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. 2007 Jan 30;19(4):149–165. doi: 10.1111/j.1600-079X.1995.tb00184.x

Minireview The influence of season, photoperiod, and pineal melatonin on immune function

Randy J Nelson 1,✉, Gregory E Demas 1, Sabra L Klein 1, Lance J Kriegsfeld 1
PMCID: PMC7166827  PMID: 8789246

Abstract

Abstract: In addition to the well‐documented seasonal cycles of mating and birth, there are also significant seasonal cycles of illness and death among many animal populations. Challenging winter conditions (i.e., low ambient temperature and decreased food availability) can directly induce death via hypothermia, starvation, or shock. Coping with these challenges can also indirectly increase morbidity and mortality by increasing glucocorticoid secretion, which can compromise immune function. Many environmental challenges are recurrent and thus predictable; animals could enhance survival, and presumably increase fitness, if they could anticipate immunologically challenging conditions in order to cope with these seasonal threats to health. The annual cycle of changing photoperiod provides an accurate indicator of time of year and thus allows immunological adjustments prior to the deterioration of conditions. Pineal melatonin codes day length information. Short day lengths enhance several aspects of immune function in laboratory studies, and melatonin appears to mediate many of the enhanced immunological effects of photoperiod. Generally, field studies report compromised immune function during the short days of autumn and winter. The conflict between laboratory and field data is addressed with a multifactor approach. The evidence for seasonal fluctuations in lymphatic tissue size and structure, as well as immune function and disease processes, is reviewed. The role of pineal melatonin and the hormones regulated by melatonin is discussed from an evolutionary and adaptive functional perspective. Finally, the clinical significance of seasonal fluctuations in immune function is presented. Taken together, it appears that seasonal fluctuations in immune parameters, mediated by melatonin, could have profound effects on the etiology and progression of diseases in humans and nonhuman animals. An adaptive functional perspective is critical to gain insights into the interaction among melatonin, immune function, and disease processes.

Keywords: seasonality, immunity, lymphatic tissue, androgens, estrogens, glucocorticoids, stress, photoperiod, day length, melatonin, prolactin

Literature cited

  1. Abu‐Zeid, Y. A. , Abdulhadi N. H., Theander T. G., Hvkd L., Saeed B. O., Jepsen S., Jepsen J. B., Bayoumi R. A. (1992) Seasonal changes in cell mediated immune responses to soluble Plasmodium falciparum antigens in children with haemoglobin AA and haemoglobin AS. Trans. Royal Soc. Trop. Med. & Hyg. 86: 20–22. [DOI] [PubMed] [Google Scholar]
  2. Acheson, E.D. , Bachrach CA., Wright F. M. (1960) Some comments on the relationship of the distribution of multiple sclerosis to latitude, solar radiation and other variables. Acta Psychiat. Neorolog. Scand. 35 [suppl. 147]: 132–147. [DOI] [PubMed] [Google Scholar]
  3. Ader, R. , Cohen N. (1993) Psychoneuroimmunology: conditioning and stress. Ann. Rev. Psychol. 44: 53–85. [DOI] [PubMed] [Google Scholar]
  4. Aime, P. (1912) Note sur le thymus chez les cheloniens. Comptes Rendus des seances de la societe de biologie et de ses filialses. 72: 889–890. [Google Scholar]
  5. Amat, J. , Torres A. (1993) Circannual rhythm in the effects of stress on the humoral immune response of the rat. Neuro-sci. Lett. 160: 190–192. [DOI] [PubMed] [Google Scholar]
  6. Aoyama, H. , Mori W., Mori N. (1986) Anti‐glucocorticoid effects of melatonin in young rats. Acta Pathol. Jpn. 36: 423–428. [DOI] [PubMed] [Google Scholar]
  7. Aoyama, H. , Mori W., Mori N. (1987) Anti‐glucocorticoid effects of melatonin in adult rats. Acta Pathol. Jpn. 37: 1143–1148. [DOI] [PubMed] [Google Scholar]
  8. Applegate, J.E. , Beaudoin R. L. (1970) Mechanism of spring relapse in avian malaria: Effect of gonadotropin and corticosterone. J. Wildlife Dis. 6: 443–447. [DOI] [PubMed] [Google Scholar]
  9. Araneo, B.A. , Shelby J., Li G.Z., Ku W., Daynes R.A. (1993) Administration of dehydroepiandrosterone to burned mice preserves normal immunologic competence. Arch. Surg. 128: 318–325. [DOI] [PubMed] [Google Scholar]
  10. Arkins, S. , Dantzer R., Kelley K.W. (1993) Somatolactogens, somamedins, and immunity. J. Dairy Sci. 76: 2437–2450. [DOI] [PubMed] [Google Scholar]
  11. Barni, S. , Lissoni P., Cazzaniga M., Ardizzoia A., Mere‐Galli S., Fossati V., Fumagalli L., Brivio F., Tancini G. (1995) A randomized study of low‐dose subcutaneous interleukin‐2 plus melatonin versus supportive care alone in metastatic colorectal cancer patients progressing under 5‐fluorouracil and folates. Oncology 52: 243–245. [DOI] [PubMed] [Google Scholar]
  12. Bartness, T.J. , Goldman B.D. (1989) Mammalian pineal melatonin: A clock for all seasons. Experientia 45: 939–945. [DOI] [PubMed] [Google Scholar]
  13. Baxter, J. , Forsham P. (1972) The effects of glucorticoids. Am. J. Med. 53: 573–589. [DOI] [PubMed] [Google Scholar]
  14. Beal, S.M. (1983) Some epidemiological factors about sudden infant death syndrome (SIDS) in South Australia In: Sudden Infant Death Syndrome, Tildon J.D., Roeder L.M., and Steinshreider A., eds. Academic Press: New York , pp. 15–28. [Google Scholar]
  15. Becker, J. , Veit G., Handgretinger R., Attanasio A., Bruchett G., Treuner I., Niethammer D., Gupta T.K Das (1988) Circadian variations in the immunomodulatory role of the pineal gland. Neuroendocrinol. Lett. 10: 65–72. [Google Scholar]
