Advertisement

Circadian Organization of the Immune Response

Lessons from the Adjuvant Arthritis Model
  • Daniel P. Cardinali
  • Ana I. Esquifino
  • Georges J.M. Maestroni
  • Seithikurippu R. Pandi-Perumal

Abstract

Organisms populating the Earth are under the steady influence of daily and seasonal changes resulting from the planet's rotation and orbit around the sun. This periodic pattern is most prominently manifested by the light-dark cycle and has led to the establishment of endogenous circadian timing systems that synchronize biological functions to the environment. This is the basis of predictive homeostasis (Moore-Ede 1986), evolving as an adaptation to anticipate predictable changes in the environment, such as light and darkness, temperature, food availability or predator activity. Therefore, the circadian clock is one of the most indispensable biological functions for living organisms that acts like a multifunctional timer to adjust the homeostatic system, including sleep and wakefulness, hormonal secretions and various other bodily functions, to the 24-h cycle (Buijs, van Eden, Goncharuk, and Kalsbeek 2003; Collins and Blau 2006; Hastings, Reddy, and Maywood 2003). In mammals, the circadian system is composed of many individual, tissue-specific cellular clocks. To generate coherent physiological and behavioral responses, the phases of this multitude of cellular clocks are orchestrated by a master circadian pacemaker residing in the suprachiasmatic nuclei (SCN) of the hypothalamus.

Keywords

Circadian Clock Clock Gene Adjuvant Arthritis Melatonin Receptor Melatonin Treatment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acuña-Castroviejo, D., Reiter, R.J., Menendez-Pelaez, A., Pablos, M.I., and Burgos, A. (1994) Characterization of high-affinity melatonin binding sites in purified cell nuclei of rat liver. J Pineal Res 16, 100–112.PubMedCrossRefGoogle Scholar
  2. Akbulut, K.G., Gonul, B., and Akbulut, H. (2001) The effects of melatonin on humoral immune responses of young and aged rats. Immunol Invest 30, 17–20.PubMedCrossRefGoogle Scholar
  3. Albrecht, U., and Eichele, G. (2003) The mammalian circadian clock. Curr Opin Genet Dev 13, 271–277.PubMedCrossRefGoogle Scholar
  4. Arendt, J., Middleton, B., Stone, B., and Skene D. (1999) Complex effects of melatonin: Evidence for photoperiodic responses in humans? Sleep 22, 625–635.PubMedGoogle Scholar
  5. Arjona, A., and Sarkar, D.K. (2005) Circadian oscillations of clock genes, cytolytic factors, and cytokines in rat NK cells. J Immunol 174, 7618–7624.PubMedGoogle Scholar
  6. Arzt, E.S., Fernandez-Castelo, S., Finocchiaro, L.M., Criscuolo, M.E., Diaz, A., Finkielman, S., and Nahmod, V.E. (1988) Immunomodulation by indoleamines: Serotonin and melatonin action on DNA and interferon-gamma synthesis by human peripheral blood mononuclear cells. J Clin Immunol 8, 513–520.PubMedCrossRefGoogle Scholar
  7. Bauhofer, A., Witte, K., Celik, I., Pummer, S., Lemmer, B., and Lorenz, W. (2001) Sickness behaviour, an animal equivalent to human quality of life, is improved in septic rats by GCSF and antibiotic prophylaxis. Langenbeck's Arch Surg 386, 132–140.CrossRefGoogle Scholar
  8. Bendele, A.M. (2001) Animal models of rheumatoid arthritis. J Musculoskel Neuron Interact 1, 377–385.Google Scholar
  9. Bentivoglio, M., Grassi-Zucconi, G., Peng, Z.C., and Kristensson, K. (1994) Sleep and timekeeping changes, and dysregulation of the biological clock in experimental trypanosomiasis. Bull Soc Pathol Exotique 87, 372–375.Google Scholar
  10. Beskonakli, E., Palaoglu, S., Aksaray, S., Alanoglu, G., Turhan, T., and Taskin, Y. (2001) Effect of pinealectomy on immune parameters in rats with Staphylococcus aureus infection. Neurosurg Rev 24, 26–30.PubMedCrossRefGoogle Scholar
  11. Bluthe, R.M., Walter, V., Parnet, P., Laye, S., Lestage, J., Verrier, D., Poole, S., Stenning, B.E., Kelley, K.W., and Dantzer, R. (1994) Lipopolysaccharide induces sickness behaviour in rats by a vagal mediated mechanism. C R Acad Sci III 317, 499–503.PubMedGoogle Scholar
  12. Boggio, V., Castrillon, P., Pérez Lloret, S., Riccio, P., Esquifino, A.I., Cardinali, D.P., and Cutrera, R.A. (2003) Cerebroventricular administration of interferon-gamma modifies locomotor activity in the golden hamster. NeuroSignals 12, 89–94.PubMedCrossRefGoogle Scholar
  13. Boivin, D.B., James, F.O., Wu, A., Cho-Park, P.F., Xiong, H., and Sun, Z.S. (2003) Circadian clock genes oscillate in human peripheral blood mononuclear cells. Blood 102, 4143–4145.PubMedCrossRefGoogle Scholar
  14. Bonilla, E., Rodon, C., Valero, N., Pons, H., Chacin-Bonilla, L., Garcia, T.J., Rodriguez, Z., Medina-Leendertz, S., and Anez, F. (2001) Melatonin prolongs survival of immunodepressed mice infected with the Venezuelan equine encephalomyelitis virus. Trans R Soc Trop Med Hyg 95, 207–210.PubMedCrossRefGoogle Scholar
