Role of melatonin on embryo viability in sheep
José-Alfonso Abecia A C , Fernando Forcada A , María-Isabel Vázquez B , Teresa Muiño-Blanco A , José A. Cebrián-Pérez A , Rosaura Pérez-Pe A and Adriana Casao A
+ Author Affiliations
- Author Affiliations
A Instituto Universitario de Investigación en Ciencias Ambientales de Aragón (IUCA), Universidad de Zaragoza, Facultad de Veterinaria, Miguel Servet, 177, 50013 Zaragoza, Spain.
B Departamento de Reproducción Animal, Facultad de Agronomía y Veterinaria, Universidad Nacional de Río Cuarto, Ruta Nacional 36, Km 601, 5800 Río Cuarto, Córdoba, Argentina.
C Corresponding author. Email: [email protected]
Reproduction, Fertility and Development 31(1) 82-92 https://doi.org/10.1071/RD18308
Published online: 3 December 2018
Abstract
Melatonin is a natural hormone synthesised in the pineal gland, the activity of which is regulated by day–night perception and dictates seasonal rhythms in reproduction in ovine species. Exogenous melatonin, administered via subcutaneous implants, is used to prolong the breeding season of ewes and can increase the proportion of pregnant ewes (fertility rate) and litter size. The increased proportion of ewes that become pregnant and the number of lambs born per lambing among melatonin-treated sheep may be caused by increased embryo survival, through enhanced luteal function, reduced antiluteolytic mechanisms, or improved embryo quality. This review focuses on the effects of melatonin on embryo viability and summarises the processes by which this hormone affects the ovary, follicle, oocyte, corpus luteum and embryo. Moreover, the effects of melatonin on the mechanisms of in vivo maternal recognition of pregnancy in sheep and the protective action that it appears to have on the in vitro procedures that are used to obtain healthy embryos are reviewed.
Additional keywords: follicle, ovary, oxidative stress, uterus.
References
Abecia, J. A., Forcada, F., and Lozano, J. M. (1999). A preliminary report on the effect of dietary energy on prostaglandin F-2 alpha production in vitro, interferon-tau synthesis by the conceptus, endometrial progesterone concentration on Days 9 and 15 of pregnancy and associated rates of embryo wastage in ewes. Theriogenology 52, 1203–1213.| A preliminary report on the effect of dietary energy on prostaglandin F-2 alpha production in vitro, interferon-tau synthesis by the conceptus, endometrial progesterone concentration on Days 9 and 15 of pregnancy and associated rates of embryo wastage in ewes.Crossref | GoogleScholarGoogle Scholar |
Abecia, J. A., Forcada, F., and Zuniga, O. (2002). The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro. Vet. Res. Commun. 26, 151–158.
| The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro.Crossref | GoogleScholarGoogle Scholar |
Abecia, J. A., Palacín, I., Forcada, F., and Valares, J. A. (2006). The effect of melatonin treatment on the ovarian response of ewes to the ram effect. Domest. Anim. Endocrinol. 31, 52–62.
| The effect of melatonin treatment on the ovarian response of ewes to the ram effect.Crossref | GoogleScholarGoogle Scholar |
Abecia, J. A., Forcada, F., Casao, A., and Palacín, I. (2008). Effect of exogenous melatonin on the ovary, the embryo and the establishment of pregnancy in sheep. Animal 2, 399–404.
| Effect of exogenous melatonin on the ovary, the embryo and the establishment of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |
Abecia, J. A., Forcada, F., and González-Bulnes, A. (2011). Pharmaceutical control of reproduction in sheep and goats. Vet. Clin. North Am. Food Anim. Pract. 27, 67–79.
| Pharmaceutical control of reproduction in sheep and goats.Crossref | GoogleScholarGoogle Scholar |
Berlinguer, F., Leoni, G. G., Succu, S., Spezzigu, A., Madeddu, M., Satta, V., Bebbere, D., Contreras-Solis, I., Gonzalez-Bulnes, A., and Naitana, S. (2009). Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. J. Pineal Res. 46, 383–391.
| Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model.Crossref | GoogleScholarGoogle Scholar |
Bittman, E. L., and Karsch, F. J. (1984). Nightly duration of pineal melatonin secretion determines the reproductive response to inhibitory daylength in the ewe. Biol. Reprod. 30, 585–593.
