Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH FRONT

Role of oxidant–antioxidant balance in reproduction of domestic animals

Saranika Talukder A , Kendra L. Kerrisk A , Gianfranco Gabai B and Pietro Celi C D E
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Science, The University of Sydney, Camden, NSW 2570, Australia.

B Dipartimento di Biomedicina Comparata e Alimentazione, Università di Padova, Italy.

C DSM Nutritional Products, Columbia, MD 21163, USA.

D Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Vic. 3010, Australia.

E Corresponding author. Email: pietro.celi@dsm.com

Animal Production Science 57(8) 1588-1597 https://doi.org/10.1071/AN15619
Submitted: 16 September 2015  Accepted: 26 February 2017   Published: 5 April 2017

Abstract

Reproductive process leads to dynamic changes in metabolism and energy consumption, which may be responsible for the excessive production of free radicals (oxidants) that are generated during the physiological process of oxygen consumption. As the ovary is a metabolically active organ, it produces oxidants. Growing follicles, granulose cells of Graffian follicles and ovulated follicles all produce both enzymatic and non-enzymatic antioxidants to preserve themselves from the oxidative damage of oxidants. Oxidants and antioxidants are involved in several reproductive functions such as the regulation of follicular fluid environment, folliculogenesis, steroidogenesis, corpus luteum function, and luteolysis. In this article, the currently available literature is reviewed in relation to the roles of oxidants and oxidative stress in both normal and abnormal reproductive physiological processes.

Additional keywords: antioxidants, female reproduction, ovulation, oxidative stress.


References

Agarwal A, Gupta S, Sharma R (2005) Role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology 3, 28
Role of oxidative stress in female reproduction.Crossref | GoogleScholarGoogle Scholar |

Al-Gubory KH, Solari A, Mirman B (1999) Effects of luteectomy on the maintenance of pregnancy, circulating progesterone concentrations and lambing performance in sheep. Reproduction, Fertility and Development 11, 317–322.
Effects of luteectomy on the maintenance of pregnancy, circulating progesterone concentrations and lambing performance in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVSltr8%3D&md5=7b5443d23019680c9a5b844000c9fa54CAS |

Al-Gubory KH, Bolifraud P, Germain G, Nicole A, Ceballos-Picot I (2004) Antioxidant enzymatic defence systems in sheep corpus luteum throughout pregnancy. Reproduction (Cambridge, England) 128, 767–774.
Antioxidant enzymatic defence systems in sheep corpus luteum throughout pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFSrsw%3D%3D&md5=9e78b5e6e8b256371f983281d058d133CAS |

Al-Gubory KH, Fowler PA, Garrel C (2010) The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. The International Journal of Biochemistry & Cell Biology 42, 1634–1650.
The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrtb7L&md5=37484623d3fe4933a912198b1fdeee86CAS |

Al-Gubory KH, Garrel C, Faure P, Sugino N (2012) Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress. Reproductive Biomedicine Online 25, 551–560.
Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2jtbjI&md5=ee36c9f42682ed1836076a4dc0953c63CAS |

Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecology Letters 7, 363–368.
Increased susceptibility to oxidative stress as a proximate cost of reproduction.Crossref | GoogleScholarGoogle Scholar |

Aréchiga CF, Staples CR, McDowell LR, Hansen PJ (1998) Effects of timed insemination and supplemental beta-carotene on reproduction and milk yield of dairy cows under heat stress. Journal of Dairy Science 81, 390–402.
Effects of timed insemination and supplemental beta-carotene on reproduction and milk yield of dairy cows under heat stress.Crossref | GoogleScholarGoogle Scholar |

Arikan S, Dildar K, Arikan Ç, Akçay T, Davas I (2001) Lipid peroxidation and antioxidant status in maternal and cord blood. Gynecologic and Obstetric Investigation 51, 145–149.
Lipid peroxidation and antioxidant status in maternal and cord blood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Wisbs%3D&md5=a18b8018b7acf4c7c7135362218fe02dCAS |

