Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Astaxanthin counteracts the effects of heat shock on the maturation of bovine oocytes

J. Ispada A , T. A. Rodrigues A , P. H. B. Risolia B , R. S. Lima B , D. R. Gonçalves A , D. Rettori A , M. Nichi C , W. B. Feitosa A and F. F. Paula-Lopes A B D
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, Federal University of Sao Paulo, 275 Prof. Artur Riedel Street, Diadema-SP, 09913-030, Brazil.

B Institute of Biosciences, State University of Sao Paulo, Rubião Júnior, S/N, Botucatu-SP, 18618-970, Brazil.

C Department of Animal Reproduction, University of Sao Paulo, 87 Prof. Dr. Orlando Marques de Paiva Avenue, Sao Paulo-SP, 05508-270, Brazil.

D Corresponding author. Email: ffpaulalopes@gmail.com

Reproduction, Fertility and Development 30(9) 1169-1179 https://doi.org/10.1071/RD17271
Submitted: 13 July 2017  Accepted: 31 January 2018   Published: 28 March 2018

Abstract

The cellular mechanisms induced by elevated temperature on oocytes are not fully understood. However, there is evidence that some of the deleterious effects of heat shock are mediated by a heat-induced increase in reactive oxygen species (ROS). In this context, carotenoid antioxidants might have a thermoprotective effect. Therefore, the objective of this study was to determine the role of astaxanthin (AST) on oocyte ROS production and on the redox profile and developmental competency of cumulus-oocyte complexes (COCs) after 14 h heat shock (41°C) during in vitro maturation (IVM). Exposure of oocytes to heat shock during IVM increased ROS and reduced the ability of the oocyte to cleave and develop to the blastocyst stage. However, 12.5 and 25 nM astaxanthin rescued these negative effects of heat shock; astaxanthin counteracted the heat shock-induced increase in ROS and restored oocyte developmental competency. There was no effect of astaxanthin on maturation medium lipid peroxidation or on glutathione peroxidase and catalase activity in oocytes and cumulus cells. However, astaxanthin stimulated superoxide dismutase (SOD) activity in heat-shocked cumulus cells. In conclusion, direct heat shock reduced oocyte competence, which was restored by astaxanthin, possibly through regulation of ROS and SOD activity in oocytes and COCs.

Additional keywords: antioxidant enzymes, cumulus cells, oxidative stress, temperature.


References

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=2335f35aecde7c8be17e65b80d314eabCAS |

Altan, O., Pabuçcuoğlu, A., Altan, A., Konyalioğlu, S., and Bayraktar, H. (2003). Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. Br. Poult. Sci. 44, 545–550.
Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1Gkur0%3D&md5=398f92ad5632a8708f079ecd8fafdfaeCAS |

Aréchiga, C. F., Ealy, A. D., and Hansen, P. J. (1995). Evidence that glutathione is involved in thermotolerance of preimplantation murine embryos. Biol. Reprod. 52, 1296–1301.
Evidence that glutathione is involved in thermotolerance of preimplantation murine embryos.Crossref | GoogleScholarGoogle Scholar |

Ascari, I. J., Alves, N. G., Jasmin, J., Lima, R. R., Quintão, C. C. R., Oberlender, G., Moraes, E. A., and Camargo, L. S. A. (2017). Addition of insulin-like growth factor I to the maturation medium of bovine oocytes subjected to heat shock: effects on the production of reactive oxygen species, mitochondrial activity and oocyte competence. Domest. Anim. Endocrinol. 60, 50–60.
Addition of insulin-like growth factor I to the maturation medium of bovine oocytes subjected to heat shock: effects on the production of reactive oxygen species, mitochondrial activity and oocyte competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXlvVCnurg%3D&md5=b6b97106e5854e862fab3d08ae42b71dCAS |

Augusti, P. R., Quatrin, A., Somacal, S., Conterato, G. M., Sobieski, R., Ruviaro, A. R., Maurer, L. H., Duarte, M. M., Roehrs, M., and Emanuelli, T. (2012). Astaxanthin prevents changes in the activities of thioredoxin reductase and paraoxonase in hypercholesterolemic rabbits. J. Clin. Biochem. Nutr. 51, 42–49.
Astaxanthin prevents changes in the activities of thioredoxin reductase and paraoxonase in hypercholesterolemic rabbits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1WksbbP&md5=5973bf5b96abe62a07598ff461d72447CAS |

