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Developmental competence and expression pattern of bubaline (Bubalus bubalis) oocytes subjected to elevated temperatures during meiotic maturation in vitro

  • Gamete Biology
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Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Objective

To determine the direct effect of physiologically relevant high temperatures (40.5 and 41.5 °C) for two time periods (12 and 24 h) on bubaline oocytes during in vitro maturation.

Method

The control group oocytes were cultured at 38.5 °C for 24 h. The treatment 1 (T1) and 3 (T3) group oocytes were cultured at 40.5 and 41.5 °C respectively, for the first 12 h and at 38.5 °C for rest of the 12 h. However, treatment 2 (T2) and 4 (T4) group oocytes were cultured at 40.5 and 41.5 °C for complete 24 h.

Results

Development of oocytes to blastocyst was severely compromised (p < 0.001) when matured at 40.5 and 41.5 °C for both exposure periods (12 h and 24 h). It was found that the cleavage rates, blastocyst yield and mean cell number decreased remarkably (p < 0.001) in the treatment groups compared to control. The relative mRNA expression of heat shock protein (Hsp 70.1, 70.2, 70.8, 60, 10 and HSF1), pro-apoptotic (caspases-3, −7, −8, Bid and Bax) and oxidative stress (iNOS) related genes was significantly higher (p < 0.05) in all the treatment groups compared to control. However, mRNA abundance of anti-apoptotic (Bcl-2, Mcl-1, Bcl-xl), glucose transport (Glut1, Glut3 and IGF1R), developmental competence (ZAR1 and BMP15) and oxidative stress (MnSOD) related genes was significantly decreased (p < 0.05) in the treatment groups compared to control.

Conclusion

The present study clearly establishes that physiologically relevant elevated temperatures during in vitro meiotic maturation reduce developmental competence of bubaline oocytes.

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References

  1. Ealy AD, Howell JL, Monterroso VH, Arechiga CF, Hansen PJ. Developmental changes in sensitivity of bovine embryos to heat shock and use of antioxidants as thermoprotectants. J Anim Sci. 1995;73(5):1401–7.

    PubMed  CAS  Google Scholar 

  2. Collier RJ, Beede DK, Thatcher WW, Israel LA, Wilcox CJ. Influences of environment and its modification on dairy animal health and production. J Dairy Sci. 1982;65(11):2213–27. doi:10.3168/jds.S0022-0302(82)82484-3.

    Article  PubMed  CAS  Google Scholar 

  3. Aggarwal A, Upadhyay RC. Studies on evaporative heat losses from skin and pulmonary surfaces in male buffaloes exposed to solar radiations. Buffalo J. 1998;2:179–87.

    Google Scholar 

  4. Das SK, Upadhyay RC, Madan ML. Heat stress in Murrah buffalo calves. Livest Prod Sci. 1999;61:71–8.

    Article  Google Scholar 

  5. Sethi RK, Bharadwaj A, Chopra SC. Effect of heat stress on buffaloes under different shelter strategies. Indian J Anim Sci. 1994;64(11):1282–5.

    Google Scholar 

  6. Ashour G, Shafie MM. Water balance in riverine buffaloes. Mobilization of body fluids under heat and dehydration stresses. International Symposium on Prospects of Buffalo Production in the Mediterranean and Middle East. EAAP Publ. 1993;62:194–7.

    Google Scholar 

  7. Badinga L, Thatcher WW, Diaz T, Drost M, Wolfenson D. Effect of environmental heat stress on follicular development and steriodogenesis in lactating Holstein cows. Theriogenology. 1993;39(4):797–810. doi:10.1016/0093-691X(93)90419-6.

    Article  PubMed  CAS  Google Scholar 

  8. Nandi S, Chauhan MS, Palta P. Effect of environmental temperature on quality and developmental competence in vitro of buffalo oocytes. Vet Rec. 2001;148(9):278–9.

    Article  PubMed  CAS  Google Scholar 

  9. El-Naby, Al-shimaa Al-H HK, Mahmoud GM, Ahmed YF, Abouel-Roos MEA, Abdel-Ghaffar AE. Effect of season of the year ovarian structures on oocytes recovery rate and quality and meiotic competence in Egyptian buffaloes. Glob Vet. 2013;10:408–12. doi:10.5829/idosi.gv.2013.10.4.7281.

    Google Scholar 

  10. Al-Katanani YM, Lopes P, Hansen PJ. Effect of season and exposure to heat stress on oocyte competence in holstein cows. J Dairy Sci. 2002;85(2):390–6.

