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Vertebrate reproductive science and technology
REVIEW

Physiological parameters related to oocyte nuclear differentiation for the improvement of IVM/IVF outcomes in women and cattle

Jose Buratini A B * , Ana Caroline Silva Soares B , Rodrigo Garcia Barros C , Thaisy Tino Dellaqua B , Valentina Lodde C , Federica Franciosi C , Mariabeatrice Dal Canto A , Mario Mignini Renzini A and Alberto Maria Luciano C
+ Author Affiliations
- Author Affiliations

A Biogenesi Reproductive Medicine Centre – Eugin Group, Istituti Clinici Zucchi, Monza, Italy.

B Department of Structural and Functional Biology, Sao Paulo State University, Botucatu, Brazil.

C Reproductive and Developmental Biology Laboratory, Department of Health, Animal Science and Food Safety, University of Milan, Milan, Italy.

* Correspondence to: j.buratini@unesp.br

Reproduction, Fertility and Development 34(2) 27-35 https://doi.org/10.1071/RD21278
Published online: 8 November 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the IETS

Abstract

In vitro maturation (IVM) has been applied in numerous different contexts and strategies in humans and animals, but in both cases it represents a challenge still far from being overcome. Despite the large dataset produced over the last two decades on the mechanisms that govern antral follicular development and oocyte metabolism and differentiation, IVM outcomes are still unsatisfactory. This review specifically focuses on data concerning the potential consequences of using supraphysiological levels of FSH during IVM, as well as on the regulation of oocyte chromatin dynamics and its utility as a potential marker of oocyte developmental competence. Taken together, the data revisited herein indicate that a significant improvement in IVM efficacy may be provided by the integration of pre-OPU patient-specific protocols preparing the oocyte population for IVM and more physiological culture systems mimicking more precisely the follicular environment that would be experienced by the recovered oocytes until completion of metaphase II.

Keywords: bovine, cumulus cells, chromatin configuration, FSH, germinal vesicle, human, in vitro maturation (IVM), oocyte.


References

Abbassi, L, El-Hayek, S, Carvalho, KF, Wang, W, Yang, Q, Granados-Aparici, S, Mondadori, R, Bordignon, V, and Clarke, HJ (2021). Epidermal growth factor receptor signaling uncouples germ cells from the somatic follicular compartment at ovulation. Nature Communications 12, 1438.
Epidermal growth factor receptor signaling uncouples germ cells from the somatic follicular compartment at ovulation.Crossref | GoogleScholarGoogle Scholar | 33664246PubMed |

Albertini, DF, Combelles, CM, Benecchi, E, and Carabatsos, MJ (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 | 11427152PubMed |

Albertini, DF, Sanfins, A, and Combelles, CMH (2003). Origins and manifestations of oocyte maturation competencies. Reproductive BioMedicine Online 6, 410–415.
Origins and manifestations of oocyte maturation competencies.Crossref | GoogleScholarGoogle Scholar | 12831584PubMed |

Albuz, FK, Sasseville, M, Lane, M, Armstrong, DT, Thompson, JG, and Gilchrist, RB (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Human Reproduction 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 | 20870682PubMed |

Alper, MM, and Fauser, BC (2017). Ovarian stimulation protocols for IVF: is more better than less? Reproductive BioMedicine Online 34, 345–353.
Ovarian stimulation protocols for IVF: is more better than less?Crossref | GoogleScholarGoogle Scholar | 28169189PubMed |

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. Molecular Reproduction and Development 71, 358–367.
The potential role of gap junction communication between cumulus cells and bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 15822117PubMed |

Baart, EB, Martini, E, Eijkemans, MJ, Van Opstal, D, Beckers, NGM, Verhoeff, A, Macklon, NS, and Fauser, BCJM (2007). Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial. Human Reproduction 22, 980–988.
Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial.Crossref | GoogleScholarGoogle Scholar | 17204525PubMed |

Baruselli, PS, Batista, EOS, Vieira, LM, Ferreira, RM, Guerreiro, BG, Bayeux, BM, Sales, JNS, Souza, AH, and Gimenes, LU (2016). Factors that interfere with oocyte quality for in vitro production of cattle embryos: effects of different developmental & reproductive stages. Animal Reproduction 13, 264–272.
Factors that interfere with oocyte quality for in vitro production of cattle embryos: effects of different developmental & reproductive stages.Crossref | GoogleScholarGoogle Scholar |

Blanco, MR, Demyda, S, Moreno Millán, M, and Genero, E (2011). Developmental competence of in vivo and in vitro matured oocytes: a review. Biotechnology and Molecular Biology Reviews 6, 155–165.