| Nightly duration of pineal melatonin secretion determines the reproductive response to inhibitory daylength in the ewe.Crossref | GoogleScholarGoogle Scholar |
Bittman, E. L., Dempsey, R. J., and Karsch, F. J. (1983). Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113, 2276–2283.
| Pineal melatonin secretion drives the reproductive response to daylength in the ewe.Crossref | GoogleScholarGoogle Scholar |
Bojanowska, E., and Forsling, M. L. (1997). The effects of melatonin on vasopressin secretion in vivo: interactions with acetylcholine and prostaglandins. Brain Res. Bull. 42, 457–461.
| The effects of melatonin on vasopressin secretion in vivo: interactions with acetylcholine and prostaglandins.Crossref | GoogleScholarGoogle Scholar |
Brzezinski, A., Seibel, M. M., Lynch, H. J., Deng, M. H., and Wurtman, R. J. (1987). Melatonin in human preovulatory follicular fluid. J. Clin. Endocrinol. Metab. 64, 865–867.
| Melatonin in human preovulatory follicular fluid.Crossref | GoogleScholarGoogle Scholar |
Bubenik, G. A. (2002). Gastrointestinal melatonin: localization, function, and clinical relevance. Dig. Dis. Sci. 47, 2336–2348.
| Gastrointestinal melatonin: localization, function, and clinical relevance.Crossref | GoogleScholarGoogle Scholar |
Buffoni, A., Vozzi, P. A., Gonzalez, D. M., Rios, G., Viegas-Bordeira, H., and Abecia, J. A. (2014). The effect of melatonin and season on in vivo embryo production of Dohne merino ewes. Small Rumin. Res. 120, 121–124.
| The effect of melatonin and season on in vivo embryo production of Dohne merino ewes.Crossref | GoogleScholarGoogle Scholar |
Carcangiu, V., Mura, M. C., Vacca, G. M., Pazzola, M., Dettori, M. L., Luridiana, S., and Bini, P. P. (2009). Polymorphism of the melatonin receptor MT1 gene and its relationship with seasonal reproductive activity in the Sarda sheep breed. Anim. Reprod. Sci. 116, 65–72.
| Polymorphism of the melatonin receptor MT1 gene and its relationship with seasonal reproductive activity in the Sarda sheep breed.Crossref | GoogleScholarGoogle Scholar |
Casao, A., Ait, A., Meziane, M., Cebrián-Pérez, J. A., Muiño-Blanco, T., Abecia, J. A., and Forcada, F. (2009). The effects of low concentrations of melatonin on in vitro maturation and fertilization of oocytes and on early embryo development in sheep. In ‘Proceedings of the XIII Jornadas sobre Producción Animal’, 12–13 May 2009, Zaragoza, Spain. (Ed. M. Joy.) pp. 696–698. (Asociación Interprofesional para el Desarrollo Agrario: Zaragoza.)
Casao, A., Abecia, J. A., Cebrián-Pérez, J. A., Muiño-Blanco, T., Vázquez, M. I., and Forcada, F. (2010a). The effects of melatonin on in vitro oocyte competence and embryo development in sheep. Span. J. Agric. Res. 8, 35–41.
| The effects of melatonin on in vitro oocyte competence and embryo development in sheep.Crossref | GoogleScholarGoogle Scholar |
Casao, A., Perez-Pe, R., Forcada, F., Abecia, J. A., Cebrian-Perez, J. A., and Muiño-Blanco, T. (2010b). Melatonin receptors MT1A/B presence on in vitro obtained sheep blastocysts. In ‘Proceedings of the XXXV Jornadas SEOC’, 22–24 September 2010, Valladolid, Spain. (Ed. L. Rodríguez.) pp. 163–167. (Sociedad Española de Ovinotecnia y Caprinotecnia: Zaragoza.)
