Essential actions of melatonin in protecting the ovary from oxidative damage

Theriogenology

Volumn 82, Issue 7, 2014, Pages 925-932

  Cruz, M H C ^a   Leal, C L V ^a   Cruz, J F ^b   Tan, D X ^c   Reiter, R J ^c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDADE ESTADUAL DO SUDOESTE DA BAHIA   (Brazil)

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

Author keywords

Follicle; Oxidative stress; Radical scavenging; Reactive species

Indexed keywords

MELATONIN;

ANIMAL; FEMALE; GENE EXPRESSION REGULATION; METABOLISM; OVARY; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; MELATONIN; OVARY; OXIDATIVE STRESS;

EID: 84908031545     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2014.07.011     Document Type: Review

References (96)

1. Devine P.J., Perreault S.D., Luderer U. Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol Reprod 2012, 86:27.
2. 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.
3. Tamura H., Nakamura Y., Korkmaz A., Manchester L.C., Tan D.X., Sugino N., et al. Melatonin and the ovary: physiological and pathophysiological implication. Fertil Steril 2009, 92:328-343.
4. 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.
5. 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.
6. 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.
7. Reiter R.J., Tan D.X., Manchester L.C., El-Sawi M.R. Melatonin reduces oxidant damage and promotes mitochondrial respiration implications for aging. Ann N Y Acad Sci 2002, 959:238-250.
8. Korkmaz A., Rosales-Corral S., Reiter R.J. Gene regulation by melatonin linked to epigenetic phenomena. Gene 2012, 503:1-11.
9. Halliwell B. Free radicals and antioxidants: updating a personal view. Nutr Rev 2012, 70:257-265.
10. Bashan N., Kovsan J., Kachko I., Ovadia H., Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev 2009, 89:27-71.
11. Reiter R.J., Carneiro R.C., Oh C.S. Melatonin in relation to cellular antioxidative defense mechanisms. Horm Metab Res 1997, 29:363-372.
12. 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 invitro fertilization. Fertil Steril 2011, 96:1357-1361.
13. Dennery P.A. Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today 2007, 81:155-162.
14. Martin-Romero F.J., Miguel-Lasobras E.M., Dominguez-Arroyo J.A., Gonzalez-Carrera E., Alvarez I.S. Contribution of culture media to oxidative stress and its effects on human oocytes. Reprod Biomed Online 2008, 17:652-661.
15. Agarwal A., Aponte-Mellado A., Premkumar B.J., Shaman A., Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 2012, 10:49.
16. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 2002, 82:47-95.
17. Zamberlam G., Portela V., de Oliveira J.F., Gonçalves P.B., Price C.A. Regulation of inducible nitric oxide synthase expression in bovine ovarian granulosa cells. Mol Cell Endocrinol 2011, 335:189-194.
18. Mani S.K., Allen J.M., Rettori V., McCann S.M., O'Malley B.W., Clark J.H. Nitric oxide mediates sexual behavior in female rats. Proc Natl Acad Sci U S A 1994, 91:6468-6472.
19. Van Voorhis B.J., Dunn M.S., Snyder G.D., Weiner C.P. Nitric oxide: an autocrine regulator of human granulosa-luteal cell steroidogenesis. Endocrinology 1994, 135:1799-1806.
20. Gomes E.C., Silva A.N., de Oliveira M.R. Oxidants, antioxidants, and the beneficial roles of exercise-induced production of reactive species. Oxid Med Cell Longev 2012, 2012:756132.
21. Tamura H., Takasaki A., Taketani T., Tanabe M., Kizuka F., Lee L., et al. The role of melatonin as an antioxidant in the follicle. J Ovarian Res 2012, 5:5.
22. Gutteridge J.M. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 1995, 41:1819-1828.
23. Esterbauer H., Schaur J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malondialdehyde and related aldehydes. Free Radic Biol Med 1991, 11:81-128.
