Microbial Source of Melatonin and Its Clinical Aspects

  • Sanjay Kumar
  • Brendan Patrick Mulligan
  • Shreesh Ojha
  • Alex Tinson
Chapter

Abstract

Melatonin chemically known as N-acetyl-5-methoxytryptamine is a small physiological compound of diversified functions. Melatonin has been found in phylogenetically different taxa of bacteria, unicellular eukaryote, microalgae, plants, fungi, and animals. Identification of melatonin in many of these microorganisms is missing, and its function is rarely known. Although, melatonin in microorganisms is not essentially involved in circadian process, rather, it exhibits antioxidant property also and may protect chlorophyll pigment to damage from stress and free radicals. Mostly, the pathway for melatonin synthesis in microorganisms shows similarity with vertebrates. Investigation on melatonin in some organisms allows more concrete discussion about their possible role. The various functions of melatonin in human including sleep and regulation of circadian rhythm has been well characterized. Here, we have focused on the mechanism of immune regulatory, antioxidant, and scavenging property of melatonin during pathogenesis caused by fungi, bacteria, and virus. This article will provide a view on microbial sources and possible therapeutic aspects of melatonin in future.

Keywords

Melatonin Circadian process Immune regulation Antioxidant property Scavenger of free radicals 

Notes

Acknowledgment

The authors thank the Department of President Affairs (DOPA), Abu Dhabi, UAE, for financial support and facilities. We also thank Dr. Sudhuman Singh, a postdoctoral fellow, Haifa University, Israel, for providing the articles.

