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

Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes

A. Bunel A , A. L. Nivet A , P. Blondin B , C. Vigneault B , F. J. Richard A and M. A. Sirard A C
+ Author Affiliations
- Author Affiliations

A Centre de Recherche en Biologie de la Reproduction, Faculté des Sciences de l’Agriculture et de l’Alimentation, Département des Sciences Animales, Université Laval, Québec, QC G1V 0A6, Canada.

B L’Alliance Boviteq, 19320 Grand rang St-François, Saint-Hyacinthe, Québec, QC J2T 5H1, Canada.

C Corresponding author. Email: marc-andre.sirard@fsaa.ulaval.ca

Reproduction, Fertility and Development 26(6) 855-865 https://doi.org/10.1071/RD13061
Submitted: 23 February 2013  Accepted: 4 June 2013   Published: 5 July 2013

Abstract

The final days before ovulation impact significantly on follicular function and oocyte quality. This study investigated the cumulus cell (CC) transcriptomic changes during the oocyte developmental competence acquisition period. Six dairy cows were used for 24 oocyte collections and received FSH twice daily over 3 days, followed by FSH withdrawal for 20, 44, 68 and 92 h in four different oestrous cycles for each of the six cows. Half of the cumulus–oocyte complexes were subjected to in vitro maturation, fertilisation and culture to assess blastocyst rate. The other half of the CC underwent microarray analysis (n = 3 cows, 12 oocyte collections) and qRT-PCR (n = 3 other cows, 12 oocyte collections). According to blastocyst rates, 20 h of FSH withdrawal led to under-differentiated follicles (49%), 44 and 68 h to the most competent follicles (71% and 61%) and 92 h to over-differentiated ones (51%). Ten genes, from the gene lists corresponding to the three different follicular states, were subjected to qRT-PCR. Interestingly, CYP11A1 and NSDHL gene expression profiles reflected the blastocyst rate. However most genes were associated with the over-differentiated status: GATM, MAN1A1, VNN1 and NRP1. The early period of FSH withdrawal has a minimal effect on cumulus gene expression, whereas the longest period has a very significant one and indicates the beginning of the atresia process.

Additional keywords: coasting, follicular cells, FSH withdrawal, in vitro maturation, microarray.


References

Aparicio, I. M., Garcia-Herreros, M., O’Shea, L. C., Hensey, C., Lonergan, P., and Fair, T. (2011). Expression, regulation and function of progesterone receptors in bovine cumulus–oocyte complexes during in vitro maturation. Biol. Reprod. 84, 910–921.
Expression, regulation and function of progesterone receptors in bovine cumulus–oocyte complexes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGisrw%3D&md5=f35dcb1280177fd3ef99f08a6acb6721CAS | 21228216PubMed |

Assidi, M., Dieleman, S. J., and Sirard, M. A. (2010). Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Reproduction 140, 835–852.
Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFKqtb4%3D&md5=6629f0dda324ce31bb9081c4ddadb81cCAS | 20724459PubMed |

Assou, S., Haouzi, D., Mahmoud, K., Aouacheria, A., Guillemin, Y., Pantesco, V., Reme, T., Dechaud, H., De Vos, J., and Hamamah, S. (2008). A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol. Hum. Reprod. 14, 711–719.
A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2gtw%3D%3D&md5=36329239ec45abd45983c43de0f1deb2CAS | 19028806PubMed |

Berruyer, C., Martin, F. M., Castellano, R., Macone, A., Malergue, F., Garrido-Urbani, S., Millet, V., Imbert, J., Dupre, S., Pitari, G., Naquet, P., and Galland, F. (2004). Vanin-1–/– mice exhibit a glutathione-mediated tissue resistance to oxidative stress. Mol. Cell. Biol. 24, 7214–7224.
Vanin-1–/– mice exhibit a glutathione-mediated tissue resistance to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlOjtL4%3D&md5=86082f3a25865f50cbb322b9f139f626CAS | 15282320PubMed |

