Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Genetic variation in resistance of the preimplantation bovine embryo to heat shock

Peter J. Hansen
+ Author Affiliations
- Author Affiliations

Department of Animal Sciences, D. H. Barron Reproductive and Perinatal Biology Research Program, and Genetics Institute, University of Florida, Gainesville, FL 32611-0910, USA. Email: pjhansen@ufl.edu

Reproduction, Fertility and Development 27(1) 22-30 https://doi.org/10.1071/RD14311
Published: 4 December 2014

Abstract

Reproduction is among the physiological functions in mammals most susceptible to disruption by hyperthermia. Many of the effects of heat stress on function of the oocyte and embryo involve direct effects of elevated temperature (i.e. heat shock) on cellular function. Mammals limit the effects of heat shock by tightly regulating body temperature. This ability is genetically controlled: lines of domestic animals have been developed with superior ability to regulate body temperature during heat stress. Through experimentation in cattle, it is also evident that there is genetic variation in the resistance of cells to the deleterious effects of elevated temperature. Several breeds that were developed in hot climates, including Bos indicus (Brahman, Gir, Nelore and Sahiwal) and Bos taurus (Romosinuano and Senepol) are more resistant to the effects of elevated temperature on cellular function than breeds that evolved in cooler climates (Angus, Holstein and Jersey). Genetic differences are expressed in the preimplantation embryo by Day 4–5 of development (after embryonic genome activation). It is not clear whether genetic differences are expressed in cells in which transcription is repressed (oocytes >100 µm in diameter or embryos at stages before embryonic genome activation). The molecular basis for cellular thermotolerance has also not been established, although there is some suggestion for involvement of heat shock protein 90 and the insulin-like growth factor 1 system. Given the availability of genomic tools for genetic selection, identification of genes controlling cellular resistance to elevated temperature could be followed by progress in selection for those genes within the populations in which they exist. It could also be possible to introduce genes from thermotolerant breeds into thermally sensitive breeds. The ability to edit the genome makes it possible to design new genes that confer protection of cells from stresses like heat shock.

Additional keywords: breed, cattle, thermotolerance.


References

Al-Katanani, Y. M., Webb, D. W., and Hansen, P. J. (1999). Factors affecting seasonal variation in 90-day nonreturn rate to first service in lactating Holstein cows in a hot climate. J. Dairy Sci. 82, 2611–2616.
Factors affecting seasonal variation in 90-day nonreturn rate to first service in lactating Holstein cows in a hot climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXis1Kq&md5=e61cb50597f38d307b2d64d526f96d92CAS | 10629807PubMed |

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.
Effect of season and exposure to heat stress on oocyte competence in Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitV2rsb0%3D&md5=2a2b023731e0f297e08b436076244432CAS | 11913699PubMed |

Andreu-Vázquez, C., López-Gatius, F., García-Ispierto, I., Maya-Soriano, M. J., Hunter, R. H., and López-Béjar, M. (2010). Does heat stress provoke the loss of a continuous layer of cortical granules beneath the plasma membrane during oocyte maturation? Zygote 18, 293–299.
Does heat stress provoke the loss of a continuous layer of cortical granules beneath the plasma membrane during oocyte maturation?Crossref | GoogleScholarGoogle Scholar | 20331910PubMed |

Badinga, L., Thatcher, W. W., Diaz, T., Drost, M., and Wolfenson, D. (1993). Effect of environmental heat stress on follicular development and steroidogenesis in lactating Holstein cows. Theriogenology 39, 797–810.
Effect of environmental heat stress on follicular development and steroidogenesis in lactating Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvVKnu78%3D&md5=0ea28c18a9bcc9d57f6fdf3f8c4e1ed8CAS | 16727254PubMed |

Baruselli, P. S., Ferreira, R. M., Sales, J. N., Gimenes, L. U., Sá Filho, M. F., Martins, C. M., Rodrigues, C. A., and Bó, G. A. (2011). Timed embryo transfer programs for management of donor and recipient cattle. Theriogenology 76, 1583–1593.
Timed embryo transfer programs for management of donor and recipient cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbnvVSkug%3D%3D&md5=13f5942de54f4e5e199df0d826aac436CAS | 21798580PubMed |

