Role of melatonin on production and preservation of gametes and embryos: A brief review

Animal Reproduction Science

Volumn 145, Issue 3-4, 2014, Pages 150-160

  Cruz, Maria Helena Coelho ^a,b   Leal, Claudia Lima Verde ^b   Cruz, Jurandir Ferreira da ^c   Tan, Dun Xian ^a   Reiter, Russel J ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSIDADE ESTADUAL DO SUDOESTE DA BAHIA   (Brazil)

Author keywords

Embryo development; Mammal; Melatonin; Oocyte; Spermatozoa

Indexed keywords

MAMMALIA;

MELATONIN;

ANIMAL; ANIMAL DISEASE; ANIMAL EMBRYO; EMBRYO DEVELOPMENT; MAMMAL; METABOLISM; OOCYTE; PHYSIOLOGY; PRESERVATION; REVIEW; SPERMATOZOON;

EMBRYO DEVELOPMENT; MAMMAL; MELATONIN; OOCYTE; SPERMATOZOA;

ANIMALS; EMBRYO, MAMMALIAN; MAMMALS; MELATONIN; PRESERVATION, BIOLOGICAL;

EID: 84895780831     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2014.01.011     Document Type: Review

References (133)

1. Abecia J.A., Forcada F., Zúñiga O. The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro. Vet. Res. Commun. 2002, 26:151-158.
2. Adriaens I., Jacquet P., Cortvrindt R., Janssen K., Smitz J. Melatonin has dose-dependent effects on folliculogenesis, oocyte maturation capacity and steroidogenesis. Toxicology 2006, 228:333-343.
3. Agarwal A., Gupta S., Sharma R.K. Role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 2005, 3:28.
4. Ali A.A., Bilodeau J.F., Sirard M.A. An antioxidant requirement for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 2003, 59:939-949.
5. Ambruosi B., Lacalandra G.M., Iorga A.I., De Santis T., Mugnier S., Matarrese R., Goudet G., Dell'Aquila M.E. Cytoplasmic lipid droplets and mitochondrial distribution in equine oocytes: Implications on oocyte maturation, fertilization and developmental competence after ICSI. Theriogenology 2009, 71:1093-1104.
6. Amireault P., Dubé F. Serotonin and its antidepressant-sensitive transporter in mouse cumulus-oocyte complexes and embryo. Biol. Reprod. 2005, 773:358-365.
7. Ansel L., Bentsen A.H., Ancel C., Bolborea M., Klosen P., Mikkelsen J.D., Simonneaux V. Peripheral kisspeptin reverses short photoperiod-induced gonadal regression in Syrian hamsters by promoting GNRH release. Reproduction 2011, 142:417-425.
8. Arendt J. Melatonin and the pineal gland: influence on mammalian seasonal and circadian physiology. Rev. Reprod. 1998, 3:13-22.
9. Arendt J. Importance and relevance of melatonin to human biological rhythms. J. Neuroendocrinol. 2003, 15:427-431.
10. Ashrafi I., Kohram H., Ardabili F.F. Antioxidative effects of melatonin on kinetics, microscopic and oxidative parameters of cryopreserved bull spermatozoa. Anim. Reprod. Sci. 2013, 139:25-30.
11. Axelrod J., Wurtman R.J., Winget C.M. Melatonin synthesis in the hen pineal gland and its control by light. Nature 1964, 14:1134.
12. Banerjee J., Maitra D., Diamond M.P., Abu-Soud H.M. Melatonin prevents hypochlorous acid-induced alterations in microtubule and chromosomal structure in metaphase-II mouse oocytes. J. Pineal Res. 2012, 53:122-128.
13. Barrett P., Bolborea M. Molecular pathways involved in seasonal body weight and reproductive responses governed by me latonin. J. Pineal Res. 2012, 52:376-388.