Aurousseau B, Gruffat D, Durand D (2006) Gestation linked radical oxygen species fluxes and vitamins and trace mineral deficiencies in the ruminant. Reproduction, Nutrition, Development 46, 601–620.
Gestation linked radical oxygen species fluxes and vitamins and trace mineral deficiencies in the ruminant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SjsLc%3D&md5=b5991b44ffb5095820ae60a6e9909ce4CAS |

Behrman HR, Kodaman PH, Preston SL, Gao S (2001) Oxidative stress and the ovary. Journal of the Society for Gynecologic Investigation 8, S40–S42.
Oxidative stress and the ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXht1OqsbY%3D&md5=dc225745ba4b9e01a29eb142721a4b50CAS |

Bordignon M, Da Dalt L, Marinelli L, Gabai G (2014) Advanced oxidation protein products are generated by bovine neutrophils and inhibit free radical production in vitro. Veterinary Journal 199, 162–168.
Advanced oxidation protein products are generated by bovine neutrophils and inhibit free radical production in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2gt7%2FJ&md5=6fe6661e671bc28724fbffb27776ad4dCAS |

Brännström M, Mayrhofer G, Robertson SA (1993) Localization of leukocyte subsets in the rat ovary during the periovulatory period. Biology of Reproduction 48, 277–286.
Localization of leukocyte subsets in the rat ovary during the periovulatory period.Crossref | GoogleScholarGoogle Scholar |

Bučević-Popović V, Delaš I, Međugorac S, Pavela-Vrančić M, Kulišić-Bilušić T (2014) Oxidative stability and antioxidant activity of bovine, caprine, ovine and asinine milk. International Journal of Dairy Technology 67, 394–401.
Oxidative stability and antioxidant activity of bovine, caprine, ovine and asinine milk.Crossref | GoogleScholarGoogle Scholar |

Castillo C, Hernandez J, Bravo A, Lopez-Alonso M, Pereira V, Benedito JL (2005) Oxidative status during late pregnancy and early lactation in dairy cows. Veterinary Journal 169, 286–292.
Oxidative status during late pregnancy and early lactation in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVOitr0%3D&md5=47c92bab05ddd3c9c27ebe0c729bde0fCAS |

Celi P (2010) The role of oxidative stress in small ruminants’ health and production. Revista Brasileira de Zootecnia 39, 348–363.
The role of oxidative stress in small ruminants’ health and production.Crossref | GoogleScholarGoogle Scholar |

Celi P (2011a) Biomarkers of oxidative stress in ruminant medicine. Immunopharmacology and Immunotoxicology 33, 233–240.
Biomarkers of oxidative stress in ruminant medicine.Crossref | GoogleScholarGoogle Scholar |

Celi P (2011b) Oxidative stress in ruminants. In ‘Studies on veterinary medicine. Vol. 5’. (Eds L Mandelker, P Vajdovich) pp. 191–231. (Humana Press: Totowa, NJ)

Celi P, Gabai G (2015) Oxidant/antioxidant balance in animal nutrition and health: the role of protein oxidation. Frontiers in Veterinary Science 2, 48
Oxidant/antioxidant balance in animal nutrition and health: the role of protein oxidation.Crossref | GoogleScholarGoogle Scholar |

Celi P, Merlo M, Da Dalt L, Stefani A, Barbato O, Gabai G (2011) Relationship between late embryonic mortality and the increase in plasma advanced oxidised protein products (AOPP) in dairy cows. Reproduction, Fertility and Development 23, 527–533.
Relationship between late embryonic mortality and the increase in plasma advanced oxidised protein products (AOPP) in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFKnsL0%3D&md5=77f4e498fffb0b46d2361364b7081720CAS |

Celi P, Merlo M, Barbato O, Gabai G (2012) Relationship between oxidative stress and the success of artificial insemination in dairy cows in a pasture-based system. Veterinary Journal 193, 498–502.
Relationship between oxidative stress and the success of artificial insemination in dairy cows in a pasture-based system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvVektL4%3D&md5=e29acc55b93c3104ab809726db6a048fCAS |