Bettegowda, A., Patel, O. V., Lee, K. B., Park, K. E., Salem, M., Yao, J., Ireland, J. J., and Smith, G. W. (2008). Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications. Biol. Reprod. 79, 301–309.
Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWmsLo%3D&md5=b025586980df0dc567c5fd26f66bb0d6CAS | 18417713PubMed |

Blondin, P., Bousquet, D., Twagiramungu, H., Barnes, F., and Sirard, M. A. (2002). Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol. Reprod. 66, 38–43.
Manipulation of follicular development to produce developmentally competent bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1ylsA%3D%3D&md5=40dd11f59fc74e77fa737ce4840b4fe1CAS | 11751261PubMed |

Cheriyath, V., Leaman, D. W., and Borden, E. C. (2011). Emerging roles of FAM14 family members (G1P3/ISG 6–16 and ISG12/IFI27) in innate immunity and cancer. J. Interferon Cytokine Res. 31, 173–181.
Emerging roles of FAM14 family members (G1P3/ISG 6–16 and ISG12/IFI27) in innate immunity and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1Ohtw%3D%3D&md5=4989394474b8543339ea9973a6a87ee1CAS | 20939681PubMed |

Cillo, F., Brevini, T. A., Antonini, S., Paffoni, A., Ragni, G., and Gandolfi, F. (2007). Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 134, 645–650.
Association between human oocyte developmental competence and expression levels of some cumulus genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVCisw%3D%3D&md5=585cfa71f21428505a557729d7852e9eCAS | 17965254PubMed |

Eppig, J. J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–838.
Oocyte control of ovarian follicular development and function in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVWjsw%3D%3D&md5=ec70e9109e26ec24fd1da9fdc5425372CAS | 11732978PubMed |

Duncan, W. C., van den Driesche, S., and Fraser, H. M. (2008). Inhibition of vascular endothelial growth factor in the primate ovary up-regulates hypoxia-inducible factor-1alpha in the follicle and corpus luteum. Endocrinology 149, 3313–3320.
Inhibition of vascular endothelial growth factor in the primate ovary up-regulates hypoxia-inducible factor-1alpha in the follicle and corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1amurY%3D&md5=e0d632eebf222fc6521e063df4c2bc3eCAS | 18388198PubMed |

Feuerstein, P., Cadoret, V., Dalbies-Tran, R., Guerif, F., Bidault, R., and Royere, D. (2007). Gene expression in human cumulus cells: one approach to oocyte competence. Hum. Reprod. 22, 3069–3077.
Gene expression in human cumulus cells: one approach to oocyte competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlKltLjP&md5=ad0fd6027269e1a35577310a038469d1CAS | 17951581PubMed |

Feuerstein, P., Puard, V., Chevalier, C., Teusan, R., Cadoret, V., Guerif, F., Houlgatte, R., and Royere, D. (2012). Genomic assessment of human cumulus cell marker genes as predictors of oocyte developmental competence: impact of various experimental factors. PLoS ONE 7, e40449.
Genomic assessment of human cumulus cell marker genes as predictors of oocyte developmental competence: impact of various experimental factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCgu7rI&md5=03c5bdff15dacc6d8fbcaf4ba6c0e4b2CAS | 22848380PubMed |

First, N. L., Leibfried-Rutledge, M. L., and Sirard, M. A. (1988). Cytoplasmic control of oocyte maturation and species differences in the development of maturational competence. Prog. Clin. Biol. Res. 267, 1–46.
| 1:CAS:528:DyaL1MXltVKh&md5=18fca449e3f30ebeed3e38545387192bCAS | 3070560PubMed |

Fischer, B., Kunzel, W., Kleinstein, J., and Gips, H. (1992). Oxygen tension in follicular fluid falls with follicle maturation. Eur. J. Obstet. Gynecol. Reprod. Biol. 43, 39–43.
Oxygen tension in follicular fluid falls with follicle maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK387ks1Klsw%3D%3D&md5=7bac959c2bd73163c6d03dbb0cc372e8CAS | 1737607PubMed |