Casao, A., Mendoza, N., Pérez-Pé, R., Grasa, P., Abecia, J. A., Forcada, F., Cebrián-Pérez, J. A., and Muino-Blanco, T. (2010c). Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate. J. Pineal Res. 48, 39–46.
| Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate.Crossref | GoogleScholarGoogle Scholar |
Casao, A., Gallego, M., Abecia, J. A., Forcada, F., Pérez-Pé, R., Muiño-Blanco, T., and Cebrián-Pérez, J. A. (2012). Identification and immunolocalisation of melatonin MT1 and MT2 receptors in Rasa Aragonesa ram spermatozoa. Reprod. Fertil. Dev. 24, 953–961.
| Identification and immunolocalisation of melatonin MT1 and MT2 receptors in Rasa Aragonesa ram spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Casao, A., Pérez-Pe, R., Forcada, F., Abecia, J. A., Cebrian-Perez, J. A., and Muiño-Blanco, T. (2013). Melatonin secretion in sheep cumulus cells and its possible effect on DNA damage during in vitro maturation. In ‘Proceedings of the XV Jornadas sobre Producción Animal’, 17–18 May 2013, Zaragoza, Spain. (Ed. A. Sanz.) pp. 368–370. (Asociación Interprofesional para el Desarrollo Agrario: Zaragoza.)
Casao, A., Perez-Pe, R., Cebrian-Perez, J. A., Muino-Blanco, T., Forcada, F., and Abecia, J. A. (2018). Presence of melatonin receptors in ovine blastocysts. Reprod. Fert. Dev. , .
Chemineau, P., Malpaux, B., Pelletier, J., Leboeuf, B., Delgadillo, J. A., Deletang, F., Pobel, T., and Brice, G. (1996). Emploi des implants demelatonine et des traitements photoperiodiques pour maııtriser la reproduction saissoniere chez les ovins et les caprins (use of melatonin implants and photoperiodic treatments to control seasonal reproduction on sheep and goats). INRA Prod. Anim. 9, 45–60.
Chuffa, L. G. A., Seiva, F. R. F., Fávaro, W. J., Teixeira, G. R., Amorim, J. P. A., Mendes, L. O., Fioruci, B. A., Pinheiro, P. F. F., Fernandes, A. A. H., Franci, J. A. A., Delella, F. K., Martinez, M., and Martinez, F. E. (2011). Melatonin reduces LH, 17beta-estradiol and induces differential regulation of sex steroid receptors in reproductive tissues during rat ovulation. Reprod. Biol. Endocrinol. 9, 108.
| Melatonin reduces LH, 17beta-estradiol and induces differential regulation of sex steroid receptors in reproductive tissues during rat ovulation.Crossref | GoogleScholarGoogle Scholar |
Coge, F., Guenin, S. P., Fery, I., Migaud, M., Devavry, S., Slugocki, C., Legros, C., Ouvry, C., Cohen, W., Renault, N., Nosjean, O., Malpaux, B., Delagrange, P., and Boutin, J. A. (2009). The end of a myth: cloning and characterization of the ovine melatonin MT2 receptor. Br. J. Pharmacol. 158, 1248–1262.
| The end of a myth: cloning and characterization of the ovine melatonin MT2 receptor.Crossref | GoogleScholarGoogle Scholar |
Cruz, M. H., Leal, C. L., da Cruz, J. F., Tana, D., 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 | GoogleScholarGoogle Scholar |
Diaz, E., Pazo, D., Esquifino, A. I., and Diaz, B. (2000). Effects of ageing and exogenous melatonin on pituitary responsiveness to GnRH in rats. J. Reprod. Fertil. 119, 151–156.
Dubocovich, M. L., and Markowska, M. (2005). Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 27, 101–110.
| Functional MT1 and MT2 melatonin receptors in mammals.Crossref | GoogleScholarGoogle Scholar |
Durotoye, L. A., Webley, G. E., and Rodway, R. G. (1997). Stimulation of the production of progesterone by the corpus luteum of the ewe by the perfusion of melatonin in vivo and by treatment of granulosa cells with melatonin in vitro. Res. Vet. Sci. 62, 87–91.
| Stimulation of the production of progesterone by the corpus luteum of the ewe by the perfusion of melatonin in vivo and by treatment of granulosa cells with melatonin in vitro.Crossref | GoogleScholarGoogle Scholar |
El-Raey, M., Geshi, M., Somfai, T., Kaneda, M., Hirako, M., Abdel-Ghaffar, A. E., Sosa, G. A., El-Roos, M. E., 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 | GoogleScholarGoogle Scholar |
English, J., Poulton, A. L., Arendt, J., and Symons, A. M. (1986). A comparison of the efficiency of melatonin treatments in advancing oestrus in ewes. J. Reprod. Fertil. 77, 321–327.
