Reciprocal regulation of the neural and innate immune systems

Nature Reviews Immunology

Volumn 11, Issue 9, 2011, Pages 625-632

  Irwin, Michael R ^a   Cole, Steven W ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENERGIC SYSTEM; CENTRAL NERVOUS SYSTEM; FATIGUE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE RESPONSE; INNATE IMMUNITY; LEUKOCYTE; MOLECULAR PATHOLOGY; NERVE CELL; NONHUMAN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PRIORITY JOURNAL; REVIEW;

CENTRAL NERVOUS SYSTEM; CYTOKINES; ENDOCRINE SYSTEM; GENES, MHC CLASS II; HUMANS; IMMUNITY, INNATE; INFLAMMATION; LEUKOCYTES; NEUROIMMUNOMODULATION; SIGNAL TRANSDUCTION;

EID: 80052091705     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3042     Document Type: Review

References (81)

1. Matzinger, P. Friendly and dangerous signals: is the tissue in control? Nature Immunol. 8, 11-13 (2007). (Pubitemid 46242350)
2. Glaser, R. & Kiecolt-Glaser, J. K. Stress-induced immune dysfunction: implications for health. Nature Rev. Immunol. 5, 243-251 (2005). (Pubitemid 40364825)
3. 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. Nature Rev. Neurosci. 9, 46-56 (2008). (Pubitemid 350295688)
4. McEwen, B. S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873-904 (2007). (Pubitemid 47086281)
5. Powell, N. D., Mays, J. W., Bailey, M. T., Hanke, M. L. & Sheridan, J. F. Immunogenic dendritic cells primed by social defeat enhance adaptive immunity to influenza A virus. Brain Behav. Immun. 25, 46-52 (2011).
6. Cole, S. W., Hawkley, L. C., Arevalo, J. M. & Cacioppo, J. T. Transcript origin analysis identifies antigen-presenting cells as primary targets of socially regulated gene expression in leukocytes. Proc. Natl Acad. Sci. USA 108, 3080-3085 (2011).
7. Cohen, S., Janicki-Deverts, D. & Miller, G. E. Psychological stress and disease. JAMA 298, 1685-1687 (2007). (Pubitemid 47606658)
8. Amit, I. et al. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 326, 257-263 (2009).
9. Decker, T., Muller, M. & Stockinger, S. The yin and yang of type I interferon activity in bacterial infection. Nature Rev. Immunol. 5, 675-687 (2005). (Pubitemid 43086170)
10. Finch, C. E. Evolution in health and medicine Sackler colloquium. Evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. Proc. Natl Acad. Sci. USA 1, 1718-1724 (2010).
11. Sapolsky, R., Rivier, C., Yamamoto, G., Plotsky, P. & Vale, W. Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science 238, 522-524 (1987). (Pubitemid 17147036)
12. Berkenbosch, F., VanOers, J., DelRey, A., Tilders, F. & Besedovsky, H. Corticotropin-releasing factor-producing neurons in the rat activated by interleukin-1. Science 238, 524-526 (1987).
13. Besedovsky, H., del Rey, A., Sorkin, E. & Dinarello, C. A. Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science 233, 652-654 (1986). (Pubitemid 16011614)
14. Rhen, T. & Cidlowski, J. A. Antiinflammatory action of glucocorticoids-new mechanisms for old drugs. N. Engl. J. Med. 353, 1711-1723 (2005).
15. 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. 21, 9-19 (2007). (Pubitemid 44872932)
16. Cole, S. et al. Computational identification of gene-social environment interaction at the human IL6 locus. Proc. Natl Acad. Sci. USA 107, 5681-5686 (2010).
17. Collado-Hidalgo, A., Sung, C. & Cole, S. Adrenergic inhibition of innate anti-viral response: PKA blockade of type I interferon gene transcription mediates catecholamine support for HIV-1 replication. Brain Behav. Immun. 20, 552-563 (2006). (Pubitemid 44528951)
18. Nance, D. M. & Sanders, V. M. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav. Immun. 21, 736-745 (2007). (Pubitemid 47002215)