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=99af087f755967c3fb5b6fc25ba2f48aCAS |

Bayir, H., Fadeel, B., Palladino, M. J., Witasp, E., Kurnikov, I. V., Tyurina, Y. Y., Tyurin, V. A., Amoscato, A. A., Jiang, J., Kochanek, P. M., DeKosky, S. T., Greenberger, J. S., Shvedova, A. A., and Kagan, V. E. (2006). Apoptotic interactions of cytochrome c: redox flirting with anionic phospholipids within and outside of mitochondria. Biochim. Biophys. Acta 1757, 648–659.
Apoptotic interactions of cytochrome c: redox flirting with anionic phospholipids within and outside of mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmsl2jtLk%3D&md5=a93191f0bb86f8086e09d7c5f145f4b3CAS |

Cardounel, A. J., Dumitrescu, C., Zweier, J. L., and Lockwood, S. F. (2003). Direct superoxide anion scavenging by a disodium disuccinate astaxanthin derivative: relative efficacy of individual stereoisomers versus the statistical mixture of stereoisomers by electron paramagnetic resonance imaging. Biochem. Biophys. Res. Commun. 307, 704–712.
Direct superoxide anion scavenging by a disodium disuccinate astaxanthin derivative: relative efficacy of individual stereoisomers versus the statistical mixture of stereoisomers by electron paramagnetic resonance imaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVCrsb8%3D&md5=cb8b38544d3d4dcd66a3979d1621cae6CAS |

Comhaire, F. H., El Garem, Y., Mahmoud, A., Eertmans, F., and Schoonjans, F. (2005). Combined conventional/antioxidant “Astaxanthin” treatment for male infertility: a double blind, randomized trial. Asian J. Androl. 7, 257–262.
Combined conventional/antioxidant “Astaxanthin” treatment for male infertility: a double blind, randomized trial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFSksL%2FJ&md5=c50bfa5d96f87b9d2423c16a28897c1eCAS |

de Matos, D. G., Furnus, C. C., and Moses, D. F. (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420–1425.
Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvVWktrY%3D&md5=04a7cdddbaf4a197875d02fa3756fcceCAS |

de Matos, D. G., Gasparrini, B., Pasqualini, S. R., and Thompson, J. G. (2002). Effect of glutathione synthesis stimulation during in vitro maturation of ovine oocytes on embryo development and intracellular peroxide content. Theriogenology 57, 1443–1451.
Effect of glutathione synthesis stimulation during in vitro maturation of ovine oocytes on embryo development and intracellular peroxide content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVCnt7c%3D&md5=36945cef293fd168cdec127d2017a3f8CAS |

Di Mascio, P., Kaiser, S., and Sies, H. (1989). Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch. Biochem. Biophys. 274, 532–538.
Lycopene as the most efficient biological carotenoid singlet oxygen quencher.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlvVOjt7c%3D&md5=f5716753b2c2e1dee00464a5ac6eb32eCAS |

Do, L. T., Luu, V. V., Morita, Y., Taniguchi, M., Nii, M., Peter, A. T., and Otoi, T. (2015). Astaxanthin present in the maturation medium reduces negative effects of heat shock on the developmental competence of porcine oocytes. Reprod. Biol. 15, 86–93.
Astaxanthin present in the maturation medium reduces negative effects of heat shock on the developmental competence of porcine oocytes.Crossref | GoogleScholarGoogle Scholar |

Draper, H. H., Csallany, A. S., and Hadley, M. (2000). Urinary aldehydes as indicators of lipid peroxidation in vivo. Free Radic. Biol. Med. 29, 1071–1077.
Urinary aldehydes as indicators of lipid peroxidation in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXot1yhur4%3D&md5=995d8427f9f99650efa0a3a5e0bcfdb4CAS |

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.
Influence of postbreeding thermal stress on conception rate in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3M3hsVCmtA%3D%3D&md5=a38ea2d9e4b5824e8169b70d5b71d7f6CAS |

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=a377404c54c87e5fd47c13ebd2ddc5d5CAS |

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=c0ad863f6e01cafcc700163591266ce8CAS |

Edwards, J. L., Bogart, A. N., Rispoli, L. A., Saxton, A. M., and Schrick, F. N. (2009). Developmental competence of bovine embryos from heat-stressed ova. J. Dairy Sci. 92, 563–570.
Developmental competence of bovine embryos from heat-stressed ova.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1KisrY%3D&md5=e99567b5596047b01a72ff964607cc60CAS |

