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

Relationship between late embryonic mortality and the increase in plasma advanced oxidised protein products (AOPP) in dairy cows

Pietro Celi A , Mariacristina Merlo B , Laura Da Dalt B , Annalisa Stefani C , Olimpia Barbato D and Gianfranco Gabai B E
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Science, University of Sydney, Franklin Lab, Narellan, NSW 2567, Australia.

B Department of Experimental Veterinary Science, University of Padova, Agripolis, 35020 Legnaro (PD), Italy.

C Istituto Zooprofilattico Sperimentale, Agripolis, 35020 Legnaro (PD), Italy.

D Department of Biopathological Veterinary Science, Faculty of Veterinary Medicine, University of Perugia, via San Costanzo, 4 -- 06126 Perugia, Italy.

E Corresponding author. Email: gianfranco.gabai@unipd.it

Reproduction, Fertility and Development 23(4) 527-533 https://doi.org/10.1071/RD10268
Submitted: 10 October 2010  Accepted: 9 November 2010   Published: 11 April 2011

Abstract

The involvement of protein oxidation in embryonic mortality (EM) has been poorly investigated in cows. Advanced oxidation protein products (AOPP) are markers of protein oxidation generated by activated neutrophils and involved in inflammation. The aim of this work was to study AOPP in cow plasma and their relationship with late EM. The outcomes of 158 artificial inseminations (AI) were examined in 72 cows, which were classified ex post on the basis of blood progesterone and pregnancy-associated glycoprotein concentrations and clinical confirmation of pregnancy into the following categories: (1) positive (AI+, resulted in pregnancy, n = 58), (2) negative (AI–, did not result in pregnancy, n = 86) and (3) embryonic mortality (EM, n = 14). Plasma protein fractions, malondialdehyde (MDA), total glutathione and AOPP were measured at AI (Day 0) and on Days 15, 28, 35, 45 and 60. MDA was significantly higher in EM than AI+ and AI– animals on Day 45, and than AI+ animals on Day 60 (P < 0.05). Mean plasma AOPP concentrations were significantly higher in the EM group (P < 0.01) and the ratio of AOPP : albumin was significantly higher in the EM group on Days 15, 28, 45 and 60 (P < 0.05). Based on the temporal pattern of the AOPP : albumin ratio, we propose that oxidative stress is implicated in and may possibly be a cause of EM.

Additional keywords: inflammation, protein oxidation.


References

Agarwal, A., Gupta, S., and Sharma, R. K. (2005). Role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 3, 28.
Role of oxidative stress in female reproduction.Crossref | GoogleScholarGoogle Scholar | 16018814PubMed |

Baker, M. A., Cerniglia, G. J., and Linzell, J. L. (1990). Microtitre plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal. Biochem. 190, 360–365.
Microtitre plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmt1Ons70%3D&md5=553b91f35bd91494b60b776e29e8184dCAS | 2291479PubMed |

Battocchio, M., Gabai, G., Mollo, A., Veronesi, M. C., Soldano, F., Bono, G., and Cairoli, F. (1999). Agreement between ultrasonographic classification of the CL and plasma progesterone concentration in dairy cows. Theriogenology 51, 1059–1069.
Agreement between ultrasonographic classification of the CL and plasma progesterone concentration in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ptFeksg%3D%3D&md5=074e7ace98257a343c0f76c30497a3a1CAS | 10729026PubMed |

Bondurant, R. H. (1999). Inflammation in the bovine reproductive tract. J. Anim. Sci. 77, 101–110.
| 1:CAS:528:DyaK1MXlvFWhtbc%3D&md5=9231a63888706072faaab7f0f687046aCAS | 15526785PubMed |

Capeillère-Blandin, C., Gausson, V., Descamps-Latscha, B., and Witko-Sarsat, V. (2004). Biochemical and spectrophotometric significance of advanced oxidized protein products. Biochim. Biophys. Acta 1689, 91–102.
Biochemical and spectrophotometric significance of advanced oxidized protein products.Crossref | GoogleScholarGoogle Scholar | 15196590PubMed |