Chauhan SS, Celi P, Ponnampalam EN, Leury BJ, Liu F, Dunshea FR (2014) Antioxidant dynamics in the live animal and implications for ruminant health and product (meat/milk) quality: role of vitamin E and selenium. Animal Production Science 54, 1525–1536.
Antioxidant dynamics in the live animal and implications for ruminant health and product (meat/milk) quality: role of vitamin E and selenium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVWjtrbL&md5=b9977004cc73a78a87ee5fd618e155f0CAS |

Chew BP, Holpuch DM, O’Fallon JV (1984) Vitamin A and beta-carotene in bovine and porcine plasma, liver, corpora lutea and follicular fluid. Journal of Dairy Science 67, 1316–1322.
Vitamin A and beta-carotene in bovine and porcine plasma, liver, corpora lutea and follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXksFagsr4%3D&md5=2ca0a024716e727af68f25e0d3b07feeCAS |

Cook J (2009) Understanding conception rates in dairy herds. In Practice 31, 262–266.
Understanding conception rates in dairy herds.Crossref | GoogleScholarGoogle Scholar |

Covarrubias L, Hernández-García D, Schnabel D, Salas-Vidal E, Castro-Obregón S (2008) Function of reactive oxygen species during animal development: passive or active? Developmental Biology 320, 1–11.
Function of reactive oxygen species during animal development: passive or active?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVCgtbY%3D&md5=72b546253f018879e8f68758738a1878CAS |

Espey L (1980) Ovulation as an inflammatory reaction: a hypothesis. Biology of Reproduction 22, 73–106.
Ovulation as an inflammatory reaction: a hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsVCnsbs%3D&md5=611654044712240cfcddadf064605b0dCAS |

Fox PF, Kelly AL (2006) Indigenous enzymes in milk: overview and historical aspects, Part 1. International Dairy Journal 16, 500–516.
Indigenous enzymes in milk: overview and historical aspects, Part 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFGht70%3D&md5=20b114d64be997507222e1432f9973a9CAS |

Fujii J, Iuchi Y, Okada F (2005) Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reproductive Biology and Endocrinology 3, 43
Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system.Crossref | GoogleScholarGoogle Scholar |

Garrel C, Fowler PA, Al-Gubory KH (2010) Developmental changes in antioxidant enzymatic defences against oxidative stress in sheep placentomes. The Journal of Endocrinology 205, 107–116.
Developmental changes in antioxidant enzymatic defences against oxidative stress in sheep placentomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFGqtrs%3D&md5=a4d54a1bcd9cfe8a578c4e44279fe187CAS |

Gillis EH, Gosling JP, Sreenan JM, Kane M (2002) Development and validation of a biosensor-based immunoassay for progesterone in bovine milk. Journal of Immunological Methods 267, 131–138.
Development and validation of a biosensor-based immunoassay for progesterone in bovine milk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVWnt7o%3D&md5=6fba7d5fd3226b3b728aaada30df7acbCAS |

Graves-Hoagland RL, Hoagland TA, Woody CO (1988) Effect of beta-carotene and vitamin A on progesterone production by bovine luteal cells. Journal of Dairy Science 71, 1058–1062.
Effect of beta-carotene and vitamin A on progesterone production by bovine luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktlOjs78%3D&md5=c26d3c7fc841fddece1c07e6f2b1fc1cCAS |

Guérin P, El Mouatassim S, Ménézo Y (2001) Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Human Reproduction Update 7, 175–189.
Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings.Crossref | GoogleScholarGoogle Scholar |

Hitchler MJ, Domann FE (2014) Regulation of CuZnSOD and its redox signalling potential: implications for amyotrophic lateral sclerosis. Antioxidants & Redox Signalling 20, 1590–1598.
Regulation of CuZnSOD and its redox signalling potential: implications for amyotrophic lateral sclerosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsFCrt7c%3D&md5=4b0859d4167a1fd97e833b869b4c5d8fCAS |

Inaba T, Mezan M, Shimizu R, Nakano Y, Mori J (1986) Plasma concentration of beta-carotene and vitamin A in cows with ovarian cysts. Japanese Journal of Veterinary Science 48, 1275–1278.

