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

Journal of Assisted Reproduction and Genetics

Volumn 31, Issue 10, 2014, Pages 1349-1360

  Ashraf, Syma ^a   Shah, Syed Mohammad ^a   Saini, Neha ^a   Dhanda, Suman ^b   Kumar, Anil ^a   Goud, T Sridhar ^a   Singh, M K ^a   Chauhan, M S ^a   Upadhyay, R C ^a  

^a NATIONAL DAIRY RESEARCH INSTITUTE   (India)

^b KURUKSHETRA UNIVERSITY   (India)

Author keywords

Bubaline; Embryo; Heat stress; In vitro maturation; Oocyte

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; CASPASE; CASPASE 3; CASPASE 7; CASPASE 8; CHAPERONIN 60; EARLY PREGNANCY FACTOR; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN MCL 1; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; ZAR1 PROTEIN;

ARTICLE; ARTIFICIAL INSEMINATION; BLASTOCYST; CELL COUNT; CONTROLLED STUDY; FERTILIZATION IN VITRO; GENE EXPRESSION; GLUCOSE TRANSPORT; HIGH TEMPERATURE; IN VITRO OOCYTE MATURATION; IN VITRO STUDY; MEIOSIS; NONHUMAN; OOCYTE; OXIDATIVE STRESS; WATER BUFFALO; ANIMAL; APOPTOSIS; BUFFALO; GENETICS; HEAT; PHYSIOLOGY;

BUBALUS; BUBALUS BUBALIS;

ANIMALS; APOPTOSIS; BLASTOCYST; BUFFALOES; HEAT-SHOCK PROTEINS; HOT TEMPERATURE; MEIOSIS; OOCYTES; OXIDATIVE STRESS; RNA, MESSENGER;

EID: 84918828189     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-014-0275-3     Document Type: Article

References (53)

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.
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.
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.
4. Das SK, Upadhyay RC, Madan ML. Heat stress in Murrah buffalo calves. Livest Prod Sci. 1999;61:71–8.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
15. Hansen PJ, Arechiga CF. Strategies for managing reproduction in heat stressed dairy Cows. J Dairy Sci. 1999;82(2):36–50.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
45. Christianson DW. Structural chemistry and biology of Manganese metalloenzymes. Prog Biophys Mol Biol. 1997;67(2–3):217–52.
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.
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.
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.
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.
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.
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.
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.
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.