  16. Berczi, I. (1986) The influence of the pituitary‐adrenal axis on the immune system In: Pituitary Function and Immunity, Berczi I. ed. CRC Press: Boca Raton , FL , pp. 49–433. [Google Scholar]
  17. Berman, L. (1921) The Glands Regulating Personality. McGrath: College Park . [Google Scholar]
  18. Bernton, E.W. , Bryant H.U., Holaday J.W. (1991) In: Psychoneuroimmunology, Ader R., Felten D. L., Cohen N. ed. Academic Press: New York , pp. 403–328. [Google Scholar]
  19. Bernton, E. , Bryant H., Holaday J., Dave J. (1992) Prolactin and prolactin secretagogues reverse immunosuppression in mice treated with cycteamine, glucocorticoids, or cyclosporin‐A. Brain Behav. Immun. 6: 394–408. [DOI] [PubMed] [Google Scholar]
  20. Besedovsky, H.O. , DEL Rey A. (1991) Feed‐back interactions between immunological cells and the hypothalamus‐pituitary‐adrenal axis. Nether. J. Med. 39: 274–280. [PubMed] [Google Scholar]
  21. Besedovsky, H.O. , DEL Rey A., AND Sorkin E. (1981) Lym‐phokine‐containing supernatants from Con A‐stimulated cells increase corticosterone blood level. J. Immunol., 126: 385–387. [PubMed] [Google Scholar]
  22. Besedovsky, H.O. , DEL Rey A., Sorkin E. (1983) What do the immune system and the brain know about each other Immunol. Today 4: 342–346. [DOI] [PubMed] [Google Scholar]
  23. Besedovsky, H.O. , DEL Rey A., Sorkin E., Dinarello C.A. (1986) Immunoregulatory feedback between interleukin‐1 and glucocorticoid hormones. Science 233: 652–654. [DOI] [PubMed] [Google Scholar]
  24. Biller, J. , Jones M. P., Bruno A., Adams H. P., Banwart K. (1988) Seasonal variation of stroke‐does it exist Neuroepidemiology 7: 89–98. [DOI] [PubMed] [Google Scholar]
  25. Bittman, E.L. (1984) Melatonin and photoperiodic time measurement: Evidence from rodents and ruminants In: The Pineal Gland, Reiter R. J., ed. Raven Press: New York , pp. 155–192. [Google Scholar]
  26. Black, PH. (1994) Central nervous system‐immune system interactions: psychoneuroendocrinology of stress and its immune consequences. Antimicrob. Agents Chemother. 38: 1–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Blask, D.E. (1985) The pineal: an oncostatic gland? In: The Pineal Gland, Reiter R. J., ed. Raven Press: New York , pp. 253–284. [Google Scholar]
  28. Blom, L. , Dahlquist G. (1985) Epidemiological aspects of the natural history of childhood diabetes. Acta. Pediatr. Scand. Suppl. 320: 20–25. [DOI] [PubMed] [Google Scholar]
  29. Blom, J.M.C. , Gerber J., Nelson R. J. (1994) Immune function in deer mice: Developmental and photoperiodic effects. Am. J. Physiol. 267: R596–R601. [DOI] [PubMed] [Google Scholar]
  30. Boctor, F.N. , Charmy R. A., Cooper E. L. (1989) Seasonal differences in the rhythmicity of human male and female lymphocyte blastogenic responses. Immunol. Invest. 18: 775–784. [DOI] [PubMed] [Google Scholar]
  31. Boucek, R.J. , Alvarez T. R. (1970) 5‐hydroxytryptamine: a cytospecific growth mediator of cultured fibroblasts. Science 167: 898–899. [DOI] [PubMed] [Google Scholar]
  32. Bradley, A.J. , Mcdonald I. R., Lee A. K. (1980) Stress and mortality in a small marsupial (Antechinus stuarti Macleay). Gen. Comp. Endocrinol. 40: 188–200. [DOI] [PubMed] [Google Scholar]
  33. Brainard, G.C. , Knobler R. L., Podolin P. L., Lavasa M., Lubin F. D. (1987) Neuroimmunology: modulation of the hamster immune system by photoperiod. Life Sci. 40: 1319–1326. [DOI] [PubMed] [Google Scholar]
  34. Brainard, G.C. , Vaughan M. K., Reiter R. J. (1986) Effect of light irradiance and wavelength on the Syrian hamster reproductive system. Endocrinology 119: 648–654. [DOI] [PubMed] [Google Scholar]
  35. Brainard, G.C. , Watson‐Whitmeyer M., Knobler R.L., Lubin F.D. (1988) Neuroendocrine regulation of immune parameters. Ann. NY Acad. Sci. 540: 704–706. [DOI] [PubMed] [Google Scholar]
  36. Bratescu, A. , M, Teodorescu (1981) Circannual variations in the B cell/ T cell ratio in normal human peripheral blood. J. Allergy Clin. Immunol. 68: 273–280. [DOI] [PubMed] [Google Scholar]
  37. Brick, J.E. , Wilson D.A., Walker S. E. (1985) Hormonal modulation to thymus‐independent and thymus‐dependent antigens in autoimmune NZB/W mice. J. Immunol. 134: 3693–3698. [PubMed] [Google Scholar]
  38. Brock, M.A. (1983) Seasonal rhythmicity in lymphocyte blastogenic responses of mice persist in a constant environment. J. Immunol. 130: 2586–2588. [PubMed] [Google Scholar]
  39. Bronson, F.H. (1989) Mammalian Reproductive Biology. University of Chicago Press: Chicago . [Google Scholar]
  40. Bronson, F.H. (1995) Seasonal variation in human reproduction: Environmental factors. Q. Rev. Biol. 70: 141–164. [DOI] [PubMed] [Google Scholar]
  41. Bronson, F.H. , Heideman P.D. (1994) Seasonal regulation of reproduction in mammals In: The Physiology of Reproduction vol. 2, 2nd ed. Knobil E. and Neill J. D. ed. Raven Press: NY , pp. 541–584. [Google Scholar]
  42. Calvo, J.R. , Rafii‐El‐Idrissi M., Pozo D., Guerrero J. M. (1995) Immunomodulatory role of melatonin: specific binding sites in human and rodent lymphoid cells. J. Pineal Res. 18: 119–126. [DOI] [PubMed] [Google Scholar]
  43. Caroleo, M.C. , Frasca D., Nistico G., Doria G. (1992) Melatonin as immunomodulator in immunodeficient mice. Immunopharmacology 23: 81–89. [DOI] [PubMed] [Google Scholar]
  44. Caroleo, M.C. , Nistico G., Doria G. (1992) Effect of melatonin on the immune system. Pharmacol. Res. 26 [suppl]: 34–37. [DOI] [PubMed] [Google Scholar]
  45. Carpenter, R.G. , Gardner A. (1990) Environmental findings and sudden infant death syndrome. Lung Suppl: 358–367. [DOI] [PubMed] [Google Scholar]
