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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Embryotropic actions of follistatin: paracrine and autocrine mediators of oocyte competence and embryo developmental progression

Sandeep K. Rajput A , KyungBon Lee A , Guo Zhenhua A B , Liu Di B , Joseph K. Folger A and George W. Smith A C
+ Author Affiliations
- Author Affiliations

A Laboratory of Mammalian Reproductive Biology and Genomics, Department of Animal Science, Michigan State University, East Lansing, MI 48824, USA.

B Animal Husbandry Research Institute of Heilongjiang Academy of Agricultural Sciences, 368 Xuefu Road, Harbin 150086, PR China.

C Corresponding author. Email: smithge7@msu.edu

Reproduction, Fertility and Development 26(1) 37-47 https://doi.org/10.1071/RD13282
Published: 5 December 2013

Abstract

Despite several decades since the birth of the first test tube baby and the first calf derived from an in vitro-fertilised embryo, the efficiency of assisted reproductive technologies remains less than ideal. Poor oocyte competence is a major factor limiting the efficiency of in vitro embryo production. Developmental competence obtained during oocyte growth and maturation establishes the foundation for successful fertilisation and preimplantation embryonic development. Regulation of molecular and cellular events during fertilisation and embryo development is mediated, in part, by oocyte-derived factors acquired during oocyte growth and maturation and programmed by factors of follicular somatic cell origin. The available evidence supports an important intrinsic role for oocyte-derived follistatin and JY-1 proteins in mediating embryo developmental progression after fertilisation, and suggests that the paracrine and autocrine actions of oocyte-derived growth differentiation factor 9, bone morphogenetic protein 15 and follicular somatic cell-derived members of the fibroblast growth factor family impact oocyte competence and subsequent embryo developmental progression after fertilisation. An increased understanding of the molecular mechanisms mediating oocyte competence and stage-specific developmental events during early embryogenesis is crucial for further improvements in assisted reproductive technologies.

Additional keywords: assisted reproductive technologies, bovine, early embryonic development, egg, TGFβ signalling.


References

Amiridis, G. S., and Cseh, S. (2012). Assisted reproductive technologies in the reproductive management of small ruminants. Anim. Reprod. Sci. 130, 152–161.
Assisted reproductive technologies in the reproductive management of small ruminants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zht1GhtQ%3D%3D&md5=f4585e7139940b8432846c420500a03fCAS | 22381207PubMed |

Balemans, W., and Van Hul, W. (2002). Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250, 231–250.
Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsFSnt78%3D&md5=662de7d5dc44f5d0c5ae2830e9088487CAS | 12376100PubMed |

Barnes, F. L., and First, N. L. (1991). Embryonic transcription in in vitro cultured bovine embryos. Mol. Reprod. Dev. 29, 117–123.
Embryonic transcription in in vitro cultured bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFWhurs%3D&md5=a594fdef3758a028e0c7b21a7715fc87CAS | 1878221PubMed |

Battaglia, D. E., Klein, N. A., and Soules, M. R. (1996). Changes in centrosomal domains during meiotic maturation in the human oocyte. Mol. Hum. Reprod. 2, 845–851.
Changes in centrosomal domains during meiotic maturation in the human oocyte.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szotVCgtw%3D%3D&md5=2d3d65cf6639ae1e7e6846c3504e3356CAS | 9237224PubMed |

Bavister, B. D. (1995). Culture of preimplantation embryos: facts and artifacts. Hum. Reprod. Update 1, 91–148.
Culture of preimplantation embryos: facts and artifacts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2Fps1Cisw%3D%3D&md5=628fc147a2fc59f739cd692a36d2cadaCAS | 15726768PubMed |

Ben-Haroush, A., Abir, R., Ao, A., Jin, S., Kessler-Icekson, G., Feldberg, D., and Fisch, B. (2005). Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses. Fertil. Steril. 84, 1257–1268.
Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOqtb7N&md5=9dfc60028a3365d4b00d8d101f3740a1CAS | 16210019PubMed |

Bettegowda, A., Yao, J., Sen, A., Li, Q., Lee, K.-B., Kobayashi, Y., Patel, O. V., Coussens, P. M., Ireland, J. J., and Smith, G. W. (2007). JY-1, an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle. Proc. Natl Acad. Sci. USA 104, 17 602–17 607.
JY-1, an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht12msbjJ&md5=2f8141e23e1c808c036b8bb3aeb041fbCAS |

Bettegowda, A., Lee, K. B., and Smith, G. W. (2008). Cytoplasmic and nuclear determinants of the maternal to embryonic transition. Reprod. Fertil. Dev. 20, 45–53.
Cytoplasmic and nuclear determinants of the maternal to embryonic transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFCis7Y%3D&md5=a14a213ceb5791728a2114016c54d1deCAS | 18154697PubMed |

Betts, D. H., and Madan, P. (2008). Permanent embryo arrest: molecular and cellular concepts. Mol. Hum. Reprod. 14, 445–453.
Permanent embryo arrest: molecular and cellular concepts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSjsr7I&md5=506ca89f7001f577cee6085595e33e19CAS | 18511487PubMed |

Borowczyk, E., Caton, J. S., Redmer, D. A., Bilski, J. J., Weigl, R. M., Vonnahme, K. A., Borowicz, P. P., Kirsch, J. D., Kraft, K. C., Reynolds, L. P., and Grazul-Bilska, A. T. (2006). Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep. J. Anim. Sci. 84, 1593–1599.
| 1:CAS:528:DC%2BD28XkvFOqsb8%3D&md5=b395b79e73f67e1ce4cbc173fa9baa23CAS | 16699117PubMed |

