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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Predictive value of bovine follicular components as markers of oocyte developmental potential

Satoko Matoba A C , Katrin Bender B , Alan G. Fahey A , Solomon Mamo A , Lorraine Brennan B , Patrick Lonergan A and Trudee Fair A D
+ Author Affiliations
- Author Affiliations

A School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland.

B Institute of Food and Health, Conway Institute, University College Dublin, Belfield, Dublin 4, Ireland.

C Present address: National Livestock Breeding Center, Odakurahara 1, Nishigo, Fukushima 961-8511, Japan.

D Corresponding author. Email: trudee.fair@ucd.ie

Reproduction, Fertility and Development 26(2) 337-345 https://doi.org/10.1071/RD13007
Submitted: 21 June 2012  Accepted: 18 January 2013   Published: 21 March 2013

Abstract

The follicle is a unique micro-environment within which the oocyte can develop and mature to a fertilisable gamete. The aim of this study was to investigate the ability of a panel of follicular parameters, including intrafollicular steroid and metabolomic profiles and theca, granulosa and cumulus cell candidate gene mRNA abundance, to predict the potential of bovine oocytes to develop to the blastocyst stage in vitro. Individual follicles were dissected from abattoir ovaries, carefully ruptured under a stereomicroscope and the oocyte was recovered and individually processed through in vitro maturation, fertilisation and culture. The mean (± s.e.m.) follicular concentrations of testosterone (62.8 ± 4.8 ng mL–1), progesterone (616.8 ± 31.9 ng mL–1) and oestradiol (14.4 ± 2.4 ng mL–1) were not different (P > 0.05) between oocytes that formed (competent) or failed to form (incompetent) blastocysts. Principal-component analysis of the quantified aqueous metabolites in follicular fluid showed differences between oocytes that formed blastocysts and oocytes that degenerated; l-alanine, glycine and l-glutamate were positively correlated and urea was negatively correlated with blastocyst formation. Follicular fluid associated with competent oocytes was significantly lower in palmitic acid (P = 0.023) and total fatty acids (P = 0.031) and significantly higher in linolenic acid (P = 0.036) than follicular fluid from incompetent oocytes. Significantly higher (P < 0.05) transcript abundance of LHCGR in granulosa cells, ESR1 and VCAN in thecal cells and TNFAIP6 in cumulus cells was associated with competent compared with incompetent oocytes.

Additional keywords: cattle, follicular fluid, IVF, metabolomics, mRNA expression, oocyte quality.


References

Adriaenssens, T., Wathlet, S., Segers, I., Verheyen, G., De Vos, A., Van der Elst, J., Coucke, W., Devroey, P., and Smitz, J. (2010). Cumulus cell gene expression is associated with oocyte developmental quality and influenced by patient and treatment characteristics. Hum. Reprod. 25, 1259–1270.
Cumulus cell gene expression is associated with oocyte developmental quality and influenced by patient and treatment characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFOjsbY%3D&md5=4308a412f14c6dce3b27fc662dea1220CAS | 20228394PubMed |

Assidi, M., Dufort, I., Ali, A., Hamel, M., Algriany, O., Dielemann, S., and Sirard, M. A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol. Reprod. 79, 209–222.
Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWms7o%3D&md5=2d3803a6998081a883758471616f201dCAS | 18417710PubMed |

Bender, K., Walsh, S., Evans, A. C. O., Fair, T., and Brennan, L. (2010). Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows. Reproduction 139, 1047–1055.
Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXns12qsbs%3D&md5=6169bea462f4d1f1edc632e7125f21c8CAS | 20385782PubMed |

Bligh, E. G., and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917.
A rapid method of total lipid extraction and purification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1MXhtVSgt70%3D&md5=cc01ae73966d033e8c0506071699032aCAS | 13671378PubMed |

Cetica, P., Pintos, L., Dalvit, G., and Beconi, M. (2003). Involvement of enzymes of amino acid metabolism and tricarboxylic acid cycle in bovine oocyte maturation in vitro. Reproduction 126, 753–763.
Involvement of enzymes of amino acid metabolism and tricarboxylic acid cycle in bovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFWktg%3D%3D&md5=74f471be787999546296e1b51d2dc748CAS | 14748694PubMed |