    Article  PubMed  CAS  Google Scholar 

  11. Rocha A, Randel RD, Broussard JR, Lim JM, Blair RM, Roussel JD, et al. High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows. Theriogenology. 1998;49(3):657–65. doi:10.1016/S0093- 69X(98)00016-8.

    Article  PubMed  CAS  Google Scholar 

  12. Putney DJ, Mullins S, Thatcher WW, Drost M, Gross TS. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Anim Reprod Sci. 1989;19:37–51.

    Article  Google Scholar 

  13. Chauhan MS, Singla SK, Palta P, Manik RS, Madan ML. In vitro maturation and fertilization, and subsequent development of buffalo (Bubalus bubalis) embryos: effects of oocyte quality and type of serum. Reprod Fertil Dev. 1998;10(2):173–7.

    Article  PubMed  CAS  Google Scholar 

  14. Ju JC, Tseng JK. Nuclear and cytoskeletal alterations of in vitro matured porcine oocyte under hyperthermia. Mol Reprod Dev. 2004;68(1):125–33. doi:10.1002/mrd.20054.

    Article  PubMed  CAS  Google Scholar 

  15. Hansen PJ, Arechiga CF. Strategies for managing reproduction in heat stressed dairy Cows. J Dairy Sci. 1999;82(2):36–50.

    Google Scholar 

  16. Cartmill JA, El-Zarkouny SZ, Hensley BA, Rozell TG, Smith JF, Stevenson JS. An alternative AI breeding protocol for dairy cows exposed to elevated ambient temperatures before or after calving or both. J Dairy Sci. 2001;84(4):799–806. doi:10.3168/jds.S0022-0302(01)74536-5.

    Article  PubMed  CAS  Google Scholar 

  17. Gwazdauskas FC, Thatcher WW, Wilcox CJ. Physiological, environmental, and hormonal factors at insemination which may affect conception. J Dairy Sci. 1973;56(7):873–7. doi:10.3168/jds.S0022-0302(73)85270-1.

    Article  PubMed  CAS  Google Scholar 

  18. Cavestany D, El-Wishy AB, Foote RH. Effect of season and high environmental temperature on fertility of Holstein cattle. J Dairy Sci. 1985;68(6):1471–8. doi:10.3168/jds.S0022-0302(85)80985-1.

    Article  PubMed  CAS  Google Scholar 

  19. Roth Z, Hansen PJ. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod. 2004;71(6):1898–906. doi:10.1095/biolreprod.104.031690.

    Article  PubMed  CAS  Google Scholar 

  20. Rensis FD, Scaramuzzi RJ. Heat stress and seasonal effects on reproduction in the dairy cow-a review. Theriogenology. 2003;60(6):1139–51. doi:10.1016/S0093691X(03)00126-2..

    Article  PubMed  Google Scholar 

  21. Edwards JL, Saxton AM, Lawrence JL, Payton RR, Dunlap JR. Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. J Dairy Sci. 2005;88(12):4326–33. doi:10.3168/jds.S0022-0302(05)73119-2.

    Article  PubMed  CAS  Google Scholar 

  22. Schrock GE, Saxton AM, Schrick FN, Edwards JL. Early in vitro fertilization improves development of bovine ova heat stressed during in vitro maturation. J Dairy Sci. 2005;90(9):4297–303. doi:10.3168/jds.2007-0002.

    Article  Google Scholar 

  23. Mishra V, Mishra AK, Sharma R. Effect of ambient temperature on in vitro fertilization of bubaline oocyte. Anim Reprod Sci. 2007;100(3–4):379–84. doi:10.1016/j.anireprosci.2006.10.020..

    Article  PubMed  CAS  Google Scholar 

  24. de Torres-Junior Jr S, de Pires FAM, de Sá WF, de Ferreira MA, Viana JH, Camargo LS, et al. Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology. 2008;69(2):155–66. doi:10.1016/j.theriogenology.2007.06.023.

    Article  CAS  Google Scholar 

  25. Yadav A, Singh KP, Singh MK, Saini N, Palta P, Manik RS, et al. 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. 2013;48(5):858–65. doi:10.1111/rda.12175.

    Article  PubMed  CAS  Google Scholar 

  26. Edwards JL, Hansen PJ. Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol Reprod Dev. 1997;46(2):138–45. doi:10.1002/(SICI)1098-2795(199702)46:2<138::AID-MRD4>3.0.CO;2-R.

    Article  PubMed  CAS  Google Scholar 

  27. Jousan FD, Hansen PJ. Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signalling. Mol Reprod Dev. 2007;74(2):189–96. doi:10.1002/mrd.20527.

