Peripheral reproductive organ health and melatonin: Ready for prime time

International Journal of Molecular Sciences

Volumn 14, Issue 4, 2013, Pages 7231-7272

  Reiter, Russel J ^a   Rosales Corral, Sergio A ^a   Manchester, Lucien C ^a   Tan, Dun Xian ^a  

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

Author keywords

Antioxidant; Melatonin; Oocyte; Ovarian follicle; Parturition; Placenta; Sperm

Indexed keywords

MELATONIN; PLACEBO; REACTIVE OXYGEN METABOLITE;

AMNION; AMNION FLUID; ANTIOXIDANT ACTIVITY; ARTIFICIAL INSEMINATION; CELL PROTECTION; CYTOTROPHOBLAST; DRUG MECHANISM; FEMALE INFERTILITY; FERTILIZATION IN VITRO; HORMONE ACTION; HUMAN; NONHUMAN; OVARY FOLLICLE; PLACENTA; PREGNANCY OUTCOME; PREGNANCY RATE; REPRODUCTIVE HEALTH; REVIEW; SEMEN ANALYSIS; STEROIDOGENESIS; SYNCYTIOTROPHOBLAST; ANIMAL; FEMALE; FEMALE GENITAL SYSTEM; HEALTH; MALE; MALE GENITAL SYSTEM; METABOLISM; PHYSIOLOGY;

ANIMALS; FEMALE; GENITALIA, FEMALE; GENITALIA, MALE; HEALTH; HUMANS; MALE; MELATONIN;

EID: 84875999961     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14047231     Document Type: Review

References (258)

1. Lerner, A.B.; Case, J.D.; Takahashi, Y.; Lee, Y.; Mori, W. Isolation of melatonin, the pineal factor that lightens melanocytes. J. Am. Chem. Soc. 1958, 80, 2587.
2. Launay, J.M.; Lemaitre, B.J.; Husson, H.P.; Dreux, C.; Hartmann, L.; da Prada, M. Melatonin synthesis by rabbit platelets. Life Sci. 1982, 31, 1487-1494.
3. Reiter, R.J.; Richardson, B.A.; Matthews, S.A.; Lane, S.J.; Ferguson, B.N. Rhythms of immunoreactive melatonin in the retina and Harderian glands of rats: Persistence after pinealectomy. Life Sci. 1983, 32, 1299-1236.
4. Huether, G.; Poeggeler, B.; Reimer, A.; George, A. Effects of tryptophan administration on circulating melatonin levels in chicks and rats: Evidence for stimulation of melatonin synthesis and release in the gastrointestinal tract. Life Sci. 1992, 51, 946-953.
5. Abe, M.; Itoh, M.T.; Miyata, M.; Shimizu, K.; Sumi, Y. Circadian rhythm of serotonin N-acetyltransferace activity in rat lens. Exp. Eye Res. 2000, 70, 805-808.
6. Reed, B.L. The control of circadian pigment changes in the pencil fish: A proposed role for melatonin. Life Sci. 1968, 7, 961-973.
7. Panke, E.S.; Rollag, M.D.; Reiter, R.J. Pineal melatonin concentrations in the Syrian hamster. Endocrinology 1979, 104, 194-197.
8. Birkeland, A.J. Plasma melatonin levels and nocturnal transitions between sleep and wakefulness. Neuroendocrinology 1982, 34, 126-131.
9. Lewy, A.J.; Sack, R.L.; Miller, L.S.; Hoban, T.M.; Singer, C.M.; Samples, J.R.; Krauss, G.L. The use of plasma melatonin levels and light in the assessment and treatment of chronobiologic sleep and mood disorders. J. Neural Transm. 1986, 21, 311-322.
10. Reiter, R.J. Pineal control of a seasonal reproductive rhythm in male golden hamsters exposed to natural daylight and temperature. Endocrinology 1973, 92, 423-430.
11. Reiter, R.J.; Vaughan, M.K.; Blask, D.E.; Johnson, L.Y. Melatonin: Its inhibition of pineal antigonadotrophic activity in male hamsters. Science 1974, 185, 1169-1171.
12. Lincoln, G.A.; Short, R.V. Seasonal breeding: Nature's contraceptive. Rec. Progr. Horm. Res. 1980, 36, 1-52.
13. Reiter, R.J. The melatonin rhythm: Both a clock and a calendar. Expenientia 1993, 49, 654-664.
14. Molina-Carballo, A.; Munoz-Hoyos, A.; Reiter, R.J.; Sanchez-Forte, M.; Moreno-Madrid, F.; Rufo-Campos, M.; Molina-Font, J.A.; Acuna-Castroviejo, D. Utility of high doses of melatonin as adjunctive anticonvulsant therapy in a child with severe myoclonic epilepsy: Two years' experience. J. Pineal Res. 1997, 23, 97-106.
15. Swarnakar, S.; Paul, S.; Singh, L.P.; Reiter, R.J. Matrix metalloproteinases in health and disease: Regulation by melatonin. J. Pineal Res. 2011, 50, 8-20.
16. Tosini, G.; Baba, K.; Hwang, C.K.; Iuvane, D.M. Melatonin, an underappreciated player in retinal physiology and pathophysiology. Exp. Eye Res. 2012, 103, 82-89.
17. Escames, G.; Ozturk, G.; Bano-Otalora, B.; Pozo, M.J.; Madrid, J.A.; Reiter, R.J.; Serrano, E.; Concepcion, M.; Acuna-Castroviejo, D. Exercise and melatonin in humans: Reciprocal benefits. J. Pineal Res. 2012, 52, 1-11.
18. Cardinali, D.P.; Srinivasan, V.; Brzezinski, A.; Brown, G.M. Melatonin and its analogs in insomnia and depression. J. Pineal Res. 2012, 52, 365-375.
19. Axelrod, J.; Wurtman, R.J.; Snyder, S.H. Control of hydroxyindole-O-methyltransferase activity in the rat pineal gland by environment lighting. J. Biol. Chem. 1965, 240, 949-954.
20. Manchester, L.C.; Poeggeler, B.; Alvares, F.L.; Ogden, G.B.; Reiter, R.J. Melatonin immunoreactivity in the photosynthetic prokaryote Rhodospirillum rubrum: Implications for an ancient antioxidant system. Cell. Mol. Biol. Res. 1996, 41, 391-395.
21. Tilden, A.R.; Becker, M.A.; Amma, L.L.; Arciniega, J.; McGaw, A.K. Melatonin production in an aerobic photosynthetic bacterium: An evolutionarily early association with darkness. J. Pineal Res. 1997, 22, 102-106.
22. Poeggeler, B.; Hardeland, R. Detection and quantification of melatonin in a dinoflagellate, Gonyaulax polyedra: Solutions to the problem of methoxyindole destruction in non-vertebrate material. J. Pineal Res. 1994, 17, 1-10.
23. Hardeland, R.; Balzer, I.; Poeggeler, B.; Fuhrberg, B.; Uria, H.; Behrmann, G.; Wolf, R.; Meyer, T.J.; Reiter, R.J. On the primary functions of melatonin in evolution: Mediation of photoperiodic signals in a unicell, photooxidation, and scavenging of free radicals. J. Pineal Res. 1995, 18, 104-111.
24. Dubbels, R.; Reiter, R.J.; Klenke, E.; Goebel, A.; Schnakenberg, E.; Ehlers, C.; Schiawa, H.W.; Schlvat, W. Melatonin in edible plants identified by radioimmunoassay and high performance liquid chromatography-mass spectrometry. J. Pineal Res. 1995, 18, 28-31.