Johansson B, Persson Waller K, Jensen SK, Lindqvist H, Nadeau E (2014) Status of vitamins E and A and beta-carotene and health in organic dairy cows fed a diet without synthetic vitamins. Journal of Dairy Science 97, 1682–1692.
Status of vitamins E and A and beta-carotene and health in organic dairy cows fed a diet without synthetic vitamins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXis1GjtLk%3D&md5=0349c00d4a293c362d7b30afd6a158f9CAS |

Kankofer M, Albera E, Feldman M, Gundling N, Hoedemaker M (2010) Comparison of antioxidative/oxidative profiles in blood plasma of cows with and without retained fetal placental membranes. Theriogenology 74, 1385–1395.
Comparison of antioxidative/oxidative profiles in blood plasma of cows with and without retained fetal placental membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Cls77F&md5=7c2581c532be4258f51423ff4071c5e7CAS |

Kawaguchi S, Sakumoto R, Okuda K (2013a) Induction of the expression of antioxidant enzymes by luteinizing hormone in the bovine corpus luteum. The Journal of Reproduction and Development 59, 219–224.
Induction of the expression of antioxidant enzymes by luteinizing hormone in the bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtF2is73J&md5=7482678e32d3125c49152bb7f1358d98CAS |

Kawaguchi S, Bowolaksono A, Sakumoto R, Okuda K (2013b) Luteoprotective roles of luteinizing hormone are mediated by not only progesterone production but also glucocorticoid conversion in bovine corpus luteum. Molecular Reproduction and Development 80, 204–211.
Luteoprotective roles of luteinizing hormone are mediated by not only progesterone production but also glucocorticoid conversion in bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslWqu78%3D&md5=f7e05ddf3bfba32e7692fc84fdae84e8CAS |

Kawaguchi S, Bowolaksono A, Yoshioka S, Sakumoto R, Okuda K (2013c) Luteoprotective mechanisms of prostaglandin F2α stimulated by luteinizing hormone in the bovine corpus luteum. The Journal of Reproduction and Development 59, 225–230.
Luteoprotective mechanisms of prostaglandin F2α stimulated by luteinizing hormone in the bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtF2is73L&md5=f168eb3ee0d6721f14b5cd1482f69d27CAS |

Kawashima C, Kida K, Schweigert FJ, Miyamoto A (2009) Relationship between plasma beta-carotene concentrations during the peripartum period and ovulation in the first follicular wave postpartum in dairy cows. Animal Reproduction Science 111, 105–111.
Relationship between plasma beta-carotene concentrations during the peripartum period and ovulation in the first follicular wave postpartum in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCgs7%2FK&md5=23338c35ba7ed024d4cc9a994af13461CAS |

Kawashima C, Nagashima S, Sawada K, Schweigert FJ, Miyamoto A, Kida K (2010) Effect of beta-carotene supply during close-up dry period on the onset of first postpartum luteal activity in dairy cows. Reproduction in Domestic Animals 45, e282–e287.

Korbecki J, Baranowska-Bosiacka I, Gutowska I, Chlubek D (2013) The effect of reactive oxygen species on the synthesis of prostanoids from arachidonic acid. Journal of Physiology and Pharmacology 64, 409–421.

Lean IJ, DeGaris PJ, Celi P, McNeill DM, Rodney RM, Fraser DR (2014) Influencing the future: energy, protein and calcium influences during late gestation. Animal Production Science 54, 1177–1189.

Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A (2005) Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485–495.
Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=810f9d37288f5abe314ba521172a7facCAS |

Lista G, Castoldi F, Compagnoni G, Maggioni C, Cornélissen G, Halberg F (2009) Neonatal and maternal concentrations of hydroxil radical and total antioxidant system: protective role of placenta against fetal oxidative stress. Neuroendocrinology Letters 31, 319–324.