De Wit, A. A., Cesar, M. L., and Kruip, T. A. (2001). Effect of urea during in vitro maturation on nuclear maturation and embryo development of bovine cumulus–oocyte complexes. J. Dairy Sci. 84, 1800–1804.
Effect of urea during in vitro maturation on nuclear maturation and embryo development of bovine cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFaqurg%3D&md5=6202a54570e75644b94d4958ffa2c97aCAS | 11518303PubMed |

Forde, N., Rogers, M., Canty, M. J., Lonergan, P., Smith, G. W., Coussens, P. M., Ireland, J. J., and Evans, A. C. O. (2008). Association of the prion protein and its expression with ovarian follicle development in cattle. Mol. Reprod. Dev. 75, 243–249.
Association of the prion protein and its expression with ovarian follicle development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVCrtg%3D%3D&md5=2be58601a75c3f091de8b8b7b472bd56CAS | 17595008PubMed |

Fülöp, C., Szántó, S., Mukhopadhyay, D., Bárdos, T., Kamath, R. V., Rugg, M. S., Day, A. J., Salustri, A., Hascall, V. C., Glant, T. T., and Mikecz, K. (2003). Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 130, 2253–2261.
Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice.Crossref | GoogleScholarGoogle Scholar | 12668637PubMed |

Grøndahl, M. L., Borup, R., Lee, Y. B., Myrhøj, V., Meinertz, H., and Sørensen, S. (2009). Differences in gene expression of granulosa cells from women undergoing controlled ovarian hyperstimulation with either recombinant follicle-stimulating hormone or highly purified human menopausal gonadotrophin. Fertil. Steril. 91, 1820–1830.
Differences in gene expression of granulosa cells from women undergoing controlled ovarian hyperstimulation with either recombinant follicle-stimulating hormone or highly purified human menopausal gonadotrophin.Crossref | GoogleScholarGoogle Scholar | 18439596PubMed |

Haggarty, P., Wood, M., Ferguson, E., Hoad, G., Srikantharajah, A., Milne, E., Hamilton, M., and Bhattacharya, S. (2006). Fatty-acid metabolism in human preimplantation embryos. Hum. Reprod. 21, 766–773.
Fatty-acid metabolism in human preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhs1Sks7w%3D&md5=e4d67533ae3bef7820eb2e45efd0d8b5CAS | 16311299PubMed |

Hamel, M., Dufort, I., Robert, C., Leveille, M. C., Leader, A., and Sirard, M. A. (2010). Identification of follicular marker genes as pregnancy predictors for human IVF: new evidence for the involvement of luteinization process. Mol. Hum. Reprod. 16, 548–556.
Identification of follicular marker genes as pregnancy predictors for human IVF: new evidence for the involvement of luteinization process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlegt7w%3D&md5=152ce01a88d54e0f3bd0d6138c76bad6CAS | 20610614PubMed |

Hemmings, K. E., Leese, H. J., and Picton, H. M. (2012). Amino acid turnover by bovine oocytes provides an index of oocyte developmental competence in vitro. Biol. Reprod. 86, 1–12.

Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and Callesen, H. (1999). High bovine blastocyst development in a static in vitro-production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum proteins. Theriogenology 52, 683–700.
High bovine blastocyst development in a static in vitro-production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum proteins.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=bda1bd1463ad693633a4028a58f68438CAS | 10734366PubMed |

Jiye, A., Huang, Q., Wang, G., Zha, W., Yan, B., Ren, H., Gu, S., Zhang, Y., Zhang, Q., Shao, F., Sheng, L., and Sun, J. (2008). Global analysis of metabolites in rat and human urine based on gas chromatography/time-of-flight mass spectrometry. Anal. Biochem. 379, 20–26.
Global analysis of metabolites in rat and human urine based on gas chromatography/time-of-flight mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1czptVWnsg%3D%3D&md5=bc3a0bcc07f9bced89e9b6390addd5cdCAS | 18486586PubMed |