14. Berlinguer F., Leoni G.C., Succu S., Spezzigu A., Madeddu M., Satta V., Bebbere D., Contreras-Solis I., Gonzalez-Bulnes A., Naitana S. Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. J. Pineal Res. 2009, 46:383-391.
15. Boga J.A., Coto-Montes A., Rosales-Corral S.A., Tan D.X., Reiter R.J. Beneficial actions of melatonin in the management of viral infections: a new use for this molecular handyman?. Rev. Med. Virol. 2012, 22:323-338.
16. Bornman M.S., Oosthuizen J.M.C., Barnard H.C., Schulenburg G.W., Boomker D., Reif S. Melatonin and sperm motility. Andrologia 1989, 21:483-485.
17. Casao A., Abecia J.A., Cebrian Perez J.A., Muiño-Blanco T., Vázquez M.I., Forcada F. The effects of melatonin on in vitro oocyte competence and embryo development in sheep. Span. J. Agric. Res. 2010, 8:35-41.
18. Chai K., Liu X., Zhang Y., Lin H. Day-night and reproductive cycle profiles of melatonin receptor, KISS, and GnRH expression in orange-spotted grouper (Epinephelus coioides). Mol. Reprod. Dev. 2013, 80:535-548.
19. Chen Y.C., Sheen J.M., Tiao M.M., Tain Y.L., Huang L.T. Roles of melatonin in fetal programming in compromised pregnancies. Int. J. Mol. Sci. 2013, 6:5380-5401.
20. Choi J., Park S.M., Lee M., Kim J.H., Jeong Y.I., Lee J.Y., Park S.W., Kim H.S., Hossein M.S., Jeong Y.W., Kim S., Hyun S.H., Hwang W.S. Anti-apoptotic effect of melatonin on porcine parthenogenic embryos. Mol. Reprod. Dev 2008, 75:1127-1135.
21. Dair E.L., Simoes R.S., Simoes M.J., Romeu L.R., Oliveira-Filho R.M., Haidar M.A., Baracat E.C., Soares J.M. Effects of melatonin on the endometrial morphology and embryo implantation in rats. Fertil. Steril. 2008, 89:1299-1305.
22. de Leon P.M., Campos V.F., Corcini C.D., Santos E.C., Rambo G., Lucia T., Deschamps J.C., Collares T. Cryopreservation of immature equine oocytes, comparing a solid surface vitrification process with open pulled straws and the use of a synthetic ice blocker. Theriogenology 2012, 77:21-27.
23. Dennery P.A. Effects of oxidative stress on embryonic development. Birth Defects Res. C: Embryo Today 2007, 81:155-162.
24. du Plessis S.S., Hagenaar K., Lampiao F. The in vitro effects of melatonin on human sperm function and its scavenging activities on NO and ROS. Andrologia 2010, 42:112-116.
25. Dubocovich M.L. Melatonin receptors: role on sleep and circadian rhythm regulation. Sleep Med. 2007, 8:34-42.
26. Dubocovich M.L., Markowska M. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 2005, 27:101-110.
27. El-Raey M., Geshi M., Somfai T., Kaneda M., Hirako M., Abdel-Ghaffar A.E., Sosa G.A., Abau El-Roos M.E.A., Nagai T. Evidence of melatonin synthesis in the cumulus oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Mol. Reprod. Dev 2011, 78:250-262.
28. Favetta L.A., St John E.J., King W.A., Betts D.H. High levels of p66shc and intracellular ROS in permanently arrested early embryos. Free Radic. Biol. Med. 2007, 42:1201-1210.
29. Forcada F., Abecia J.A., Cebrian-Perez J.A., Muino T., Valares J.A., Palacin I., Casao A. The effect of melatonin implants during the seasonal anestrous on embryo production after superovulation in aged high-prolificacy Rasa aragonesa ewes. Theriogenology 2006, 65:356-365.
