Circadian rhythm and the immune response: A review

International Reviews of Immunology

Volumn 28, Issue 1-2, 2009, Pages 93-108

  Habbal, O A ^a   Al Jabri, A A ^a  

^a SULTAN QABOOS UNIVERSITY   (Oman)

Author keywords

Circadian rhythm; Immune response; Immunity; Neuroendocrine

Indexed keywords

CYCLIC AMP; GROWTH HORMONE; HYDROCORTISONE; MELATONIN; NALTREXONE; PROLACTIN; TESTOSTERONE; TUMOR NECROSIS FACTOR ALPHA;

AUTOIMMUNITY; BIOLOGICAL RHYTHM; BRAIN FUNCTION; CIRCADIAN RHYTHM; DRUG MECHANISM; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOMODULATION; IMMUNOREGULATION; NARCOLEPSY; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SLEEP DEPRIVATION; SLEEP PATTERN; SLEEP TIME; SLEEP WAKING CYCLE; WAKEFULNESS;

ANIMALS; CIRCADIAN RHYTHM; CYTOKINES; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; LIGHT; MELATONIN; NEUROPEPTIDES; NEUROSECRETORY SYSTEMS;

EID: 60849096964     PISSN: 08830185     EISSN: 15635244     Source Type: Journal    
DOI: 10.1080/08830180802645050     Document Type: Review

References (70)