| A comparison of the efficiency of melatonin treatments in advancing oestrus in ewes.Crossref | GoogleScholarGoogle Scholar |
Eryilmaz, O. G., Devran, A., Sarikaya, E., Aksakal, F. N., Mollamahmutoğlu, L., and Cicek, N. (2011). Melatonin improves the oocyte and the embryo in IVF patients with sleep disturbances, but does not improve the sleeping problems. J. Assist. Reprod. Genet. 28, 815–820.
| Melatonin improves the oocyte and the embryo in IVF patients with sleep disturbances, but does not improve the sleeping problems.Crossref | GoogleScholarGoogle Scholar |
Espino, J., Ortiz, A., Bejarano, I., Lozano, G. M., Monllor, F., García, J. F., Rodríguez, A. B., and Pariente, J. A. (2011). Melatonin protects human spermatozoa from apoptosis via melatonin receptor- and extracellular signal-regulated kinase-mediated pathways. Fertil. Steril. 95, 2290–2296.
| Melatonin protects human spermatozoa from apoptosis via melatonin receptor- and extracellular signal-regulated kinase-mediated pathways.Crossref | GoogleScholarGoogle Scholar |
Forcada, F., and Abecia, J. A. (2006). The effect of nutrition on the seasonality of reproduction in ewes. Reprod. Nutr. Dev. 46, 355–365.
| The effect of nutrition on the seasonality of reproduction in ewes.Crossref | GoogleScholarGoogle Scholar |
Forcada, F., Zarazaga, L., and Abecia, J. A. (1995). Effect of exogenous melatonin and plane of nutrition after weaning on estrous activin, endocrine status and ovulation rate in Salz ewes lambing in the seasonal anestrus. Theriogenology 43, 1179–1193.
| Effect of exogenous melatonin and plane of nutrition after weaning on estrous activin, endocrine status and ovulation rate in Salz ewes lambing in the seasonal anestrus.Crossref | GoogleScholarGoogle Scholar |
Forcada, F., Abecia, J. A., Cebrián-Perez, J. A., Muiño-Blanco, T., Valares, J. A., Palacín, I., and Casao, A. (2006). The effect of melatonin implants during the seasonal anestrus on embryo production after superovulation in aged high-prolificacy Rasa Aragonesa ewes. Theriogenology 65, 356–365.
| The effect of melatonin implants during the seasonal anestrus on embryo production after superovulation in aged high-prolificacy Rasa Aragonesa ewes.Crossref | GoogleScholarGoogle Scholar |
Forcada, F., Abecia, J. A., Casao, A., Cebrián-Pérez, J. A., Muiño-Blanco, M. T., and Palacín, I. (2007). Effects of ageing and exogenous melatonin on pituitary responsiveness to GnRH in ewes during anestrus and the reproductive season. Theriogenology 67, 855–862.
| Effects of ageing and exogenous melatonin on pituitary responsiveness to GnRH in ewes during anestrus and the reproductive season.Crossref | GoogleScholarGoogle Scholar |
Fu, Y., He, C.-J., Ji, P.-Y., Zhuo, Z.-Y., Tian, X.-Z., Wang, F., Tan, D.-X., and Liu, G.-S. (2014). Effects of melatonin on the proliferation and apoptosis of sheep granulosa cells under thermal stress. Int. J. Mol. Sci. 15, 21090–21104.
| Effects of melatonin on the proliferation and apoptosis of sheep granulosa cells under thermal stress.Crossref | GoogleScholarGoogle Scholar |
Gimeno, M. F., Fuentes, A. M., Landa, A., Sterinspeziale, N., Cardinali, D. P., and Gimeno, A. L. (1980). Melatonin – inhibitor of prostaglandin release. Acta Physiol.Latinoamer. 30, 38–39.