30. Frungieri M.B., Mayerhofer A., Zitta K., Pignataro O.P., Calandra R.S., Gonzalez-Calvar S.I. Direct action of melatonin on Syrian hamster testes: melatonin subtype 1a receptors, inhibition of androgen production, and interaction with local corticotropin-releasing hormone system. Endocrinology 2005, 146:1541-1552.
31. Fujimoto V.Y., Bloom M.S., Huddleston H.G., Shelley W.B., Ocque A.J., Browne R.W. Correlations of follicular fluid oxidative stress biomarkers and enzyme activities with embryo morphology parameters during in vitro fertilization. Fertil. Steril. 2011, 96:1357-1361.
32. Fujinoki M. Melatonin-enhanced hyperactivation of hamster sperm. Reproduction 2008, 136:533-541.
33. Galano A., Tan D.X., Reiter R.J. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J. Pineal Res. 2011, 51:1-16.
34. Galano A., Tan D.X., Reiter R.J. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. J. Pineal Res. 2013, 54:245-257.
35. Gao C., Han H.B., Tian X.Z., Tan D.X., Wang L., Zhou G.B., Zhu S.E., Liu G.S. Melatonin promotes embryonic development and reduces reactive oxygen species in vitrified mouse 2-cell embryos. J. Pineal Res. 2012, 52:305-311.
36. Garcia J.J., Reiter R.J., Guerrero J.M., Escames G., Yu B.P., Oh C.S., Muñoz-Hoyos H. Melatonin prevents changes in microsomal membrane fluidity during induced lipid peroxidation. FEBS Lett. 1997, 408:297-300.
37. Ghasemi F.M., Faghani M., Khajehjahromi S., Bahadori M., Nasiri E., Hemadi M. Effect of melatonin on proliferative activity and apoptosis in spermatogenic cells in mouse under chemotherapy. Reprod. Contracept. 2010, 21:79-94.
38. Goud A.P., Goud P.T., Diamond M.P., Gonik B., Abu-Soud H.M. Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic. Biol. Med. 2008, 44:1295-1304.
39. Hao Y., Lai L., Mao J., Im G.S., Bonk A., Prather R.S. Apoptosis and in vitro development of preimplantation porcine embryos derived in vitro or by nuclear transfer. Biol. Reprod. 2003, 69:501-507.
40. Hardeland R. Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification toradical avoidance. Endocrine 2005, 27:119-130.
41. Hardeland R., Pandi-Perumal S.R. Melatonin, a potent agent in antioxidative defense: actions as a natural food constituent, gastrointestinal factor, drug and prodrug. Nutr. Metab. 2005, 2:22.
42. Hardeland R., Cardinali D.P., Srinivasan V., Spence D.W., Brown G.M., Pandi-Perumal S.R. Melatonin-a pleiotropic, orchestrating regulator molecule. Prog. Neurobiol. 2011, 93:350-384.
43. Hastings M.H., Maywood E.S., Reddy A.B. Two decades of circadian time. J. Neuroendocrinol. 2008, 28:812-819.
44. Hoffman R.A., Reiter R.J. Pineal gland: influence on gonads of male hamsters. Science 1965, 148:1609-1611.
45. Ishizuka B., Kuribayashi Y., Murai K., Amemiya A., Itoh M.T. The effect of melatonin on in vitro fertilization and embryo development in mice. J. Pineal Res. 2000, 28:48-51.
46. Itoh M.T., Ishizaka B., Kuribayashi Y., Amemiya A., Sumi Y. Melatonin, its precursors, and synthesizing enzyme activities in the human ovary. Mol. Hum. Reprod. 1999, 5:402-408.
47. Iuvone P.M., Tosini G., Pozdeyev N., Hague R., Klein D.C., Chaurasia S.S. Circadian clocks, clock networks, arylalkylamine N-acetyltransferase, and melatonin in the retina. Prog. Retinal Eye Res. 2005, 24:433-436.
