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Vertebrate reproductive science and technology
RESEARCH ARTICLE

An integrated approach to bovine oocyte quality: from phenotype to genes

Leslie Angulo A B C D , Catherine Guyader-Joly E , Sylvain Auclair A B C , Christelle Hennequet-Antier F , Pascal Papillier A B C , Mekki Boussaha G , Sébastien Fritz D G , Karine Hugot G , François Moreews H I , Claire Ponsart D J , Patrice Humblot D K and Rozenn Dalbies-Tran A B C L
+ Author Affiliations
- Author Affiliations

A INRA, UMR85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France.

B CNRS, UMR7247, F-37380 Nouzilly, France.

C Université François Rabelais de Tours, F-37041 Tours, France.

D Union Nationale des Coopératives d’Elevage et d’Insémination Animale, F-94704 Maisons-Alfort, France.

E Union Nationale des Coopératives d’Elevage et d’Insémination Animale, F-38300 Chateauvillain, France.

F INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France.

G INRA, UMR 1313 Génétique Animale et Biologie Intégrative, 78350 Jouy-en-Josas, France.

H INRA Sigenae, UMR1348 PEGASE 35042 Rennes, France.

I Genscale, Institut de recherche en informatique et systèmes aléatoires (IRISA), 35042 Rennes, France.

J ANSES, Laboratoire de Santé Animale, 14 rue Pierre et Marie Curie, F-94701 Maisons-Alfort, France.

K Department of Clinical Sciences, Division of Reproduction, Swedish University of Agricultural Sciences, SE-750 07 Uppsala, Sweden.

L Corresponding author. Email: dalbies@tours.inra.fr

Reproduction, Fertility and Development 28(9) 1276-1287 https://doi.org/10.1071/RD14353
Submitted: 20 September 2014  Accepted: 7 January 2015   Published: 18 February 2015

Abstract

In cattle, early embryonic failure plays a major role in the limitation of reproductive performance and is influenced by genetic effects. Suboptimal oocyte quality, including an inadequate store of maternal factors, is suspected to contribute to this phenomenon. In the present study, 13 Montbeliarde cows were phenotyped on oocyte quality, based on their ability to produce viable embryos after in vitro maturation, fertilisation and culture for 7 days. This discriminated two groups of animals, exhibiting developmental rates below 18.8% or above 40.9% (relative to cleaved embryos). Using microarrays, transcriptomic profiles were compared between oocytes collected in vivo from these two groups of animals. The difference in oocyte development potential was associated with changes in transcripts from 60 genes in immature oocytes and 135 genes in mature oocytes (following Bonferroni 5% correction). Of these, 16 and 32 genes were located in previously identified fertility quantitative trait loci. A subset of differential genes was investigated on distinct samples by reverse transcription–quantitative polymerase chain reaction. For SLC25A16, PPP1R14C, ROBO1, AMDHD1 and MEAF6 transcripts, differential expression was confirmed between high and low oocyte potential animals. Further sequencing and searches for polymorphisms will pave the way for implementing their use in genomic selection.

Additional keywords: development, embryo, fertility, gene expression, transcriptome.


References

Barreau, C., Paillard, L., and Osborne, H. B. (2005). AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33, 7138–7150.
AU-rich elements and associated factors: are there unifying principles?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKqsA%3D%3D&md5=d8b51a182bf1cd20c2465e92230e3c65CAS | 16391004PubMed |

Chu, T., Dufort, I., and Sirard, M. A. (2012). Effect of ovarian stimulation on oocyte gene expression in cattle. Theriogenology 77, 1928–1938.
Effect of ovarian stimulation on oocyte gene expression in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksFensrc%3D&md5=72ca7c92286e9dd0c7daf7b4959c52dcCAS | 22444561PubMed |

Colucci-Guyon, E., Portier, M. M., Dunia, I., Paulin, D., Pournin, S., and Babinet, C. (1994). Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79, 679–694.
Mice lacking vimentin develop and reproduce without an obvious phenotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1Gksrk%3D&md5=d4fe9635ee73b6b6d692c949345e0078CAS | 7954832PubMed |

