Acute and chronic stress induced changes in sensitivity of peripheral inflammatory pathways to the signals of multiple stress systems - 2011 Curt Richter Award Winner

Psychoneuroendocrinology

Volumn 37, Issue 3, 2012, Pages 307-316

  Rohleder, Nicolas ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

Acetylcholine; Acute stress; Catecholamine; Chronic low grade inflammation; Chronic stress; Cytokines; Glucocorticoid; HPA axis; Parasympathetic nervous system; Sympathetic nervous system

Indexed keywords

ACETYLCHOLINE; BETA 2 ADRENERGIC RECEPTOR; CATECHOLAMINE; CD11B ANTIGEN; GAMMA INTERFERON; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 5; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ACUTE STRESS; ADRENERGIC SYSTEM; BREAST CANCER; CANCER FATIGUE; CANCER SURVIVOR; CAREGIVER; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CHRONIC STRESS; CYTOKINE PRODUCTION; ENDOCRINE FUNCTION; GENE EXPRESSION; GENE TRANSLOCATION; GLUCOCORTICOID RESISTANCE; GLUCOCORTICOID SENSITIVITY; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFLAMMATION; LEUKOCYTE; MENTAL STRESS; NEUTROPHIL; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REVIEW; VAGUS NERVE STIMULATION;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; GLUCOCORTICOIDS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFLAMMATION; INFLAMMATION MEDIATORS; PITUITARY-ADRENAL SYSTEM; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 84856582487     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2011.12.015     Document Type: Review

References (92)

1. Avitsur R., Kavelaars A., Heijnen C., Sheridan J.F. Social stress and the regulation of tumor necrosis factor-alpha secretion. Brain Behav Immun 2005, 19:311-317.
2. Avitsur R., Powell N., Padgett D.A., Sheridan J.F. Social interactions, stress, and immunity. Immunol Allergy Clin North Am 2009, 29:285-293.
3. Avitsur R., Stark J.L., Sheridan J.F. Social stress induces glucocorticoid resistance in subordinate animals. Horm Behav 2001, 39:247-257.
4. Bailey M.T., Avitsur R., Engler H., Padgett D.A., Sheridan J.F. Physical defeat reduces the sensitivity of murine splenocytes to the suppressive effects of corticosterone. Brain Behav Immun 2004, 18:416-424.
5. Bamberger C.M., Schulte H.M., Chrousos G.P. Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocr Rev 1996, 17:245-261.
6. Besedovsky H.O., del Rey A., Sorkin E., Da Prada M., Keller H.H. Immunoregulation mediated by the sympathetic nervous system. Cell Immunol 1979, 48:346-355.
7. Besedovsky H.O., del Rey A. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr Rev 1996, 17:64-102.
8. Bierhaus A., Wolf J., Andrassy M., Rohleder N., Humpert P.M., Petrov D., Ferstl R., von Eynatten M., Wendt T., Rudofsky G., Joswig M., Morcos M., Schwaninger M., McEwen B., Kirschbaum C., Nawroth P.P. A mechanism converting psychosocial stress into mononuclear cell activation. Proc Natl Acad Sci U S A 2003, 100:1920-1925.
9. Binder E.B., Salyakina D., Lichtner P., Wochnik G.M., Ising M., Putz B., Papiol S., Seaman S., Lucae S., Kohli M.A., Nickel T., Kunzel H.E., Fuchs B., Majer M., Pfennig A., Kern N., Brunner J., Modell S., Baghai T., Deiml T., Zill P., Bondy B., Rupprecht R., Messer T., Kohnlein O., Dabitz H., Bruckl T., Muller N., Pfister H., Lieb R., Mueller J.C., Lohmussaar E., Strom T.M., Bettecken T., Meitinger T., Uhr M., Rein T., Holsboer F., Muller-Myhsok B. Polymorphisms in Fkbp5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat Genet 2004, 36:1319-1325.
10. Borovikova L.V., Ivanova S., Zhang M., Yang H., Botchkina G.I., Watkins L.R., Wang H., Abumrad N., Eaton J.W., Tracey K.J. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000, 405:458-462.
11. Bower J.E., Ganz P.A., Aziz N., Olmstead R., Irwin M.R., Cole S.W. Inflammatory responses to psychological stress in fatigued breast cancer survivors: relationship to glucocorticoids. Brain Behav Immun 2007, 21:251-258.