24. Pizzimenti S., Toaldo C., Pettazzoni P., Dianzani U.M., Barrera G. The "two-faced" effects of reactive oxygen species and the lipid peroxidation product 4-hydroxynonenal in the hallmarks of cancer. Cancers (Basel) 2010, 2:338-363.
25. Richter C. Biophysical consequences of lipid peroxidation in membranes. Chem Phys Lipids 1987, 44:175-189.
26. Stadtman E.R. Protein oxidation and aging. Science 1992, 257:1220-1224.
27. Reiter R.J. The role of the neurohormone melatonin as a buffer against macromolecular oxidative damage. Neurochem Int 1995, 27:453-460.
28. Kim C.H., Jeon H.M., Lee S.Y., Jeong E.K., Ju M.K., Park B.J., et al. Role of reactive oxygen species-dependent protein aggregation in metabolic stress-induced necrosis. Int J Oncol 2010, 37:97-102.
29. Yu B.P. Cellular defenses against damage from reactive oxygen species. Physiol Rev 1994, 74:1399162.
30. Davis K.L., Martin E., Turko I.V., Murad F. Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 2001, 41:203-236.
31. Monteiro H.P., Gruia-Gray J., Peranovich T.M.S., Oliveira L.C.B., Stern A. Nitric oxide stimulates tyrosine phosphorylation of focal adhesion kinase, SRC kinase, and mitogen-activated protein kinases in murine fibroblasts. Free Radic Biol Med 2000, 28:174-182.
32. Ménézo Y., Dale B., Cohen M. DNA damage and repair in human oocytes and embryos: a review. Zygote 2010, 18:357-365.
33. Evans M.D., Dizdaroglu M., Cooke M.S. Oxidative DNA damage and disease: induction, repair and significance. Mutat Res 2004, 567:1-61.
34. Chappel S. The role of mitochondria from mature oocyte to viable blastocyst. Obstet Gynecol Int 2013, 2013:183024.
35. Richter C. Reactive oxygen and DNA damage in mitochondria. Mutat Res 1992, 275:249-255.
36. Wiseman H., Halliwell B. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J 1996, 313:17-29.
37. 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.
38. Reiter R.J., Fraschini F. Endocrine aspects of the mammalian pineal gland: a review. Neuroendocrinology 1969, 5:219-255.
39. Barrett P., Bolborea M. Molecular pathways involved in seasonal body weight and reproductive responses governed by melatonin. J Pineal Res 2012, 52:376-388.
40. Tan D.X., Reiter R.J., Manchester L.C., Yan M.T., El Sawi M., Sainz R.M., et al. 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.
41. Reiter R.J., Tan D.X., Gitto E., Sainz R.M., Mayo J.C., Leon J., et al. Pharmacological utility of melatonin in reducing oxidative cellular and molecular damage. Pol J Pharmacol 2004, 56:159-170.
42. 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.
43. Urata Y., Honma S., Goto S., Todoroki S., Iida T., Cho S., et al. Melatonin induces gammaglutamylcysteine synthetase mediated by activator protein-1 in human vascular endothelial cells. Free Radic Biol Med 1999, 27:838-847.
44. Hardeland R. Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification to radical avoidance. Endocrine 2005, 27:119-130.
45. Lowes D.A., Webster N.R., Murphy M.P., Galley H.F. Antioxidants that protect mitochondria reduce interleukin-6 and oxidative stress, improve mitochondrial function, and reduce biochemical markers of organ dysfunction in a rat model of acute sepsis. Br J Anaesth 2012, 110:472-480.
46. Carlomagno G., Nordio M., Chiu T.T., Unfer V. Contribution of myo-inositol and melatonin to human reproduction. Eur J Obstet Gynecol Reprod Biol 2011, 159:267-272.
47. Reiter R.J., Tan D.X., Manchester L.C., Qi W. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem Biophys 2001, 34:237-256.
48. 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.
49. Ferreira S.G., Peliciari-Garcia R.A., Takahashi-Hyodo S.A., Rodrigues A.C., Amaral F.G., Berra C.M., et al. Effects of melatonin on DNA damage induced by cyclophosphamide in rats. Braz J Med Biol Res 2013, 46:278-286.