48. Jang H., Kim Y., Kim B., Park I., Cheong H., Kim J., Park C., Kong H., Lee H., Yang B. Ameliorative effects of melatonin against hydrogen peroxide-induced oxidative stress on boar sperm characteristics and subsequent in vitro embryo development. Reprod. Domest. Anim. 2010, 45:943-950.
49. Ji Y.L., Wang H., Meng C., Zhao X.F., Zhang C., Zhang Y., Zhao M., Chen Y.H., Meng X.H., Xu D.X. Melatonin alleviates cadmium-induced cellular stress and germ cell apoptosis in testes. J. Pineal Res. 2012, 52:71-79.
50. Kang J.T., Koo O.J., Kwon D.K., Park H.J., Jang G., Kong S.K., Lee B.C. Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. J. Pineal Res. 2009, 46:22-28.
51. Khalil W.A., Marei W.F., Khalid M. Protective effects of antioxidants on linoleic acid-treated bovine oocytes during maturation and subsequent embryo development. Theriogenology 2013, 15:161-168.
52. Kim M.K., Park E.A., Kim H.J., Choi W.Y., Cho J.H., Lee W.S., Cha K.Y., Kim Y.S., Lee D.R., Yoon T.K. Does supplementation of in-vitro culture medium with melatonin improve IVF outcome in PCOS?. Reprod. Biomed. Online 2013, 26:22-29.
53. Korkmaz A., Reiter R.J. Epigenetic regulation: a new research area for melatonin?. J. Pineal Res. 2008, 44:41-44.
54. Korkmaz A., Rosales-Corral S., Reiter R.J. Gene regulation by melatonin linked to epigenetic phenomena. Gene 2012, 503:1-11.
55. Kurcer Z., Hekimoglu A., Aral F., Baba F., Sahna E. Effect of melatonin on epididymal sperm quality after testicular ischemia/reperfusion in rats. Fertil. Steril. 2010, 93:1545-1549.
56. Leon J., Acuña-Castroviejo D., Sainz R.M., Mayo J.C., Tan D.X., Reiter R.J. Melatonin and mitochondrial function. Life Sci. 2004, 75:765-790.
57. Leon J., Acuña-Castroviejo D., Escames G., Tan D.-X., Reiter R.J. Melatonin mitigates mitochondrial malfunction. J. Pineal Res. 2005, 38:1-9.
58. Lerner, A.B., Case, J.D., Takahashi, Y., Lee, Y., Mori, W., 1958. Isolation of melatonin, the pineal factor that lightens melanocytes. J. Am. Chem. Soc. 80, 2587.
59. Lerner A.B., Case J.D., Heinzelmann R.V. Structure of melatonin. J. Am. Chem. Soc. 1959, 81:6084-6085.
60. 1 melatonin receptor function through heterodimerization. EMBO J. 2006, 25:3012-3023.
61. Li L., Xu J.N., Wong Y.H., Wong J.T., Pang S.F., Shiu S.Y. Molecular and cellular analyses of melatonin receptor-mediated cAMP signaling in rat corpus epididymis. J. Pineal Res. 1998, 25:219-228.
62. Li X.X., Yang X.G., Lu Y.Q., Lu S.S., Zhang M., Yao H.L., Meng L.J., Lu K.H. Protective effects of melatonin against oxidative stress in flow cytometry-sorted buffalo sperm. Reprod. Domest. Anim. 2012, 47:299-307.
63. Lincoln G.A., Clarke I.J. Refractoriness to a static melatonin signal develops in the pituitary gland for the control of prolactin secretion in the ram. Biol. Reprod. 1997, 57:460-467.
64. Lincoln G.A., Short R.V. Seasonal breeding: nature's contraceptive. Recent Prog. Horm. Res. 1980, 36:1-52.
65. Liu Y.X. Involvement of plasminogen activator and plasminogen activator inhibitor type 1 in spermatogenesis, sperm capacitation, and fertilization. Semin. Thromb. Hemost. 2007, 33:29-40.