25. Hattori, A.; Migitaka, H.; Iigo, M.; Itoh, M.; Yamamato, K.; Ohtani-Kaneko, R.; Hara, M.; Suzuki, T.; Reiter, R.J. Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochem. Mol. Biol. Int. 1995, 35, 627-634.
26. Kolar, J.; Machackova, I. Melatonin in higher plants: Occurrence and possible functions. J. Pineal Res. 2005, 39, 333-341.
27. Stankov, B.; Reiter, R.J. Melatonin receptors: Current status, facts and hypotheses. Life Sci. 1990, 46, 971-982.
28. Reppert, S.M.; Henshaw, D.; Schwartz, W.J.; Weaver, D.R. The circadian-gated timing of birth in rats: Disruption by maternal SCN lesions or by removal of the fetal brain. Brain Rec. 1987, 403, 398-402.
29. Dubocovich, M.L.; Markowska, M. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 2005, 27, 101-110.
30. Acuna-Castroviejo, D.; Reiter, R.J.; Menendez-Pelaez, A.; Pablos, M.I.; Burgos, A. Characterization of high-affinity melatonin binding sites in purified cell nuclei. J. Pineal Res. 1994, 16, 100-112.
31. Steinhilber, D.; Brungs, M.; Werz, O.; Weisenberg, I.; Danielsson, C.; Kahlen, J.P.; Nayeri, S.; Schrader, M.; Carlberg, C. The nuclear receptor for melatonin represses 5-lipoxygenase gene expression in human B lymphocytes. J. Biol. Chem. 1995, 270, 7037-7040.
32. Lardone, P.J.; Guerrero, J.M.; Fernandez-Santos, J.M.; Rubio, A.; Martin-Lacave, F.; Carrillo-Vico, A. Melatonin synthesized in T-lymphocytes as a ligand of the retinoic acid-related orphan receptor. J. Pineal Res. 2011, 51, 454-462.
33. Benitez-King, G.; Huerto-Delgadillo, L.; Anton-Tay, F. Binding of H3-melatonin to calmodulin. Life Sci. 1993, 53, 201-207.
34. Pozo, D.; Reiter, R.J.; Calvo, J.R.; Guerrero, J.M. Inhibition of cerebellar nitric oxide synthase and cyclic GMP production by melatonin via complex formation with calmodulin. J. Cell Biochem. 1997, 65, 430-442.
35. Boutin, J.A. Melatonin binding site MT3 is QR2: State of the art. J. Soc. Biol. 2007, 201, 97-103.
36. Wang, X. The antiapoptotic activity in neurodegenerative diseases. CNS Neurosci. Ther. 2009, 15, 345-357.
37. 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.
38. Hardeland, R.; Reiter, R.J.; Poeggeler, B.; Tan, D.X. The significance of the metabolism of the neurohormone melatonin: Antioxidative protection and formation of bioactive substances. Neurosci. Biobehav. Rev. 1993, 17, 347-357.
39. Tan, D.X.; Manchester, L.C.; Reiter, R.J.; Oi, W.; Kim, S.J.; El-Sokkary, G.H. Ischemia/reperfusion-induced arrhythmias in the isolated rat heart: Prevention by melatonin. J. Pineal Res. 1999, 25, 184-191.
40. Reiter, R.J.; Paradies, S.D.; Manchester, L.C.; Tan, D.X. Reducing oxidative/nitrosative stress: A newly-discovered gene for melatonin. Crit. Rev. Biochem. Mol. Biol. 2009, 44, 175-200.
41. Sewerynek, E.; Abe, M.; Reiter, R.J.; Barlow-Walden, L.R.; Chen, L.; McCabe, T.J.; Roman, L.J.; Diaz-Lopez, B. Melatonin administration prevents lipopolysaccharide-induced oxidative damage in phenobarbital-treated animals. J. Cell. Biochem. 1995, 58, 436-444.
42. Melchiorri, D.; Reiter, R.J.; Sewerynek, E.; Hara, M.; Chen, L.; Nistico, G. Paraquat toxicity and oxidative damage: Reduction by melatonin. Biochem. Pharmacol. 1996, 51, 1095-1099.
43. Reiter, R.J.; Tan, D.X.; Manchester, L.C.; Terron, M.P.; Flores, L.J.; Koppisepi, S. Medical implications of melatonin: Receptor-mediated and receptor-independent actions. Adv. Med. Soc. 2007, 52, 11-28.
44. 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.
45. Tan, D.X.; Manchester, L.C.; Reiter, R.J.; Qi, W.B.; Karbownik, M.; Calvo, J.R. Significance of melatonin in antioxidative defense system: Reactions and products. Biol. Signals Recept. 2000, 9, 137-159.
46. Tan, D.X.; Manchester, L.C.; Terron, M.P.; Flores, L.J.; Reiter, R.J. One molecule, many derivatives: A never-ending interaction of melatonin with reactive oxygen and nitrogen species? J. Pineal Res. 2007, 42, 28-42.
47. Hardeland, R.; Tan, D.X.; Reiter, R.J. Kynuramines, metabolites of melatonin and other indoles: The resurrection of an almost forgotten class of biogenic amines. J. Pineal Res. 2009, 47, 109-126.
48. 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, in press.
49. Gomez, F.J.; Raba, J.; Cerutti, S.; Silva, M.F. Monitoring melatonin and its isomes in Vitis vinifera cv Malbed by UHPLC-MS/MS from grape to bottle. J. Pineal Res. 2012, 52, 349-355.
50. 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.
51. Vitalini, S.; Gardana, C.; Simonetti, P.; Fico, G.; Irit, M. Melatonin, melatonin isomers and stilbenes in Italian traditional grape products and their antiradical capacity. J. Pineal Res. 2013, in press.
52. Iriti, M.; Varoni, E.M.; Vitalini, S. Melatonin in traditional Mediterranean diets. J. Pineal Res. 2010, 49, 101-105.
53. Luchetti, F.; Canonico, B.; Betti, M.; Arcangeletti, M.; Pilotti, F.; Piroddi, M.; Canesi, L.; Papa, S.; Galli, F. Melatonin signaling and cell protection function. FASEB J. 2010, 24, 3603-3624.
54. Tan, D.X.; Hardeland, R.; Manchester, L.C.; Korkmaz, A.; Ma, S.; Rosales-Corral, S.; Reiter, R.J. Functional roles of melatonin in plants and perspectives in nutritional and agricultural science. J. Exp. Biol. 2012, 63, 577-597.
55. 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.
56. Mauriz, J.L.; Callado, D.S.; Veneroso, C.; Reiter, R.J.; Gonzalez-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.
57. Dominguez-Rodriguez, A.; Abreu-Gonzalez, P.; Avanzas, R. The role of melatonin in acute myocardial infarction. Front. Biosci. 2012, 17, 2433-2441.
58. Tamura, H.; Takasaki, A.; Taketani, T.; Tanabe, M.; Kizuka, F.; Lee, L.; Tamura, I.; Maekawa, R.; Aasada, H.; Yamagata, Y.; et al. Melatonin as a free radical scavenger in the ovarian follicle. Endocr. J. 2013, in press.
59. Maldonado, M.D.; Murrillo-Cabezas, F.; Terron, M.P.; Flores, L.F.; Tan, D.X.; Manchester, L.C.; Reiter, R.J. The potential of melatonin in reducing morbidity-mortality after craniocerebral trauma. J. Pineal Res. 2006, 42, 1-11.