Lotthammer KH (1979) Importance of beta-carotene for the fertility of dairy cattle. Feedstuffs 51, 37–38.

Maedomari N, Kikuchi K, Ozawa M, Noguchi J, Kaneko H, Ohnuma K, Nakai M, Shino M, Nagai T, Kashiwazaki N (2007) Cytoplasmic glutathione regulated by cumulus cells during porcine oocyte maturation affects fertilization and embryonic development in vitro. Theriogenology 67, 983–993.
Cytoplasmic glutathione regulated by cumulus cells during porcine oocyte maturation affects fertilization and embryonic development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitFOns70%3D&md5=e4b521da8393887ba2562ed5b4b26524CAS |

Miszkiel G, Skarzynski D, Bogacki M, Kotwica J (1999) Concentrations of catecholamines, ascorbic acid, progesterone and oxytocin in the corpora lutea of cyclic and pregnant cattle. Reproduction, Nutrition, Development 39, 509–516.
Concentrations of catecholamines, ascorbic acid, progesterone and oxytocin in the corpora lutea of cyclic and pregnant cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsFeksb4%3D&md5=bf5224178fed697c1a37f98bfbeb7dc8CAS |

Miyazaki T, Sueoka K, Dharmarajan AM, Atlas SJ, Bulkley GB, Wallach EE (1991) Effect of inhibition of oxygen free radical on ovulation and progesterone production by the in-vitro perfused rabbit ovary. Journal of Reproduction and Fertility 91, 207–212.
Effect of inhibition of oxygen free radical on ovulation and progesterone production by the in-vitro perfused rabbit ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXksVaiu70%3D&md5=8d8966c194e956c165db251c8fb54966CAS |

Mori T, Amano T, Shimizu H (2000) Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biology of Reproduction 62, 913–919.
Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFajt7k%3D&md5=167adf81594d72337f77f1a247a8b439CAS |

Myatt L, Cui X (2004) Oxidative stress in the placenta. Histochemistry and Cell Biology 122, 369–382.
Oxidative stress in the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXoslGit7g%3D&md5=f466f236527c8c71316cac1463e42544CAS |

Nilsson JA (2002) Metabolic consequences of hard work. Proceedings. Biological Sciences 269, 1735–1739.
Metabolic consequences of hard work.Crossref | GoogleScholarGoogle Scholar |

Noda Y, Ota K, Shirasawa T, Shimizu T (2012) Copper/zinc superoxide dismutase insufficiency impairs progesterone secretion and fertility in female mice. Biology of Reproduction 86, 1–8.
Copper/zinc superoxide dismutase insufficiency impairs progesterone secretion and fertility in female mice.Crossref | GoogleScholarGoogle Scholar |

Nordéus K, Båge R, Gustafsson H, Humblot P, Söderquist L (2012) The influence of oestrous substances on cyclicity and oestrous behaviour in dairy heifers. Acta Veterinaria Scandinavica 54, 26
The influence of oestrous substances on cyclicity and oestrous behaviour in dairy heifers.Crossref | GoogleScholarGoogle Scholar |

Okuda K, Korzekwa A, Shibaya M, Murakami S, Nishimura R, Tsubouchi M, Woclawek-Potocka I, Skarzynski DJ (2004) Progesterone is a suppressor of apoptosis in bovine luteal cells. Biology of Reproduction 71, 2065–2071.
Progesterone is a suppressor of apoptosis in bovine luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsrrE&md5=e03d4286e9075bade3f092f4e85b1f24CAS |

Oliveira RC, Guerreiro BM, Morais NN, Araujo RL, Pereira RA, Pereira MN (2015) Supplementation of prepartum dairy cows with beta-carotene. Journal of Dairy Science 98, 6304–6314.
Supplementation of prepartum dairy cows with beta-carotene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFOktbzO&md5=b1ceb101012dbc26c62c58df808e8c7bCAS |

Pandey AN, Tripathi A, PremKumar KV, Shrivastav TG, Chaube SK (2010) Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes. Journal of Cellular Biochemistry 111, 521–528.
Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtleqs7zI&md5=ee4b368c5815efeb5d302011d677c6bfCAS |

Pedernera M, Celi P, García SC, Salvin HE, Barchia I, Fulkerson WJ (2010) Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. Veterinary Journal 186, 352–357.
Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFWqtrbN&md5=55673488d463de283c36a9f653f38c3aCAS |

Pham-Huy LA, He H, Pham-Huy C (2008) Free radicals, antioxidants in disease and health. International Journal of Biomedical Science; IJBS 4, 89–96.