66. Luther J.S., Redmer D.A., Reynolds L.P., Choi J.T., Pant D., Navanukraw C., Arnold D.R., Scheaffer A.N., Borowicz P., Kirsch J.D., Weigl R.M., Kraft K.C., Grazul-Bilska A.T. Ovarian follicular development and oocyte quality in anestrous ewes treated with melatonin, a controlled internal drug release (CIDR) device and follicle stimulating hormone. Theriogenology 2005, 63:2136-2146.
67. Malpaux B., Viguie C., Skinner D.C., Thiery A.C., Pelletier J., Chemineau P. Seasonal breeding in sheep: mechanism of action of melatonin. Anim. Reprod. Sci. 1996, 42:109-117.
68. Manjunatha B.M., Devaraj M., Gupta P.S.P., Ravindra J.P., Nandi S. Effect of taurine and melatonin in the culture medium on buffalo in vitro embryo development. Reprod. Domest. Anim. 2009, 44:12-16.
69. Maronde E., Stehle J. The mammalian pineal gland: known facts, unknown facets. Trends Endocrinol. Metab. 2007, 18:142-149.
70. Martin-Hildago D., Baron F.J., Bragado M.J., Carmona P., Robina A., Garcia-Marin L.J., Gil M.C. The effect of melatonin on the quality of extended boar semen after long-term storage at 17°C. Theriogenology 2011, 75:1550-1560.
71. Mason A.O., Greives T.J., Scotti M.A., Levine J., Frommeyer S., Ketterson E.D., Demas G.E., Kriegsfeld L.J. Suppression of kisspeptin expression and gonadotropic axis sensitivity following exposure to inhibitory day lengths in female Siberian hamsters. Horm. Behav. 2007, 52:492-498.
72. Mata-Campuzano M., Alvarez-Rodríguez M., del Olmo E., Fernández-Santos M.R., Garde J.J., Martínez-Pastor F. Quality, oxidative markers and DNA damage (DNA) fragmentation of red deer thawed spermatozoa after incubation at 37°C in presence of several antioxidants. Theriogenology 2012, 78:1005-1019.
73. Mauriz J.L., Collado P.S., Veneroso C., Reiter R.J., González-Gallego J. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J. Pineal Res. 2013, 54:1-14.
74. Misztal T., Romanowicz K., Barcikowski B. Melatonin-a modulator of the GnRH/LH axis in sheep. Reprod. Biol. 2002, 2:267-275.
75. Mohseni M., Mihandoost E., Shirazi A., Sepehrizadeh Z., Bazzaz J.T., Ghazi-khansari M. Melatonin may play a role in modulation of bax and bcl-2 expression levels to protect rat peripheral blood lymphocytes from gamma irradiation-induced apoptosis. Mutat. Res. 2012, 739:19-27.
76. Nakamura Y., Tamura H., Takayama H., Kato H. Increased endogenous level of melatonin in preovulatory human follicles does not directly influence progesterone production. Fertil. Steril. 2003, 80:1012-1016.
77. Nakano M., Kato Y., Tsunoda Y. Effect of melatonin treatment on the developmental potential of parthenogenetic and somatic cell nuclear-transferred porcine oocytes in vitro. Zygote 2012, 20:199-207.
78. Nanassy L., Lee K., Javor A., Machaty Z. Effects of activation methods and culture conditions on development of parthenogenetic porcine embryos. Anim. Reprod. Sci. 2008, 104:264-274.
79. Nosjean O., Ferro M., Coge F., Beauverger P., Henlin F.M., Lefoulon F., Fauchere J.L., Delagrange P., Canet E., Boutin J.A. Identification of the melatonin-binding site MT3 as the quinone reductase 2. J. Biol. Chem. 2000, 275:31311-31317.
80. Okatani Y., Wakatsuki A., Kaneda C. Melatonin increases activities of glutathione peroxidase and superoxide dismutase in fetal rat brain. J. Pineal Res. 2000, 28:89-96.