  46. Casson, P.R. , Anaderson R. N., Herrod H. G., Stentz F. B., Straughn A. B., Abraham G. E., Buster J. E. (1993) Oral dehydroepiandrosterone in physiologic doses modulates immune function in postmenopausal women. Am. J. Obstet. Gynecol. 169: 1536–1539. [DOI] [PubMed] [Google Scholar]
  47. Castanon, N. , Dulluc J., Moal M. E, Mormede P. (1992) Prolactin as a link between behavioral and immune differences between the Roman rat lines. Physiol. Behav. 51: 1235–1241. [DOI] [PubMed] [Google Scholar]
  48. Cavallaro, J.J. , Monto A. S. (1970) Community‐wide outbreak of infection with a 229E‐like coronavirus in Tecumseh, Michigan. J. Infect. Dis. 122: 272–279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Champney, T.H. , Holtorf A. P., Craft CM., Reiter R. J. (1986) Hormonal modulation of pineal melatonin synthesis in rats and Syrian hamsters: Effects of streptozotocin‐induced diabetes and insulin injections. Comp. Biochem. Physiol. A. 83: 391–395. [DOI] [PubMed] [Google Scholar]
  50. Champney, T.H. , Mcmurray, D.N. (1991) Spleen morphology and lymphoproliferative activity in short photoperiod exposed hamsters In: Role of Melatonin and Pineal Peptides in Neuroimmunomodulation, Franchini F., Reiter R. ed. Plenum Press: New York , pp. 219–223. [Google Scholar]
  51. Chen, Y , Johnson A. G. (1993) In vivo activation of macrophages by prolactin from young and aging mice. Int. J. Immunopharmacol. 15: 39–45. [DOI] [PubMed] [Google Scholar]
  52. Chernin, E. (1952) The relapse phenomenon in Leucocytozoan infections of the domestic duck. Am. J. Hyg. 56: 101–118. [DOI] [PubMed] [Google Scholar]
  53. Chleboun, J.O. , Gray B.N. (1987) The profile of breast cancer in Western Australia. Med. J. Austr. 147: 331–334. [PubMed] [Google Scholar]
  54. Chougnet, C , Deloron P., Lepers J. P., Tallet S., Rason M. D., Astagneau P., Savel J., Coulanges P. (1990) Humoral and cell‐mediated immune responses to the Plasmodium falciparum antigens PF155/RESA and CS protein: Seasonal variations in a population recently reexposed to endemic malaria. Am. J. Trop. Med. Hyg. 43: 234–242. [DOI] [PubMed] [Google Scholar]
  55. Claman, H.N. (1972) Corticosteroids and lymphoid cells. N. Eng. J. Med. 287: 388–397. [DOI] [PubMed] [Google Scholar]
  56. Coatney, G.R. , Cooper W. C. (1948) Recrudescence and relapse in the vivax malaria. Proc. Fourth Int. Congr. Trop. Med. and Malaria 1: 629–639. [PubMed] [Google Scholar]
  57. Cohen, P. , Wax Y., Modan B. (1983) Seasonality in the occurrence of breast cancer. Cancer Res. 43: 892–896. [PubMed] [Google Scholar]
  58. Cornelius, C.E. (1971) Seasonality of gonorrhea in the United States. HSMHA 86: 157–160. [PMC free article] [PubMed] [Google Scholar]
  59. Danel, L. , Sovweine G., Monier J.C, Saez S. (1983) Specific estrogen binding sites in human lymphoid cells and thymic cells. J. Steroid Biochem, 18: 559–563. [DOI] [PubMed] [Google Scholar]
  60. Davenport, C.B. (1922) Multiple sclerosis from east and point of geographic distribution and race. Arch. Neurol. Psychiatr. 8: 51–58. [Google Scholar]
  61. Demas, G.E. , Nelson R. N. (1996) Photoperiod and temperature interact to affect immune parameters in male deer mice (Peromyscus maniculatus). J. Biol Rhythms (In press). [DOI] [PubMed] [Google Scholar]
  62. Descoteaux, J.P. , Mihok S. (1986) Serologic study on the prevalence of murine viruses in a population of wild meadow voles (Microtus pennsylvanicus). J. Wildlife Dis. 22: 314–319. [DOI] [PubMed] [Google Scholar]
  63. Devecerski, V. (1963) Contributions a ľ etude de ľ effect de ľ epiphysectomie sur ľ histophysiologie du thymus. Acta Anat. 54: 352–353. [Google Scholar]
  64. Dobrowsolska, A. , Gromadzda‐Ostrowska J. (1984) Age and androgen‐related changes in morphological parameters, haematological indices and serum protein fraction in common vole (Microtus arvalis pall) growing in different photo‐periods. Comp. Biochem. Physiol. 79A 241–249. [DOI] [PubMed] [Google Scholar]
  65. Douglas, A.S. , Russell D., Allan T. M. (1990) Seasonal, regional and secular variations of cardiovascular and cerebrovascular mortality in New Zealand. Aust. N.Z. J. Med. 20: 669–676. [DOI] [PubMed] [Google Scholar]
  66. Dunn, A. (1989) Psychoneuroimmunology for the psycho‐neuroendocrinologist: A review of animal studies of nervous system‐immune system interactions. Psychoneuroendo-crinology 14: 251–274. [DOI] [PubMed] [Google Scholar]
  67. Dunnigan, M.G. , Harland W. A., Fyfe T (1970) Seasonal incidence and mortality of ischaemic heart‐disease. Lancet 2: 793–796. [DOI] [PubMed] [Google Scholar]
  68. EL Ridi, R. , Badir N., EL Rouby S. (1981) Effect of seasonal variations on the immume system of the snake Psammophis schokar . J. Exp. Zool. 216: 357–365. [Google Scholar]
  69. Fange, R. , Silverin B. (1985) Variation of lymphoid activity in the spleen of a migratory bird, the pied flycatcher (Ficedula hypoleuca; Aves, Paseriforms). J. Morphol. 184: 33–40. [DOI] [PubMed] [Google Scholar]
  70. Fauci, S. (1975) Corticosteroids and circulatory lymphocytes. Transplant Proc. 7: 37–40. [PubMed] [Google Scholar]
  71. Gavier‐Widen, D. , Morner T. (1991) Epidemiology and diagnosis of the European brown hare syndrome in Scandinavian countries: a review. Rev. Sci. Tech. 10: 453–458. [DOI] [PubMed] [Google Scholar]
  72. Gilkerson, J. , Jorm L.R., Love D. N., Lawrence G. L., Whalley J. M. (1994) Epidemiological investigation of equid herp‐esvirus‐4 (EHV‐4) excretion assessed by nasal swabs taken from thoroughbred foals. Vet. Microbiol. 39: 275–283. [DOI] [PubMed] [Google Scholar]
  73. Giordano, M. , Vermeulen M., Palermo M.S. (1993) Seasonal variations in antibody cellular cytotoxicity regulation by melatonin. FASEB J. 7: 1052–1054. [DOI] [PubMed] [Google Scholar]