50. Sliwinski T., Rozej W., Morawiec-Bajda A., Morawiec Z., Reiter R., Blasiak J. Protective action of melatonin against oxidative DNA damage: chemical inactivation versus base-excision repair. Mutat Res 2007, 634:220-227.
51. Tamura H., Takasaki A., Taketani T., Tanabe M., Kizuka F., Lee L., et al. Melatonin as a free radical scavenger in the ovarian follicle. Endocr J 2013, 60:1-13.
52. 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.
53. 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.
54. Al-Gubory K.H., Bolifraud P., Germain G., Nicole A., Ceballos-Picot I. Antioxidant enzymatic defence systems in sheep corpus luteum throughout pregnancy. Reproduction 2004, 128:767-774.
55. Halliwell B., Gutteridge J.M. Free radicals and antioxidant protection: mechanisms and significance in toxicology and disease. Hum Toxicol 1988, 7:7-13.
56. Hussein T.S., Froiland D.A., Amato F., Thompson J.G., Gilchrist R.B. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci 2005, 118:5257-5268.
57. Foghi A., Ravandi A., Teerds K.J., Van Der Donk H., Kuksis A., Dorrington J. Fas-induced apoptosis in rat thecal/interstitial cells signals through sphingomyelin-ceramide pathway. Endocrinology 1998, 139:2041-2047.
58. Savill J., Fadok V. Corpse clearance defines the meaning of cell death. Nature 2000, 407:784-788.
59. Ott M., Robertson J.D., Gogvadze V., Zhivotovsky B., Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci U S A 2002, 99:1259-1263.
60. Hsu S.Y., Lai R.J., Finegold M., Hsueh A.J. Targeted overexpression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology 1996, 137:4837-4843.
61. Ptak A., Ludewig G., Kapiszewska M., Magnowska Z., Lehmler H.J., Robertson L.W., et al. Induction of cytochromes P450, caspase-3 and DNA damage by PCB3 and its hydroxylated metabolites in porcine ovary. Toxicol Lett 2006, 166:200-211.
62. Brzezinski A., Seibel M.M., Lynch H.J., Deng M.H., Wurtman R.J. Melatonin in human preovulatory follicular fluid. J Clin Endocrinol Metab 1987, 64:865-867.
63. 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.
64. Cruz M.H., Leal C.L., de Cruz J.F., Tan D.X., Reiter R.J. Role of melatonin on production and preservation of gametes and embryos: a brief review. Anim Reprod Sci 2014, 145:150-160.
65. Rocha R.M., Lima L.F., Alves A.M., Celestino J.J., Matos M.H., Lima-Verde I.B., et al. Interaction between melatonin and follicle-stimulating hormone promotes invitro development of caprine preantral follicles. Domest Anim Endocrinol 2013, 44:1-9.
66. Tamura H., Nakamura Y., Terron M.P., Flores L.J., Manchester L.C., Tan D.X., et al. Melatonin and pregnancy in the human. Reprod Toxicol 2008, 25:291-303.
67. Liu F., Ng T.B. Effect of pineal indoles on activities of the antioxidant defense enzymes superoxide dismutase, catalase, and glutathione reductase, and levels of reduced and oxidized glutathione in rat tissues. Biochem Cell Biol 2000, 78:447-453.
68. Wang F., Tian X., Zhang L., Tan D., Reiter R.J., Liu G. Melatonin promotes the invitro development of pronuclear embryos and increases the efficiency of blastocyst implantation in murine. J Pineal Res 2013, 55:267-274.
69. 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.
70. 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.
71. 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.
72. Tripathi A., Khatun S., Pandey A.N., Mishra S.K., Chaube R., Shrivastava T.G., et al. Intracellular levels of hydrogen peroxide and nitric oxide in oocyte at various stages of meiotic cell cycle and apoptosis. Free Radic Res 2009, 43:287-294.
73. Cui M.S., Wang X.L., Tang D.W., Zhang J., Liu Y., Zeng S.M. Acetylation of H4K12 in porcine oocytes during invitro aging: potential role of ooplasmic reactive oxygen species. Theriogenology 2011, 75:638-646.
