathophysiological processes underlying emotional triggering of acute cardiac events. Proc. Natl. Acad. Sci. U.S.A. 2006;103:4322–4327
  54. Strike PC, Steptoe A. Psychosocial factors in the development of coronary artery disease. Prog. Cardiovasc. Dis. 2004;46:337–347
  55. Strike PC, Steptoe A. Behavioral and emotional triggers of acute coronary syndromes: a systematic review and critique. Psychosom. Med. 2005;67:179–186
  56. Vendrell J, Broch M, Vilarrasa N, Molina A, Gomez JM, Gutierrez C, et al. Resistin, adiponectin, ghrelin, leptin, and proinflammatory cytokines: relationships in obesity. Obes. Res. 2004;12:962–971
  57. Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB. Elevated C-reactive protein levels in overweight and obese adults. JAMA. 1999;282:2131–2135
  58. Wirtz PH, Ehlert U, Emini L, Rudisuli K, Groessbauer S, Gaab J, et al. Anticipatory cognitive stress appraisal and the acute procoagulant stress response in men. Psychosom. Med. 2006;68:851–858
  59. Wirtz PH, Elsenbruch S, Emini L, Rudisuli K, Groessbauer S, Ehlert U. Perfectionism and the cortisol response to psychosocial stress in men. Psychosom. Med. 2007;69:249–255
  60. Wirtz PH, Kanel RV, Emini L, Suter T, Fontana A, Ehlert U. Variations in anticipatory cognitive stress appraisal and differential proinflammatory cytokine expression in response to acute stress. Brain Behav. Immun. 2007;21:851–859
  61. Wirtz PH, Von Kanel R, Frey K, Ehlert U, Fischer JE. Glucocorticoid sensitivity of circulating monocytes in essential hypertension. Am. J. Hypertens. 2004;17:489–494
  62. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 1990;249:1431–1433
  63. Yamakawa T, Tanaka S, Yamakawa Y, Kiuchi Y, Isoda F, Kawamoto S, et al. Augmented production of tumor necrosis factor-alpha in obese mice. Clin. Immunol. Immunopathol. 1995;75:51–56

PII: S0306-4530(08)00134-0

doi: 10.1016/j.psyneuen.2008.05.002

Psychoneuroendocrinology
Volume 33, Issue 8 , Pages 1102-1110 , September 2008