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

Steroid hormones interact with natriuretic peptide C to delay nuclear maturation, to maintain oocyte–cumulus communication and to improve the quality of in vitro-produced embryos in cattle

Ana Caroline S. Soares A , Valentina Lodde B , Rodrigo G. Barros A , Christopher A. Price C , Alberto M. Luciano B and José Buratini A D
+ Author Affiliations
- Author Affiliations

A Ovarian Molecular Physiology Laboratory, Department of Physiology, Institute of Biosciences, Sao Paulo State University, Botucatu, Sao Paulo, 18618-970, Brazil.

B Reproductive and Developmental Biology Laboratory, Department of Health, Animal Science and Food Safety, University of Milan, Via Celoria, 10 - 20133, Milan, Italy.

C Centre de recherche en reproduction et fertility, Faculté de médecine vétérinaire, Université de Montréal, 3200 Sicotte, Saint-Hyacinthe, Québec J2S 7C6, Canada.

D Corresponding author. Email: buratini@ibb.unesp.br

Reproduction, Fertility and Development 29(11) 2217-2224 https://doi.org/10.1071/RD16320
Submitted: 16 August 2016  Accepted: 13 February 2017   Published: 30 March 2017

Abstract

In vivo, oocyte maturation is triggered by the ovulatory LH surge, whereas in vitro it is precociously induced when the cumulus–oocyte complex is removed from the follicle. Natriuretic peptide C (NPPC) delays germinal vesicle breakdown (GVBD) while increasing oocyte–cumulus communication during in vitro maturation (IVM) in cattle. In the present study we first tested the hypothesis that steroids secreted by the follicle (17β-oestradiol, progesterone and androstenedione) interact with NPPC to delay GVBD and to maintain oocyte–cumulus communication as assessed by transfer of a dye (Lucifer Yellow) from the oocyte to cumulus cells. Then, we assessed the effects of steroid hormones and NPPC, alone and in combination in a pre-IVM culture, on embryo production. The combination of NPPC with steroids delayed GVDB, increased natriuretic peptide receptor 2 (NPR2) mRNA abundance in cumulus cells during culture, and maintained oocyte–cumulus communication at levels not different from non-cultured controls. The addition of steroids and/or NPPC to a pre-IVM culture did not alter blastocyst rates after IVF, but supplementation with steroids increased blastocyst total cell number. The present study provides evidence, for the first time in cattle, that steroids interact with NPPC to regulate oocyte nuclear maturation and oocyte–cumulus communication, and improve oocyte developmental competence.

Additional keywords: amphiregulin, cumulus cells, follicle stimulating hormone, gap junctions, in vitro maturation, meiosis, natriuretic peptide receptor 2.


References

Aardema, H., Roelen, B. A., van Tol, H. T., Oei, C. H., Gadella, B. M., and Vos, P. L. (2013). Follicular 17β-estradiol and progesterone concentrations and degree of cumulus cell expansion as predictors of in vivo-matured oocyte developmental competence in superstimulated heifers. Theriogenology 80, 576–583.
Follicular 17β-estradiol and progesterone concentrations and degree of cumulus cell expansion as predictors of in vivo-matured oocyte developmental competence in superstimulated heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVKrurnF&md5=20d5a86f1df3d0a2f9712177108a4788CAS |

Albertini, D. F., Combelles, C. M., Benecchi, E., and Carabatsos, M. J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121, 647–653.
Cellular basis for paracrine regulation of ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVaisbY%3D&md5=1f238b4e423853e7101563418028658eCAS |

Albuz, F. K., Sasseville, M., Lane, M., Armstrong, D. T., Thompson, J. G., and Gilchrist, R. B. (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 25, 2999–3011.
Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbotlKnsg%3D%3D&md5=7f3e4a55365616ad1f1f715847b20391CAS |

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=cb1aaa5f0e1a564926fea71f294760edCAS |