  15. Bourin, P., Mansour, I., Doinel, C., Roue, R., Rouger, P. and Levi, F. (1993) Circadian rhythms of circulating NK cells in healthy and human immunodeficiency virus-infected men. Chronobiol Int 10, 298–305.PubMedGoogle Scholar
  16. Bowman, S.J. (2002) Hematological manifestations of rheumatoid arthritis. Scand J Rheumatol 31, 251–259.PubMedCrossRefGoogle Scholar
  17. Bruno, V.A., Scacchi, P., Pérez Lloret, S., Esquifino, A.I., Cardinali, D.P. and Cutrera, R.A. (2005) Melatonin treatment counteracts the hyperthermic effect of lipopolysaccharide injection in the syrian hamster. Neurosci Lett 389, 169–172.PubMedCrossRefGoogle Scholar
  18. Brusco, L.I., Garcia Bonacho, M., Esquifino, A.I., and Cardinali, D.P. (1998) Diurnal rhythms in norepinephrine and acetylcholine synthesis of sympathetic ganglia, heart and adrenals of aging rats. Effect of melatonin. J Auton Nerv Syst 74, 49–61.PubMedCrossRefGoogle Scholar
  19. Brydon, L., Petit, L., de Coppet, P., Barrett, P., Morgan, P.J., Strosberg, A.D., and Jockers, R. (1999) Polymorphism and signalling of melatonin receptors. Reprod Nutr Dev 39, 315–324.PubMedGoogle Scholar
  20. Buijs, R.M., van Eden, C.G., Goncharuk, V.D., and Kalsbeek, A. (2003) The biological clock tunes the organs of the body: Timing by hormones and the autonomic nervous system. J Endocrinol 177, 17–26.PubMedCrossRefGoogle Scholar
  21. Calvino, B., Crepon-Bernard, M.O., and Le Bars, D. (1987) Parallel clinical and behavioural studies of adjuvant-induced arthritis in the rat: Possible relationship with 'chronic pain'. Behav Brain Res 24, 11–29.PubMedCrossRefGoogle Scholar
  22. Cano, P., Cardinali, D.P., Castrillón, P., Reyes Toso, C., and Esquifino, A.I. (2001) Agedependent changes in 24-hour rhythms of catecholamine content and turnover in hypothalamus, corpus striatum and pituitary gland of rats injected with Freund's adjuvant. BMC Physiol 1, 14.PubMedCrossRefGoogle Scholar
  23. Cano, P., Cardinali, D.P., Fernandez, P., Reyes Toso, C., and Esquifino, A.I. (2006) 24-Hour rhythms of splenic mitogenic responses, lymphocyte subset populations and interferon γ release after calorie restriction or social isolation of rats. Biol Rhythm Res 37(3), 255–263.CrossRefGoogle Scholar
  24. Cano, P., Cardinali, D.P., Jimenez, V., Alvarez, M.P., Cutrera, R.A., and Esquifino, A.I. (2005) Effect of interferon-gamma treatment on 24-hour variations in plasma ACTH, growth hormone, prolactin, luteinizing hormone and follicle-stimulating hormone of male rats. Neuroimmunomodulation 12, 146–151.PubMedCrossRefGoogle Scholar
  25. Cardinali, D., Della Maggiore, V., Selgas, L., and Esquifino, A. (1996a) Diurnal rhythm in ornithine decarboxylase activity and noradrenergic and cholinergic markers in rat submaxillary lymph nodes. Brain Res 711, 153–162.CrossRefGoogle Scholar
  26. Cardinali, D.P. (1981) Melatonin. A mammalian pineal hormone. Endocr Rev 2, 327–346.PubMedGoogle Scholar
  27. Cardinali, D.P., Brusco, L.I., Selgas, L., and Esquifino, A.I. (1998a) Diurnal rhythms in ornithine decarboxylase activity and norepinephrine and acetylcholine synthesis in submaxillary lymph nodes and spleen of young and aged rats during Freund's adjuvantinduced arthritis. Brain Res 789, 283–292.CrossRefGoogle Scholar
  28. Cardinali, D.P., Brusco, L.I., Cutrera, R.A., Castrillon, P., and Esquifino, A.I. (1999) Melatonin as a time-meaningful signal in circadian organization of immune response. Biol Signals Recept 8, 41–48.PubMedCrossRefGoogle Scholar
  29. Cardinali, D.P., Brusco, L.I., Garcia, B.M., and Esquifino, A.I. (1998b) Effect of melatonin on 24-hour rhythms of ornithine decarboxylase activity and norepinephrine and acetylcholine synthesis in submaxillary lymph nodes and spleen of young and aged rats. Neuroendocrinology 67, 349–362.CrossRefGoogle Scholar
  30. Cardinali, D.P., Cutrera, R.A., Castrillon, P., and Esquifino, A.I. (1996b) Diurnal rhythms in ornithine decarboxylase activity and norepinephrine and acetylcholine synthesis of rat submaxillary lymph nodes: Effect of pinealectomy, superior cervical ganglionectomy and melatonin replacement. Neuroimmunomodulation 3, 102–111.Google Scholar
  31. Cardinali, D.P., Cutrera, R.A., Garcia Bonacho, M., and Esquifino, A.I. (1997a) Effect of pinealectomy, superior cervical ganglionectomy and melatonin treatment on 24-hour rhythms in ornithine decarboxylase and tyrosine hydroxylase activities of rat spleen. J Pineal Res 22, 210–220.CrossRefGoogle Scholar
  32. Cardinali, D.P., and Esquifino, A.I. (1998) Neuroimmunoendocrinology of the cervical autonomic nervous system. Biomed Rev 9, 47–59.Google Scholar
