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Developmental and molecular responses of buffalo (Bubalus bubalis) cumulus–oocyte complex matured in vitro under heat shock conditions

Published online by Cambridge University Press:  22 May 2018

Ashraf El-Sayed*
Affiliation:
Cairo University Research Park (CURP), Faculty of Agriculture, Cairo University, 12613 Giza, Egypt. Department of Animal Production, Faculty of Agriculture, Cairo University, 12613 Giza, Egypt.
Rehab Nagy
Affiliation:
Buffalo Breeding Research Department, Animal Production Research Institute, Dokki, Giza, Egypt.
Amal K. El-Asheeri
Affiliation:
Department of Animal Production, Faculty of Agriculture, Cairo University, 12613 Giza, Egypt.
Liala N. Eid
Affiliation:
Buffalo Breeding Research Department, Animal Production Research Institute, Dokki, Giza, Egypt.
*
All correspondence to: Ashraf El-Sayed. Cairo University Research Park (CURP), Faculty of Agriculture, Cairo University, 12613 Giza, Egypt. E-mail: [email protected]

Summary

To investigate the effects of physiologically relevant heat shock during oocyte maturation, buffalo cumulus–oocyte complexes (COCs) were cultured at 38.5°C (control) or were exposed to 39.5°C (T1) or 40.5°C (T2) for the first 6 h of in vitro maturation (IVM), followed by 38.5°C through the next 18 h/IVM and early embryonic development up to the blastocyst stage. Gene expression analysis was performed on selected target genes (HSF-1, HSF-2, HSP-70, HSP-90, BAX, p53, SOD1, COX1, MAPK14) in denuded oocytes and their isolated cumulus cells resulting from control COCs as well as from COCs exposed to a temperature of 39.5°C (T1). The results indicated that heat shock significantly (P < 0.01) decreased the maturation rate in T1 and T2 cells compared with the control. After in vitro fertilization (IVF), cleavage rate was lower (P < 0.01) for oocytes exposed to heat stress, and the percentage of oocytes arrested at the 2- or 4-cell stage was higher (P < 0.01) than that of the control. The percentage of oocytes that developed to the 8-cell, 16-cell or blastocyst stage was lower (P < 0.01) in both T1 and T2 groups compared with the control group. mRNA expression levels for the studied genes were decreased (P < 0.05) in treated oocytes (T1) except for HSP-90 and HSF-1, which were increased. In cumulus cells isolated from COCs (T1), the expression for the target genes was upregulated except for BAX, which was downregulated. The results of this study demonstrated that exposure of buffalo oocytes to elevated temperatures for 6 h severely compromised their developmental competence and gene expression.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Abdoon, A.S., Gabler, C., Holder, C., Kandil, O.M. & Einspanier, R. (2014). Seasonal variations in developmental competence and relative abundance of gene transcripts in buffalo (Bubalus bubalis) oocytes. Theriogenology 82, 1055–67.CrossRefGoogle ScholarPubMed
Abou-Bakr, S. (2008). Estimation of breeding values of total milk yield of Egyptian buffalo under different production systems (PhD thesis, Cairo University).Google Scholar
Aggarwal, A. & Upadhyay, R.C. (1998). Studies on evaporative heat losses from skin and pulmonary surfaces in male buffaloes exposed to solar radiations. Buffalo J. 2, 179–87.Google Scholar
Akerfelt, M., Morimoto, R.I. & Sistonen, L. (2010). Heat shock factors: Integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell. Biol. 11, 545–55.Google Scholar