60. Gitto, E.; Pellegrino, S.; Gitto, P.; Barberi, I.; Reiter, R.J. Oxidative stress of the newborn in the pre-and postnatal period and the clinical utility of melatonin. J. Pineal Res. 2008, 46, 128-139.
61. Hoffman, R.A.; Reiter, R.J. Pineal gland: Influence on gonads of male hamsters. Science 1995, 148, 1609-1611.
62. Reiter, R.J. The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev. 1980, 1, 109-131.
63. Brainard, G.C.; Petterbarg, L.J.; Richardson, B.A.; Reiter, R.J. Pineal melatonin in Syrian hamsters: Circadian and seasonal rhythms in animals maintained under laboratory and nocturnal conditions. Neuroendocrinology 1982, 35, 342-348.
64. Reiter, R.J. Evidence for refractoriness of the pituitary-gonadal axis to the pineal gland in golden hamsters and its possible implications in annual reproductive rhythms. Anal. Rec. 1972, 173, 365-371.
65. Carter, D.S.; Goldman, B.D. Antigonadal effects of timed melatonin infusion in pinealectomized male Djungarian hamsters (Phodopus sungorus sungorus): Duration is the critical parameter. Endocrinology 1983, 113, 1261-1266.
66. Karsch, F.J.; Bittman, E.L.; Foster, D.L.; Goodman, R.L.; Legan, S.J.; Robinson, J.E. Neuroendocrine basis of seasonal reproduction. Rec. Progr. Horm. Res. 1984, 41, 185-232.
67. Lincoln, G.A. Decoding the nightly melatonin signal through circadian clockwork. Mol. Cell. Endocrinol. 2006, 252, 69-73.
68. Barrett, P.; Bolboren, M. Molecular pathways involved in the seasonal body weight and reproductive responses governed by melatonin. J. Pineal Res. 2012, 52, 376-388.
69. Vanecek, J. Cellular mechanisms of melatonin action. Physiol. Rev. 1998, 78, 687-721.
70. Ishii, H.; Tanaka, N.; Kobayashi, M.; Kato, M.; Sakuma, Y. Gene structures, biochemical characterization and distribution of rat melatonin receptors. J. Physiol. Sci. 2009, 59, 37-47.
71. 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.
72. Ekmekcioglu, C. Melatonin receptors in humans: Biological role and clinical relevance. Biomed. Pharmacother. 2006, 60, 97-108.
73. Niles, L.P.; Wang, J.; Shen, L.; Lobb, D.K.; Younglai, E.V. Melatonin receptor mRNA expression in human granulosa cells. Mol. Cell. Endocrinol. 1999, 156, 107-110.
74. Soares, J.M., Jr.; Masana, M.I.; Ersahin, D.; Dubocovich, M.L. Functional melatonin receptors in rat ovaries at various stages of the estrous cycle. J. Pharmacol. Exp. Ther. 2003, 306, 694-702.
75. Brzezinski, A.; Seibel, M.M.; Lynch, H.J.; Deng, M.; Wurtman, R.J. Melatonin in human preovulatory follicular fluid. J. Clin. Endocrinol. Metab. 1987, 64, 865-867.
76. Ronnberg, L.; Kauppila, A.; Leppaluoto, J.; Martikainen, H.; Vakkuri, O. Circadian and seasonal variation in human preovulatory fluid melatonin concentration. J. Clin. Endocrinol. Metab. 1990, 71, 492-496.
77. 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.
78. Espey, L.L. Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol. Reprod. 1994, 50, 233-238.
79. Shi, J.M.; Tian, X.Z.; Zhan, 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.
80. 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.
81. Salhab, M.; Dhorne-Pollets, S.; Auclair, S.; Guyader-Joly, C.; Brisard, D.; Dalbies-Tran, R.; Dupont, J.; Ponsart, G.; Mermillod, P.; Uzbekova, S. In vitro maturation of oocytes alters gene expression and signaling pathways in bovine cumulus cells. Mol. Reprod. Dev. 2013, 80, 166-182.
82. Johnston, J.D.; Bashforth, R.; Diack, A.; Andersson, H.; Lincoln, G.A.; Hazelrigg, D.G. Rhythmic melatonin secretion does not correlate with the expression of arylalkylamine N-acetyltransferase, inducible cyclic AMP early repressor period 1 or cytochrome 1 mRNA in the sheep pineal. Neuroscience 2004, 124, 789-795.
83. Liu, T.; Borjigin, J. N-acetyltransferase is not the rate limiting enzyme of melatonin synthesis at night. J. Pineal Res. 2005, 39, 91-96.
84. Brannstrom, M.; Enskog, A. Leukocyte networks and ovulation. J. Reprod. Immunol. 2002, 57, 47-60.
85. Tamanini, C.; de Ambrogi, M. Angiogenesis in developing follicle and corpus luteum. Reprod. Domest. Anim. 2004, 39, 206-216.
86. Richards, J.S. Ovulation: New factors that prepare the oocyte for fertilization. Mol. Cell. Endocrinol. 2005, 234, 75-79.
87. Brannstrom, M.; Norman, R.J. Involvement of leucocytes and cytokines in the ovulatory process and corpus luteum function. Hum. Reprod. 1993, 8, 1762-1775.
88. Behrman, H.R.; Kodaman, P.H.; Preston, S.L.; Gao, S. Oxidative stress and the ovary. J. Soc. Gynecol. Investig. 2001, 8, S40-S42.
89. Sugino, N. Reactive oxygen species in ovarian physiology. Reprod. Med. Biol. 2005, 4, 31-44.
90. 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.
91. Allegra, M.; Reiter, R.J.; Tan, D.X.; Gentile, C.; Tesoriere, L.; Livrea, M.A. The chemistry of melatonin's interaction with reactive species. J. Pineal Res. 2003, 34, 1-10.
92. Antolin, I.; Rodriguez, C.; Sainz, R.M.; Mayo, J.C.; Uria, H.; Kotler, M.L.; Rodriguez-Colunga, M.J.; Toliva, D.; Menendez-Pelaez, A. Neurohormone melatonin prevents cell damage: Effect on gene expression for antioxidant enzymes. FASEB J. 1996, 10, 882-890.
93. 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.
94. Tomas-Zapico, C.; Coto-Montes, A. A proposed mechanism to explain the stimulating effect of melatonin on antioxidative enzymes. J. Pineal Res. 2005, 39, 99-104.
95. 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.
96. Tamura, H.; Takasaki, A.; Miwa, I.; Taniguchi, K.; Maekawa, R.; Asada, H.; Taketani, T.; Matsuoka, A.; Yamagata, Y.; Shimamura, K.; et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J. Pineal Res. 2008, 44, 280-287.
97. 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.
98. Qian, Y.; Shi, W.Q.; Ding, J.T.; Sha, J.H.; Fan, B.Q. Predictive value of the area of expanded cumulus mass on development of porcine oocytes matured and fertilized in vitro. J. Reprod. Dev. 2003, 49, 167-174.
99. Gutinsky, C.; Dalvit, G.C.; Pintos, L.N.; Thompson, J.G.; Beconi, M.T.; Cetica, P.D. Influence of hyaluronic acid synthesis and cumulus mucification on bovine oocyte in vitro maturation, fertilisation and embryo development. Reprod. Fertil. Dev. 2007, 19, 488-497.