Gebhardt, K. M., Feil, D. K., Dunning, K. R., Lane, M., and Russell, D. L. (2011). Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer. Fertil. Steril. 96, 47–52.
Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosFWgsbY%3D&md5=c60eb2b36306aee3d5d18eda4c6dadf9CAS | 21575950PubMed |

Gilchrist, R. B., Ritter, L. J., and Armstrong, D. T. (2004). Oocyte–somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–446.
Oocyte–somatic cell interactions during follicle development in mammals.Crossref | GoogleScholarGoogle Scholar | 15271471PubMed |

Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVKmurY%3D&md5=97f7a19cad1bb4c5a191a9fe4e6ab0c5CAS | 18175787PubMed |

Good, P. J., Rebbert, M. L., and Dawid, I. B. (1993). Three new members of the RNP protein family in Xenopus. Nucleic Acids Res. 21, 999–1006.
Three new members of the RNP protein family in Xenopus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkt1ejtr0%3D&md5=3e2e53c517f302ef19cb3386886b6facCAS | 8451200PubMed |

Grupen, C. G., and Armstrong, D. T. (2010). Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM. Reprod. Fertil. Dev. 22, 1100–1109.
Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVOgu7vN&md5=1852eef0ffa8cef12e7a50b30c403e80CAS | 20797348PubMed |

Guidobaldi, H. A., Teves, M. E., Unates, D. R., Anastasia, A., and Giojalas, L. C. (2008). Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte–cumulus complex. PLoS ONE 3, e3040.
Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte–cumulus complex.Crossref | GoogleScholarGoogle Scholar | 18725941PubMed |

Hamel, M., Dufort, I., Robert, C., Leveille, M. C., Leader, A., and Sirard, M. A. (2010). Genomic assessment of follicular marker genes as pregnancy predictors for human IVF. Mol. Hum. Reprod. 16, 87–96.
Genomic assessment of follicular marker genes as pregnancy predictors for human IVF.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlCisA%3D%3D&md5=7d5b9f64f8f823892aa8959dccc931e6CAS | 19778949PubMed |

Hasegawa, J., Yanaihara, A., Iwasaki, S., Otsuka, Y., Negishi, M., Akahane, T., and Okai, T. (2005). Reduction of progesterone receptor expression in human cumulus cells at the time of oocyte collection during IVF is associated with good embryo quality. Hum. Reprod. 20, 2194–2200.
Reduction of progesterone receptor expression in human cumulus cells at the time of oocyte collection during IVF is associated with good embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1Gnurw%3D&md5=51c5165a93d5cddd3743147d82f60848CAS | 15802315PubMed |

Hasegawa, J., Yanaihara, A., Iwasaki, S., Mitsukawa, K., Negishi, M., and Okai, T. (2007). Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI. J. Assist. Reprod. Genet. 24, 463–466.
Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI.Crossref | GoogleScholarGoogle Scholar | 17846881PubMed |

Irving-Rodgers, H. F., Harland, M. L., Sullivan, T. R., and Rodgers, R. J. (2009). Studies of granulosa cell maturation in dominant and subordinate bovine follicles: novel extracellular matrix focimatrix is co-ordinately regulated with cholesterol side-chain cleavage CYP11A1. Reproduction 137, 825–834.
Studies of granulosa cell maturation in dominant and subordinate bovine follicles: novel extracellular matrix focimatrix is co-ordinately regulated with cholesterol side-chain cleavage CYP11A1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKgtbo%3D&md5=51557ea3e22925bf1c319d48ef2c8c64CAS | 19261832PubMed |

