Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Beneficial effects of melatonin on in vitro embryo production from juvenile goat oocytes

Sandra Soto-Heras A , Montserrat Roura A , Maria G. Catalá A , Irene Menéndez-Blanco A , Dolors Izquierdo A , Ali A. Fouladi-Nashta B and Maria T. Paramio A C
+ Author Affiliations
- Author Affiliations

A Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Universitat Autònoma de Barcelona, Travessera dels Turons s/n, 08193 Bellaterra, Barcelona, Spain.

B Reproduction Genes and Development Group, Department of Veterinary Basic Sciences, The Royal Veterinary College, Hawkshead Lane, Hatfield, Herts AL97TA, UK.

C Corresponding author. Email: teresa.paramio@uab.cat

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17170
Submitted: 25 January 2017  Accepted: 31 May 2017   Published online: 19 June 2017

Abstract

Melatonin is a universal antioxidant that improves in vitro embryo production in several species. The aims of this study were to determine the melatonin concentration in the ovarian follicular fluid (FF) of juvenile goats and the effect of melatonin during in vitro maturation (IVM) on embryo development. The FF melatonin concentration was 0.57­–1.07 × 10-9 M, increasing with follicular diameter. Oocytes were matured, fertilised and cultured under conventional conditions. Blastocyst development, embryo quality and levels of reactive oxygen species (ROS) and reduced glutathione were assessed. In Experiment 1 different melatonin concentrations (10-3, 10-7, 10-9, 10-11 M) were added to the IVM medium, which contained cysteamine as antioxidant, and no differences were observed. In Experiment 2, melatonin (10-7 M) was tested in the presence or absence of cysteamine (experimental groups: melatonin, cysteamine, melatonin + cysteamine, non-antioxidant). The melatonin group presented a higher blastocyst rate than the non-antioxidant group (28.9 vs 11.7%; P < 0.01) and a higher total cell number than the cysteamine group (225.1 vs 129.0; P < 0.05). Oocytes from the melatonin and cysteamine groups had lower ROS levels than those from the non-antioxidant group. This study shows that melatonin is an interesting tool for improving oocyte competence in juvenile goats as it increases embryo production and quality.

Additional keywords: cysteamine, embryo development, in vitro maturation, oocyte competence, reactive oxygen species.


References

Bahadori, M. H., Ghasemian, F., Ramezani, M., and Asgari, Z. (2013). Melatonin effect during different maturation stages of oocyte and subsequent embryo development in mice. Iran. J. Reprod. Med. 11, 11–18.
| 1:CAS:528:DC%2BC3sXpsFCnsrw%3D&md5=7221c8389170646d9bdea67d6e451c56CAS |

Banerjee, J., Maitra, D., Diamond, M. P., and Abu-Soud, H. M. (2012). Melatonin prevents hypochlorous acid-induced alterations in microtubule and chromosomal structure in metaphase-II mouse oocytes. J. Pineal Res. 53, 122–128.
Melatonin prevents hypochlorous acid-induced alterations in microtubule and chromosomal structure in metaphase-II mouse oocytes.CrossRef | 1:CAS:528:DC%2BC38Xht1arurzO&md5=e54d7375499004d424a0cc5a9cf39010CAS |

Barros, V. R. P., Cavalcante, A. Y. P., Macedo, T. J. S., Barberino, R. S., Lins, T. L. B., Gouveia, B. B., Menezes, V. G., Queiroz, M. A. A., Araújo, V. R., Palheta, R. C., Leite, M. C. P., and Matos, M. H. T. (2013). Immunolocalization of melatonin and follicle-stimulating hormone receptors in caprine ovaries and their effects during in vitro development of isolated pre-antral follicles. Reprod. Domest. Anim. 48, 1025–1033.
Immunolocalization of melatonin and follicle-stimulating hormone receptors in caprine ovaries and their effects during in vitro development of isolated pre-antral follicles.CrossRef | 1:CAS:528:DC%2BC3sXhslKnsrzP&md5=7a124cfdd38c8817844a1a890facaa11CAS |

Casao, A., Abecia, J. A., Cebrián-Pérez, J. A., Muiño-Blanco, T., Vázquez, M. I., and Forcada, F. (2010). The effects of melatonin on in vitro oocyte competence. Span. J. Agric. Res. 8, 35–41.
The effects of melatonin on in vitro oocyte competence.CrossRef |