100. Benitez-King, G.; Soto-Vega, E.; Dominguez-Rodriguez, G. Melatonin modulates microfilament phenotypes in epithelial cells: Implications for adhesion and inhibition of cancer cell migration. Histol. Histopathol. 2009, 24, 789-799
101. Acuna-Castroviejo, D.; Escames, G.; Rodriguez, M.; Lopez, L.C. Melatonin role in the mitochondrial function. Front. Biosci. 2007, 12, 947-963.
102. Rocha, R.M.P.; Lima, L.F.; Alves, A.M.C.V.; Celestino, J.J.H.; Matos, M.H.T.; Lima-Verde, I.B.; Bernuci, M.P.; Lopes, C.A.P.; Bao, S.N.; Campello, C.C.; et al. Interaction between melatonin and follicle-stimulating hormone promotes in vitro development of caprine preantral follicles. Dom. Anim. Endocrinol. 2013, 44, 1-9.
103. Dhalpuria, S.; Vyas, S.; Purohit, G.N.; Patkak, K.M. Songraphic monitoring of early follicle growth induced by melatonin implants in camels and the subsequent fertility. J. Ultrasound 2012, 15, 135-141.
104. Wilson, P.R.; Walker, I.H.; Bond, D.B.; Middleberg, A.; Staples, L.D. Field evaluation of melatonin implants to advance the breeding season in 1-year-old formed red deer hinds. N. Z. Vet. J. 1991, 39, 23-28.
105. Chemineau, P.; Berthelot, X.; Daneau, A.; Maurice, F.; Viguie, C.; Malpaux, B. Can melatonin be used in out-of-season reproduction in domestic mammals? Contracept. Fertil. Sex. 1993, 21, 733-738, [in French].
106. De Nicolo, G.; Morris, S.T.; Kenyon, P.R.; Morel, P.C.; Parkinson, T.J. Melatonin-improved reproductive performance in sheep bred out of season. Anim. Reprod. Sci. 2008, 109, 124-133.
107. Scott, P.R.; Sargison, N.D.; Macrae, A.L.; Gaugh, M.R. Melatonin treatment prior to the normal breeding season increases fetal number in United Kingdom sheep flocks. Vet. J. 2009, 182, 198-202.
108. Sirotkin, A.V.; Schaeffer, H.J. Direct regulation of mammalian reproductive organs by serotonin and melatonin. J. Endocrinol. 1997, 154, 1-5.
109. Murayama, T.; Kawashima, M.; Takahashi, T.; Yasuoka, T.; Kuwayama, T.; Tanaka, K. Direct action of melatonin on hen ovarian granulosa cells to lower responsiveness to luteinizing hormone. Proc. Soc. Exp. Biol. 1997, 215, 386-392.
110. Tamura, H.; Nakamura, Y.; Takiguchi, S.; Kashida, S.; Yamagata, Y.; Sugino, N.; Kato, H. Melatonin directly suppresses steroid production by preovulatory follicles in the cyclic hamster. J. Pineal Res. 1998, 35, 135-141.
111. Woo, M.M.M.; Tai, C.J.; Kang, S.K.; Nathwani, P.M.; Pang, S.F.; Leung, P.C.K. Direct action of melatonin in human granulosa-luteal cells. J. Clin. Endocrinol. Metab. 2001, 86, 4789-4797.
112. Fiske, V.M.; Parker, K.L.; Ulmer, R.A.; Ow, C.H.; Aziz, N. Effect of melatonin alone or in combination with human chorionic gonadotropin or ovine luteinizing hormone on the in vitro secretion of estrogens or progesterone by granulosa cells of rats. Endocrinology 1984, 114, 407-410.
113. Baratta, M.; Tamanini, C. Effect of melatonin on the in vitro secretion of progesterone and estradiol-17β by ovine granulosa cells. Acta Endocrinol. 1992, 127, 366-370.
114. Tanavde, V.S.; Maitra, A. In vitro modulation of steroidogenesis and gene expression by melatonin: A study with porcine antral follicles. Endocrinol. Res. 2003, 29, 399-410.
115. Webley, G.E.; Luck, M.R. Melatonin directly stimulates the secretion of progesterone by human bovine granulosa cells luteinized in vitro. J. Reprod. Fertil. 1986, 78, 711-717.
116. 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.
117. Hemadi, M.M.; Abolhassani, F.; Akbari, M.; Sobhani, A.; Pasbakhsh, P.; Ahrlund-Richter, L.; Modaresi, M.H.; Salehnia, M. Melatonin promotes the cumulus-oocyte complexes quality of vitrified-thawed murine ovaries with increases mean number of follicles survival and ovary size following heterotopic transplantation. Eur. J. Pharmacol. 2009, 618, 84-90.
118. Mazoochi, T.; Salehnia, M.; Valojerdi, M.R.; Mowla, S.J. Morphologic, ultrastructural, and biochemical identification of apoptosis in vitrified-warmed mouse ovarian tissue. Fertil. Steril. 2008, 90, 1480-1486.
119. Venegas, C.; Garcia, J.A.; Escames, G.; Ortiz, F.; Lopez, A.; Doerrier, G.; Garcia-Corzo, L.; Lopez, L.C.; Reiter, R.J.; Acuna-Castroviejo, D. Extrapineal melatonin: Analysis of its subcellular distribution and daily fluctuations. J. Pineal Res. 2012, 52, 217-227.
120. Vaughan, G.M.; Pelham, R.W.; Pang, S.F.; Laughlin, L.L.; Wilson, K.M.; Sandock, K.L.; Vaughan, M.K.; Koslow, S.H.; Reiter, R.J. Nocturnal elevation of plasma melatonin and urinary 5-hydroxyindoleacetic acid in young men: Attempts at modification by brief changes in environmental lighting and sleep and by autonomic drugs. J. Clin. Endocrinol. Metab. 1976, 42, 752-764.
121. Sun, X.; Liu, T.; Deng, J.; Borjigin, J. Long term invivo microdialysis. J. Pineal Res. 2003, 35, 118-124.
122. Lewy, A.J. Effects of light on human melatonin production and the human circadian system. Prog. Neuropsychopharmacol. Biol. Psychiatry 1983, 1, 551-556.
123. Yu, H.S.; Pang, S.F.; Tang, P.L. Increase in the level of retinal melatonin and its persistence of its diurnal rhythm after pinealectomy. J. Endocrinol. 1981, 91, 477-481.
124. Huether, G. The contribution of extrapineal sites of melatonin synthesis to circulating melatonin levels in higher vertebrates. Experientia 1993, 49, 665-670.
125. Bubenik, G.A. Localization, physiological significance and possible clinical implication of gastrointestinal melatonin. Biol. Signals Recept. 2001, 10, 350-366.
126. Tan, D.X.; Manchester, L.C.; Hardeland, R.; Lopez-Burillo, S.; Mayo, J.C.; Sainz, R.M.; Reiter, R.J. Melatonin: A hormone, a tissue factor, an autocoid, a paracoid and an antioxidant vitamin. J. Pineal Res. 2003, 34, 74-79.
127. Slominski, R.M.; Reiter, R.J.; Schlabritz-Loutsevitch, N.; Ostrom, R.S.; Slominski, A.T. Membrane melatonin receptors in peripheral tissues: Distribution and functions. Mol. Cell. Endocrinol. 2012, 351, 152-166.
128. Hardeland, R. Antioxidative protection by melatonin: Multiplicity of mechanisms from radical detoxification to radical avoidance. Endocrine 2005, 27, 119-130.