Basiricò, L., Morera, P., Primi, V., Lacetera, N., Nardone, A., and Bernabucci, U. (2011). Cellular thermotolerance is associated with heat shock protein 70.1 genetic polymorphisms in Holstein lactating cows. Cell Stress Chaperones 16, 441–448.
Cellular thermotolerance is associated with heat shock protein 70.1 genetic polymorphisms in Holstein lactating cows.Crossref | GoogleScholarGoogle Scholar | 21274669PubMed |

Block, J., Chase, C. C., and Hansen, P. J. (2002). Inheritance of resistance of bovine preimplantation embryos to heat shock: relative importance of the maternal vs paternal contribution. Mol. Reprod. Dev. 63, 32–37.
Inheritance of resistance of bovine preimplantation embryos to heat shock: relative importance of the maternal vs paternal contribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVems70%3D&md5=f6c0bb2f8f36410271e38510fc627b1eCAS | 12211058PubMed |

Bonilla, A. Q., Oliveira, L. J., Ozawa, M., Newsom, E. M., Lucy, M. C., and Hansen, P. J. (2011). Developmental changes in thermoprotective actions of insulin-like growth factor-1 on the preimplantation bovine embryo. Mol. Cell. Endocrinol. 332, 170–179.
Developmental changes in thermoprotective actions of insulin-like growth factor-1 on the preimplantation bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WqtLbF&md5=362f15d2a06f21b86cdc555cbb63316bCAS | 20965229PubMed |

Cabrera, V. E. (2014). Economics of fertility in high-yielding dairy cows on confined TMR systems. Animal 8, 211–221.
Economics of fertility in high-yielding dairy cows on confined TMR systems.Crossref | GoogleScholarGoogle Scholar | 24679357PubMed |

Carstens, G. E., Mostyn, P. M., Lammoglia, M. A., Vann, R. C., Apter, R. C., and Randel, R. D. (1997). Genotypic effects on norepinephrine-induced changes in thermogenesis, metabolic hormones, and metabolites in newborn calves. J. Anim. Sci. 75, 1746–1755.
| 1:CAS:528:DyaK2sXkt1Gmtrg%3D&md5=adc29ed19141e6edae551570d4bc3b7dCAS | 9222830PubMed |

Chandolia, R. K., Peltier, M. R., Tian, W., and Hansen, P. J. (1999). Transcriptional control of development, protein synthesis and heat-induced heat shock protein 70 synthesis in 2-cell bovine embryos. Biol. Reprod. 61, 1644–1648.
Transcriptional control of development, protein synthesis and heat-induced heat shock protein 70 synthesis in 2-cell bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1ynt7k%3D&md5=694f2cb2f9ad12e2992b21a832290371CAS | 10570014PubMed |

Davis, M. E., Rutledge, J. J., Cundiff, L. V., and Hauser, E. R. (1983). Life cycle efficiency of beef production: II. Relationship of cow efficiency ratios to traits of the dam and progeny weaned. J. Anim. Sci. 57, 852–866.
| 1:STN:280:DyaL2c%2FmtFCmsA%3D%3D&md5=d5518a672ee960d71520ec4941d2ef04CAS | 6643302PubMed |

de Castro e Paula, L. A., and 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, 1338–1350.
Modification of actions of heat shock on development and apoptosis of cultured preimplantation bovine embryos by oxygen concentration and dithiothreitol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1aks7Y%3D&md5=885dad50572f8e28a767fc02641700d5CAS | 18246528PubMed |

Dikmen, S., Martins, L., Pontes, E., and Hansen, P. J. (2009). Genotype effects on body temperature in dairy cows under grazing conditions in a hot climate including evidence for heterosis. Int. J. Biometeorol. 53, 327–331.
Genotype effects on body temperature in dairy cows under grazing conditions in a hot climate including evidence for heterosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mrkt1WntA%3D%3D&md5=57f5a9c321e58819cdaf0f16402cc0deCAS | 19263087PubMed |

Dikmen, S., Cole, J. B., Null, D. J., and Hansen, P. J. (2013). Genome-wide association mapping for identification of quantitative trait loci for rectal temperature during heat stress in Holstein cattle. PLoS ONE 8, e69202.
Genome-wide association mapping for identification of quantitative trait loci for rectal temperature during heat stress in Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1eju7%2FF&md5=4d46c54ab261bf644b2805133302fc7bCAS | 23935954PubMed |

