Seasonality in mammalian reproduction: a review

Authors

DOI:

https://doi.org/10.33448/rsd-v9i10.8236

Keywords:

Circadian Rhythm; Gonadotropins; Melatonin; Photoperiod.

Abstract

Some factors related to the external environment directly or indirectly influence the animals, causing them to exhibit specific characteristics in their reproductive physiology. Among the environmental variables, there is the daily photoperiod, which allows classifying the seasonal species in short- day animals (buffaloes and small ruminants) and long-day (horses). Thus, in these species the functioning of the hypothalamic-pituitary-gonadal axis is modulated by the action of melatonin that is released in concentrations proportional to light intensity. Melatonin influences the release direct of GnRH and indirect of gonadotropins (FSH and LH), as well as gametogenesis influence, the synthesis of sex hormones and sexual behavior. The aim of this review is to evaluate the influence of photoperiod on reproductive physiology, analyzing the effects of circadian rhythm and the physiological aspects of melatonin in the regulation and modulation of animal reproduction.

References

Abecia, J. A., Forcada, F., & González-Bulnes, A. (2012). Hormonal control of reproduction in small ruminants. Animal Reproduction Science, 130 (3-4), 173-179.

Aguirre, V., Orihuela, A., & Vazquez, R. (2007). Effect of semen collection frequency on seasonal variation in sexual behaviour, testosterone, testicular size and semen characteristics of tropical hair sheep (Ovis aries). Tropical Animal Health and Production, 39(4), 271-277, 2007.

Arendt, J. (1995). Melatonin and the mammalian pineal gland. London/UK: Chapman & Hall.

Arendt, J. (1998). Melatonin and the pineal gland: influence on mammalian seasonal and circadian physiology. Reviews of Reproduction, 3(1), 13-22.

Arroyo, L. J., Gallegos-Sánchez, J., Villa-Godoy, A., Berruecos, J. M., Perera, G., & Valencia, J. (2007). Reproductive activity of Pelibuey and Suffolk ewes at 19º north latitude. Animal Reproduction Science, 102(2), 24-30.

Avdi, M., Banos, G., Stefos, K., & Chemineau, P. (2004). Seasonal variation in testicular volume and sexual behavior of Chios and Serres rams. Theriogenology, 62(1-2), 275–282.

Baler, R., Covington, S., & Klein, D. C. (1999). Rat arylalkylamine N-acetyltransferase gene: upstream and intronic components of a bipartite promoter. Biology of the Cell, 91, 699-705.

Baratta, M., & Tamanini, C. (1992). Effect of melatonin on the in vitro secretion of progesterone and estradiol 17β by ovine granulosa cells. Acta Endocrinologica, 127(4), 366–370.

Barker, J. L., & Ransom, B. R. (1978). Pentobarbitone pharmacology of mammalian central neurones grown in tissue culture. The Journal of Physiology, 280, 355–372.

Barrell, G. K., Moenter, S. M., Caraty, A., & Karsch, F. J. (1992). Seasonal changes of gonadotrophin-releasing hormone secretion in the ewe. Biology of Reproduction, 46, 1130–1135.

Berlinguer, F.; Leoni, G. G.; Succu, S.; Spezzigu, A.; Madeddu, M.; Satta, V.; Bebbere, D.; Contreras-Solis, I.; Gonzalez-Bulnes, A.; Naitana, S. (2009). Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model. Journal of Pineal Research, 46(4), 383–391.

Bertrand, F.; Viguié, C.; Picard, S.; Malpaux, B. (1998). Median eminence dopaminergic activation is critical for the early long-day inhibition of luteinizing hormone secretion in the ewe. Endocrinology, 139(12), 5094–5102.

Bittman, E. L., Kaynard, A. H., Olster, D. H., Robinson, J. E., Yellon, S. M.; Karsch, F. J. (1985). Pineal melatonin mediates photoperiodic control of pulsatile luteinizing hormone secretion in the ewe. Neuroendocrinology, 40, 409-418.

Bittman, E. L. (1993). The sites and consequences of melatonin binding in mammals. American Zoologist, 33, 200–211.

Bogusz, A. L., Hardy, S. L., Lehman, M. N., Connors, J. M., Hileman, S. M., Sliwowska, J. H.; Billings, H. J., Mcmanus, C. J., Valent, M., Singh, S. R., Nestor, C. C.; Coolen, L. M.; Goodman, R. L. (2008). Evidence that γ-aminobytyric acid is part of the neural circuit mediating estradiol negative feedback in anestrous ewes. Endocrinology, 149(6), 2762-2772.

Bour, B., Palmer, E., Driancourt, M. A. (1985). Stimulation of ovarian activity in the pony mare during winter anoestrus. In: Ellendorff, F. & Elsaesser, F. (Ed.). Endocrine causes of seasonal and lactational anestrus in farm animals (pp.85-97). Dordrecht: Martinus Nijhoff Publisher.