Ali, A., Abdel-Razek, A.Kh., Derar, R., Abdel-Rheem, H.A. & Shehata, S.H. (2009). Forms of reproductive disorders in cattle and buffaloes in Middle Egypt. Reprod. Domest. Anim. 44, 580–6.Google Scholar
Ali, A., Bharadwaj, S., O'Carroll, R. & Ovsenek, N. (1998). HSP90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes. Mol. Cell. Biol. 18, 4949–60.CrossRefGoogle ScholarPubMed
Al-Katanani, Y.M., Paula-Lopes, F.F. & Hansen, P.J. (2002). Effect of season and exposure to heat stress on oocyte competence in Holstein cows. J. Dairy. Sci. 8, 390–6.CrossRefGoogle Scholar
Archana, P.R., Aleena, J., Pragana, P., Vidya, M.K., Abdul Niyas, P.A., Bagath, M., Krishnan, G., Manimaran, A., Beena, V., Kurien, E.K., Sejian, V. & Bahtta, R. (2017). Role of heat shock proteins in livestock adaptation to heat stress. J. Dairy Vet. Anim. Res. 5, 00127.Google Scholar
Ashraf, S., Shah, S.M., Saini, N., Dhanda, S., Singh, M.K. & Chauhan, M.S. (2014). Developmental competence and expression pattern of bubaline (Bubalus bubalis) oocytes subjected to elevated temperatures during meiotic maturation in vitro. J. Assist. Reprod. Genet. 31, 1349–60.Google Scholar
Ashraf, S., Raies-ul-Haq, M., Dhanda, S., Kumar, A., Sridhar, G.T., Chauhan, M.S. & Upadhyay, R.C. (2016). Heat stress and antioxidant enzyme activity in bubaline (Bubalus bubalis) oocytes during in vitro maturation. Int. J. Biometeorol. 60, 1357–66.Google Scholar
Atlante, A., Calissano, P. & Bobba, A. (2000). Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ros scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J. Biol. Chem. 275, 37159–66.Google Scholar
Badinga, L., Thatcher, W.W., Diaz, T., Drost, M. & Wolfenson, D. (1993). Effect of environmental heat stress on follicular development and steriodogenesis in lactating Holstein cows. Theriogenology 39, 797810.CrossRefGoogle Scholar
Beckham, J.T., Mackanos, M.A., Crooke, C., Takahashi, T., O'Connell Rodwell, C. & Contag, C.H. (2004). Assessment of cellular response to thermal laser injury through bioluminescence imaging of heat shock protein 70. Photochem. Photobiol. 79, 7685.CrossRefGoogle ScholarPubMed
Belhadj Slimen, I., Najar, T., Ghram, A. & Abdrrabba, M. (2016). Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J. Anim. Physiol. Anim. Nutr. 100, 401–12.CrossRefGoogle ScholarPubMed
Biamonti, G. & Caceres, J.F. (2009). Cellular stress and RNA splicing. Trends Biochem. Sci. 34, 146–53.CrossRefGoogle ScholarPubMed
Bilodeau, J.F., Chatterjee, S., Sirard, M.A. & Gagnon, C. (1999). Levels of antioxidant defenses are decreased in bovine spermatozoa after a cycle of freezing and thawing. Mol. Reprod. Dev. 55, 282–8.Google Scholar
Bulman, A.L. & Nelson, H.C. (2005). Role of trehalose and heat in the structure of the C-terminal activation domain of the heat shock transcription factor. Proteins 58, 826–35.CrossRefGoogle ScholarPubMed
Cánepa, M.J., Ortega, N.M., Monteleone, M.C., Mucci, N., Kaiser, G.G., Brocco, M. & Mutto, A. (2014). Expression profile of genes as indicators of developmental competence and quality of in vitro fertilization and somatic cell nuclear transfer bovine embryos. PLoS One 9, e108139.CrossRefGoogle ScholarPubMed
Cavestany, D., El-Whishy, A.B. & Foot, R.H. (1985). Effect of season and high environmental temperature on fertility of Holstein cattle. J. Dairy Sci. 68, 1471–8.CrossRefGoogle ScholarPubMed
Cowan, K.J. & Storey, K.B. (2003). Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress. J. Exp. Biol. 206, 1107–15.CrossRefGoogle ScholarPubMed