Katsumata, T., Noguchi, S., Yonezawa, N., Tanokura, M., and Nakano, M. (1996). Structural characterization of the n-linked carbohydrate chains of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Eur. J. Biochem. 240, 448–453.
Structural characterization of the n-linked carbohydrate chains of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsF2gtL8%3D&md5=26a475cb866ac6b83ea9076a767613cbCAS | 8841411PubMed |

Knight, P. G., and Glister, C. (2003). Local roles of TGF-beta superfamily members in the control of ovarian follicle development. Anim. Reprod. Sci. 78, 165–183.
Local roles of TGF-beta superfamily members in the control of ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gtr4%3D&md5=9c23198fde442c95dea4512590136041CAS | 12818643PubMed |

Kuo, S. W., Ke, F. C., Chang, G. D., Lee, M. T., and Hwang, J. J. (2011). Potential role of follicle-stimulating hormone (FSH) and transforming growth factor (TGFbeta1) in the regulation of ovarian angiogenesis. J. Cell. Physiol. 226, 1608–1619.
Potential role of follicle-stimulating hormone (FSH) and transforming growth factor (TGFbeta1) in the regulation of ovarian angiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1GisL8%3D&md5=51f5f66f078d060caaa77ba15a640f17CAS | 20945379PubMed |

Kurschat, P., Bielenberg, D., Rossignol-Tallandier, M., Stahl, A., and Klagsbrun, M. (2006). Neuron restrictive silencer factor NRSF/REST is a transcriptional repressor of neuropilin-1 and diminishes the ability of semaphorin 3A to inhibit keratinocyte migration. J. Biol. Chem. 281, 2721–2729.
Neuron restrictive silencer factor NRSF/REST is a transcriptional repressor of neuropilin-1 and diminishes the ability of semaphorin 3A to inhibit keratinocyte migration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVehtw%3D%3D&md5=efd719350bfb433b9479da4b4870abbdCAS | 16330548PubMed |

Lee, M. S., Liu, C. H., Lee, T. H., Wu, H. M., Huang, C. C., Huang, L. S., Chen, C. M., and Cheng, E. H. (2010). Association of creatin kinase B and peroxiredoxin 2 expression with age and embryo quality in cumulus cells. J. Assist. Reprod. Genet. 27, 629–639.
Association of creatin kinase B and peroxiredoxin 2 expression with age and embryo quality in cumulus cells.Crossref | GoogleScholarGoogle Scholar | 20721618PubMed |

Liu, Z., Rudd, M. D., Hernandez-Gonzalez, I., Gonzalez-Robayna, I., Fan, H. Y., Zeleznik, A. J., and Richards, J. S. (2009). FSH and FOXO1 regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells. Mol. Endocrinol. 23, 649–661.
FSH and FOXO1 regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFCgtrw%3D&md5=cb59719c8d31d70b986fdd6abd630fdbCAS | 19196834PubMed |

McKenzie, L. J., Pangas, S. A., Carson, S. A., Kovanci, E., Cisneros, P., Buster, J. E., Amato, P., and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum. Reprod. 19, 2869–2874.
Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crotVyisA%3D%3D&md5=3bc7b20c436ff6bc47fad14216d965f5CAS | 15471935PubMed |

Mingoti, G. Z., Garcia, J. M., and Rosa-e-Silva, A. A. (2002). Steroidogenesis in cumulus cells of bovine cumulus–oocyte complexes matured in vitro with BSA and different concentrations of steroids. Anim. Reprod. Sci. 69, 175–186.
Steroidogenesis in cumulus cells of bovine cumulus–oocyte complexes matured in vitro with BSA and different concentrations of steroids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xms1Citg%3D%3D&md5=9909d6997e3bf7307366f4083a07cdbaCAS | 11812628PubMed |

Nivet, A. L., Bunel, A., Labrecque, R., Belanger, J., Vigneault, C., Blondin, P., and Sirard, M. A. (2012). FSH withdrawal improves developmental competence of oocytes in the bovine model. Reproduction 143, 165–171.
FSH withdrawal improves developmental competence of oocytes in the bovine model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1Kkt70%3D&md5=641f3a053a565bc7e1ef2cd4aa535ceeCAS | 22080141PubMed |