  33. Cardinali, D.P., and Esquifino, A.I. (2003) Circadian disorganization in experimental arthritis. NeuroSignals 12, 267–282.PubMedCrossRefGoogle Scholar
  34. Cardinali, D.P., García, A.P., Cano, P., and Esquifino, A.I. (2004) Melatonin role in experimental arthritis. Curr Drug Targets—Immune-Endocr Metab Dis 4, 1–22.CrossRefGoogle Scholar
  35. Cardinali, D.P., Golombek, D.A., Rosenstein, R.E., Cutrera, R.A., and Esquifino, A.I. (1997b) Melatonin site and mechanism of action: Single or multiple? J Pineal Res 23, 32–39.CrossRefGoogle Scholar
  36. Cardinali, D.P., Lynch, H.J., and Wurtman, R.J. (1972) Binding of melatonin to human and rat plasma proteins. Endocrinology 91, 1213–1218.PubMedGoogle Scholar
  37. Cardinali, D.P., and Pevet, P. (1998) Basic aspects of melatonin action. Sleep Med Rev 2, 175–190.PubMedCrossRefGoogle Scholar
  38. Cardinali, D.P., and Romeo, H.E. (1991) The autonomic nervous system of the cervical region as a channel of neuroendocrine communication. Front Neuroendocrinol 12, 278–297.Google Scholar
  39. Cardinali, D.P., and Stern, J.E. (1994) Peripheral neuroendocrinology of the cervical autonomic nervous system. Braz J Med Biol Res 27, 573–599.PubMedGoogle Scholar
  40. Castrillón, P., Cardinali, D.P., Pazo, D., Cutrera, R.A., and Esquifino, A.I. (2001) Effect of superior cervical ganglionectomy on 24-h variations in hormone secretion from anterior hypophysis and in hypothalamic monoamine turnover, during the preclinical phase of Freund's adjuvant arthritis in rats. J Neuroendocrinol 13, 288–295.PubMedCrossRefGoogle Scholar
  41. Castrillon, P.O., Esquifino, A.I., Varas, A., Zapata, A., Cutrera, R.A., and Cardinali, D.P. (2000) Effect of melatonin treatment on 24-h variations in responses to mitogens and lymphocyte subset populations in rat submaxillary lymph nodes. J Neuroendocrinol 12, 758–765.PubMedCrossRefGoogle Scholar
  42. Chacon, F., Cano, P., Jimenez, V., Cardinali, D.P., Marcos, A., and Esquifino, A.I. (2004) 24-Hour changes in circulating prolactin, follicle-stimulating hormone, luteinizing hormone and testosterone in young male rats subjected to calorie restriction. Chronobiol Int 21, 393–404.PubMedCrossRefGoogle Scholar
  43. Chacon, F., Esquifino, A.I., Perelló, M., Cardinali, D.P., Spinedi, E., and Alvarez, M.P. (2005) 24-Hour changes in ACTH, corticosterone, growth hormone and leptin levels in young male rats subjected to calorie restriction. Chronobiol Int 22, 253–265.PubMedCrossRefGoogle Scholar
  44. Chan, M.Y., Pang, S.F., Tang, P.L., and Brown, G.M. (1984) Studies on the kinetics of melatonin and N-acetylserotonin in the rat at mid-light and mid-dark. J Pineal Res 1, 227–236.PubMedCrossRefGoogle Scholar
  45. Collins, B., and Blau, J. (2006) Keeping time without a clock. Neuron 50, 348–350.PubMedCrossRefGoogle Scholar
  46. Crespo, E., Macias, M., Pozo, D., Escames, G., Martin, M., Vives, F., Guerrero, J.M. and Acuña-Castroviejo, D. (1999) Melatonin inhibits expression of the inducible NO synthase II in liver and lung and prevents endotoxemia in lipopolysaccharide-induced multiple organ dysfunction syndrome in rats. FASEB J 13, 1537–1546.PubMedGoogle Scholar
  47. Currier, N.L., Sun, L.Z., and Miller, S.C. (2000) Exogenous melatonin: Quantitative enhancement in vivo of cells mediating non-specific immunity. J Neuroimmunol 104, 101–108.PubMedCrossRefGoogle Scholar
  48. Cuzzocrea, S., and Reiter, R.J. (2002) Pharmacological actions of melatonin in acute and chronic inflammation. Curr Top Med Chem 2, 153–165.PubMedCrossRefGoogle Scholar
  49. Dantzer R. (2001) Cytokine-induced sickness behavior: Mechanisms and implications. Ann N Y Acad Sci 933, 222–234.PubMedCrossRefGoogle Scholar
  50. del Gobbo, V., Libri, V., Villani, N., Calio, R., and Nistico, G. (1989) Pinealectomy inhibits interleukin-2 production and natural killer activity in mice. Int J Immunopharmacol 11, 567–573.PubMedCrossRefGoogle Scholar
  51. Drazen, D.L., and Nelson, R.J. (2001) Melatonin receptor subtype MT2 (Mel 1b) and not mt1(Mel 1a) is associated with melatonin-induced enhancement of cell-mediated and humoral immunity. Neuroendocrinology 74, 178–184.PubMedCrossRefGoogle Scholar
  52. Dubocovich, M.L., Cardinali, D.P., Delagrange, P., Krause, D.N., Strosberg, D., Sugden, D., and Yocca, F.D. (2000) Melatonin receptors. In: IUPHAR Ed. The IUPHAR Compendium of Receptor Characterization and Classification, 2nd. Edn. IUPHAR Media, London, pp. 271–277.Google Scholar