Dangi, S.S., Gupta, M., Nagar, V., Yadav, V.P., Dangi, S.K., Shankar, O., Chouhan, V.S., Kumar, P., Singh, G. & Sarkar, M. (2014). Impact of short-term heat stress on physiological responses and expression profile of HSPs in Barbari goats. Int. J. Biometeorol. 58, 2085–93.Google Scholar
Das, S.K., Upadhyay, R.C. & Madan, M.L. (1999). Heat stress in Murrah buffalo calves. Livest. Prod. Sci. 61, 71–8.CrossRefGoogle Scholar
De Castro e Paula, L.A. & Hansen, P.J. (2008). Modification of actions of heat shock on development and apoptosis of cultured preimplantation bovine embryos by oxygen concentration and dithiothreitol. Mol. Reprod. Dev. 75, 1338–50.Google Scholar
Deb, R., Sajjanar, B., Singh, U., Kumar, S., Singh, R., Sengar, G. & Sharma, A. (2014). Effect of heat stress on the expression profile of Hsp90 among Sahiwal (Bos indicus) and Frieswal (Bos indicus × Bos taurus) breed of cattle: a comparative study. Gene 536, 435–40.CrossRefGoogle ScholarPubMed
Ealy, A.D., Howell, J.L., Monterroso, V.H., Arechiga, C.F. & Hansen, P.J. (1995). Developmental changes in sensitivity of bovine embryos to heat shock and use of antioxidants as thermoprotectants. J. Anim. Sci. 73, 1401–7.Google Scholar
Edwards, J.L. & Hansen, P.J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol. Reprod. Dev. 46, 138–45.Google Scholar
Edwards, J.L., Saxton, A.M., Lawrence, J.L., Payton, R.R. & Dunlap, J.R. (2005). Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. J. Dairy Sci. 88, 4326–33.Google Scholar
El-Sayed, A., Ashour, G., Khalifa, M. & Gad, A. (2015). Vitrification assessment of buffalo (Bubalus bubalis) oocytes: morphological and molecular aspects. Egyptian. J. Anim. Prod. 52 (Suppl.), 17.Google Scholar
Fissore, R.A., Kurokawa, M., Knott, J., Zhang, M. & Smyth, J. (2002). Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–54.CrossRefGoogle ScholarPubMed
Funahashi, H. & Day, B.N. (1995). Effects of cumulus cells on glutathione content of porcine oocyte during in vitro maturation. J. Anim. Sci. 73 (Suppl. 1), 90 (abstract).Google Scholar
Fu, Y., He, C.J., Ji, P.Y., Zhuo, Z.Y., Tian, X. Z., Wang, F. & Liu, G.S. (2014). Effects of melatonin on the proliferation and apoptosis of sheep granulosa cells under thermal stress. Int. J. Mol. Sci. 15, 21090–104.CrossRefGoogle ScholarPubMed
Gardiner, C.S., Salmen, J.J. & Brandt, C.J. (1998). Glutathione is present in reproductive tract Secretions and improves development of mouse embryos after chemically-induced glutathione depletion. Biol. Reprod. 59, 431–6.Google Scholar
Garrido, C., Gurbuxani, S., Ravagnan, L. & Kroemer, G. (2001). Heat shock proteins: Endogenous modulators of apoptotic cell death. Biochem. Biophys. Res. Commun. 286, 433–42.Google Scholar
Ghanem, N. & El-Sayed, A. (2012). Expression of selected candidate genes during in vitro oocyte maturation and early embryonic development on in vitro generated Egyptian buffalo (Bubalus bubalis) embryos. Egyptian J. Anim. Prod. 49 (Suppl.), 1928.Google Scholar
Gwazdauskas, F.C., Thatcher, W.W. & Wilcox, C.J. (1973). Physiological, environmental, and hormonal factors at insemination which may affect conception. J. Dairy Sci. 56, 873–7.Google Scholar
Hansen, P.J. (2013). Cellular and molecular bas is of therapies to ameliorate effects of heat stress on embryonic development in cattle. Anim. Reprod. 10, 322–33.Google Scholar
Hu, H., Wang, J., Gao, H., Li, S., Zhang, Y. & Zheng, N. (2015). Heat induced apoptosis and gene expression in bovine mammary epithelial cells. Anim. Prod. Sci. 56, 918–26.CrossRefGoogle Scholar