Blondin, P, and Sirard, MA (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Molecular Reproduction and Development 41, 54–62.
Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 7619506PubMed |

Blondin, P, Coenen, K, Guilbault, LA, and Sirard, M-A (1996). Superovulation can reduce the developmental competence of bovine embryos. Theriogenology 46, 1191–1203.
Superovulation can reduce the developmental competence of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 16727982PubMed |

Blondin, P, Bousquet, D, Twagiramungu, H, Barnes, F, and Sirard, M-A (2002). Manipulation of follicular development to produce developmentally competent bovine oocytes. Biology of Reproduction 66, 38–43.
Manipulation of follicular development to produce developmentally competent bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 11751261PubMed |

Bouniol-Baly, C, Hamraoui, L, Guibert, J, Beaujean, N, Szöllösi, MS, and Debey, P (1999). Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biology of Reproduction 60, 580–587.
Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes.Crossref | GoogleScholarGoogle Scholar | 10026102PubMed |

Buratini, J, Soares, ACS, and Barros, RG (2017). Follicular environment and oocyte maturation: roles of local peptides and steroids. Animal Reproduction 14, 601–606.
Follicular environment and oocyte maturation: roles of local peptides and steroids.Crossref | GoogleScholarGoogle Scholar |

Buratini, J, Dellaqua, TT, Dal Canto, M, and Renzini, MM (2020). Oocyte secreted factors regulate FSHR and AMH mRNA levels in cumulus cells. Fertility and Sterility 114, e440.
Oocyte secreted factors regulate FSHR and AMH mRNA levels in cumulus cells.Crossref | GoogleScholarGoogle Scholar |

Caixeta, ES, Ripamonte, P, Franco, MM, Junior, JB, and Dode, MAN (2009). Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. Reproduction, Fertility and Development 21, 655–664.
Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence.Crossref | GoogleScholarGoogle Scholar |

Cakmak, H, Franciosi, F, Musa Zamah, A, Cedars, MI, and Conti, M (2016). Dynamic secretion during meiotic reentry integrates the function of the oocyte and cumulus cells. Proceedings of the National Academy of Sciences of the United States of America 113, 2424–2429.
Dynamic secretion during meiotic reentry integrates the function of the oocyte and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 26864200PubMed |

Chen, J, Torcia, S, Xie, F, Lin, C-J, Cakmak, H, Franciosi, F, Horner, K, Onodera, C, Song, JS, Cedars, MI, Ramalho-Santos, M, and Conti, M (2013). Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nature Cell Biology 15, 1415–1423.
Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 24270888PubMed |

Combelles, CM, Albertini, DF, and Racowsky, C (2003). Distinct microtubule and chromatin characteristics of human oocytes after failed in-vivo and in-vitro meiotic maturation. Human Reproduction 18, 2124–2130.
Distinct microtubule and chromatin characteristics of human oocytes after failed in-vivo and in-vitro meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 14507833PubMed |

Combelles, CM, Carabatsos, MJ, Kumar, TR, Matzuk, MM, and Albertini, DF (2004). Hormonal control of somatic cell oocyte interactions during ovarian follicle development. Molecular Reproduction and Development 69, 347–355.
Hormonal control of somatic cell oocyte interactions during ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 15349847PubMed |

Conti, M, Hsieh, M, Zamah, AM, and Oh, JS (2012). Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Molecular and Cellular Endocrinology 356, 65–73.
Novel signaling mechanisms in the ovary during oocyte maturation and ovulation.Crossref | GoogleScholarGoogle Scholar | 22101318PubMed |

Coticchio, G, Dal Canto, M, Fadini, R, Mignini Renzini, M, Guglielmo, MC, Miglietta, S, Palmerini, MG, Macchiarelli, G, and Nottola, SA (2016). Ultrastructure of human oocytes after in vitro maturation. Molecular Human Reproduction 22, 110–118.
Ultrastructure of human oocytes after in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 26646501PubMed |

Dal Canto, M, Coticchio, G, Mignini Renzini, M, De Ponti, E, Novara, PV, Brambillasca, F, Comi, R, and Fadini, R (2012). Cleavage kinetics analysis of human embryos predicts development to blastocyst and implantation. Reproductive BioMedicine Online 25, 474–480.
Cleavage kinetics analysis of human embryos predicts development to blastocyst and implantation.Crossref | GoogleScholarGoogle Scholar | 22995750PubMed |