Fatehi, A. N., Roelen, B. A., Colenbrander, B., Schoevers, E. J., Gadella, B. M., Beverst, M. M., and van den Hurk, R. (2005). Presence of cumulus cells during in vitro fertilization protects the bovine oocyte against oxidative stress and improves first cleavage but does not affect further development. Zygote 13, 177–185.
Presence of cumulus cells during in vitro fertilization protects the bovine oocyte against oxidative stress and improves first cleavage but does not affect further development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtlSisb0%3D&md5=3c6ba5960a25ec5e494935c08e69349eCAS |

Franceschelli, S., Pesce, M., Ferrone, A., De Lutiis, M. A., Patruno, A., Grilli, A., Felaco, M., and Speranza, L. (2014). Astaxanthin treatment confers protection against oxidative stress in U937 cells stimulated with lipopolysaccharide reducing O2− production. PLoS One 9, e88359.
Astaxanthin treatment confers protection against oxidative stress in U937 cells stimulated with lipopolysaccharide reducing O2 production.Crossref | GoogleScholarGoogle Scholar |

Gendelman, M., and Roth, Z. (2012). 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=f88e9252411f5665c400cf781529a22dCAS |

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=dcdaee25ac1118490cffbc3132ba5bc4CAS |

Goto, S., Kogure, K., Abe, K., Kimata, Y., Kitahama, K., Yamashita, E., and Terada, H. (2001). Efficient radical trapping at the surface and inside the phospholipid membrane is responsible for highly potent antiperoxidative activity of the carotenoid astaxanthin. Biochim. Biophys. Acta 1512, 251–258.
Efficient radical trapping at the surface and inside the phospholipid membrane is responsible for highly potent antiperoxidative activity of the carotenoid astaxanthin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt12iurw%3D&md5=9f60ba8635b1842a8065678d4a124338CAS |

Haghighat, N., and Van Winkle, L. J. (1990). Developmental change in follicular cell enhanced amino acid uptake into mouse oocytes that depends on intact gap junctions and transport system Gly. J. Exp. Zool. 253, 71–82.
Developmental change in follicular cell enhanced amino acid uptake into mouse oocytes that depends on intact gap junctions and transport system Gly.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtFKgs7k%3D&md5=e577dff1caf4cbb2dcad6f055be375a3CAS |

Hama, S., Uenishi, S., Yamada, A., Ohgita, T., Tsuchiya, H., Yamashita, E., and Kogure, K. (2012). Scavenging of hydroxyl radicals in aqueous solution by astaxanthin encapsulated in liposomes. Biol. Pharm. Bull. 35, 2238–2242.
Scavenging of hydroxyl radicals in aqueous solution by astaxanthin encapsulated in liposomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1KgtbY%3D&md5=3ece80f9814f38ce3523173b2ebb6e00CAS |

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 |

Harmon, R. J., Lu, M., Trammel, D. S., and Smith, B. A. (1997). Influence of heat stress and calving on antioxidant activity in bovine blood. J. Dairy Sci. 80, 264.

Jackson, H. L., Cardounel, A. J., Zweier, J. L., and Lockwood, S. F. (2004). Synthesis, characterization, and direct aqueous superoxide anion scavenging of a highly water-dispersible astaxanthin–amino acid conjugate. Bioorg. Med. Chem. Lett. 14, 3985–3991.
Synthesis, characterization, and direct aqueous superoxide anion scavenging of a highly water-dispersible astaxanthin–amino acid conjugate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1ehu7k%3D&md5=38d6dc063845e0f82378a54f884099e8CAS |

Jang, H. Y., Ji, S. J., Kim, Y. H., Lee, H. Y., Shin, J. S., Cheong, H. T., Kim, J. T., Park, I. C., Kong, H. S., Park, C. K., and Yang, B. K. (2010). Antioxidative effects of astaxanthin against nitric oxide-induced oxidative stress on cell viability and gene expression in bovine oviduct epithelial cell and the developmental competence of bovine IVM/IVF embryos. Reprod. Domest. Anim. 45, 967–974.
Antioxidative effects of astaxanthin against nitric oxide-induced oxidative stress on cell viability and gene expression in bovine oviduct epithelial cell and the developmental competence of bovine IVM/IVF embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WrsLvE&md5=546c66d5b15d9e45dc52d9501894de00CAS |

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 |

Kanani, B. P., Daneshyar, M., Aliakbarlu, J., and Hamian, F. (2017). Effect of dietary turmeric and cinnamon powders on meat quality and lipid peroxidation of broiler chicken under heat-stress condition. Vet. Res. Forum 8, 163–169.

