Role of Melatonin in Modulation of Immune Status of Pregnant Female Indian Short Nosed Fruit Bat Cynopterus sphinx
DOI:
https://doi.org/10.18311/jer/2016/18089Keywords:
Cynopterus sphinx, Immunity, Melatonin, Pregnancy.Abstract
Pregnancy is associated with profound immunological changes that are characterized by a strong activation of certain components of the innate immune defense and a down-regulation of adaptive immune functions. This shift in balance of the immune system towards an innate dominance is thought to be important for the maintenance of pregnancy. Based on our observation in the short nosed fruit bat Cynopterus sphinx, a seasonal breeder, we show for the first time that melatonin injection to the pregnant females significantly increases lymphocyte proliferation of spleen and consequently the circulating level of lymphocytes and percent stimulation ratio of splenocytes, thereby improving immune status during pregnancy. We have reported earlier that during pregnancy melatonin level increases significantly which in turn might improve the maternal immunity. Towards establishing this inference we used a physiological dose of p-chlorophenylalanine (p-CPA), an indirect antagonist of melatonin, which reduced circulatory melatonin level and thereby reduced the immune status. It is conceived that specific immune adaptation is conveyed to the fetus through placental transfer of melatonin thereby controlling fetal immunity as well. This could be an adaptation during pregnancy to protect the mother from various external threats.Downloads
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Billington WD. The normal fetomaternal immune relationship.Baillieres Clin Obstet Gynaecol. 1992; 6(3):417–38 https://doi.org/10.1016/S0950-3552(05)80004-5
Dudley DJ, Chen CL, Mitchell MD, Daynes RA, Araneo BA. Adaptive immune responses during murinepregnancy: pregnancy induced regulation of lymphokine production by activated T lymphocytes. Am J Onstet Gynecol. 1993; 168(4):1155–63. https://doi.org/10.1016/0002-9378(93)90361-L
Luppi P. How immune mechanisms are affected by pregnancy. Vaccine. 2003; 21(24):3352–7. https://doi.org/10.1016/S0264-410X(03)00331-1
Sacks G, Sargent I, Redman C. An innate view of human pregnancy. Immunol Today. 1999; 20(3):114–8. https://doi.org/10.1016/S0167-5699(98)01393-0
Shibuya T, Izuchi K, Kuroiwa A, Okabe N, Shirakawa K. Study on nonspecific immunity in pregnant women: Increased chemiluminescence response of peripheral blood phagocytes. Am J Reprod Immunol Microbiol. 1987; 15(1):19–23. https://doi.org/10.1111/ j.1600 -0897 .1987.tb00144.x PMid:3425776
Wegmann TG, Lin H, Guilbert L, Mosmann TR.Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today. 1993; 14(7):353–6. https://doi.org/10.1016/0167-5699(93)90235-D
Saafela S, Reiter RJ. Function of melatonin in thermoregulatory processes. Life Sci. 1994; 54(5):295–311. https://doi.org/10.1016/0024-3205(94)00786-1
Reiter RJ. Pineal metabolism: Cell biology of its synthesis and its physiological interactions. Endocrine Rev. 1991; 12(2):151–80. https://doi.org/10.1210/ edrv-12- 2- 151 PMid:1649044
Gupta S. Recent developments in clinical immunology.Allergy Proc. 1990; 11(3):105–7. https://doi.org/10.2500/108854190778880204 PMid:2370001
Maestroni GJ. The immunoneeuroendocrine role of melatonin. J Pineal Res. 1993; 14(1):1–10. https://doi.org/10.1111/j.1600-079X.1993.tb00478.x PMid:8483103 11. Maier SF, Watkins LR, Fleshner M. Psychoneuroimmunology.The interface between behavior, brain and immunity.Am Psychol. 1994; 49(12):1004–17. https://doi.org/10.1037/0003-066X.49.12.1004 PMid:7818221
Pauly JL, Sokal JE. A simplified technique for in vitro studies of lymphocyte reactivity. Proc Soc Exp Biol Med. 1972; 140(1):40–4. https://doi.org/10.3181/00379727-140-36391
Rollag MD, Niswender GD. Radioimmunoassay of serum concentrations of melatonin in sheep exposed to different light regimes. Endocrinology. 1976; 98:482–8. https://doi.org/10.1210/endo-98-2-482 PMid:1248456
Brunning Jl, Knitz BL. Computational handbook of statistics.2nd ed. Chicago: Scott Foresman; 1977
Ehrlich P. Collected Papers Z. Hygiene 12, 183. 1892; 2:31– 44.
Brambell FWR. The transmission of passive immunity from mother to young. North Holland, Amterdam; 1970.