Atef, A., François, P., Christian, V., and Marc-André, S. (2005). The potential role of gap junction communication between cumulus cells and bovine oocytes during in vitro maturation. Mol. Reprod. Dev. 71, 358–367.
The potential role of gap junction communication between cumulus cells and bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFyhsrY%3D&md5=4f2ad994f920164e0198a1c510205c91CAS |

Beg, M. A., Bergfelt, D. R., Kot, K., and Ginther, O. J. (2002). Follicle selection in cattle: dynamics of follicular fluid factors during development of follicle dominance. Biol. Reprod. 66, 120–126.
Follicle selection in cattle: dynamics of follicular fluid factors during development of follicle dominance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1yktg%3D%3D&md5=bf18c00b57da09a216e3278cbb491e31CAS |

Blaha, M., Nemcova, L., and Prochazka, R. (2015). Cyclic guanosine monophosphate does not inhibit gonadotropin-induced activation of mitogen-activated protein kinase 3/1 in pig cumulus–oocyte complexes. Reprod. Biol. Endocrinol. 13, 1.
Cyclic guanosine monophosphate does not inhibit gonadotropin-induced activation of mitogen-activated protein kinase 3/1 in pig cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar |

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=09930e76bc2df5a6c04dffcca6298bd5CAS |

El-Hayek, S., and Clarke, H. J. (2015). Follicle-stimulating hormone increases gap junctional communication between somatic and germ-line follicular compartments during murine oogenesis. Biol. Reprod. 93, 47.
Follicle-stimulating hormone increases gap junctional communication between somatic and germ-line follicular compartments during murine oogenesis.Crossref | GoogleScholarGoogle Scholar |

Emori, C., Wigglesworth, K., Fujii, W., Naito, K., Eppig, J. J., and Sugiura, K. (2013). Cooperative effects of 17β-estradiol and oocyte-derived paracrine factors on the transcriptome of mouse cumulus cells. Endocrinology 154, 4859–4872.
Cooperative effects of 17β-estradiol and oocyte-derived paracrine factors on the transcriptome of mouse cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2itL%2FM&md5=96da62b02fd38145aead8cb8a9cd7dc4CAS |

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=d573a31f6bf47a980fe3192c8653357cCAS |

Farin, C. E., Rodriguez, K. F., Alexander, J. E., Hockney, J. E., Herrick, J. R., and Kennedy-Stoskopf, S. (2007). The role of transcription in EGF- and FSH-mediated oocyte maturation in vitro. Anim. Reprod. Sci. 98, 97–112.
The role of transcription in EGF- and FSH-mediated oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Sksr0%3D&md5=f1c1cb1f02ac913bffdaca5a1fe15491CAS |

Fortune, J. E., and Hansel, W. (1985). Concentrations of steroids and gonadotropins in follicular fluid from normal heifers and heifers primed for superovulation. Biol. Reprod. 32, 1069–1079.
Concentrations of steroids and gonadotropins in follicular fluid from normal heifers and heifers primed for superovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltFKnt7Y%3D&md5=e9dccc43d1e084b1925619da6a467de1CAS |

Franciosi, F., Coticchio, G., Lodde, V., Tessaro, I., Modina, S. C., Fadini, R., Dal Canto, M., Renzini, M. M., Albertini, D. F., and Luciano, A. M. (2014). Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol. Reprod. 91, 61.
Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes.Crossref | GoogleScholarGoogle Scholar |

Gilchrist, R. B. (2011). Recent insights into oocyte–follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod. Fertil. Dev. 23, 23–31.
Recent insights into oocyte–follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation.Crossref | GoogleScholarGoogle Scholar |

Gilchrist, R. B., Luciano, A. M., Richani, D., Zeng, H., Wang, X., De Vos, M., Sugimura, S., Smitz, J., Richard, F. J., and Thompson, J. G. (2016). Oocyte maturation and quality: role of cyclic nucleotides. Reproduction 152, R143–R157.
Oocyte maturation and quality: role of cyclic nucleotides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXktlajsb4%3D&md5=a82c6ba1a0055e11804ddf7233083bbcCAS |