    Article  PubMed  CAS  Google Scholar 

  28. Zoheir KMA, Abdoon AS, Mahrous KF, Amer MA, Zaher MM, Li-Guo Y, et al. Effects of season on the quality and in vitro maturation rate of Egyptian buffalo (Bubalus bubalis) oocytes. J Cell Anim Biol. 2007;1(2):29–33.

    Google Scholar 

  29. Payton RR, Romar R, Coy P, Saxton AM, Lawrence JL, Edwards JL. Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biol Reprod. 2004;71(4):1303–8.

    Article  PubMed  CAS  Google Scholar 

  30. Rispoli LA, Lawrence JL, Payton RR, Saxton MA, Schrock GE, Schrick FN, et al. Disparate consequences of heat stress exposure during meiotic maturation: embryo development after chemical activation vs fertilization of bovine oocytes. Reproduction. 2011;142:832–43. doi:10.1530/REP-11-0032.

    Article  Google Scholar 

  31. Edwards JL, Hansen PJ. Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes. Biol Reprod. 1996;55(2):340–6. doi:10.1095/biolreprod55.2.341.

    Article  CAS  Google Scholar 

  32. Lawrence JL, Payton RR, Godkin JD, Saxton AM, Schrick FN, Edwards JL. Retinol improves development of bovine oocytes compromised by heat stress during maturation. J Dairy Sci. 2004;87(8):2449–54. doi:10.3168/jds.S0022-0302(04)73368-8..

    Article  PubMed  CAS  Google Scholar 

  33. de CastroePaula LA, Hansen PJ. Modification of actions of heat shock on development and apoptosis of cultured preimplantation bovine embryos by oxygen concentration and dithiothreitol. Mol Reprod Dev. 2008;75(8):1338–50. doi:10.1002/mrd.20866.

    Article  Google Scholar 

  34. Sugiyama S, McGowan M, Phillips N, Kafi M, Young M. Effects of increased ambient temperature during IVM and/or IVF on the in vitro development of bovine zygotes. Reprod Domest Anim. 2007;42(3):271–4. doi:10.1111/j.1439 0531.2006.00776.

    Article  PubMed  CAS  Google Scholar 

  35. Jin YX, Lee JY, Choi SH, Kim T, Cui XS, Kim NH. Heat shock induces apoptosis related gene expression and apoptosis in porcine parthenotes developing in vitro. Anim Reprod Sci. 2007;100(1–2):118–27. doi:10.1016/j.anireprosci.2006.06.017.

    Article  PubMed  CAS  Google Scholar 

  36. Perez GI, Tao X-J, Tilly JL. Fragmentation and death (a.k.a. apoptosis) of ovulated oocytes. Mol Hum Reprod. 1999;5(5):414–20.

    Article  PubMed  CAS  Google Scholar 

  37. Kelly MB, Salvesen GS. Mechanisms of caspase activation. Curr Opin Cell Biol. 2003;15(6):725–31. doi:10.1016/j.ceb.2003.10.009.

    Article  Google Scholar 

  38. Kawarsky SJ, King WA. Expression and localization of heat shock protein 70 in culture of bovine oocytes and embryos. Zygote. 2001;9(1):39–50.

    Article  PubMed  CAS  Google Scholar 

  39. Salvetti NR, Stangaferro ML, Palomar MM, Alfaro NS, Rey F, Gimeno EJ, et al. Cell proliferation and survival mechanisms underlying the abnormal persistence of follicular cysts in bovines with cystic ovarian disease induced by ACTH. Anim Reprod. 2010;122(1 2):98–110. doi:10.1016/j.anireprosci.2010.08.003.

    Article  CAS  Google Scholar 

  40. Oliveira ATD, Lopes RFF, Rodrigues JL. Gene expression and developmental competence of bovine embryos produced in vitro under varying embryo density conditions. Theriogenology. 2005;64(7):1559–72. doi:10.1016/j therigenology 2005.03.019.

    Article  PubMed  Google Scholar 

  41. Mortensen CJ, Choi YH, Ing NH, Kraemer DC, Vogelsang MM, Hinrichs K. Heat shock protein 70 gene expression in equine blastocysts after exposure of oocytes to high temperatures in vitro or in vivo after exercise of donor mares. Theriogenology. 2010;74(3):374–83. doi:10.1016/j.theriogenology.2010.02.020.

    Article  PubMed  CAS  Google Scholar 

  42. Fiorenza MT, Bevilacqua A, Canterini S, Torcia S, Pontecorvi M. Early transcriptional activation of the Hsp70.1 gene by osmotic stress in one-cell embryos of the mouse. Biol Reprod. 2004;70(6):1606–13.