  74. Glezen, W.P. , Payne A.A., Snyder D.N., Downs T.D. (1982) Mortality and influenza. J. Infect. Dis. 146: 313–321. [DOI] [PubMed] [Google Scholar]
  75. DEL Gobbo, V , Libri V., Villani N., Calio R., Nistico G. (1989) Pinealectomy inhibits interleukin‐2 production and natural killer cell activity in mice. Int. J. Immunopharmacol. 11: 567–573. [DOI] [PubMed] [Google Scholar]
  76. Goldman, B.D. (1983) The physiology of melatonin in mammals. Pineal Res. Rev. 1: 145. [Google Scholar]
  77. Goldman, B.D. , Nelson R. J. (1993) Melatonin and seasonality in mammals In: Melatonin: Biosynthesis, Physiological Effects and Clinical Applications, Yu H.S., Reiter R.J. ed. CRC Press: New York , pp. 225–252. [Google Scholar]
  78. Gregoire, C. (1945) Sure le mechanism de ľ hypertrophie physique declutched par la castration. Archives Internationales des Pharmaodynmie et de Therapie 67: 45–77. [Google Scholar]
  79. Grossman, C.J. (1984) Regulation of the immune system by sex steroids. Endocrine Rev. 5: 435–455. [DOI] [PubMed] [Google Scholar]
  80. Grossman, C.J. (1985) Interactions between the gonadal steroids and the immune system. Science 227: 257–261. [DOI] [PubMed] [Google Scholar]
  81. Guerero, J.M. , Reiter R. J. (1992) A brief survey of pineal gland‐immune system interrelationships. Endocr. Res. 18: 91–113. [DOI] [PubMed] [Google Scholar]
  82. Gupta, D. (1990) The pineal gland: its immunomodulatory role In: Advances in Pineal Research, vol. 4, Reiter R. J. and Lukaszyk A. ed. John Libbey: London , pp. 265–285. [Google Scholar]
  83. Hall, C.B. (1991) Respiratory syncytial virus In: Textbook of Pediatric Infectious Diseases, Feigin R.D., and Cherry J. D., eds. WB Saunders: Philadelphia , pp. 1633–1655. [Google Scholar]
  84. Hall, N.R. , Goldstein A. L. (1984) In: Psychoneuroendocrinology, Ader R. ed. Academic Press: New York , pp. 512–543. [Google Scholar]
  85. Hammar, J.A. (1929) Die menschenthymus in Gezundheit und Krakheit. II Das Organ unter anomale Verhaltniss. Zeitung Mikroskopanatomie Forschung, 16 [Supplement]: 22–26. [Google Scholar]
  86. Hamre, D. , Beem M. (1972) Virologic studies of acute respiratory disease in young adults. V. Coronavirus 229E infections during six years of surveillance. Am. J. Epidemiol. 96: 94–106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Hansson, I. , Holmdahl R., Mattsson R. (1993) Pinealectomy ameliorates collagen II‐induced arthritis in mice. Clin. Exp. Immunol. 92: 432–436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Hauger, R.L. , Millan M. A., Lorang M., Harwood M.J.P., Aguilera G. (1988) Corticotropin releasing factor receptors and pituitary adrenal responses during immobilization stress. Endocrinology 123: 396–405. [DOI] [PubMed] [Google Scholar]
  89. Heldmaier, G. , Steinlechner S., Ruf T., Wiesinger H., Klingenspor M. (1989) Photoperiod and thermoregulation in vertebrates: Body temperature rhythms and thermogenic acclimation. J. Biol. Rhythms 4: 251–265. [PubMed] [Google Scholar]
  90. Hendley, J.O. , Fishburne H. B., Gwaltney J. M. (1972) Coronavirus infections in working adults. Eight-year study with 229E and OC43. Am. Rev. Respir. Dis. 105: 805–811. [DOI] [PubMed] [Google Scholar]
  91. Henken, A.M. , Brandsma, H.A. (1982) The effect of environmental temperature on immune response and metabolism of the young chicken. 2. Effect of the immune response to sheep red blood cells on energy metabolism. Poultry Sci. 61: 1667–1677. [DOI] [PubMed] [Google Scholar]
  92. Hohn, E.O. (1947) Seasonal cyclical changes in the thymus of the mallard. J. Exp. Biol. 24: 184–191. [DOI] [PubMed] [Google Scholar]
  93. Hohn, E.O. (1956) Seasonal recrudescence of the thymus in adult birds. Can. J. Biochem. Physiol. 34: 90–101. [PubMed] [Google Scholar]
  94. Hostmark, J.G. , Laerum O. D., Farsund T. (1984) Seasonal variations of symptoms and occurrence of human bladder carcinomas. Scand. J. Urol. Nephrol. 18: 107–111. [DOI] [PubMed] [Google Scholar]
  95. Hughes, C.S. , Gaskall R. M., Jones R. C., Bradbury J. M., Jordan F.T.W. (1989) Effects of certain stress factors on the re‐excretion of infectious laryngotracheitis virus from latently infected carrier birds. Res. Vet. Sci. 46: 274–274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Hussein, M.F. , Badir N., EL Ridi R., EL Deeb S. (1979) Effect of seasonal variation on immune system of the lizard. Scincus scincus . J. Exp. Zool. 212: 91–92. [Google Scholar]
  97. Inman, R.D. (1978) Immunologic sex differences and the female preponderance in systemic lupus erythematosus. Arthritis Rheum. 21: 849–852. [DOI] [PubMed] [Google Scholar]
  98. Isogai, H. , Isogai E., Masuzawa T., Yanagihara Y., Matsubara M., Shimanuki M., Seta T., Fukai K., Kurosawa N., Enokidani M. (1992) Seroepidemiological survey for antibody to Borrelia burdorferi in cows. Microbiol. Immunol. 36: 1029–1039. [DOI] [PubMed] [Google Scholar]
  99. Jacobsen, H.K. , Janerich D. T. (1977) Seasonal variation in the diagnosis of breast cancer. Proc. Am. Assoc. Cancer Res. 18: 93. [Google Scholar]
  100. John, J.L. (1994) The avian spleen: A neglected organ. Q. Rev. Biol., 69: 327–351. [DOI] [PubMed] [Google Scholar]
  101. Jose, D.G. , Good R. A. (1973) Quantitative effects of nutritionally essential amino acid deficiencies upon immune responses to tumors in mice. J. Exp. Med. 137: 1–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Kapikian, A. Z. , Kim H.W., Wyatt R. G., Cline W. L., Arrobio J. O., Brandt CD., Rodriguez W. J., Sack D. A., Chanock R. M., Parrott R. H. (1976) Human reovirus‐like agent as the major pathogen associated with “winter” gastroenteritis in hospitalized infants and young children. N. Engl. J. Med. 294: 965–972. [DOI] [PubMed] [Google Scholar]