Grazul-Bilska, A. T., Reynolds, L. P., and Redmer, D. A. (1997). Gap junctions in the ovaries. Biol. Reprod. 57, 947–957.
Gap junctions in the ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvFSjurs%3D&md5=f583ff778031805fad9042af577a7d8fCAS |

Ireland, J. J., and Roche, J. F. (1983). Growth and differentiation of large antral follicles after spontaneous luteolysis in heifers: changes in concentration of hormones in follicular fluid and specific binding of gonadotropins to follicles. J. Anim. Sci. 57, 157–167.
Growth and differentiation of large antral follicles after spontaneous luteolysis in heifers: changes in concentration of hormones in follicular fluid and specific binding of gonadotropins to follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXkvF2msb8%3D&md5=665d3d151ef21c2f357ba1c7fb51cc54CAS |

Jakobsen, A. S., Thomsen, P. D., and Avery, B. (2006). Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro. Theriogenology 65, 870–881.
Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar |

Kaneko, H., Terada, T., Taya, K., Watanabe, G., Sasamoto, S., Hasegawa, Y., and Igarashi, M. (1991). Ovarian follicular dynamics and concentrations of oestradiol-17 beta, progesterone, luteinizing hormone and follicle stimulating hormone during the periovulatory phase of the oestrous cycle in the cow. Reprod. Fertil. Dev. 3, 529–535.
Ovarian follicular dynamics and concentrations of oestradiol-17 beta, progesterone, luteinizing hormone and follicle stimulating hormone during the periovulatory phase of the oestrous cycle in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1CrtLc%3D&md5=842a4e0c68783c14c0761c3d310a9f43CAS |

Komar, C. M., Berndtson, A. K., Evans, A. C., and Fortune, J. E. (2001). Decline in circulating estradiol during the periovulatory period is correlated with decreases in estradiol and androgen, and in messenger RNA for p450 aromatase and p450 17alpha-hydroxylase, in bovine preovulatory follicles. Biol. Reprod. 64, 1797–1805.
Decline in circulating estradiol during the periovulatory period is correlated with decreases in estradiol and androgen, and in messenger RNA for p450 aromatase and p450 17alpha-hydroxylase, in bovine preovulatory follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGgtL8%3D&md5=beb2fa7dd4f1565ba6d3933b9ad27f1bCAS |

Lodde, V., Modina, S., Galbusera, C., Franciosi, F., and Luciano, A. M. (2007). Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 74, 740–749.
Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVGrt7c%3D&md5=f02917d93ce4e19c40978e91b67d9c4fCAS |

Lodde, V., Franciosi, F., Tessaro, I., Modina, S. C., and Luciano, A. M. (2013). Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte. J. Assist. Reprod. Genet. 30, 1219–1226.
Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte.Crossref | GoogleScholarGoogle Scholar |

Luciano, A. M., Modina, S., Vassena, R., Milanesi, E., Lauria, A., and Gandolfi, F. (2004). Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol. Reprod. 70, 465–472.
Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsl2juw%3D%3D&md5=df143bd14b2b235d41dee57ebbd26da4CAS |

Luciano, A. M., Franciosi, F., Modina, S. C., and Lodde, V. (2011). Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol. Reprod. 85, 1252–1259.
Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ShsLfI&md5=f95f205bc7cbf51b7bfe82099f74bc4fCAS |

Luciano, A. M., Franciosi, F., Dieci, C., and Lodde, V. (2014). Changes in large-scale chromatin structure and function during oogenesis: a journey in company with follicular cells. Anim. Reprod. Sci. 149, 3–10.
Changes in large-scale chromatin structure and function during oogenesis: a journey in company with follicular cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFGmtLfM&md5=982023ad0029b77f5a5b116890ad1d79CAS |