Przybylska J, Albera E, Kankofer M (2007) Antioxidants in bovine colostrum. Reproduction in Domestic Animals 42, 402–409.
Antioxidants in bovine colostrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptlKns7o%3D&md5=ae9f109b75bafcc14a7b37fd6a1fbca7CAS |

Ramos R, Oliveira M, Izaguirry A, Vargas L, Soares M, Mesquita F, Santos F, Binelli M (2015) The periovulatory endocrine milieu affects the uterine redox environment in beef cows. Reproductive Biology and Endocrinology 13, 39
The periovulatory endocrine milieu affects the uterine redox environment in beef cows.Crossref | GoogleScholarGoogle Scholar |

Rapoport R, Sklan D, Wolfenson D, Shaham-Albalancy A, Hanukoglu I (1998) Antioxidant capacity is correlated with steroidogenic status of the corpus luteum during the bovine estrous cycle. Biochimica et Biophysica Acta 1380, 133–140.
Antioxidant capacity is correlated with steroidogenic status of the corpus luteum during the bovine estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhsFaqurg%3D&md5=b9eae5d0b06ee477c8f6286f372836d7CAS |

Rizzo A, Minoia G, Trisolini C, Manca R, Sciorsci RL (2007) Concentrations of free radicals and beta-endorphins in repeat breeder cows. Animal Reproduction Science 100, 257–263.
Concentrations of free radicals and beta-endorphins in repeat breeder cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVOrt74%3D&md5=25def8246f22f9baa9e36f1898de9adcCAS |

Rizzo A, Minoia G, Trisolini C, Mutinati M, Spedicato M, Jirillo F, Sciorsci RL (2009) Reactive oxygen species (ROS): involvement in bovine follicular cysts etiopathogenesis. Immunopharmacology and Immunotoxicology 31, 631–635.
Reactive oxygen species (ROS): involvement in bovine follicular cysts etiopathogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlekt7bK&md5=49fd25c53585a67957d5c75b80f4a6f5CAS |

Rizzo A, Roscino MT, Binetti F, Sciorsci RL (2012) Roles of reactive oxygen species in female reproduction. Reproduction in Domestic Animals 47, 344–352.
Roles of reactive oxygen species in female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtlOktb8%3D&md5=e826f94772f83678c5d0241fdf9902bfCAS |

Sasaki J, Nomura T, Mori H, Watanabe S, Kanda S, Sato E, Inoue M, Watanabe H, Utsumi K (1994) Detection of manganese superoxide dismutase mRNA in the theca interna cells of rat ovary during the ovulatory process by in situ hybridization. Histochemistry 102, 173–176.
Detection of manganese superoxide dismutase mRNA in the theca interna cells of rat ovary during the ovulatory process by in situ hybridization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsVOgt7c%3D&md5=38215a718f1ba05f0a7b9e307ade377eCAS |

Sato EF, Kobuchi H, Edashige K, Takahashi M, Yoshioka T, Utsumi K, Inoue M (1992) Dynamic aspects of ovarian superoxide dismutase isozymes during the ovulatory process in the rat. FEBS Letters 303, 121–125.
Dynamic aspects of ovarian superoxide dismutase isozymes during the ovulatory process in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVGns7g%3D&md5=1bde16babff74cc06218a6b61e6e0c03CAS |

Sawada M, Carlson JC (1996) Intracellular regulation of progesterone secretion by the superoxide radical in the rat corpus luteum. Endocrinology 137, 1580–1584.