Brann, D. W., & Maresh, V. B. (1994). Excitatory amino acids: function and significance in reproduction and neuroendocrine regulation. Frontiers in Neuroendocrinology, 15(1), 3–49.

Brannstrom, M.; Enskog, A. (2002). Leukocyte networks and ovulation. Journal of Reproductive Immunology, 57, 47-60.

Brannstrom, M., & Norman, R. J. (1993). Involvement of leukocytes and cytokines in the ovulatory process and corpus luteum function. Human Reproduction, 8(10), 1762-1775.

Brzezinski, A., Seibel, M. M., Lynch, H. J., Deng, M. H., & Wurtman, R. J. (1987). Melatonin in human preovulatory follicular fluid. The Journal of Clinical Endocrinology & Metabolism, 64, 865–867.

Brydon, L., Roka, F., Petit, L., Coppet, P., Tissot, M., Barrett, P., Morgan, P. J.; Nanoff, C.; Strosberg, A. D.; Jockers, R. (1999). Dual signaling of human Mel1a melatonin receptors via Gi2 , Gi3, and Gq/11 Proteins. Molecular Endocrinology, 13(12), 2025–2038.

Chattoraj, A., Bhattacharyya, S.; Basu, D.; Bhattacharya, S.; Bhattacharya, S.; Maitra, S. K. (2005). Melatonin accelerates maturation inducing hormone (MIH): induced oocyte maturation in carps. General and Comparative Endocrinology, 140, 145–55.

Clarke, I. J., & Cummins, J. T. (1984). Direct pituitary effects of estrogen and progesterone on gonadotropin secretion in the ovarictomized ewe. Neuroendocrinology, 39(3), 267-274.

Clarke, I. J. (1993). Variable patterns of gonadotropin-releasing hormone secretion during the estrogen-induced luteinizing hormone surge in ovariectomized ewes. Endocrinology, 133(4), 1624-1632.

Clarke, I. J., Smith, J. T., Caraty, A., Goodman, R. L., & Lehman, M. N. (2009). Kisspetin and seasonality in sheep. Peptides, 30, 154-163.

Diaz, E., Garidou, M. L., Dardente, H., Salingre, A., Pévet, P.; Simonneaux, V. (2003). Expression and regulation of Icer mRNA in the Syrian hamster pineal gland. Molecular and Cellular Endocrinology, 112, 163–169.

Ding, J. M., Faiman, L. E., Hurst, W. J., Kuriashkina, L. R., Gillette, M. U. (1997). Resetting the biological clock: mediation of nocturnal CREB phosphorylation via light, glutamate, and nitric oxide. The Journal of Neuroscience, 17(2), 667–675.

Dobbins, A., Lubbers, L. S., Jackson, G. L., Kuehl, D. E., Hileman, S. M. (2004). Neuropeptide Y gene expression in male sheep: influence of photoperiod and testosterone. Neuroendocrinology, 79, 82–89.

Drijfhout, W. J., Van Der Linde, A. G., Kooi, S. E., Grol, C. J., Westerink, B. H. C. (1996). Norepinephrine release in the rat pineal gland: the input from the biological clock measured by in vivo microdialysis. Journal of Neurochemistry, 66, 748–755.

Dubocovich, M. L. (1988). Pharmacology and function of melatonin receptors. The FASEB Journal, 2, 2765–2773.

Dubocovich, M. L. (1995). Melatonin receptors: are there multiple subtypes? Trends in Pharmacological Sciences, 16, 50–56.

Dyrmundsson, Ó. R. (1978). Studies on the breeding season of Icelandic ewes and ewes lambs. Journal of Agricultural Science, 90, 275-281.

Ekmekcioglu, C. (2006). Melatonin receptors in humans: Biological role and clinical relevance. Biomedicine & Pharmacotherapy, 60, 97–108.

Espey, L. L. (1994). Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biology of Reproduction, 50, 233–238.

Fernandes, R. M. F. (2006). O sono normal. Medicina (Ribeirão Preto), 39(2), 157-168.

Fiske, V. M., Parker, K. L., Ulmer, R. A., Ow, C. H.; Aziz, N. (1984). 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, 114(2), 407–410.

Frungieri, M. B., Mayerhofer, A., Zitta, K., Pigataro, O. P., Calandra, R. S., Gonzalez-Calvar, S. I. (2005). Direct Effect of Melatonin on Syrian hamster testes: melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system. Endocrinology, 146(3), 1541–1552.

Gallegos-Sánchez, J., Delaleu, B., Caraty, A., Malpaux, B., Thiery, J. C. (1997). Estradiol acts locally within the retrochiasmatic area to inhibit pulsatile luteinizing-hormone release in the female sheep during anestrus. Biology of Reproduction, 56, 1544–1549.

Gastel, J. A., Roseboom, P. H., Rinaldi, P. A., Weller, J. L. Klein, D. C. (1998). Melatonin production: proteasomal proteolysis in serotonin N-acetyltransferase regulation melatonin production: proteasomal proteolysis in serotonin N-acetyltransferase regulation. Science, 279, 1358–1360.