Macaulay, A. D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M. A., Clarke, H. J., Khandjian, É., 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 |

Park, J. Y., Su, Y. Q., Ariga, M., Law, E., Jin, S. L., and Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.
EGF-like growth factors as mediators of LH action in the ovulatory follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVKlsg%3D%3D&md5=0fa39ea4352d45b49ef2f9668d563f95CAS |

Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=91eac11c0ea6f3f03935d293079e5320CAS |

Pincus, G., and Enzmann, E. V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J. Exp. Med. 62, 665–675.
The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3crjs1agtA%3D%3D&md5=08ff0b428aa8ffb6c73c047728f67284CAS |

Ramakers, C., Ruijter, J. M., Deprez, R. H., and Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–66.
Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1Kks70%3D&md5=826b69327963ea41db6cd141a10ae5e0CAS |

Richani, D., Wang, X., Zeng, H. T., Smitz, J., Thompson, J. G., and Gilchrist, R. B. (2014). Pre-maturation with cAMP modulators in conjunction with EGF-like peptides during in vitro maturation enhances mouse oocyte developmental competence. Mol. Reprod. Dev. 81, 422–435.
Pre-maturation with cAMP modulators in conjunction with EGF-like peptides during in vitro maturation enhances mouse oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivFais74%3D&md5=73d13cb768a8fcd3b37beec9d29988bdCAS |

Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–248.
Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=b1311147b0c039d6783153079f8b6ad3CAS |

Sánchez, F., and Smitz, J. (2012). Molecular control of oogenesis. Biochim. Biophys. Acta 1822, 1896–1912.
Molecular control of oogenesis.Crossref | GoogleScholarGoogle Scholar |

Sartori, R., Gimenes, L. U., Monteiro, P. L., Melo, L. F., Baruselli, P. S., and Bastos, M. R. (2016). Metabolic and endocrine differences between Bos taurus and Bos indicus females that impact the interaction of nutrition with reproduction. Theriogenology 86, 32–40.
Metabolic and endocrine differences between Bos taurus and Bos indicus females that impact the interaction of nutrition with reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmslKru7c%3D&md5=dc0f10d84bad61db3ddaa3df4045f305CAS |

Sugimura, S., Ritter, L. J., Sutton-McDowall, M. L., Mottershead, D. G., Thompson, J. G., and Gilchrist, R. B. (2014). Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: effects on gap junction-mediated metabolite supply. Mol. Hum. Reprod. 20, 499–513.
Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: effects on gap junction-mediated metabolite supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotF2ku78%3D&md5=28032182af3fd4b28129c24d29413f74CAS |

Sugiura, K., Su, Y. Q., Li, Q., Wigglesworth, K., Matzuk, M. M., and Eppig, J. J. (2010). Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15. Mol. Endocrinol. 24, 2303–2314.
Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVenu78%3D&md5=4e6b77d2221ff68fa53f8dda3fd82988CAS |

Zhang, M., Su, Y. Q., Sugiura, K., Xia, G., and Eppig, J. J. (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–369.
Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OisL7P&md5=f13117860c2f5b987a0fa9108bc70b0aCAS |

Zhang, M., Su, Y. Q., Sugiura, K., Wigglesworth, K., Xia, G., and Eppig, J. J. (2011). Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology 152, 4377–4385.
Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOrtb3J&md5=7011d73b7f6b1ef7c7572ba6e94237beCAS |

Zhong, Y., Lin, J., Liu, X., Hou, J., Zhang, Y., and Zhao, X. (2016). C-Type natriuretic peptide maintains domestic cat oocytes in meiotic arrest. Reprod. Fertil. Dev. 28, 1553–1559.
C-Type natriuretic peptide maintains domestic cat oocytes in meiotic arrest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhtl2msbfE&md5=32550a84b5ca4edb30025f6060afd647CAS |