Schweigert FJ (2003) Changes in the concentration of β-carotene, alpha-tocopherol and retinal in the bovine corpusluteum during the ovarian cycle. Archives of Animal Nutrition 57, 307–310.
Changes in the concentration of β-carotene, alpha-tocopherol and retinal in the bovine corpusluteum during the ovarian cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotF2qu7c%3D&md5=fdc5cd72f413cf0e896f64a9ce412d46CAS |

Shirai F, Kawaguchi M, Yutsudo M, Dohi Y (2002) Human peripheral blood polymorphonuclear leukocytes at the ovulatory period are in an activated state. Molecular and Cellular Endocrinology 196, 21–28.
Human peripheral blood polymorphonuclear leukocytes at the ovulatory period are in an activated state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVOmsLY%3D&md5=c60cb52b56935175f2b7e3c4b8053c3eCAS |

Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N (2011) Reactive oxygen species are indispensable in ovulation. Proceedings of the National Academy of Sciences, USA 108, 1462–1467.
Reactive oxygen species are indispensable in ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Smt74%3D&md5=1ccabd7d5f77ed2dbedfda05128c07a8CAS |

Silanikove N, Merin U, Leitner G (2006) Physiological role of indigenous milk enzymes: an overview of an evolving picture. International Dairy Journal 16, 533–545.
Physiological role of indigenous milk enzymes: an overview of an evolving picture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFGht7g%3D&md5=847da5ea30b102b29e4ec7aa44e3c6f5CAS |

Skarzynski DJ, Okuda K (2010) Inter- and intra-cellular mechanisms of prostaglandin F2alpha action during corpus luteum regression in cattle. Society of Reproduction and Fertility 67, 305–324.

Skarzynski DJ, Ferreira-Dias G, Okuda K (2008) Regulation of luteal function and corpus luteum regression in cows: hormonal control, immune mechanisms and intercellular communication. Reproduction in Domestic Animals 43, 57–65.
Regulation of luteal function and corpus luteum regression in cows: hormonal control, immune mechanisms and intercellular communication.Crossref | GoogleScholarGoogle Scholar |

Sridhar MG, Setia S, John M, Bhat V, Nandeesha H, Sathiyapriya V (2007) Oxidative stress varies with the mode of delivery in intrauterine growth retardation: association with Apgar score. Clinical Biochemistry 40, 688–691.
Oxidative stress varies with the mode of delivery in intrauterine growth retardation: association with Apgar score.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtVGrt78%3D&md5=57524eccbd3ad767a2e9f2c7b73f272cCAS |

Sugino N (2005) Reactive oxygen species in ovarian physiology. Reproductive Medicine and Biology 4, 31–44.

Sugino N (2006) Roles of reactive oxygen species in the corpus luteum. Animal Science Journal 77, 556–565.
Roles of reactive oxygen species in the corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Gjsbs%3D&md5=ff32284912cfab5b534754832f7b7ff9CAS |

Sugino N, Telleria CM, Gibori G (1998) Differential regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase in the rat corpus luteum: induction of manganese superoxide dismutase messenger ribonucleic acid by inflammatory cytokines. Biology of Reproduction 59, 208–215.
Differential regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase in the rat corpus luteum: induction of manganese superoxide dismutase messenger ribonucleic acid by inflammatory cytokines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFakt78%3D&md5=2358830d2215c0cd1f69a3eaa0ad84efCAS |

Suzuki T, Sugino N, Fukaya T, Sugiyama S, Uda T, Takaya R, Yajima A, Sasano H (1999) Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertility and Sterility 72, 720–726.
Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MvkvFChtQ%3D%3D&md5=5bdb79414bc11e02df07df573620684cCAS |

Talbott H, Delaney A, Zhang P, Yu Y, Cushman RA, Cupp AS, Hou X, Davis JS (2014) Effects of IL8 and immune cells on the regulation of luteal progesterone secretion. Reproduction (Cambridge, England) 148, 21–31.
Effects of IL8 and immune cells on the regulation of luteal progesterone secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyrtrbN&md5=6b65da3a38373f94a640c25ea518a187CAS |