Karppi, J., Rissanen, T. H., Nyyssönen, K., Kaikkonen, J., Olsson, A. G., Voutilainen, S., and Salonen, J. T. (2007). Effects of astaxanthin supplementation on lipid peroxidation. Int. J. Vitam. Nutr. Res. 77, 3–11.
Effects of astaxanthin supplementation on lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslOgtr0%3D&md5=484481b248c13c4f6202d19528b80a1bCAS |

Khan, I., Lee, K. L., Xu, L., Mesalam, A., Chowdhury, M. M. R., Joo, M. D., Ihsan-ul-Haq, , Mirza, B., and Kong, I. K. (2017). Improvement of in vitro-produced bovine embryo treated with coagulansin-a under heat-stressed condition. Reproduction 153, 421–431.
Improvement of in vitro-produced bovine embryo treated with coagulansin-a under heat-stressed condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtVSltLbM&md5=cbcf1fb2a2be9a19fa1fbfeb0f78d3c6CAS |

Kuroki, T., Ikeda, S., Okada, T., Maoka, T., Kitamura, A., Sugimoto, M., and Kume, S. (2013). Astaxanthin ameliorates heat stress-induced impairment of blastocyst development in vitro:–astaxanthin colocalization with and action on mitochondria. J. Assist. Reprod. Genet. 30, 623–631.
Astaxanthin ameliorates heat stress-induced impairment of blastocyst development in vitro:–astaxanthin colocalization with and action on mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3srgt1Gluw%3D%3D&md5=28fd95bb0be028bfbefd0e650df6855fCAS |

Lee, D. H., Kim, C. S., and Lee, Y. J. (2011). Astaxanthin protects against MPTP/MPP+-induced mitochondrial dysfunction and ROS production in vivo and in vitro. Food Chem. Toxicol. 49, 271–280.
Astaxanthin protects against MPTP/MPP+-induced mitochondrial dysfunction and ROS production in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1agsbfJ&md5=fd87f152ad4f591c9e81e75392445bfdCAS |

Leibfried, L., and First, N. L. (1979). Characterization of bovine follicular oocytes and their ability to mature in vitro. J. Anim. Sci. 48, 76–86.
Characterization of bovine follicular oocytes and their ability to mature in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c%2Fgs1arsA%3D%3D&md5=5a6d19d7a07ed7f00df2a1d8e1f82326CAS |

Li, R., Wu, H., Zhuo, W. W., Mao, Q. F., Lan, H., Zhang, Y., and Hua, S. (2015). Astaxanthin normalizes epigenetic modifications of bovine somatic cell cloned embryos and decreases the generation of lipid peroxidation. Reprod. Domest. Anim. 50, 793–799.
Astaxanthin normalizes epigenetic modifications of bovine somatic cell cloned embryos and decreases the generation of lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFGitbnL&md5=c1a211fda17c7bab3929854a30982894CAS |

Lima, R. S., Risolia, P. H. B., Ispada, J., Assumpção, M. E. O. A., Visintin, J. A., Orlandi, C., and Paula-Lopes, F. F. (2017). Role of insulin-like growth factor 1 on cross-bred Bos indicus cattle germinal vesicle oocytes exposed to heat shock. Reprod. Fertil. Dev. 29, 1405–1414.
Role of insulin-like growth factor 1 on cross-bred Bos indicus cattle germinal vesicle oocytes exposed to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtVCit7fI&md5=9b1a81aa7e606d539ade0e0241e5608eCAS |

Lord-Fontaine, S., and Averill-Bates, D. A. (2002). Heat shock inactivates cellular antioxidant defenses against hydrogen peroxide: protection by glucose. Free Radic. Biol. Med. 32, 752–765.
Heat shock inactivates cellular antioxidant defenses against hydrogen peroxide: protection by glucose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFWnur8%3D&md5=c2a44c441f3ee41571b45c71c067760bCAS |