81. Pandey A.N., Tripathi A., Premkumar K.V., Shrivastav T.G., Chaube S.K. Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes. J. Cell Biochem. 2010, 111:521-528.
82. Papis K., Poleszczuk O., Wenta-Muchalska E., Modlinski J.A. Melatonin effect in bovine embryo development in vitro in relation to oxygen concentration. J. Pineal Res. 2007, 43:321-326.
83. Picinato M.C., Hirata A.E., Cipolla-Neto J., Curi R., Carvalho C.R., Anhê G.F., Carpinelli A.R. Activation of insulin and IGF-1 signaling pathways by melatonin through MT1 receptor in isolated rat pancreatic islets. J. Pineal Res. 2008, 44:88-94.
84. Radogna F., Diederich M., Ghibelli L. Melatonin: a pleiotropic molecule regulating inflammation. Biochem. Pharmacol. 2010, 80:1844-1852.
85. Rao M.V., Gangadharan B. Antioxidant potential of melatonin against mercury induced intoxication in spermatozoa in vitro. Toxicol. In Vitro 2008, 22:935-942.
86. Reiter R.J. The melatonin rhythm: both a clock and a calendar. Expenientia 1993, 49:654-664.
87. Reiter R.J. Melatonin: lowering the high price of free radicals. News Physiol. Sci. 2000, 15:246-250.
88. Reiter R.J., Fraschini F. Endocrine aspects of the mammalian pineal gland: a review. Neuroendocrinology 1969, 5:219-255.
89. Reiter R.J., Hester R.J. Interrelationships of the pineal gland, the superior cervical ganglia and the photoperiod in the regulation of the endocrine systems of hamsters. Endocrinology 1966, 79:1168-1170.
90. Reiter R.J., Tan D.X., Osuna C., Gitto E. Actions of melatonin in the reduction of oxidative stress: a review. J. Biomed. Sci. 2000, 7:444-458.
91. Reiter R.J., Calvo J.R., Karbownik M., Qi W., Tan D.X. Melatonin and its relation to the immune system and inflammation. Ann. N. Y. Acad. Sci. 2000, 917:376-386.
92. Reiter R.J., Tan D.X., Manchester L.C., Pilar Terron M., Flores L.J., Koppisepi S. Medical implications of melatonin: receptor-mediated and receptor-independent actions. Adv. Med. Sci 2007, 52:11-28.
93. Reiter R.J., Tan D.X., Manchester L.C., Paredes S.D., Mayo J.C., Sainz R.M. Melatonin and reproduction revisited. Biol. Reprod. 2009, 81:445-456.
94. Reiter R.J., Tan D.X., Fuentes-Broto L. Melatonin: a multitasking molecule. Prog. Brain Res. 2010, 181:127-151.
95. Reiter R.J., Rosales-Corral S.A., Manchester L.C., Tan D.X. Peripheral reproductive organ health and melatonin: ready for prime time. Int. J. Mol. Sci. 2013, 14:7231-7272.
96. Reiter R.J., Tan D.X., Rosales-Corral S., Manchester L.C. The universal nature, unequal distribution and antioxidant functions of melatonin and its derivatives. Mini Rev. Med. Chem. 2013, 13:373-384.
97. Revel F.G., Saboureau M., Masson-Pevet M., Pevet P., Mikkelsen J.D., Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr. Biol. 2006, 16:1730-1735.
98. Revel F.G., Masson-Pévet M., Pévet P., Mikkelsen J.D., Simonneaux V. Melatonin controls seasonal breeding by a network of hypothalamic targets. Neuroendocrinology 2009, 90:1-14.
99. Rodriguez C., Mayo J.C., Sainz R.M., Antolin I., Herrera F., Martin V., Reiter R.J. Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 2004, 36:1-9.