Gauche, H., Calvo, M. C. M., Assis, M. A. A. de (2006). Ritmos circadianos de consumo alimentar nos lanches e refeições de adultos: aplicação do semanáio alimentar. Brazilian Journal of Nutrition, 19(2), 177-185.

Gauer, F., Poirel, V. J., Garidou, M. L., Simonneaux, V.; Pevet, P. (1999). Molecular cloning of the arylalkylamine- N -acetyltransferase and daily variations of its mRNA expression in the Syrian hamster pineal gland. Molecular Brain Research, 7, 87–95.

Gayrard, V., Malpaux, B., Tillet, Y.; Thiery, J. C. (1994). Estradiol increases tyrosine hydroxylase activity of the A15 nucleus dopaminergic neurons during long days in the ewe. Biology of Reproduction, 50, 1168–1177.

Gayrard, V., Thiéry, J. C., Thibault, J., Tillet, Y. (1995). Efferent projections from the retrochiasmatic area to the median eminence and to the pars nervosa of the hypophysis with special reference to the A15 dopaminergic cell group in the sheep. Cell and Tissue Research, 281, 561–567.

Godley, W. C., Wilson, R. L., Hurs, V. (1966). Effect of Controlled Environment on the Reproductive Performance of Ewes. Journal of Animal Science, 25(1), 212-216.

Goldman, B. D. (2001). Mammalian Photoperiodic System: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. Journal of Biological Rhythms, 16(4), 283–301.

Gómez-Brunet, A. G., Malpaux, B., Daveau, A., Taragnat, C.; Chemineau P. (2002). Genetic variability in melatonin secretion originates in the number of pinealocytes in sheep. Journal of Endocrinology, 172(2), 397–404.

Goodman, R. L., Meyer, S. L. (1984). Effects of pentobarbital secretion luteinizing anesthesia evidence hormone on tonic for active luteinizing inhibition hormone of in the ewe: in anestrus. Biology of Reproduction, 30, 374–381.

Goodman, R. L., Inskeep, E. K. (2006). Neuroendocrine Control of the Ovarian Cycle of the Sheep. In: Neill, J. D. & Knobil, E. (Ed.). Physiology of Reproduction. 3. ed. (2389-2428). London: Elsevier.

Gordon, I. (1997). Controlled Reproduction in Sheep and Goats. Wallingford/UK: CABI Publishing.

Guerin, M. V.; Wang, X. J. (1994). Environmental temperature has an influence on timing of the first ovulation of seasonal estrus in the mare. Theriogenology, 42(6), 1053-1060.

Guha, M., Maity, P., Choubey, V., Mitra, K., Reiter, R. J.; Bandyopadhyay, U. (2007). Melatonin inhibits free radical-mediated mitochondrial-dependent hepatocyte apoptosis and liver damage induced during malarial infection. Journal of Pineal Research, 43, 372–381.

Hannibal, J., Ding, J. M., Chen, D.,, Fahrenkrug, J., Larsen, P. J., Gillette, U. M., Mikkelsen, J. D. (1997). Pituitary adenylate cyclase-activating peptide (PACAP) in the retinohypothalamic tract: a potential daytime regulator of the biological clock. The Journal of Neuroscience, 17(7), 2637–2644.

Hardy, S. L., Anderson, G. M., Valent, M., Connors, J. M., Goodman, R. L. (2003). Evidence that estrogen receptor alpha, but not beta, mediates seasonal changes in the response of the ovine retrochiasmatic area to estradiol. Biology of Reproduction, 68, 846–852.

Havern, R. L.; Whisnant, C. S.; Goodman, R. L. (1994). Dopaminergic structures in the ovine hypothalamus mediating estradiol negative feedback in anestrous ewes. Endocrinology, 134, 1905-1914.

Herbison, A. E. (1995). Neurochemical identity of neurons expressing oestrogen and androgen receptors in sheep hypothalamus. Journal of Reproduction and Fertility. Supplement, 49, 271-283.

Hsu, S. Y., Lai, R. J., Finegold, M.; Hsueh, A. J. (1996). Targeted overexpression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology, 137, 4837–4843.

I’anson, H., Legan, S. J. (1988). Changes in LH pulse frequency and serum progesterone concentrations during the transition to breeding season in ewes. Journal of Reproduction and Fertility, 82(1), 341–351.

Illnerova, H., Hoffmann, K., Vanecek, J. (1984). Adjustment of pineal melatonin and N-acetyltransferase rhythms to change from long to short photoperiod in the Djungarian hamster Phodopus sungorus. Neuroendocrinology, 38(3), 226–231.

Ishizuka, B., Kuribayashi, Y., Murai, K., Amemiya, A., Itoh, M. T. (2000). The effect of melatonin on in vitro fertilization and embryo development in mice. Journal of Pineal Research, 28(1), 48–51.

