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Effect of exogenous melatonin on the ovary, the embryo and the establishment of pregnancy in sheep

Published online by Cambridge University Press:  01 March 2008

J. A. Abecia ,
F. Forcada ,
A. Casao  and
I. Palacín
J. A. Abecia*
Affiliation:
Departamento de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Miguel Servet, 177, 50013 Zaragoza, Spain
F. Forcada
Affiliation:
Departamento de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Miguel Servet, 177, 50013 Zaragoza, Spain
A. Casao
Affiliation:
Departamento de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Miguel Servet, 177, 50013 Zaragoza, Spain
I. Palacín
Affiliation:
Departamento de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Miguel Servet, 177, 50013 Zaragoza, Spain
*
E-mail: alf@unizar.es
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Abstract

Administration of melatonin to advance the breeding season in sheep has been widely used, since this hormone conveys the photoperiodic signal to the reproductive neuroendocrine axis. An increased lambing percentage has been reported following such treatment during anoestrus, which could be mediated through a higher rate of embryonic survival, either by an improvement in luteal function or by a reduction in the antiluteolytic mechanisms. The aim of this article is to review the body of knowledge on the effect of melatonin on the ovine ovary, the embryo and the establishment of pregnancy. Some studies using synchronized ewes have found that melatonin treatments during anoestrus do not improve ovulation rate by modifying the timing of follicle emergence, but increasing the number of ovulatory follicles by decreasing the atresia of medium and large follicles. On the other hand, the addition of melatonin to the in vitro maturation medium does not improve oocyte maturation rate in oocytes from sheep ovaries recovered either in anoestrus or in the breeding season. However, a luteotrophic effect of melatonin at either short or medium term has been reported. We have recently observed that melatonin implants tend to improve the survival of embryos collected from ewes after superovulation in anoestrus. More specifically, melatonin induced a significant reduction of the number and rate of non-viable (degenerate and retarded) embryos. Preliminary data from our laboratory suggest that the uterine sensitivity to progesterone – in terms of progesterone receptor expression – of superovulated ewes could be reduced by melatonin treatment. It can be concluded that the success of exogenous melatonin as a means to improve lamb production of sheep is due, at least in part, to an improvement of luteal support and embryonic survival.

Keywords

embryomelatoninovarypregnancy
Type
Full Paper
Information
animal , Volume 2 , Issue 3 , March 2008 , pp. 399 - 404
Copyright
Copyright © The Animal Consortium 2008