Catalá, M. G., Izquierdo, D., Uzbekova, S., Morató, R., Roura, M., Romaguera, R., Papillier, P., and Paramio, M. T. (2011). Brilliant Cresyl Blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep. Reproduction 142, 517–527.
Brilliant Cresyl Blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep.CrossRef |

Chattoraj, A., Bhattacharyya, S., Basu, D., Bhattacharya, S., Bhattacharya, S., and Maitra, S. K. (2005). Melatonin accelerates maturation inducing hormone (MIH): induced oocyte maturation in carps. Gen. Comp. Endocrinol. 140, 145–155.
Melatonin accelerates maturation inducing hormone (MIH): induced oocyte maturation in carps.CrossRef | 1:CAS:528:DC%2BD2MXivVSnug%3D%3D&md5=158db42718f2c173ec91fb4624f61f00CAS |

Cruz, M. H. C., Leal, C. L. V., da Cruz, J. F., Tan, D. X., and Reiter, R. J. (2014). Role of melatonin on production and preservation of gametes and embryos: a brief review. Anim. Reprod. Sci. 145, 150–160.
Role of melatonin on production and preservation of gametes and embryos: a brief review.CrossRef | 1:CAS:528:DC%2BC2cXivFCksb8%3D&md5=575bfcba00eea671323bf6959bb0291eCAS |

Deleuze, S., and Goudet, G. (2010). Cysteamine supplementation of in vitro maturation media: a review. Reprod. Domest. Anim. 45, e476–e482.
Cysteamine supplementation of in vitro maturation media: a review.CrossRef | 1:CAS:528:DC%2BC3cXhs1WrsLfF&md5=38caa018c0446e25567d3d20520d176bCAS |

Devine, P. J., Perreault, S. D., and Luderer, U. (2012). Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol. Reprod. 86, 27.
Roles of reactive oxygen species and antioxidants in ovarian toxicity.CrossRef |

El-Raey, M., Geshi, M., Somfai, T., Kaneda, M., Hirako, M., Abdel-Ghaffar, A. E., Sosa, G. A., El-Roos, M. E. A. A., and Nagai, T. (2011). Evidence of melatonin synthesis in the cumulus–oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle. Mol. Reprod. Dev. 78, 250–262.
Evidence of melatonin synthesis in the cumulus–oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle.CrossRef | 1:CAS:528:DC%2BC3MXkvFajurc%3D&md5=7f5a218c8600f86bb902abd7923ade5cCAS |

Franco, R., and Cidlowski, J. A. (2009). Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ. 16, 1303–1314.
Apoptosis and glutathione: beyond an antioxidant.CrossRef | 1:CAS:528:DC%2BD1MXhtFajt7vO&md5=f876071e706d942dcf4ecf5d24b70594CAS |

Goud, A. P., Goud, P. T., Diamond, M. P., Gonik, B., and Abu-Soud, H. M. (2008). Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic. Biol. Med. 44, 1295–1304.
Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid.CrossRef | 1:CAS:528:DC%2BD1cXktV2gtr4%3D&md5=77395fd313b8ee0dfcc172855350d19aCAS |

Guérin, P., El Mouatassim, S., and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–189.
Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings.CrossRef |

He, C., Wang, J., Zhang, Z., Yang, M., Li, Y., Tian, X., Ma, T., Tao, J., Zhu, K., Song, Y., Ji, P., and Liu, G. (2016). Mitochondria synthesize melatonin to ameliorate its function and improve mice oocyte’s quality under in vitro conditions. Int. J. Mol. Sci. 17, 939.
Mitochondria synthesize melatonin to ameliorate its function and improve mice oocyte’s quality under in vitro conditions.CrossRef |

Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum proteins. Theriogenology 52, 683–700.
High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum proteins.CrossRef | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=4b5bf1ef366000f0c309b3ada47205f5CAS |

Jiao, G. Z., Cao, X. Y., Cui, W., Lian, H. Y., Miao, Y. L., Wu, X. F., Han, D., and Tan, J. H. (2013). Developmental potential of prepubertal mouse oocytes is compromised due mainly to their impaired synthesis of glutathione. PLoS One 8, e58018.
Developmental potential of prepubertal mouse oocytes is compromised due mainly to their impaired synthesis of glutathione.CrossRef | 1:CAS:528:DC%2BC3sXkt1Wht7g%3D&md5=a7a1f369238b21bdec80068c0f3d0367CAS |