Dessie, S. W., Rings, F., Holker, M., Gilles, M., Jennen, D., Tholen, E., Havlicek, V., Besenfelder, U., Sukhorukov, V. L., Zimmermann, U., Endter, J. M., Sirard, M. A., Schellander, K., and Tesfaye, D. (2007). Dielectrophoretic behavior of in vitro-derived bovine metaphase II oocytes and zygotes and its relation to in vitro embryonic developmental competence and mRNA expression pattern. Reproduction 133, 931–946.
Dielectrophoretic behavior of in vitro-derived bovine metaphase II oocytes and zygotes and its relation to in vitro embryonic developmental competence and mRNA expression pattern.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlGnu7o%3D&md5=03301fa0d5bd36f0964a8c59ddc338e1CAS | 17616723PubMed |

Diskin, M. G., Parr, M. H., and Morris, D. G. (2011). Embryo death in cattle: an update. Reprod. Fertil. Dev. 24, 244–251.
| 1:STN:280:DC%2BC383ptFClsw%3D%3D&md5=3a78065b9ca9c9f7ebaaff59aab27a46CAS | 22394965PubMed |

Dorji, , Ohkubo, Y., Miyoshi, K., and Yoshida, M. (2012). Gene expression differences in oocytes derived from adult and prepubertal Japanese black cattle during in vitro maturation. Reprod. Domest. Anim. 47, 392–402.
Gene expression differences in oocytes derived from adult and prepubertal Japanese black cattle during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVKmt7c%3D&md5=00b1bc3321c0ef65d6248e2ec95771f1CAS | 21906190PubMed |

Ghanem, N., Holker, M., Rings, F., Jennen, D., Tholen, E., Sirard, M. A., Torner, H., Kanitz, W., Schellander, K., and Tesfaye, D. (2007). Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave. BMC Dev. Biol. 7, 90.
Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave.Crossref | GoogleScholarGoogle Scholar | 17662127PubMed |

Goehler, H., Lalowski, M., Stelzl, U., Waelter, S., Stroedicke, M., Worm, U., Droege, A., Lindenberg, K. S., Knoblich, M., Haenig, C., Herbst, M., Suopanki, J., Scherzinger, E., Abraham, C., Bauer, B., Hasenbank, R., Fritzsche, A., Ludewig, A. H., Bussow, K., Coleman, S. H., Gutekunst, C. A., Landwehrmeyer, B. G., Lehrach, H., and Wanker, E. E. (2004). A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington’s disease. Mol. Cell 15, 853–865.
A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington’s disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXosl2jsb8%3D&md5=8856eb769d31d56eec919dfaad03c668CAS | 15383276PubMed |

Graindorge, A., Thuret, R., Pollet, N., Osborne, H. B., and Audic, Y. (2006). Identification of post-transcriptionally regulated Xenopus tropicalis maternal mRNAs by microarray. Nucleic Acids Res. 34, 986–995.
Identification of post-transcriptionally regulated Xenopus tropicalis maternal mRNAs by microarray.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhs1Skuro%3D&md5=627a674a2a7cf3007b105c1bff2e7e92CAS | 16464828PubMed |

Grimard, B., Freret, S., Chevallier, A., Pinto, A., Ponsart, C., and Humblot, P. (2006). Genetic and environmental factors influencing first service conception rate and late embryonic/foetal mortality in low fertility dairy herds. Anim. Reprod. Sci. 91, 31–44.
Genetic and environmental factors influencing first service conception rate and late embryonic/foetal mortality in low fertility dairy herds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gns7nJ&md5=10e1f8a67e76dbae793e4ad8bb6fa298CAS | 16310097PubMed |

Guyader Joly, C., Ponchon, S., Thuard, J. M., Durand, M., Nibart, M., Marquant-Le Guienne, B., and Humblot, P. (1997). Effects of superovulation on repeated ultrasound guided oocyte collection and in vitro embryo production in pregnant heifers. Theriogenology 47, 157.
Effects of superovulation on repeated ultrasound guided oocyte collection and in vitro embryo production in pregnant heifers.Crossref | GoogleScholarGoogle Scholar |