Nivet, A. L., Vigneault, C., Blondin, P., and Sirard, M. A. (2013). Changes in granulosa cells gene expression associated with increased oocyte competence in bovine. Reproduction 145, 555–565.
Changes in granulosa cells gene expression associated with increased oocyte competence in bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWmsbnJ&md5=0bcc8949d812877c620883ff544432d6CAS | 23564726PubMed |

Nuttinck, F., Marquant-Le Guienne, B., Clement, L., Reinaud, P., Charpigny, G., and Grimard, B. (2008). Expression of genes involved in prostaglandin E2 and progesterone production in bovine cumulus–oocyte complexes during in vitro maturation and fertilization. Reproduction 135, 593–603.
Expression of genes involved in prostaglandin E2 and progesterone production in bovine cumulus–oocyte complexes during in vitro maturation and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Wqtbg%3D&md5=eee029907bdf9f373400106edfc076f4CAS | 18411408PubMed |

Ohashi, M., Mizushima, N., Kabeya, Y., and Yoshimori, T. (2003). Localization of mammalian NAD(P)H steroid dehydrogenase-like protein on lipid droplets. J. Biol. Chem. 278, 36 819–36 829.
Localization of mammalian NAD(P)H steroid dehydrogenase-like protein on lipid droplets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnt1ejtbw%3D&md5=bf2bb2201143873bf40a6ee38f376cb7CAS |

Pitari, G., Malergue, F., Martin, F., Philippe, J. M., Massucci, M. T., Chabret, C., Maras, B., Dupre, S., Naquet, P., and Galland, F. (2000). Pantetheinase activity of membrane-bound Vanin-1: lack of free cysteamine in tissues of Vanin-1 deficient mice. FEBS Lett. 483, 149–154.
Pantetheinase activity of membrane-bound Vanin-1: lack of free cysteamine in tissues of Vanin-1 deficient mice.Crossref | GoogleScholarGoogle Scholar | 11042271PubMed |

Regassa, A., Rings, F., Hoelker, M., Cinar, U., Tholen, E., Looft, C., Schellander, K., and Tesfaye, D. (2011). Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells. BMC Genomics 12, 57.
Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvVKmt7k%3D&md5=beb87f7034f7a991ada40f347cd0b8f2CAS | 21261964PubMed |

Revah, I., Gadella, B. M., Flesch, F. M., Colenbrander, B., and Suarez, S. S. (2000). Physiological state of bull sperm affects fucose- and mannose-binding properties. Biol. Reprod. 62, 1010–1015.
Physiological state of bull sperm affects fucose- and mannose-binding properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFajtLY%3D&md5=3d76cea4627d14123d7adddbbfcace5eCAS | 10727271PubMed |

Robert, C., Nieminen, J., Dufort, I., Gagne, D., Grant, J. R., Cagnone, G., Plourde, D., Nivet, A. L., Fournier, E., Paquet, E., Blazejczyk, M., Rigault, P., Juge, N., and Sirard, M. A. (2011). Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays. Mol. Reprod. Dev. 78, 651–664.
Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGns7vK&md5=90672a103801857bbf3c1c8d7419f125CAS | 21812063PubMed |

Rossignol, M., Pouyssegur, J., and Klagsbrun, M. (2003). Characterization of the neuropilin-1 promoter; gene expression is mediated by the transcription factor Sp1. J. Cell. Biochem. 88, 744–757.
Characterization of the neuropilin-1 promoter; gene expression is mediated by the transcription factor Sp1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslWisL0%3D&md5=27ac25457e0ff1f21bef8a6fad0c016cCAS | 12577308PubMed |