Kang, J. T., Koo, O. J., Kwon, D. K., Park, H. J., Jang, G., Kang, S. K., and Lee, B. C. (2009). Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. J. Pineal Res. 46, 22–28.
Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells.CrossRef | 1:CAS:528:DC%2BD1MXlsV2rtQ%3D%3D&md5=46f93934abb79891ac558ce9cb3532eaCAS |

Koeman, J., Keefer, C. L., Baldassarre, H., and Downey, B. R. (2003). Developmental competence of prepubertal and adult goat oocytes cultured in semi-defined media following laparoscopic recovery. Theriogenology 60, 879–889.
Developmental competence of prepubertal and adult goat oocytes cultured in semi-defined media following laparoscopic recovery.CrossRef |

Korkmaz, A., Rosales-Corral, S., and Reiter, R. J. (2012). Gene regulation by melatonin linked to epigenetic phenomena. Gene 503, 1–11.
Gene regulation by melatonin linked to epigenetic phenomena.CrossRef | 1:CAS:528:DC%2BC38XntF2isb4%3D&md5=fac45677a7eac0e5405597d5f88868b9CAS |

Lane, M., and Gardner, D. K. (1997). Differential regulation of mouse embryo development and viability by amino acids. J. Reprod. Fertil. 109, 153–164.
Differential regulation of mouse embryo development and viability by amino acids.CrossRef | 1:CAS:528:DyaK2sXhs1Gls78%3D&md5=afc0eb58dd351989b1384e8f257f3291CAS |

Leoni, G. G., Succu, S., Satta, V., Paolo, M., Bogliolo, L., Bebbere, D., Spezzigu, A., Madeddu, M., Berlinguer, F., Ledda, S., and Naitana, S. (2009). In vitro production and cryotolerance of prepubertal and adult goat blastocysts obtained from oocytes collected by laparoscopic oocyte-pick-up (LOPU) after FSH treatment. Reprod. Fertil. Dev. 21, 901–908.
In vitro production and cryotolerance of prepubertal and adult goat blastocysts obtained from oocytes collected by laparoscopic oocyte-pick-up (LOPU) after FSH treatment.CrossRef | 1:CAS:528:DC%2BD1MXhtVartbfN&md5=5497dfa7420736df0849840e8b198e9eCAS |

Leoni, G. G., Palmerini, M. G., Satta, V., Succu, S., Pasciu, V., Zinellu, A., Carru, C., Macchiarelli, G., Nottola, S. A., Naitana, S., and Berlinguer, F. (2015). Differences in the kinetic of the first meiotic division and in active mitochondrial distribution between prepubertal and adult oocytes mirror differences in their developmental competence in a sheep model. PLoS One 10, e0124911.
Differences in the kinetic of the first meiotic division and in active mitochondrial distribution between prepubertal and adult oocytes mirror differences in their developmental competence in a sheep model.CrossRef |

Li, Y., Wang, J., Zhang, Z., Yi, J., He, C., Wang, F., Tian, X., Yang, M., Song, Y., He, P., and Liu, G. (2016). Resveratrol compares with melatonin in improving in vitro porcine oocyte maturation under heat stress. J. Anim. Sci. Biotechnol. 7, 33.
Resveratrol compares with melatonin in improving in vitro porcine oocyte maturation under heat stress.CrossRef |

Lord, T., Nixon, B., Jones, K. T., and Aitken, R. J. (2013). Melatonin prevents postovulatory oocyte aging in the mouse and extends the window for optimal fertilization in vitro. Biol. Reprod. 88, 67.
Melatonin prevents postovulatory oocyte aging in the mouse and extends the window for optimal fertilization in vitro.CrossRef |

Morton, K. M. (2008). Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes. Reprod. Domest. Anim. 43, 137–143.
Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes.CrossRef |