Goodarzi, A., Shahneh, A. Z., Kohram, H., Sadeghi, M., Moazenizadeh, M. H., Fouladi-Nashta, A., and Davachi, N. D. (2018). Effect of melatonin supplementation in the long-term preservation of the sheep ovaries at different temperatures and subsequent in vitro embryo production. Theriogenology 106, 265–270.
| Effect of melatonin supplementation in the long-term preservation of the sheep ovaries at different temperatures and subsequent in vitro embryo production.Crossref | GoogleScholarGoogle Scholar |
Hao, Y., Zhang, Z., Han, D., Cao, Y., Zhou, P., Wei, Z., Lv, M., and Chen, D. (2017). Gene expression profiling of human blastocysts from in vivo and ‘rescue IVM’ with or without melatonin treatment. Mol. Med. Rep. 16, 1278–1288.
| Gene expression profiling of human blastocysts from in vivo and ‘rescue IVM’ with or without melatonin treatment.Crossref | GoogleScholarGoogle Scholar |
Haresign, W., Peters, A. R., and Staples, L. D. (1990). The effect of melatonin implants on breeding activity and litter size in commercial sheep flocks in the UK. Anim. Prod. 50, 111–121.
| The effect of melatonin implants on breeding activity and litter size in commercial sheep flocks in the UK.Crossref | GoogleScholarGoogle Scholar |
He, C., Ma, T., Shi, J. M., Zhang, Z. Z., Wang, J., Zhu, K. F., Li, Y., Yang, M. H., Song, Y. K., and Liu, G. S. (2016). Melatonin and its receptor MT1 are involved in the downstream reaction to luteinizing hormone and participate in the regulation of luteinization in different species. J. Pineal Res. 61, 279–290.
| Melatonin and its receptor MT1 are involved in the downstream reaction to luteinizing hormone and participate in the regulation of luteinization in different species.Crossref | GoogleScholarGoogle Scholar |
Hu, W. (2009). The role of p53 gene family in reproduction. Cold Spring Harb. Perspect. Biol. 1, .
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 | GoogleScholarGoogle Scholar |
Kim, M.-R., and Tilly, J. L. (2004). Current concepts in Bcl-2 family member regulation of female germ cell development and survival. Biochim. Biophys. Acta 1644, 205–210.
| Current concepts in Bcl-2 family member regulation of female germ cell development and survival.Crossref | GoogleScholarGoogle Scholar |
Kurutas, E. B. (2016). The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr. J. 15, 71–93.
| The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state.Crossref | GoogleScholarGoogle Scholar |
Lemley, C. O., and Vonnahme, K. A. (2017). Physiology and endocrinology symposium: alterations in uteroplacental hemodynamics during melatonin supplementation in sheep and cattle. J. Anim. Sci. 95, 2211–2221.
Lerner, A. B., Case, J. D., Takahashi, Y., Lee, T. H., and Mori, W. (1958). Isolation of melatonin, the pineal gland factor that lightens melanocytes. J. Am. Chem. Soc. 80, 2587.
| Isolation of melatonin, the pineal gland factor that lightens melanocytes.Crossref | GoogleScholarGoogle Scholar |
Li, S., Givalois, L., and Pelletir, G. (1997). Effects of ageing and melatonin administration on gonadotropin-releasing hormones (GnRH) gene expression in the male and female rat. Peptides 18, 1023–1028.
| Effects of ageing and melatonin administration on gonadotropin-releasing hormones (GnRH) gene expression in the male and female rat.Crossref | GoogleScholarGoogle Scholar |
Lima, G. N., Maganhin, C. C., Simões, R. S., Baracat, M. C. P., da Silva Sasso, G. R., Fuchs, L. F. P., de Jesus Simões, M., Baracat, E. C., and Júnior, J. M. S. (2015). Steroidogenesis-related gene expression in the rat ovary exposed to melatonin supplementation. Clinics 70, 144–151.
| Steroidogenesis-related gene expression in the rat ovary exposed to melatonin supplementation.Crossref | GoogleScholarGoogle Scholar |
Lincoln, G. A. (1990). Correlation with changes in horns and pelage, but not reproduction, of seasonal cycles in the secretion of prolactin in rams of wild, feral and domesticated breeds of sheep. J. Reprod. Fertil. 90, 285–296.