Guyader-Joly, C., Ponchon, S., Durand, M., Heyman, Y., Renard, J. P., and Menezo, Y. (1999). Effect of lecithin on in vitro and in vivo survival of in vitro produced bovine blastocysts after cryopreservation. Theriogenology 52, 1193–1202.
Effect of lecithin on in vitro and in vivo survival of in vitro produced bovine blastocysts after cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVKrtw%3D%3D&md5=137d1a82161efec536d9f8c9dd419eadCAS | 10735097PubMed |

Hamatani, T., Falco, G., Carter, M. G., Akutsu, H., Stagg, C. A., Sharov, A. A., Dudekula, D. B., VanBuren, V., and Ko, M. S. (2004). Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 13, 2263–2278.
Age-associated alteration of gene expression patterns in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1Onu7k%3D&md5=7b188ed580c78f36aa6e957827fae7eaCAS | 15317747PubMed |

Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009a). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1–13.
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists.Crossref | GoogleScholarGoogle Scholar |

Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009b). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57.
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCkurnI&md5=e95521288c9064241695903dc4556814CAS |

Huang, W., Kirkpatrick, B. W., Rosa, G. J. M., and Khatib, H. (2010). A genome-wide association study using selective DNA pooling identifies candidate markers for fertility in Holstein cattle. Anim. Genet. 41, 570–578.
A genome-wide association study using selective DNA pooling identifies candidate markers for fertility in Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cblvVCmsg%3D%3D&md5=721c41e4ca5897b23b0c9aa07c066a40CAS | 20394602PubMed |

Humblot, P. (2001). Use of pregnancy specific proteins and progesterone assays to monitor pregnancy and determine the timing, frequencies and sources of embryonic mortality in ruminants. Theriogenology 56, 1417–1433.
Use of pregnancy specific proteins and progesterone assays to monitor pregnancy and determine the timing, frequencies and sources of embryonic mortality in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjslyqsA%3D%3D&md5=1b1d3892780c5a67f2dbd95eb7494337CAS | 11768808PubMed |

Katz-Jaffe, M. G., McCallie, B. R., Preis, K. A., Filipovits, J., and Gardner, D. K. (2009). Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes. Theriogenology 71, 939–946.
Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVWltLg%3D&md5=ffc980f26f324681783f13c32723ba16CAS | 19150733PubMed |

Kocabas, A. M., Crosby, J., Ross, P. J., Otu, H. H., Beyhan, Z., Can, H., Tam, W. L., Rosa, G. J., Halgren, R. G., Lim, B., Fernandez, E., and Cibelli, J. B. (2006). The transcriptome of human oocytes. Proc. Natl Acad. Sci. USA 103, 14 027–14 032.
The transcriptome of human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCmur7I&md5=f11cb4bbc829f4dc94452ae0e44ffaf6CAS |

Kong, Q., Xie, B., Li, J., Huan, Y., Huang, T., Wei, R., Lv, J., Liu, S., and Liu, Z. (2014). Identification and characterization of an oocyte factor required for porcine nuclear reprogramming. J. Biol. Chem. 289, 6960–6968.
Identification and characterization of an oocyte factor required for porcine nuclear reprogramming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjvV2jur8%3D&md5=abcfa857700a2f724b4529ac9e5952beCAS | 24474691PubMed |

Labrecque, R., Vigneault, C., Blondin, P., and Sirard, M. A. (2013). Gene expression analysis of bovine oocytes with high developmental competence obtained from FSH-stimulated animals. Mol. Reprod. Dev. 80, 428–440.
| 1:CAS:528:DC%2BC3sXmsVejsL4%3D&md5=edd4f4af05d2544c2dbf8066d9f71d14CAS | 23559376PubMed |