Ibrahim, M.A.R. (2012). Water buffalo for our next generation in Egypt and in the world. Scientific Papers Anim. Sci. LV, 183–92.Google Scholar
Jia, Y., Sinha Hikim, A.P., Swerdloff, R.S., Lue, Y.H., Vera, Y., Zhang, X.S., Hu, Z.Y., Li, Y.C., Liu, Y.X. & Wang, C. (2007). Signaling pathways for germ cell death in adult cynomolgus monkeys (Macaca fascicularis) induced by mild testicular hyperthermia and exogenous testosterone treatment. Biol. Reprod. 77, 8392.Google Scholar
Johnson, C., Jia, Y., Wang, C., Lue, Y., Swerdloff, R.S., Zhang, X., Hu, Z., Li, Y., Liu, Y. & Sinha Hikim, A.P. (2008). Role of caspase 2 in apoptotic signaling in primate and murine germ cells. Biol. Reprod. 79, 806–14.Google Scholar
Jolly, C., Vourc'h, C., Robert-Nicoud, M. & Morimoto, R.I. (1999). Intron-independent association of splicing factors with active genes. J. Cell. Biol. 145, 1133–43.Google Scholar
Jousan, F.D. & Hansen, P.J. (2007). Insulin-like growth factor promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling. Mol. Reprod. Dev. 74, 189–96.Google Scholar
Jousan, F.D. & Hansen, P.J. (2004). Insulin-like growth factor-I as a survival factor for the bovine preimplantation embryo exposed to heat shock. Biol. Reprod. 71, 1665–70.Google Scholar
Ju, J.C., Jiang, S., Tseng, J.K., Parks, J.E. & Yang, X. (2005). Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes. Theriogenology 64, 1677–89.CrossRefGoogle ScholarPubMed
Kapila, N., Kishore, A., Sodhi, M., Sharma, A., Mohanty, A.K., Kumar, P. & Mukesh, M. (2013). Temporal changes in mRNA expression of heat shock protein genes in mammary epithelial cells of riverine buffalo in response to heat stress in vitro. Int. J. Anim. Biotech. 3, 59.Google Scholar
Khairy, M.A., Zoheir, Abdoon A.S., Mahrous, K.F., Amer, M.A., Zaher, M.M., Li-Guo, Y. & El-Nahass, E.M. (2007). Effects of season on the quality and in vitro maturation rate of Egyptian buffalo (Bubalus bubalis) oocytes. J. Cell. Anim. Biol. 1, 2933.Google Scholar
Kimura, N., Tsunoda, S., Iuchi, Y., Abe, H., Totsukawa, K. & Fujii, J. (2010). Intrinsic oxidative stress causes either 2-cell arrest or cell death depending on developmental stage of the embryos from SOD1-deficient mice. Mol. Hum. Reprod. 16, 441–51.Google Scholar
Kishore, A., Sodhi, M., Kumari, P., Mohanty, A.K., Sadana, D.K., Kapila, N., Khate, K., Shandilya, U., Kataria, R.S. & Mukesh, M. (2014). Peripheral blood mononuclear cells: a potential cellular system to understand differential heat shock response across native cattle (Bos indicus), exotic cattle (Bos taurus), and riverine buffaloes (Bubalus bubalis) of India. Cell Stress Chaperones 19, 613–21.Google Scholar
LaRosa, C. & Downs, S.M. (2006). Meiotic induction by heat stress in mouse oocytes: involvement of AMP-activated protein kinase and MAPK family members. Biol. Reprod. 76, 476–86.CrossRefGoogle ScholarPubMed
Le Masson, F. & Christians, E. (2011). HSFs and regulation of Hsp70.1 (Hspa1b) in oocytes and preimplantation embryos: New insights brought by transgenic and knockout mouse models. Cell Stress Chaperones 16, 275–85.Google Scholar
Lenz, R.W., Ball, G.D., Leibfried, M.L., Ax, R.L. & First, N.L. (1983). In vitro maturation and fertilization of bovine oocytes are temperature-dependent processes. Biol. Reprod. 29, 173–9.Google Scholar
Li, L., Wu, J., Luo, M., Sun, Y. & Wang, G. (2016). The effect of heat stress on gene expression, synthesis of steroids, and apoptosis in bovine granulosa cells. Cell Stress Chaperones 21, 467–75.Google Scholar