Malayer, J. R., Hansen, P. J., and Buhi, W. C. (1988). Effect of day of oestrus cycle, side of the reproductive tract and heat shock on in vitro protein secretion by bovine endometrium. J. Reprod. Fertil. 84, 567–578.
Effect of day of oestrus cycle, side of the reproductive tract and heat shock on in vitro protein secretion by bovine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltler&md5=90b248b98b728e650d03b9a676e44647CAS |

Maya-Soriano, M. J., Taberner, E., and López-Béjar, M. (2013). Retinol improves in vitro oocyte nuclear maturation under heat stress in heifers. Zygote 21, 377–384.
Retinol improves in vitro oocyte nuclear maturation under heat stress in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Sis7zJ&md5=9dffaeaade9c6f706c514cb8714ea0bdCAS |

Miki, W., Yamaguchi, K., and Konosu, S. (1982). Comparison of carotenoids in the ovaries of marine fish and shellfish. Comp. Biochem. Physiol. B 71, 7–11.
Comparison of carotenoids in the ovaries of marine fish and shellfish.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL387jslyhsQ%3D%3D&md5=6e1a9599e2044beb27ce62b37cca66a8CAS |

Nabenishi, H., Ohta, H., Nishimoto, T., Morita, T., Ashizawa, K., and Tsuzuki, Y. (2012a). The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote 20, 249–259.
The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVWjsr3M&md5=5947e263f958b370d7a0b899120e16d3CAS |

Nabenishi, H., Takagi, S., Kamata, H., Nishimoto, T., Morita, T., Ashizawa, K., and Tsuzuki, Y. (2012b). 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=393ff70d82da431f5a8c5f82e28557d2CAS |

Namekawa, T., Ikeda, S., Sugimoto, M., and Kume, S. (2010). Effects of astaxanthin-containing oil on development and stress-related gene expression of bovine embryos exposed to heat stress. Reprod. Domest. Anim. 45, e387–e391.
Effects of astaxanthin-containing oil on development and stress-related gene expression of bovine embryos exposed to heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WrsLbE&md5=2eb8c549f2cd74aca2b3414b3178bebeCAS |

Nichi, M., Bols, P. E., Züge, R. M., Barnabe, V. H., Goovaerts, I. G., Barnabe, R. C., and Cortada, C. N. (2006). Seasonal variation in semen quality in Bos indicus and Bos taurus bulls raised under tropical conditions. Theriogenology 66, 822–828.
Seasonal variation in semen quality in Bos indicus and Bos taurus bulls raised under tropical conditions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvltVyhsw%3D%3D&md5=240c836010a16846dc6ab75788772133CAS |

Ozawa, M., Hirabayashi, M., and Kanai, Y. (2002). Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro. Reproduction 124, 683–689.
Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1KksQ%3D%3D&md5=ea60e5c6f95b51ad8a6f163ea51c74e9CAS |

Panasenko, O. M., Sharov, V. S., Briviba, K., and Sies, H. (2000). Interaction of peroxynitrite with carotenoids in human low density lipoproteins. Arch. Biochem. Biophys. 373, 302–305.
Interaction of peroxynitrite with carotenoids in human low density lipoproteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVWj&md5=592186c58bf9e1474cc2087a14c5a8e5CAS |

Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
Capacitation of bovine sperm by heparin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkslWit7g%3D&md5=3ec83c37942901ba3ecae3e2b74f5461CAS |

Paula-Lopes, F. F., Al-Katanani, Y. M., Majewski, A. C., McDowell, L. R., and Hansen, P. J. (2003). Manipulation of antioxidant status fails to improve fertility of lactating cows or survival of heat-shocked embryos. J. Dairy Sci. 86, 2343–2351.
Manipulation of antioxidant status fails to improve fertility of lactating cows or survival of heat-shocked embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltlSrtLo%3D&md5=ede58a068b50e497b7611844032c4630CAS |

Payton, R. R., Romar, R., Coy, P., Sexton, 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=3b0dcf738a2c6ded9b0531ea18a3c56eCAS |

Putney, D. J., Drost, M., and Thatcher, W. W. (1988). Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between Days 1 to 7 post insemination. Theriogenology 30, 195–209.
Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between Days 1 to 7 post insemination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFahug%3D%3D&md5=15f7889a5b843dc120fc4ec9714df953CAS |