Nikmard, F., Hosseini, E., Bakhtiyari, M., Ashrafi, M., Amidi, F., and Aflatoonian, R. (2017). Effects of melatonin on oocyte maturation in PCOS mouse model. Anim. Sci. J. 88, 586–592.
Effects of melatonin on oocyte maturation in PCOS mouse model.CrossRef | 1:CAS:528:DC%2BC2sXlsFKltrc%3D&md5=ec05ffa9b6d52c4b2955e4803880c1a6CAS |

Paramio, M. T., and Izquierdo, D. (2014). Current status of in vitro embryo production in sheep and goats. Reprod. Domest. Anim. 49, 37–48.
Current status of in vitro embryo production in sheep and goats.CrossRef |

Park, S. H., Cho, H. S., and Yu, I. J. (2014). Effect of bovine follicular fluid on reactive oxygen species and glutathione in oocytes, apoptosis and apoptosis-related gene expression of in vitro-produced blastocysts. Reprod. Domest. Anim. 49, 370–377.
Effect of bovine follicular fluid on reactive oxygen species and glutathione in oocytes, apoptosis and apoptosis-related gene expression of in vitro-produced blastocysts.CrossRef | 1:CAS:528:DC%2BC2cXns12mu7k%3D&md5=326548cdb51c0979a00c26890f203be9CAS |

Parrish, J. J., Susko-Parrish, J. L., Leibfried-Rutledge, M. L., Critser, E. S., Eyestone, W. H., and First, N. L. (1986). Bovine in vitro fertilization with frozen–thawed semen. Theriogenology 25, 591–600.
Bovine in vitro fertilization with frozen–thawed semen.CrossRef | 1:STN:280:DC%2BD283pvV2itQ%3D%3D&md5=c238a263d539c324481592d69c9c168bCAS |

Reiter, R. J., Tan, D.-X., Manchester, L. C., Paredes, S. D., Mayo, J. C., and Sainz, R. M. (2009). Melatonin and reproduction revisited. Biol. Reprod. 81, 445–456.
Melatonin and reproduction revisited.CrossRef | 1:CAS:528:DC%2BD1MXhtVChu77F&md5=8d294c547d1815be8fd280e279a5ae0aCAS |

Reiter, R. J., Mayo, J. C., Tan, D.-X., Sainz, R. M., Alatorre-Jimenez, M., and Qin, L. (2016). Melatonin as an antioxidant: underpromises but overdelivers. J. Pineal Res. 61, 253–278.
Melatonin as an antioxidant: underpromises but overdelivers.CrossRef | 1:CAS:528:DC%2BC28Xht12ksbjJ&md5=2602c9ac212de126640101111023f0c9CAS |

Remião, M. H., Lucas, C. G., Domingues, W. B., Silveira, T., Barther, N. N., Komninou, E. R., Basso, A. C., Jornada, D. S., Beck, R. C. R., Pohlmann, A. R., Junior, A. S. V., Seixas, F. K., Campos, V. F., Guterres, S. S., and Collares, T. (2016). Melatonin delivery by nanocapsules during in vitro bovine oocyte maturation decreased the reactive oxygen species of oocytes and embryos. Reprod. Toxicol. 63, 70–81.
Melatonin delivery by nanocapsules during in vitro bovine oocyte maturation decreased the reactive oxygen species of oocytes and embryos.CrossRef |

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., Báo, S. N., Campello, C. C., Rodrigues, A. P. R., and Figueiredo, J. R. (2013). Interaction between melatonin and follicle-stimulating hormone promotes in vitro development of caprine preantral follicles. Domest. Anim. Endocrinol. 44, 1–9.
Interaction between melatonin and follicle-stimulating hormone promotes in vitro development of caprine preantral follicles.CrossRef | 1:CAS:528:DC%2BC38Xht1ekur%2FN&md5=93336168c84ef8a54204aa723f628778CAS |

Rodrigues-Cunha, M. C., Mesquita, L. G., Bressan, F., del Collado, M., Balieiro, J. C. C., Schwarz, K. R. L., de Castro, F. C., Watanabe, O. Y., Watanabe, Y. F., de Alencar Coelho, L., and Leal, C. L. V. (2016). Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology 86, 1685–1694.
Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development.CrossRef | 1:CAS:528:DC%2BC28XpvFejs7c%3D&md5=cd43c69a2dcbcd077064c0dac3349c42CAS |