  53. Esquifino, A., Selgas, L., Arce, A., Della Maggiore, V., and Cardinali, D. (1996) Twenty four hour rhythms in immune responses in rat submaxillary lymph nodes and spleen. Effect of cyclosporine. Brain Behav Immun 10, 92–102 Esquifino, A.I., Alvarez, M.P., Cano, P., Chacon, F., Reyes Toso, C.F., and Cardinali, D.P. (2004a) 24-Hour pattern of circulating prolactin and growth hormone levels and submaxillary lymph node immune responses in growing male rats subjected to social isolation. Endocrine 25, 41–48.PubMedCrossRefGoogle Scholar
  54. Esquifino, A.I., and Cardinali, D.P. (1994) Local regulation of the immune response by the autonomic nervous system. Neuroimmunomodulation 1, 265–273.PubMedCrossRefGoogle Scholar
  55. Esquifino, A.I., Castrillón, P., Chacon, F., Cutrera, R.A., and Cardinali, D.P. (2001) Effect of local sympathectomy on 24-hour changes in mitogenic responses and lymphocyte subset populations in rat submaxillary lymph nodes during the preclinical phase of Freund's adjuvant arthritis. Brain Res 888, 227–234.PubMedCrossRefGoogle Scholar
  56. Esquifino, A.I., Castrillon, P., Garcia Bonacho, M., Vara, E., and Cardinali, D.P. (1999a) Effect of melatonin treatment on 24-hour rhythms of serum ACTH, growth hormone, prolactin, luteinizing hormone and insulin in rats injected with Freund's adjuvant. J Pineal Res 27, 15–23.CrossRefGoogle Scholar
  57. Esquifino, A.I., Chacon, F., Cano, P., Marcos, A., Cutrera, R.A., and Cardinali, D.P. (2004b) 24-Hour rhythms of mitogenic responses, lymphocyte subset populations and amino acid content in submaxillary lymph nodes of growin male rats subjected to calorie restriction. J Neuroimmunol 156, 66–73.CrossRefGoogle Scholar
  58. Esquifino, A.I., Chacon, F., Jimenez, V., Reyes Toso, C., and Cardinali, D.P. (2004c) 24-Hour changes in circulating prolactin, follicle-stimulating hormone, luteinizing hormone and testosterone in male rats subjected to social isolation. J Circad Rhythms 2, 1.CrossRefGoogle Scholar
  59. Esquifino, A.I., Selgas, L., Vara, E., Arce, A., and Cardinali, D.P. (1999b) Twenty-four hour rhythms of hypothalamic corticotropin-releasing hormone, thyrotropin-releasing hormone, growth hormone-releasing hormone and somatostatin in rats injected with Freund's adjuvant. Biol Signals Recept 8, 178–190.CrossRefGoogle Scholar
  60. Feldmann, M., Brennan, F.M., Foxwell, B.M., and Maini, R.N. (2001) The role of TNF alpha and IL-1 in rheumatoid arthritis. Curr Dir Autoimmun 3, 188–199.PubMedGoogle Scholar
  61. Filipski, E., King, V.M., Etienne, M.C., Li, X., Claustrat, B., Granda, T.G., Milano, G., Hastings, M.H., and Levi, F. (2004) Persistent twenty-four hour changes in liver and bone marrow despite suprachiasmatic nuclei ablation in mice. Am J Physiol Regul Integr Comp Physiol 287, R844–R851.PubMedGoogle Scholar
  62. Fraschini, F., Demartini, G., Esposti, D., and Scaglione, F. (1998) Melatonin involvement in immunity and cancer. Biol Signals 7, 61–72.PubMedCrossRefGoogle Scholar
  63. Fukuhara, C., and Tosini, G. (2003) Peripheral circadian oscillators and their rhythmic regulation. Front Biosci 8, d642–d651.PubMedCrossRefGoogle Scholar
  64. Garcia Bonacho, M., Cardinali, D.P., Castrillon, P., Cutrera, R.A., and Esquifino, A.I. (2001) Aging-induced changes in 24-h rhythms of mitogenic responses, lymphocyte subset populations and neurotransmitter and amino acid content in rat submaxillary lymph nodes during Freund's adjuvant arthritis. Exp Gerontol 36, 267–282.CrossRefGoogle Scholar
  65. Garcia Bonacho, M., Esquifino, A.I., Castrillon, P., Reyes Toso, C., and Cardinali, D.P. (2000) Age-dependent effect of Freund's adjuvant on 24-hour rhythms in plasma prolactin, growth hormone, thyrotropin, insulin, follicle-stimulating hormone, luteinizing hormone and testosterone in rats. Life Sci 66, 1969–1977.PubMedCrossRefGoogle Scholar
  66. Garcia-Maurino, S., Gonzalez-Haba, M.G., Calvo, J.R., Rafii-el-Idrissi, M., Sanchez- Margalet, V., Goberna, R., and Guerrero, J.M. (1997) Melatonin enhances IL-2, IL-6, and IFN-gamma production by human circulating CD4+ cells: A possible nuclear receptormediated mechanism involving T helper type 1 lymphocytes and monocytes. J Immunol 159, 574–581.PubMedGoogle Scholar
  67. Giordano, M., and Palermo, M.S. (1991) Melatonin-induced enhancement of antibodydependent cellular cytotoxicity. J Pineal Res 10, 117–121.PubMedCrossRefGoogle Scholar
  68. Goodson, N., and Symmons, D. (2002) Rheumatoid arthritis in women: Still associated with an increased mortality. Ann Rheum Dis 61, 955–956.PubMedCrossRefGoogle Scholar
  69. Guerrero, J.M., and Reiter, R.J. (2002) Melatonin-immune system relationships. Curr Top Med Chem 2, 167–179.PubMedCrossRefGoogle Scholar
  70. Halberg, F., Johnson, E.A., Brown, B.W., and Bittner, J.J. (1960) Susceptibility rhythm to E. coli endotoxin and bioassay. Proc Soc Exp Biol Med 103, 142–144.PubMedGoogle Scholar