Dikmen, S., Khan, F. A., Huson, H. J., Sonstegard, T. S., Moss, J. I., Dahl, G. E., and Hansen, P. J. (2014). The SLICK locus derived from Senepol cattle confers thermotolerance to intensively-managed lactating Holstein cows. J. Dairy Sci. 97, 5508–5520.
The SLICK locus derived from Senepol cattle confers thermotolerance to intensively-managed lactating Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFSht7rJ&md5=00d1ab73befed35c6ba369511134df91CAS | 24996281PubMed |

Drost, M., Ambrose, J. D., Thatcher, M.-J., Cantrell, C. K., Wolfsdorf, K. E., Hasler, J. F., and Thatcher, W. W. (1999). Conception rates after artificial insemination or embryo transfer in lactating dairy cows during summer in Florida. Theriogenology 52, 1161–1167.
Conception rates after artificial insemination or embryo transfer in lactating dairy cows during summer in Florida.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFaluw%3D%3D&md5=428547b1202996bb078b8f570c7ffd72CAS | 10735094PubMed |

Dunlap, S. E., and Vincent, C. K. (1971). Influence of postbreeding thermal stress on conception rate in beef cattle. J. Anim. Sci. 32, 1216–1218.
| 1:STN:280:DyaE3M3hsVCmtA%3D%3D&md5=f4b9cdfb0115418d205d5e62a986c3e6CAS | 5087369PubMed |

Ealy, A. D., Drost, M., and Hansen, P. J. (1993). Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J. Dairy Sci. 76, 2899–2905.
Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FksVSmtQ%3D%3D&md5=3a6a00b4055b4b24239cf71e3b14b019CAS | 8227617PubMed |

Eberhardt, B. G., Satrapa, R. A., Capinzaiki, C. R., Trinca, L. A., and Barros, C. M. (2009). Influence of the breed of bull (Bos taurus indicus vs. Bos taurus taurus) and the breed of cow (Bos taurus indicus, Bos taurus taurus and crossbred) on the resistance of bovine embryos to heat. Anim. Reprod. Sci. 114, 54–61.
Influence of the breed of bull (Bos taurus indicus vs. Bos taurus taurus) and the breed of cow (Bos taurus indicus, Bos taurus taurus and crossbred) on the resistance of bovine embryos to heat.Crossref | GoogleScholarGoogle Scholar | 18980815PubMed |

Edwards, J. L., and Hansen, P. J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol. Reprod. Dev. 46, 138–145.
Differential responses of bovine oocytes and preimplantation embryos to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXoslWhtQ%3D%3D&md5=41a79ccc611bef31d01115495ea7473dCAS | 9021745PubMed |

Edwards, J. L., Ealy, A. D., Monterroso, V. H., and Hansen, P. J. (1997). Ontogeny of temperature-regulated heat shock protein 70 synthesis in preimplantation bovine embryos. Mol. Reprod. Dev. 48, 25–33.
Ontogeny of temperature-regulated heat shock protein 70 synthesis in preimplantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlt1SisrY%3D&md5=02b756a388fa5394a38ac9576395652bCAS | 9266758PubMed |

Fair, T., Hyttel, P., and Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437–442.
Bovine oocyte diameter in relation to maturational competence and transcriptional activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVGisb4%3D&md5=4117e4dc4bc41ae728dd5fd8dff27e27CAS | 8607973PubMed |

Ferreira, R. M., Ayres, H., Chiaratti, M. R., Ferraz, M. L., Araújo, A. B., Rodrigues, C. A., Watanabe, Y. F., Vireque, A. A., Joaquim, D. C., Smith, L. C., Meirelles, F. V., and Baruselli, P. S. (2011). The low fertility of repeat-breeder cows during summer heat stress is related to a low oocyte competence to develop into blastocysts. J. Dairy Sci. 94, 2383–2392.
The low fertility of repeat-breeder cows during summer heat stress is related to a low oocyte competence to develop into blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mvnt1Wisg%3D%3D&md5=bdf447542fd51bdf091e62ab356ccfafCAS | 21524528PubMed |

Gendelman, M., and Roth, Z. (2012a). 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. Biol. Reprod. 86, 1–9.
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.Crossref | GoogleScholarGoogle Scholar | 21957191PubMed |

Gendelman, M., and Roth, Z. (2012b). In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression. Anim. Reprod. Sci. 134, 125–134.
In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2rurjM&md5=3663598485e22d7e46a223bbb6f59762CAS | 22898494PubMed |