Itoh, M. T., Ishizuka, B., Kuribayashi, Y., Amemiya, A.; Sumi, Y. (1999). Melatonin, its precursors, and synthesizing enzyme activities in the human ovary. Molecular Human Reproduction, 5(5), 402–408.

Johnston, J. D., Bashforth, R., Diack, A., Andersson, H., Lincoln, G. A.; Hazlerigg, D. G. (2004). Rhythmic melatonin secretion does not correlate with the expression of arylalkylamine n-acetyltransferase, inducible cyclic AMP early repressor, period1 or cryptochrome1 mRNA in the sheep pineal. Neuroscience, 124, 789–795.

Kang, J. T., Koo, O. J., Kwon, D. K., Park, H. J., Jang, G., Kang, S. K., 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. Journal of Pineal Research, 46, 22–28.

Karsch, F. J., Goodman, R. L., Legan, S. J. (1980). Feedback basis of seasonal breeding: test of an hypothesis. Journal of Reproduction and Fertility, 58, 521–535.

Karsch, F. J., Bittman, E. L., Foster, D. L., Goodman, R. L.; Legan, S. J.; Robinson, J. E. (1984). Neuroendocrine basis of seasonal reproduction. Recent Progress in Hormone Research, 40, 185–232.

Karsch, F. J., Cummins, J. T., Thomas, G. B.; Clarke, I. J. (1987). Steroid feedback inhibition of pulsatile secretion of gonadotropin-releasing hormone in the ewe. Biology of Reproduction, 36(5), 1207–1218.

Karsch, F. J., Dahl, G. E., Evans, N. P., Manning, J. M., Mayfield, K. P., Moenter, S. M., Foster, D. L. (1993). Seasonal changes in gonadotropin-releasing hormone secretion in the ewe: alteration in response to the negative feedback action of estradiol. Biology of Reproduction, 49(6), 1377–1383.

Kennaway, D. J., Voultsios, A. (2000). Circadian rhythm of free melatonin in human plasma. Journal of Clinical Endocrinology and Metabolism, 83(3), 1013–1015.

Kennaway, D. J. (2005). The role of circadian rhythmicity in reproduction. Human Reproduction Update, 11(1), 91-101.

Kim, J. K., Lee, C. J. (2000). Effect of exogenous melatonin on the ovarian follicles in gamma-irradiated mouse. Mutation Research, 449(1-2), 33-39.

Klein, D. C. (1985). Photoneural Regulation of the Mammalian Pineal Gland. CIBA Foundation Symposia, 117, 38-56.

Klein, D. C., Coon, S. L., Roseboom, P. H., Weller, J. L., Bernard, M., Gastel, J. A., Zatz, M., Iuvone, P. M., Rodriguez, I. R., Bégay, V., Falcón, J., Cahill, G. M., Cassone, V. M., Baler, R. (1997). The melatonin rhythms generating enzyme: molecular regulation of serotonin N-acetyltransferase in the pineal gland. Recent Progress in Hormone Research, 52, 307–357.

Lee, C. J., Do, B. R., Lee, Y. H., Park, J. H., Kim, S. J., Kim, J. K., Roh, S. I.; Yoon, Y. D.; Yoon, H. S. (2001). Ovarian expression of melatonin Mel1a receptor mRNA during mouse development. Molecular Reproduction and Development, 59(2), 126–132.

Legan, S. J., Karsch, F. J., Foster, D. L. (1977). The endocrine control of seasonal reproductive function in the ewe: A marked change in response to the negative feedback action of estradiol on luteinizing hormone secretion. Endocrinology, 101, 818-824.

Lehman, M. N., Karsch, F. J. (1993). Do gonadotropin releasing hormone, tyrosine hydroxylase-, and β-endorphin-immunoreactive neurons contain estrogen receptors? A double-label immunocytochemical study in the Suffolk ewe. Endocrinology, 133, 887–895.

Lehman, M. N., Durham, D. M., Jansen, H. T., Adrian, B.; Goodman, R. L. (1996). Dopaminergic A14/A15 neurons are activated during estradiol negative feedback in the anestrous ewe. Endocrinology, 137, 4443–4450.

Lincoln, G. A., Davidson, W. (1977). The relationship between sexual and aggressive behaviour, and pituitary and testicular activity during the seasonal sexual cycle of rams, and the influence of photoperiod. Journal of Reproduction and Fertility, 49(2), 267–276.

Liu, T.; Borjigin, J. (2005). N-acetyltransferase is not the rate-limiting enzyme of melatonin synthesis at night. Journal of Pineal Research, 39, 91-96.

Mallampati, R. S., Pope, A. L., Casida, L. E. (1971). Effect of suckling on postpartum anestrus in ewes lambing in different seasons of the year. Journal of Animal Science, 32(4), 673–678.

Malpaux, B., Daveau, A., Maurice, F.; Gayrard, V.; Thiery, J. C. (1993). Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biology of Reproduction, 48, 752–760.

Malpaux, B., Viguié, C., Skinner, D. C., Thiéry, J. C.; Chemineau, P. (1997). Control of the circannual rhythm of reproduction by melatonin in the ewe. Brain Research Buletin, 44, 431–438.