1. K. Shih, J. Jamison, A. Conforto, and S. Swadron, Effects of disrupted circadian rhythm on decision-making in emergency medicine residents. Ann Emerg Med 48: 31-32, 2006.
2. J.A. Horne and L.A. Reyner, Driver sleepiness: Comparisons of practical countermeasures - caffeine and nap. Psychophysiology 33: 306-309, 1996.
3. I. Tizard I, Sickness behavior, its mechanisms and significance. Animal Health Res Rev 9: 87-99, 2008.
4. M.F. Bear, B.W. Connors, and M.A. Paradiso, Gene expression during sleeping and waking. In: Neuroscience, Exploring the Brain, 2nd edition, Chapter 19, Rhythms of the Brain (S. Katz, Ed., pp. 606-631). Baltimore, MD: Lippincott Williams & Wilkins, 2007.
5. C. Cirelli and G. Tonini, Differences in gene expression between sleep and waking as revealed by mRNA differential display. Mol Brain Res 56: 293-305, 1998.
6. F.S. Ruiz, M.L. Andersen, A. Zager, R.C.S. Martins, and S. Tufik, Sleep deprivation reduces the lymphocyte count in a non-obese mouse model of type 1 diabetes mellitus. Braz J Med Biol Res 40: 633-637, 2007.
7. C.A. Everson and W.R. Crowley, Reductions in circulating anabolic hormones induced by sustained sleep deprivation in rats. Am J Physiol Endocrinol Metab 286: 1060-1070, 2004.
8. M.C. Moore-Ede, Physiology of the circadian timing system: Predictive versus reactive homeostasis. AJP - Reg Integr Comp Physiol 250: 737-752, 1986.
9. B. Collins and J. Blau, Keeping time without a clock. Neuron 50: 348-350, 2006.
10. D.P. Cardinali, A.I. Esquifino, J.M. Maestroni, and S.R. Pandi-Perumal, Circadian organisation of the immune response. Lessons from the adjuvant arthritis model. In: Neuroimmunology of Sleep (S.R. Pandi-Perumal, D.P. Cardinali, and G. Chrousos, Eds., pp. 59-86). New York: Springer-Verlag, 2007.
11. C.B. Saper, T.E. Scammell, and J. Lu, Hypothalamic regulation of sleep and circadian rhythm. Nature 437: 1257-1263, 2005.
12. T. Mochizuki, A. Crocker, S. McCormack, M. Yanagisawa, T. Sakurai, and T.E. Scammell, Behavioral state instability in orexin knock-out mice. J Neurosci 24: 6291-6300, 2004.
13. C.B. Saper, J. Lu, T.C. Chou, and J. Gooley, The hypothalamic integrator for circadian rhythms. Trends Neurosci 28: 152-157, 2005.
14. K.N. Paul, F.W. Turek, and M.H. Kryger, Influence of sex on sleep regulatory mechanisms. J Women's Health 17: 1201-1208, 2008.
15. C.A. Czeisler, J.F. Duffy, T.L. Shanahan, E.N. Brown, J.F. Mitchell, D.W. Rimmer, J.M. Ronda, E.J. Silva, J.S. Allan, D. Dijk, and R.E. Kronauer RE, Stability, precision, and near-24-hour period of the human circadian pacemaker. Science 284: 2177-2181, 1999.
16. D.J. Earnest and C.D. Sladek, Circadian vasopressin release from perfused rat suprachiasmatic explants in vitro: Effects of acute stimulation. Brain Res 422: 398-402, 1987.
17. F.W. Turek Are the suprachiasmatic nuclei the location of the biological clock in mammals? Nature 292: 289-290, 1981.
18. M.R. Ralph, R.G. Foster, F.C. Davies, and M. Menaker, Transplanted suprachiasmatic nucleus determines circadian period. Science 247: 975-978, 1990.
19. D.M. Edgar, W.C. Dement, and C.A. Fuller, Effect of SCN lesions on sleep in squirrel monkeys: Evidence for opponent processes in sleep-wake regulation. J Neurosci 13: 1065-1079, 1993.
20. D.J. Kennaway, Light, neurotransmitters, and the suprachiasmatic nucleus control of pineal melatonin production in the rat. Neurosignals 6: 247-254, 1997.
21. M.E. Jewett, D.W. Rimmer, J.F. Duffy, E.B. Klerman, R.E. Kronauer, and C.A. Czeisler, Human circadian pacemaker is sensitive to light throughout subjective day without evidence of transients. Am J Physiol Regul Integr Comp Physiol 273: 1800-1809, 1997.
22. C.A. Czeisler, The Effect of Light on the Human Circadian Pacemaker. Circadian Clocks and their Adjustment. Ciba Found Symp 183: 254-302, 2007.
23. M. von Schantz, I. Provencio, and R.G. Foster RG, Recent developments in circadian photoreception: More than meets the eye. Invest Ophthalmol Vis Sci 41: 1605-1607, 2000.
24. C.A. Czeisler, T.L. Shanahan, E.B. Klerman, H. Martens, D.J. Brotman, J.S. Emens, T. Klein, and J.F. Rizzo 3rd, Suppression of melatonin secretion in some blind patients by exposure to bright light. N Engl J Med 332: 54-55, 1995.