  103. Kasper, S. , Rosenthal N. E., Barberi S., Williams A., Tamarkin L., Rogers S. L., Pillemer S. R. (1991) Immunological correlates of seasonal fluctuations in mood and behavior and their relationship to phototherapy. Psychiatr. Res. 36: 253–264. [DOI] [PubMed] [Google Scholar]
  104. Kawate, T. , Abo T., Hinnma S., Kumagau K. (1981) Studies on the bioperiodicity of the immune response. II. Covariations of murine T and B cells and a role of corticosteroids. J. Immunol. 126: 1364. [PubMed] [Google Scholar]
  105. Kelley, K.W. (1985) Immunological consequences of changing environmental stimuli In: Animal Stress, Moberg G. P., ed. American Physiology Society: Bethesda , pp. 193–223. [Google Scholar]
  106. Kirkham, N. , Machin D., Cotton D.W.K., Pike J. M. (1985) Seasonality and breast cancer. Eur. J. Surg. Oncol. 11: 143–146. [PubMed] [Google Scholar]
  107. Krause, R (1922) Die Milz In: Mikroskopische Anatomie der Wirbeltiere, Vogel und Reptilien, vol. 2, Verlag W. De Gruyter u. Co.: Berlin . [Google Scholar]
  108. Kuci, S. , Becker J., Veit G. (1983) Circadian variations of the immunomodulatory role of the pineal gland. Neuroendocrinol. Lett. 10: 65–79. [Google Scholar]
  109. Kuhl, H. , Gross M. M., Schneider W., Weber W., Mehlis M., Stegmuller M., Taubert H.D. (1983) The effect of sex steroids and hormonal contraceptives upon thymus and spleen of intact female rats. Contraception 28: 587–601. [DOI] [PubMed] [Google Scholar]
  110. Kurtzke, J.F. (1975) A reassessment of the distribution of multiple sclerosis. Acta Neurol. Scand. 51: 137–157. [DOI] [PubMed] [Google Scholar]
  111. Kurtzke, J.F. (1980) Geographic distribution of multiple sclerosis: An update with special reference to Europe and the Mediterranean region. Acta Neurol. Scand. 62: 65–80. [DOI] [PubMed] [Google Scholar]
  112. Levi, F.A. , Canon C., Touitou Y., T.J. SULON, Mechkouri , et al., 1988. Circadian rhythms in circulating T lymphocyte subtypes and plasma testosterone, total and free Cortisol in five healthy men. Clin. Exp. Immunol. 71: 329–335. [PMC free article] [PubMed] [Google Scholar]
  113. Limburge, CD. (1950) The geographic distribution of multiple sclerosis and its estimated prevalence in the United States. Proc. Assoc. Res. Nervous Mental Dis. 28: 15–24. [PubMed] [Google Scholar]
  114. Lissoni, P. , S, Barni , Tancini G., Mainini E., Piglia F., Maestroni G.J., Lewinski A. (1995) Immunoendocrine therapy with low‐dose subcutaneous interleukin‐2 plus melatonin of locally advanced or metastatic endocrine tumors. Oncology 52: 163–166. [DOI] [PubMed] [Google Scholar]
  115. Lissoni, P. , Meregalli S., Fossati V., Paolorossi F., Barni S., Tancini G., Frigerio F. (1994) A randomized study of immunotherapy with low‐dose subcutaneous interleukin‐2 plus melatonin vs chemotherapy with cisplatin and etoposide as first‐line therapy for advanced non‐small cell lung cancer. Tumori 80: 464–467. [DOI] [PubMed] [Google Scholar]
  116. Liu, Z.M. , Pang S. F. (1993) [125I]iodomelatonin binding sites in the bursa of Fabricus of birds: Binding characteristics, subcellular distribution, diurnal variations and age studies. J. Endocrinol. 138: 51–57. [DOI] [PubMed] [Google Scholar]
  117. Lochmiller, R.L. , Vesty, M.R. , Mcmurry S. T. (1994) Temporal variation in humoral and cell‐mediated immune response in a Sigmodon hispidus population. Ecology 75: 236–245. [Google Scholar]
  118. Lopez‐Gonzales, M.A. , Calvo J. R., Osuna C., Guerrero J. M. (1992) Interaction of melatonin with human lymphocytes: Evidence for binding sites coupled to potentiation of cyclic AMP stimulated vasoactive intestinal peptide and activation of cyclic GMP. J. Pineal Res. 12: 97–104. [DOI] [PubMed] [Google Scholar]
  119. Lord, R.D. (1992) Seasonal reproduction of vampire bats and its relation to seasonality of bovine rabies. J. Wildlife Dis. 28: 292–294. [DOI] [PubMed] [Google Scholar]
  120. Loria, R.M. , Padgett D. A. (1992) Mobilization of cutaneous immunity for systematic protection against infections. Ann. NY Acad. Sci. 650: 363–366. [DOI] [PubMed] [Google Scholar]
  121. Lynch, H.J. , Deng M. H., Wurtman R. J. (1984) Light intensities required to suppress nocturnal melatonin secretion in albino and pigmented rats. Life Sci. 35: 841–847. [DOI] [PubMed] [Google Scholar]
  122. Lyngbye, J. , Kr0ll J. (1971) Quantitative immunoelectro‐phoresis of proteins in serum from a normal population: Season‐, age‐, and sex‐related variations. Clin. Chem. 17: 495–500. [PubMed] [Google Scholar]
  123. Mccruden, A.B. , Stimson W. H. (1984) Androgen receptors in human thymus. Immunol. Lett. 8: 49–53. [DOI] [PubMed] [Google Scholar]
  124. Mccruden, A.B. , Stimson W. H. (1991) Sex hormones and immune function In: Psychoneuroimmunology. Ader R. and Cohen J. ed. Academic Press: New York , pp. 475–493. [Google Scholar]
  125. Mcdonald, I.R. , Lee A. K., Bradley A. J., Than K. A. (1981) Endocrine changes in dasyurid marsupials with differing mortality patterns. Gen. Comp. Endocrinol. 44: 292–301. [DOI] [PubMed] [Google Scholar]
  126. Macmurray, J.R , Barker J. P., Armstrong J. D., Bozzetti L. P., Kuhn I. N. (1983) Circannual changes in immune function. Life Sci. 32: 2363–2370. [DOI] [PubMed] [Google Scholar]
  127. Maestroni, G.J. (1993) The immunoendocrine role of melatonin. J. Pineal Res. 14: 1–10. [DOI] [PubMed] [Google Scholar]
  128. Maestroni, G.J.M. , Conti A., Pierpoli W. (1986) Role of the pineal gland in immunity. Circadian synthesis and release of melatonin modulates the antibody response and antagonizes the immunosuppressive effect of corticosterone. J. Neuroimmunol. 13: 19–30. [DOI] [PubMed] [Google Scholar]