De La Fuente, R (2006). Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Developmental Biology 292, 1–12.
Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 16466710PubMed |

De Vos, M, Smitz, J, Thompson, JG, and Gilchrist, RB (2016). The definition of IVM is clear—variations need defining. Human Reproduction 31, 2411–2415.
The definition of IVM is clear—variations need defining.Crossref | GoogleScholarGoogle Scholar | 27664204PubMed |

De Vos, M, Grynberg, M, Ho, TM, Yuan, Y, Albertini, DF, and Gilchrist, RB (2021). Perspectives on the development and future of oocyte IVM in clinical practice. Journal of Assisted Reproduction and Genetics 38, 1265–1280.
Perspectives on the development and future of oocyte IVM in clinical practice.Crossref | GoogleScholarGoogle Scholar | 34218388PubMed |

Dieci, C, Lodde, V, Labreque, R, Dufort, I, Tessaro, I, Sirard, MA, and Luciano, AM (2016). Differences in cumulus cell gene expression indicate the benefit of a pre-maturation step to improve in-vitro bovine embryo production. Molecular Human Reproduction 22, 882–897.
| 27559149PubMed |

Donnay, I, Faerge, I, Grøndahl, C, Verhaeghe, B, Sayoud, H, Ponderato, N, Galli, C, and Lazzari, G (2004). Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes. Theriogenology 62, 1093–1107.
Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes.Crossref | GoogleScholarGoogle Scholar | 15289049PubMed |

Eppig, JJ, O’Brien, MJ, Pendola, FL, and Watanabe, S (1998). Factors affecting the developmental competence of mouse oocytes grown in vitro: follicle-stimulating hormone and insulin. Biology of Reproduction 59, 1445–1453.
Factors affecting the developmental competence of mouse oocytes grown in vitro: follicle-stimulating hormone and insulin.Crossref | GoogleScholarGoogle Scholar | 9828191PubMed |

Fadini, R, Dal Canto, MB, Renzini, MM, Brambillasca, F, Comi, R, Fumagalli, D, Lain, M, Merola, M, Milani, R, and De Ponti, E (2009). Effect of different gonadotrophin priming on IVM of oocytes from women with normal ovaries: a prospective randomized study. Reproductive BioMedicine Online 19, 343–351.
Effect of different gonadotrophin priming on IVM of oocytes from women with normal ovaries: a prospective randomized study.Crossref | GoogleScholarGoogle Scholar | 19778479PubMed |

Fadini, R, Mignini Renzini, M, Dal Canto, M, Epis, A, Crippa, M, Caliari, I, Brigante, C, and Coticchio, G (2013). Oocyte in vitro maturation in normo-ovulatory women. Fertility and Sterility 99, 1162–1169.
Oocyte in vitro maturation in normo-ovulatory women.Crossref | GoogleScholarGoogle Scholar | 23433517PubMed |

Fadini, R, Coticchio, G, Brambillasca, F, Mignini Renzini, M, Novara, PV, Brigante, C, De Ponti, E, and Dal Canto, M (2015). Clinical outcomes from mature oocytes derived from preovulatory and antral follicles: reflections on follicle physiology and oocyte competence. Journal of Assisted Reproduction and Genetics 32, 255–261.
Clinical outcomes from mature oocytes derived from preovulatory and antral follicles: reflections on follicle physiology and oocyte competence.Crossref | GoogleScholarGoogle Scholar | 25449291PubMed |

Fortune, JE, and Hansel, W (1985). Concentrations of steroids and gonadotropins in follicular fluid from normal heifers and heifers primed for superovulation. Biology of Reproduction 32, 1069–1079.
Concentrations of steroids and gonadotropins in follicular fluid from normal heifers and heifers primed for superovulation.Crossref | GoogleScholarGoogle Scholar | 3926013PubMed |

Franciosi, F, Coticchio, G, Lodde, V, Tessaro, I, Modina, SC, Fadini, R, Dal Canto, M, Renzini, MM, Albertini, DF, and Luciano, AM (2014). Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biology of Reproduction 91, 61.
Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes.Crossref | GoogleScholarGoogle Scholar | 25078681PubMed |

Gilchrist, RB (2011). Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reproduction, Fertility and Development 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 |