References

  1. Agorastos A, Huber CG (2011) The role of melatonin in glaucoma: implications concerning pathophysiological relevance and therapeutic potential. J Pineal Res 50:1–7. doi: 10.1111/j.1600-079X.2010.00816.x CrossRefPubMedGoogle Scholar
  2. Ancín-Azpilicueta C, Gonzaĺez-Marco A, Jimeńez-Moreno N (2008) Current knowledge about the presence of amines in wine. Crit Rev Food Sci Nutr 48:257–275. doi: 10.1080/10408390701289441 CrossRefPubMedGoogle Scholar
  3. Arevalo-Villena M, Bartowsky EJ, Capone D, Sefton MA (2010) Production of indole by wine-associated microorganisms under oenological conditions. Food Microbiol 27:685–690. doi: 10.1016/j.fm.2010.03.011 CrossRefPubMedGoogle Scholar
  4. Barrett BK, Newbolt L, Edwards S (1994) The membrane destabilizing action of the antibacterial agent chlorohexidine. FEMS Microbiol Lett 119:249–253. doi: 10.1111/j.1574-6968.1994.tb06896 CrossRefGoogle Scholar
  5. Ben-Nathan D, Maestroni GJ, Lustig S, Conti A (1995) Protective effects of melatonin in mice infected with encephalitis viruses. Arch Virol 140:223–230. doi: 10.1007/BF01309858 CrossRefPubMedGoogle Scholar
  6. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073. doi: 10.1126/science.1067262 CrossRefPubMedGoogle Scholar
  7. Blask DE, Sauer LA, Dauchy RT (2002) Melatonin as a chronobiotic/anticancer agent: cellular, biochemical, and molecular mechanisms of action and their implications for circadian-based cancer therapy. Curr Top Med Chem 2:113–132. doi: 10.2174/1568026023394407
  8. Blask DE, Dauchy RT, Sauer LA (2005) Putting cancer to sleep at night: the neuroendocrine/circadian melatonin signal. Endocrine 27:179–188. doi: 10.1385/ENDO:27:2:179 CrossRefPubMedGoogle Scholar
  9. Bochkov DV, Sysolyatin SV, Kalashnikov AI, Surmacheva IA (2012) Shikimic acid: review of its analytical, isolation, and purification techniques from plant and microbial sources. J Chem Biol 5:5–17. doi: 10.1007/s12154-011-0064-8 CrossRefPubMedGoogle Scholar
  10. Boga JA, Coto-Montes A, Rosales-Corral SA, Tan DX, Reiter RJ (2012) Beneficial actions of melatonin in the management of viral infections: a new use for this “molecular handyman”. Rev Med Virol 22:323–338. doi: 10.1002/rmv.1714 CrossRefPubMedGoogle Scholar
  11. Bonilla E, Valero N, Pons H, Chacín-Bonilla L (1997) Melatonin protects mice infected with Venezuelan equine encephalomyelitis virus. Cell Mol Life Sci 53:430–434. doi: 10.1007/s000180050051 CrossRefPubMedGoogle Scholar
  12. Byeon Y, Lee HY, Lee K, Park S, Back K (2014) Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT. J Pineal Res 56:107–114. doi: 10.1111/jpi.12103 CrossRefPubMedGoogle Scholar
  13. Cannom RR, French SW, Johnston D, Edwards JE Jr, Filler SG (2002) Candida albicans stimulates local expression of leukocyte adhesion molecules and cytokines in vivo. J Infect Dis 186:389–396. doi: 10.1086/341660 CrossRefPubMedGoogle Scholar
  14. Chastre J, Trouillet JL (2000) Problem pathogens Pseudomonas aeruginosa and Acinetobacter. Semin Respir Infect 15:287–298. doi: 10.1053/srin.2000.20944 CrossRefPubMedGoogle Scholar
  15. Chen G, Huo Y, Tan DX, Liang Z, Zhang W, Zhang Y (2003) Melatonin in Chinese medicinal herbs. Life Sci 73:19–26. doi: 10.1016/S0024-3205(03)00252-2 CrossRefPubMedGoogle Scholar
  16. Christin L, Wysong T, Meshulam R, Hastey E, Simons ER, Diamond R (1998) Human platelets damage Aspergillus fumigates hyphae and may supplement killing neutrophils. Infect Immun 66:1181–1189PubMedPubMedCentralGoogle Scholar
  17. Currier NL, Sun LZ, Miller SC (2000) Exogenous melatonin: quantitative enhancement in vivo of cells mediating nonspecific immunity. J Neuroimmunol 104:101–108. doi: 10.1016/S0165-5728(99)00271-4 CrossRefPubMedGoogle Scholar
  18. Dubbels R, Reiter RJ, Klenke E, Goebel A, Schnakenberg E, Ehlers C, Schiwara HW, Schloot W (1995) Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry. J Pineal Res 18:28–31. doi: 10.1111/j.1600-079X.1995.tb00136.x CrossRefPubMedGoogle Scholar