Gendelman, M., Aroyo, A., Yavin, S., and Roth, Z. (2010). Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos. Reproduction 140, 73–82.
Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVWls77N&md5=26a4e26ecc480ea7a265c6641292ad4eCAS | 20395426PubMed |

Graf, A., Krebs, S., Zakhartchenko, V., Schwalb, B., Blum, H., and Wolf, E. (2014). Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc. Natl Acad. Sci. USA 111, 4139–4144.
Fine mapping of genome activation in bovine embryos by RNA sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlyhsrs%3D&md5=7d286cc16ea47f4b5d1a6d5ed0061426CAS | 24591639PubMed |

Hammond, A. C., Olson, T. A., Chase, C. C., Bowers, E. J., Randel, R. D., Murphy, C. N., Vogt, D. W., and Tewolde, A. (1996). Heat tolerance in two tropically adapted Bos taurus breeds, Senepol and Romosinuano, compared with Brahman, Angus, and Hereford cattle in Florida. J. Anim. Sci. 74, 295–303.
| 1:CAS:528:DyaK28XhslCntb8%3D&md5=dde45df97f11cbf057daa58e2200ff65CAS | 8690664PubMed |

Hansen, P. J. (2007). Exploitation of genetic and physiological determinants of embryonic resistance to elevated temperature to improve embryonic survival in dairy cattle during heat stress. Theriogenology 68, S242–S249.
Exploitation of genetic and physiological determinants of embryonic resistance to elevated temperature to improve embryonic survival in dairy cattle during heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitbk%3D&md5=feebed6178c3978c9ada1c6e0d8298f3CAS | 17482669PubMed |

Hansen, P. J. (2009). Effects of heat stress on mammalian reproduction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3341–3350.
Effects of heat stress on mammalian reproduction.Crossref | GoogleScholarGoogle Scholar | 19833646PubMed |

Hansen, P. J. (2012). Supplemental antioxidants to improve reproduction in dairy cattle: why, when and how effective are they? In ‘Recent Advances in Animal Nutrition 2012’. (Eds P. C. Garnsworthy and J. Wiseman.) pp. 37–52. (Nottingham University Press: Nottingham.)

Hansen, P. J. (2013). Cellular and molecular basis of therapies to ameliorate effects of heat stress on embryonic development in cattle. Anim. Reprod. 10, 322–333.

Hayes, B. J., Bowman, P. J., Chamberlain, A. J., Savin, K., van Tassell, C. P., Sonstegard, T. S., and Goddard, M. E. (2009). A validated genome wide association study to breed cattle adapted to an environment altered by climate change. PLoS ONE 4, e6676.
A validated genome wide association study to breed cattle adapted to an environment altered by climate change.Crossref | GoogleScholarGoogle Scholar | 19688089PubMed |

Hernández-Cerón, J., Chase, C. C., and Hansen, P. J. (2004). Differences in heat tolerance between preimplantation embryos from Brahman, Romosinuano, and Angus breeds. J. Dairy Sci. 87, 53–58.
Differences in heat tolerance between preimplantation embryos from Brahman, Romosinuano, and Angus breeds.Crossref | GoogleScholarGoogle Scholar | 14765810PubMed |

Hirai, K., Sasaki, H., Yamamoto, H., Sakamoto, H., Kubota, Y., Kakizoe, T., Terada, M., and Ochiya, T. (2004). HST-1/FGF-4 protects male germ cells from apoptosis under heat-stress condition. Exp. Cell Res. 294, 77–85.
HST-1/FGF-4 protects male germ cells from apoptosis under heat-stress condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsV2gs7Y%3D&md5=cd3d9356d9b66ecba3158f87e5289cd5CAS | 14980503PubMed |

Howard, J. T., Kachman, S. D., Snelling, W. M., Pollak, E. J., Ciobanu, D. C., Kuehn, L. A., and Spangler, M. L. (2013). Beef cattle body temperature during climatic stress: a genome-wide association study. Int. J. Biometeorol. , .
Beef cattle body temperature during climatic stress: a genome-wide association study.Crossref | GoogleScholarGoogle Scholar | 24362770PubMed |

Jousan, F. D., and 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, 1665–1670.
Insulin-like growth factor-I as a survival factor for the bovine preimplantation embryo exposed to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1yitr0%3D&md5=67421da8c65a42bade373833f6434e4eCAS | 15253925PubMed |