  71. Hansson, I., Holmdahl, R., and Mattsson, R. (1992) The pineal hormone melatonin exaggerates development of collagen-induced arthritis in mice. J Neuroimmunol 39, 23–30.PubMedCrossRefGoogle Scholar
  72. Hansson, I., Holmdahl, R., and Mattsson, R. (1993) Pinealectomy ameliorates collagen Iiinduced arthritis in mice. Clin Exp Immunol 92, 432–436.PubMedCrossRefGoogle Scholar
  73. Hardeland, R., Pandi-Perumal, S.R., and Cardinali, D.P. (2006) Melatonin. Int J Biochem Cell Biol 38, 313–316.PubMedCrossRefGoogle Scholar
  74. Hastings, M.H., Reddy, A.B., and Maywood, E.S. (2003) A clockwork web: Circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 4, 649–661.PubMedCrossRefGoogle Scholar
  75. Haus, E., and Smolensky, M.H. (1999) Biologic rhythms in the immune system. Chronobiol Int 16, 581–622.PubMedCrossRefGoogle Scholar
  76. Holoshitz, J., Matiau, J., and Cohen, I. (1984) Arthritis induced in rats by cloned T lymphocytes responsive to mycobacteria but not to collagen type II. J Clin Invest 73, 211–215.PubMedGoogle Scholar
  77. Hrushesky, W.J.M., Langevin, T., Kim, Y.J., and Wood, P.A. (1994) Circadian dynamics of tumor necrosis factor α (cachectin) lethality. J Exp Med 180, 1059–1065.PubMedCrossRefGoogle Scholar
  78. Jimenez, V., Cardinali, D.P., Alvarez, M.P., Fernandez, M.P., Boggio, V., and Esquifino, A.I. (2005) Effect of chronic ethanol feeding on 24-hour rhythms of mitogenic responses and lymphocyte subset populations in thymus and spleen of peripubertal male rats. Neuroimmunomodulation 12 (6), 357–365.PubMedCrossRefGoogle Scholar
  79. Jimenez, V., Cardinali, D.P., Cano, P., Alvarez, M.P., Reyes Toso, C., and Esquifino, A.I. (2004) Effect of ethanol on 24-hour hormonal changes in peripubertal male rats. Alcohol 34, 127–132.PubMedCrossRefGoogle Scholar
  80. Johnson, R.W. (2002) The concept of sickness behavior: A brief chronological account of four key discoveries. Vet Immunol Immunopathol 87, 443–450.PubMedCrossRefGoogle Scholar
  81. Kastin, A.J., Pan, W., Maness, L.M., and Banks, W.A. (1999) Peptides crossing the bloodbrain barrier: Some unusual observations. Brain Res 848, 96–100.PubMedCrossRefGoogle Scholar
  82. Knight, B., Katz, D.R., Isenberg, D.A., Ibrahim, M.A., Le Page, S., Hutchings, P., Schwartz, R.S., and Cooke, A. (1992) Induction of adjuvant arthritis in mice. Clin Exp Immunol 90, 459–465.PubMedCrossRefGoogle Scholar
  83. Kobayashi, H., Oishi, K., Hanai, S., and Ishida, N. (2004) Effect of feeding on peripheral circadian rhythms and behaviour in mammals. Genes Cells 9, 857–864.PubMedCrossRefGoogle Scholar
  84. Konakchieva, R., Kyurkchiev, S., Kehayov, I., Taushanova, P., and Kanchev, L. (1995) Selective effect of methoxyindoles on the lymphocyte proliferation and melatonin binding to activated human lymphoid cells. J Neuroimmunol 63, 125–132.PubMedCrossRefGoogle Scholar
  85. Krueger, J.M., Obal, F., Fang, J., Kubota, T., and Taishi, P. (2001) The role of cytokines in physiological sleep regulation. Ann N Y Acad Sci 933, 211–221.PubMedCrossRefGoogle Scholar
  86. Kusanagi, H., Mishima, K., Satoh, K., Echizenya, M., Katoh, T., and Shimizu, T. (2004) Similar profiles in human period 1 gene expression in peripheral mononuclear and polymorphonuclear cells. Neurosci Lett 365, 124–127.PubMedCrossRefGoogle Scholar
  87. Lakin-Thomas, P.L. (2006) Transcriptional feedback oscillators: Maybe, maybe not. J Biol Rhythms 21, 83–92.PubMedCrossRefGoogle Scholar
  88. Lancel, M., Mathias, S., Faulhaber, J., and Schiffelholz, T. (1996) Effect of interleukin-1 β on EEG power density during sleep depends on circadian phase. Am J Physiol Regul Integr Comp Physiol 270, R830–R837.Google Scholar
  89. Larson, S.J. (2002) Behavioral and motivational effects of immune-system activation. J Gen Psychol 129, 401–414.PubMedCrossRefGoogle Scholar
  90. Lewinski, A., Zelazowski, P., Sewerynek, E., Zerek-Melen, G., Szkudlinski, M., and Zelazowska, E. (1989) Melatonin-induced suppression of human lymphocyte natural killer activity in vitro. J Pineal Res 7, 153–164.PubMedCrossRefGoogle Scholar
  91. Lewy, A.J., Ahmed, S., and Sack, R.L. (1996) Phase shifting the human circadian clock using melatonin. Behav Brain Res 73, 131–134.PubMedCrossRefGoogle Scholar
  92. Liebmann, P.M., Wolfler, A., Felsner, P., Hofer, D., and Schauenstein, K. (1997) Melatonin and the immune system. Int Arch Allergy Immunol 112, 203–211.PubMedCrossRefGoogle Scholar
  93. Lissoni, P., Barni, S., Brivio, F., Rossini, F., Fumagalli, L., Ardizzoia, A., and Tancini, G. (1995) A biological study on the efficacy of low-dose subcutaneous interleukin- 2 plus melatonin in the treatment of cancer-related thrombocytopenia. Oncology 52, 360–362.PubMedGoogle Scholar