  19. Dubocovich ML, Markowska M (2005) Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 27:101–110. doi: 10.1385/ENDO:27:2:101 CrossRefPubMedGoogle Scholar
  20. Filler SG, Pfunder AS, Spellberg BJ, Spellberg JP, Edwards JE Jr (1996) Candida albicans stimulates cytokine production and leukocyte adhesion molecule expression by endothelial cells. Infect Immun 64:2609–2612PubMedPubMedCentralGoogle Scholar
  21. Fuhrberg B, Hardeland R, Poeggeler B, Behrmann G (1997) Dramatic rises of melatonin and 5-methoxytryptamine in Gonyaulax exposed to decreased temperature. Biol Rhythm Res 28:144–150. doi: 10.1076/brhm.28.1.144.12978 CrossRefGoogle Scholar
  22. Garcia-Maurino S, Pozo D, Calvo JR, Guerrero JM (2000) Correlation between nuclear melatonin receptor expression and enhanced cytokine production in human lymphocytic and monocytic cell lines. J Pineal Res 29:129–137. doi: 10.1034/j.1600-079X.2000.290301.x CrossRefPubMedGoogle Scholar
  23. Giese MJ, Shum DC, Rayner SA, Mondino BJ, Berliner JA (2000) Adhesion molecule expression in a rat model of Staphylococcus aureus endophthalmitis. Invest Ophthalmol Vis Sci 41:145–153PubMedGoogle Scholar
  24. Gilad E, Laudon M, Matzkin H, Pick E, Sofer M, Braf Z, Zisapel N (1996) Functional melatonin receptors in the human prostate epithelial cells. Endocrinology 137:1412–1417. doi: 10.1210/en.137.4.1412 PubMedGoogle Scholar
  25. Gitto E, Pellegrino S, Gitto P, Barberi I, Reiter RJ (2009) Oxidative stress of the newborn in the pre- and postnatal period and the clinical utility of melatonin. J Pineal Res 46:128–139. doi: 10.1111/j.1600-079X.2008.00649.x CrossRefPubMedGoogle Scholar
  26. Gulcin I, Buyukokuroglu ME, Kufrevioglu OI (2003) Metal chelating and hydrogen peroxide scavenging effects of melatonin. J Pineal Res 34:278–281. doi: 10.1034/j.1600-079X.2003.00042.x CrossRefPubMedGoogle Scholar
  27. Hardeland R (2010) Melatonin metabolism in the central nervous system. Curr Neuropharmacol 8:168–181. doi: 10.2174/157015910792246244 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hardeland R, Balzer L, Poeggeler B, Fuhrberg B, Uria H, Behrmann G, Wolf R, Meyer TJ, Reiter RJ (1995) On the primary functions of melatonin in evolution: mediation of photoperiodic signals in a unicell, photooxidation and scavenging of free radicals. J Pineal Res 18:104–111. doi: 10.1111/j.1600-079X.1995.tb00147.x CrossRefPubMedGoogle Scholar
  29. Hardeland R, Pandi-Perumal SR, Poeggeler BM (2007) Melatonin in plants—Focus on a vertebrate night hormone with cytoprotective properties. Funct Plant Sci Biotechnol 1:32–45Google Scholar
  30. Helmeste D, Tang SW, Vu R (1998) Inhibition of platelet serotonin uptake by cytochrome P 450 inhibitors miconazole and econazole. Life Sci 62:2203–2208. doi: 10.1016/S0024-3205(98)00198-2 CrossRefPubMedGoogle Scholar
  31. Huletsky A, Giroux R, Rossbach V, Gagnon M, Vaillancourt M, Bernier M, Gagnon F, Truchon K, Bastien M, Picard FJ, van Belkum A, Ouellette M, Roy PH, Bergeron MG (2004) New real-time PCR assay for rapid detection of methicillin-resistant Staphylococcus aureus directly from specimens containing a mixture of staphylococci. J Clin Microbiol 42:1875–1884. doi: 10.1128/JCM.42.5.1875-1884.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ivanova EA, Bechtold DA, Dupré SM, Brennand J, Barrett P, Luckman SM, Loudon AS (2008) Altered metabolism in the melatonin-related receptor (GPR50) knockout mouse. Am J Physiol Endocrinol Metab 294:176–182. doi: 10.1152/ajpendo.00199.2007 CrossRefGoogle Scholar
  33. Jeong SH, Bae IK, Park KO, An YJ, Sohn SG, Jang SJ, Sung KH, Yang KS, Lee K, Young D, Lee SH (2006) Outbreaks of imipenemresistant Acinetobacter baumannii producing carbapenemases in Korea. J Microbiol 44:423–431PubMedGoogle Scholar
  34. Jiménez-Caliani AJ, Jiménez-Jorge S, Molinero P, Guerrero JM, Fernández-Santos JM, Martín-Lacave I, Osuna C (2005) Dual effect of melatonin as proinflammatory and antioxidant in collagen-induced arthritis in rats. J Pineal Res 38:93–99. doi: 10.1111/j.1600-079X.2004.00175.x CrossRefPubMedGoogle Scholar