Jousan, F. D., and Hansen, P. J. (2007). Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through action independent of its anti-apoptotic actions requiring PI3K signaling. Mol. Reprod. Dev. 74, 189–196.
Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through action independent of its anti-apoptotic actions requiring PI3K signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsV2rtQ%3D%3D&md5=c06747cbc97da4900efe94ed019d099cCAS | 16955404PubMed |

Ju, J. C., Jiang, S., Tseng, J. K., Parks, J. E., and Yang, X. (2005). Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes. Theriogenology 64, 1677–1689.
Heat shock reduces developmental competence and alters spindle configuration of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 15951010PubMed |

Kamwanja, L. A., Chase, C. C., Gutierrez, J. A., Guerriero, V., Olson, T. A., Hammond, A. C., and Hansen, P. J. (1994). Responses of bovine lymphocytes to heat shock as modified by breed and antioxidant status. J. Anim. Sci. 72, 438–444.
| 1:CAS:528:DyaK2cXitFelu7c%3D&md5=9885b6d4904dbfbc570c4f8858187ed1CAS | 8157528PubMed |

Kishore, A., Sodhi, M., Kumari, P., Mohanty, A. K., Sadana, D. K., Kapila, N., Khate, K., Shandilya, U., Kataria, R. S., and Mukesh, M. (2013). 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 , .
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.Crossref | GoogleScholarGoogle Scholar | 24363171PubMed |

Krininger, C. E., Stephens, S. H., and Hansen, P. J. (2002). Developmental changes in inhibitory effects of arsenic and heat shock on growth of pre-implantation bovine embryos. Mol. Reprod. Dev. 63, 335–340.
Developmental changes in inhibitory effects of arsenic and heat shock on growth of pre-implantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnslSnsbk%3D&md5=84e3aef9789d7867b476dbb3ee18b6a8CAS | 12237949PubMed |

Krininger, C. E., Block, J., Al-Katanani, Y. M., Rivera, R. M., Chase, C. C., and Hansen, P. J. (2003). Differences between Brahman and Holstein cows in response to estrus synchronization, superovulation and resistance of embryos to heat shock. Anim. Reprod. Sci. 78, 13–24.
Differences between Brahman and Holstein cows in response to estrus synchronization, superovulation and resistance of embryos to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjs1WrtL8%3D&md5=2fa03e336f9f373a18a9928f5f2012fbCAS | 12753779PubMed |

Lacetera, N., Bernabucci, U., Scalia, D., Basiricò, L., Morera, P., and Nardone, A. (2006). Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. J. Dairy Sci. 89, 4606–4612.
Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWgsrrI&md5=2d3b51352360cfe85f85b96f24dce25fCAS | 17106092PubMed |

Lazzari, G., Colleoni, S., Duchi, R., Galli, A., Houghton, F. D., and Galli, C. (2011). Embryonic genotype and inbreeding affect preimplantation development in cattle. Reproduction 141, 625–632.
Embryonic genotype and inbreeding affect preimplantation development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFCisro%3D&md5=7ed4f8308eacf2d89445d59117b4e460CAS | 21310813PubMed |

Li, Q., Han, J., Du, F., Ju, Z., Huang, J., Wang, J., Li, R., Wang, C., and Zhong, J. (2011a). Novel SNPs in HSP70A1A gene and the association of polymorphisms with thermo tolerance traits and tissue specific expression in Chinese Holstein cattle. Mol. Biol. Rep. 38, 2657–2663.
Novel SNPs in HSP70A1A gene and the association of polymorphisms with thermo tolerance traits and tissue specific expression in Chinese Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktlOksLw%3D&md5=189cdb2e7310a2e7cb658e06aa0f4070CAS | 21082257PubMed |

Li, Q. L., Ju, Z. H., Huang, J. M., Li, J. B., Li, R. L., Hou, M. H., Wang, C. F., and Zhong, J. F. (2011b). Two novel SNPs in HSF1 gene are associated with thermal tolerance traits in Chinese Holstein cattle. DNA Cell Biol. 30, 247–254.
Two novel SNPs in HSF1 gene are associated with thermal tolerance traits in Chinese Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVWls7Y%3D&md5=fede035a4833b100fcf1102c22572874CAS | 21189066PubMed |

Lim, J. M., Liou, S. S., and Hansel, W. (1996). Intracytoplasmic glutathione concentration and the role of β-mercaptoethanol in preimplantation development of bovine embryos. Theriogenology 46, 429–439.
Intracytoplasmic glutathione concentration and the role of β-mercaptoethanol in preimplantation development of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsFSjtLk%3D&md5=56de11af3d166602f0511ef52a019a40CAS | 16727911PubMed |