  94. Lundkvist, G.B., Andersson, A., Robertson, B., Rottenberg, M.E., and Kristensson, K. (1999) Light-dependent regulation and postnatal development of the interferon-gamma receptor in the rat suprachiasmatic nuclei. Brain Res 849, 231–234.PubMedCrossRefGoogle Scholar
  95. Lundkvist, G.B., Hill, R.H., and Kristensson, K. (2002) Disruption of circadian rhythms in synaptic activity of the suprachiasmatic nuclei by African trypanosomes and cytokines. Neurobiol Dis 11, 20–27.PubMedCrossRefGoogle Scholar
  96. Lundkvist, G.B., Robertson, B., Mhlanga, J.D., Rottenberg, M.E., and Kristensson, K. (1998) Expression of an oscillating interferon-gamma receptor in the suprachiasmatic nuclei. Neuroreport 9, 1059–1063.PubMedCrossRefGoogle Scholar
  97. Maestroni, G.J. (1995) T-helper-2 lymphocytes as a peripheral target of melatonin. J Pineal Res 18, 84–89.PubMedCrossRefGoogle Scholar
  98. Maestroni, G.J. (1996) Melatonin as a therapeutic agent in experimental endotoxic shock. J Pineal Res 20, 84–89.PubMedCrossRefGoogle Scholar
  99. Maestroni, G.J. (2001) The immunotherapeutic potential of melatonin. Exp Opin Invest Drugs 10, 467–476.CrossRefGoogle Scholar
  100. Maestroni, G.J., Conti A., and Pierpaoli, W. (1988) Pineal melatonin, its fundamental immunoregulatory role in aging and cancer. Ann N Y Acad Sci 521, 140–148.PubMedCrossRefGoogle Scholar
  101. Maestroni, G.J., Sulli, A., Pizzorni, C., Villaggio, B., and Cutolo, M. (2002) Melatonin in rheumatoid arthritis: Synovial macrophages show melatonin receptors. Ann N Y Acad Sci 966, 271–275.PubMedGoogle Scholar
  102. Majde, J.A., and Krueger, J.M. (2005) Links between the innate immune system and sleep. J Allergy Clin Immunol 116, 1188–1198.PubMedCrossRefGoogle Scholar
  103. Marpegan, L., Bekinschtein, T.A., Costas, M.A., and Golombek, D.A. (2005) Circadian responses to endotoxin treatment in mice. J Neuroimmunol 160, 102–109.PubMedCrossRefGoogle Scholar
  104. Marpegan, L., Bekinschtein, T.A., Freudenthal, R., Rubio, M.F., Ferreyra, G.A., Romano, A., and Golombek, D.A. (2004) Participation of transcription factors from the Rel/NF-[kappa]B family in the circadian system in hamsters. Neurosci Lett 358, 9–12.PubMedCrossRefGoogle Scholar
  105. Martins E., Ligeiro De Oliveira A.P., Fialho De Araujo A.M., Tavares D.L., Cipolla-Neto J. and Costa Rosa L.F. (2001) Melatonin modulates allergic lung inflammation. J. Pineal Res. 31, 363–369.PubMedCrossRefGoogle Scholar
  106. Mazzoccoli, G., Balzanelli, M., Giuliani, A., De Cata, A., La Viola, M., Carella, A.M., Bianco, G., and Tarquini, R. (1999) Lymphocyte subpopulations anomalies in lung cancer patients and relationship to the stage of disease. In Vivo 13, 205–209.PubMedGoogle Scholar
  107. McCann, S.M., Kimura, M., Karanth, S., Yu, W.H., and Rettori, V. (2002) Role of nitric oxide in the neuroendocrine response to cytokines. Front Horm Res 29, 117–129.PubMedGoogle Scholar
  108. Missbach, M., Jagher, B., Sigg, I., Nayeri, S., Carlberg, C., and Wiesenberg, I. (1996) Thiazolidine diones, specific ligands of the nuclear receptor retinoid Z receptor/retinoid acid receptor-related orphan receptor alpha with potent antiarthritic activity. J Biol Chem 271, 13515–13522.PubMedCrossRefGoogle Scholar
  109. Moore-Ede, M.C. (1986) Physiology of the circadian system: Predictive versus reactive homeostasis. Am J Physiol 250, R737–R752.PubMedGoogle Scholar
  110. Morrey, K.M., McLachlan, J.A., Serkin, C.D., and Bakouche, O. (1994) Activation of human monocytes by the pineal hormone melatonin. J Immunol 153, 2671–2680.PubMedGoogle Scholar
  111. Motzkus, D., Albrecht, U., and Maronde, E. (2002) The human PER1 gene is inducible by interleukin-6. J Mol Neurosci 18, 105–109.PubMedCrossRefGoogle Scholar
  112. Murphy, P.J., and Campbell, S.S. (1996) Physiology of the circadian system in animals and humans. J Clin Neurophysiol 13, 2–16.PubMedCrossRefGoogle Scholar
  113. Nava, F., Carta, G., and Haynes, L.W. (2000) Lipopolysaccharide increases argininevasopressin release from rat suprachiasmatic nucleus slice cultures. Neurosci Lett 288, 228–230.PubMedCrossRefGoogle Scholar
  114. Negrette, B., Bonilla, E., Valero, N., Pons, H., Garcia, T.J., Chacin-Bonilla, L., Medina-Leendertz, S., and Anez, F. (2001) Melatonin treatment enhances the efficiency of mice immunization with Venezuelan equine encephalomyelitis virus TC-83. Neurochem Res 26, 767–770.PubMedCrossRefGoogle Scholar
  115. Neidhart, M., and Larson, D. (1990) Freund's complete adjuvant induces ornithine decarboxylase activity in the central nervous system of male rats and triggers the release of pituitary hormones. J Neuroimmunol 26, 97–105.PubMedCrossRefGoogle Scholar
  116. Neidhart, M. (1996) Effect of Freund's complete adjuvant on the diurnal rhythms of neuroendocrine processes and ornithine decarboxylase activity in various tissues of male rats. Experientia 52, 900–908.PubMedCrossRefGoogle Scholar