12. Bower J.E., Ganz P.A., Irwin M.R., Arevalo J.M., Cole S.W. Fatigue and gene expression in human leukocytes: increased Nf-Kappab and decreased glucocorticoid signaling in breast cancer survivors with persistent fatigue. Brain Behav Immun 2011, 25:147-150.
13. Bruchfeld A., Goldstein R.S., Chavan S., Patel N.B., Rosas-Ballina M., Kohn N., Qureshi A.R., Tracey K.J. Whole blood cytokine attenuation by cholinergic agonists ex vivo and relationship to vagus nerve activity in rheumatoid arthritis. J Intern Med 2010, 268:94-101.
14. Capellino S., Straub R.H. Neuroendocrine immune pathways in chronic arthritis. Best Pract Res Clin Rheumatol 2008, 22:285-297.
15. Capitanio J.P., Mendoza S.P., Cole S.W. Nervous temperament in infant monkeys is associated with reduced sensitivity of leukocytes to Cortisol's influence on trafficking. Brain Behav Immun 2011, 25:151-159.
16. Cole S.W. Social regulation of leukocyte homeostasis: the role of glucocorticoid sensitivity. Brain Behav Immun 2008, 22:1049-1055.
17. Cole S.W., Hawkley L.C., Arevalo J.M., Sung C.Y., Rose R.M., Cacioppo J.T. Social regulation of gene expression in human leukocytes. Genome Biol 2007, 8:R189.
18. Cole S.W., Mendoza S.P., Capitanio J.P. Social stress desensitizes lymphocytes to regulation by endogenous glucocorticoids: insights from in vivo cell trafficking dynamics in rhesus macaques. Psychosom Med 2009, 71:591-597.
19. Danesh J., Whincup P., Walker M., Lennon L., Thomson A., Appleby P., Gallimore J.R., Pepys M.B. Low grade inflammation and coronary heart disease: prospective study and updated meta-analyses. BMJ 2000, 321:199-204.
20. deKloet C.S., Vermetten E., Bikker A., Meulman E., Geuze E., Kavelaars A., Westenberg H.G., Heijnen C.J. Leukocyte glucocorticoid receptor expression and immunoregulation in veterans with and without post-traumatic stress disorder. Mol Psychiatry 2007, 12:443-453.
21. del Rey A., Besedovsky H.O., Sorkin E., da Prada M., Arrenbrecht S. Immunoregulation mediated by the sympathetic nervous system II. Cell Immunol 1981, 63:329-334.
22. DeRijk R.H., Petrides J., Deuster P., Gold P.W., Sternberg E.M. Changes in corticosteroid sensitivity of peripheral blood lymphocytes after strenous exercise in humans. J Clin Endocrinol Metab 1996, 81:228-235.
23. Dhabhar F.S. Stress-induced augmentation of immune function-the role of stress hormones. Leukocyte trafficking, and cytokines. Brain Behav Immun 2002, 16:785-798.
24. Dhabhar F.S., Miller A.H., McEwen B.S., Spencer R.L. Stress-induced changes in blood leukocyte distribution. Role of adrenal steroid hormones. J Immunol 1996, 157:1638-1644.
25. Ebrecht M., Buske-Kirschbaum A., Hellhammer D., Kern S., Rohleder N., Walker B., Kirschbaum C. Tissue specificity of glucocorticoid sensitivity in healthy adults. J Clin Endocrinol Metab 2000, 85:3733-3739.
26. Elenkov I.J., Wilder R.L., Chrousos G.P., Vizi E.S. The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000, 52:595-638.
27. Engler H., Bailey M.T., Engler A., Stiner-Jones L.M., Quan N., Sheridan J.F. Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 2008, 33:108-117.
28. Engler H., Engler A., Bailey M.T., Sheridan J.F. Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice. J Neuroimmunol 2005, 163:110-119.
29. Ershler W.B., Keller E.T. Age-associated increased interleukin-6 gene expression. Late-life diseases, and frailty. Annu Rev Med 2000, 51:245-270.
30. Felten D.L., Felten S.Y., Bellinger D.L., Carlson S.L., Ackerman K.D., Madden K.S., Olschowki J.A., Livnat S. Noradrenergic sympathetic neural interactions with the immune system: structure and function. Immunol Rev 1987, 100:225-260.
31. Hansson G.K. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005, 352:1685-1695.
32. Heijnen C.J. Receptor regulation in neuroendocrine-immune communication: current knowledge and future perspectives. Brain Behav Immun 2007, 21:1-8.