  129. Maestroni, G.J.M. , Pierpoli W. (1981) Pharmacologic control of the hormonally mediated immune response In: Psychoneuroimmunology, Ader R. ed. Academic Press: New York , pp. 405–425. [Google Scholar]
  130. Mahmoud, I. , Salman S. S., Al‐Khateet A. (1994) Continuous darkness and continuous light induced structural changes in the rat thymus. J Anat. 185: 143–149. [PMC free article] [PubMed] [Google Scholar]
  131. Maier, S.F. , Watkins L. R., Fleshner M. (1994) Psychoneuroimmunology: The interface between behavior, brain, and immunity. Am. Psychol. 49: 1004–1017. [DOI] [PubMed] [Google Scholar]
  132. Martin‐Cacao, A. , Lopez‐Gonzalez M. A., Reiter R. J., Calvo J.R., Guerrero J.M. (1993) Binding of 2‐[125I]melatonin by rat thymus membranes during postnatal development. Immunol. Lett. 36: 59–64. [DOI] [PubMed] [Google Scholar]
  133. Mason, B.H. , Holdaway I. M., Mullins PR., Kay R.G., Skinner S.J. (1985) Seasonal variation in breast cancer detection: Correlation with tumour progesterone receptor status. Breast Cancer Res. Treat. 5: 171–176. [DOI] [PubMed] [Google Scholar]
  134. Matera, L. , Cesano A., Bellone G., Oberholtzer E. (1992) Modulatory effect of prolactin on the resting and mitogen‐induced activity of T, B, and NK lymphocytes. Brain Behav. Immun. 6: 409–417. [DOI] [PubMed] [Google Scholar]
  135. Mihok, S. , Schwartz B. (1989) Anemia at the onset of winter in the meadow vole (Microtus pennsylvanicus). Comp. Bio-chem. Physiol. 94A: 289–304. [DOI] [PubMed] [Google Scholar]
  136. Milcu, S.M. , Pitis M. (1943) Contributions a ľ etude de la correlation thymo‐epiphysaire. Acta Endocrinol. (Bucarest) 9: 13–15. [Google Scholar]
  137. Miller, H. (1992) Respiratory syncytial virus and the use of ribavirin. Maternal Child Nursing 17: 238–241. [DOI] [PubMed] [Google Scholar]
  138. Moffatt, C.A. , Devries A. C., Nelson R. J. (1993) Winter adaptations of male deer mice and prairie voles that vary in reproductive responsiveness to photoperiod. J. Biol. Rhythms 8: 221–232. [DOI] [PubMed] [Google Scholar]
  139. Monjan, A.A. (1981) Stress and immunologic competence: Studies in animals In: Psychoneuroimmunology, Ader R., ed. Academic Press: New York , pp. 185–228. [Google Scholar]
  140. Morales, A.J. , Nolan J. J., Nelson J. C., Yen S. S. (1994) Effects of replacement dose of dehydroepiandrosterone in men and women of advancing age. J. Clin. Endocrinol. Metab. 78: 1360–1367. [DOI] [PubMed] [Google Scholar]
  141. Munck, A. , Guyre P. M. (1991) Glucocorticoids and immune function In: Psychoneuroimmunology. Ader R., Felten D. L., and Cohen N., eds. Academic Press: New York , pp. 447–474. [Google Scholar]
  142. Myers, M.J. , Peterson B. H. (1985) Estradiol induced alterations of the immune system. I. Enhancement of IgM production. Int. J. Immunopharmacol. 7: 207–213. [DOI] [PubMed] [Google Scholar]
  143. Nakono, K. , Susuki S., Oh C. (1987) Significance of increased secretion of glucocorticoids in mice and rats injected with bacterial endotoxin. Brain Behav. Immunol. 1: 159–172. [DOI] [PubMed] [Google Scholar]
  144. Nelson, R.J. (1990) Photoperiodic responsiveness in house mice. Physiol. Behav. 48: 403–408. [DOI] [PubMed] [Google Scholar]
  145. Nelson, R.J. , Badura L. L., Goldman B. D. (1990) Mechanisms of seasonal cycles of behavior. Ann. Rev. Psychol. 41: 81–109. [DOI] [PubMed] [Google Scholar]
  146. Nelson, R.J. , Blom J. M. C. (1994) Photoperiodic effects on tumor development and immune function. J. Biol. Rhythms 9: 233–249. [DOI] [PubMed] [Google Scholar]
  147. Nelson, R.J. , Demas G. E. (1996) Seasonal changes in immune function. Q. Rev. Biol. (In press). [DOI] [PubMed] [Google Scholar]
  148. Nelson, R.J. , Moffatt C. A., Goldman B. D. (1994) Photoperiodic effects on reproductive function in male rats. J. Pineal Res. 17: 123–131. [DOI] [PubMed] [Google Scholar]
  149. Neri, B. , Fiorelli C., Moroni F., Nicita G., Paoletti M. C., Ponchietti R., Raugei A., Santoni G., Trippitelli A., Grechi G. (1994) Modulation of human lymphoblastoid interferon activity by melatonin in metastatic renal cell carcinoma. A phase II study. Cancer 73: 3015–3019. [DOI] [PubMed] [Google Scholar]
  150. Newson, J. (1962) Seasonal differences in reticulocyte count, hemoglobin levels and spleen weight in wild voles. Brt. J. Haematol. 8: 296–302. [DOI] [PubMed] [Google Scholar]
  151. Nilsson, B. , Carlsson S., Damber M. K., Lindblom D., Sodergard R., VON Schoultz B. (1984) Specific binding of 17‐beta estradiol in the human thymus. Am. J. Obstet. Gynecol. 149: 544–547. [DOI] [PubMed] [Google Scholar]
  152. Nordby, G. , Cassidy J. (1983) Seasonal effect on the variability of summer immunoglobulin levels. Hum. Biol. 55: 797–809. [PubMed] [Google Scholar]
  153. Oakeson, B.B. (1953) Cyclic changes in liver and spleen weight in migratory white‐crowned sparrows. Condor 55: 3–16. [Google Scholar]
  154. Oakeson, B.B. (1956) Liver and spleen weights in migratory white‐crowned sparrows. Condor 58: 3–16. [Google Scholar]
  155. O'leary, A. (1990) Stress, emotion, and human immune function. Psychol. Bull. 108: 363–382. [DOI] [PubMed] [Google Scholar]
  156. Olcese, J. , Reuss S. (1986) Magnetic field effects on pineal gland melatonin synthesis: Comparative studies on albino and pigmented rodents. Brain Res. 369: 365–368. [DOI] [PubMed] [Google Scholar]
  157. Ownby, H.E. , Frederick J., Mortensen R. F., Ownby D. R., Russo J. (1986) Seasonal variation in tumor size at diagnosis and immunologic responses in human breast cancer. Invasion Metastasis 6: 246–256. [PubMed] [Google Scholar]