Heller J, Holzer G, Schimrigk K. Immunological differentiation between neuroborreliosis and multiple sclerosis.J Neurol. 1990; 237(8):465–70. https://doi.org/10.1007/ BF00314763 PMid:2074447
Malanchere E, Huetz F, Coutinho A. Maternal IgG stimulates B lineage cell development in the progeny. Eur J Immunol. 1997; 27(3):788–93. https://doi.org/10.1002/ eji.1830270330 PMid:9079823
Stirrat GM. Pregnancy and immunity. BMJ. 1994; 308(6941):1385–6. https://doi.org/10.1136/bmj. 308. 6941.1385 PMid:8019246 PMCid:PMC2540390
Matthiesen L, Berg G, Ernerudh J, Hakansson L.Lymphocyte subsets and mitogen stimulation of blood lymphocytes in normal pregnancy. Am J Reprod Immunol.1996; 35(2):70–9. https://doi.org/10.1111/j.1600-0897.1996. tb00010.x PMid:8839133
Faas MM, Moes H, de Vos P. Monocyte cytokine production during pregnancy. J Leukoc Biol. 2004; 75(2):153–4.https://doi.org/10.1189/jlb.0903419 PMid:14694184
van Kampen C, Mallard BA. Effects of peripartum stress and health on circulating bovine lymphocyte subsets. Vet Immunol Immunopathol. 1997; 59(1-2):79–91. https://doi.org/10.1016/S0165-2427(97)00069-X
Glassman AB, Bennet CE, Christopher JB, Self S. Immunity during pregnancy: Lymphocyte subpopulations and mitogen responsiveness. Ann Clin Lab Sci. 1985; 15(5):357–62.PMid:2865928
Chacin MFL, Hansen PJ, Drost M. Effects of stage of the estrous cycle and steroid treatment on uterine immunoglobin content and polymorphonuclear leukocytes incattle. Theriogenology. 1990; 34(6):1169–84. https://doi.org/10.1016/S0093-691X(05)80016-0
Rai S, Haldar C. Pineal control of immune status and haematological changes in blood and bone marrow of male squirrels (Funambulus pennanti) during their reproductively active phase. Comp Biochem Physiol (C). 2003; 136:319–28.
Maestroni GJ. The photoperiod transducer melatonin and the immune-hematopoetic system. J Photochem Photobiol B. 1998; 43(3):186–92. https://doi.org/10.1016/S10111344(98)00107-9
Skwarlo-Sonta K. Melatonin in immunity: Comparative aspects. Neuro- Endocrinol Lett. 2002; 1:61–6.
Haldar C, Singh SS. Seasonal changes in melatonin and immunological adaptations in birds. J Endocrinol Reprod.2001; 5(1,2):49–63.
Nelson RJ, Drazen DL. Melatonin mediates seasonal adjustments in immune function. Reprod Nutr Dev. 1999; 39(3):383–98. https://doi.org/10.1051/rnd:19990310
Haldar C, Singh R, Guchhait P. Relationship between the annual rhythms in melatonin and immune system status in the tropical palm squirrel, Funambulus pennant.Chronobiol Int. 2001; 18(1):61–9. https://doi.org/10.1081/ CBI-100001174 PMid:11247114
Rai S, Haldar C, Singh SS. Trade off between L-thyroxin and melatonin regulation in immune regulation of Indian palm squirrel, Funambulus pennanti during reproductively inactive phase. J Neuroendocrinol. 2005; 182:103–10. https:// doi.org/10.1159/000091034 PMid:16424677
Guerrero JM, Reiter RJ. A brief survey of pineal glandimmune system interrelationships. Endocr Res. 1992; 18(2):91–113. https://doi.org/10.1080/07435809209035401
Coroleo MC, Frasca D, Nistigo G, Doria G. Melatonin as immunomodulatory in immunodeficient mice.Immunopharmacol. 1992; 23:81–9. https://doi.org/10.1016/0162 -3109 (92)90031-7
Yu Q, Miller SC, Osmond DG. Melatonin inhibits apoptosis during early B-cell development in mouse bone marrow. J Pineal Res. 2000; 29(2):86–93. https://doi.org/10.1034/ j.1600-079X.2000.290204.x PMid:10981821
Calvo JR, Raffi-el-Idrissi M, Pozo D, Guerrero JM.Immunomodulatory role of melatonin: Specific binding sites in human and rodent lymphoid cells. J Pineal Res. 1995; 18(3):119–26. https://doi.org/10.1111/j.1600079X.1995.tb00149.x PMid:7562368
Pang CS, Pang SF. High affinity specific binding of 2-[125I] iodomelatonin by spleen membrane preparations of chicken. J Pineal Res. 1992; 12(4):167–73. https://doi.org/10.1111/j.1600-079X.1992.tb00044.x
Lopez-Gonzales MA, Calvo JR, Osuna C, Guerrero JM.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. 1992; 12(3):97–104. https:// doi.org/10.1111/j.1600-079X.1992.tb00034.x
Martini-Cacao A, Lopez-Gonzalez Ma, Reiter RJ, Calvo JR, Guerrero JM. Binding of 2-[125I] melatonin by rat thymus membranes during postnatal development. Immunol Lett. 1992; 36(1):59–64. https://doi.org/10.1016/0165-2478(93)90069-E
Poon AM, Pang SF. Constant light exposure increases 2-[125I] iodomelatonin binding sites in the guinea pig spleen. Neurosci Lett. 1992; 146(1):41–4. https://doi.org/10.1016/0304-3940(92)90167-6
Rafii-el-Idrissi M, Calvo JR, Pozo D, Harmouch A, Guerrero JM. Specific binding of 2-[125I] iodomelatonin by rat splenocytes: characterization and its role on regulation of cyclic AMP production. J Neuroimmunol. 1995; 57(1-2):171–8.https://doi.org/10.1016/0165-5728(94)00182-N
Yu CL, Lin WM, Liao TS, Tsai CY, Sun KH, Chen KH.Tamm-Horsfall Glycoprotein (THG) purified from normal human pregnancy urine increases phagocytosis, complement receptor expressions and arachidonic acid metabolism of polymorphonuclear neutrophils.Immunopharmacology. 1992; 24(3):181–90. https://doi.org/10.1016/0162-3109(92)90074-M
Nelson RJ, Demas GE. Seasonal changes in immune function. Q Rev Biol. 1996; 71(4):511–48. https://doi.org/10.1086/419555
John J. The avian spleen: a neglected organ-Q. Rev Biol.1994; 69:327–51. https://doi.org/10.1086/418649
McCruden AB, Stimpson WH. Sex hormones and immune function. Ader R, editor. Psycho-neuroimmunology.New York: Academic Press; 1991. p. 457–93. https://doi.org/10.1016/B978-0-12-043780-1.50021-X