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References

Abecia, JA, Forcada, F, Lozano, JM 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.CrossRefGoogle Scholar
Abecia, JA, Forcada, F, Zuniga, O 2002. The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro. Veterinary Research Communications 26, 151–158.CrossRefGoogle ScholarPubMed
Abecia, JA, Palacin, I, Forcada, F, Valares, JA 2006. The effect of melatonin treatment on the ovarian response of ewes to the ram effect. Domestic Animal Endocrinology 31, 52–62.CrossRefGoogle Scholar
Bister, JL, Noel, B, Perrad, B, Mandiki, SNM, Mbayahaga, J, Paquay, R 1999. Control of ovarian follicles activity in the ewe. Domestic Animal Endocrinology 17, 315–328.CrossRefGoogle ScholarPubMed
Bittman, EL, Dempsey, RJ, Karsch, FJ 1983. Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113, 2276–2283.CrossRefGoogle ScholarPubMed
Bojanowska, E, Forsling, ML 1997. The effects of melatonin on vasopressin secretion in vivo: interactions with acetylcholine and prostaglandins. Brain Research Bulletin 42, 457–461.CrossRefGoogle ScholarPubMed
Cagnacci, A, Kräuchi, K, WirzJustice, A, Volpe, A 1997. Homeostatic versus circadian effects of melatonin on core body temperature in humans. Journal of Biological Rhythms 12, 509–517.CrossRefGoogle ScholarPubMed
Chemineau, P, Vandaele, E, Brice, G, Jardon, C 1991. The use of melatonin in improving reproduction performance in sheep. Recueil de Médecine Vétérinaire 167, 227–239.Google Scholar
Dimitriadis, JO, Papanikolau, T, Vainas, E, Amiridis, GS, Valasi, I, Samartzi, F, Rekkas, CA 2005. Effects of melatonin on in vitro maturation of bovine oocytes. Reproduction in Domestic Animals 40, 397.Google Scholar
Durotoye, LA, Webley, GE, Rodway, RG 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. Research in Veterinary Science 62, 87–91.CrossRefGoogle ScholarPubMed
Espinar, A, Osuna, C, Feliu, C, Guerrero, JM 1994. High-activity of retinal n-acetyltransferase in the early development of the chick-embryo – independence of lighting conditions. Neuroscience Letters 179, 103–106.CrossRefGoogle ScholarPubMed
Forcada, F, Abecia, JA, Sierra, I 1992. Seasonal-changes in estrus activity and ovulation rate in Rasa Aragonesa ewes maintained at 2 different body condition levels. Small Ruminant Research 8, 313–324.CrossRefGoogle Scholar
Forcada, F, Zarazaga, L, Abecia, JA 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.CrossRefGoogle Scholar
Forcada, F, Abecia, JA, Cebrián-Perez, JA, Muiño-Blanco, T, Valares, JA, Palacín, I, 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.CrossRefGoogle ScholarPubMed
Garde López-Brea, JJ, Pérez-Guzmán, MD, Pérez Garnelo, SS, Garzón Sigler, A, Montoro Angulo, V 1996. Características seminales de corderos de raza Manchega tratados con implantes de melatonina. Archivos de Zootecnia 45, 395–401.Google Scholar
Gimeno, MF, Fuentes, AM, Landa, A, Sterinspeziale, N, Cardinali, DP, Gimeno, AL 1980. Melatonin – inhibitor of prostaglandin release. Acta Physiologica Latinoamericana 30, 38–39.Google Scholar
Gómez Brunet, A, López Sebastian, A, Picazo, RA, Cabellos, B, Goddard, S 1995. Reproductive response and LH-secretion in ewes treated with melatonin implants and induced to ovulate with the ram effect. Animal Reproduction Science 39, 23–34.CrossRefGoogle Scholar
Gonzalez-Bulnes, A, Garcia-Garcia, RM, Santiago-Moreno, J, Dominguez, V, Lopez-Sebastian, A, Cocero, MJ 2003. Reproductive season affects inhibitory effects from large follicles on the response to superovulatory FSH treatments in ewes. Theriogenology 60, 281–288.CrossRefGoogle ScholarPubMed
Haresign, W 1992. The effect of implantation of lowland ewes with melatonin on the time of mating and reproductive performance. Animal Production 54, 31–39.Google Scholar
Haresign, W, Peters, AR, Staples, LD 1990. The effect of melatonin implants on breeding activity and litter size in commercial sheep flocks in the UK. Animal Production 50, 111–121.Google Scholar