Li, Q.L., Ju, Z.H., Huang, J.M., Li, J.B., Li, R.L. & Hou, M.H. (2011). Two novel SNPs in HSF1 gene are associated with thermal tolerance traits in Chinese Holstein cattle. DNA Cell. Biol. 30, 247–54.Google Scholar
Liu, Z., Fan, H., Wang, Y. & Richards, J.S. (2010). Targeted disruption of Mapk14 (p38MAPKα) in granulosa cells and cumulus cells causes cell-specific changes in gene expression profiles that rescue COC expansion and maintain fertility. Mol. Endocrinol. 24, 1794–804.CrossRefGoogle ScholarPubMed
Li, Y., Zhang, Z., He, C., Zhu, K., Xu, Z., Ma, T. & Liu, G. (2015). Melatonin protects porcine oocyte in vitro maturation from heat stress. J. Pineal. Res. 59, 365–75.CrossRefGoogle ScholarPubMed
Lockshin, R.A. & Zakeri, Z. (2007). Cell death in health and disease. J. Cell. Mol. Med. 11, 1214–24.Google Scholar
Manjari, R., Yadav, M., Ramesh, K., Uniyal, S., Rastogi, S.K., Sejian, V. & Hyder, I. (2015). HSP70 as a marker of heat and humidity stress in tarai buffalo. Trop. Anim. Health Prod. 47, 111–6.CrossRefGoogle ScholarPubMed
Marai, I.F. & Haeeb, A.A. (2010). Buffalo's biological functions as affected by heat stress a review. Livest. Sci. 127, 89109.Google Scholar
Mathew, A. & Morimoto, R.I. (1998). Role of the heat-shock response in the life and death of proteins. Ann. N. Y. Acad. Sci. 851, 99111.CrossRefGoogle ScholarPubMed
Maya-Soriano, M.J., López-Gatius, F., Andreu-Vázquez, C. & López-Béjar, M. (2013). Bovine oocytes show a higher tolerance to heat shock in the warm compared with the cold season of the year. Theriogenology 79, 299305.Google Scholar
Mishra, S.R. & Palai, T.K. (2014). Importance of heat shock protein 70 in livestock - at cellular level. J. Mol. Pathophysiol. 3, 30–2.Google Scholar
Mishra, V., Misra, A.K. & Sharma, R. (2007). Effect of ambient temperature on in vitro fertilization of bubaline oocyte. Anim. Reprod. Sci. 100, 379–84.CrossRefGoogle ScholarPubMed
Nabenishi, H., Takagi, S., Kamata, H., Nishimoto, T., Morita, T., Ashizawa, K. & Tsuzuki, Y. (2012). The role of mitochondrial transition pores on bovine oocyte competence after heat stress, as determined by effects of cyclosporin A. Mol. Reprod. Dev. 79, 3140.Google Scholar
Nadeau, K., Das, A. & Walsh, C.T. (1993). Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem. 268, 1479–87.Google Scholar
Nandi, S., Chauhan, M.S. & Palta, P. (2001). Effect of environmental temperature on quality and developmental competence in vitro of buffalo. Vet. Record. 48, 278–9.Google Scholar
Nasr-Esfahani, M.H., Aitken, R.J. & Johnson, M.H. (1990). Hydrogen peroxide levels in mouse oocytes And early cleavage stage embryos developed in vitro or in vivo. Development 109, 501–7.CrossRefGoogle ScholarPubMed
Noda, Y., Matsumot, O.H. & Umaoka, Y. (1991). Involvement of superoxide radicals in the mouse 2-cell block. Mol. Reprod. Dev. 28, 356–60.Google Scholar
Nolan, Y., Verker, E., Lynch, A.M. & Lynch, M.A. (2003). Evidence that lipopolysaccharide-induced cell death is mediated by accumulation of reactive oxygen species and activation of p38 in rat cortex and hippocampus. Exp. Neurol. 184, 794804.Google Scholar
Ostling, P., Bjork, J.K., Roos-Mattjus, P., Mezger, V. & Sistonen, L. (2007). Heat shock factor 2 (HSF2) contributes to inducible expression of hsp genes through interplay with HSF1. J. Biol. Chem. 282, 7077–86.Google Scholar