74. Agarwal A., Gupta S., Sharma R.K. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005, 3:28.
75. Zhang M., Ouyang H., Xia G. The signal pathway of gonadotropins induced mammalian oocyte meiotic resumption. Mol Hum Reprod 2009, 15:399-409.
76. Kowaltowski A.J., Vercesi A.E. Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med 1999, 26:463-471.
77. Reiter R.J. Melatonin: lowering the high price of free radicals. News Physiol Sci 2000, 15:246-250.
78. Leon J., Acuña-Castroviejo D., Escames G., Tan D.-X., Reiter R.J. Melatonin mitigates mitochondrial malfunction. J Pineal Res 2005, 38:1-9.
79. 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 evolution in eukaryotes. J Pineal Res 2013, 54:127-138.
80. Venegas C., García J.A., Escames G., Ortiz F., López A., Doerrier C., et al. Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations. J Pineal Res 2012, 52:217-227.
81. Çelik O., Naz iroğlu M. Melatonin modulates apoptosis and TRPM2 channels in transfected cells activated by oxidative stress. Physiol Behav 2012, 107:458-465.
82. Tamura H., Takasaki A., Miwa I., Taniguchi K., Maekawa R., Asada H., 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.
83. Espey L.L. Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol Reprod 1994, 50:233-238.
84. Sugino N. Roles of reactive oxygen species in the corpus luteum. Anim Sci J 2006, 77:556-565.
85. Lee S., Acosta T.J., Nakagawa Y., Okuda K. Role of nitric oxide in the regulation of superoxide dismutase and prostaglandin F (2alpha) production in bovine luteal endothelial cells. J Reprod Dev 2010, 56:454-459.
86. Rizzo A., Roscino M.T., Binetti F., Sciorsci R.L. Roles of reactive oxygen species in female reproduction. Reprod Domest Anim 2012, 47:344-352.
87. Vu H.V., Acosta T.J., Yoshioka S., Abe H., Okuda K. Roles of prostaglandin F2alpha and hydrogen peroxide in the regulation of copper/zinc superoxide dismutase in bovine corpus luteum and luteal endothelial cells. Reprod Biol Endocrinol 2012, 26:87.
88. Sugino N., Takiguchi S., Kashida S., Takayama H., Yamagata Y., Nakamura Y., et al. Suppression of intracellular superoxide dismutase activity by antisense oligonucleotides causes inhibition of progesterone production by rat luteal cells. Biol Reprod 1999, 61:1133-1138.
89. Taketani T., Tamura H., Takasaki A., Lee L., Kizuka F., Tamura I., et al. Protective role of melatonin in progesterone production by human luteal cells. J Pineal Res 2011, 51:207-213.
90. Minegishi K., Tanaka M., Nishimura O., Tanigaki S., Miyakoshi K., Ishimoto H., et al. Reactive oxygen species mediate leukocyte-endothelium interactions in prostaglandin F2alpha-induced luteolysis in rats. Am J Physiol Endocrinol Metab 2002, 283:1308-1315.
91. Miyamoto K., Sato E.F., Kasahara E., Jikumaru M., Hiramoto K., Tabata H., et al. Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria. Free Radic Biol Med 2010, 49:674-681.
92. Tanaka M., Miyazaki T., Tanigaki S., Kasai K., Minegishi K., Miyakoshi K., et al. Participation of reactive oxygen species in PGF2alpha-induced apoptosis in rat luteal cells. J Reprod Fertil 2000, 120:239-245.
93. Hayashi K., Miyamoto A., Konari A., Ohtani M., Fukui Y. Effect of local interaction of reactive oxygen species with prostaglandin F (2alpha) on the release of progesterone in ovine corpora lutea invivo. Theriogenology 2003, 59:1335-1344.
94. Scarpellini F., Mastrone M., Sbracia M., Scarpellini L. Serum lipoperoxide level variations in normal and luteal phase defect cycles. Gynecol Obstet Invest 1996, 42:28-30.
95. Maganhin C.C., Fuchs L.F., Simões R.S., Oliveira-Filho R.M., de Jesus Simões M., Baracat E.C., et al. Effects of melatonin on ovarian follicles. Eur J Obstet Gynecol Reprod Biol 2013, 166:178-184.
96. Hockenbery D.M., Oltvai Z.N., Yin X.-M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993, 75:241-251.