Jozwik, M., Teng, C., and Battaglia, F. C. (2006). Amino acid, ammonia and urea concentrations in human pre-ovulatory ovarian follicular fluid. Hum. Reprod. 21, 2776–2782.
Amino acid, ammonia and urea concentrations in human pre-ovulatory ovarian follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVynsr7M&md5=6c961fd957358d10bb798df812dca181CAS | 16950828PubMed |

Lédée, N., Dubanchet, S., Oger, P., Meynant, C., Lombroso, R., Ville, Y., and Chaouat, G. (2007). Uterine receptivity and cytokines: new concepts and new applications. Gynecol. Obstet. Invest. 64, 138–143.
Uterine receptivity and cytokines: new concepts and new applications.Crossref | GoogleScholarGoogle Scholar | 17934309PubMed |

Lee, E. S., and Fukui, Y. (1996). Synergistic effect of alanine and glycine on bovine embryos cultured in a chemically defined medium and amino acid uptake by in vitro-produced bovine morulae and blastocysts. Biol. Reprod. 55, 1383–1389.
Synergistic effect of alanine and glycine on bovine embryos cultured in a chemically defined medium and amino acid uptake by in vitro-produced bovine morulae and blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkvFWntQ%3D%3D&md5=21fa10b382a7d4e1bbec953a8eea503cCAS | 8949897PubMed |

Lee, S., Kang, D. W., Hudgins-Spivey, S., Krust, A., Lee, E. Y., Koo, Y., Cheon, Y., Gye, M. C., Chambon, P., and Ko, C. (2009). Theca-specific oestrogen receptor-alpha knockout mice lose fertility prematurely. Endocrinology 150, 3855–3862.
Theca-specific oestrogen receptor-alpha knockout mice lose fertility prematurely.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsV2ru7c%3D&md5=a89dbd56e85fa8273df40278c11528d6CAS | 19423761PubMed |

Leroy, J. L. M. R., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and 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=cd82fd88938bb4bfbef1f4cb6ee5e020CAS |

Luo, W., Gumen, A., Haughian, J. M., and Wiltbank, M. C. (2011). The role of luteinizing hormone in regulating gene expression during selection of a dominant follicle in cattle. Biol. Reprod. 84, 369–378.
The role of luteinizing hormone in regulating gene expression during selection of a dominant follicle in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVelt78%3D&md5=a8dd71fdcdb4cfbc003de19fda82ccbfCAS | 20962252PubMed |

Marei, W. F., Wathes, D. C., and Fouladi-Nashta, A. A. (2009). The effect of linolenic acid on bovine oocyte maturation and development. Biol. Reprod. 81, 1064–1072.
The effect of linolenic acid on bovine oocyte maturation and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2lt7vL&md5=723304df9e34ac8a15a75e7fa3a466afCAS | 19587335PubMed |

Matoba, S., Fair, T., and Lonergan, P. (2010). Maturation, fertilisation and culture of bovine oocytes and embryos in an individually identifiable manner: a tool for studying oocyte developmental competence. Reprod. Fertil. Dev. 22, 839–851.
Maturation, fertilisation and culture of bovine oocytes and embryos in an individually identifiable manner: a tool for studying oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 20450836PubMed |

Mu, Y. M., Yanase, T., Nishi, Y., Tanaka, A., Saito, M., Jin, C. H., Mukasa, C., Okabe, T., Nomura, M., Goto, K., and Nawata, H. (2001). Saturated FFAs, palmitic acid and stearic acid, induce apoptosis in human granulosa cells. Endocrinology 142, 3590–3597.
Saturated FFAs, palmitic acid and stearic acid, induce apoptosis in human granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1Sqt7o%3D&md5=3b8b1308dfe7898176366412b96ff14dCAS | 11459807PubMed |

O’Shea, L. C., Mehta, J., Lonergan, P., Hensey, C., and Fair, T. (2012). Developmental competence in oocytes and cumulus cells: candidate genes and networks. Syst. Biol. Reprod. Med. 58, 88–101.
Developmental competence in oocytes and cumulus cells: candidate genes and networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktV2nt7k%3D&md5=2693b9071cf618b0084c78bd808b6589CAS | 22313243PubMed |