129. Hardeland, R.; Pandi-Perumal, S.R.; Cardinali, D.P. Melatonin. Int. J. Biochem. Cell Biol. 2006, 38, 313-316.
130. Iwazaki, S.; Nakazawa, K.; Sakai, J.; Kometani, K.; Mitsutoshi, I.; Yoshimura, Y.; Maruyama, T. Melatonin as a local regulator of human placental function. J. Pineal Res. 2005, 39, 261-265.
131. Stehle, J.H.; Sadde, A.; Rawashdeh, O.; Ackermann, K.; Jilg, A.; Sebesteng, 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.
132. Maronde, E.; Saade, A.; Ackermann, K.; Gougran-Botros, H.; Pagan, C.; Box, R.; Bourgeron, T.; Dehghani, F.; Stehte, J.H. Dynamics of enzymatic protein complexes offer a novel principle for the regulation of melatonin synthesis in the human pineal gland. J. Pineal Res. 2011, 51, 145-155.
133. Lanoix, D.; Beghdadi, H.; Lafond, J.; Vaillancourt, C. Human placental trophoblasts synthesize melatonin and express its receptors. J. Pineal Res. 2008, 45, 50-60.
134. Sainz, R.M.; Mayo, J.C.; Rodriguez, C.; Tan, D.X.; Lopez-Burillo, S.; Reiter, R.J. Melatonin and cell death: Differential actions in normal and cancer cells. Cell. Mol. Life Sci. 2003, 60, 1407-1426.
135. Lanoix, D.; Lacasse, A.A.; Reiter, R.J.; Vaillancourt, C. Melatonin, the smart killer: The human trophoblast as a model. Mol. Cell. Endocrinol. 2012, 348, 1-11.
136. Vaillancourt, C.; Lanoix, D.; LeBellego, F.; Daoud, G.; Lafond, J. Involvement of MAPK signaling in human villous trophoblast differentiation. Mini Rev. Med. Chem. 2009, 9, 962-973.
137. Castellucci, M.; Kaufmann, P.; Bischof, F. Extracellular matrix influences hormone and protein production by human chorionic villi. Cell Tiss. Res. 1990, 262, 135-142.
138. Fisher, S.J.; Cui, T.Y.; Zhang, L.; Hartman, L.; Grahl, K.; Zhang, G.Y.; Tarpey, J.; Damsky, C.H. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J. Cell. Biol. 1989, 109, 891-902.
139. Saundararajan, R.; Rao, A.J. Trophoblast "pseudo-tumorigenesis": Significance and contributory factors. Reprod. Biol. Endocrinol. 2004, 2, 15.
140. Mounier, C.; Barbeau, B.; Vaillancourt, C. Endocrinology and cell signaling in human villous trophoblast. Meth. Mol. Biol. 2009, 550, 89-102.
141. Fulia, F.; Gitto, E.; Cuzzocrea, S.; Reiter, R.J.; Dugo, L.; Gitto, P.; Barberi, S.; Cordaro, S.; Barberi, I. Increased levels of malondialdehyde and nitrite/nitrate in the blood of asphyxiated newborns: Reduction by melatonin. J. Pineal Res. 2001, 31, 343-349.
142. Richter, H.G.; Hansell, J.A.; Rout, S.; Giussani, D.A. Melatonin improves placental efficiency and birth weight and increases the placental expression of antioxidant enzymes in undernourished pregnancy. J. Pineal Res. 2009, 46, 357-364.
143. Chen, Y.C.; Tain, Y.L.; Sheen, J.M.; Huang, L.T. Melatonin in neonates and children. J. Formosa Med. Assoc. 2012, 111, 57-66.
144. Mitchell, M.D.; Sayers, L.; Keirse, M.J.; Anderson, A.B.; Turnbull, A.C. Melatonin in amniotic fluid during human parturition. Br. J. Obstet. Gynecol. 1978, 85, 684-686.
145. Kivela, A.; Kauppila, A.; Leppaluoto, J.; Vakkuri, O. Serum and amniotic fluid melatonin during human labor. J. Clin. Endocrinol. Metab. 1989, 69, 1065-1069.
146. Ciesla, W. Low ACTH and high melatonin concentrations in amniotic fluid as hormonal markers of high risk of fetal abnormalities. Preliminary studies. Perinat. Diagn. 1998, 18, 980-983.
147. Kaneko, Y.; Hayaski, T.; Yu, S.; Tajiri, N.; Bae, E.C.; Solomita, M.A.; Cheda, S.H.; Weinbren, N.L.; Parolini, O.; Borlongan, C.V. Human amniotic epithelial cells express melatonin receptor MT1, but not melatonin receptor MT2: A new perspective on neuroprotection. J. Pineal Res. 2011, 50, 272-280.
148. Xu, D.X.; Wang, H.; Ning, H.; Zhao, L.; Chen, Y.H. Maternally administered melatonin differentially regulates lipopolysaccharide-induced proinflammatory and anti-inflammatory cytokines in maternal serum, amniotic fluid, fetal liver, and fetal brain. J. Pineal Res. 2007, 43, 74-79.
149. Glattre, E.; Bjerkedal, T. The 24-hour rhythmicity of birth: A population study. Acta Obstet. Gynecol. Scand. 1983, 62, 31-36.
150. Cagnacci, A.; Soldani, R.; Melis, G.B.; Volpe, A. Diurnal rhythms of labor and delivery in women: Modulation by parity and seasons. Am. J. Obstet. Gynecol. 1998, 178, 140-145.
151. Ducsay, C.A.; Yellon, S.M. Photoperiod regulation of uterine activity and melatonin rhythms in pregnant rhesus macaque. Biol. Reprod. 1991, 44, 967-974.
152. Dickmeis, T. Glucocorticoids and the circadian clock. J. Endocrinol. 2009, 200, 3-22.
153. 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.
154. Reppert, S.M.; Weaver, D.R.; Ebisawa, T. Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and circadian responses. Neuron 1994, 13, 1175-1186.
155. Takayama, H.; Nakamura, Y.; Tamura, H.; Yamagata, Y.; Harada, A.; Nakata, M.; Surgino, N.; Kato, H. Pineal gland (melatonin) affects the parturition time, but not luteal function and fetal growth, in pregnant rats. Endocr. J. 2003, 50, 37-43.
156. Nathanielsz, P.W.; Guiseani, D.A.; Mecenas, C.A.; Wu, W.; Winter, J.A.; Garcia-Villar, R.; Baguma-Nibasheka, M.; Honnebier, M.B.; McDonald, T.J. Regulation of the switch from myometrial contractures to contractions in late pregnancy: Studies in pregnant sheep and monkey. Reprod. Fertil. Rev. 1995, 7, 595-602.
157. Leake, R.D.; Weitzman, R.E.; Glatz, T.H.; Fisher, D.A. Plasma oxytocin concentrations in men, nonpregnant women and pregnant women before and during spontaneous labor. J. Clin. Endocrinol. Metab. 1981, 53, 730-733.
158. Thornton, S.; Davison, J.M.; Baylis, P.H. Plasma oxytocin during the first and second stages of spontaneous human labor. Acta Endocrinol. 1992, 126, 425-429.
159. Chard, T. Fetal and maternal oxytocin in human parturition. Am. J. Perinatol. 1989, 6, 145-152.
160. Petraglia, F.; Imperatore, A.; Challis, J.R.G. Neuroendocrine mechanisms in pregnancy and parturition. Endocr. Rev. 2010, 31, 783-816.
161. Schlabritz-Loutsevitch N.; Hellner, N.; Middendorf, R.; Muller, D.; Olcese, J. The human myometrium as a target for melatonin. J. Clin. Endocrinol. Metab. 2003, 88, 908-913.