Lequarre, A. S., Vigneron, C., Ribaucour, F., Holm, P., Donnay, I., Dalbies-Tran, R., Callesen, H., and Mermillod, P. (2005). Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology 63, 841–859.
Influence of antral follicle size on oocyte characteristics and embryo development in the bovine.Crossref | GoogleScholarGoogle Scholar | 15629802PubMed |

Li, L., Zheng, P., and Dean, J. (2010). Maternal control of early mouse development. Development 137, 859–870.
Maternal control of early mouse development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1Kjs7k%3D&md5=34028fd4196b7af3922bee30ae736f89CAS | 20179092PubMed |

Maalouf, W. E., Alberio, R., and Campbell, K. H. (2008). Differential acetylation of histone H4 lysine during development of in vitro fertilized, cloned and parthenogenetically activated bovine embryos. Epigenetics 3, 199–209.
Differential acetylation of histone H4 lysine during development of in vitro fertilized, cloned and parthenogenetically activated bovine embryos.Crossref | GoogleScholarGoogle Scholar | 18698155PubMed |

Macaulay, A. D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M. A., Clarke, H. J., Khandjian, E. W., Richard, F. J., Hyttel, P., and Robert, C. (2014). The gametic synapse: RNA transfer to the bovine oocyte. Biol. Reprod. 91, 90.
The gametic synapse: RNA transfer to the bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 25143353PubMed |

Machado, S. A., Reichenbach, H. D., Weppert, M., Wolf, E., and Goncalves, P. B. (2006). The variability of ovum pick-up response and in vitro embryo production from monozygotic twin cows. Theriogenology 65, 573–583.
The variability of ovum pick-up response and in vitro embryo production from monozygotic twin cows.Crossref | GoogleScholarGoogle Scholar | 16045974PubMed |

Mamo, S., Carter, F., Lonergan, P., Leal, C. L., Al Naib, A., McGettigan, P., Mehta, J. P., Evans, A. C., and Fair, T. (2011). Sequential analysis of global gene expression profiles in immature and in vitro matured bovine oocytes: potential molecular markers of oocyte maturation. BMC Genomics 12, 151.
Sequential analysis of global gene expression profiles in immature and in vitro matured bovine oocytes: potential molecular markers of oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktVWisLw%3D&md5=b02f0f4ec8e42081dec8644906026733CAS | 21410957PubMed |

Pan, H., Ma, P., Zhu, W., and Schultz, R. M. (2008). Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev. Biol. 316, 397–407.
Age-associated increase in aneuploidy and changes in gene expression in mouse eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVKrtLw%3D&md5=a112cc0d42e5e681bde336e2c404177aCAS | 18342300PubMed |

Ponter, A. A., Guyader-Joly, C., Nuttinck, F., Grimard, B., and Humblot, P. (2012). Oocyte and embryo production and quality after OPU-IVF in dairy heifers given diets varying in their n-6/n-3 fatty acid ratio. Theriogenology 78, 632–645.
Oocyte and embryo production and quality after OPU-IVF in dairy heifers given diets varying in their n-6/n-3 fatty acid ratio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFertrk%3D&md5=90153de869af3a42bfb99ffb61b4ad7dCAS | 22537996PubMed |

Richter, J. D. (1999). Cytoplasmic polyadenylation in development and beyond. Microbiol. Mol. Biol. Rev. 63, 446.
| 1:STN:280:DyaK1M3os1ektg%3D%3D&md5=152ca3b5873b79ac4d508db5c1d8cfddCAS | 10357857PubMed |

Ritchie, M. E., Silver, J., Oshlack, A., Holmes, M., Diyagama, D., Holloway, A., and Smyth, G. K. (2007). A comparison of background correction methods for two-colour microarrays. Bioinformatics 23, 2700–2707.
A comparison of background correction methods for two-colour microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1KmtLjM&md5=8ccc863b0ce1507374b7bf644122737aCAS | 17720982PubMed |