Rodríguez-González, E., López-Bejar, M., Mertens, M. J., and Paramio, M. T. (2003). Effects on in vitro embryo development and intracellular glutathione content of the presence of thiol compounds during maturation of prepubertal goat oocytes. Mol. Reprod. Dev. 65, 446–453.
Effects on in vitro embryo development and intracellular glutathione content of the presence of thiol compounds during maturation of prepubertal goat oocytes.CrossRef |

Romaguera, R., Casanovas, A., Morató, R., Izquierdo, D., Catalá, M., Jimenez-Macedo, A. R., Mogas, T., and Paramio, M. T. (2010). Effect of follicle diameter on oocyte apoptosis, embryo development and chromosomal ploidy in prepubertal goats. Theriogenology 74, 364–373.
Effect of follicle diameter on oocyte apoptosis, embryo development and chromosomal ploidy in prepubertal goats.CrossRef | 1:STN:280:DC%2BC3cnntVGltA%3D%3D&md5=c3591e02426a526e2664683385c4513bCAS |

Sakaguchi, K., Itoh, M. T., Takahashi, N., Tarumi, W., and Ishizuka, B. (2013). The rat oocyte synthesises melatonin. Reprod. Fertil. Dev. 25, 674–682.
The rat oocyte synthesises melatonin.CrossRef | 1:CAS:528:DC%2BC3sXmt1Cgs7s%3D&md5=892411466df90eeb186f33e85e049889CAS |

Salimi, M., Salehi, M., Masteri Farahani, R., Dehghani, M., Abadi, M., Novin, M. G., Nourozian, M., and Hosseini, A. (2014). The effect of melatonin on maturation, glutathione level and expression of HMGB1 gene in brilliant cresyl blue (BCB) stained immature oocyte. Cell J. 15, 294–301.
| 1:CAS:528:DC%2BC2cXlsF2jtr8%3D&md5=fe6143934f5428af70865f1e6294bb21CAS |

Sampaio, R. V, Conceição, S. D. B., Miranda, M. S., Sampaio, Lde. F., and Ohashi, O. M. (2012). 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. 10, 103.
MT3 melatonin binding site, MT1 and MT2 melatonin receptors are present in oocyte, but only MT1 is present in bovine blastocyst produced in vitro.CrossRef | 1:CAS:528:DC%2BC3sXltFSms70%3D&md5=8ede79ca8a252d8ac2e1be539f4fd587CAS |

Shi, J. M., Tian, X. Z., Zhou, G. B., Wang, L., Gao, C., Zhu, S. E., Zeng, S. M., Tian, J. H., and Liu, G. S. (2009). Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes. J. Pineal Res. 47, 318–323.
Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes.CrossRef | 1:CAS:528:DC%2BD1MXhtlOqtLnP&md5=0b2a97885b94eb203f9a63b1571f9afaCAS |

Song, C., Peng, W., Yin, S., Zhao, J., Fu, B., Zhang, J., Mao, T., Wu, H., and Zhang, Y. (2016). Melatonin improves age-induced fertility decline and attenuates ovarian mitochondrial oxidative stress in mice. Sci. Rep. 6, 35165.
Melatonin improves age-induced fertility decline and attenuates ovarian mitochondrial oxidative stress in mice.CrossRef | 1:CAS:528:DC%2BC28Xhs1yisrnF&md5=763555a1b8df640141540bad464e97e3CAS |

Sugden, D. (1989). Melatonin biosynthesis in the mammalian pineal gland. Experientia 45, 922–932.
Melatonin biosynthesis in the mammalian pineal gland.CrossRef | 1:CAS:528:DyaK3cXhs1egsA%3D%3D&md5=348c029be992e04cadcbe0fe88b23471CAS |

Takada, L., Junior, A. M., Mingoti, G. Z., Balieiro, J. C. C., Cipolla-Neto, J., and Coelho, L. A. (2012). Effect of melatonin on DNA damage of bovine cumulus cells during in vitro maturation (IVM) and on in vitro embryo development. Res. Vet. Sci. 92, 124–127.
Effect of melatonin on DNA damage of bovine cumulus cells during in vitro maturation (IVM) and on in vitro embryo development.CrossRef | 1:CAS:528:DC%2BC3MXhs1emtb%2FL&md5=1f61c3f2bdfa23ccf83fae1bfc96331cCAS |