Castillo, C., Hernandez, J., Bravo, A., Lopez-Alonso, M., Pereira, V., and Benedito, J. L. (2005). Oxidative status during late pregnancy and early lactation in dairy cows. Vet. J. 169, 286–292.
Oxidative status during late pregnancy and early lactation in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVOitr0%3D&md5=4f5f9c4aba4a1068a49d41398ed554a7CAS | 15727923PubMed |

Celi, P., and Raadsma, H. W. (2010). Effects of Yerba Mate (Ilex paraguariensis) supplementation on the productive performance of dairy cows during mid-lactation Anim. Prod. Sci. 50, 339–344.
Effects of Yerba Mate (Ilex paraguariensis) supplementation on the productive performance of dairy cows during mid-lactationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1yrsLY%3D&md5=760382c2bc76689e1c055f32b3d6ad18CAS |

Celi, P., and Robinson, A. (2010). Effects of Yerba Mate (Ilex paraguariensis) supplementation on the performance of dairy calves. Anim. Prod. Sci. 50, 376–381.
Effects of Yerba Mate (Ilex paraguariensis) supplementation on the performance of dairy calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1yrs70%3D&md5=e5b5cd37d456684b0771ec0f3b14175eCAS |

Chou, M.-Y., Hartvigsen, K., Hansen, L. F., Fogelstrand, L., Shaw, P. X., Boullier, A., Binder, C. J., and Witztum, J. L. (2008). Oxidation-specific epitopes are important targets of innate immunity. J. Intern. Med. 263, 479–488.
Oxidation-specific epitopes are important targets of innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsV2ltLs%3D&md5=7ef80085ad6977c2facb6c81803cd23aCAS | 18410591PubMed |

Dean, R. T., Fu, S., Stocker, R., and Davies, M. J. (1997). Biochemistry and pathology of radical-mediated protein oxidation. Biochem. J. 324, 1–18.
| 1:CAS:528:DyaK2sXjsFCjurs%3D&md5=894a0e7b1e5adab1b73c7541f9553107CAS | 9164834PubMed |

Fujii, J., Ichi, Y., and Okada, F. (2005). Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reprod. Biol. Endocrinol. 3, 43–53.
Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system.Crossref | GoogleScholarGoogle Scholar | 16137335PubMed |

Gabai, G., Testoni, S., Piccinini, R., Marinelli, L., and Stradaioli, G. (2004). Oxidative stress in primiparous cows in relation to dietary starch and the progress of lactation. Anim. Sci. 79, 99–108.

Goff, A. K. (2002). Embryonic signals and survival. Reprod. Domest. Anim. 37, 133–139.
Embryonic signals and survival.Crossref | GoogleScholarGoogle Scholar | 12071886PubMed |

Gray, C. A., Bartol, F. F., Tarleton, B. J., Wiley, A. A., Johnson, G. A., Bazer, F. W., and Spencer, T. E. (2001). Developmental biology of uterine glands. Biol. Reprod. 65, 1311–1323.
Developmental biology of uterine glands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVeku7g%3D&md5=6ca8f6af299a203f74d89aa944cf6b12CAS | 11673245PubMed |

Green, M. P., Hunter, M. G., and Mann, G. E. (2005). Relationship between maternal hormone secretion and embryo development on Day 5 of pregnancy in dairy cows. Anim. Reprod. Sci. 88, 179–189.
Relationship between maternal hormone secretion and embryo development on Day 5 of pregnancy in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvV2mtrc%3D&md5=ccc10a6b1e79068b6ee457fa64e21041CAS | 16143210PubMed |

Guérin, P. E. l., Mouatassim, S., and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–189.
Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings.Crossref | GoogleScholarGoogle Scholar | 11284661PubMed |

Hansen, P. J. (2002). Embryonic mortality in cattle from the embryo’s perspective. J. Anim. Sci. 80, E33–E44.

