Abstract
Heat stress can potentially affect most aspects of reproduction in mammals. To our knowledge, no studies have ever been conducted for evaluating the influences of hot season on the developmental competence of ewe oocytes. In the present study, for the first time, we evaluated the effects of season (winter or summer), in vitro thermal stress, and their interaction on the ewe oocytes harvested from slaughterhouse ovaries. Cumulus-oocyte complexes (COCs) were either incubated at 39 °C for the entire length of IVM period or first incubated at 41 °C for 12 h and then at 39 °C. Evaluated endpoints included the ratios of total aspirated COCs/ovary and good-quality COCs/ovary, the apoptosis (Annexin V staining) and nuclear maturation of oocytes after 24-h IVM, and the developmental competence of oocytes after IVF. Our results showed that the number of aspirated oocytes per ovary was similar in both seasons, but the winter ovaries yielded significantly more oocytes with acceptable morphology in winter than in summer (2.1 ± 0.14 vs. 1.5 ± 0.09, P < 0.05). There was a significant interaction between season and thermal stress on the apoptosis, some nuclear maturation parameters, and blastocyst development of oocytes (P < 0.05). Although the winter oocytes were more developmentally competent than the summer oocytes, the winter oocytes were more sensitive to the thermal stress than summer oocytes. In conclusion, the developmental competence of ovine oocytes was lower in summer than in winter. However, it seemed that summer oocytes were more resistant to the in vitro thermal stress during IVM period compared with winter oocytes.
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References
Abdoon, A.S., Gabler, C., Holder, C., Kandil, O.M. and Einspanier, R., 2014. Seasonal variations in developmental competence and relative abundance of gene transcripts in buffalo (Bubalus bubalis) oocytes, Theriogenology, 82, 1055–1067
Al-Katanani, Y.M., Paula-Lopes, F.F. and Hansen, P.J., 2002. Effect of season and exposure to heat stress on oocyte competence in Holstein cows, J Dairy Sci, 85, 390–396
Beere, H.M. and Green, D.R., 2001. Stress management - heat shock protein-70 and the regulation of apoptosis, Trends in cell biology, 11, 6–10
Bell, A.W., McBride, B.W., Slepetis, R., Early, R.J. and Currie, W.B., 1989. Chronic Heat Stress and Prenatal Development in Sheep: I. Conceptus Growth and Maternal Plasma Hormones and Metabolites, Journal of Animal Science, 67, 3289–3299
Bertoldo, M., Holyoake, P.K., Evans, G. and Grupen, C.G., 2010. Oocyte developmental competence is reduced in sows during the seasonal infertility period, Reprod Fertil Dev, 22, 1222–1229
Casu, S., Cappai, P. and Naitana, S., 1990. Effects of high temperatures on reproduction in small ruminants In: B. Ronchi, A. Nardone and J.G. Boyazoglu (eds), International Symposium on Animal Husbandry in Warm Climates, 1990, (EAAP Publication, Viterbo, Italy), 103–111
de S. Torres-Júnior, J.R., de F.A. Pires, M., de Sá, W.F., de M. Ferreira, A., Viana, J.H., Camargo, L.S., Ramos, A.A., Folhadella, I.M., Polisseni, J., de Freitas, C., Clemente, C.A., de Sá Filho, M.F., Paula-Lopes, F.F., Baruselli, P.S., 2008. Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle, Theriogenology, 69, 155–166
Di Francesco, S., Boccia, L., Campanile, G., Di Palo, R., Vecchio, D., Neglia, G., Zicarelli, L. and Gasparrini, B., 2011. The effect of season on oocyte quality and developmental competence in Italian Mediterranean buffaloes (Bubalus bubalis), Animal Reproduction Science, 123, 48–53
Dutt, R.H., 1964. Detrimental effects of high ambient temperature on fertility and early embryo survival in sheep, Int J Biometeorol, 8, 47–56
Gendelman, M. and Roth, Z., 2012. Seasonal Effect on Germinal Vesicle-Stage Bovine Oocytes Is Further Expressed by Alterations in Transcript Levels in the Developing Embryos Associated with Reduced Developmental Competence, Biology of Reproduction, 86, 1–9
Hansen, P.J., 2009. Effects of heat stress on mammalian reproduction, Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 364, 3341–3350
Hill, T.G. and Alliston, C.W., 1981. Effects of thermal stress on plasma concentrations of luteinizing hormone, progesterone, prolactin and testosterone in the cycling ewe, Theriogenology, 15, 201–209
Kalo, D. and Roth, Z., 2011. Involvement of the sphingolipid ceramide in heat-shock-induced apoptosis of bovine oocytes, Reprod Fertil Dev, 23, 876–888
Kleemann, D.O. and Walker, S.K., 2005. Fertility in South Australian commercial Merino flocks: relationships between reproductive traits and environmental cues, Theriogenology, 63, 2416–2433