López-Gatius, F., Santolaria, P., Mundet, I., and Yániz, J. L. (2005). Walking activity at estrus and subsequent fertility in dairy cows. Theriogenology 63, 1419–1429.
Walking activity at estrus and subsequent fertility in dairy cows.Crossref | GoogleScholarGoogle Scholar | 15725448PubMed |

Loureiro, B., Bonilla, L., Block, J., Fear, J. M., Bonilla, A. Q. S., and Hansen, P. J. (2009). Colony stimulating factor 2 improves development and post-transfer survival of bovine embryos produced in vitro. Endocrinology 150, 5046–5054.
Colony stimulating factor 2 improves development and post-transfer survival of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCht7bF&md5=65e3733d1dd721d9af4ccb977214a029CAS | 19797121PubMed |

Malayer, J. R., and Hansen, P. J. (1990). Differences between Brahman and Holstein cows in heat-shock induced alterations of protein secretion by oviducts and uterine endometrium. J. Anim. Sci. 68, 266–280.
| 1:STN:280:DyaK3c7ltlOgtA%3D%3D&md5=d4162669a2ae42258576aa4d742c4265CAS | 2303398PubMed |

Meyerhoeffer, D. C., Wettemann, R. P., Coleman, S. W., and Wells, M. E. (1985). Reproductive criteria of beef bulls during and after exposure to increased ambient temperature. J. Anim. Sci. 60, 352–357.
| 1:STN:280:DyaL2M7ot1ehtw%3D%3D&md5=b36dd452b356a137583bf6772f2a424eCAS | 3988628PubMed |

Murphy, M. E. (2013). The HSP70 family and cancer. Carcinogenesis 34, 1181–1188.
The HSP70 family and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptFCnt7w%3D&md5=33ccfd2acd2ece8f2f26e06cecea65d4CAS | 23563090PubMed |

Nabenishi, H., Takagi, S., Kamata, H., Nishimoto, T., Morita, T., Ashizawa, K., and 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.
The role of mitochondrial transition pores on bovine oocyte competence after heat stress, as determined by effects of cyclosporin A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFeit7vJ&md5=f946b840393171c80550ac22749fd891CAS | 22128015PubMed |

Nebel, R. L., Jobst, S. M., Dransfield, M. B. G., Pandolfi, S. M., and Bailey, T. L. (1997). Use of radio frequency data communication system, HeatWatch®, to describe behavioral estrus in dairy cattle. J. Dairy Sci. 80, 179.

Olson, T. A., Lucena, C., Chase, C. C., and Hammond, A. C. (2003). Evidence of a major gene influencing hair length and heat tolerance in Bos taurus cattle. J. Anim. Sci. 81, 80–90.
| 1:CAS:528:DC%2BD3sXhtFagsL0%3D&md5=1b3587c8de1269fc461d6ad34eb00b05CAS | 12597376PubMed |

Paula-Lopes, F. F., Chase, C. C., Al-Katanani, Y. M., Krininger, C. E., Rivera, R. M., Tekin, S., Majewski, A. C., Ocon, O. M., Olson, T. A., and Hansen, P. J. (2003). Genetic divergence in cellular resistance to heat shock in cattle: differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures. Reproduction 125, 285–294.
Genetic divergence in cellular resistance to heat shock in cattle: differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVKlt7c%3D&md5=d3ad96a8eb8e1a415d5d8f17610417d4CAS | 12578542PubMed |

Payton, R. R., Romar, R., Coy, P., Saxton, A. M., Lawrence, J. L., and 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, 1303–1308.
Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqtbk%3D&md5=3fe7338e6aed3d0bb39607255ba65a3eCAS | 15201201PubMed |

Pegorer, M. F., Vasconcelos, J. L., Trinca, L. A., Hansen, P. J., and Barros, C. M. (2007). Influence of sire and sire breed (Gyr versus Holstein) on establishment of pregnancy and embryonic loss in lactating Holstein cows during summer heat stress. Theriogenology 67, 692–697.
Influence of sire and sire breed (Gyr versus Holstein) on establishment of pregnancy and embryonic loss in lactating Holstein cows during summer heat stress.Crossref | GoogleScholarGoogle Scholar | 17118436PubMed |