Johnson, G. A., Burghardt, R. C., Bazer, F. W., and Spencer, T. E. (2003). Osteopontin: roles in implantation and placentation. Biol. Reprod. 69, 1458–1471.
Osteopontin: roles in implantation and placentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosV2kur8%3D&md5=7349651cb8933d8f489827a005f5c261CAS | 12890718PubMed |

Kalousová, M., Zima, T., Tesař, V., Dusilová-Sulková, S., and Skrha, J. (2005). Advanced glycosylation end products in chronic diseases – clinical chemistry and genetic background. Mutat. Res. 579, 37–46.
Advanced glycosylation end products in chronic diseases – clinical chemistry and genetic background.Crossref | GoogleScholarGoogle Scholar | 16084533PubMed |

Kaneko, J. J., Harvey, J. W., and Bruss, M. L. (2008). ‘Clinical Biochemistry of Domestic Animals.’ 6th edn. (Academic Press: Oxford.)

Kaufmann, T. B., Drillich, M., Tenhagen, B.-A., Forderung, D., and Heuwieser, W. (2009). Prevalence of bovine subclinical endometritis 4 h after insemination and its effects on first service conception rate. Theriogenology 71, 385–391.
Prevalence of bovine subclinical endometritis 4 h after insemination and its effects on first service conception rate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FhslSiuw%3D%3D&md5=3f0c8a7c78b76c460079d191e306926aCAS | 18801562PubMed |

Kurien, B. T., Hensley, K., Bachmann, M., and Scofield, R. H. (2006). Oxidatively modified auto-antigens in autoimmune diseases. Free Radic. Biol. Med. 41, 549–556.
Oxidatively modified auto-antigens in autoimmune diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntlCqtrc%3D&md5=2764a3983a97eea4fc1119ae03f3938cCAS | 16863987PubMed |

López-Gatius, F., Garbayo, J. M., Santolaria, P., Yániz, J., Ayad, A., de Sousa, N. M., and Beckers, J. F. (2007). Milk production correlates negatively with plasma levels of pregnancy-associated glycoprotein (PAG) during the early fetal period in high producing dairy cows with lively fetuses. Domest. Anim. Endocrinol. 32, 29–42.
Milk production correlates negatively with plasma levels of pregnancy-associated glycoprotein (PAG) during the early fetal period in high producing dairy cows with lively fetuses.Crossref | GoogleScholarGoogle Scholar | 16423500PubMed |

Mann, G. E., and Lamming, G. E. (1999). The influence of progesterone during early pregnancy in cattle. Reprod. Domest. Anim. 34, 269–274.
The influence of progesterone during early pregnancy in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Knu7Y%3D&md5=51a67d7ef6b5d80782dc71e3c657a1c3CAS |

Mantovani, R., Sgorlon, S., Marinelli, L., Bailoni, L., Bittante, G., and Gabai, G. (2010). Oxidative stress indicators and metabolic adaptations in response to the omission of the dry period in dairy cows. J. Dairy Res. 77, 273–279.
| 1:CAS:528:DC%2BC3cXnvV2rsbo%3D&md5=aff0b11dabd389934c4b200938fb3591CAS | 20334713PubMed |

Miller, J. K., Brzezinska-Slebodzinska, E., and Madsen, F. C. (1993). Oxidative stress, antioxidants and animal function. J. Dairy Sci. 76, 2812–2823.
Oxidative stress, antioxidants and animal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1Olt7g%3D&md5=d99ad9ef4a7186c775ff81c4773261f6CAS | 8227685PubMed |

National Research Council (2001). ‘Nutrient Requirements of Dairy Cattle: Seventh Revised Edition.’ (National Academic Press: Washington, DC.)

Pedernera, M., Celi, P., García, S. C., Salvin, H. E., Barchia, I., and Fulkerson, W. J. (2009). Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. Vet. J. , .
Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture.Crossref | GoogleScholarGoogle Scholar | 19804998PubMed |

Perényi, Z., Szenci, O., Sulon, J., Drion, P. V., and Beckers, J. F. (2002). Comparison of the ability of three radioimmunoassays to detect pregnancy-associated glycoproteins in bovine plasma. Reprod. Domest. Anim. 37, 100–104.
Comparison of the ability of three radioimmunoassays to detect pregnancy-associated glycoproteins in bovine plasma.Crossref | GoogleScholarGoogle Scholar | 11975748PubMed |

Perry, G. A., Geary, T. W., Lucy, M. C., and Smith, M. F. (2002). Effect of follicle size at the time of induced ovulation on luteal function and fertility. ‘Proceedings of the American Society of Animal Science, Western Section 53, 45–48.