162. Sharkey, J.T.; Puttaramu, R.; Word, R.A.; Olcese, J. Melatonin synergizes with oxytocin to enhance contractility of human myometrial smooth muscle cells. J. Clin. Endocrinol. Metab. 2009, 94, 421-427.
163. Sharkey, J.; Cable, C.; Olcese, J. Melatonin sensitizes human myometrial cells to oxytocin in a PKCα/ERK-dependent manner. J. Clin. Endocrinol. Metab. 2010, 95, 2902-2908.
164. Olcese, J.; Lozier, S.; Paradise, B.S. Melatonin and the circadian timing of human parturition. Reprod. Sci. 2013, 20, 168-174.
165. Nakamara, Y.; Tamura, H.; Kashida, S.; Takayama, H.; Yamagata, Y.; Kurube, A.; Sergino, N.; Kato, H. Changes of serum melatonin level and its relationship to feto-placental unit during pregnancy. J. Pineal Res. 2001, 30, 29-33.
166. Kivela, A. Serum melatonin during human pregnancy. Acta. Endocrinol. 1991, 124, 233-237.
167. Gravett, M.G.; Rubens, C.E.; Nunes, T.M. Global report on preterm birth and stillbirth (2 of 7): Discovery science. BMC Pregnancy Childbirth 2010, 10, doi:10.1186/1471-2393-10-S1-S2.
168. Kwon, S.Y.; McIntyre, P.B.; Flecker, A.S.; Campbell, L.M. Mercury biomagnification in the food web of a neotropical stream. Sci. Total Environ. 2012, 417-418, 92-97.
169. Kirk, J.L.; Lehnherr, I.; Andersson, M.; Braune, B.M.; Chan, L.; Dastoor, A.P.; Durnford, D.; Gleason, A.L.; Loseto, L.L.; Steffen, A.; et al. Mercury in Arctic marine ecosystems: Sources, pathways and exposure. Environ. Res. 2012, 119, 64-87.
170. Koedrith, P.; Seo, Y.R. Advances in carcinogenic metal toxicity and potential molecular markers. Int. J. Mol. Sci. 2011, 12, 9576-9595.
171. Pal, P.B.; Pal, S.; Das, J.; Sil, P.C. Modulation of mercury-induced mitochondrial-dependent apoptosis by glycine in hepatocytes. Amino Acids 2012, 42, 1669-1683.
172. Rao, M.V.; Gangadharan, B. Antioxidant potential of melatonin against mercury induced intoxication in spermatozoa in vitro. Toxicol In Vitro 2008, 22, 935-942.
173. 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.
174. Peiris-John, R.J.; Wickremasinghe, R. Impact of low-level exposure to organophosphates on human reproduction and survival. Trans. R. Soc. Trop. Med. Hyg. 2008, 102, 239-245.
175. Jurewicz, J.; Hanke, W.; Radwan, M.; Bonde, J.P. Environmental factors and semen quality. Int. J. Occup. Med Environ Health 2009, 22, 305-329.
176. 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.
177. Tamme, L.A.; Still, D.L.; Acromite, M.T. Hypoxia and flight performance of military instructor pilots in a flight simulator. Aviat. Space Environ. Med. 2010, 81, 654-659.
178. 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.
179. Shiu, S.Y.; Li, L.; Siu, S.W.; Xi, S.C.; Fong, S.W.; Pang, S.F. Biological basis and possible physiological implications of melatonin receptor-mediated signaling in the rat epididymis. Biol. Signals Recept. 2000, 9, 172-187.
180. Li, L.; Wong, J.T.; Pang, S.F.; Shiu, S.Y. Melatonin-induced stimulation of rat corpus epididymal epithelial cell proliferation. Life Sci. 1999, 65, 1067-1076.
181. Sonmez, M.; Yüce, A.; Türk, G. The protective effects of melatonin and vitamin E on antioxidant enzyme activities and epididymal sperm characteristics of homocysteine treated male rats. Reprod. Toxicol. 2007, 23, 226-231.
182. 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.
183. Reiter, R.J. Exogenous and endogenous control of the annual reproductive cycle in the male golden hamster: Participation of the pineal gland. J. Exp. Zool. 1975, 191, 111-120.
184. Chaves, E.M.; Aguilera-Merlo, C.; Cruceno, A.; Fogal, T.; Piezzi, R.; Scardapane, L.; Dominquez, S. Seasonal morphological variations and age-related changes of the seminal vesicle of viscacha (Lagostomus maximus maximus): An ultrastructural and immunohistochemical study. Anat. Rec. 2012, 295, 886-895.
185. Jung-Hynes, B.; Huang, W.; Reiter, R.J.; Ahmad, N. Melatonin synchronizes dysregulated circadian rhythm circuitry in human prostate cancer cells. J. Pineal Res. 2010, 49, 60-68.
186. Shiu, S.Y.; Leung, W.Y.; Tam, C.W.; Liu, V.W.; Yao, K.M. Melatonin MT(1) receptor-induced translational up-regulation of p27(Kip 1) in prostate cancer antiproliferation is mediated via inhibition of constitutively active nuclear factor kappa B (NF-κB): Potential implications on prostate cancer chemoprevention and therapy. J. Pineal Res. 2012, in press.
187. Karasek, M.; Pawlikowski, M. Pineal gland, melatonin and cancer. Neuroendocrinol. Lett. 1999, 20, 139-144.
188. Shiu, S.Y. Toward rational and evidence-based use of melatonin in prostate cancer prevention and treatment. J. Pineal Res. 2007, 43, 1-9.
189. Casao, A.; Gallego, M.; Abecia, J.A.; Forcada, F.; Perez-Pe, R.; Muino-Blanco, T.; Cebrian-Perez, J.A. Identification and immunolocalisation of melatonin MT(1) and MT(2) receptors in Rasa aragonesa ram spermatozoa. Reprod. Fertil. Dev. 2012, 24, 953-961.
190. Kaya, A.; Aksoy, M.; Baspinar, N.; Yildiz, C.; Ataman, M.B. Effect of melatonin implantation to sperm donor rams on post-thaw viability and acrosomal integrity of sperm cells in the breeding and non-breeding season. Reprod. Domest. Anim. 2001, 36, 211-215.
191. Casao, A.; Vega, S.; Palacin, I.; Perez-Pe, R.; Levina, A.; Quintin, F.J.; Sevilla, E.; Abecia, J.A.; Cebrian-Perez, J.A.; Forcada, F.; et al. Effects of melatonin implants during non-breeding season on sperm motility and reproductive parameters in Rasa aragonesa rams. Reprod. Domest. Anim. 2010, 45, 425-432.
192. Webster, J.R.; Suttie, J.M.; Veenoliet, B.A.; Manley, T.R.; Littlejohn, R.P. Effect of melatonin implants in secretion of luteinizing hormone in intact and castrated rams. J. Reprod. Fertil. 1991, 92, 21-31.
193. 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.
194. Rosa, H.J.; Juniper, D.T.; Bryant, M.J. Effects of recent sexual experience and melatonin treatment of rams on plasma testosterone concentrations, sexual behavior and ability to induce ovulation in seasonally anestrous ewes. J. Reprod. Fertil. 2000, 120, 169-176.
195. Casao, A.; Luna, C.; Serrano, E. Quantification of Melatonin on Oxidized Proteins and Lipids in Ram Semen in the Breeding and Non-breeding Season. In XIII Jornadas sobre Produccion Animal; AIDA: Zaragoza, Spain, 2009; pp. 723-725.