Pakarainen, T., Ahtiainen, P., Zhang, F. P., Rulli, S., Poutanen, M., and Huhtaniemi, P. (2007). Extragonadal LH/hCG action - not yet time to rewrite textbooks. Mol. Cell. Endocrinol. 269, 9–16.
Extragonadal LH/hCG action - not yet time to rewrite textbooks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjslSqsbk%3D&md5=20ae41927f26f917272e4ba86d511745CAS | 17350753PubMed |

Reis, A., Rooke, J. A., McCallum, G. J., Staines, M. E., Ewen, M., Lomax, M. A., and McEvoy, T. G. (2003). Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro. Reprod. Fertil. Dev. 15, 275–284.
Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Cgur0%3D&md5=e779e7e142fe560e5295d479c49ee5c8CAS | 14588185PubMed |

Revelli, A., Delle Piane, L., Casano, S., Molinari, E., Massobrio, M., and Rinaudo, P. (2009). Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod. Biol. Endocrinol. 7, 40.
Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics.Crossref | GoogleScholarGoogle Scholar | 19413899PubMed |

Russell, D. L., Doyle, K. M., Ochsner, S. A., Sandy, J. D., and Richards, J. S. (2003a). Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J. Biol. Chem. 278, 42 330–42 339.
Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1amu74%3D&md5=d21e35b9ec48c7f8582150c01b391205CAS |

Russell, D. L., Ochsner, S. A., Hsieh, M., Mulders, S., and Richards, J. S. (2003b). Hormone-regulated expression and localization of versican in the rodent ovary. Endocrinology 144, 1020–1031.
Hormone-regulated expression and localization of versican in the rodent ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslCqtr0%3D&md5=51067f07e7408f21c254c67cc4d5781eCAS | 12586779PubMed |

Sandy, J. D., Westling, J., Kenagy, R. D., Iruela-Arispe, M. L., Verscharen, C., Rodriguez-Mazaneque, J. C., Zimmermann, D. R., Lemire, J. M., Fischer, J. W., Wight, T. N., and Clowes, A. W. (2001). Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J. Biol. Chem. 276, 13 372–13 378.
Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFymt70%3D&md5=bd9c3f1befd453c08308d9a05664be4bCAS |

Santos, P., Marques, A., Antunes, G., Chaveiro, A., Andrade, M., Borba, A., and da Silva, F. M. (2009). Effects of plasma urea nitrogen levels on the bovine oocyte ability to develop after in vitro fertilization. Reprod. Domest. Anim. 44, 783–787.
Effects of plasma urea nitrogen levels on the bovine oocyte ability to develop after in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSjt7bJ&md5=7b7a1aa203406e7a1e18d5be1b98aeb5CAS | 18992098PubMed |

Sinclair, K. D., Lunn, L. A., Kwong, W. Y., Wonnacott, K., Linforth, R. S., and Craigon, J. (2008). Amino acid and fatty acid composition of follicular fluid as predictors of in vitro embryo development. Reprod. Biomed. Online 16, 859–868.
Amino acid and fatty acid composition of follicular fluid as predictors of in vitro embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotFars70%3D&md5=67825ef679c11022cd4c2fc0f8933b62CAS | 18549697PubMed |

Tesfaye, D., Ghanem, N., Carter, F., Fair, T., Sirard, M. A., Hoelker, M., Schellander, K., and Lonergan, P. (2009). Gene expression profile of cumulus cells derived from cumulus-oocyte complexes matured either in vivo or in vitro. Reprod. Fertil. Dev. 21, 451–461.
Gene expression profile of cumulus cells derived from cumulus-oocyte complexes matured either in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFemsb8%3D&md5=67727bb4c37b5526a4f3c4fffe627f1cCAS | 19261222PubMed |

Vanholder, T., Leroy, J. L., Soom, A. V., Opsomer, G., Maes, D., Coryn, M., and de Kruif, A. (2005). Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Anim. Reprod. Sci. 87, 33–44.
Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktVOju74%3D&md5=df3d7202ce6adae70e3a89068a8765e3CAS | 15885439PubMed |