  117. Niehaus, G.D., Ervin, E., Patel, A., Khanna, K., Vanek, V.W., and Fagan, D.L. (2002) Circadian variation in cell-adhesion molecule expression by normal human leukocytes. Can J Physiol Pharmacol 80, 935–940.PubMedCrossRefGoogle Scholar
  118. Obal, F., and Krueger, J.M. (2005) Humoral mechanisms of sleep. In: P.L. Parmeggiani and R. Velluti (Eds.), The Physiological Nature of Sleep. Imperial College Press, London, pp. 23–44.Google Scholar
  119. Ohdo, S., Koyanagi, S., Suyama, H., Higuchi, S., and Aramaki, H. (2001) Changing the dosing schedule minimizes the disruptive effects of interferon on clock function. Nat Med 7, 356–360.PubMedCrossRefGoogle Scholar
  120. Okamura, H. (2003) Integration of mammalian circadian clock signals: From molecule to behavior. J Endocrinol 177, 3–6.PubMedCrossRefGoogle Scholar
  121. Pandi-Perumal, S.R., Smits, M., Spence, W., Srinivasan, V., Cardinali, D.P., Lowe, A.D., and Kayumov L. (in press) Dim light melatonin onset (DLMO): A tool for the analysis of circadian phase in human sleep and chronobiological disorders. Prog Neuro-Psychopharmacol Biol Psychiatry. Google Scholar
  122. Pazo, D., Cardinali, D.P., Garcia Bonacho, M., Reyes Toso, C., and Esquifino A.I. (2000) Effect of melatonin treatment on 24-hour variations in hypothalamic serotonin and dopamine turnover during the preclinical phase of Freund's adjuvant arthritis in rats. Biol Rhythm Res 32, 202–211.CrossRefGoogle Scholar
  123. Pearson, C.M. (1956) Development of arthritis, periarthritis and periostitis in rats given adjuvant. Proc Soc Exp Biol Med 91, 95–103.PubMedGoogle Scholar
  124. Pelegri, C., Vilaplana, J., Castellote, C., Rabanal, M., Franch, A., and Castell, M. (2003) Circadian rhythms in surface molecules of rat blood lymphocytes. Am J Physiol Cell Physiol 284, C67–C76.PubMedGoogle Scholar
  125. Perelló, M., Chacon, F., Cardinali, D.P., Esquifino, A.I., and Spinedi, E. (2006) Effect of social isolation on 24-hour pattern of stress hormones and leptin in rats. Life Sci 78, 1857–1862.PubMedCrossRefGoogle Scholar
  126. Persengiev, S.P., and Kyurkchiev, S. (1993) Selective effect of melatonin on the proliferation of lymphoid cells. Int J Biochem 25, 441–444.PubMedCrossRefGoogle Scholar
  127. Petrovsky, N., and Harrison, L.C. (1998) The chronobiology of human cytokine production. Int Rev Immunol 16, 635–649.PubMedGoogle Scholar
  128. Pioli, C., Caroleo, M.C., Nistico, G., and Doria, G. (1993) Melatonin increases antigen presentation and amplifies specific and non-specific signals for T-cell proliferation. Int J Immunopharmacol 15, 463–468.PubMedCrossRefGoogle Scholar
  129. Poon, A.M., Liu, Z.M., Pang, C.S., Brown, G.M., and Pang, S.F. (1994) Evidence for a direct action of melatonin on the immune system. Biol Signals 3, 107–117.PubMedGoogle Scholar
  130. Pozo, D., Delgado, M., Fernandez-Santos, J.M., Calvo, J.R., Gomariz, R.P., Martin-Lacave, I., Ortiz, G.G. and Guerrero, J.M. (1997) Expression of the Mel 1a-melatonin receptor mRNA in T and B subsets of lymphocytes from rat thymus and spleen. FASEB J 11, 466–473.PubMedGoogle Scholar
  131. Raghavendra, V., Singh, V., Kulkarni, S.K., and Agrewala, J.N. (2001a) Melatonin enhances Th2 cell mediated immune responses: Lack of sensitivity to reversal by naltrexone or benzodiazepine receptor antagonists. Mol Cell Biochem 221, 57–62.CrossRefGoogle Scholar
  132. Raghavendra, V., Singh, V., Shaji, A.V., Vohra, H., Kulkarni, S.K., and Agrewala, J.N. (2001b) Melatonin provides signal 3 to unprimed CD4+ T cells but failed to stimulate LPS primed B cells. Clin Exp Immunol 124, 414–422.CrossRefGoogle Scholar
  133. Raynaud, F., Mauviard, F., Geoffriau, M., Claustrat, B., and Pevet, P. (1993) Plasma 6-hydroxymelatonin, 6-sulfatoxymelatonin and melatonin kinetics after melatonin administration to rats. Biol Signals 2, 358–366.PubMedGoogle Scholar
  134. Reginster, J.Y. (2002) The prevalence and burden of arthritis. Rheumatol (Oxford) 41(Suppl 1), 3–6.CrossRefGoogle Scholar
  135. Reiter, R.J. (1998) Cytoprotective properties of melatonin: Presumed association with oxidative damage and aging. Nutrition 14, 691–696.PubMedCrossRefGoogle Scholar
  136. Reiter, R.J., Tan, D., Cabrera, J., D'Arpa, D., Sainz, R.M., Mayo, J.C., and Ramos, S. (1999) The oxidant/antioxidant network: Role of melatonin. Biol Signals Recept 8, 56–63.PubMedCrossRefGoogle Scholar
  137. Reiter, R.J., Tan, D.X., and Burkhardt, S. (2002) Reactive oxygen and nitrogen species and cellular and organismal decline: Amelioration with melatonin. Mech Ageing Dev 123, 1007–1019.PubMedCrossRefGoogle Scholar