Ishwar, AK, Memon, MA 1996. Embryo transfer in sheep and goats: a review. Small Ruminant Research 19, 35–43.CrossRefGoogle Scholar
Iuvone, PM, Gan, JW 1994. Melatonin receptor-mediated inhibition of cyclic AMP accumulation in chick retinal cell cultures. Journal of Neurochemistry 63, 118–124.CrossRefGoogle ScholarPubMed
Jabbour, HN, Ryan, JP, Evans, G, Maxwell, WMC 1991. Effects of season, GnRH administration and lupin supplementation on the ovarian and endocrine responses of merino ewes treated with PMSG and FSH-P to induce superovulation. Reproduction, Fertility, and Development 3, 699–707.CrossRefGoogle ScholarPubMed
Kaya, A, Baspinar, N, Yildiz, C, Kurtoglu, F, Ataman, MB, Haliloglu, S 2000. Influence of melatonin implantation on sperm quality, biochemical composition of the seminal plasma and plasma testosterone levels in rams. Revue de Médecine Vétérinaire 151, 1143–1146.Google Scholar
Lamming, GE, Wathes, DC, Flint, AP, Payne, JH, Stevenson, KR, Vallet, JL 1995. Local action of trophoblast interferons in suppression of the development of oxytocin and oestradiol receptors in ovine endometrium. Journal of Reproduction and Fertility 105, 165–175.CrossRefGoogle ScholarPubMed
Lopez Sebastian, A, Cognie, Y, Cocero, MJ, Delafuente, J, Poulin, N 1990. Effect of season and duration of FSH treatment on embryo production in sheep. Theriogenology 34, 175–180.CrossRefGoogle Scholar
Luther, JS, Redmer, DA, Reynolds, LP, Choi, JT, Pant, D, Navanukraw, C, Arnold, DR, Scheaffer, AN, Borowicz, P, Kirsch, JD, Weigl, RM, Kraft, KC, Grazul-Bilska, AT 2005. Ovarian follicular development and oocyte quality in anestrous ewes treated with melatonin, a controlled internal drug release (CIDR) device and follicle stimulating hormone. Theriogenology 63, 2136–2146.CrossRefGoogle ScholarPubMed
McElhinny, AS, Davis, FC, Warner, CM 1996. The effect of melatonin on cleavage rate of C57BL/6 and CBA/Ca preimplantation embryos cultured in vitro. Journal of Pineal Research 21, 44–48.CrossRefGoogle ScholarPubMed
McEvoy, TG, Robinson, JJ, Aitken, RP, Robertson, IS 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.CrossRefGoogle ScholarPubMed
McLeod, BJ, Haresign, W, Lamming, GE 1982. The induction of ovulation and luteal function in seasonally anestrous ewes treated with small-dose multiple injections of GnRH. Journal of Reproduction and Fertility 65, 215–221.CrossRefGoogle Scholar
McLeod, BJ, Capel, J, Lamming, GE, Haresign, W, Peters, AR 1984. Continuous v. pulsatile administration of GnRH to induce ovulation in the cow and ewe. Journal of Steroid Biochemistry and Molecular Biology 20, 1400.CrossRefGoogle Scholar
Meikle, A, Kulcsar, M, Chilliard, Y, Febel, H, Delavaud, C, Cavestany, D, Chilibroste, P 2004. Effects of parity and body condition at parturition on endocrine and reproductive parameters of the cow. Reproduction (Cambridge, England) 127, 727–737.CrossRefGoogle ScholarPubMed
Mitchell, LM, Dingwall, WS, Mylne, MJA, Hunton, J, Matthews, K, Gebbie, FE, McCallum, GJ, McEvoy, TG 2002. Season affects characteristics of the pre-ovulatory LH surge and embryo viability in superovulated ewes. Animal Reproduction Science 74, 163–174.CrossRefGoogle ScholarPubMed
Noël, B, Mandiki, SMN, Perrad, B, Bister, JL, Paquay, R 1999. Terminal follicular growth, ovulation rate and hormonal secretion after melatonin pretreatment prior to FGA-PMSG synchronisation in Suffolk ewes at the onset of the breeding season. Small Ruminant Research 32, 269–277.CrossRefGoogle Scholar
Rao, BS, Naidu, KS, Amarnath, D, Vagdevi, R, Rao, AS, Brahmaiah, KV, Rao, VH 2002. In vitro maturation of sheep oocytes in different media during breeding and non-breeding seasons. Small Ruminant Research 43, 31–36.CrossRefGoogle Scholar
Robinson, JJ, Wigzell, S, Aitken, RP, Wallace, JM, Ireland, S, Robertson, IS 1991. The modifying effects of melatonin, ram exposure and plane of nutrition on the onset of ovarian activity, ovulation rate and the endocrine status of ewes. Animal Reproduction Science 26, 73–91.CrossRefGoogle Scholar