Marai, I.F.M., El-Darawany, A.A., Fadiel, A. and Abdel-Hafez, M.A.M., 2007. Physiological traits as affected by heat stress in sheep—A review, Small Ruminant Research, 71, 1–12
Maya-Soriano, M.J., Lopez-Gatius, F., Andreu-Vazquez, C. and Lopez-Bejar, M., 2013. Bovine oocytes show a higher tolerance to heat shock in the warm compared with the cold season of the year, Theriogenology, 79, 299–305
Mosser, D.D., Caron, A.W., Bourget, L., Denis-Larose, C. and Massie, B., 1997. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis, Molecular and cellular biology, 17, 5317–5327
Naqvi, S.M.K., Maurya, V.P., Gulyani, R., Joshi, A. and Mittal, J.P., 2004. The effect of thermal stress on superovulatory response and embryo production in Bharat Merino ewes, Small Ruminant Research, 55, 57–63
Paes, V.M., Vieira, L.A., Correia, H.H.V., Sa, N.A.R., Moura, A.A.A., Sales, A.D., Rodrigues, A.P.R., Magalhaes-Padilha, D.M., Santos, F.W., Apgar, G.A., Campello, C.C., Camargo, L.S.A. and Figueiredo, J.R., 2016. Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus-oocyte complex, Theriogenology, 86, 994–1003
Paula-Lopes, F.F. and Hansen, P.J., 2002. Heat shock-induced apoptosis in preimplantation bovine embryos is a developmentally regulated phenomenon, Biology of Reproduction, 66, 1169–1177
Pribenszky, C., Vajta, G., Molnar, M., Du, Y., Lin, L., Bolund, L. and Yovich, J., 2010. Stress for stress tolerance? A fundamentally new approach in mammalian embryology, Biology of Reproduction, 83, 690–697
Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C. and Pounds, J.A., 2003. Fingerprints of global warming on wild animals and plants, Nature, 421, 57–60
Roth, Z., 2017. Effect of Heat Stress on Reproduction in Dairy Cows: Insights into the Cellular and Molecular Responses of the Oocyte, Annu Rev Anim Biosci, 5, 151–170
Roth, Z. and Hansen, P.J., 2004a. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation, Biology of Reproduction, 71, 1898–1906
Roth, Z. and Hansen, P.J., 2004b. Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation, Biology of Reproduction, 71, 2072–2078
Roth, Z., Meidan, R., Braw-Tal, R. and Wolfenson, D., 2000. Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows, J. Reprod. Fertil., 120, 83–90
Roth, Z., Meidan, R., Shaham-Albalancy, A., Braw-Tal, R. and Wolfenson, D., 2001. Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles, Reproduction, 121, 745–751
Roth, Z., Bor, A., Braw-Tal, R. and Wolfenson, D., 2004. Carry-over effect of summer thermal stress on characteristics of the preovulatory follicle of lactating cows, Journal of Thermal Biology, 29, 681–685
Sawyer, G., 1979. The influence of radiant heat load on reproduction in the Merino ewe. II. The relative effects of heating before and after insemination, Australian Journal of Agricultural Research, 30, 1143–1149
Shirazi, A., Shams-Esfandabadi, N., Ahmadi, E. and Heidari, B., 2010. Effects of growth hormone on nuclear maturation of ovine oocytes and subsequent embryo development, Reproduction in Domestic Animals, 45, 530–536
Shokrollahi, E., Barati, F. and Gooraninejad, S., 2014. Efficacy of Histoprep gradient for isolating ovine epididymal sperm, Small Ruminant Research, 119, 96–99
Takuma, T., Sakai, S., Ezoe, D., Ichimaru, H., Jinnouchi, T., Kaedei, Y., Nagai, T. and Otoi, T., 2010. Effects of season and reproductive phase on the quality, quantity and developmental competence of oocytes aspirated from Japanese black cows, J. Reprod. Dev., 56, 55–59
Trout, J.P., McDowell, L.R. and Hansen, P.J., 1998. Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress, J Dairy Sci, 81, 1244–1250
Tseng, J.K., Tang, P.C. and Ju, J.C., 2006. In vitro thermal stress induces apoptosis and reduces development of porcine parthenotes, Theriogenology, 66, 1073–1082
Zeron, Y., Ocheretny, A., Kedar, O., Borochov, A., Sklan, D. and Arav, A., 2001. Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles, Reproduction, 121, 447–454
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The authors would like to thank the Research Institute of Animal Embryo technology (Shahrekord University, Shahrekord, Iran) for technical and financial supports.
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Ahmadi, E., Nazari, H. & Hossini-Fahraji, H. Low developmental competence and high tolerance to thermal stress of ovine oocytes in the warm compared with the cold season. Trop Anim Health Prod 51, 1611–1618 (2019). https://doi.org/10.1007/s11250-019-01854-w
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DOI: https://doi.org/10.1007/s11250-019-01854-w