| Correlation with changes in horns and pelage, but not reproduction, of seasonal cycles in the secretion of prolactin in rams of wild, feral and domesticated breeds of sheep.Crossref | GoogleScholarGoogle Scholar |
Loren, P., Sánchez, R., Arias, M. E., Felmer, R., Risopatrón, J., and Cheuquemán, C. (2017). Melatonin scavenger properties against oxidative and nitrosative stress: impact on gamete handling and in vitro embryo poduction in humans and other mammals. Int. J. Mol. Sci. 18, 1119.
| Melatonin scavenger properties against oxidative and nitrosative stress: impact on gamete handling and in vitro embryo poduction in humans and other mammals.Crossref | GoogleScholarGoogle Scholar |
Maganhin, C. C., Simoes, R. S., Fuchs, L. F. P., Sasso, G. R. S., Simoes, M. J., Baracat, E. C., and Soares, J. M. (2014). Melatonin influences on steroidogenic gene expression in the ovary of pinealectomized rats. Fertil. Steril. 102, 291–298.
| Melatonin influences on steroidogenic gene expression in the ovary of pinealectomized rats.Crossref | GoogleScholarGoogle Scholar |
Manca, M. E., Manunta, M. L., Spezzigu, A., Torres-Rovira, L., Gonzalez-Bulnes, A., Pasciu, V., Piu, P., Leoni, G. G., Succu, S., Chesneau, D., Naitana, S., and Berlinguer, F. (2014). Melatonin deprival modifies follicular and corpus luteal growth dynamics in a sheep model. Reproduction 147, 885–895.
| Melatonin deprival modifies follicular and corpus luteal growth dynamics in a sheep model.Crossref | GoogleScholarGoogle Scholar |
Martínez-Royo, A., Lahoz, B., Alabart, J. L., Folch, J., and Calvo, J. H. (2012). Characterisation of the melatonin receptor 1A (MTNR1A) gene in the Rasa Aragonesa sheep breed: association with reproductive seasonality. Anim. Reprod. Sci. 133, 169–175.
| Characterisation of the melatonin receptor 1A (MTNR1A) gene in the Rasa Aragonesa sheep breed: association with reproductive seasonality.Crossref | GoogleScholarGoogle Scholar |
Martino, N. A., Ariu, F., Bebbere, D., Uranio, M. F., Chirico, A., Marzano, G., Sardanelli, A. M., Cardinali, A., Minervini, F., Bogliolo, L., and Dell’Aquila, M. E. (2016). Supplementation with nanomolar concentrations of verbascoside during in vitro maturation improves embryo development by protecting the oocyte against oxidative stress: a large animal model study. Reprod. Toxicol. 65, 204–211.
| Supplementation with nanomolar concentrations of verbascoside during in vitro maturation improves embryo development by protecting the oocyte against oxidative stress: a large animal model study.Crossref | GoogleScholarGoogle Scholar |
Mateescu, R. G., Lunsford, A. K., and Thonney, M. L. (2009). Association between melatonin receptor 1A gene polymorphism and reproductive performance in Dorset ewes. J. Anim. Sci. 87, 2485–2488.
| Association between melatonin receptor 1A gene polymorphism and reproductive performance in Dorset ewes.Crossref | GoogleScholarGoogle Scholar |
McEvoy, T. G., Robinson, J. J., Aitken, R. P., and Robertson, I. S. (1998). Melatonin treatment of embryo donor and recipient ewes during anestrus affects their endocrine status, but not ovulation rate, embryo survival or pregnancy. Theriogenology 49, 943–955.
| Melatonin treatment of embryo donor and recipient ewes during anestrus affects their endocrine status, but not ovulation rate, embryo survival or pregnancy.Crossref | GoogleScholarGoogle Scholar |
Mitchell, L. M., Dingwall, W. S., Mylne, M. J. A., Hunton, J., Matthews, K., Gebbie, F. E., McCallum, G. J., and McEvoy, T. G. (2002). Season affects characteristics of the pre-ovulatory LH surge and embryo viability in superovulated ewes. Anim. Reprod. Sci. 74, 163–174.
| Season affects characteristics of the pre-ovulatory LH surge and embryo viability in superovulated ewes.Crossref | GoogleScholarGoogle Scholar |
Ortavant, R., Pelletier, J., Ravault, J. P., Thimonier, J., and Volland-Nail, P. (1985). Photoperiod: main proximal and distal factor of the circannual cycle of reproduction in farm mammals. Oxf. Rev. Reprod. Biol. 7, 306–345.