100. Rodriguez-Osorio N., Kim I.J., Wang H. Melatonin increases cleavage rate of porcine preimplantation embryos in vitro. J. Pineal Res. 2007, 43:283-288.
101. Rosa H.J.D., Bryant M.J. Seasonality of reproduction in sheep. Small Rum. Res. 2003, 48:155-171.
102. Roy D., Belsham D.D. Melatonin receptor activation regulates GnRH gene expression and secretion in GT1-7 GnRH neurons, signal transduction mechanisms. Biol. Chem. 2002, 277:251-258.
103. Sampaio R.V., Conceição S., Miranda M.S., Sampaio L., de F., Ohashi O.M. MT3 melatonin binding site, MT1 and MT2 melatonin receptors are present in oocyte, but only MT1 is present in bovine blastocyst produced in vitro. Reprod. Biol. Endocrinol. 2012, 3(10):103.
104. Sarabia L., Maurer I., Bustos-Obregon E. Melatonin prevents damage elicited by organophosphorous pesticide diazinon on mouse sperm DNA. Ecotoxicol. Environ. Saf. 2009, 72:663-668.
105. Sariozkan S., Bucak M.N., Tuncer P.B., Taşdemir U., Kinet H., Ulutaş P.A. Effects of different extenders and centrifugation/washing on postthaw microscopic-oxidative stress parameters and fertilizing ability of Angora buck sperm. Theriogenology 2010, 73:316-323.
106. Shang E.H., Zhdanova I.V. The circadian system is a target and modulator of prenatal cocaine effects. PLoS ONE 2007, 2:e587.
107. Shi J.M., Tian X.Z., Zhou G.B., Wang L., Gao C., Zhu S.E., Zeng S.M., Tian J.H., Liu G.S. Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes. J. Pineal Res. 2009, 47:318-323.
108. Smirnov A.N. Nuclear melatonin receptors. Biochemistry 2001, 66:19-26.
109. Somfai T., Ozawa M., Noguchi J., Kaneko H., Kuriani Karja N.W., Farhudin M., Dinnyés A., Nagai T., Kikuchi K. Developmental competence of in vitro-fertilized porcine oocytes after in vitro maturation and solid surface vitrification: effect of cryopreservation on oocyte antioxidative system and cell cycle. Cryobiology 2007, 55:115-126.
110. Stehle J.H., Saade A., Rawashdeh O., Ackermann K., Jilg A., Sebestény T., Maronde E. A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases. J. Pineal Res. 2011, 51:17-43.
111. Sturmey R.G., Reis A., Leese H.J., McEvoy T.G. Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 2009, 44:50-58.
112. Succu S., Berlinguer F., Pasciu V., Satta V., Leoni G.G., Naltana S. Melatonin protects ram spermatozoa from cryopreservation injuries in a dose-dependent manner. J. Pineal Res. 2011, 50:310-318.
113. Sugden D. Melatonin biosynthesis in the mammalian pineal gland. Experientia 1989, 45:922-932.
114. Tamura H., Nakamura Y., Terron M.P., Flores L.J., Manchester L.C., Tan D.X., Sugino N., Reiter R.J. Melatonin and pregnancy in the human. Reprod. Toxicol. 2008, 25:291-303.
115. Tamura H., Nakamura Y., Korkmaz A., Manchester L.C., Tan D.X., Sugino N., Reiter R.J. Melatonin and the ovary: physiological and pathophysiological implication. Fertil. Steril. 2009, 92:328-343.
116. Tamura H., Takasaki A., Taketani T., Tanabe M., Kizuka F., Lee L., Tamura I., Maekawa R., Aasada H., Yamagata Y., Sugino N. The role of melatonin as an antioxidant in the follicle. J. Ovarian Res. 2012, 25:5.
117. Tamura H., Takasaki A., Taketani T., Tanabe M., Kizuka F., Lee L., Tamura I., Maekawa R., Aasada H., Yamagata Y., Sugino N. Melatonin as a free radical scavenger in the ovarian follicle. Endocr. J. 2013, 60:1-13.