Malpaux, B., Daveau, A., Maurice-Mandon, F., Duarte, G., Chemineau, P. (1998). Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology, 139(4), 1508–1516.

Malpaux, B., Migaud, M., Tricoire, H., Chemineau, P. (2001). Biology of mammalian photoperiodism and critical role of pineal gland and melatonin. Journal of Biological Rhythms, 16, 336-347.

Malpaux, B. Seasonal regulation of reproduction in mammals. (2006). In: Neill, J. D. & Knobil, E. (Ed.). Physiology of Reproduction. 3. ed. (2231-2281). London: Elsevier.

Marques, N., Menna-Barreto, L. (2003). Cronobiologia: princípios e aplicações. 3. ed. São Paulo: Editora Fiocruz.

Masana, M. I., Dubocovich, M. L. (2001). Melatonin receptor signaling: finding the path through the dark. Science STKE, 107(pe39), 1–5.

Masson-Pevet, M., George, D., Kalsbeek, A., Saboureau, M., Lakhadar-Ghazal, N., Pévet, P. (1994). An attempt to correlate brain areas containing melatonin-binding sites with rhythmic functions: a study in five hibernator species. Cell and Tissue Research, 278, 97–106.

Mcmanus, C. J., Valent, M., Connors, J. M., Hileman, S. M., Goodman, R. L. (2004). Time of year alters response to nitric oxide synthase inhibition in seasonally anestrous ewes. Annual Meeting of Society for Neuroscience, Abstr. 756.23.

Messner, M., Huether, G., Lorf, T., Ramadori, G., Schwörer, H. (2001). Presence of melatonin in the human hepatobiliary-gastrointestinal tract. Life Sciences, 69, 543-551.

Migaud, M., Daveau, A., Malpaux, B. (2005). MTNR1A melatonin receptors in the ovine pre-mammillary hypothalamus: day-night variation in the expression of the transcripts. Biology of Reproduction, 72, 393–398.

Moore, R. Y., & Eichler V. B. (1972). Loss of circadian adrenal corticosterone rhythm following suprachiasmatic nucleus lesions in the rat. Brain Research, 42(1), 201-206.

Morgan, P. J., Barrett, P., Howell, H. E., Helliwell, R. (1994). Melatonin receptors: localization, molecular pharmacology and physiological significance. Neurochemistry International, 24, 101–146.

Nagy, P., Guillaume, D., & Daels, P. (2000). Seasonality in mares. Animal Reproduction Science, 60-61, 245-262.

Nakamura, Y., Tamura, H., Takayama, H., Kato, H. (2003). Increased endogenous level of melatonin in preovulatory human follicles does not directly influence progesterone production. Fertility and Sterility, 80(4), 1012-1016.

Nakazawa, K., Marubayashi, U., & Mccann, S. M. (1991). Mediation of the short-loop negative feedback of luteinizing hormone (LH) on LH-releasing hormone release by melatonininduced inhibition of LH release from the pars tuberalis. Proceedings of National Academy of Sciences of the United States, 88, 7576–7579.

Niles, L. P., Wang, J., Shen, L., Lobb, D. K., Younglai, E. V. (1999). Melatonin receptor mRNA expression in human granulosa cells. Molecular and Cellular Endocrinology, 156, 107-110.

Nosjean, O., Nicolas, J. P., Klupsch, F., Delagrange, P., Canet, E., & Boutin, J. A. (2001). Comparative pharmacological studies of melatonin receptors: MT1, MT2 and MT3/QR2. Tissue distribution of MT3/QR2. Biochemical Pharmacology, 61, 1369–1379.

Ortavant, R., Bocquier, F., Pelletier, J., Ravault, J. P., Thimonier, J., & Volland-Nail, P. (1988). Seasonality of reproduction in sheep and its control by photoperiod. Australian Journal of Biological Sciences, 41(1), 69–85.

Pereira, A. S., Shitsuka, D. M., Parreira, F. J., & Shitsuka, R. (2018). Metodologia da pesquisa científica. [e-book]. Santa Maria. Ed. UAB/NTE/UFSM. Recuperado de https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computacao_MetodologiaPesquisa-Cientifica.pdf?sequence=1.

Pontes, G. N., Cardoso, E. C., Carneiro-Sampaio, M. M. S., Markus, R. P. (2006). Injury switches melatonin production source from endocrine (pineal) to paracrine (phagocytes) - melatonin human colostrum and colostrum phagocytes. Journal of Pineal Research, 41, 136-141.

Ratts, V. S., Flaws, J. A., Kolp, R.; Sorenson, C. M., & Tilly, J. L. (1995). Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology, 136, 3665–3668.

Ravault, J. P., Chesneau, D. (1999). The onset of increased melatonin secretion after the onset of darkness in sheep depends on the photoperiod. Journal of Pineal Research, 27(1), 1–8.