19. Lee, H. J. et al. GATA-3 induces T helper cell type 2 (Th2) cytokine expression and chromatin remodeling in committed Th1 cells. J. Exp. Med. 192, 105-115 (2000). (Pubitemid 30470811)
20. Panina-Bordignon, P. et al. β2-agonists prevent Th1 development by selective inhibition of interleukin 12. J. Clin. Invest. 100, 1513-1519 (1997). (Pubitemid 27425778)
21. Cole, S. W., Korin, Y. D., Fahey, J. L. & Zack, J. A. Norepinephrine accelerates HIV replication via protein kinase A-dependent effect on cytokine production. J. Immunol. 161, 610-616 (1998). (Pubitemid 28323521)
22. Grebe, K. M. et al. Cutting edge: sympathetic nervous system increases proinflammatory cytokines and exacerbates influenza A virus pathogenesis. J. Immunol. 184, 540-544 (2009).
23. Cole, S. W. et al. Social regulation of gene expression in human leukocytes. Genome Biol. 8, 1-13 (2007).
24. Sloan, E. K. et al. Social stress enhances sympathetic innervation of primate lymph nodes: mechanisms and implications for viral pathogenesis. J. Neurosci. 27, 8857-8865 (2007). (Pubitemid 47292761)
25. Kiecolt-Glaser, J. K. et al. Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc. Natl Acad. Sci. USA 100, 9090-9095 (2003). (Pubitemid 36899228)
26. Miller, G. E. et al. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-κB signaling. Biol. Psychiatry 64, 266-272 (2008).
27. Pace, T. W. et al. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am. J. Psychiatry 163, 1630-1633 (2006). (Pubitemid 44465765)
28. Bierhaus, A. et al. A mechanism converting psychosocial stress into mononuclear cell activation. Proc. Natl Acad. Sci. USA 100, 1920-1925 (2003). (Pubitemid 36254549)
29. Goebel, M. U., Mills, P. J., Irwin, M. R. & Ziegler, M. G. Interleukin-6 and tumor necrosis factor-α production after acute psychological stress, exercise, and infused isoproterenol: differential effects and pathways. Psychosom. Med. 62, 591-598 (2000). (Pubitemid 30604804)
30. Bower, J. E. et al. Inflammatory responses to psychological stress in fatigued breast cancer survivors: relationship to glucocorticoids. Brain Behav. Immun. 21, 251-258 (2007). (Pubitemid 46199108)
31. Richlin, V. A., Arevalo, J. M., Zack, J. A. & Cole, S. W. Stress-induced enhancement of NF-κB DNA-binding in the peripheral blood leukocyte pool: effects of lymphocyte redistribution. Brain Behav. Immun. 18, 231-237 (2004). (Pubitemid 38429764)
32. Miller, G. E. et al. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc. Natl Acad. Sci. USA 106, 14716-14721 (2009).
33. Engler, H., Bailey, M. T., Engler, A. & Sheridan, J. F. Effects of repeated social stress on leukocyte distribution in bone marrow, peripheral blood and spleen. J. Neuroimmunol. 148, 106-115 (2004). (Pubitemid 38229563)
34. Wohleb, E. S. et al. β-adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31, 6277-6288 (2011).
35. Chen, E. et al. Genome-wide transcriptional profiling linked to social class in asthma. Thorax 64, 38-43 (2009).
36. Irwin, M. R., Wang, M., Campomayor, C. O., Collado-Hidalgo, A. & Cole, S. Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch. Intern. Med. 166, 1756-1762 (2006). (Pubitemid 44414465)
37. Irwin, M. R. et al. Sleep loss activates cellular inflammatory signaling. Biol. Psychiatry 64, 538-540 (2008).
38. Motivala, S. & Irwin, M. R. Sleep and immunity: cytokine pathways linking sleep and health outcomes. Curr. Dir. Psychol. Sci. 16, 21-25 (2007).
39. Meier-Ewert, H. K. et al. Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. J. Am. Coll. Cardiol. 43, 678-683 (2004). (Pubitemid 38229544)
40. Irwin, M. R., Carrillo, C. & Olmstead, R. Sleep loss activates cellular markers of inflammation: sex differences. Brain Behav. Immun. 24, 54-57 (2010).