118. Tan D.X., Chen L.D., Poeggeler B., Manchester L.C., Reiter R.J. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr. J. 1993, 1:57-60.
119. Tan D.X., Reiter R.J., Manchester L.C., Yan M.T., El-Sawi M., Sainz R.M., Mayo J.C., Kohen R., Allegra M., Hardeland R. Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr. Top. Med. Chem. 2002, 2:181-197.
120. Tan D.X., Manchester L.C., Terron M.P., Flores L.J., Tamura H., Reiter R.J. Melatonin as a naturally occurring co-substrate of quinone reductase-2, the putative MT3 melatonin membrane receptor: hypothesis and significance. J. Pineal Res. 2007, 43:317-320.
121. Tan D.X., Hardeland R., Manchester L.C., Rosales-Corral S., Coto-Montes A., Boga J.A., Reiter R.J. Emergence of naturally occurring melatonin isomers and their proposed nomenclature. J. Pineal Res. 2012, 53:113-121.
122. Thuwanut P., Chatdarong K., Bergqvist A.S., Söderquist L., Thiangtum K., Tongthainan D., Axnér E. The effects of antioxidants on semen traits and in vitro fertilizing ability of sperm from the flat-headed cat (Prionailurus planiceps). Theriogenology 2011, 76:115-125.
123. Tsantarliotou M.P., Kokolis N.A., Smokovitis A. Melatonin administration increased plasminogen activator activity in ram spermatozoa. Theriogenology 2008, 69:458-465.
124. Tsutsui K., Ubuka T., Bentley G.E., Kriegsfeld L.J. Review: regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals. Front. Neurosci. 2013, 16(7):60.
125. Vargas A., Bustos-Obregon E., Hartley R. Effects of hypoxia on epididymal sperm parameters and protective role of ibuprofen and melatonin. Biol. Res. 2011, 44:161-167.
126. Vázquez M.I., Abecia J.A., Forcada F., Casao A. Effects of exogenous melatonin on in vivo embryo viability and oocyte competence of undernourished ewes after weaning during the seasonal anestrus. Theriogenology 2010, 74:618-626.
127. Venegas C., García J.A., Escames G., Ortiz F., López A., Doerrier C., García-Corzo L., López L.C., Reiter R.J., Acuña-Castroviejo D. Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations. J. Pineal Res. 2012, 52:217-227.
128. Vijayalaxmi Reiter R.J., Tan D.X., Herman T.S., Thomas C.R. Melatonin as a radioprotective agent: a review. Int. J. Radiat. Oncol. Biol. Phys. 2004, 59:639-653.
129. Vincent L., Cohen W., Delagrange P., Boutin J.A., Nosjean O. Molecular and cellular pharmacological properties of 5-methoxycarbonylamino-N-acetyltryptamine (MCA-NAT): a nonspecific MT3 ligand. J. Pineal Res. 2010, 48:222-229.
130. Von Gall C., Garabette M.L., Kell C.A., Frenzel S. Rhythmic gene expression in pituitary cells depends on temporally defined heterologous sensitization by the neurohormone melatonin. Nat. Neurosci. 2002, 5:234-238.
131. Wang F., Tian X., Zhang L., Tan D., Reiter R.J., Liu G. Melatonin promotes the in vitro development of pronuclear embryos and increases the efficiency of blastocyst implantation in murine. J. Pineal Res. 2013, (in press).
132. Woo M.M., Tai C.J., Kang S.K., Nathwani S.P., Pang S.F., Leung P.C. Direct action of melatonin in human granulosa-luteal cells. J. Clin. Endocrinol Metab. 2001, 86:4789-4797.
133. Yonei Y., Hattori A., Tsutsui K., Okawa M., Ishizuka B. Effects of melatonin: basics studies and clinical applications. Anti-Aging Med. 2010, 7:85-91.