Talukder S, Ingenhoff L, Kerrisk KL, Celi P (2014a) Plasma oxidative stress biomarkers and progesterone profiles in a dairy cow diagnosed with an ovarian follicular cyst. The Veterinary Quarterly 34, 113–117.
Plasma oxidative stress biomarkers and progesterone profiles in a dairy cow diagnosed with an ovarian follicular cyst.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M%2Fot12jug%3D%3D&md5=aa9ff1f13e56266d785f99fd33ac8439CAS |

Talukder S, Kerrisk KL, Ingenhoff L, Gabai G, Garcia SC, Celi P (2014b) Changes in plasma oxidative stress biomarkers in dairy cows after oestrus synchronization with controlled internal drug release (CIDRs) and prostaglandin F2α (PGF2α). Animal Production Science 54, 1490–1496.

Talukder S, Kerrisk KL, Gabai G, Fukutomi A, Celi P (2015) Changes in milk oxidative stress biomarkers in lactating dairy cows with ovulatory and an-ovulatory oestrous cycles. Animal Reproduction Science 158, 86–95.
Changes in milk oxidative stress biomarkers in lactating dairy cows with ovulatory and an-ovulatory oestrous cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosFKmsro%3D&md5=322dba06859078b7becea069b765bdf0CAS |

Tatemoto H, Muto N, Sunagawa I, Shinjo A, Nakada T (2004) Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biology of Reproduction 71, 1150–1157.
Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqt7c%3D&md5=6dee3c97b1c1af9c604a920d73a8fb14CAS |

Van Hoeck V, Sturmey RG, Bermejo-Alvarez P, Rizos D, Gutierrez-Adan A, Leese HJ, Bols PE, Leroy JL (2011) Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6, e23183
Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKmsLjM&md5=af78bbecbf4f5baedc30e6d3c9427701CAS |

Van Hoeck V, Leroy JLMR, Arias-Alvarez M, Rizos D, Gutierrez-Adan A, Schnorbusch K, Bols PEJ, Leese HJ, Sturmey RG (2013) Oocyte developmental failure in response to elevated non-esterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33–44.
Oocyte developmental failure in response to elevated non-esterified fatty acid concentrations: mechanistic insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGisb8%3D&md5=ec16e9dd22ef5821d4c2f2bab697d38aCAS |

Walusimbi SS, Pate JL (2013) Physiology and endocrinology symposium: role of immune cells in the corpus luteum. Journal of Animal Science 91, 1650–1659.
Physiology and endocrinology symposium: role of immune cells in the corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFWrtbw%3D&md5=8f9196a9fc5a8d463f9ea70d63297a4cCAS |

Wink DA, Hines HB, Cheng RY, Switzer CH, Flores-Santana W, Vitek MP, Ridnour LA, Colton CA (2011) Nitric oxide and redox mechanisms in the immune response. Journal of Leukocyte Biology 89, 873–891.
Nitric oxide and redox mechanisms in the immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFKqurg%3D&md5=9df70a259fc801fa1cdac55263b121f4CAS |

Yacobi K, Tsafriri A, Gross A (2007) Luteinizing hormone-induced caspase activation in rat preovulatory follicles is coupled to mitochondrial steroidogenesis. Endocrinology 148, 1717–1726.
Luteinizing hormone-induced caspase activation in rat preovulatory follicles is coupled to mitochondrial steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVOht7g%3D&md5=1d981867197e0c15763f496bf0c9317aCAS |

Zachara B, Wardak C, Didkowski W, Maciag A, Marchaluk E (1993) Changes in blood selenium and glutathione concentrations and glutathione peroxidase activity in human pregnancy. Gynecologic and Obstetric Investigation 35, 12–17.
Changes in blood selenium and glutathione concentrations and glutathione peroxidase activity in human pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitFSjuro%3D&md5=2642b05149c2eab6183d0faeb07f760aCAS |