25. K.J. Reid, A.M. Chang, and P.C. Zee, Circadian rhythm sleep disorders. Med Clin N Am 88: 631-651, 2004.
26. D.J. Dijk and D.M. Edgar, Circadian and homeostatic control of wakefulness and sleep. In: Regulation of Sleep and Circadian Rhythms (F.W. Turek and P.C. Zee, Eds., pp. 111-147). New York: Marcel Dekker, 1999.
27. H. Danker-Hopfe, S. Kraemer, H. Dorn, A. Schmidt, I. Ehlert, and W.M. Herrmann, Time-of-day variations in different measures of sleepiness (MSLT, pupillography, and SSS) and their interrelations. Psychophysiology 38: 828-835, 2001.
28. D.J. Dijk, D.P. Brunner, D.G.M. Beersma, and A.A. Borbély, Electroencephalogram power density and slow wave sleep as a function of prior waking and circadian phase. Sleep 13: 430-440, 1990.
29. O. Habbal, G. Leeming, and J.M. McLean, Cellular proliferation in the lymphoid tissues of an inbred (RT1a) rat strain during the oestrous cycle. Acta Anatomica Basel 131: 156-160, 1988.
30. O. Habbal and J.M. McLean, An increase in thymocyte proliferation during pseudopregnancy in two inbred strains of rat. Acta Anatomica Basel 144: 296-303, 1992.
31. O. Habbal and J.M. McLean, The immune response to coitus and conception. Rev. Article. Saudi Med J 13: 178-186, 1993.
32. O.A. Habbal and J.M. McLean, Pre-implantation immune-suppression in the pregnant rat: A possible role of seminal plasma. SQU J Med Sci 1: 10-15, 1999.
33. O. Habbal and J.M. McLean, Lymphoid tissue changes during early syngeneic pregnancy in the RT1u rat. Acta Anatomica Basel 144: 363-370, 1992.
34. O.A. Habbal and M.F. Abu-Hijleh, Aging and the immune response. J Bah Med Soc 7: 124-133, 1995.
35. O.A. Habbal and M.F. Abu-Hijleh, The effect of stress on the immune system. Emir Med J 13: 91-99, 1995.
36. N. Petrovsky, Towards a unified model of neuroendocrine-immune interaction. Immunol Cell Biol 79: 350-357, 2001.
37. P. Entzian, K. Linnemann, M. Schlaak, and P. Zabel, Obstructive sleep apnea syndrome and circadian rhythms of hormones and cytokines. Am J Respir Crit Care Med 153: 1080-1086, 1996.
38. G. Cavadini, S. Perzilka, P. Kohler, C. Jud, I. Tobler, T. Birchler, and A. Fontana, TNF-α suppresses the expression of clock genes by interfering with E-box-medicated transcription. Proc Natl Acad Sci USA (PANAS) 104: 12843-12848, 2007.
39. D.A. Padgett and R. Glaser, How stress influences the immune response. Trends Immunol 24: 444-448, 2003.
40. D. Lorton, C. Lubahn, C. Estus, B.A. Millar, J.L. Carter, C.A. Wood, and D.L. Bellinger, Bidirectional Communication between the brain and the immune system: Implications for physiological sleep and disorders with disrupted sleep. NeuroimmunoModulation 13: 5-6, 2006.
41. E. Späth-Schwalbe, K. Hansen, F. Schmidt, H. Schrezenmeier, L. Marshall, K. Burger, H.L. Fehm, and J. Born, Acute effects of recombinant human interleukin-6 on endocrine and central nervous sleep functions in healthy men. J Endocrinol Metab 83: 1573-1579, 1998.
42. A. Bryant, J. Trinder, and N. Curtis, Sick and tired: Does sleep have a vital role in the immune system? The relationship between brain and peripheral cytokines. Nat Rev Immunol 4: 457-467, 2004.
43. J. Born, D. Uthgenannt, C. Dodt, D. Nünninghoff, E. Ringvolt, T. Wagner, and H.L. Fehm, Cytokines production and lymphocyte subpopulations in aged humans. An assessment during nocturnal sleep. Mech Ageing Dev 84: 113-126, 1995.
44. T. Lange, L. Marshall, E. Späth-Schwalbe, H.L. Fehm, and J. Born, Systemic immune parameters and sleep after ultra-low dose administration of IL-2 in healthy men. Brain Behav Immunol 16: 663-674, 2002.
45. A.M. Drewes, Pain and sleep disturbances with special reference to fibromyalgia and rheumatoid arthritis. Rheumatology 38: 1035-1044, 1999.
46. R. Baschetti, A.C. Chester, N.F. Devitt, A.L. Komaroff, Chronic fatigue syndrome. J Am Med Asso (JAMA) 279: 431-433, 1998.
47. M. Cutolo, R.H. Straub, and F. Buttgereit, Circadian rhythms of nocturnal hormones in rheumatoid arthritis: translation from bench to bedside. Ann Rheum Dis 67: 905-908, 2008.
48. R.J. Martin, L.C. Cicutto, H.R. Smith, R.D. Ballard, and S.J. Szelfer, Airways inflammation in nocturnal asthma. Am Rev Respir Dis 143: 531-537, 1991.