Paula-Lopes, F.F. & Hansen, P.J. (2002). Apoptosis is an adaptive response in bovine pre-implantation embryos that facilitates survival after heat shock. Biochem. Biophys. Res. Commun. 95, 3742.Google Scholar
Paula-Lopes, F.F., Milazzotto, M., Assumpcao, M.E.O.A. & Visintin, J.A. (2008). Heat shock-induced damage in bovine oocytes. Reprod. Fertil. Dev. 43, 208.Google Scholar
Paula-Lopes, F.F., Lima, R.S., Risolia, P.H., Ispada, J., Assumpção, M.E. & Visintin, J.A. (2012). Heat stress induced alteration in bovine oocytes: functional and cellular aspects. Anim. Reprod. 9, 395403.Google Scholar
Pavani, K.C., Baron, E., Correia, P., Lourenço, J. & Bettencourt, B.F. (2016). Gene expression, oocyte nuclear maturation and developmental competence of bovine oocytes and embryos produced after in vivo and in vitro heat shock. Zygote 28, 112.Google Scholar
Payton, R.R., Lawrence, J.L., Saxton, A.M., Dunlap, J.R. & Edwards, J.L. (2003). Cortical granule types and nuclear stage of bovine oocytes after exposure to elevated temperature during maturation. Theriogenology 59, 496.Google Scholar
Payton, R.R., Romar, R., Coy, P., Saxton, A.M., Lawrence, J.L. & Edwards, J.L. (2004). Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biol. Reprod. 71, 1303–8.Google Scholar
Payton, R.R., Rispoli, L.A., Saxton, A.M. & Edwards, J.L. (2011). Impact of heat stress exposure during meiotic maturation on oocyte, surrounding cumulus cell, and embryo RNA populations. J. Reprod. Dev. 57, 481–91.Google Scholar
Prochazka, R., Blaha, M. & Nemcova, L. (2012). Signaling pathways regulating FSH- and amphiregulin-induced meiotic resumption and cumulus cell expansion in the pig. Reproduction. 144, 535–46.Google Scholar
Rahman, M.B., Vandaele, L., Rijsselaere, T., Maes, D., Shamsuddin, M., & Van Soom, A. (2012). Role of mitogen-activated protein kinase (MAPK) 14-signalling pathway in bovine spermatozoa exposed to heat stress in vitro. Reprod. Domest. Anim. 47, 71.Google Scholar
Rispoli, L.A., Lawrence, J.L., Payton, R.R., Saxton, M.A., Schrock, G.E. & Schrick, F.N. (2011). Disparate consequences of heat stress exposure during meiotic maturation: embryo development after chemical activation vs fertilization of bovine oocytes. Reproduction 142, 832–43.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2004). Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71, 1898–906.CrossRefGoogle ScholarPubMed
Roth, Z. & Hansen, P.J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–44.CrossRefGoogle ScholarPubMed
Roth, Z., Arav, A., Bor, A., Zeron, Y., Braw-Tal, R. & Wolfenson, D. (2001). Improvement of quality of oocytes collected in the autumn by enhanced removal of impaired follicles from previously heat-stressed cows. Reproduction 122, 737–44.Google Scholar
Rutledge, R.L., Monson, D.L., Northey, A. & Leibfried-Rutledge, M.I. (1999). Seasonality of cattle embryo production in a temperate region. Theriogenology 51, 330.Google Scholar
Sadeesh, E.M., Sikka, P., Balhara, A.K. & Balhara, S. (2016). Developmental competence and expression profile of genes in buffalo (Bubalus bubalis) oocytes and embryos collected under different environmental stress. Cytotechnology 68, 2271–85.Google Scholar
Sakatani, M., Kobayashi, S. & Takahashi, M. (2004). Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos. Mol. Reprod. Dev. 67, 7782.Google Scholar
Sakatani, M., Yamanaka, K., Kobayashi, S. & Takahashi, M. (2008). Heat shock-derived reactive oxygen species induce embryonic mortality in in vitro early stage bovine embryos. J. Reprod. Dev. 54, 496501.CrossRefGoogle ScholarPubMed