Shimizu, T., Jayawardana, B. C., Nishimoto, H., Kaneko, E., Tetsuka, M., and Miyamoto, A. (2006). Hormonal regulation and differential expression of neuropilin (NRP)-1 and NRP-2 genes in bovine granulosa cells. Reproduction 131, 555–559.
Hormonal regulation and differential expression of neuropilin (NRP)-1 and NRP-2 genes in bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs12jsLk%3D&md5=fdf28795fc908be5a6a02d4e80866c73CAS | 16514198PubMed |

Shin, S. Y., Lee, H. J., Ko, D. S., Lee, H. C., and Park, W. I. (2005). The regulators of VEGF expression in mouse ovaries. Yonsei Med. J. 46, 679–686.
The regulators of VEGF expression in mouse ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSrtLnJ&md5=fcc2d44fd13e3417e48736a912954488CAS | 16259067PubMed |

Sirard, M. A., and Coenen, K. (2006). In vitro maturation and embryo production in cattle. Methods Mol. Biol. 348, 35–42.
In vitro maturation and embryo production in cattle.Crossref | GoogleScholarGoogle Scholar | 16988370PubMed |

Tanghe, S., Van Soom, A., Duchateau, L., and De Kruif, A. (2004). Inhibition of bovine sperm–oocyte fusion by the p-aminophenyl derivative of d-mannose. Mol. Reprod. Dev. 67, 224–232.
Inhibition of bovine sperm–oocyte fusion by the p-aminophenyl derivative of d-mannose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVKqsg%3D%3D&md5=9a7833fa093891a043a1bdfda7e71d53CAS | 14694439PubMed |

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 |

Teves, M. E., Barbano, F., Guidobaldi, H. A., Sanchez, R., Miska, W., and Giojalas, L. C. (2006). Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil. Steril. 86, 745–749.
Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCqsLzJ&md5=355f9b1966bca42811d915cedca58991CAS | 16784744PubMed |

Valdembri, D., Caswell, P. T., Anderson, K. I., Schwarz, J. P., Konig, I., Astanina, E., Caccavari, F., Norman, J. C., Humphries, M. J., Bussolino, F., and Serini, G. (2009). Neuropilin-1/GIPC1 signalling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol. 7, e25.
Neuropilin-1/GIPC1 signalling regulates alpha5beta1 integrin traffic and function in endothelial cells.Crossref | GoogleScholarGoogle Scholar | 19175293PubMed |

Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome. Biol. 3, –RESEARCH0034.11.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar | 12184808PubMed |

van Montfoort, A. P., Geraedts, J. P., Dumoulin, J. C., Stassen, A. P., Evers, J. L., and Ayoubi, T. A. (2008). Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis. Mol. Hum. Reprod. 14, 157–168.
Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvFSisrs%3D&md5=27df8b6c0ab901d2ac89adbc9f1c99efCAS | 18204071PubMed |

Walsh, S. W., Williams, E. J., and Evans, A. C. (2011). A review of the causes of poor fertility in high milk-producing dairy cows. Anim. Reprod. Sci. 123, 127–138.
A review of the causes of poor fertility in high milk-producing dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3gt1eguw%3D%3D&md5=51937d53a3ee6cf098d104b729e5aaf2CAS | 21255947PubMed |

Yamashita, Y., Shimada, M., Okazaki, T., Maeda, T., and Terada, T. (2003). Production of progesterone from de novo-synthesized cholesterol in cumulus cells and its physiological role during meiotic resumption of porcine oocytes. Biol. Reprod. 68, 1193–1198.
Production of progesterone from de novo-synthesized cholesterol in cumulus cells and its physiological role during meiotic resumption of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVert7c%3D&md5=79c6c2666ee8579cb0493e2f02ed4fbdCAS | 12606468PubMed |

Zhang, X., Jafari, N., Barnes, R. B., Confino, E., Milad, M., and Kazer, R. R. (2005). Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil. Steril. 83, 1169–1179.
Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFaruro%3D&md5=8cdb7c32897270a6442f54dcaadf1e91CAS | 15831290PubMed |