Putney, D. J., Drost, M., and Thatcher, W. W. (1988a). Embryonic development in superovulated dairy cattle exposed to elevated ambient temperature between days 1 to 7 post insemination. Theriogenology 30, 195–209.
Embryonic development in superovulated dairy cattle exposed to elevated ambient temperature between days 1 to 7 post insemination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFahug%3D%3D&md5=f616636bef69bd06e1b6fbae4962f463CAS | 16726462PubMed |

Putney, D. J., Thatcher, W. W., Drost, M., Wright, J. M., and Delorenzo, A. (1988b). Influence of environmental temperature on reproductive performance of bovine embryo donors and recipients in the southwest region of the United States. Theriogenology 30, 905–922.
Influence of environmental temperature on reproductive performance of bovine embryo donors and recipients in the southwest region of the United States.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFaqug%3D%3D&md5=6cbe1fa181efa0b2ec0d1c4beaad52daCAS | 16726533PubMed |

Putney, D. J., Mullins, S., Thatcher, W. W., Drost, M., and Gross, T. S. (1989). Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Anim. Reprod. Sci. 19, 37–51.
Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination.Crossref | GoogleScholarGoogle Scholar |

Richter, K., Haslbeck, M., and Buchner, J. (2010). The heat shock response: life on the verge of death. Mol. Cell 40, 253–266.
The heat shock response: life on the verge of death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCjtr7E&md5=2610411e51988accde6f2eb97b2ea5faCAS | 20965420PubMed |

Rivera, R. M., Kelley, K. L., Erdos, G. W., and Hansen, P. J. (2003). Alterations in ultrastructural morphology of two-cell bovine embryos produced in vitro and in vivo following a physiologically-relevant heat shock. Biol. Reprod. 69, 2068–2077.
Alterations in ultrastructural morphology of two-cell bovine embryos produced in vitro and in vivo following a physiologically-relevant heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCnsbc%3D&md5=7ace6018c0ed1915014d94591bf07ac2CAS | 12930717PubMed |

Roth, Z., and Hansen, P. J. (2004). Involvement of apoptosis in disruption of oocyte competence by heat shock in cattle. Biol. Reprod. 71, 1898–1906.
Involvement of apoptosis in disruption of oocyte competence by heat shock in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsrzL&md5=ce44e78eb822b58fedcc7a3068792c51CAS | 15306551PubMed |

Roth, Z., and Hansen, P. J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–244.
Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1yrsrg%3D&md5=568148b038482c67e83f9aade4d1f32eCAS | 15695618PubMed |

Sakatani, M., Kobayashi, S., and 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.
Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1ems7o%3D&md5=ab98cece8ac4ebad64ac13ba77225bc8CAS | 14648877PubMed |

Sakatani, M., Suda, I., Oki, T., Kobayashi, S., Kobayashi, S., and Takahashi, M. (2007). Effects of purple sweet potato anthocyanins on development and intracellular redox status of bovine preimplantation embryos exposed to heat shock. J. Reprod. Dev. 53, 605–614.
Effects of purple sweet potato anthocyanins on development and intracellular redox status of bovine preimplantation embryos exposed to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosVylsLk%3D&md5=654ef37aa594dc5f4702c93aef3ae2aeCAS | 17325453PubMed |

Sakatani, M., Alvarez, N. V., Takahashi, M., and Hansen, P. J. (2012). Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle. J. Dairy Sci. 95, 3080–3091.
Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xntlyrtrc%3D&md5=b1afbdb7a027e7106d298f75a22d416bCAS | 22612944PubMed |

Satrapa, R. A., Razza, E. M., Castilho, A. C., Simões, R. A., Silva, C. F., Nabhan, T., Pegorer, M. F., and Barros, C. M. (2013). Differential expression of IGF family members in heat-stressed embryos produced in vitro from OPU-derived oocytes of Nelore (Bos indicus) and Holstein (Bos taurus) cows. Reprod. Domest. Anim. 48, 1043–1048.
Differential expression of IGF family members in heat-stressed embryos produced in vitro from OPU-derived oocytes of Nelore (Bos indicus) and Holstein (Bos taurus) cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslKnsrvF&md5=2d86c172fb1126267cbc3ac2e7a7caf3CAS | 23889323PubMed |