Bultman, S. J., Gebuhr, T. C., Pan, H., Svoboda, P., Schultz, R. M., and Magnuson, T. (2006). Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 20, 1744–1754.
Maternal BRG1 regulates zygotic genome activation in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvV2ksLg%3D&md5=8001718971a74a6598a4bf3b6e639373CAS | 16818606PubMed |

Buratini, J., Pinto, M. G., Castilho, A. C., Amorim, R. L., Giometti, I. C., Portela, V. M., Nicola, E. S., and Price, C. A. (2007). Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2B, in bovine follicles. Biol. Reprod. 77, 743–750.
Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2B, in bovine follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFahsb3F&md5=a768ca63abd45d53a1697ce431525915CAS | 17582010PubMed |

Burns, K. H., Viveiros, M. M., Ren, Y., Wang, P., DeMayo, F. J., Frail, D. E., Eppig, J. J., and Matzuk, M. M. (2003). Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300, 633–636.
Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVymu7w%3D&md5=2413a9cf49901ceef2a6a228d13f0f50CAS | 12714744PubMed |

Caixeta, E. S., Sutton-McDowall, M. L., Gilchrist, R. B., Thompson, J. G., Price, C. A., Machado, M. F., Lima, P. F., and Buratini, J. (2013). Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus-oocyte complexes. Reproduction 146, 27–35.
Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus-oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFejsLbJ&md5=c1dabdf35ff95cc29ba2e66e6ce925f8CAS | 23641036PubMed |

Calarco, P. G., Donahue, R. P., and Szollosi, D. (1972). Germinal vesicle breakdown in the mouse oocyte. J. Cell Sci. 10, 369–385.
| 1:STN:280:DyaE387lvVygug%3D%3D&md5=d0e59c4ed0f664df0d5624e3c354a140CAS | 5018030PubMed |

Camp, T. A., Rahal, J. O., and Mayo, K. E. (1991). Cellular localization and hormonal regulation of follicle-stimulating hormone and luteinizing hormone receptor messenger RNAs in the rat ovary. Mol. Endocrinol. 5, 1405–1417.
Cellular localization and hormonal regulation of follicle-stimulating hormone and luteinizing hormone receptor messenger RNAs in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslWjt7Y%3D&md5=47d3af5aee4775044dd640602e7b2ac4CAS | 1723141PubMed |

Canipari, R., Epifano, O., Siracusa, G., and Salustri, A. (1995). Mouse oocytes inhibit plasminogen activator production by ovarian cumulus and granulosa cells. Dev. Biol. 167, 371–378.
Mouse oocytes inhibit plasminogen activator production by ovarian cumulus and granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjs1eksbo%3D&md5=7784779ee0dafe57150db6ea321a02deCAS | 7851658PubMed |

Cheng, Y., Gaughan, J., Midic, U., Han, Z., Liang, C. G., Patel, B. G., and Latham, K. E. (2013). Systems genetics implicates cytoskeletal genes in oocyte control of cloned embryo quality. Genetics 193, 877–896.
Systems genetics implicates cytoskeletal genes in oocyte control of cloned embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWnu7rP&md5=7b9f73980eb5681e6b543f958fddd8b9CAS | 23307892PubMed |

Cox, J. F., and Alfaro, V. (2007). In vitro fertilization and development of OPU derived goat and sheep oocytes. Reprod. Domest. Anim. 42, 83–87.
In vitro fertilization and development of OPU derived goat and sheep oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s%2FitVaqtA%3D%3D&md5=86943dca5a9db922dfa919fa9ec3c88fCAS | 17214779PubMed |

Damiani, P., Fissore, R. A., Cibelli, J. B., Long, C. R., Balise, J. J., Robl, J. M., and Duby, R. T. (1996). Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol. Reprod. Dev. 45, 521–534.
Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsVWgt7k%3D&md5=0fd398202043e198851a5c32f6fdccdeCAS | 8956291PubMed |

Daniels, R., Hall, V., and Trounson, A. O. (2000). Analysis of gene transcription in bovine nuclear transfer embryos reconstructed with granulosa cell nuclei. Biol. Reprod. 63, 1034–1040.
Analysis of gene transcription in bovine nuclear transfer embryos reconstructed with granulosa cell nuclei.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslyltLY%3D&md5=167e84d80f2cefbfa50e07144f9b3894CAS | 10993824PubMed |

Davis, W., and Schultz, R. M. (1997). Role of the first round of DNA replication in reprogramming gene expression in the preimplantation mouse embryo. Mol. Reprod. Dev. 47, 430–434.
Role of the first round of DNA replication in reprogramming gene expression in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkt1Cjsb4%3D&md5=97231cfc05cfa915b49f28f5a931973dCAS | 9211427PubMed |

Davis, B. J., Lennard, D. E., Lee, C. A., Tiano, H. F., Morham, S. G., Wetsel, W. C., and Langenbach, R. (1999). Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta. Endocrinology 140, 2685–2695.
Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtlKhtb4%3D&md5=494c2a67ea07771d06baffcf1e6a6771CAS | 10342859PubMed |

De Sousa, P. A., Caveney, A., Westhusin, M. E., and Watson, A. J. (1998). Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology 49, 115–128.
Temporal patterns of embryonic gene expression and their dependence on oogenetic factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFCrug%3D%3D&md5=a72c7e75ea19e315ed9f7b1aacf63d88CAS | 10732125PubMed |