Rispoli, L. A., Payton, R. R., Gondro, C., Saxton, A. M., Nagle, K. A., Jenkins, B. W., Schrick, F. N., and Edwards, J. L. (2013). Heat stress effects on the cumulus cells surrounding the bovine oocyte during maturation: altered matrix metallopeptidase 9 and progesterone production. Reproduction 146, 193–207.
Heat stress effects on the cumulus cells surrounding the bovine oocyte during maturation: altered matrix metallopeptidase 9 and progesterone production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlSnsb%2FN&md5=11a6f046d8d73f56e8c29b471d46544cCAS |

Rocha, A., Randel, R. D., Broussard, J. R., Lim, J. M., Blair, R. M., Roussel, J. D., Godke, R. A., and Hansel, W. (1998). High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows. Theriogenology 49, 657–665.
High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1GqsQ%3D%3D&md5=0bb2c146629f01ea205672b008acbf19CAS |

Rodrigues, T. A., Ispada, J., Risolia, P. H., Rodrigues, M. T., Lima, R. S., Assumpção, M. E., Visintin, J. A., and Paula-Lopes, F. F. (2016). Thermoprotective effect of insulin-like growth factor 1 on in vitro-matured bovine oocyte exposed to heat shock. Theriogenology 86, 2028–2039.
Thermoprotective effect of insulin-like growth factor 1 on in vitro-matured bovine oocyte exposed to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1egtrzO&md5=818b64d699625262e4d6994e857813deCAS |

Roman-Ponce, H., Thatcher, W. W., Canton, D., Barron, D. H., and Wolcox, C. J. (1978). Thermal stress effects on uterine blood flow in dairy cows. J. Anim. Sci. 46, 175–180.
Thermal stress effects on uterine blood flow in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtFyltrg%3D&md5=e0ff7e502f0a7ba0dc809bd019ce9ed1CAS |

Roth, Z., and Hansen, P. J. (2004). Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71, 1898–1906.
Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsrzL&md5=ac04f132e9f6b4d743fb6adbb559a74bCAS |

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=dbcad9b49b528988d1d762c76ec81310CAS |

Roth, Z., Meidan, R., Braw-tal, R., and Wolfenson, D. (2000). Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J. Reprod. Fertil. 120, 83–90.
| 1:CAS:528:DC%2BD3cXntlCiurs%3D&md5=64fd1ed3f344daaf7bfac3c95a3ebc9fCAS |

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=ae651517631f27f5cbeb21c9d5a0190cCAS |

Sakatani, M., Yamanaka, K., Kobayashi, S., and Takahashi, M. (2008). Heat shock-derived reactive oxygen species induce embryonic mortality in in vitro early stage bovine embryos. J. Reprod. Dev. 54, 496–501.
Heat shock-derived reactive oxygen species induce embryonic mortality in in vitro early stage bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhslOlur0%3D&md5=45f4b8c0015798cc10f6fb621e8e2eddCAS |

Sakatani, M., Balboula, A. Z., Yamanaka, K., and Takahashi, M. (2012). Effect of summer heat environment on body temperature, estrous cycles and blood antioxidant levels in Japanese Black cow. Anim. Sci. J. 83, 394–402.
Effect of summer heat environment on body temperature, estrous cycles and blood antioxidant levels in Japanese Black cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2ju77E&md5=f45097687fbc42d9d77fc4369e47a3a9CAS |

Skibba, J. L., and Collins, F. G. (1978). Effect of temperature on biochemical functions in the isolated perfused rat liver. J. Surg. Res. 24, 435–441.
Effect of temperature on biochemical functions in the isolated perfused rat liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXkslenu7k%3D&md5=df5e58c440e34b77c7c5b9103a688478CAS |

Skibba, J. L., and Stadnicka, A. (1986). Xanthine oxidase (XO) activity at hyperthermic temperatures as a source of free radicals. Proc. Am. Assoc. Cancer Res. 27, 400.