33. Huston J.M., Ochani M., Rosas-Ballina M., Liao H., Ochani K., Pavlov V.A., Gallowitsch-Puerta M., Ashok M., Czura C.J., Foxwell B., Tracey K.J., Ulloa L. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J Exp Med 2006, 203:1623-1628.
34. Jänig W., Habler H.J. Neurophysiological analysis of target-related sympathetic pathways - from animal to human: similarities and differences. Acta Physiol Scand 2003, 177:255-274.
35. Kavelaars A., Ballieux R.E., Heijnen C.J. Differential effects of beta-endorphin on camp levels in human peripheral blood mononuclear cells. Brain Behav Immun 1990, 4:171-179.
36. Kavelaars A., Kuis W., Knook L., Sinnema G., Heijnen C.J. Disturbed neuroendocrine-immune interactions in chronic fatigue syndrome. J Clin Endocrinol Metab 2000, 85:692-696.
37. Kiecolt-Glaser J.K., Preacher K.J., MacCallum R.C., Atkinson C., Malarkey W.B., Glaser R. Chronic stress and age-related increases in the proinflammatory cytokine Il-6. Proc Natl Acad Sci U S A 2003, 100:9090-9095.
38. Kohm A.P., Sanders V.M. Norepinephrine: a messenger from the brain to the immune system. Immunol Today 2000, 21:539-542.
39. Kumsta R., Entringer S., Koper J.W., van Rossum E.F., Hellhammer D.H., Wust S. Glucocorticoid receptor gene polymorphisms and glucocorticoid sensitivity of subdermal blood vessels and leukocytes. Biol Psychol 2008, 79:179-184.
40. Malpas S.C. Sympathetic nervous system overactivity and its role in the development of cardiovascular disease. Physiol Rev 2010, 90:513-557.
41. Mausbach B.T., Aschbacher K., Mills P.J., Roepke S.K., von Kanel R., Patterson T.L., Dimsdale J.E., Ziegler M.G., Ancoli-Israel S., Grant I. A 5-year longitudinal study of the relationships between stress, coping, and immune cell beta(2)-adrenergic receptor sensitivity. Psychiatry Res 2008, 160:247-255.
42. McKay L.I., Cidlowski J.A. Molecular control of immune/inflammatory responses: interactions between nuclear factor-kappa B and steroid receptor-signaling pathways. Endocr Rev 1999, 20:435-459.
43. Miller G.E., Blackwell E. Turning up the heat: inflammation as a mechanism linking chronic stress, depression, and heart disease. Curr Dir Psychol Sci 2006, 15:269-272.
44. Miller G.E., Cohen S., Ritchey A.K. Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid-resistance model. Health Psychol 2002, 21:531-541.
45. Miller G.E., Chen E., Fok A.K., Walker H., Lim A., Nicholls E.F., Cole S., Kobor M.S. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci U S A 2009, 106:14716-14721.
46. Miller G.E., Chen E., Sze J., Marin T., Arevalo J.M., Doll R., Ma R., Cole S.W. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased Nf-Kappab signaling. Biol Psychiatry 2008, 64:266-272.
47. Miller G.E., Gaudin A., Zysk E., Chen E. Parental support and cytokine activity in childhood asthma: the role of glucocorticoid sensitivity. J Allergy Clin Immunol 2009, 123:824-830.
48. Miller G.E., Rohleder N., Stetler C., Kirschbaum C. Clinical depression and regulation of the inflammatory response during acute stress. Psychosom Med 2005, 67:679-687.
49. Mohamed-Ali V., Flower L., Sethi J., Hotamisligil G., Gray R., Humphries S.E., York D.A., Pinkney J. Beta-adrenergic regulation of Il-6 release from adipose tissue: in vivo and in vitro studies. J Clin Endocrinol Metab 2001, 86:5864-5869.
50. Mommersteeg P.M., Heijnen C.J., Kavelaars A., van Doornen L.J. Immune and endocrine function in burnout syndrome. Psychosom Med 2006, 68:879-886.
51. Nance D.M., Sanders V.M. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav Immun 2007, 21:736-745.
52. O'Donovan A., Sun B., Cole S., Rempel H., Lenoci M., Pulliam L., Neylan T. Transcriptional control of monocyte gene expression in post-traumatic stress disorder. Dis Markers 2011, 30:123-132.
53. Otte C., Wust S., Zhao S., Pawlikowska L., Kwok P.Y., Whooley M.A. Glucocorticoid receptor gene and depression in patients with coronary heart disease: the heart and soul study - 2009 Curt Richter Award Winner. Psychoneuroendocrinology 2009, 34:1574-1581.