Diaz, F. J., Wigglesworth, K., and Eppig, J. J. (2007). Oocytes determine cumulus cell lineage in mouse ovarian follicles. J. Cell Sci. 120, 1330–1340.
Oocytes determine cumulus cell lineage in mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsFSjtLw%3D&md5=6f0160ba29a608f9ac940abd07cd9fd0CAS | 17389684PubMed |

Dong, J., Albertini, D. F., Nishimori, K., Kumar, T. R., Lu, N., and Matzuk, M. M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–535.
Growth differentiation factor-9 is required during early ovarian folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1GrsL0%3D&md5=fbb33b034202b0ae72df13e0dc389e1fCAS | 8849725PubMed |

Downs, S. M., and Mastropolo, A. M. (1994). The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev. Biol. 162, 154–168.
The participation of energy substrates in the control of meiotic maturation in murine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVyitLs%3D&md5=87207f0cd39847c08c51d874fd69585bCAS | 8125183PubMed |

Dragovic, R. A., Ritter, L. J., Schulz, S. J., Amato, F., Armstrong, D. T., and Gilchrist, R. B. (2005). Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology 146, 2798–2806.
Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkslehsrg%3D&md5=464f3aea34db8106781e69902d64bd54CAS | 15761035PubMed |

Edwards, R. G., Fishel, S. B., Cohen, J., Fehilly, C. B., Purdy, J. M., Slater, J. M., Steptoe, P. C., and Webster, J. M. (1984). Factors influencing the success of in vitro fertilization for alleviating human infertility. J. In Vitro Fert. Embryo Transf. 1, 3–23.
Factors influencing the success of in vitro fertilization for alleviating human infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M3mtlWkuw%3D%3D&md5=6c5978d2f068c9e1a7c7b22a7cf7d066CAS | 6242159PubMed |

Eppig, J. J. (1981). Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biol. Reprod. 25, 191–195.
Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlsVChtr8%3D&md5=7e5c227f15aaa677f78a63a3789b2e3aCAS | 6793100PubMed |

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 |

Eppig, J. J., Wigglesworth, K., and Pendola, F. L. (2002). The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc. Natl Acad. Sci. USA 99, 2890–2894.
The mammalian oocyte orchestrates the rate of ovarian follicular development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Crtb0%3D&md5=e81155320a89b7fde1ba4ec9a340a86bCAS | 11867735PubMed |

Eppig, J. J., Pendola, F. L., Wigglesworth, K., and Pendola, J. K. (2005). Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol. Reprod. 73, 351–357.
Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1yqsLk%3D&md5=0ba0ce7f81f904fd48de58613495b41bCAS | 15843493PubMed |

Fields, S. D., Hansen, P. J., and Ealy, A. D. (2011). Fibroblast growth factor requirements for in vitro development of bovine embryos. Theriogenology 75, 1466–1475.
Fibroblast growth factor requirements for in vitro development of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt1KjsLk%3D&md5=a333d96652f859cf3d115f8e4a4c5afbCAS | 21295834PubMed |

Folger, J. K., Zhenhua, G., Di, L., Camsari, C., Knott, J. G., and Smith, G. W. (2013). Opposing effects of follistatin versus the BMP binding protein noggin on ealry development of bovine embryos in vitro. In ‘Proceedings of the 46th Annual Meeting, Society for the Study of Reproduction’, 22–25 July 2013, Montreal, Canada. Available from http://precis.preciscentral.com/utils/ip/SearchResults.asp?EventId=7750ca35

Fülöp, C., Szánto, 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 |

Galloway, S. M., McNatty, K. P., Cambridge, L. M., Laitinen, M. P., Juengel, J. L., Jokiranta, T. S., McLaren, R. J., Luiro, K., Dodds, K. G., Montgomery, G. W., Beattie, A. E., Davis, G. H., and Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279–283.
Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvFKltbs%3D&md5=149d3099a91c35d86335b481fb27241fCAS | 10888873PubMed |

Gilchrist, R. B., Ritter, L. J., and Armstrong, D. T. (2004a). 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., Ritter, L. J., Cranfield, M., Jeffery, L. A., Amato, F., Scott, S. J., Myllymaa, S., Kaivo-Oja, N., Lankinen, H., Mottershead, D. G., Groome, N. P., and Ritvos, O. (2004b). Immunoneutralization of growth differentiation factor 9 reveals it partially accounts for mouse oocyte mitogenic activity. Biol. Reprod. 71, 732–739.
Immunoneutralization of growth differentiation factor 9 reveals it partially accounts for mouse oocyte mitogenic activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFejtLY%3D&md5=ec81a99fa518ebe057e64d91a1ff7d36CAS | 15128595PubMed |

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 |

Glister, C., Kemp, C. F., and Knight, P. G. (2004). Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction 127, 239–254.
Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVWrtL8%3D&md5=6ac97304298d9dccd17780b70c091d74CAS | 15056790PubMed |

Gosden, R., and Lee, B. (2010). Portrait of an oocyte: our obscure origin. J. Clin. Invest. 120, 973–983.
Portrait of an oocyte: our obscure origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVChsrY%3D&md5=d048c57c0b308876870f05a146148492CAS | 20364095PubMed |

Gurtu, V. E., Verma, S., Grossmann, A. H., Liskay, R. M., Skarnes, W. C., and Baker, S. M. (2002). Maternal effect for DNA mismatch repair in the mouse. Genetics 160, 271–277.
| 1:CAS:528:DC%2BD38XhsFKqsbk%3D&md5=a72b61307c1d1b509da49e7ae605ea2fCAS | 11805062PubMed |