Rondon, Z, Forcada, F, Zarazaga, L, Abecia, JA, Lozano, JM 1996. Oestrous activity, ovulation rate and plasma melatonin concentrations in Rasa Aragonesa ewes maintained at two different and constant body condition score levels and implanted or reimplanted with melatonin. Animal Reproduction Science 41, 225–236.CrossRefGoogle Scholar
Ryan, JP, Hunton, JR, Maxwell, WMC 1991. Increased production of sheep embryos following superovulation of merino ewes with a combination of pregnant mare serum gonadotropin and follicle stimulating hormone. Reproduction, Fertility, and Development 3, 551–560.CrossRefGoogle ScholarPubMed
Schiewe, MC, Fitz, TA, Brown, JL, Stuart, LD, Wildt, DE 1991. Relationship of estrus synchronization method, circulating hormones, luteinizing-hormone and prostaglandin F2-alpha receptors and luteal progesterone concentration to premature luteal regression in superovulated sheep. Journal of Reproduction and Fertility 93, 19–30.CrossRefGoogle ScholarPubMed
Short, RV 1969. Implantation and the maternal recognition of pregnancy. In Foetal autonomy (ed. G Wolstenholme and M O’Connor), pp. 2–26. Ciba Foundation Churchill, London.Google Scholar
Southee, JA, Hunter, MG, Haresign, W 1988. Function of abnormal corpora lutea in vivoafter GnRH-induced ovulation in the anestrous ewe. Journal of Reproduction and Fertility 84, 131–137.CrossRefGoogle Scholar
Spencer, TE, Burghardt, RC, Johnson, GA, Bazer, FW 2004. Conceptus signals for establishment and maintenance of pregnancy. Animal Reproduction Science 82–83, 537–550.CrossRefGoogle ScholarPubMed
Stenbak, TK, Redmer, DA, Berginski, HR, Erickson, AS, Navanukraw, C, Toutges, MJ, Bilski, JJ, Kirsch, JD, Kraft, KC, Reynolds, LP, Grazul-Bilska, AT 2001. Effects of follicle stimulating hormone (FSH) on follicular development, oocyte retrieval, and in vitro fertilization (IVF) in ewes during breeding season and seasonal anestrus. Theriogenology 56, 51–64.CrossRefGoogle ScholarPubMed
Trounson, AO, Willadsen, SM, Moor, RM 1976. Effect of prostaglandin analog cloprostenol on estrus, ovulation and embryonic viability in sheep. Journal of Agricultural Science 86, 609–611.CrossRefGoogle Scholar
Wallace, JM, Robinson, JJ, Wigzell, S, Aitken, RP 1988. The effect of melatonin on the peripheral concentrations of LH and progesterone postestrus and on conception rate in ewes. Animal Production 46, 499.Google Scholar
Webley, GE, Luck, MR 1986. Melatonin directly stimulates the secretion of progesterone by human and bovine granulosa cells in vitro. Journal of Reproduction and Fertility 78, 711–717.CrossRefGoogle ScholarPubMed
Webley, GE, Luck, MR, Hearn, JP 1988. Stimulation of progesterone secretion by cultured human granulosa cells with melatonin and catecholamines. Journal of Reproduction and Fertility 84, 669–677.CrossRefGoogle ScholarPubMed
Yeates, NTM 1949. The breeding season of the sheep with particular reference to its modification by artificial means using light. Journal of Agricultural Science 39, 1–43.CrossRefGoogle Scholar
Yie, SM, Niles, LP, Younglai, EV 1995. Melatonin receptors on human granulosa cell membranes. Journal of Clinical Endocrinology and Metabolism 80, 1747–1749.Google ScholarPubMed
Zhao, H, Poon, AM, Pang, SF 2000. Pharmacological characterization, molecular subtyping, and autoradiographic localization of putative melatonin receptors in uterine endometrium of estrous rats. Life Sciences 66, 1581–1591.CrossRefGoogle ScholarPubMed
Zhao, H, Pang, SF, Poon, AM 2002. Variations of mt1 melatonin receptor density in the rat uterus during decidualization, the estrous cycle and in response to exogenous steroid treatment. Journal of Pineal Research 33, 140–145.CrossRefGoogle ScholarPubMed
Zúñiga, O, Forcada, F, Abecia, JA 2002. The effect of melatonin implants on the response to the male effect and on the subsequent cyclicity of Rasa Aragonesa ewes implanted in April. Animal Reproduction Science 72, 165–174.CrossRefGoogle Scholar