Roberts, R. M., Xie, S., and Mathialagan, N. (1996). Maternal recognition of pregnancy. Biol. Reprod. 54, 294–302.
Maternal recognition of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltF2qtg%3D%3D&md5=92da0ef1fa18e04ccc0d32e2796b0063CAS | 8788179PubMed |

Serrano, B., Lopez-Gatius, F., Hunter, R. H. F., Santolaria, P., Garcia-Ispierto, I., Bech-Sabat, G., Sousa, N. M., Beckers, J. F., and Yaniz, J. S. (2009). Anomalous pregnancies during late-embryonic early-foetal period in high-producing dairy cows. Reprod. Domest. Anim. 44, 672–676.
Anomalous pregnancies during late-embryonic early-foetal period in high-producing dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrgsFGksQ%3D%3D&md5=7746b03d0f6f70b92531ae0b6c503921CAS | 18694426PubMed |

Shanti, A., Santanam, N., Morales, A. J., Parthasarathy, S., and Murphy, A. A. (1999). Autoantibodies to markers of oxidative stress are elevated in women with endometriosis. Fertil. Steril. 71, 1115–1118.
Autoantibodies to markers of oxidative stress are elevated in women with endometriosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3oslKltw%3D%3D&md5=7c34d58ba7a79dae4d8aa363b67664ffCAS | 10360920PubMed |

Sies, H. (1991). Oxidative stress: from basic research to clinical application. Am. J. Med. 91, S31–S38.
Oxidative stress: from basic research to clinical application.Crossref | GoogleScholarGoogle Scholar |

Singh, J., Murray, R. D., Mshelia, G., and Woldehiwet, Z. (2008). The immune status of the bovine uterus during the peripartum period. Vet. J. 175, 301–309.
The immune status of the bovine uterus during the peripartum period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlOqurk%3D&md5=b9fc45d2d3e784bdd64230de2d7a6abcCAS | 17400489PubMed |

Sordillo, L. M., Contreras, G. A., and Aitken, S. L. (2009). Metabolic factors affecting the inflammatory response of periparturient dairy cows. Anim. Health Res. Rev. 10, 53–63.
Metabolic factors affecting the inflammatory response of periparturient dairy cows.Crossref | GoogleScholarGoogle Scholar | 19558749PubMed |

Sugino, N. (2006). Roles of reactive oxygen species in the corpus luteum. Anim. Sci. J. 77, 556–565.
Roles of reactive oxygen species in the corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Gjsbs%3D&md5=949f59fd6d089eb1b0dac843d14c578bCAS |

Szenci, O., Taverne, M. A. M., Beckers, J. F., Sulon, J., Varga, J., Börzsönyi, L., Hanzen, C., and Schekk, G. (1998). Evaluation of false ultrasonographic diagnoses in cows by measuring plasma levels of bovine pregnancy-associated glycoprotein 1. Vet. Rec. 142, 304–306.
Evaluation of false ultrasonographic diagnoses in cows by measuring plasma levels of bovine pregnancy-associated glycoprotein 1.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3jtV2mtg%3D%3D&md5=00e4638de9165319bd2130518d308170CAS | 9569497PubMed |

Szenci, O., Beckers, J. F., Sulon, J., Bevers, M. M., Borzsonyi, L., Fodor, L., Kovacs, F., and Taverne, M. A. M. (2003). Effect of induction of late embryonic mortality on plasma profiles of pregnancy-associated glycoprotein 1 in heifers. Vet. J. 165, 307–313.
Effect of induction of late embryonic mortality on plasma profiles of pregnancy-associated glycoprotein 1 in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFWlt7g%3D&md5=d4431b105b74c3f2b017668b4ca9ecd5CAS | 12672378PubMed |

Tanaka, M., Kamiya, Y., Kamiya, M., Shioya, S., and Nakai, Y. (2007). Antiradical function of sulfhydryl residues and oxidative stress markers in dairy cattle plasma. Anim. Sci. J. 78, 61–65.
Antiradical function of sulfhydryl residues and oxidative stress markers in dairy cattle plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXis1Omsrw%3D&md5=9db6672884e25ed653a686dd8514e6b7CAS |