He, C. L., Damiani, P., Parys, J. B., and Fissore, R. A. (1997). Calcium, calcium release receptors, and meiotic resumption in bovine oocytes. Biol. Reprod. 57, 1245–1255.
Calcium, calcium release receptors, and meiotic resumption in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvFSktb0%3D&md5=b92cfaecbe089bf0b4ac31cc34452fa9CAS | 9369194PubMed |

Heikinheimo, O., and Gibbons, W. E. (1998). The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine. Mol. Hum. Reprod. 4, 745–756.
The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtFWksbs%3D&md5=18d858b72c6b40c06210edc376adbe17CAS | 9733431PubMed |

Hizaki, H., Segi, E., Sugimoto, Y., Hirose, M., Saji, T., Ushikubi, F., Matsuoka, T., Noda, Y., Tanaka, T., Yoshida, N., Narumiya, S., and Ichikawa, A. (1999). Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc. Natl Acad. Sci. USA 96, 10 501–10 506.
Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFemsrg%3D&md5=373a1d914e41a053287c301ed5662ff0CAS |

Hussein, T. S., Froiland, D. A., Amato, F., Thompson, J. G., and Gilchrist, R. B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257–5268.
Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWru7rK&md5=ee8bcd954ae434cb8b69c0f07e43eb02CAS | 16263764PubMed |

Hussein, T. S., Thompson, J. G., and Gilchrist, R. B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–521.
Oocyte-secreted factors enhance oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2gsb4%3D&md5=b2e5191f8ae9d995fe2b016c8c4c10b6CAS | 16854407PubMed |

Hussein, T. S., Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2011). Temporal effects of exogenous oocyte-secreted factors on bovine oocyte developmental competence during IVM. Reprod. Fertil. Dev. 23, 576–584.
Temporal effects of exogenous oocyte-secreted factors on bovine oocyte developmental competence during IVM.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFKnsLw%3D&md5=0cebd8c266c58746a7e8f9b06c25ecd2CAS | 21557924PubMed |

Inge, G. B., Brinsden, P. R., and Elder, K. T. (2005). Oocyte number per live birth in IVF: were Steptoe and Edwards less wasteful? Hum. Reprod. 20, 588–592.
Oocyte number per live birth in IVF: were Steptoe and Edwards less wasteful?Crossref | GoogleScholarGoogle Scholar | 15689347PubMed |

Inman, G. J., Nicolas, F. J., Callahan, J. F., Harling, J. D., Gaster, L. M., Reith, A. D., Laping, N. J., and Hill, C. S. (2002). SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65–74.
SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Kqtb4%3D&md5=e084d51c78c2cec14109d85b11968de2CAS | 12065756PubMed |

Kaivo-Oja, N., Mottershead, D. G., Mazerbourg, S., Myllymaa, S., Duprat, S., Gilchrist, R. B., Groome, N. P., Hsueh, A. J., and Ritvos, O. (2005). Adenoviral gene transfer allows Smad-responsive gene promoter analyses and delineation of type I receptor usage of transforming growth factor-beta family ligands in cultured humangranulosa luteal cells. J. Clin. Endocrinol. Metab. 90, 271–278.
Adenoviral gene transfer allows Smad-responsive gene promoter analyses and delineation of type I receptor usage of transforming growth factor-beta family ligands in cultured humangranulosa luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFertw%3D%3D&md5=2d5ebb6e5437fbf75c75a2308cd0a715CAS | 15483083PubMed |

Kaivo-Oja, N., Jeffery, L. A., Ritvos, O., and Mottershead, D. G. (2006). Smad signalling in the ovary. Reprod. Biol. Endocrinol. 4, 21.
Smad signalling in the ovary.Crossref | GoogleScholarGoogle Scholar | 16611366PubMed |

Kang, M. K., and Han, S. J. (2011). Post-transcriptional and post-translational regulation during mouse oocyte maturation. BMB Reports 44, 147–157.
Post-transcriptional and post-translational regulation during mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFClur4%3D&md5=1e711841090ac037ec705fd1b4ee31f2CAS | 21429291PubMed |

Kathirvel, M., Soundian, E., and Kumanan, V. (2013). Differential expression dynamics of growth differentiation factor9 (GDF9) and bone morphogenetic factor15 (BMP15) mRNA transcripts during maturation of buffalo () cumulus–oocyte complexes. SpringerPlus 2, 206.
Differential expression dynamics of growth differentiation factor9 (GDF9) and bone morphogenetic factor15 (BMP15) mRNA transcripts during maturation of buffalo () cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 23724366PubMed |

Krause, C., Guzman, A., and Knaus, P. (2011). Noggin. Int. J. Biochem. Cell Biol. 43, 478–481.
Noggin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFGmtL8%3D&md5=4164d693c49067815a018bea2b1f7c56CAS | 21256973PubMed |

Krisher, R. L. (2004). The effect of oocyte quality on development. J Anim Sci 82, E14–E23.
| 15471793PubMed |

Laurinčik, J., Hyttel, P., Baran, V., Eckert, J., Lucas-Hahn, A., Pivko, J., Niemann, H., Brem, G., and Schellander, K. (1998). A detailed analysis of pronucleus development in bovine zygotes in vitro: cell-cycle chronology and ultrastructure. Mol. Reprod. Dev. 50, 192–199.
A detailed analysis of pronucleus development in bovine zygotes in vitro: cell-cycle chronology and ultrastructure.Crossref | GoogleScholarGoogle Scholar | 9590536PubMed |

Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H., and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol. Reprod. 67, 767–775.
Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsV2js7Y%3D&md5=5f6f0fad6db3e4374cc9ff92580670a7CAS | 12193383PubMed |

Lechniak, D., Pers-Kamczyc, E., and Pawlak, P. (2008). Timing of the first zygotic cleavage as a marker of developmental potential of mammalian embryos. Reprod. Biol. 8, 23–42.
Timing of the first zygotic cleavage as a marker of developmental potential of mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 18432305PubMed |

Lee, K. B., Bettegowda, A., Wee, G., Ireland, J. J., and Smith, G. W. (2009). Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis. Endocrinology 150, 2463–2471.
Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFCisrg%3D&md5=ff82bd76b50df730aea915af94cdd0edCAS | 19179440PubMed |

Leese, H. J. (1995). Metabolic control during preimplantation mammalian development. Hum. Reprod. Update 1, 63–72.
Metabolic control during preimplantation mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3jsFSmuw%3D%3D&md5=4c98b646ebce31589791fc48bc06a616CAS | 9080207PubMed |

Li, R., Norman, R. J., Armstrong, D. T., and Gilchrist, R. B. (2000). Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol. Reprod. 63, 839–845.
Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFCiu7g%3D&md5=0ebb0b94388faae78b4796fd949b1bf5CAS | 10952929PubMed |

Li, L., Baibakov, B., and Dean, J. (2008). A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev. Cell 15, 416–425.
A subcortical maternal complex essential for preimplantation mouse embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOit7vL&md5=223359704b589197c846cb9597936a5fCAS | 18804437PubMed |

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=fc0a728bc68c08404f6776e8a30b6394CAS | 20179092PubMed |

Liang, C. G., Su, Y. Q., Fan, H. Y., Schatten, H., and Sun, Q. Y. (2007). Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol. Endocrinol. 21, 2037–2055.
Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSqtb7N&md5=e34cf91761d7e128cdd16758c296b358CAS | 17536005PubMed |

Lim, H., Paria, B. C., Das, S. K., Dinchuk, J. E., Langenbach, R., Trzaskos, J. M., and Dey, S. K. (1997). Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91, 197–208.
Multiple female reproductive failures in cyclooxygenase 2-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntVyiu7o%3D&md5=6b5e05faa9ff75cd58bb6a7e675b992eCAS | 9346237PubMed |

Lin, S. Y., Morrison, J. R., Phillips, D. J., and de Kretser, D. M. (2003). Regulation of ovarian function by the TGF-beta superfamily and follistatin. Reproduction 126, 133–148.
Regulation of ovarian function by the TGF-beta superfamily and follistatin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFyjsbs%3D&md5=88ea947c3b4e07d077f1559cec7d9dd0CAS | 12887271PubMed |

Lonergan, P., and Fair, T. (2008). In vitro-produced bovine embryos: dealing with the warts. Theriogenology 69, 17–22.
In vitro-produced bovine embryos: dealing with the warts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2sjhvVOqtg%3D%3D&md5=5db4be5f3a8bceef8802633bd39aa56dCAS | 17950823PubMed |

Ma, J., Zeng, F., Schultz, R. M., and Tseng, H. (2006). Basonuclin: a novel mammalian maternal-effect gene. Development 133, 2053–2062.
Basonuclin: a novel mammalian maternal-effect gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtV2itbo%3D&md5=77d4ec6841a8855d1bd3a8848a1c2d5fCAS | 16624857PubMed |

Manova, K., Huang, E. J., Angeles, M., De Leon, V., Sanchez, S., Pronovost, S. M., Besmer, P., and Bachvarova, R. F. (1993). The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia. Dev. Biol. 157, 85–99.
The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXksVWktr0%3D&md5=e4458ca89a4ed5824a4fbdcf2cd1cc68CAS | 7683286PubMed |

Mapletoft, R. J., and Hasler, J. F. (2005). Assisted reproductive technologies in cattle: a review. Rev. Sci. Tech. 24, 393–403.
| 1:STN:280:DC%2BD2MvksVaitw%3D%3D&md5=742ef081786c295743d0e6afee9b5aceCAS | 16110904PubMed |

Matzuk, M. M., Burns, K. H., Viveiros, M. M., and Eppig, J. J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178–2180.
Intercellular communication in the mammalian ovary: oocytes carry the conversation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFGhsbw%3D&md5=ceb8b0b1eee8c8846954bca35e8757afCAS | 12077402PubMed |

Mazerbourg, S., Klein, C., Roh, J., Kaivo-Oja, N., Mottershead, D. G., Korchynskyi, O., Ritvos, O., and Hsueh, A. J. (2004). Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol. Endocrinol. 18, 653–665.
Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivFCqtrs%3D&md5=687cdcff7633514a1d9d4ca005b4002aCAS | 14684852PubMed |

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 |

McLay, D. W., and Clarke, H. J. (2003). Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125, 625–633.
Remodelling the paternal chromatin at fertilization in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVKmur0%3D&md5=28533e54241451fa8872e7175c183f35CAS | 12713425PubMed |

McNatty, K. P., Juengel, J. L., Reader, K. L., Lun, S., Myllymaa, S., Lawrence, S. B., Western, A., Meerasahib, M. F., Mottershead, D. G., Groome, N. P., Ritvos, O., and Laitinen, M. P. (2005). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 129, 481–487.
Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjs1ertb0%3D&md5=3fcac6e1069bbbbde6ec8ef0d4f29523CAS | 15798023PubMed |