Skibba, J. L., Quebbman, E. J., and Kalbfleisch, J. H. (1986). Nitrogen metabolism and lipid peroxidation during hyperthermic perfusion of human livers with cancers. Cancer Res. 46, 6000–6003.
| 1:CAS:528:DyaL28Xmt1ekt7k%3D&md5=bdc36dc1240e2224e90dba178cdf2b77CAS |

Skibba, J. L., Stadnicka, A., Kalbfleisch, J. H., and Powers, R. H. (1989). Effects of hyperthermia on xanthine oxidase activity and glutathione levels in the perfused rat liver. J. Biochem. Toxicol. 4, 119–125.
Effects of hyperthermia on xanthine oxidase activity and glutathione levels in the perfused rat liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlsFyn&md5=a0ab8e489fa87d236ecd64d30de03bc8CAS |

Speranza, L., Pesce, M., Patruno, A., Franceschelli, S., de Lutiis, M. A., Grilli, A., and Felaco, M. (2012). Astaxanthin treatment reduced oxidative-induced pro-inflammatory cytokines secretion in U937: SHP-1 as a novel biological target. Mar. Drugs 10, 890–899.
Astaxanthin treatment reduced oxidative-induced pro-inflammatory cytokines secretion in U937: SHP-1 as a novel biological target.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmtlalsrw%3D&md5=637f6fcef36e65de3b15f158e3c1dd60CAS |

Stahl, W., and Sies, H. (2005). Bioactivity and protective effects of natural carotenoids. Biochim. Biophys. Acta 1740, 101–107.
Bioactivity and protective effects of natural carotenoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFCrsb8%3D&md5=be56b129ccf0f96ab7312db27c0abeffCAS |

Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and develop- mental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and develop- mental capacity after in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKjtrk%3D&md5=b8e5c3a1cfbd7b13c2b27ee048e40c4aCAS |

Tanghe, S., Van Soom, A., Nauwynck, H., Coryn, M., and de Kruif, A. (2002). Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation and fertilization. Mol. Reprod. Dev. 61, 414–424.
Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFCgtbk%3D&md5=3b8fa73c4ab1b6f62c8983eeb1c5d187CAS |

Tarazona, A. M., Rodríguez, J. I., Restrepo, L. F., and Olivera-Angel, M. (2006). Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro. Reprod. Domest. Anim. 41, 5–11.
Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28%2FjsVWnuw%3D%3D&md5=9f6f371a402d5c7f326181cd1ec52319CAS |

Tatemoto, H., Sakurai, N., and Muto, N. (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805–810.
Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFCiu78%3D&md5=70d3fff1bf2f22e1397282bb17316a76CAS |

Ticianelli, J. S., Emanuelli, I. P., Satrapa, R. A., Castilho, A. C., Loureiro, B., Sudano, M. J., Fontes, P. K., Pinto, R. F., Razza, E. M., Surjus, R. S., Sartori, R., Assumpção, M. E., Visintin, J. A., Barros, C. M., and Paula-Lopes, F. F. (2017). Gene expression profile in heat-shocked Holstein and Nelore oocytes and cumulus cells. Reprod. Fertil. Dev. 29, 1787–1802.
Gene expression profile in heat-shocked Holstein and Nelore oocytes and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtlSkurvN&md5=65f1cbbd4d57373cec19cc3cd9497436CAS |

Wang, L., Wang, D., Zou, X., and Xu, C. (2009). Mitochondrial functions on oocytes and preimplantation embryos. J. Zhejiang Univ. Sci. B 10, 483–492.
Mitochondrial functions on oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotV2qtbo%3D&md5=4aa8fbeb8410a8ae6373a3c68967cb3dCAS |

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=d3ded12a1b27c912986d4fbf91d3f31cCAS |

Xu, J., Rong, S., Gao, H., Chen, C., Yang, W., Deng, Q., Huang, Q., Xiao, L., and Huang, F. (2017). A combination of flaxseed oil and astaxanthin improves hepatic lipid accumulation and reduces oxidative stress in high fat-diet fed rats. Nutrients 9, 271–284.
A combination of flaxseed oil and astaxanthin improves hepatic lipid accumulation and reduces oxidative stress in high fat-diet fed rats.Crossref | GoogleScholarGoogle Scholar |

Xuan, R. R., Niu, T. T., and Chen, H. M. (2016). Astaxanthin blocks preeclampsia progression by suppressing oxidative stress and inflammation. Mol. Med. Rep. 14, 2697–2704.
Astaxanthin blocks preeclampsia progression by suppressing oxidative stress and inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvFSjtbjN&md5=71ce54e6c95ff8af4ab51bb4065f424fCAS |

Young, A. J., and Lowe, G. M. (2001). Antioxidant and pro-oxidant properties of carotenoids. Arch. Biochem. Biophys. 385, 20–27.
Antioxidant and pro-oxidant properties of carotenoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovFyjs7g%3D&md5=da03eea8b74ba54daf25c52350b022ffCAS |