  158. Paavonen, T. , Andersson L. C. (1985) The oestrogen antagonists, tamoxifen and FC‐1157a, display oestrogen like effects on human lymphocyte functions in vitro. Clin. Exp. Immunol. 61: 467–474. [PMC free article] [PubMed] [Google Scholar]
  159. Pang, C.S. , Brown G.M., Tang P. L., Cheng K. M., Pang S. F. (1993) 2[125I]iodomelatonin binding sites in the lung and heart: a link between the photoperiodic signal, melatonin, and the cardiopulminary system. Biol. Signals 2: 228–236. [DOI] [PubMed] [Google Scholar]
  160. Pang, C.S. , Pang S. F. (1992) High affinity specific binding of 2‐[I]iodomelatonin by spleen membrane preparations of chicken. J. Pineal Res. 12: 167–173. [DOI] [PubMed] [Google Scholar]
  161. Persengiev, S. , Patchev V., Velev B. (1991) Melatonin effects on thymus steroid receptors in the course of primary antibody responses: significance of circulating gluccocorticoid levels. Int. J. Biochem. 23: 1487–1489. [DOI] [PubMed] [Google Scholar]
  162. Pioli, C , Carleo C., Nistico G., Doria G. (1993) Melatonin increases antigen presentation and amplifies specific and nonspecific signals for t‐cell proliferation. Int. J. Immunopharmacol. 15: 463–468. [DOI] [PubMed] [Google Scholar]
  163. Poffebbarger, M. , Fuller G. M. (1976) Is melatonin a microtubule inhibitor Exp. Cell Res. 103: 135–141. [DOI] [PubMed] [Google Scholar]
  164. Poon, A.M. , Liu Z. M., Pang C. S., Pang S. F. (1994) Evidence for a direct action of melatonin on the immune system. Biol. Signals 3: 107–117. [DOI] [PubMed] [Google Scholar]
  165. Poon, A.M. , Liu Z. M., Tang F., Pang S. F. (1994) Cortisol decreases 2[125I] iodomelatonin binding sites in the duck thymus. Eur. J. Endocrinol. 130: 320–324. [DOI] [PubMed] [Google Scholar]
  166. Poon, A.M. , Pang S. F. (1992) [125I]Iodomelatonin binding sites in spleens of guinea pigs. Life Sci. 50: 1719–1726. [DOI] [PubMed] [Google Scholar]
  167. Rafii‐El‐Idrissi, M. , Calvo J. R., Pozo D., Harmouch A., Guerrero J. M. (1995) Specific binding of 2‐[125I]iodomelatonin by rat splenocytes: characterization and its role on regulation of cyclic AMP production. J. Neuroimmunol. 57: 171–178. [DOI] [PubMed] [Google Scholar]
  168. Rasmussen, K.R. , Martin E. G., Healey M. C. (1993) Effects of dehydroepiandrosterone in immuno suppressed rats infected with Cryptosporidium parvum . J. Parasitol. 79: 364–370. [PubMed] [Google Scholar]
  169. Ratajczak, H.V. , Thomas P. T., Sothern R. B., Vollmuch T., Heck J. D. (1993) Evidence for genetic basis of seasonal differences in antibody formation between two mouse strains. Chronobiol. Int. 10: 383–394. [DOI] [PubMed] [Google Scholar]
  170. Reber, P.M. (1993) Prolactin and immunomodualtion. Am J. Med. 95: 637–644. [DOI] [PubMed] [Google Scholar]
  171. Reiter, R.J. (1991) Melatonin: the chemical expression of darkness. Mol. Cell. Endocrinol. 79: C 153–158. [DOI] [PubMed] [Google Scholar]
  172. DEL Rey, A. , Besedovsky H., Sorkin E. (1984) Endogenous blood levels of corticosterone control the immunologic cell mass and B‐cell activity in mice. J. Immunol. 133: 572–575. [PubMed] [Google Scholar]
  173. Riddle, O. (1924) Studies on the physiology of reproduction in birds. XIX. A hitherto unknown function of the thymus. Am. J. Physiol. 68: 557–580. [Google Scholar]
  174. Riddle, O. (1928) Sex and seasonal differences in weight of liver and spleen. Proc. Soc. Exp. Biol. Med. 25: 474–476. [Google Scholar]
  175. Rosen, L.N. , Livingstone I. R., Rosenthal N. E. (1991) Multiple sclerosis and latitude: A new perspective on an old association. Med. Hypoth. 36: 376–378. [DOI] [PubMed] [Google Scholar]
  176. Saarela, S. , Reiter R. J. (1994) Function of melatonin in thermoregulatory processes. Life Sci. 54: 295–311. [DOI] [PubMed] [Google Scholar]
  177. Sabharwal, P. , Glaser R., Lafuse W., Varma S., Liu Q., Arkins S., Kooijman R., Kutz L., Kelley K. W., Malarkey W. B. (1992) Prolactin synthesized and secreted by human peripheral blood mononuclear cells: an autocrine growth factor for lymphoproliferation. Proc. Nat. Acad. Sci. 89: 7713–7716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  178. Sankila, R. , Joensuu H., Pukkala E., Toikkanen S. (1993) Does the month of diagnosis affect survival of cancer patients Br. J. Cancer 67: 838–841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  179. Sasson, S. M. MAYER (1981) Antiglucocorticoid activity of androgens in rat thymus lymphocytes. Endocrinology 108: 760–766. [DOI] [PubMed] [Google Scholar]
  180. Schuurs, A.H.W.M. , Verheul H.A.M. (1990) Effects of gender and sex steroids on the immune response. J. Steroid Bio-chem. 35: 157–172. [DOI] [PubMed] [Google Scholar]
  181. Sealander, J.A. , Bickerstaff L. K. (1967) Seasonal changes in reticulocyte number and in relative weights of the spleen, thymus, and kidneys in the northern red‐backed mouse. Can. J. Zool. 45: 253–260. [DOI] [PubMed] [Google Scholar]
  182. Shifrine, M. , Rosenblatt L. S., Taylor N., Hetherington N. W., Matthews V. J., Wilson ED. (1980a) Seasonal variations in lectin‐induced lymphocyte transformation in beagle dogs. J. Interdiscipl. Cycle Res. 11: 219–231. [Google Scholar]
  183. Shifrine, M. , Taylor N., Rosenblatt L. S., Wilson F. (1980b) Seasonal variation in cell mediated immunity of clinically normal dogs. Exp. Hemat. 8: 318–326. [PubMed] [Google Scholar]
  184. Shivatcheva, T.M. , Hadjioloff A. I. (1987a) Seasonal involution of gut‐associated lymphoid tissue of the European ground squirrel. Dev. Comp. Immunol. 11: 791–799. [DOI] [PubMed] [Google Scholar]
  185. Shivatcheva, T.M. , Hadjioloff A. I. (1987b) Seasonal involution of the splenic lymphoid tissue of the European ground squirrel. Arkhiv. Anat. Gist. Embriol. 92: 48–53. [DOI] [PubMed] [Google Scholar]