Mehmood, A., Anwar, M., and Saqlan Naqvi, S. M. (2007). Capacitation of frozen thawed buffalo bull (Bubalus bubalis) spermatozoa with higher heparin concentrations. Reprod. Domest. Anim. 42, 376–379.
Capacitation of frozen thawed buffalo bull (Bubalus bubalis) spermatozoa with higher heparin concentrations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2svhvV2rtA%3D%3D&md5=8d7025ee374ea6089ead1bcbcaa5b42aCAS | 17635774PubMed |

Michael, D. D., Alvarez, I. M., Ocon, O. M., Powell, A. M., Talbot, N. C., Johnson, S. E., and Ealy, A. D. (2006). Fibroblast growth factor-2 is expressed by the bovine uterus and stimulates interferon-tau production in bovine trophectoderm. Endocrinology 147, 3571–3579.
Fibroblast growth factor-2 is expressed by the bovine uterus and stimulates interferon-tau production in bovine trophectoderm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlOrsbk%3D&md5=e801e58c4b7f53fde2988956ddf052f2CAS | 16574787PubMed |

Miller, D. J., Eckert, J. J., Lazzari, G., Duranthon-Richoux, V., Sreenan, J., Morris, D., Galli, C., Renard, J. P., and Fleming, T. P. (2003). Tight junction messenger RNA expression levels in bovine embryos are dependent upon the ability to compact and in vitro culture methods. Biol. Reprod. 68, 1394–1402.
Tight junction messenger RNA expression levels in bovine embryos are dependent upon the ability to compact and in vitro culture methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVeruro%3D&md5=48562be9f4027415fe4570e962a4baddCAS | 12606485PubMed |

Miyoshi, T., Otsuka, F., Inagaki, K., Otani, H., Takeda, M., Suzuki, J., Goto, J., Ogura, T., and Makino, H. (2007). Differential regulation of steroidogenesis by bone morphogenetic proteins in granulosa cells: involvement of extracellularly regulated kinase signaling and oocyte actions in follicle-stimulating hormone-induced estrogen production. Endocrinology 148, 337–345.
Differential regulation of steroidogenesis by bone morphogenetic proteins in granulosa cells: involvement of extracellularly regulated kinase signaling and oocyte actions in follicle-stimulating hormone-induced estrogen production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFSisQ%3D%3D&md5=4adc827954c41ceea7392e5d6ff5a58aCAS | 17008391PubMed |

Munné, S., Alikani, M., Tomkin, G., Grifo, J., and Cohen, J. (1995). Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertil. Steril. 64, 382–391.
| 7615118PubMed |

Nuttinck, F., Gall, L., Ruffini, S., Laffont, L., Clement, L., Reinaud, P., Adenot, P., Grimard, B., Charpigny, G., and Marquant-Le Guienne, B. (2011). PTGS2-related PGE2 affects oocyte MAPK phosphorylation and meiosis progression in cattle: late effects on early embryonic development. Biol. Reprod. 84, 1248–1257.
PTGS2-related PGE2 affects oocyte MAPK phosphorylation and meiosis progression in cattle: late effects on early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFemu7s%3D&md5=d634fa4fea2813ef89ac6edc62c22f3cCAS | 21293029PubMed |

Otsuka, F., Moore, R. K., Iemura, S., Ueno, N., and Shimasaki, S. (2001). Follistatin inhibits the function of the oocyte-derived factor BMP-15. Biochem. Biophys. Res. Commun. 289, 961–966.
Follistatin inhibits the function of the oocyte-derived factor BMP-15.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVWjuro%3D&md5=24bd9d8888ac7e1eeb1cb2ecec7d0ac9CAS | 11741284PubMed |

Otsuka, F., McTavish, K. J., and Shimasaki, S. (2011). Integral role of GDF-9 and BMP-15 in ovarian function. Mol. Reprod. Dev. 78, 9–21.
Integral role of GDF-9 and BMP-15 in ovarian function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvV2muw%3D%3D&md5=50f1b9c72dbe425ee67940ea80eb0189CAS | 21226076PubMed |

Patel, O. V., Bettegowda, A., Ireland, J. J., Coussens, P. M., Lonergan, P., and Smith, G. W. (2007). Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes. Reproduction 133, 95–106.
Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1aju7w%3D&md5=d54c38ed9969a300fcf199cc6a359efaCAS | 17244736PubMed |

Payer, B., Saitou, M., Barton, S. C., Thresher, R., Dixon, J. P., Zahn, D., Colledge, W. H., Carlton, M. B., Nakano, T., and Surani, M. A. (2003). Stella is a maternal effect gene required for normal early development in mice. Curr. Biol. 13, 2110–2117.
Stella is a maternal effect gene required for normal early development in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1Oqsb4%3D&md5=d92693b4a290ff9af5c440abd91e5e21CAS | 14654002PubMed |

Pennetier, S., Uzbekova, S., Perreau, C., Papillier, P., Mermillod, P., and Dalbies-Tran, R. (2004). Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos. Biol. Reprod. 71, 1359–1366.
Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGquro%3D&md5=65cac0a1628a54c7731e35e4d2ce612dCAS | 15189828PubMed |