Reiter, R. J. (1994). Melatonin suppression by static and extremely low frequency electromagnetic fields: relationship to the reported increased incidence of cancer. Reviews on Environmental Health, 10(3-4), 171-86.

Reiter, R. J., Tan, D. X., Manchester, L. C., Paredes, S. D., Mayo, J. C., Sainz, R. M. (2009). Melatonin and Reproduction Revisited. Biology of Reproduction, 81(3), 445–456.

Reiter, R. J., Rosales-Corral, S. A., Manchester, L. C., Tan, D. X. (2013). Peripheral reproductive organ health and melatonin: ready for prime time. International Journal of Molecular Science, 14, 7231-7272.

Richards, J. S. (2005). Ovulation: new factors that prepare the oocyte for fertilization. Molecular and Cellular Endocrinology, 234, 75-79.

Richter, H. G., Torres-Farfán, C., Rojas-Garcia, P. P., Campino, C., Torrealba, F., Serón-Ferré, M. (2004). The Circadian Timing System: Making Sense of day/night gene expression. Biological Research, 37(1), 11-28.

Robinson, J. E., & Karsch, F. J. (1984). Refractoriness to inductive day lengths terminates the breeding season of the Suffolk ewe. Biology of Reproduction, 31, 656–663.

Robinson, J. E., Radford, H. M., Karsch, F. J. (1985). Seasonal changes in pulsatile luteinizing hormone (LH) secretion in the ewe: relationship of frequency of LH pulses to day length and response to estradiol negative feedback. Biology of Reproduction, 33(2), 324–334.

Robinson, J. J. (1996). Nutrition and Reproduction. Animal Reproduction Science, 42(1-4), 25-34.

Rocha, R. M. P., Matos, M. H. T., Lima, L. F., Saraiva, M. V. A., Alves, A. M. C. V., Rodrigues, A. P. R., Figueiredo, J. R. (2011). Melatonina e reprodução animal: implicações na fisiologia ovariana. Acta Veterinaria Brasilica, 5(2), 147-157.

Rönnberg, L., Kauppila, A., Leppäluoto, J., Martikainen, H.; Vakkuri, O. (1990). Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration. Journal of Clinical Endocrinology and Metabolism, 71(2), 492–496.

Rosa, H. J. D., Bryant, M. J. (2002). The ‘ram effect’ as a way of modifying the reproductive activity in the ewe: a review. Small Ruminant Research, 45, 1–16.

Rosa, H. J. D., Bryant, M. J. (2003). Seasonality of reproduction in sheep. Small Ruminant Research, 48(3), 155-171.

Salhab, M., Dhorne-Pollet, S., Auclair, S., Guyader-Joly, C., Brisard, D., Dalbies-Tran, R.; Dupont, J.; Ponsart, C.; Mermillod, P.; Uzbekova, S. (2013). In vitro maturation of oocytes alters gene expression and signaling pathways in bovine cumulus cells. Molecular Reproduction and Development, 80, 166–182.

Schaeffer, H. J., Sirotkin, A. V. (1997). Melatonin and serotonin regulate the release of insulin-like growth factor-I, oxytocin and progesterone by cultured human granulosa cells. Experimental and Clinical Endocrinology and Diabetes, 105(2), 109–112.

Schomerus, C., Korf, H. W., Laedtke, E., Weller, J. L., Klein, D. C. (2000). Selective Adrenergic/Cyclic AMP-Dependent Switch-Off of Proteasomal Proteolysis Alone Switches on Neural Signal Transduction : An Example from the Pineal Gland. Journal of Neurochemistry, 75(2), 2123–2132.

Simonneaux, V. & Ribelayga, C. (2003). Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacological Reviews, 55(2), 325-395.

Skene, D. J., Papagiannidou, E., Hashemi, E., Snelling, J., Lewis, D. F., Fernandez, M., Ionnides, C. (2001). Contribution of CYP1A2 in the hepatic metabolism of melatonin: studies with isolated microsomal preparations and liver slices. Journal of Pineal Research, 31, 333–342.

Sliwowska, J. H., Billings, H. J., Goodman, R. L., Coolen, L. M., & Lehman, M. N. (2004). The premammillary hypothalamic area of the ewe: anatomical characterization of a melatonin target a area mediating seasonal reproduction. Biology of Reproduction, 70, 1768–1775.

Smith, J. T., Li, Q., Pereira, A., Clarke, I. J. (2009). Kisspeptin neurons in the ovine arcuate nucleus and preoptic area are involved in the preovulatory luteinizing hormone surge. Endocrine Reviews, 150(12), 5530–5538.

Smith, J. T. (2012). The role of kisspeptin and gonadotropin inhibitory hormone in the seasonal regulation of reproduction in sheep. Domestic Animal Endocrinology, 43(2), 75–84.

Soares Junior, J. M. (2003). Functional melatonin receptors in rat ovaries at various stages of the estrous cycle. Journal of Pharmacology and Experimental Therapeutics, 306(2), 694–702.