196. Casao, A.; Mendoza, N.; Perez-Pe, R.; Grasa, P.; Abecia, J.A.; Forcada, F.; Cebrian-Perez, J.A.; Muino-Blanco, T. Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate. J. Pineal Res. 2010, 48, 39-46.
197. Balao da Silva, C.M.; Macias-Garcia, B.; Miro-Moran, A.; Gonzalez-Fernandez, L.; Morillo-Rodriguez, A.; Ortega-Fervisola, C.; Gallardo-Balanos, J.M.; Stillwell, G.; Topea, J.A.; Pena, F.J. Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. J. Pineal Res. 2011, 51, 172-179.
198. Bendahmane, M.; Lynch, C.; Tulsiani, D.R.P. Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa. Arch. Biochem. Biophys. 2001, 390, 1-8.
199. Tukiani, D.R.F.; Zeng, H.T.; Ibou-Haila, A. Biology of sperm capacitation: Evidence for multiple signaling pathways. Reprod. Fertil. 2007, 63, 357-372.
200. 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.
201. Ortega Ferrusola, C.; Gonzalez-Fernandez, L.; Macias Garcia, B.; Salazar-Sandoval, C.; Morillo-Rodriguez, A.; Rodriguez Martinez, H.; Tapia, J.A.; Pena, F.J. Effect of cryopreservation on nitric oxide production in stallion spermatozoa. Biol. Reprod. 2009, 81, 1106-1111.
202. Johnson, L.A.; Weitze, K.F.; Fiser, P.; Maxwell, W.M. Storage of boar semen. Anim. Reprod. Sci. 2000, 62, 143-172.
203. 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.
204. Garcia, J.J.; Reiter, R.J.; Guerrero, J.M.; Escames, G.; Yu, B.; Oh, C.S.; Munoz-Hayos, A. Melatonin prevents changes in microsomal membrane fluidity during induced lipid peroxidation. FEBS Lett. 1997, 408, 297-300.
205. Martin, M.; Macias, M.; Escames, G.; Reiter, R.J.; Agapito, M.T.; Ortiz, G.G.; Acuna-Castroviejo, D. Melatonin-induced increased activity of the respiratory chain complexes I and IV can prevent mitochondrial damage induced by ruthenium red in vivo. J. Pineal Res. 2000, 28, 242-248.
206. Martin, M.; Macias, M.; Leon, J.P.; Escames, G.; Khaldy, H.; Acuna-Castroviejo, D. Melatonin increases the activity of oxidative phosphorylation enzymes and the production of ATP in rat brain and liver mitochondria. Int. J. Biochem. Cell Biol. 2002, 34, 348-357.
207. Leon, J.; Acuna-Castroviejo, D.; Sainz, R.M.; Mayo, J.C.; Tan, D.X.; Reiter, R.J. Melatonin and mitochondrial function. Life Sci. 2004, 75, 765-790.
208. Jou, M.J.; Peng, T.I.; Yu, P.Z.; Jou, S.B.; Reiter, R.J.; Chen, J.Y.; Wu, H.Y.; Chen, C.C.; Hsu, L.F. Melatonin protects against common deletion of mitochondrial DNA-augmented mitochondrial oxidative stress and apoptosis. J. Pineal Res. 2007, 43, 389-403.
209. Benitez-King, G.; Anton-Tay, F. Calmodulin mediates melatonin cytoskeletal effects. Experientia 1993, 49, 35-41.
210. Johnson, L.A. Sexing mammalian sperm for production of offspring: The state-of-the-art. Anim. Reprod. Sci. 2000, 60-61, 93-107.
211. Agawal, A.; Probakaran, A.S. Mechanism, measurements, and prevention of oxidative stress in male reproductive physiology. Indian J. Exp. Biol. 2005, 43, 963-974.
212. 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. Dom. Anim. 2012, 47, 299-307.
213. Fujinoki, M. Melatonin-enhanced hyperactivation of hamster sperm. Reproduction 2008, 136, 533-541.
214. Fujinoki, M.; Suzuki, T.; Takayama, T.; Shibahara, H.; Ohtake, H. Profiling of proteins phosphorylated or dephosphorylated during hyperactivation via activation on hamster spermatozoa. Reprod. Med. Biol. 2006, 5, 123-135.
215. Pitout, N.J.; VanVuuren, R.J.J.; van Aswegen, C.H.; Theron, J.J. Melatonin and sperm motility. S. Afr. Med. J. 1991, 79, 683.
216. Du Toit, D.; Bornman, M.S.; van Aswegen, C.H.; du Plessis, D.J. Sialic acid concentration and sperm motility. Arch. Androl. 1994, 32, 21-23.
217. Browning, C.; Beresford, J.; Fraser, N.; Giles, H. Pharmacological characterization of human recombinant melatonin mt1 and MT2 receptors. Br. J. Pharmacol. 2000, 129, 877-886.
218. 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.
219. Luboshitzky, R.; Shen-Orr, Z.; Nave, R.; Lavi, S.; Lavie, P. Melatonin administration alters semen quality in healthy men. J. Androl. 2002, 23, 572-578.
220. Lerchl, A. Melatonin administration alters semen quality in normal men. J. Androl. 2004, 25, 185-187.
221. Acuna-Castroviejo, D.; Lopez, L.C.; Escames, G.; Lopez, A.; Garcia, J.A.; Reiter, R.J. Melatonin-mitochondria interplay in health and disease. Curr. Top. Med. Chem. 2011, 11, 221-240.
222. Shang, X.; Huang, Y.; Ye, Z.; Yu, X.; Gu, W. Protection of melatonin against damage of sperm mitochondrial function induced by reactive oxygen species. Zhonghaw Nan Ke Xue 2004, 10, 604-607, [In Chinese].
223. 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.
224. Espino, J.; Bejarano, I.; Ortiz, A.; Lozano, G.M.; Garcia, J.F.; Pariente, J.A.; Rodriguez, A.B. Melatonin as a potential tool against oxidative damage and apoptosis in ejaculated human spermatozoa. Fertil. Steril. 2010, 94, 1915-1917.
225. Espino, J.; Ortiz, A.; Bejarano, I.; Lozano, G.M.; Monllor, F.; Garcia, J.F.; Rodriguez, A.B.; Pariente, J.A. Melatonin protects human spermatozoa from apoptosis via melatonin receptor-and extracellular signal-regulated kinase-mediated pathways. Fertil. Steril. 2011, 95, 2290-2296.
226. Ortiz, A.; Espino, J.; Bejarano, I.; Lozano, G.M.; Monllor, F.; Garcia, J.F.; Pariente, J.A.; Rodriguez, A.B. High endogenous melatonin concentrations enhance sperm quality and short-term in vitro exposure improves aspects of sperm motility. J. Pineal Res. 2011, 50, 132-139.
227. Oba, S.; Nakamura, K.; Sahashi, Y.; Hattori, A.; Nagata, C. Consumption of vegetables alters urinary 6-sulfatoxymelatonin concentrations. J. Pineal Res. 2008, 45, 17-23.
228. Tan, D.X.; Manchester, L.C.; Liu, X.; Rosales-Corral, S.A.; Acuna-Castroviejo, D.; Reiter, R.J. Mitochondria and chloroplasts as the original sites of melatonin synthesis: A hypothesis related to melatonin's primary function and evaluation in eukaryotes. J. Pineal Res. 2013, 54, 127-138.
229. Reiter, R.J.; Richardson, B.A.; Johnson, L.J.; Ferguson, B.N.; Dink, D.T. Pineal melatonin rhythm: Reduction in aging Syrian hamsters. Science 1980, 210, 1372-1373.