  35. Lass-Flörl C, Fuchs D, Ledochowski M, Speth C, Dierich MP, Würzner R (2003) Antifungal properties of 5-hydroxytryptamine (serotonin) against Candida species in vitro. J Med Microbiol 52:169–171. doi: 10.1099/jmm.0.04987-0 CrossRefPubMedGoogle Scholar
  36. Laudon M, Gilad E, Matzkin H, Braf Z, Zisapel N (1998) Putatitive melatonin receptors in benign prostate tissue. J Clin Endocrinol Metab 81:1336–1342. doi: 10.1210/jcem.81.4.8636329 Google Scholar
  37. Limson J, Nyokong T, Daya S (1998) The interaction of melatonin and its precursors with aluminium, cadmium, copper, iron, lead, and zinc: an adsorptive voltammetric study. J Pineal Res 24:15–21. doi: 10.1111/j.1600-079X.1998.tb00361.x CrossRefPubMedGoogle Scholar
  38. Liu Y, Tsinoremas NF, Johnson CH, Lebedeva NV, Golden SS, Ishiura M, Kondo T (1995) Circadian orchestration of gene expression in cyanobacteria. Genes Dev 9:1469–1478. doi: 10.1101/gad.9.12.1469 CrossRefPubMedGoogle Scholar
  39. Maestroni GJM (1995) T-helper 2 lymphocytes as peripheral target of melatonin signaling. J Pineal Res 18:84–89. doi: 10.1111/j.1600-079X.1995.tb00144.x CrossRefPubMedGoogle Scholar
  40. Maestroni GJM (2001) The immunotherapeutic potential of melatonin. Expert Opin Investig Drugs 10:467–476. doi: 10.1517/13543784.10.3.467 CrossRefPubMedGoogle Scholar
  41. Mailliet F, Ferry G, Vella F, Berger S, Cogé F, Chomarat P, Mallet C, Guénin SP, Guillaumet G, Viaud-Massuard MC, Yous S, Delagrange P, Boutin JA (2005) Characterization of the elatoninergic MT3 binding site on the NRH: quinone oxidoreductase 2 enzyme. Biochem Pharmacol 71:74–88. doi: 10.1016/j.bcp.2005.09.030 CrossRefPubMedGoogle Scholar
  42. Manchester LC, Poeggeler B, Alvares FL, Ogden GB, Reiter RJ (1995) Melatonin immunoreactivity in the photosynthetic prokaryote Rhodospirillum rubrum: implications for an ancient antioxidant system. Cell Mol Biol Res 41:391–395PubMedGoogle Scholar
  43. McGuire NL, Kangas K, Bentley GE (2011) Effects of melatonin on peripheral reproductive function: regulation of testicular GnIH and testosterone. Endocrinology 152:3461–3470. doi: 10.1210/en.2011-1053 CrossRefPubMedGoogle Scholar
  44. Miller SC, Pandi-Perumal SR, Esquifino AI, Cardinali DP, Maestroni GJ (2006) The role of melatonin in immuno-enhancement: potential application in cancer. Int J Exp Pathol 87:81–87. doi: 10.1111/j.0959-9673.2006.00474.x CrossRefPubMedPubMedCentralGoogle Scholar
  45. Moore RY (1997) Circadian rhythms: basic neurobiology and clinical applications. Annu Rev Med 48:253–266. doi: 10.1146/annurev.med.48.1.253 CrossRefPubMedGoogle Scholar
  46. Motilva V, García-Mauriño S, Talero E, Illanes M (2011) New paradigms in chronic intestinal inflammation and colon cancer: role of melatonin. J Pineal Res 51:44–60. doi: 10.1111/j.1600-079X.2011.00915.x CrossRefPubMedGoogle Scholar
  47. Nakamura Y, Tamura H, Kashida S, Takayama H, Yagamata Y, Karube A, Sugino N, Kato H (2001) Changes of serum melatonin level and its relationship to feto-placental unit during pregnancy. J Pineal Res 30:29–33. doi: 10.1034/j.1600-079X.2001.300104.x CrossRefPubMedGoogle Scholar
  48. Olecese J (2007) Melatonin effects on uterine physiology. In: Pandi-Perumal SR, Cardinali DP (eds) Melatonin: from molecules to therapy. Nova Science, New York, pp 205–225Google Scholar
  49. Park SY, Jang WJ, Yi EY, Jang JY, Jung Y, Jeong JW, Kim YJ (2010) Melatonin suppresses tumor angiogenesis by inhibiting HIF-1alpha stabilization under hypoxia. J Pineal Res 48:178–184. doi: 10.1111/j.1600-079X.2009.00742.x CrossRefPubMedGoogle Scholar
  50. Park S, Lee DE, Jang H, Byeon Y, Kim YS, Back K (2013) Melatonin-rich transgenic rice plants exhibit resistance to herbicide-induced oxidative stress. J Pineal Res 54:258–263. doi: 10.1111/j.1600-079X.2012.01029.x CrossRefPubMedGoogle Scholar
  51. Reinhart K, Bayer O, Brunkhorst F, Meisner M (2002) Markers of endothelial damage in organ dysfunction and sepsis. Crit Care Med 30:302–312. doi: 10.1097/00003246-200205001-00021 CrossRefGoogle Scholar