Sousa, C. E. C., Cruz-Machado, S. S., Tamura, E. K. (2008). Os ritmos circadiano e a reprodução em mamíferos. Boletim do Centro de Biologia da Reprodução, 27(1-2), 15-20.

Souza, C. J. H., Campbell, B. K.; Baird, D. T. (1997). Follicular dynamics and ovarian steroid secretion in sheep during the follicular and early luteal phases of the estrous cycle. Biology of Reproduction, 56(2), 483–488.

Standaert, D. G.; Galanter, J. M. (2009). Farmacologia da Neurotransmissão Dopaminérgica. In: Golan, D. E., et al. (Ed.). Princípios de farmacologia: a base fisiopatológica da farmacoterapia. (2e ed.) (166-185). São Paulo: Guanabara Koogan S.A.

Stanisiewski, E. P., Chapin, L. T., Ames, N. K., Zinn, S. A., Tucker, H. A. (1988). Melatonin and prolactin concentrations in blood of cattle exposed to 8, 16 or 24 hours of daily light. Journal of Animal Science, 66, 727-734.

Stefanovic, I., Adrian, B., Jansen, H. T., Lehman, M. N., Goodman, R. L. (2000). The ability of estradiol to induce Fos expression in a subset of estrogen receptor-a-containing neurons in the preoptic area of the ewe depends onrReproductive status. Endocrinology, 141(1), 190–196.

Stefulj, J., Hörtner, M., Ghosh, M., Schauenstein, K.; Rinner, I., Wölfler, A., Semmler, J.; Liebmann, P. M. (2001). Gene expression of the key enzymes of melatonin synthesis in extrapineal tissues of the rat. Journal of Pineal Research, 30(4), 243-247.

Stehle, J. H., Von Gall, C., Schomerus, C., Korf, H. W. (2001). Of Rodents and Ungulates and Melatonin: Creating a Uniform Code for Darkness by Different Signaling Mechanisms. Journal of Biological Rhythms, 16, 312–325.

Stephan, F. K., Zucker, I. (1972). Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proceedings of the National Academy of Sciences of the United States, 69(6), 1583-1586.

Strada, S. J., Klein, D. C., Weller, J., Weiss, B. (1972). Effect of Norepinephrine on the Concentration of Adenosine 3′,5′-Monophosphate of Rat Pineal Gland in Organ Culture. Endocrinology, 90, 1470-147.

Sugden, D.; Ceña, V.; Klein, D. C. (1987). Hydroxyindole O-methyltransferase. Methods in Enzymology, 142, 590-596.

Tamura, H., Nakamura, Y., Korkmaz, A., Manchester, L. C., Tan, D. X., Sugino, N. Reiter, R. J. (2009). Melatonin and the ovary: physiological and pathophysiological implications. Fertility and Sterility, 92(1), 328-343.

Tamura, H. Takasaki, A., Taketani, T., Tanabe, M., Kizuka, F., Lee, L., Tamura, I., Maekawa, R., Asada, H., Yamagata, Y., Sugino, N. (2012). The role of melatonin as an antioxidant in the follicle. Journal of Ovarian Research, 5, 2-9.

Tamura, H., Takasaki, A., Taketani, T.; Tanabe, M., Kizuka, F., Lee, L., Tamura, I., Maekawa, R., Asada, H., Yamagata, Y., Sugino, N. (2013). Melatonin as a free radical scavenger in the ovarian follicle. Endocrine Journal, 60(1), 1-13.

Tan, D. X., Manchester, L. C., Terron, M. P., Flores, L. J.; Tamura, H.; Reiter, R. J. (2007). Melatonin as a naturally occurring co-substrate of quinone reductase-2, the putative MT3 melatonin membrane receptor: hypothesis and significance. Journal of Pineal Research, 43, 317–320.

Tanavde V. S., Maitra A. (2003). In vitro modulation of steroidogenesis and gene expression by melatonin: a study with porcine antral follicles. Endocrine Research, 29(4), 399–410.

Tassigny, X. A., Colledge, W. H. (2010). The role of kisspeptin signaling in reproduction. Physiology, 25(4), 207-217.

Tena-Sempere, M., Huhtaniemi, I. Gonadotropins and gonadotropin receptors. (2003). In: Fauser, B.C.J.M. (Ed.) Reproductive Medicine: Molecular, Cellular and Genetic Fundamentals. (pp.225-244). New York: Parthenon.

Thiéry, J. C., Martin, G. B. (1991). Neurophysiological control of the secretion of gonadotrophin-releasing hormone and luteinizing hormone in the sheep - a review. Reproduction, Fertility and Development, 3(3), 137–173.

Thiéry, J. C.; Gayrard, V.; Corre, S. L.; Viguié, C.; Martin, G. B.; Chemineau, P.; Malpaux, B. (1995). Dopaminergic control of LH secretion by the A15 nucleus in anoestrous ewes. Journal of reproduction and fertility. Supplement, 49, 285-96.