54. Otte C., Wust S., Zhao S., Pawlikowska L., Kwok P.Y., Whooley M.A. Glucocorticoid receptor gene, low-grade inflammation, and heart failure: the heart and soul study. J Clin Endocrinol Metab 2010, 95:2885-2891.
55. Pace T.W., Hu F., Miller A.H. Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain Behav Immun 2007, 21:9-19.
56. Pariante C.M., Miller A.H. Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment. Biol Psychiatry 2001, 49:391-404.
57. Pariante C.M. Glucocorticoid receptor function in vitro in patients with major depression. Stress 2004, 7:209-219.
58. Pavlov V.A., Wang H., Czura C.J., Friedman S.G., Tracey K.J. The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation. Mol Med 2003, 9:125-134.
59. Pawlak C.R., Jacobs R., Mikeska E., Ochsmann S., Lombardi M.S., Kavelaars A., Heijnen C.J., Schmidt R.E., Schedlowski M. Patients with systemic lupus erythematosus differ from healthy controls in their immunological response to acute psychological stress. Brain Behav Immun 1999, 13:287-302.
60. Powell N.D., Bailey M.T., Mays J.W., Stiner-Jones L.M., Hanke M.L., Padgett D.A., Sheridan J.F. Repeated social defeat activates dendritic cells and enhances toll-like receptor dependent cytokine secretion. Brain Behav Immun 2009, 23:225-231.
61. Pradhan A.D., Manson J.E., Rifai N., Buring J.E., Ridker P.M. C-Reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001, 286:327-334.
62. Quan N., Avitsur R., Stark J.L., He L., Lai W., Dhabhar F., Sheridan J.F. Molecular mechanisms of glucocorticoid resistance in splenocytes of socially stressed male mice. J Neuroimmunol 2003, 137:51-58.
63. Raison C.L., Miller A.H. When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am J Psychiatry 2003, 160:1554-1565.
64. Reber S.O., Birkeneder L., Veenema A.H., Obermeier F., Falk W., Straub R.H., Neumann I.D. Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: implications and mechanisms. Endocrinology 2007, 148:670-682.
65. Richlin V.A., Arevalo J.M., Zack J.A., Cole S.W. Stress-induced enhancement of Nf-Kappab DNA-binding in the peripheral blood leukocyte pool: effects of lymphocyte redistribution. Brain Behav Immun 2004, 18:231-237.
66. Ridker P.M., Hennekens C.H., Roitman-Johnson B., Stampfer M.J., Allen J. Plasma concentration of soluble intercellular adhesion molecule 1 and risks of future myocardial infarction in apparently healthy men. Lancet 1998, 351:88-92.
67. Rohleder N., Joksimovic L., Wolf J.M., Kirschbaum C. Hypocortisolism and increased glucocorticoid sensitivity of pro-inflammatory cytokine production in Bosnian war refugees with posttraumatic stress disorder. Biol Psychiatry 2004, 55:745-751.
68. Rohleder N., Marin T.J., Ma R., Miller G.E. Biologic cost of caring for a cancer patient: dysregulation of pro- and anti-inflammatory signaling pathways. J Clin Oncol 2009, 27:2909-2915.
69. Rohleder N., Wolf J.M., Kirschbaum C. Glucocorticoid sensitivity in humans-interindividual differences and acute stress effects. Stress 2003, 6:207-222.
70. Rohleder N., Wolf J.M., Kirschbaum C., Wolf O.T. Effects of cortisol on emotional but not on neutral memory are correlated with peripheral glucocorticoid sensitivity of inflammatory cytokine production. Int J Psychophysiol 2009, 72:74-80.
71. Rohleder N., Wolf J.M., Piel M., Kirschbaum C. Impact of oral contraceptive use on glucocorticoid sensitivity of pro-inflammatory cytokine production, after psychosocial, stress. Psychoneuroendocrinology 2003, 28:261-273.
72. Rohleder N., Wolf J.M., Wolf O.T. Glucocorticoid sensitivity of cognitive and inflammatory processes in depression and posttraumatic stress disorder. Neurosci Biobehav Rev 2010, 35:104-114.