230. Reiter, R.J.; Craft, C.M.; Johnson, J.E., Jr.; King, T.S.; Richardson, B.A.; Vaughan, G.M.; Vaughan, M.K. Age-associated reduction in nocturnal pineal melatonin levels in female rats. Endocrinology 1981, 109, 1295-1297.
231. Iguchi, H.; Kato, K.I.; Ibayashi, H. Age-dependent reduction in serum melatonin concentrations in healthy human subjects. J. Clin. Endocrinol. Metab. 1982, 55, 27-29.
232. Sack, R.L.; Lewy, A.J.; Erb, D.L.; Vollmer, W.M.; Singer, C.M. Human melatonin production decreases with age. J. Pineal Res. 1989, 3, 379-388.
233. Benot, S.; Goberna, R.; Reiter, R.J.; Garcia-Maurino, S.; Osuna, C.; Guerrero, J.M. Physiological levels of melatonin contribute to the antioxidant capacity of human serum. J. Pineal Res. 1999, 27, 59-64.
234. Sanchez-Hildalgo, M.; de la Lastra, C.A.; Carrascosa-Salmoral, M.P.; Naranjo, M.C.; Gomez-Corvera, A.; Caballero, B.; Guerrero, J.M. Age-related changes in melatonin synthesis in extrapineal tissues. Exp. Gerontol. 2009, 44, 328-334.
235. Witt-Enderby, P.A.; Radio, N.M.; Doctor, D.S.; Davis, V.L. Therapeutic treatments potentially mediated by melatonin receptors: Potential clinical uses of melatonin in the prevention of osteoporosis, cancer and as an adjuvant therapy. J. Pineal Res. 2006, 41, 297-305.
236. Sanchez-Barcelo, E.; Mediavilla, M.D.; Tan, D.X.; Reiter, R.J. Clinical uses of melatonin: Evaluation of clinical trials. Curr. Med. Chem. 2010, 17, 2070-2095.
237. Sanchez-Barcelo, E.; Mediavilla, M.D.; Tan, D.X.; Reiter, R.J. Scientific basis for the potential use of melatonin in bone diseases: Osteoporosis and adolescent idiopathic scoliosis. J. Osteoporos. 2010, doi:10.4061/2010/830231.
238. Cardinali, D.P.; Vigo, D.E.; Olivar, N.; Vidal, M.F.; Furio, A.M.; Brusco, L.I. Therapeutic application of melatonin in mild cognitive impairment. Am. J. Neurodegener. Dis. 2012, 1, 280-291.
239. Rosales-Corral, S.A.; Acuna-Castroviejo, D.; Cato-Montes, A.; Boga, J.A.; Manchester, L.C.; Fuentes-Broto, L.; Korkmaz, A.; Ma, S.; Tan, D.X.; Reiter, R.J. Alzheimer's disease: Pathological mechanisms and the beneficial role of melatonin. J. Pineal Res. 2012, 52, 167-202.
240. Reiter, R.J. Melatonin: Lowering the high price of free radicals. News Physiol. Sci. 2000, 15, 246-250.
241. Reyes, J.G.; Farias, J.G.; Henriquez-Olavavieta, S.; Madrid, E.; Parraga, M.; Zepeda, A.B.; Moreno, R.D. The hypoxic testicle; physiology and pathophysiology. Oxid. Med. Cell. Long. 2013, in press.
242. Aversa, S.; Pellegrino, S.; Barberi, I.; Reiter, R.J.; Gitto, E. Potential utility of melatonin as an antioxidant during pregnancy and during the perinatal period. J. Matern. Fetal Neonat. Med. 2012, 25, 207-221.
243. Lavranos, G.; Balla, M.; Tzortzopoulou, A.; Syriou, V.; Angelopoulou, R. Investigating ROS sources in male infertility: A common end for numerous pathways. Reprod. Toxidol. 2012, 34, 298-307.
244. Reiter, R.J. Normal patterns of melatonin levels in the pineal gland and body fluids of humans and experimental animals. J. Neural. Transm. 1986, 21, 35-54.
245. Schenker, S.; Yang, Y.; Perez, A.; Acuff, R.V.; Papas, A.M.; Henderson, G.; Lee, M.P. Antioxidant transport by the human placenta. Clin. Nutr. 1998, 17, 159-167.
246. Okatani, Y.; Okamoto, K.; Hayaski, K.; Wakatsuki, A.; Tamura, S.; Sugara, Y. Maternal-fetal transfer of melatonin in pregnant woman near term. J. Pineal Res. 1998, 26,129-134.
247. Wakatsuki, A.; Okatani, Y.; Shinokara, K.; Ikenoue, N.; Fukaya, T. Melatonin protects against isthemia/reperfusion-induced oxidative damage to mitochondria in fetal rat brain. J. Pineal Res. 2001, 31, 167-172.
248. Miller, S.L.; Yan, E.B.; Castillo-Melendez, M.; Jenkin, G.; Walker, D.W. Melatonin provides neuroprotection in the late-gestation fetal sheep brain in response to umbilical cord occlusion. Dev. Neurosci. 2005, 27, 200-210.
249. Jahnke, G.; Marr, M.; Myers, C.; Wilson, R.; Travlos, S.; Price, C. Maternal and developmental toxicity evaluation of melatonin administered orally to pregnant Sprague-Dawley rats. Toxicol. Sci. 1999, 50, 271-279.
250. Alvarez, B.E.; Rodriguez, E.D.; Alvarez, C.F.; Martinez, P.N.; Lopez, B.D. Ovarian aging: Melatonin regulation of the cytometric and endocrine evaluative pattern. Curr. Aging Sci. 2012, in press.
251. Bubenik, G.A.; Blask, D.E.; Brown, G.M.; Maestroni, G.; Pang, S.F.; Reiter, R.J.; Viswanathan, M.; Zisapel, N. Prospects on the clinical utilization of melatonin. Biol. Signals Recept. 1998, 7, 195-219.
252. Gitto, E.; Reiter, R.J.; Korbownick, M.; Tan, D.X.; Gitto, D.; Barberi, S.; Barberi, I. Causes of oxidative stress in the pre-and perinatal period. Neonatology 2002, 81, 146-157.
253. Reiter, R.J. Melatonin: Clinical relevance. Best Pract. Res. Clin. Endocrinol. Metab. 2003, 17, 273-285.
254. Blask, D.E. Melatonin, sleep disturbance and cancer risk. Sleep Med. Rev. 2009, 13, 257-264.
255. Korkmaz, A.; Reiter, R.J.; Topal, T.; Manchester, L.C.; Oter, S.; Tan, D.X. Melatonin, an established antioxidant worthy of clinical use. Mol. Med. 2009, 15, 43-50.
256. Wang, X.; Sirianni, A.; Pei, Z.; Cormier, L.; Smith, K.; Jiang, J.; Zhan, S.; Wang, H.; Zhao, R.; Yano, H.; et al. The melatonin MT1 receptor axis modulates mutant Huntingtin-mediated toxicity. J. Neurosci. 2011, 31, 14496-14507.
257. Gitto, E.; Aversa, S.; Reiter, R.J.; Barberi, I.; Pelligrino, S. Update on the use of melatonin in pediatrics. J. Pineal Res. 2011, 50, 21-28.
258. Proietti, S.; Cucina, A.; Reiter, R.J.; Bizzarsi, M. Molecular mechanisms of melatonin's inhibitory actions on breast cancer. Mol. Cell. Life Sci. 2013, in press.