Abstract
In vitro environments like heat stress usually increase the production of reactive oxygen species in bubaline oocytes which have been implicated as one of the major causes for reduced developmental competence. Oocytes during meiotic maturation are sensitive to oxidative stress, and heat stress accelerates cellular metabolism, resulting in the higher production of free radicals. Therefore, the aim of present work was to assess the impact of heat stress during meiotic maturation on bubaline cumulus–oocyte complexes (COC), denuded oocytes (DO), and cumulus cell mass in terms of their oxidative status. Accordingly, for control group, COC were matured at 38.5 °C for complete 24 h of meiotic maturation and heat stress of 40.5 and 41.5 °C was applied to COC during the first 12 h of maturation and then moved to 38.5 °C for rest of the 12 h. In another group, COC after maturation were denuded from the surrounding cumulus cells by manual pipetting. Results indicated that the production of reactive oxygen species (ROS), lipid peroxides, and nitric oxide (NO) was significantly (P < 0.05) higher in the oocytes subjected to heat stress (40.5 and 41.5 °C) during meiotic maturation compared to the oocytes matured under standard in vitro culture conditions (38.5 °C). Also, the antioxidant enzymatic activities of superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase were significantly (P < 0.05) increased in all the treatment groups compared to the control group. Therefore, the present study clearly establishes that heat stress ensues oxidative stress in bubaline oocytes which triggers the induction of antioxidant enzymatic defense system for scavenging the ROS.
Similar content being viewed by others
References
Aengwanich W, Kongbuntad W, Boonsorn T (2011) Effects of shade on physiological changes, oxidative stress, and total antioxidant power in Thai Brahman cattle. Int J Biometeorol 55:741–748
Arechiga CF, Ealy AD, Hansen PJ (1995) Evidence that glutathione is involved in thermotolerance of preimplantation murine embryos. Biol Reprod 52:1296–1301
Ashraf S, Shah SM, Saini N, Dhanda S, Singh MK, Chauhan MS et al (2014) Developmental competence and expression pattern of bubaline (Bubalus Bubalis) oocytes subjected to elevated temperatures during meiotic maturation in vitro. J Assist Reprod Genet 31:1349–1360
Bernabucci U, Ronchi B, Lacetera N, Nardone A (2002) Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. J Dairy Sci 85:2173–2179
Blondin P, Coenen K, Sirard MA (1997) The impact of reactive oxygen species on bovine sperm fertilizing ability and oocyte maturation. J Androl 18:454–460
Cetica PD, Pintos LN, Dalvit GC, Beconi MT (2001) Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51:57–64
Das SK, Upadhyay RC, Madan ML (1999) Heat stress in Murrah buffalo calves. Livest Prod Sci 61:71–78
Dubey PK, Tripathi V, Singh RP, Sharma T (2011) Influence of nitric oxide on in vitro growth, survival, steroidogenesis and apoptosis of follicle stimulating hormone stimulated buffalo (Bubalus bubalis) preantral follicles. J Vet Sci 12:257–265
Ealy AD, Drost M, Hansen PJ (1993) Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J Dairy Sci 76:2899–2905
Edwards JL, Hansen PJ (1997) Differential Responses of bovine oocytes and preimplantation embryos to heat shock. Mol Reprod Dev 46:138–145
El-Mouatassim S, Guerin P, Menezo Y (1999) Expression of gene encoding antioxidant enzymes in human and mouse oocytes during final stages of maturation. Mol Hum Reprod 5:720–725
Fisher PR, Karampetsos P, Wilczynska Z, Rosenberg LT (1991) Oxidative metabolism and heat shock-enhanced chemiluminescence in Dictyostelium. discoideum J. Cell Sci 99:741–750
Flanagan SW, Moseley PL, Buettner GR (1998) Increased flux of free radicals in cells subjected to hyperthermia: detection by electron paramagnetic resonance spin trapping. FEBS Lett 431:285–286
Goto K, Noda Y, Mori T, Nakano M (1993) Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radical Biol Med 15:69–75
Guerin P, El Mouatassim S, Menezo Y (2001) Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7:175–189
Hancock JT, Desikan R, Neill SJ (2001) Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans 29:345–360