Thimonier, J., Terqui, M., Chemineau, P. (1986). Conduite de la reproduction des petits ruminants dans les differentes parties du monde. In: Proceedings of an International Symposium on the Use of Nuclear Techniques in Studies of Animal Production and Health in Different Environments (pp. 135-147). Vienna: International Atomic Energy Agency.

Tilbrook, A. J., Clarke, I. J. (2001). Negative feedback regulation of the secretion and actions of gonadotropin-releasing hormone in males. Biology of Reproduction, 64(3), 735-742.

Tillet, Y. (1995). Distribution of neurotransmitters in the sheep brain. Journal of Reproduction and Fertility. Supplement, 49, 199-220.

Tortonese, D. J. (1999). Interaction between hypothalamic dopaminergic and opioidergic systems in the photoperiodic regulation of pulsatile luteinizing hormone secretion in sheep. Endocrinology, 140(2), 750-757.

Tosini, G., Fukuhara, C. (2002). The mammalian retina as a clock. Cell and Tissue Research, 309, 119-126.

Vanecek, J., Sugden, D., Weller, J., Klein, D. C. (1985). Atypical Synergistic α1- and β-Adrenergic Regulation of Adenosine 3′,5′-Monophosphate and Guanosine 3′,5′- Monophosphate in Rat Pinealocytes. Endocrinology, 116, 2167-217.

Vanecek, J. (1998). Cellular mechanisms of melatonin action. Physiological Reviews, 78(3), 687-721.

Van Niekerk, F. E., Van Niekerk, C. H. (1997). The effect of dietary protein on reproduction in the mare. III. Ovarian and uterine changes during the anuvulatory season, transitional and ovulatory periods in the non-pregnant mare. Journal of South African Veterianry Association, 68(3), 86-92.

Viguié, C., Thibault, J., Thiéry, J. C., Tillet, Y.; Malpaux, B. (1997). Characterization of the short day-induced decrease in median eminence tyrosine hydroxylase activity in the ewe: temporal relationship to the changes in luteinizing hormone and prolactin secretion and short day-like effect of melatonin. Endocrinology, 138(1), 499–506.

Viguié, C., Thibault, J., Thiéry, J. C.; Tillet, Y.; Malpaux, B. (1996). Photoperiodic modulation of monoamines and amino-acids involved in the control of prolactin and LH secretion in the ewe: evidence for a regulation of tyrosine hydroxylase activity. Journal of Neuroendocrinology, 8, 465–474.

Vivien-Roels, B.; Pévet, P. (1983). The pineal gland and the synchronization of reproductive cycles with variations of the environmental climatic conditions with special reference to temperature. Pineal Research Reviews, 1, 91-143.

Walton, J. S., Mcneilly, J. R., Mcneilly, A. S.; Cunningham, F. J. (1977). Changes in concentration of follicle-stimulating hormone, luteinizing hormone, prolactin and progesterone in the plasma of ewes during the transition from anoestrus to breeding activity. Journal of Endocrinology, 75, 127–136.

Wardil, L. L. (2008). Redes em biologia: introdução às redes complexas, estudo dos aspectos estruturais e dinâmicos do ciclo celular e dos ritmos circadianos. (81 p.) Dissertação (Mestrado em Física): Universidade Federal de Minas Gerais, 2008.

Webley, G. E., Luck, M. R. (1986). Melatonin directly stimulates the secretion of progesterone by human and bovine granulosa cells in vitro. Journal of Reproduction and Fertility, 78, 711–717.

Whisnant, C. S.; Goodman, R. L. (1990). Further evidence that serotonin mediates the steroid-independent inhibition of luteinizing hormone secretion in anestrous. Biological Research, 42, 656–661.

Woo, M. M. M., Tai, C. J., Kang, S. K., Nathwani, P. S., Pang, S. F., Leung, P. C. K. (2001). Direct action of melatonin in human granulosa-luteal cells. Journal of Clinical Endocrinology and Metabolism, 86(10), 4789–4797.

Xiong, J. J., Karsch, F. J., Lehman, M. N. (1997). Evidence for seasonal plasticity in the gonadotropin-releasing hormone (GnRH) system of the ewe: changes in synaptic inputs onto neurons. Endocrinology, 138(3), 1240–1250.

Yie, S. M., Niles, L. P., Younglai, E. V. (1995). Melatonin receptors on human granulose cell membranes. Journal of Clinical Endocrinology & Metabolism, 80(5), 1747–1749.

Zarazaga, L. A., Malpaux, B., Guillaume, D., Bodin, L., Chemineau, P. (1998). Genetic variability in melatonin concentrations in ewes originates in its synthesis, not in its catabolism. American Journal of Phisiology, 274, 1086–1090.

Published

02/10/2020

How to Cite

DIAS, J. C. O.; VELOSO, C. M. Seasonality in mammalian reproduction: a review. Research, Society and Development, [S. l.], v. 9, n. 10, p. e4249108236, 2020. DOI: 10.33448/rsd-v9i10.8236. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/8236. Acesso em: 20 apr. 2024.

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Review Article