Silva, C. F., Sartorelli, E. S., Castilho, A. C., Satrapa, R. A., Puelker, R. Z., Razza, E. M., Ticianelli, J. S., Eduardo, H. P., Loureiro, B., and Barros, C. M. (2013). Effects of heat stress on development, quality and survival of Bos indicus and Bos taurus embryos produced in vitro. Theriogenology 79, 351–357.
Effects of heat stress on development, quality and survival of Bos indicus and Bos taurus embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Kqs7zE&md5=37fc7119d5fd4f57c114d8ad12137334CAS | 23154141PubMed |

Soto, P., and Smith, L. C. (2009). BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes. Mol. Reprod. Dev. 76, 637–646.
BH4 peptide derived from Bcl-xL and Bax-inhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVaisL8%3D&md5=d1591e2800a2b414f37ed04420b2a05fCAS | 19062170PubMed |

Srikandakumar, A., and Johnson, E. H. (2004). Effect of heat stress on milk production, rectal temperature, respiratory rate and blood chemistry in Holstein, Jersey and Australian Milking Zebu cows. Trop. Anim. Health Prod. 36, 685–692.
Effect of heat stress on milk production, rectal temperature, respiratory rate and blood chemistry in Holstein, Jersey and Australian Milking Zebu cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crovFGhsQ%3D%3D&md5=805037063cb21d6fa548b9af55525916CAS | 15563029PubMed |

Torres-Júnior, J. R. S., Pires, M. F. A., Sá, W. F., Ferreira, A. M., Viana, J. H., Camargo, L. S., Ramos, A. A., Folhadella, I. M., Polisseni, J., Freitas, C., Clemente, C. A., Sá Filho, M. F., Paula-Lopes, F. F., and Baruselli, P. S. (2008). Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology 69, 155–166.
Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle.Crossref | GoogleScholarGoogle Scholar |

Turner, H. G. (1982). Genetic variation of rectal temperature in cows and its relationship to fertility. Anim. Prod. 35, 401–412.
Genetic variation of rectal temperature in cows and its relationship to fertility.Crossref | GoogleScholarGoogle Scholar |

Vieira, L. M., Rodrigues, C. A., Mendanha, M. F., Sá Filho, M. F., Sales, J. N., Souza, A. H., Santos, J. E., and Baruselli, P. S. (2014). Donor category and seasonal climate associated with embryo production and survival in multiple ovulation and embryo transfer programs in Holstein cattle. Theriogenology 82, 204–212.
Donor category and seasonal climate associated with embryo production and survival in multiple ovulation and embryo transfer programs in Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cnmvFWgtw%3D%3D&md5=63114e7801642710e72bbf88dcfc31c3CAS | 24768006PubMed |

Wang, Y., Huang, J., Xia, P., He, J., Wang, C., Ju, Z., Li, J., Li, R., Zhong, J., and Li, Q. (2013). Genetic variations of HSBP1 gene and its effect on thermal performance traits in Chinese Holstein cattle. Mol. Biol. Rep. 40, 3877–3882.
Genetic variations of HSBP1 gene and its effect on thermal performance traits in Chinese Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntF2jurs%3D&md5=e4ab3e4eb452d762eb43ead6445198d2CAS | 23572288PubMed |

Wijshake, T., Baker, D. J., and van de Sluis, B. (2014). Endonucleases: new tools to edit the mouse genome. Biochim. Biophys. Acta , .
Endonucleases: new tools to edit the mouse genome.Crossref | GoogleScholarGoogle Scholar | 25072958PubMed |

Wolfenson, D., Thatcher, W. W., Badinga, L., Savio, J. D., Meidan, R., Lew, B. J., Braw-Tal, R., and Berman, A. (1995). Effect of heat stress on follicular development during the estrous cycle in lactating dairy cattle. Biol. Reprod. 52, 1106–1113.
Effect of heat stress on follicular development during the estrous cycle in lactating dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXltVCjs74%3D&md5=6d583dfaf75e60fb01836040b561bf41CAS | 7626710PubMed |

Xiong, Q., Chai, J., Xiong, H., Li, W., Huang, T., Liu, Y., Suo, X., Zhang, N., Li, X., Jiang, S., and Chen, M. (2013). Association analysis of HSP70A1A haplotypes with heat tolerance in Chinese Holstein cattle. Cell Stress Chaperones 18, 711–718.
Association analysis of HSP70A1A haplotypes with heat tolerance in Chinese Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsF2gsLjN&md5=dd888a9e1a134cb6183f298c436bda1fCAS | 23543596PubMed |