Romar, R., De Santis, T., Papillier, P., Perreau, C., Thelie, A., Dell’Aquila, M. E., Mermillod, P., and Dalbies-Tran, R. (2011). Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age. Reprod. Domest. Anim. 46, e23–e30.
Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itlOhuw%3D%3D&md5=4a9eaff08fd4eda11ae79efe27346a56CAS | 20403124PubMed |

Sacan, A., Ferhatosmanoglu, N., and Ferhatosmanoglu, H. (2009). MicroarrayDesigner: an online search tool and repository for near-optimal microarray experimental designs. BMC Bioinformatics 10, 304.
MicroarrayDesigner: an online search tool and repository for near-optimal microarray experimental designs.Crossref | GoogleScholarGoogle Scholar | 19772626PubMed |

Scantland, S., Tessaro, I., Macabelli, C. H., Macaulay, A. D., Cagnone, G., Fournier, E., Luciano, A. M., and Robert, C. (2014). The adenosine salvage pathway as an alternative to mitochondrial production of ATP in maturing mammalian oocytes. Biol. Reprod. 91, 75.
The adenosine salvage pathway as an alternative to mitochondrial production of ATP in maturing mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 25078684PubMed |

Smyth, G. K. (2005) limma: linear models for microarray data. In ‘Bioinformatics and Computational Biology Solutions Using R and Bioconductor’. (Eds R. Gentleman, V. Carey, W. Huber, R. Irizarry and S. Dudoit.) pp. 397–420. (Springer: New York.)

Stringfellow, D. A., and Givens, M. D. (2010) ‘Manual of the International Embryo Transfer Society: A Procedural Guide and General Information for the Use of Embryo Transfer Technology Emphasizing Sanitary Procedures.’ 4th edn. (International Embryo Transfer Society: Savoy, IL.)

Su, Y. Q., Sugiura, K., Woo, Y., Wigglesworth, K., Kamdar, S., Affourtit, J., and Eppig, J. J. (2007). Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev. Biol. 302, 104–117.
Selective degradation of transcripts during meiotic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntlOmsg%3D%3D&md5=fa46c598e23528e95e08c324ad279882CAS | 17022963PubMed |

Tamassia, M., Heyman, Y., Lavergne, Y., Richard, C., Gelin, V., Renard, J. P., and Chastant-Maillard, S. (2003). Evidence of oocyte donor cow effect over oocyte production and embryo development in vitro. Reproduction 126, 629–637.
Evidence of oocyte donor cow effect over oocyte production and embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslaq&md5=89fce1c70b4c5d6b1559e9e1be137967CAS | 14611636PubMed |

Thélie, A., Papillier, P., Pennetier, S., Perreau, C., Traverso, J. M., Uzbekova, S., Mermillod, P., Joly, C., Humblot, P., and Dalbiès-Tran, R. (2007). Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev. Biol. 7, 125.
Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar | 17988387PubMed |

Thelie, A., Papillier, P., Perreau, C., Uzbekova, S., Hennequet-Antier, C., and Dalbies-Tran, R. (2009). Regulation of bovine oocyte-specific transcripts during in vitro oocyte maturation and after maternal–embryonic transition analyzed using a transcriptomic approach. Mol. Reprod. Dev. 76, 773–782.
Regulation of bovine oocyte-specific transcripts during in vitro oocyte maturation and after maternal–embryonic transition analyzed using a transcriptomic approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKjs7w%3D&md5=c85d0576c7733f65f4a4230773b1f5a5CAS | 19343788PubMed |

Torner, H., Ghanem, N., Ambros, C., Holker, M., Tomek, W., Phatsara, C., Alm, H., Sirard, M. A., Kanitz, W., Schellander, K., and Tesfaye, D. (2008). Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction 135, 197–212.
Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1yrtLw%3D&md5=8822a5addba98a911658babebd8dc479CAS | 18239049PubMed |

Wit, E., Nobile, A., and Khanin, R. (2005). Near-optimal designs for dual channel microarray studies. J. R. Stat. Soc. Ser. C Appl. Stat. 54, 817–830.
Near-optimal designs for dual channel microarray studies.Crossref | GoogleScholarGoogle Scholar |