Harvey MB, Arachilina Panlilio MY, Zhang X et al (1995) Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol Reprod 53:532–540
Jablonka-Shariff A, Olson LM (1998) The role of nitric oxide in oocyte meiotic maturation and ovulation: meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology 139:2944–2954
Kumar A, Kumar P, Singh SV (2007) Oxidative stress markers profile in erythrocytes of natural and heat exposed cattle and buffalos. Indian J Dairy Sci 60:114–118
Lakritz J, Leonard MJ, Eichen PA, Rottinghaus GE, Johnson GC et al (2002) Whole blood concentration of glutathione in cattle exposed to heat stress and endophyte-infected tall fescue toxins in controlled environmental conditions. Am J Vet Res 63:799–803
Li J, Billiar TR (2000) The role of nitric oxide in apoptosis. Semin Perinatol 24:46–50
Liu Y, He X-Q, Huang X, Ding L, Xu L et al (2013) Resveratrol protects mouse oocytes from Methylglyoxal-induced oxidative damage. PLoS One 8:e77960
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 79:31–40
Nagao Y, Saeki MH, Kainuma H (1994) Effects of oxygen concentration and oviductal tissue on the development of in vitro matured and fertilized bovine oocytes in protein-free medium. Theriogenology 41:681–687
Nardone A, Ronchi B, Lacetera N, Ranieri MS, Bernabucci U (2010) Effects of climate changes on animal production and sustainability of livestock systems. Livest Sci 130:57–69
Nasr-Esfahani MH, Aitken JR, Johnson MH (1990) Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed In vitro or in vivo. Development 109:501–507
National Research Council (1971) A guide to environmental research on animals. National Academy of Science, Washington
Pardo CV, Morales AT, Rio MJD, Angel MO (2007) Endogenously generated hydrogen peroxide induces apoptosis via mitochondrial damage independent of NF-kB and p53 activation in bovine embryos. Theriogenology 67:1285–1296
Pierce GB, Parchment RE, Lewellyn AL (1991) Hydrogen peroxide as a mediator of programmed cell death in the blastocyst. Differentiation 46:181–186
Rameshbabu K, Sharma R, Singh KP, George A, Chauhan MS, Singla SK et al (2012) Presence of nitric oxide synthase immunoreactivity and mRNA in buffalo (Bubalus bubalis) oocytes and embryos. Reprod Domest Anim 47:439–531
Rivera RM, Dahlgren GM, De Castro e Paula LA, Kennedy RT, Hansen PJ (2004) Actions of thermal stress in two-cell bovine embryos: oxygen metabolism, glutathione and ATP content, and the time-course of development. Reproduction 128:33–42
Roth Z, Hansen PJ (2005) Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129:235–244
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 67:77–82
Sethi RK, Bharadwaj A, Chopra SC (1994) Effect of heat stress on buffaloes under different shelter strategies. Indian J Anim Sci 64:1282–1285
Takahashi M, Nagai T, Hamano S, Kuwayama M, Okamura N, Okano A (1993) Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol Reprod 49:228–232
Yadav A, Singh KP, Singh MK, Saini N, Palta P, Manik RS et al (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 4:858–865. doi:10.1111/rda.12175
Yang HW, Hwang K-J, Kwon H-C, Kim H-S, Choi K-W, Oh KS (1998) Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Human Reprod 13:998–1002
Yoshida M, Ishigaki K, Nagai T, Chikyu M, Pursel VG (1993) Glutathione concentration during maturation and after fertilization in pig oocytes: relevance of the ability of oocytes to form male pronucleus. Biol Reprod 49:89–94
Acknowledgments
This study was supported by the National Initiative on Climate Resilient Agriculture (NICRA; Grant No. 2049/3033), Indian Council of Agricultural Research, New Delhi. The authors express sincere gratitude to the Director, National Dairy Research Institute, Karnal, for providing the necessary facilities.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have not any conflict of interest to declare.
Rights and permissions
About this article
Cite this article
Waiz, S.A., Raies-ul-Haq, M., Dhanda, S. et al. Heat stress and antioxidant enzyme activity in bubaline (Bubalus bubalis) oocytes during in vitro maturation. Int J Biometeorol 60, 1357–1366 (2016). https://doi.org/10.1007/s00484-015-1129-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-015-1129-0