  138. Reppert, S.M., Weaver, D.R., and Ebisawa, T. (1994) Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and circadian responses. Neuron 13, 1177–1185.PubMedCrossRefGoogle Scholar
  139. Roman, O., Seres, J., Herichova, I., Zeman, M., and Jurcovicova, J. (2003) Daily profiles of plasma prolactin (PRL), growth hormone (GH), insulin-like growth factor-1 (IGF-1), luteinizing hormone (LH), testosterone, and melatonin, and of pituitary PRL mRNA and GH mRNA in male long evans rats in acute phase of adjuvant arthritis. Chronobiol Int 20, 823–836.PubMedCrossRefGoogle Scholar
  140. Saper, C.B., Lu, J., Chou, T.C., and Gooley, J. (2005) The hypothalamic integrator for circadian rhythms. Trends Neurosci 28, 152–157.PubMedCrossRefGoogle Scholar
  141. Sasaki, M., Jordan, P., Joh, T., Itoh, M., Jenkins, M., Pavlick, K., Minagar, A., and Alexander, S.J. (2002) Melatonin reduces TNF- α induced expression of MAdCAM-1 via inhibition of NF-kB. BMC Gastroenterol 2, 9.PubMedCrossRefGoogle Scholar
  142. Scalabrino, G., Ferioli, M.E., Modena, D., and Fraschini, F. (1982) Enhancement of ornithine decarboxylase activity in rat adenohypophysis after pinealectomy. Endocrinology 111, 2132–2134.PubMedCrossRefGoogle Scholar
  143. Schibler, U., Ripperger, J., and Brown, S.A. (2003) Peripheral circadian oscillators in mammals: Time and food. J Biol Rhythms 18, 250–260.PubMedCrossRefGoogle Scholar
  144. Selgas, L., Pazo, D., Arce, A., Esquifino, A.I., and Cardinali, D.P. (1998) Circadian rhythms in adenohypophysial hormone levels and hypothalamic monoamine turnover in mycobacterial-adjuvant-injected rats. Biol Signals Recept 7, 15–24.PubMedCrossRefGoogle Scholar
  145. Skwarlo-Sonta, K. (2002) Melatonin in immunity: Comparative aspects. Neuroendocrinol Lett 23(Suppl 1), 61–66.PubMedCrossRefGoogle Scholar
  146. Stenzel-Poore, M., Vale, W.W., and Rivier, C. (1993) Relationship between antigen-induced immune stimulation and activation of the hypothalamic-pituitary-adrenal axis in the rat. Endocrinology 132, 1313–1318.PubMedCrossRefGoogle Scholar
  147. Sulli, A., Maestroni, G.J., Villaggio, B., Hertens, E., Craviotto, C., Pizzorni, C., Briata, M., Seriolo, B., and Cutolo, M. (2002) Melatonin serum levels in rheumatoid arthritis. Ann N Y Acad Sci 966, 276–283.PubMedCrossRefGoogle Scholar
  148. Tanaka, H., Ueta, Y., Yamashita, U., Kannan, H., and Yamashita, H. (1996) Biphasic changes in behavioral, endocrine, and sympathetic systems in adjuvant arthritis in Lewis rats. Brain Res Bull 39, 33–7X.PubMedCrossRefGoogle Scholar
  149. Ueda, H.R., Hayashi, S., Chen, W., Sano, M., Machida, M., Shigeyoshi, Y., Iino, M., and Hashimoto, S. (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37, 187–192.PubMedCrossRefGoogle Scholar
  150. Undar, L., Ertugrul, C., Altunbas, H., and Akca, S. (1999) Circadian variations in natural coagulation inhibitors protein C, protein S and antithrombin in healthy men: A possible association with interleukin-6. Thromb Haemost 81, 571–575.PubMedGoogle Scholar
  151. Vagnucci, A.H., and Winkelstein, A. (1993) Circadian rhythm of lymphocytes and their glucocorticoid receptors in HIV-infected homosexual men. J Acquir Immun Defic Syndr 6, 1238–1247.Google Scholar
  152. Wajs, E., Kutoh, E., and Gupta, D. (1995) Melatonin affects proopiomelanocortin gene expression in the immune organs of the rat. Eur J Endocrinol 133, 754–760.PubMedGoogle Scholar
  153. Whitehouse, M.W. (1988) Adjuvant-induced polyarthritis in rats. In: R.A. Greenwald and H.S. Diamad (Eds.), Handbook of Animal Models for the Rheumatic Diseases. CRC Press, New York, pp. 3–16.Google Scholar
  154. Wu, C.C., Chiao, C.W., Hsiao, G., Chen, A., and Yen, M.H. (2001) Melatonin prevents endotoxin-induced circulatory failure in rats. J Pineal Res 30, 147–156.PubMedCrossRefGoogle Scholar
  155. Wu, M.W., Li, X.M., Xian, L.J., and Levi, F. (2004) Effects of meal timing on tumor progression in mice. Life Sci 75, 1181–1193.PubMedCrossRefGoogle Scholar
  156. Yoo, S.H., Yamazaki, S., Lowrey, P.L., Shimomura, K., Ko, C.H., Buhr, E.D., Siepka, S.M., Hong, H.K., Oh, W.J., Yoo, O.J., Menaker, M., and Takahashi, J.S. (2004) Inaugural Article: PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. PNAS 101, 5339–5346.PubMedCrossRefGoogle Scholar
  157. Youssef, W.I., and Tavill, A.S. (2002) Connective tissue diseases and the liver. J Clin Gastroenterol 35, 345–349.PubMedCrossRefGoogle Scholar
  158. Yu, Q., Miller, S.C., and Osmond, D.G. (2000) Melatonin inhibits apoptosis during early Bcell development in mouse bone marrow. J Pineal Res 29, 86–93.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Daniel P. Cardinali
  • Ana I. Esquifino
  • Georges J.M. Maestroni
  • Seithikurippu R. Pandi-Perumal

There are no affiliations available

Personalised recommendations