73. Rosas-Ballina M., Goldstein R.S., Gallowitsch-Puerta M., Yang L., Valdes-Ferrer S.I., Patel N.B., Chavan S., Al-Abed Y., Yang H., Tracey K.J. The selective Alpha7 agonist Gts-21 attenuates cytokine production in human whole blood and human monocytes activated by ligands for Tlr2, Tlr3, Tlr4, Tlr9, and rage. Mol Med 2009, 15:195-202.
74. Rosas-Ballina M., Tracey K.J. The neurology of the immune system: neural reflexes regulate immunity. Neuron 2009, 64:28-32.
75. Sanders V.M., Baker R.A., Ramer-Quinn D.S., Kasprowicz D.J., Fuchs B.A., Street N.E. Differential expression of the Beta2-adrenergic receptor by Th1 and Th2 clones: implications for cytokine production and B cell help. J Immunol 1997, 158:4200-4210.
76. Sanders V.M., Munson A.E. Beta adrenoceptor mediation of the enhancing effect of norepinephrine on the murine primary antibody response in vitro. J Pharmacol Exp Ther 1984, 230:183-192.
77. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 2000, 21:55-89.
78. Schmidt D., Reber S.O., Botteron C., Barth T., Peterlik D., Uschold N., Mannel D.N., Lechner A. Chronic psychosocial stress promotes systemic immune activation and the development of inflammatory Th cell responses. Brain Behav Immun 2010, 24:1097-1104.
79. Sheridan J.F., Stark J.L., Avitsur R., Padgett D.A. Social disruption, immunity, and susceptibility to viral infection. Role of glucocorticoid insensitivity and Ngf. Ann N Y Acad Sci 2000, 917:894-905.
80. Smits H.H., Grunberg K., Derijk R.H., Sterk P.J., Hiemstra P.S. Cytokine release and its modulation by dexamethasone in whole blood following exercise. Clin Exp Immunol 1998, 111:463-468.
81. Stark J.L., Avitsur R., Padgett D.A., Campbell K.A., Beck F.M., Sheridan J.F. Social stress induces glucocorticoid resistance in macrophages. Am J Physiol Regul Integr Comp Physiol 2001, 280:R1799-R1805.
82. 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.
83. Sternberg E.M. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat Rev Immunol 2006, 6:318-328.
84. terWolbeek M., van Doornen L.J., Schedlowski M., Janssen O.E., Kavelaars A., Heijnen C.J. Glucocorticoid sensitivity of immune cells in severely fatigued adolescent girls: a longitudinal study. Psychoneuroendocrinology 2008, 33:375-385.
85. Thayer J.F., Yamamoto S.S., Brosschot J.F. The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int J Cardiol 2010, 141:122-131.
86. van den Akker E.L., Koper J.W., van Rossum E.F., Dekker M.J., Russcher H., de Jong F.H., Uitterlinden A.G., Hofman A., Pols H.A., Witteman J.C., Lamberts S.W. Glucocorticoid receptor gene and risk of cardiovascular disease. Arch Intern Med 2008, 168:33-39.
87. Wang X., Wu H., Lakdawala V.S., Hu F., Hanson N.D., Miller A.H. Inhibition of Jun N-terminal kinase (Jnk) enhances glucocorticoid receptor-mediated function in mouse hippocampal Ht22 cells. Neuropsychopharmacology 2005, 30:242-249.
88. Wirtz P.H., Von Kanel R., Frey K., Ehlert U., Fischer J.E. Glucocorticoid sensitivity of circulating monocytes in essential hypertension. Am J Hypertens 2004, 17:489-494.
89. Wirtz P.H., von Kanel R., Schnorpfeil P., Ehlert U., Frey K., Fischer J.E. Reduced glucocorticoid sensitivity of monocyte interleukin-6 production in male industrial employees who are vitally exhausted. Psychosom Med 2003, 65:672-678.
90. Wirtz P.H., Ehlert U., Emini L., Suter T. Higher body mass index (BMI) is associated with reduced glucocorticoid inhibition of inflammatory cytokine production following acute psychosocial stress in men. Psychoneuroendocrinology 2008, 33:1102-1110.
91. Wolf J.M., Rohleder N., Bierhaus A., Nawroth P.P., Kirschbaum C. Determinants of the Nf-Kappab response to acute psychosocial stress in humans. Brain Behav Immun 2009, 23:742-749.
92. Wust S., Federenko I.S., van Rossum E.F., Koper J.W., Kumsta R., Entringer S., Hellhammer D.H. A psychobiological perspective on genetic determinants of hypothalamus-pituitary-adrenal axis activity. Ann N Y Acad Sci 2004, 1032:52-62.