Takahashi, T., Takahashi, E., Igarashi, H., Tezuka, N., and Kurachi, H. (2003). Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol. Reprod. Dev. 66, 143–152.
Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization.CrossRef | 1:CAS:528:DC%2BD3sXnt1Wntr4%3D&md5=ae21be16ea98703fff58418db1b6b209CAS |

Tamura, H., Nakamura, Y., Korkmaz, A., Manchester, L. C., Tan, D. X., Sugino, N., and Reiter, R. J. (2009). Melatonin and the ovary: physiological and pathophysiological implications. Fertil. Steril. 92, 328–343.
Melatonin and the ovary: physiological and pathophysiological implications.CrossRef | 1:CAS:528:DC%2BD1MXhtFWisLrP&md5=62ac97cb9eaadd25a2be6f0a30713db9CAS |

Tamura, H., Takasaki, A., Taketani, T., Tanabe, M., Kizuka, F., Lee, L., Tamura, I., Maekawa, R., Aasada, H., Yamagata, Y., and Sugino, N. (2012). The role of melatonin as an antioxidant in the follicle. J. Ovarian Res. 5, 5.
The role of melatonin as an antioxidant in the follicle.CrossRef | 1:CAS:528:DC%2BC38XkvFertLk%3D&md5=b714e8e4b4137e03b811616533f99af8CAS |

Tamura, H., Takasaki, A., Taketani, T., Tanabe, M., Kizuka, F., Lee, L., Tamura, I., Maekawa, R., Asada, H., Yamagata, Y., and Sugino, N. (2013). Melatonin as a free radical scavenger in the ovarian follicle. Endocr. J. 60, 1–13.
Melatonin as a free radical scavenger in the ovarian follicle.CrossRef | 1:CAS:528:DC%2BC3sXntlSjs7c%3D&md5=bf54ec648679f83ca2aa4c531f3a1584CAS |

Thouas, G. A., Korfiatis, N. A., French, A. J., Jones, G. M., and Trounson, A. O. (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. Biomed. Online 3, 25–29.
Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts.CrossRef |

Tian, X., Wang, F., He, C., Zhang, L., Tan, D., Reiter, R. J., Xu, J., Ji, P., and Liu, G. (2014). Beneficial effects of melatonin on bovine oocytes maturation: a mechanistic approach. J. Pineal Res. 57, 239–247.
Beneficial effects of melatonin on bovine oocytes maturation: a mechanistic approach.CrossRef | 1:CAS:528:DC%2BC2cXhsF2ntbjE&md5=d492feccb6262f6c7dbf608672b87c8cCAS |

Tomás-Zapico, C., and Coto-Montes, A. (2005). A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J. Pineal Res. 39, 99–104.
A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes.CrossRef |

Tripathi, A., Premkumar, K. V., Pandey, A. N., Khatun, S., Mishra, S. K., Shrivastav, T. G., and Chaube, S. K. (2011). Melatonin protects against clomiphene citrate-induced generation of hydrogen peroxide and morphological apoptotic changes in rat eggs. Eur. J. Pharmacol. 667, 419–424.
Melatonin protects against clomiphene citrate-induced generation of hydrogen peroxide and morphological apoptotic changes in rat eggs.CrossRef | 1:CAS:528:DC%2BC3MXhtVGlt7nK&md5=26f368fe5a22552b91920a7c0ad6c53eCAS |

Yuan, Y., Wheeler, M. B., and Krisher, R. L. (2012). Disrupted redox homeostasis and aberrant redox gene expression in porcine oocytes contribute to decreased developmental competence. Biol. Reprod. 87, 78.
Disrupted redox homeostasis and aberrant redox gene expression in porcine oocytes contribute to decreased developmental competence.CrossRef |

Zarazaga, L. A., Celi, I., Guzmán, J. L., and Malpaux, B. (2010). Melatonin concentrations in the two jugular veins, and relationship with the seasonal reproductive activity in goats. Theriogenology 74, 221–228.
Melatonin concentrations in the two jugular veins, and relationship with the seasonal reproductive activity in goats.CrossRef | 1:CAS:528:DC%2BC3cXotVaiu78%3D&md5=9c3be90ced8c75878d1f8b359fbca3ddCAS |



Export Citation

View Altmetrics