41. O'Connor, M. F., Motivala, S. J., Valladares, E. M., Olmstead, R. & Irwin, M. R. Sex differences in monocyte expression of IL-6: role of autonomic mechanisms. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R145-R151 (2007). (Pubitemid 47096572)
42. Watkins, L. R. & Maier, S. F. Implications of immune-to-brain communication for sickness and pain. Proc. Natl Acad. Sci. USA 96, 7710-7713 (1999). (Pubitemid 29328345)
43. Miller, A. H., Maletic, V. & Raison, C. L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 65, 732-741 (2009).
44. Hart, B. L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12, 123-137 (1988). (Pubitemid 19268745)
45. Harrison, N. A. et al. Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biol. Psychiatry 66, 407-414 (2009).
46. Eisenberger, N. I., Inagaki, T. K., Rameson, L. T., Mashal, N. M. & Irwin, M. R. An fMRI study of cytokine-induced depressed mood and social pain: the role of sex differences. Neuroimage 47, 881-890 (2009).
47. Eisenberger, N. I. et al. Inflammation-induced anhedonia: endotoxin reduces ventral striatum responses to reward. Biol. Psychiatry 68, 748-754 (2010).
48. Gimeno, D. et al. Associations of C-reactive protein and interleukin-6 with cognitive symptoms of depression: 12-year follow-up of the Whitehall II study. Psychol. Med. 39, 413-423 (2009).
49. Miller, A. H., Ancoli-Israel, S., Bower, J. E., Capuron, L. & Irwin, M. R. Neuroendocrine-immune mechanisms of behavioral comorbidities in patients with cancer. J. Clin. Oncol. 26, 971-982 (2008). (Pubitemid 351409339)
50. Capuron, L. et al. Neurobehavioral effects of interferon-α in cancer patients: phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology 26, 643-652 (2002). (Pubitemid 34260983)
51. Capuron, L., Ravaud, A. & Dantzer, R. Early depressive symptoms in cancer patients receiving interleukin 2 and/or interferon α-2b therapy. J. Clin. Oncol. 18, 2143-2151 (2000). (Pubitemid 30324368)
52. Tyring, S. et al. Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet 367, 29-35 (2006). (Pubitemid 43038667)
53. Wong, M. L., Dong, C., Maestre-Mesa, J. & Licinio, J. Polymorphisms in inflammation-related genes are associated with susceptibility to major depression and antidepressant response. Mol. Psychiatry 13, 800-812 (2008).
54. Benedetti, F., Lucca, A., Brambilla, F., Colombo, C. & Smeraldi, E. Interleukin-6 serum levels correlate with response to antidepressant sleep deprivation and sleep phase advance. Prog. Neuropsychopharmacol. Biol. Psychiatry 26, 1167-1170 (2002). (Pubitemid 35256111)
55. Raison, C. L., Lowry, C. A. & Rook, G. A. Inflammation, sanitation, and consternation: loss of contact with coevolved, tolerogenic microorganisms and the pathophysiology and treatment of major depression. Arch. Gen. Psychiatry 67, 1211-1224 (2010).
56. Imeri, L. & Opp, M. R. How (and why) the immune system makes us sleep. Nature Rev. Neurosci. 10, 199-210 (2009).
57. Mullington, J. et al. Dose-dependent effects of endotoxin on human sleep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R947-R955 (2000). (Pubitemid 30215208)
58. Raison, C. L. et al. Chronic interferon-α administration disrupts sleep continuity and depth in patients with hepatitis C: association with fatigue, motor slowing, and increased evening cortisol. Biol. Psychiatry 68, 942-949 (2010).
59. Vgontzas, A. N. et al. Marked decrease in sleepiness in patients with sleep apnea by etanercept, a tumor necrosis factor-α antagonist. J. Clin. Endocrinol. Metab. 89, 4409-4413 (2004). (Pubitemid 39244447)
60. Monk, J. P. et al. Assessment of tumor necrosis factor α blockade as an intervention to improve tolerability of dose-intensive chemotherapy in cancer patients. J. Clin. Oncol. 24, 1852-1859 (2006). (Pubitemid 46638983)
61. Irwin, M. R., Olmstead, R., Valladares, E. M., Breen, E. C. & Ehlers, C. L. Tumor necrosis factor antagonism normalizes rapid eye movement sleep in alcohol dependence. Biol. Psychiatry 66, 191-195 (2009).