Palacín, I., Forcada, F., and Abecia, J. A. (2011). Meta-analysis of the efficacy of melatonin implants for improving reproductive performance in sheep. Span. J. Agric. Res. 9, 730–743.
| Meta-analysis of the efficacy of melatonin implants for improving reproductive performance in sheep.Crossref | GoogleScholarGoogle Scholar |
Papis, K., Poleszczuk, O., Wenta-Muchalska, E., and Modlinski, J. A. (2007). Melatonin effect on bovine embryo development in vitro in relation to oxygen concentration. J. Pineal Res. 43, 321–326.
| Melatonin effect on bovine embryo development in vitro in relation to oxygen concentration.Crossref | GoogleScholarGoogle Scholar |
Peris-Frau, P., Sánchez-Ajofrín, I., López-Flores, R., Iniesta-Cuerda, M., Martín-Maestro, A., Ruíz, E., Fernández-Santos, M. R., Garde, J. J., and Soler, A. J. (2017). Influence of exogenous melatonin during transport of sheep ovaries on in vitro embryo output. Reprod. Domest. Anim. 52, 80.
Reiter, R. J. (1992). The ageing pineal gland and its physiological consequences. BioEssays 14, 169–175.
| The ageing pineal gland and its physiological consequences.Crossref | GoogleScholarGoogle Scholar |
Reppert, S. M., Weaver, D. R., and Ebisawa, T. (1994). Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and circadian responses. Neuron 13, 1177–1185.
| Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and circadian responses.Crossref | GoogleScholarGoogle Scholar |
Rodriguez-Osorio, N., Kim, I. J., Wang, H., Kaya, A., and Memili, E. (2007). Melatonin increases cleavage rate of porcine preimplantation embryos in vitro. J. Pineal Res. 43, 283–288.
| Melatonin increases cleavage rate of porcine preimplantation embryos in vitro.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Smith, J. F., Cruickshank, G. F., McGowan, L. T., Parr, J., and Mortimer, B. J. (1988). Seasonal changes in oestrus, ovulation and conception of Coopworth ewes treated with CIDRs and PMSG. Proc. N.Z. Soc. Anim. Prod. 48, 99–102.
Soto-Heras, S., Roura, M., Catalá, M. G., Menéndez-Blanco, I., Izquierdo, D., Fouladi-Nashta, A. A., and Paramio, M. T. (2018). Beneficial effects of melatonin on in vitro embryo production from juvenile goat oocytes. Reprod. Fertil. Dev. 30, 253–261.
| Beneficial effects of melatonin on in vitro embryo production from juvenile goat oocytes.Crossref | GoogleScholarGoogle Scholar |
Succu, S., Pasciu, V., Manca, M. E., Chelucci, S., Torres-Rovira, L., Leoni, G. G., Zinellu, A., Carru, C., Naitana, S., and Berlinguer, F. (2014). Dose-dependent effect of melatonin on postwarming development of vitrified ovine embryos. Theriogenology 81, 1058–1066.
| Dose-dependent effect of melatonin on postwarming development of vitrified ovine embryos.Crossref | GoogleScholarGoogle Scholar |
Takada, L., Martins, A., 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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
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, 5–14.
| The role of melatonin as an antioxidant in the follicle.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Tian, X., Wang, F., Zhang, L., He, C., Ji, P., Wang, J., Zhang, Z., Lv, D., Abulizi, W., Wang, X., Lian, Z., and Liu, G. (2017). Beneficial effects of melatonin on the in vitro maturation of sheep oocytes and its relation to melatonin receptors. Int. J. Mol. Sci. 18, 834–849.
| Beneficial effects of melatonin on the in vitro maturation of sheep oocytes and its relation to melatonin receptors.Crossref | GoogleScholarGoogle Scholar |
Tsiligianni, T., Valasi, I., Cseh, S., Vainas, E., Faigl, V., Samartzi, F., Papanikolaou, T., Dovolou, E., and Amiridis, G. S. (2009). Effects of melatonin treatment on follicular development and oocyte quality in Chios ewes – short communication. Acta Vet. Hung. 57, 331–335.
