Reciprocal regulation of the neural and innate immune systems (original) (raw)
Matzinger, P. Friendly and dangerous signals: is the tissue in control? Nature Immunol.8, 11–13 (2007). ArticleCAS Google Scholar
Glaser, R. & Kiecolt-Glaser, J. K. Stress-induced immune dysfunction: implications for health. Nature Rev. Immunol.5, 243–251 (2005). ArticleCAS Google Scholar
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). ArticleCAS Google Scholar
McEwen, B. S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev.87, 873–904 (2007). PubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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. USA108, 3080–3085 (2011). ArticleCASPubMedPubMed Central Google Scholar
Cohen, S., Janicki-Deverts, D. & Miller, G. E. Psychological stress and disease. JAMA298, 1685–1687 (2007). ArticleCASPubMed Google Scholar
Amit, I. et al. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science326, 257–263 (2009). CASPubMedPubMed Central Google Scholar
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). ArticleCAS Google Scholar
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. USA1, 1718–1724 (2010). Article Google Scholar
Sapolsky, R., Rivier, C., Yamamoto, G., Plotsky, P. & Vale, W. Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science238, 522–524 (1987). ArticleCASPubMed Google Scholar
Berkenbosch, F., VanOers, J., DelRey, A., Tilders, F. & Besedovsky, H. Corticotropin-releasing factor-producing neurons in the rat activated by interleukin-1. Science238, 524–526 (1987). ArticleCASPubMed Google Scholar
Besedovsky, H., del Rey, A., Sorkin, E. & Dinarello, C. A. Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science233, 652–654 (1986). ArticleCASPubMed Google Scholar
Rhen, T. & Cidlowski, J. A. Antiinflammatory action of glucocorticoids — new mechanisms for old drugs. N. Engl. J. Med.353, 1711–1723 (2005). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Cole, S. et al. Computational identification of gene–social environment interaction at the human IL6 locus. Proc. Natl Acad. Sci. USA107, 5681–5686 (2010). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
Nance, D. M. & Sanders, V. M. Autonomic innervation and regulation of the immune system (1987–2007). Brain Behav. Immun.21, 736–745 (2007). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Panina-Bordignon, P. et al. β2-agonists prevent Th1 development by selective inhibition of interleukin 12. J. Clin. Invest.100, 1513–1519 (1997). ArticleCASPubMedPubMed Central Google Scholar
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). CASPubMed Google Scholar
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). ArticlePubMed Google Scholar
Cole, S. W. et al. Social regulation of gene expression in human leukocytes. Genome Biol.8, 1–13 (2007). Article Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Kiecolt-Glaser, J. K. et al. Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc. Natl Acad. Sci. USA100, 9090–9095 (2003). ArticleCASPubMedPubMed Central Google Scholar
Miller, G. E. et al. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-κB signaling. Biol. Psychiatry64, 266–272 (2008). ArticleCASPubMedPubMed Central Google Scholar
Pace, T. W. et al. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am. J. Psychiatry163, 1630–1633 (2006). ArticlePubMed Google Scholar
Bierhaus, A. et al. A mechanism converting psychosocial stress into mononuclear cell activation. Proc. Natl Acad. Sci. USA100, 1920–1925 (2003). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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. USA106, 14716–14721 (2009). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Chen, E. et al. Genome-wide transcriptional profiling linked to social class in asthma. Thorax64, 38–43 (2009). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Motivala, S. & Irwin, M. R. Sleep and immunity: cytokine pathways linking sleep and health outcomes. Curr. Dir. Psychol. Sci.16, 21–25 (2007). Article Google Scholar
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). ArticleCASPubMed Google Scholar
Irwin, M. R., Carrillo, C. & Olmstead, R. Sleep loss activates cellular markers of inflammation: sex differences. Brain Behav. Immun.24, 54–57 (2010). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Watkins, L. R. & Maier, S. F. Implications of immune-to-brain communication for sickness and pain. Proc. Natl Acad. Sci. USA96, 7710–7713 (1999). ArticleCASPubMedPubMed Central Google Scholar
Miller, A. H., Maletic, V. & Raison, C. L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry65, 732–741 (2009). ArticleCASPubMedPubMed Central Google Scholar
Hart, B. L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev.12, 123–137 (1988). ArticleCASPubMed Google Scholar
Harrison, N. A. et al. Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biol. Psychiatry66, 407–414 (2009). ArticlePubMedPubMed Central Google Scholar
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. Neuroimage47, 881–890 (2009). ArticleCASPubMed Google Scholar
Eisenberger, N. I. et al. Inflammation-induced anhedonia: endotoxin reduces ventral striatum responses to reward. Biol. Psychiatry68, 748–754 (2010). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Capuron, L. et al. Neurobehavioral effects of interferon-α in cancer patients: phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology26, 643–652 (2002). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Tyring, S. et al. Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet367, 29–35 (2006). ArticleCASPubMed Google Scholar
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. Psychiatry13, 800–812 (2008). ArticleCASPubMedPubMed Central Google Scholar
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. Psychiatry26, 1167–1170 (2002). ArticleCASPubMed Google Scholar
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. Psychiatry67, 1211–1224 (2010). ArticleCASPubMedPubMed Central Google Scholar
Imeri, L. & Opp, M. R. How (and why) the immune system makes us sleep. Nature Rev. Neurosci.10, 199–210 (2009). ArticleCAS Google Scholar
Mullington, J. et al. Dose-dependent effects of endotoxin on human sleep. Am. J. Physiol. Regul. Integr. Comp. Physiol.278, R947–R955 (2000). ArticleCASPubMed Google Scholar
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. Psychiatry68, 942–949 (2010). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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. Psychiatry66, 191–195 (2009). ArticleCASPubMedPubMed Central Google Scholar
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). ArticlePubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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. Psychiatry66, 871–878 (2009). ArticleCASPubMedPubMed Central Google Scholar
Heesen, C. et al. Fatigue in multiple sclerosis: an example of cytokine mediated sickness behaviour? J. Neurol. Neurosurg. Psychiatry77, 34–39 (2006). ArticleCASPubMedPubMed Central Google Scholar
Harboe, E. et al. Fatigue in primary Sjogren's syndrome — a link to sickness behaviour in animals? Brain Behav. Immun.23, 1104–1108 (2009). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Bower, J. E. et al. Inflammatory biomarkers and fatigue during radiation therapy for breast and prostate cancer. Clin. Cancer Res.15, 5534–5540 (2009). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
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). ArticlePubMed Google Scholar
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). ArticlePubMedPubMed Central Google Scholar
Pace, T. W. et al. Effect of compassion meditation on neuroendocrine, innate immune and behavioral responses to psychosocial stress. Psychoneuroendocrinology34, 87–98 (2009). ArticleCASPubMed Google Scholar
Irwin, M. R. & Olmstead, R. Mitigating cellular inflammation in older adults. Am. J. Geriatr. Psychiatry (in the press).
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). ArticlePubMedPubMed Central Google Scholar
Sloan, E. K. et al. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res.70, 7042–7052 (2010). ArticleCASPubMedPubMed Central Google Scholar
Idaghdour, Y. et al. Geographical genomics of human leukocyte gene expression variation in southern Morocco. Nature Genet.42, 62–67 (2010). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Cole, S. W. in Complex Systems Science in Biomedicine (eds Deisboeck, T. S. & Kresh, J. Y.) 605–629 (Springer, New York, 2006). Book Google Scholar