62. Dew, M. A. et al. Healthy older adults' sleep predicts all-cause mortality at 4 to 19 years of follow-up. Psychosom. Med. 65, 63-73 (2003). (Pubitemid 36143197)
63. Thomas, K. S., Motivala, S., Olmstead, R. & Irwin, M. R. Sleep depth and fatigue: role of cellular inflammatory activation. Brain Behav. Immun. 25, 53-58 (2011).
64. Cho, H. J., Seeman, T. E., Bower, J. E., Kiefe, C. I. & Irwin, M. R. Prospective association between C-reactive protein and fatigue in the coronary artery risk development in young adults study. Biol. Psychiatry 66, 871-878 (2009).
65. Heesen, C. et al. Fatigue in multiple sclerosis: an example of cytokine mediated sickness behaviour? J. Neurol. Neurosurg. Psychiatry 77, 34-39 (2006). (Pubitemid 43022687)
66. Harboe, E. et al. Fatigue in primary Sjogren's syndrome-a link to sickness behaviour in animals? Brain Behav. Immun. 23, 1104-1108 (2009).
67. Davis, M. C. et al. Chronic stress and regulation of cellular markers of inflammation in rheumatoid arthritis: implications for fatigue. Brain Behav. Immun. 22, 24-32 (2008). (Pubitemid 350216361)
68. Schubert, C., Hong, S., Natarajan, L., Mills, P. J. & Dimsdale, J. E. The association between fatigue and inflammatory marker levels in cancer patients: a quantitative review. Brain Behav. Immun. 21, 413-427 (2007). (Pubitemid 46528677)
69. Bower, J. E. et al. Inflammatory biomarkers and fatigue during radiation therapy for breast and prostate cancer. Clin. Cancer Res. 15, 5534-5540 (2009).
70. Collado-Hidalgo, A., Bower, J. E., Ganz, P. A., Cole, S. W. & Irwin, M. R. Inflammatory biomarkers for persistent fatigue in breast cancer survivors. Clin. Cancer Res. 12, 2759-2766 (2006).
71. Bower, J. E., Ganz, P. A., Irwin, M. R., Arevalo, J. M. & Cole, S. W. Fatigue and gene expression in human leukocytes: increased NF-κB and decreased glucocorticoid signaling in breast cancer survivors with persistent fatigue. Brain Behav. Immun. 25, 147-150 (2011).
72. Collado-Hidalgo, A., Bower, J. E., Ganz, P. A., Irwin, M. R. & Cole, S. W. Cytokine gene polymorphisms and fatigue in breast cancer survivors: early findings. Brain Behav. Immun. 22, 1197-1200 (2008).
73. Zautra, A. J. et al. Comparison of cognitive behavioral and mindfulness meditation interventions on adaptation to rheumatoid arthritis for patients with and without history of recurrent depression. J. Consult. Clin. Psychol. 76, 408-421 (2008). (Pubitemid 351822341)
74. Nicklas, B. J. et al. Exercise training and plasma C-reactive protein and interleukin-6 in elderly people. J. Am. Geriatr. Soc. 56, 2045-2052 (2008).
75. Pace, T. W. et al. Effect of compassion meditation on neuroendocrine, innate immune and behavioral responses to psychosocial stress. Psychoneuroendocrinology 34, 87-98 (2009).
76. Irwin, M. R. & Olmstead, R. Mitigating cellular inflammation in older adults. Am. J. Geriatr. Psychiatry (in the press).
77. Lavretsky, H. et al. Complementary use of Tai Chi Chih augments escitalopram treatment of geriatric depression: a randomized controlled trial. Am. J. Geriatr. Psychiatry 6 Mar 2011 (doi:10.1097/JGP.0b013e31820ee9ef).
78. Sloan, E. K. et al. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res. 70, 7042-7052 (2010).
79. Idaghdour, Y. et al. Geographical genomics of human leukocyte gene expression variation in southern Morocco. Nature Genet. 42, 62-67 (2010).
80. Ericsson, A., Kovacs, K. J. & Sawchenko, P. E. A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J. Neurosci. 14, 897-913 (1994). (Pubitemid 24043940)
81. Cole, S. W. in Complex Systems Science in Biomedicine (eds Deisboeck, T. S. & Kresh, J. Y.) 605-629 (Springer, New York, 2006).