| Effects of melatonin treatment on follicular development and oocyte quality in Chios ewes – short communication.Crossref | GoogleScholarGoogle Scholar |
Vázquez, M. I., Forcada, F., Casao, A., Sosa, C., Palacín, I., and Abecia, J. A. (2009). Effects of melatonin and undernutrition on the viability of ovine embryos during anestrus and the breeding season. Anim. Reprod. Sci. 112, 83–94.
| Effects of melatonin and undernutrition on the viability of ovine embryos during anestrus and the breeding season.Crossref | GoogleScholarGoogle Scholar |
Vázquez, M. I., Forcada, F., Casao, A., Abecia, J. A., Sosa, C., and Palacín, I. (2010a). Undernutrition and exogenous melatonin can affect the in vitro developmental competence of ovine oocytes on a seasonal basis. Reprod. Domest. Anim. 45, 677–684.
Vázquez, M. I., Abecia, J. A., Forcada, F., and Casao, A. (2010b). Effects of exogenous melatonin on in vivo embryo viability and oocyte competence of undernourished ewes after weaning during the seasonal anestrus. Theriogenology 74, 618–626.
| Effects of exogenous melatonin on in vivo embryo viability and oocyte competence of undernourished ewes after weaning during the seasonal anestrus.Crossref | GoogleScholarGoogle Scholar |
Vázquez, M. I., Forcada, F., Sosa, C., Casao, A., Sartore, I., Fernández-Foren, A., Meikle, A., and Abecia, J. A. (2013). Effect of exogenous melatonin on embryo viability and uterine environment in undernourished ewes. Anim. Reprod. Sci. 141, 52–61.
| Effect of exogenous melatonin on embryo viability and uterine environment in undernourished ewes.Crossref | GoogleScholarGoogle Scholar |
Wang, F., Tian, X., Zhang, L., Gao, C., He, C., Fu, Y., Ji, P., Li, Y., Li, N., and Liu, G. (2014). Beneficial effects of melatonin on in vitro bovine embryonic development are mediated by melatonin receptor 1. J. Pineal Res. 56, 333–342.
| Beneficial effects of melatonin on in vitro bovine embryonic development are mediated by melatonin receptor 1.Crossref | GoogleScholarGoogle Scholar |
Wheaton, J. E., Pohl, H. A., and Windels, H. F. (1990). Effects of melatonin and progesterone administered to ewes in spring and summer. J. Animn. Sci 68, 923–930.
| Effects of melatonin and progesterone administered to ewes in spring and summer.Crossref | GoogleScholarGoogle Scholar |
Yeates, N. T. M. (1949). The breeding season of the sheep with particular reference to its modification by artificial means using light. J. Agric. Sci. 39, 1–43.
| The breeding season of the sheep with particular reference to its modification by artificial means using light.Crossref | GoogleScholarGoogle Scholar |
Zhang, L., Chai, M., Tian, X., Wang, F., Fu, Y., He, C., Deng, S., Lian, Z., Feng, J., Tan, D., and Liu, G. (2013). Effects of melatonin on superovulation and transgenic embryo transplantation in small-tailed Han sheep (Ovis aries). Neuroendocrinol. Lett. 34, 294–301.
Zhao, H., Poon, A. M., and Pang, S. F. (2000). Pharmacological characterization, molecular subtyping, and autoradiographic localization of putative melatonin receptors in uterine endometrium of estrous rats. Life Sci. 66, 1581–1591.
| Pharmacological characterization, molecular subtyping, and autoradiographic localization of putative melatonin receptors in uterine endometrium of estrous rats.Crossref | GoogleScholarGoogle Scholar |
Zhao, H., Pang, S. F., and Poon, A. M. (2002). Variations of mt1 melatonin receptor density in the rat uterus during decidualization, the estrous cycle and in response to exogenous steroid treatment. J. Pineal Res. 33, 140–145.
| Variations of mt1 melatonin receptor density in the rat uterus during decidualization, the estrous cycle and in response to exogenous steroid treatment.Crossref | GoogleScholarGoogle Scholar |