  52. Reiter RJ (1997) Antioxidant action of melatonin. Adv Pharmacol 38:103–117. doi: 10.1016/S1054-3589(08)60981-3 CrossRefPubMedGoogle Scholar
  53. Reiter RJ, Tang J, Garcia JJ, Munoz-Hoyos A (1997a) Pharmacological actions of melatonin in oxygen radical pathophysiology. Life Sci 60:2255–2271. doi: 10.1016/S0024-3205(97)00030-1 CrossRefPubMedGoogle Scholar
  54. Reiter RJ, Carneiro RC, Oh CS (1997b) Melatonin in relation to cellular antioxidative defense mechanisms. Horm Metab Res 29:363–372. doi: 10.1055/s-2007-979057 CrossRefPubMedGoogle Scholar
  55. Reiter RJ, Calvo JR, Karbownik M, Qi W, Tan DX (2000) Melatonin and its relation to the immune system and inflammation. Ann N Y Acad Sci 917:376–386. doi: 10.1111/j.1600-079X.2004.00165.x CrossRefPubMedGoogle Scholar
  56. Reiter RJ, Gultekin F, Flores LJ, Terron MP, Tan DX (2006) Melatonin: potential utility for improving public health. Kor Hek 5:131–158. doi: 10.5455/pmb.20060502131 Google Scholar
  57. Reiter RJ, Tan DX, Rosales-Corral S, Manchester LC (2013) The universal nature, unequal distribution and antioxidant functions of melatonin and its derivatives. Mini Rev Med Chem 13:373–384. doi: 10.2174/1389557511313030006 PubMedGoogle Scholar
  58. Reppert SM (1997) Melatonin receptors: molecular biology of a new family of G protein-coupled receptors. J Biol Rhythms 12:528–531. doi: 10.1177/074873049701200606 CrossRefPubMedGoogle Scholar
  59. Rodriguez-Naranjo MI, Gil-Izquierdo A, Troncoso AM, Cantos-Villar E, Garcia-Parrilla MC (2011) Melatonin is synthesised by yeast during alcoholic fermentation in wines. Food Chem 126:1608–1613. doi: 10.1016/j.foodchem.2010.12.038 CrossRefPubMedGoogle Scholar
  60. Rodriguez-Naranjo MI, Torija MJ, Mas A, Cantos-Villar E, Garcia-Parrilla Mdel C (2012) Production of melatonin by Saccharomyces strains under growth and fermentation conditions. J Pineal Res 53:219–224. doi: 10.1111/j.1600-079X.2012.00990.x CrossRefPubMedGoogle Scholar
  61. Salomonis N, Cotte N, Zambon AC, Pollard KS, Vranizan K, Doniger SW, Dolganov G, Conklin BR (2005) Identifying genetic networks underlying myometrial transition to labor. Genome Biol 12:1–6. doi: 10.1186/gb-2005-6-2-r12 Google Scholar
  62. Sauer LA, Dauchy RT, Blask DE (2001) Polyunsaturated fatty acids, melatonin, and cancer prevention. Biochem Pharmacol 61:1455–1462. doi: 10.1016/S0006-2952(01)00634-7 CrossRefPubMedGoogle Scholar
  63. Schlabritz-Loutsevitch N, Hellner N, Middendorf R, Muller D, Olcese J (2003) The human myometrium as a target for melatonin. J Clin Endocrinol Metab 88:908–913. doi: 10.1210/jc.2002-020449 CrossRefPubMedGoogle Scholar
  64. Shimada K (1995) Aerobic anoxygenic phototrophs. In: Blankenship RE, Madigen MT, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Publishers, Dordrecht, The Netherlands, pp 105–122Google Scholar
  65. Shioi Y, Watanabe K, Takamiya K, Garrido JL, Zapata M (1995) Separation of mono- and divinyl chlorophyll species by high-performance liquid chromatography using an octadecyl polyvinyl alcohol polymer column. Anal Biochem 231:225–229. doi: 10.1006/abio.1995.1524 CrossRefPubMedGoogle Scholar
  66. Shiu SYW, Yu ZH, Chow PH, Pang SF (1996) Putative melatonin receptors in the male reproductive tissues. Front Horm Res 21:90–100. doi: 10.3109/09513590903159649 CrossRefGoogle Scholar
  67. Shiu SYW, Li L, Wong JTY, Pang SF (1997) Biology of G-protein coupled melatonin receptors in the epididymis and prostate of mammals. Chin Med J 110:648–655PubMedGoogle Scholar
  68. Silla-Santos MH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231. doi: 10.1016/0168-1605(95)00032-1 CrossRefPubMedGoogle Scholar
  69. Sprenger J, Hardeland R, Fuhrberg B, Han SZ (1999) Melatonin and other 5-methoxylated indoles in yeast: presence in high concentrations and dependence on tryptophan availability. Cytologia 64:209–213. doi: 10.1508/cytologia.64.209 CrossRefGoogle Scholar