Peura, T. T., Kleemann, D. O., Rudiger, S. R., Nattrass, G. S., McLaughlan, C. J., and Walker, S. K. (2003). Effect of nutrition of oocyte donor on the outcomes of somatic cell nuclear transfer in the sheep. Biol. Reprod. 68, 45–50.
Effect of nutrition of oocyte donor on the outcomes of somatic cell nuclear transfer in the sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVym&md5=310f6d37d9a2baed08460d68c998e7acCAS | 12493694PubMed |

Prentice-Biensch, J. R., Singh, J., Mapletoft, R. J., and Anzar, M. (2012). Vitrification of immature bovine cumulus–oocyte complexes: effects of cryoprotectants, the vitrification procedure and warming time on cleavage and embryo development. Reprod. Biol. Endocrinol. 10, 73.
Vitrification of immature bovine cumulus–oocyte complexes: effects of cryoprotectants, the vitrification procedure and warming time on cleavage and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVequ7%2FI&md5=7ed18e1e86f8728602c444217126f857CAS | 22954348PubMed |

Revel, F., Mermillod, P., Peynot, N., Renard, J. P., and Heyman, Y. (1995). Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows. J. Reprod. Fertil. 103, 115–120.
Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3it1CqsA%3D%3D&md5=64b1629f4d5561c234303a50b17d7f4eCAS | 7707286PubMed |

Richards, J. S. (2005). Ovulation: new factors that prepare the oocyte for fertilization. Mol. Cell. Endocrinol. 234, 75–79.
Ovulation: new factors that prepare the oocyte for fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1SqtLk%3D&md5=a90397eb5d608968f2965b42e4d7bdbeCAS | 15836955PubMed |

Salumets, A., Hyden-Granskog, C., Makinen, S., Suikkari, A. M., Tiitinen, A., and Tuuri, T. (2003). Early cleavage predicts the viability of human embryos in elective single embryo transfer procedures. Hum. Reprod. 18, 821–825.
Early cleavage predicts the viability of human embryos in elective single embryo transfer procedures.Crossref | GoogleScholarGoogle Scholar | 12660278PubMed |

Salustri, A., Garlanda, C., Hirsch, E., De Acetis, M., Maccagno, A., Bottazzi, B., Doni, A., Bastone, A., Mantovani, G., Beck Peccoz, P., Salvatori, G., Mahoney, D. J., Day, A. J., Siracusa, G., Romani, L., and Mantovani, A. (2004). PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131, 1577–1586.
PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKltbc%3D&md5=b320d43478a9597479743a6ffb87dc3fCAS | 14998931PubMed |

Sheth, B., Fesenko, I., Collins, J. E., Moran, B., Wild, A. E., Anderson, J. M., and Fleming, T. P. (1997). Tight junction assembly during mouse blastocyst formation is regulated by late expression of ZO-1 alpha+ isoform. Development 124, 2027–2037.
| 1:CAS:528:DyaK2sXjvV2ru7w%3D&md5=75f11f93f5b9c4485493445b1e59b177CAS | 9169849PubMed |

Sirard, M. A., Richard, F., Blondin, P., and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
Contribution of the oocyte to embryo quality.Crossref | GoogleScholarGoogle Scholar | 16256189PubMed |

Spicer, L. J., Aad, P. Y., Allen, D. T., Mazerbourg, S., Payne, A. H., and Hsueh, A. J. (2008). Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biol. Reprod. 78, 243–253.
Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Kru7o%3D&md5=46dabb3e1cc65c2deec147c8ac9e363eCAS | 17959852PubMed |

Sturmey, R. G., Reis, A., Leese, H. J., and McEvoy, T. G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44, 50–58.
Role of fatty acids in energy provision during oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar | 19660080PubMed |

Su, Y. Q., Wu, X., O’Brien, M. J., Pendola, F. L., Denegre, J. N., Matzuk, M. M., and Eppig, J. J. (2004). Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte–cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev. Biol. 276, 64–73.
Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte–cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVOlur0%3D&md5=434bff1673d2b8f0cc1eb7be79d35534CAS | 15531364PubMed |

Su, Y. Q., Sugiura, K., and Eppig, J. J. (2009). Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin. Reprod. Med. 27, 32–42.
Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVGntr0%3D&md5=5fc64ae171d24a88e687a8d6e3f2e036CAS | 19197803PubMed |

Sugiura, K., Pendola, F. L., and Eppig, J. J. (2005). Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev. Biol. 279, 20–30.
Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlemtb4%3D&md5=8d0ae004906415fd4328ac872f34117fCAS | 15708555PubMed |

Sugiura, K., Su, Y. Q., Diaz, F. J., Pangas, S. A., Sharma, S., Wigglesworth, K., O’Brien, M. J., Matzuk, M. M., Shimasaki, S., and Eppig, J. J. (2007). Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134, 2593–2603.
Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsFeju7k%3D&md5=e0f70e0d9043f5ebab28ae6065f35251CAS | 17553902PubMed |

Sutovsky, P., and Schatten, G. (1997). Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol. Reprod. 56, 1503–1512.
Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlKguro%3D&md5=2ec79a688c8004c5d03ae093834a731bCAS | 9166704PubMed |

Sutton-McDowall, M. L., Mottershead, D. G., Gardner, D. K., Gilchrist, R. B., and Thompson, J. G. (2012). Metabolic differences in bovine cumulus–oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15. Biol. Reprod. 87, 1–8.
Metabolic differences in bovine cumulus–oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15.Crossref | GoogleScholarGoogle Scholar |

Takahashi, T., Morrow, J. D., Wang, H., and Dey, S. K. (2006). Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J. Biol. Chem. 281, 37 117–37 129.
Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1elt7%2FP&md5=e263c16b81a1b603145b13f064f4116eCAS |