    Article  PubMed  CAS  Google Scholar 

  43. Morimoto RI. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 1998;12(24):3788–96. doi:10.1101/gad.12.24.3788.

    Article  PubMed  CAS  Google Scholar 

  44. Wu C. Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol. 1995;11:441–69. doi:10.1146/annurev.cb.11.110195.002301.

    Article  PubMed  CAS  Google Scholar 

  45. Christianson DW. Structural chemistry and biology of Manganese metalloenzymes. Prog Biophys Mol Biol. 1997;67(2–3):217–52.

    Article  PubMed  CAS  Google Scholar 

  46. Huo LJ, Liang CG, Yu LZ, Zhong ZS, Yang ZM, Fan HY, et al. Inducible nitric oxide synthase-derived nitric oxide regulates germinal vesicle breakdown and first polar body emission in the mouse oocyte. Reproduction. 2005;129(4):403–9. doi:10.1530/rep.1.0542..

    Article  PubMed  CAS  Google Scholar 

  47. Balasubramanian S, Son WJ, Mohana KB, Ock SA, Yoo JG, Im GS, et al. Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos. Theriogenology. 2007;68(2):265–75. doi:10.1016/j.theriogenology.2007.05.044.

    Article  PubMed  CAS  Google Scholar 

  48. Rameshbabu K, Sharma R, Singh KP, George A, Chauhan MS, Singla SK, et al. Presence of nitric oxide synthase immunoreactivity and mRNA in buffalo (Bubalus bubalis) oocytes and embryos. Reprod Dom Anim. 2012;47(2):439–531. doi:10.1111/j.1439-0531.2011.01884.

    Article  Google Scholar 

  49. Tesfaye D, Kadanga A, Rings F, Bauch K, Jennen D, Nganvongpanit K, et al. The effect of nitric oxide inhibition and temporal expression patterns of the mRNA and protein products of nitric oxide synthase genes during in vitro development of bovine pre-implantation embryos. Reprod Domest Anim. 2006;41(6):501–9. doi:10.1111/j.1439-0531.2006.00701.

    Article  PubMed  CAS  Google Scholar 

  50. Nishimoto H, Matsutani R, Yamamotol S, Takahashi T, Hayashi, Miyamoto A. Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. J Endocrinol. 2006;188(1):111–9.

    Article  PubMed  CAS  Google Scholar 

  51. Lequarre AS, Grisart B, Moreau B, Schurbiers N, Massip A, Dessy F. Glucose metabolism during bovine preimplantation development: analysis of gene expression in single oocytes and embryos. Mol Reprod Dev. 1997;48(2):216–26. doi:10.1002/(SICI)1098-2795(199710)48:2<216::AID-MRD9>3.0.CO;2-V.

    Article  PubMed  CAS  Google Scholar 

  52. Bertolini A, Beam SW, Shim H, Bertolini LR, Moyer AL, Famula TR, et al. Growth, development and gene expression by in vivo and in vitro produced day 7 and 16 bovine embryos. Mol Reprod Dev. 2002;63(3):318–28. doi:10.1002/mrd.90015.

    Article  PubMed  CAS  Google Scholar 

  53. Payton RR, Rispoli LA, Saxton AM, Edwards JL. Impact of heat stress exposure during meiotic maturation on oocyte, surrounding cumulus cell and embryo RNA populations. J Reprod Dev. 2011;57(4):481–91. doi:10.1262/jrd.10-163M.S0093691X(03)00126-2.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by 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.

Conflict of interest

None of the authors have any conflict of interest to declare.

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Authors and Affiliations

  1. Animal Biotechnology Centre, National Dairy Research Institute, Karnal, 132001, Haryana, India

    Syma Ashraf, Syed Mohammad Shah, Neha Saini, M. K. Singh & M. S. Chauhan

  2. Department of Biochemistry, Kurukshetra University, Kurukshetra, 136119, Haryana, India

    Suman Dhanda

  3. Dairy Cattle Physiology, National Dairy Research Institute, Karnal, 132001, Haryana, India

    Anil Kumar, T. Sridhar Goud & R. C. Upadhyay

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  1. Syma Ashraf
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  2. Syed Mohammad Shah
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  8. M. S. Chauhan
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  9. R. C. Upadhyay
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Corresponding author

Correspondence to M. S. Chauhan.

Additional information

Capsule Oocyte maturation is the very first and critical stage in the overall embryo development. Therefore, exploiting the genetic determinants of oocyte might prove helpful in alleviating the embryonic losses in buffalo due to heat stress.

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Ashraf, S., Shah, S.M., Saini, N. et al. 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 (2014). https://doi.org/10.1007/s10815-014-0275-3

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