  70. Srinivasan V, Pandi-Perumal SR, Spence DW, Kato H, Cardinali DP (2010) Melatonin in septic shock: some recent concepts. J Crit Care 25:1–6. doi: 10.1016/j.jcrc.2010.03.006 CrossRefGoogle Scholar
  71. Srinivasan V, Mohamed M, Kato H (2012) Melatonin in bacterial and viral infections with focus on sepsis: a review. Recent Pat Endocr Metab Immune Drug Discov 6:30–39. doi: 10.2174/187221412799015317 CrossRefPubMedGoogle Scholar
  72. Sutherland ER, Martin RJ, Ellison MC, Kraft M (2002) Immunomodulatory effects of melatonin inasthma. Am J Respir Crit Care Med 166:1055–1061. doi: 10.1164/rccm.200204-356OC CrossRefPubMedGoogle Scholar
  73. Takayama H, Nakamura Y, Tamura H, Yamagata Y, Harada A, Nakata M, Sugino N, Kato H (2003) Pineal gland (melatonin) affects the parturition time but not luteal function and fetal growth in pregnant rats. Endocr J 50:37–43. doi: 10.1507/endocrj.50.37 CrossRefPubMedGoogle Scholar
  74. Tan DX, Manchester LC, Terron MP, Flores LJ, Tamura H, Reiter RJ (2007) Melatonin as a naturally occurring co-substrate of quinone reductase-2, the putative MT3 melatonin membrane receptor: hypothesis and significance. J Pineal Res 43:317–320. doi: 10.1111/j.1600-079X.2007.00513.x CrossRefPubMedGoogle Scholar
  75. Tan DX, Hardeland R, Manchester LC, Korkmaz A, Ma S, Rosales-Corral S, Reiter RJ (2012) Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. J Exp Bot 63:577–597. doi: 10.1093/jxb/err256 CrossRefPubMedGoogle Scholar
  76. Tekbas OF, Ogur R, Korkmaz A, Kilic A, Reiter RJ (2008) Melatonin as an antibiotic: new insights into the actions of this ubiquitous molecule. J Pineal Res 44:222–226. doi: 10.1111/j.1600-079X.2007.00516.x CrossRefPubMedGoogle Scholar
  77. Thomas I, Pervis CC, Drew JE, Abramovich DR, Williams LM (2002) Melatonin receptors in human fetal brain: 2-[125I] iodomelatonin binding site and MT1 gene expression. J Pineal Res 33:218–224. doi: 10.1034/j.1600-079X.2002.02921.x CrossRefPubMedGoogle Scholar
  78. Tilden AR, Becker MA, Amma LL, Arciniega J, McGaw AK (1997) Melatonin production in an aerobic photosynthetic bacterium: an evolutionarily early association with darkness. J Pineal Res 22:102–106. doi: 10.1111/j.1600-079X.1997.tb00310.x CrossRefPubMedGoogle Scholar
  79. Torres-Farfan C, Rocco V, Monso C, Valenzuela EJ, Campino C, Germain A, Viale ML, Campino C, Torreabilo F, Valenzuela GJ, Richter HG, Seron Ferre M (2006) Maternal melatonin effects on clock gene expression in a non-human primate fetus. Endocrinology 147:4618–4626. doi: 10.1210/en.2006-0628 CrossRefPubMedGoogle Scholar
  80. Valero N, Bonilla E, Pons H, Chacin-Bonilla L, Añez F, Espina LM, Medina-Leendertz S, García Tamayo J (2002) Melatonin induces changes to serum cytokines in mice infected with the Venezuelan equine encephalomyelitis virus. Trans R Soc Trop Med Hyg 96:1–4. doi: 10.1016/S0035-9203(02)90121-5 CrossRefGoogle Scholar
  81. Vera H, Tijmes M, Valladares LE (1996) Melatonin and testicular function: characterization of binding sites for 2-[125I]-iodomelatonin in immature rat testes. Steroids 62:226–229. doi: 10.1016/S0039-128X(97)81440-7 CrossRefGoogle Scholar
  82. Wang H, Wei W, Wang NP, Gui SY, Wu L, Sun WY, Xu SY (2005) Melatonin ameliorates carbon tetrachloride-induced hepatic fibrogenesis in rats via inhibition of oxidative stress. Life Sci 26:1902–1915. doi: 10.1016/j.lfs.2005.04.013 CrossRefGoogle Scholar
  83. Ward CG, Bullen JJ, Rogers HJ (1996) Iron and infection: new developments and their implications. J Trauma 41:356–364. doi: 10.1097/00005373-199608000-00030 CrossRefPubMedGoogle Scholar
  84. Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Sanjay Kumar
    • 1
  • Brendan Patrick Mulligan
    • 1
  • Shreesh Ojha
    • 2
  • Alex Tinson
    • 1
  1. 1.IVF LaboratoryManagement of Scientific Center and Presidential Camel, Department of President AffairsAl Ain, Abu DhabiUAE
  2. 2.Department of Pharmacology and TherapeuticsCollege of Medicine and Health Sciences, United Arab Emirates UniversityAl-Ain, Abu DhabiUAE

Personalised recommendations