Salces-Ortiz, J., Gonzalez, C., Moreno-Sanchez, N., Calvo, J.H., Perez-Guzman, M.D. & Serrano, M.M. (2013). Ovine HSP90AA1 expression rate is affected by several SNPs at the promoter under both basal and heat stress conditions. PLoS One 8, e66641.Google Scholar
Sethi, R.K., Bharadwaj, A. & Chopra, S.C. (1994). Effect of heat stress on buffaloes under different shelter strategies. Indian J. Anim. Sci. 64, 1282–5.Google Scholar
Sharma, G., Nath, A., Prasad, S., Singhal, S., Singh, N., Gade, N., Dubey, P. & Saikumar, G. (2012). Expression and characterization of constitutive heat shock protein 70.1 (HSPA-1A) gene in in vitro produced and in vivo-derived buffalo (Bubalus bubalis) embryos. Reprod. Domest. Anim. 47, 975–83.Google Scholar
Shen, P.C., Lee, J.W., Cheng, W.T., Su, H.Y., Lee, S.N. & Liu, B.T. (2010). Differential thermal sensitivity between the recipient ooplasm and the donor nucleus in Holstein and Taiwan native yellow cattle. Theriogenology 74, 1587–95.Google Scholar
Stankiewicz, A.R., Lachapelle, G., Foo, C.P., Radicioni, S.M. & Mosser, D.D. (2005). Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J. Biol. Chem. 280, 38729–3.Google Scholar
Tang, S., Chen, H., Cheng, Y., Nasir, M.A., Kemper, N. & Bao, E. (2016). The interactive association between heat shock factor 1 and heat shock proteins in primary myocardial cells subjected to heat stress. Int. J. Mol. Med. 37, 5662.Google Scholar
Taqi, M.O. (2012). Milk productivity and physiological parameters of Egyptian buffalo under climatic conditions of Giza and Qena governments. Master's thesis, Cairo University.Google Scholar
Tseng, J.K., Chen, C.H., Chou, P.C., Yeh, S.P. & Ju, J.C. (2004). Influences of follicular size on parthenogenetic activation and in vitro heat shock on the cytoskeleton in cattle oocytes. Reprod. Domest. Anim. 39, 146–53.Google Scholar
Tsunoda, S., Kimura, N. & Fujii, J. (2014). Oxidative stress and redox regulation of gametogenesis, fertilization, and embryonic development. Reprod. Med. Biol. 13, 71–9.Google Scholar
Wang, Z.B., Li, M., Zhao, Y. & Xu, J.X. (2003). Cytochrome c is a hydrogen peroxide scavenger in mitochondria. Protein Pept. Lett. 10, 247–53.Google Scholar
Xiao, X., Zuo, X., Davis, A.A., McMillan, D.R., Curry, B.B. & Richardson, J.A. (1999). HSF1 is required for extra-embryonic development, postnatal growth and protection during in flammatory response in mice. EMBO J. 18, 5943–52.Google Scholar
Yadav, A., Singh, K.P., Singh, M.K., Saini, N., Palta, P., RS Manik, R.S., SK Singla, S.K., Upadhyayand, R.C. & Chauhan, M.S. (2013). Effect of physiologically relevant heat shock on development, apoptosis and expression of some genes in buffalo (Bubalus bubalis) embryos produced in vitro. Reprod. Domest. Anim. 48, 858–65.CrossRefGoogle ScholarPubMed
Zeron, Y.A., Ocheretny, O., Kedar, A., Borochov, D. & Skla Arav, A. (2001). Seasonal changes in bovine fertility: Relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121, 447–54.Google Scholar
Zoheir, K.M.A., Abdoon, A.S., Mahrous, K.F., Amer, M.A., Zaher, M.M. & Li Guo, Y. (2007). Effects of season on the quality and in vitro maturation rate of Egyptian buffalo (Bubalus bubalis) oocytes. J. Cell. Anim. Biol. 1, 2933.Google Scholar
Zuelke, K.A. & Perreault, S.D (1994). Hamster oocyte and cumulus cell glutathione concentrations increase rapidly during in vivo meiotic maturation. Biol. Reprod. 50 (Suppl. 1), 144 (abstract).Google Scholar