Thibault, C., Gerard, M., and Menezo, Y. (1975). Preovulatory and ovulatory mechanisms in oocyte maturation. J. Reprod. Fertil. 45, 605–610.
Preovulatory and ovulatory mechanisms in oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XktFSlsQ%3D%3D&md5=694ad6c6d010e9c14069635c2dda7132CAS | 812988PubMed |

Thomas, R. E., Thompson, J. G., Armstrong, D. T., and Gilchrist, R. B. (2004). Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol. Reprod. 71, 1142–1149.
Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqt7Y%3D&md5=6f6d004eb386594a3ea2d7e3ba9741d2CAS | 15189837PubMed |

Van Montfoort, A. P., Dumoulin, J. C., Kester, A. D., and Evers, J. L. (2004). Early cleavage is a valuable addition to existing embryo selection parameters: a study using single embryo transfers. Hum. Reprod. 19, 2103–2108.
Early cleavage is a valuable addition to existing embryo selection parameters: a study using single embryo transfers.Crossref | GoogleScholarGoogle Scholar | 15243008PubMed |

VandeVoort, C. A., Mtango, N. R., Lee, Y. S., Smith, G. W., and Latham, K. E. (2009). Differential effects of follistatin on nonhuman primate oocyte maturation and pre-implantation embryo development in vitro. Biol. Reprod. 81, 1139–1146.
Differential effects of follistatin on nonhuman primate oocyte maturation and pre-implantation embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2lt7jK&md5=2ce8149ca4dbc8a56e1add995399a618CAS | 19641179PubMed |

Viuff, D., Avery, B., Greve, T., King, W. A., and Hyttel, P. (1996). Transcriptional activity in in vitro produced bovine two- and four-cell embryos. Mol. Reprod. Dev. 43, 171–179.
Transcriptional activity in in vitro produced bovine two- and four-cell embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XpslWisQ%3D%3D&md5=f6045f3e05e18bdfcb3ccce117abb5ffCAS | 8824915PubMed |

Ward, W. S. (2010). Function of sperm chromatin structural elements in fertilization and development. Mol. Hum. Reprod. 16, 30–36.
Function of sperm chromatin structural elements in fertilization and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOhtrrI&md5=94e9a74eb1960db83f6334a1f838a2a0CAS | 19748904PubMed |

Wiesen, J. F., and Midgley, A. R. (1993). Changes in expression of connexin 43 gap junction messenger ribonucleic acid and protein during ovarian follicular growth. Endocrinology 133, 741–746.
Changes in expression of connexin 43 gap junction messenger ribonucleic acid and protein during ovarian follicular growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmsVKlsLo%3D&md5=bedf32f94b44774ae7540fe20f8bf6a0CAS | 8393773PubMed |

Wu, X., Viveiros, M. M., Eppig, J. J., Bai, Y., Fitzpatrick, S. L., and Matzuk, M. M. (2003). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187–191.
Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsFSktg%3D%3D&md5=3b32ee0eacabd52499b3d8a463166900CAS | 12539046PubMed |

Yang, Q. E., Fields, S. D., Zhang, K., Ozawa, M., Johnson, S. E., and Ealy, A. D. (2011). Fibroblast growth factor 2 promotes primitive endoderm development in bovine blastocyst outgrowths. Biol. Reprod. 85, 946–953.
Fibroblast growth factor 2 promotes primitive endoderm development in bovine blastocyst outgrowths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2is7bJ&md5=5a32befda16e2e5484fc13f65569b627CAS | 21778141PubMed |

Yao, J., Ren, X., Ireland, J. J., Coussens, P. M., Smith, T. P., and Smith, G. W. (2004). Generation of a bovine oocyte cDNA library and microarray: resources for identification of genes important for follicular development and early embryogenesis. Physiol. Genomics 19, 84–92.
Generation of a bovine oocyte cDNA library and microarray: resources for identification of genes important for follicular development and early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXoslShtro%3D&md5=b5a9f07993ac45f5d9bb3159b9b9eaa7CAS | 15375196PubMed |

Yeo, C. X., Gilchrist, R. B., Thompson, J. G., and Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 67–73.
Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWgsbzF&md5=3a14ae8fef165af6d8396891f9a7b813CAS | 17933754PubMed |

Zhang, L., Jiang, S., Wozniak, P. J., Yang, X., and Godke, R. A. (1995). Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro. Mol. Reprod. Dev. 40, 338–344.
Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkt1Khs7k%3D&md5=5c8bcb7377b1883ec1f1fcb8d3ef8094CAS | 7772344PubMed |

Zhang, K., Hansen, P. J., and Ealy, A. D. (2010). Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro. Reproduction 140, 815–826.
Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFKqtLY%3D&md5=28ac80fb6f011066e9dc90c36c4a0894CAS | 20876224PubMed |

Zhang, K., Hansen, P. J., and Ealy, A. D. (2011). Fibroblast growth factor 2 promotes bovine oocyte meiotic maturation and developmental competence. Reprod. Fertil. Dev. 23, 236.
Fibroblast growth factor 2 promotes bovine oocyte meiotic maturation and developmental competence.Crossref | GoogleScholarGoogle Scholar |

Zheng, P., and Dean, J. (2009). Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. Proc. Natl Acad. Sci. USA 106, 7473–7478.
Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmt1Khtrc%3D&md5=a97a952d59d2f512d8462112664fda5bCAS | 19376971PubMed |