  186. Sidky, Y.A. , Hayward J. S., Ruth R. F. (1972) Seasonal variations of the immune response of ground squirrels kept at 22–24°C. Can. J. Physiol. 50: 203–206. [DOI] [PubMed] [Google Scholar]
  187. Skwerer, R.G. , Jacobsen F. M., Duncan C. C., Kelley K. A., Sack D. A., Tamarkin L., Gaist RA., Kasper S., Rosenthal N. E. (1988) Neurobiology of seasonal affective disorder and phototherapy. J. Biol. Rhythms 3: 135–154. [DOI] [PubMed] [Google Scholar]
  188. Sonenshine, D.E. , Bozeman F. M., Williams M. S., Masiello S. A., Chadwick D. R, Stocks N. I., Lauer D. M., Elisberg B. L. (1978) Epizootiology of epidemic typhus (Rickettsi prowazekii) in flying squirrels. Am. J. Trop. Med. Hyg. 27: 339–349. [DOI] [PubMed] [Google Scholar]
  189. Stearns, S.C. (1976) Life‐history tactics: a review of the ideas. Q. Rev. Biol. 51: 3–47. [DOI] [PubMed] [Google Scholar]
  190. Sthoeger, Z.M. , Chiorazzi N., Lahita R. G. (1988) Regulation of the immune response by sex hormones. I. In vitro effects of estradiol and testosterone on pokeweed mitogen‐induced human B cell differentiation. J. Immunol. 141: 91–98. [PubMed] [Google Scholar]
  191. Stimson, W.H. (1988) Oestrogen and human T lymphocytes: presence of specific receptors in the T‐suppressor/cytotoxic subset. Scand. J. Immunol. 28: 345–350. [DOI] [PubMed] [Google Scholar]
  192. Stone, W.H. (1956) The J substance of Cattle III. Seasonal variation of the naturally occurring isoantibodies for the J substance. J. Immunol. 77: 269–376. [PubMed] [Google Scholar]
  193. Stoop, J. , Zegers B., Sander R, Ballieux R. (1969) Serum immunoglobulin levels in healthy children and adults. Clin. Exp. Immunol. 4: 101–112. [PMC free article] [PubMed] [Google Scholar]
  194. Suzuki, T , Suzuki N., Danes R.A., Engleman E. G. (1991) Dehydroepiandrosterone enhances IL2 production and cytotoxic effector function of human T cells. Clin. Immunol. Immunopathol. 61: 202–211. [DOI] [PubMed] [Google Scholar]
  195. Talleklint, L. , Jaenson T. G., Mather T. N. (1993) Seasonal variation in the capacity of the bank vole to infect larval ticks (Acari: Ixodidae) with Lyme's disease spirochete, Borrelia burgdorferi . J. Med. Entymol. 30: 812–815. [DOI] [PubMed] [Google Scholar]
  196. Tang, F , Hsieh A.C.L., Lee C. P., Baconshone J. (1984) Interaction of cold and starvation in the regulation of plasma corticosterone levels in the male rat. Horm. Metab. Res. 16: 445–448. [DOI] [PubMed] [Google Scholar]
  197. Thealander, T.G. , Hviid L., Abu‐Zeid Y. A., N.H., Abdulhadi , Saeed B. O., Jakobsen RH., Reimert CM., Jepsen S., Bayoumi R. A., Jensen J. B. (1990) Reduced cellular immune reactivity in healthy individuals during the malaria transmission season. Immunol. Lett. 25: 237–242. [DOI] [PubMed] [Google Scholar]
  198. Turek, F.W. , Desjardins C., Menaker M. (1976) Differential effects of melatonin on the testes of photoperiodic and nonphotoperiodic rodents. Biol. Reprod. 15: 94–97. [DOI] [PubMed] [Google Scholar]
  199. Valentine, G.L. , Kirkpatrick R. L. (1970) Seasonal changes in reproductive and related organs in the pine vole, Microtus pinetorum, in southwestern Virginia. J. Mammal. 51: 553–560. [PubMed] [Google Scholar]
  200. Vaughan, M.K. , Hubbard G. B., Champney T. H., Vaughan G. M., Little J. C., Reiter R. J. (1987) Splenic hypertrophy and extrameduallry hematopoiesis induced in male Syrian hamsters by short photoperiod or melatonin injections and reversed by melatonin pellets or pinealectomy. Am. J. Anat. 179: 131–136. [DOI] [PubMed] [Google Scholar]
  201. Vermeulen, M , Palermo M, Giordano M. (1993) Neonatal pinealectomy impairs murine antibody‐dependent cellular cytotoxity. J. Neuroimmunol. 43: 97–101. [DOI] [PubMed] [Google Scholar]
  202. Vindevogel, H. , Debruyne H., Pastoret P. P. (1985) Observation of pigeon herpesvirus 1 re‐excretion during the reproduction period in conventionally reared homing pigeons. J. Comp. Pathol. 95: 105–112. [DOI] [PubMed] [Google Scholar]
  203. Vollrath, L. , Huesgen A., Seidel A., Manz B., Pollow K. (1989) Serotonin and melatonin contents in the pineal glands from different stocks and strains of laboratory rats. Z. Versuchstierkd. 32: 57–63. [PubMed] [Google Scholar]
  204. Vriend, J. , Lauber J. K. (1973) Effects of light intensity, wavelength and quanta on gonads and spleen of the deer mouse. Nature 244: 37–38. [DOI] [PubMed] [Google Scholar]
  205. Webb, S.M. , Champney T. H., Lewinski A. K., Reiter R. J. (1985) Photoreceptor damage and eye pigmentation: Influence on the sensitivity of rat pineal N‐acetyltransferase activity and melatonin levels to light at night. Neuroendocrinology, 40: 205–209. [DOI] [PubMed] [Google Scholar]
  206. Weusten, J.J. , Blankenstein M. A., Gmelig‐Meyling F. H., Schuurman H.J., Kater L., Thijssen J. H. (1986) Presence of oestrogen receptors in human blood mononuclear cells and thymocytes. Acta Endocrinol. 112: 409–414. [DOI] [PubMed] [Google Scholar]
  207. Winston, M. , Johnson E., Kelleher J. K., Banerjee S., Margulis L. (1974) Melatonin: cellular effects on live stensors correlated with the inhibition of choline‐binding on microtubule protein. Cytobios 9: 237–243. [PubMed] [Google Scholar]
  208. Wurtman, R.J. , Weisel J. (1969) Environmental lighting and neuroendocrine function: Relationship between spectrum of light source and gonadal growth. Endocrinology 85: 1218–1221. [DOI] [PubMed] [Google Scholar]
  209. Zapata, A.G. , Varas A., Torroba M. (1992) Seasonal variations in the immune system of lower vertebrates. Immunol. Today 13: 142–147. [DOI] [PubMed] [Google Scholar]

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