Tietze, F. (1969). Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502–522.
Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXktVSlt7k%3D&md5=c8fc15bbc4f6966016dadb4a697830abCAS | 4388022PubMed |

Witko-Sarsat, V., Friedlander, M., Capeillère-Blandin, C., Nguyen-Khoa, T., Nguyen, A. T., Zingraff, J., Jungers, P., and Descamps-Latscha, B. (1996). Advanced oxidation protein products as a novel marker of oxidative stress in uraemia. Kidney Int. 49, 1304–1313.
Advanced oxidation protein products as a novel marker of oxidative stress in uraemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xkslagsbs%3D&md5=8fd69569777c863ad8f583c8521472c9CAS | 8731095PubMed |

Witko-Sarsat, V., Friedlander, M., Capeillère-Blandin, C., Nguyen-Khoa, T., Caeillere-Blandin, C., Nguyen, A. T., Canteluop, S., Dayer, J.-M., Jungers, P., Drueke, T., and Descamps-Latscha, B. (1998). Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. J. Immunol. 161, 2524–2532.
| 1:CAS:528:DyaK1cXlslanu7k%3D&md5=da485e28d260aace5407c6b607159e7bCAS | 9725252PubMed |

Witko-Sarsat, V., Nguyen-Khoa, T., Canteluop, S., Jungers, P., Drueke, T., and Descamps-Latscha, B. (1999). Advanced oxidation protein products as a novel molecular basis in uraemia. Nephrol. Dial. Transplant. 14, 76–78.
Advanced oxidation protein products as a novel molecular basis in uraemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlylu70%3D&md5=1dc06e38642dd410f725a950be7b5de2CAS | 10048460PubMed |

Witko-Sarsat, V., Gausson, V., Nguyen, A. T., Touam, M., Drueke, T., Santangelo, F., and Descamps-Latscha, B. (2003). AOPP-induced activation of human neutrophil and monocyte oxidative metabolism: a potential target for n-acetylcysteine treatment in dialysis patients. Kidney Int. 64, 82–91.
AOPP-induced activation of human neutrophil and monocyte oxidative metabolism: a potential target for n-acetylcysteine treatment in dialysis patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFelu7o%3D&md5=a33c17cf60c3a636b5de727ef7b472d0CAS | 12787398PubMed |

Wu, G., Fang, Y. Z., Yang, S., Lupton, J. R., and Turner, N. D. (2004). Glutathione metabolism and its implication for health. J. Nutr. 134, 489–492.
| 1:CAS:528:DC%2BD2cXitlCrurc%3D&md5=b8af32cf58e420a2e7c853740970f6b6CAS | 14988435PubMed |

Yoshida, Y., Itoh, N., Hayakawa, M., Piga, R., Cynshi, O., Jishage, K., and Niki, E. (2005). Lipid peroxidation induced by carbon tetrachloride and its inhibition by antioxidant as evaluated by an oxidative stress marker, HODE. Toxicol. Appl. Pharmacol. 208, 87–97.
Lipid peroxidation induced by carbon tetrachloride and its inhibition by antioxidant as evaluated by an oxidative stress marker, HODE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWhtb%2FL&md5=8adb48f47d90a10c19764ab118e6976bCAS | 16164964PubMed |

Zoli, A. P., Beckers, J. F., Wouters-Ballman, P., Closset, J., Falemagne, P., and Ectors, F. (1991). Purification and characterization of a bovine pregnancy-associated glycoprotein. Biol. Reprod. 45, 1–10.
Purification and characterization of a bovine pregnancy-associated glycoprotein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltVyrsLw%3D&md5=2a0ba229302539f60c9695c6a17681e2CAS | 1908709PubMed |

Zoli, A. P., Guibault, L. A., Delahaut, P., Ortiz, W. B., and Beckers, J. F. (1992). Radioimmunoassay of a bovine pregnancy-associated glycoprotein in serum: its application for pregnancy diagnosis. Biol. Reprod. 46, 83–92.
Radioimmunoassay of a bovine pregnancy-associated glycoprotein in serum: its application for pregnancy diagnosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsV2lsg%3D%3D&md5=47656d9f46256c81935c1e47b7a1f5a1CAS | 1547318PubMed |