49. I.C. Chikanza, P. Petrou, G. Kingsley, G. Chrousus, and G.S. Panayi, Defective hypothalamic response to immune and inflammatory stimuli in patients with rheumatoid arthritis. Arthritis Rheum 35: 1281-1288, 1992.
50. M. Fujitaka, S. Nomuraa, N. Sakuraa, K. Uedaa, R. Matuurab, and C. Yumibac, Morning and afternoon serum levels of cortisone and cortisol in asthmatic patients. Clinica Chimica Acta 299: 101-108, 2000.
51. M.A. Carskadon, Patterns of sleep and sleepiness in adolescents. Pediatrician 17: 5-12, 1990.
52. J. Nakayama, M. Miura, M. Honda, T. Miki, Y. Honda, and T. Arinami, Linkage of human narcolepsy with HLA association to chromosome 4p13-q21. Genomics 65: 84-86, 2000.
53. R. Hayduk, P. Flodman, M.A. Spence, M.K. Erman, and M.M. Mitler, Monozygotic twins with narcolepsy: Preliminary report. Sleep Res 25: 252, 1996.
54. Y. Honda, A monozygotic twin pair completely discordant for narcolepsy, with sleep deprivation as a possible precipitating factor. Sleep Biolog Rhythms 1: 147-149, 2003.
55. J.M. Guerrero and R.J. Reiter (Eds.), Melatonin-immune system relationships. Curr Topics Medicin Chem 2: 167-179, 2002.
56. J.E. Jan and R.D. Freeman, Melatonin therapy for circadian rhythm sleep disorders in children with multiple disabilities: What have we learned in the last decade? Dev Med Child Neurol 46: 776-782, 2004.
57. Y. Ishida, C. Yokoyama, T. Inatomi, K. Yagita, X. Dong, L. Yan, S. Yamaguchi, I. Nagatsu, T. Komori, K. Kitahama, and H. Okamura, Circadian rhythm of aromatic L-amino acid decarboxylase in the rat suprachiasmatic nucleus: Gene expression and decarboxylating activity in clock oscillating cells. Gene Cells 7: 447-459, 2002.
58. K. Swarko-Solta, M.-J. Thaela, M. Midura, B. Lech, B. Gluchowska, N. Drela, E. Kozlowska, and R. Kowalczka, Exogenous melatonin modifies the circadian rhythm but does not increase the level of some immune parameters in the chicken. J Pineal Res 12: 27-34, 1992.
59. D.P. Cardinali, L. Brusco, R.A. Cutrera, P. Castrillón, and A. Esquifino, Melatonin as time-meaningful signal in circadian organisation of immune response. Biolog Signals Recept 8: 41-48, 1999.
60. J.E. Roberts, Visible light induced changes in the immune response through an eye-brain mechanism (phtoneuroimmunology). J Photochem. Photobiol 29: 3-15, 1995.
61. J.E. Roberts, Light and Immunomodulation. Ann NY Acad Sci 971: 435-445, 2000.
62. V.D. Deshmukh, Retino-hypothalamic-pineal hypothesis in the pathophysiology of primary headaches. Med Hypoth 66: 1146-1151, 2006.
63. C. Taylor, D. Aswana, D. Fricker, A.D. Lakshmi, and I. Gomes, Mechanisms of action of antidepressants: From neurotransmitter systems to signalling pathways. Cell Signal 17: 549-557, 2005.
64. M.C. Antle, J. LeSauter, and R. Silver, Neurogenesis and ontogeny of specific cell phenotypes within the hamster suprachiasmatic nucleus. Brain Res Dev Brain Res 157: 8-18, 2005.
65. T.H. Monk, D.J. Buysse, C.F. Reynolds III, S.L. Berga, D.B. Jarrett, A.E. Begley, and D.J. Kupfer, Circadian rhythms in human performance and mood under constant conditions. J Sleep Res 6: 9-18, 1997.
66. C.G. Burkhart, Light role in immunomodulation and medical therapy. J Am Acad Dermatol 53: 1099-1100, 2005.
67. S. Guhl, R. Stefaniak, M. Strathmann, M. Babina, H. Piazena, B.M. Henz, and T. Zuberbier, Bivalent effect of UV light on human skin mast cells-low-level mediator release at baseline but potent suppression upon mast cell triggering. J Invest Dermatol 124: 453-456, 2005.
68. F. Levi, C. Canon, M. Dipalma, I. Florentin, and J.L. Misset, When should the immune clock be reset? From circadian pharmacodynamics to temporally optimized drug delivery. Ann NY Acad Sci 1618: 312-329, 1991.
69. F.A. Levi, C. Canon, Y. Touitou, J. Sulon, M. Mechkouri, E.D. Ponsart, J.P. Touboul, J.M. Vannetzel, I. Mowzowicz, A. Reinberg, and G. Mathe, Circadian rhythms in circulating T lymphocyte subtypes and plasma testosterone, total and free cortisol in five healthy men. Clin Exp Immunol 71: 329-335, 1988.
70. J.I. Webster and E.M. Sternberg, HPA axis activation in infection. J Endocrinol 181: 207-221, 2004.