Gimenes, LU, Ferraz, ML, Fantinato-Neto, P, Chiaratti, MR, Mesquita, LG, Sá Filho, MF, Meirelles, FV, Trinca, LA, Rennó, FP, Watanabe, YF, and Baruselli, PS (2015). The interval between the emergence of pharmacologically synchronized ovarian follicular waves and ovum pickup does not significantly affect in vitro embryo production in Bos indicusBos taurus, and Bubalus bubalis. Theriogenology 83, 385–393.
The interval between the emergence of pharmacologically synchronized ovarian follicular waves and ovum pickup does not significantly affect in vitro embryo production in Bos indicusBos taurus, and Bubalus bubalis.Crossref | GoogleScholarGoogle Scholar | 25447149PubMed |

Hyttel, P (1987). Bovine cumulus–oocyte disconnection in vitro. Anatomy and Embryology 176, 41–44.
Bovine cumulus–oocyte disconnection in vitro.Crossref | GoogleScholarGoogle Scholar | 3605648PubMed |

Hyttel, P, Callesen, H, and Greve, T (1986). Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. Reproduction 76, 645–656.
Ultrastructural features of preovulatory oocyte maturation in superovulated cattle.Crossref | GoogleScholarGoogle Scholar |

Hyttel, P, Callesen, H, Greve, T, and Schmidt, M (1991). Oocyte maturation and sperm transport in superovulated cattle. Theriogenology 35, 91–108.
Oocyte maturation and sperm transport in superovulated cattle.Crossref | GoogleScholarGoogle Scholar |

Jie, H, Zhao, M, Alqawasmeh, OAM, Chan, CPS, Lee, TL, Li, T, and Chan, DYL (2021). In vitro rescue immature oocytes – a literature review. Human Fertility 137, 1–20.
In vitro rescue immature oocytes – a literature review.Crossref | GoogleScholarGoogle Scholar |

Katz-Jaffe, MG, McCallie, BR, Preis, KA, Filipovits, J, and Gardner, DK (2009). Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes. Theriogenology 71, 939–946.
Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes.Crossref | GoogleScholarGoogle Scholar | 19150733PubMed |

Labrecque, R, Lodde, V, Dieci, C, Tessaro, I, Luciano, AM, and Sirard, MA (2015). Chromatin remodelling and histone m RNA accumulation in bovine germinal vesicle oocytes. Molecular Reproduction and Development 82, 450–462.
Chromatin remodelling and histone m RNA accumulation in bovine germinal vesicle oocytes.Crossref | GoogleScholarGoogle Scholar | 25940597PubMed |

Lima, PF, Ormond, CM, Caixeta, ES, Barros, RG, Price, CA, and Buratini, J (2016). Effect of kit ligand on natriuretic peptide precursor C and oocyte maturation in cattle. Reproduction 152, 481–489.
Effect of kit ligand on natriuretic peptide precursor C and oocyte maturation in cattle.Crossref | GoogleScholarGoogle Scholar | 27492081PubMed |

Lodde, V, Modina, S, Galbusera, C, Franciosi, F, and Luciano, AM (2007). Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Molecular Reproduction and Development 74, 740–749.
| 17075796PubMed |

Lodde, V, Modina, S, Maddox-Hyttel, P, Franciosi, F, Lauria, A, and Luciano, AM (2008). Oocyte morphology and transcriptional silencing in relation to chromatin remodeling during the final phases of bovine oocyte growth. Molecular Reproduction and Development 75, 915–924.
Oocyte morphology and transcriptional silencing in relation to chromatin remodeling during the final phases of bovine oocyte growth.Crossref | GoogleScholarGoogle Scholar | 17948251PubMed |

Lodde, V, Franciosi, F, Tessaro, I, Modina, SC, and Luciano, AM (2013). Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte. Journal of Assisted Reproduction and Genetics 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 | 23881161PubMed |

Luciano AM, Lodde V (2013) Changes of large-scale chromatin configuration during mammalian oocyte differentiation. In ‘Oogenesis’. (Eds G Coticchio, D Albertini, L De Santis) pp. 93–108. (Springer: London, UK)
| Crossref |

Luciano, AM, and Sirard, MA (2018). Successful in vitro maturation of oocytes: a matter of follicular differentiation. Biology of Reproduction 98, 162–169.
Successful in vitro maturation of oocytes: a matter of follicular differentiation.Crossref | GoogleScholarGoogle Scholar | 29165545PubMed |

Luciano, AM, 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. Biology of Reproduction 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 | 14568913PubMed |

Luciano, AM, Franciosi, F, Modina, SC, and Lodde, V (2011). Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biology of Reproduction 85, 1252–1259.
Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s).Crossref | GoogleScholarGoogle Scholar | 21816847PubMed |

Luciano, AM, 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. Animal Reproduction Science 149, 3–10.
Changes in large-scale chromatin structure and function during oogenesis: a journey in company with follicular cells.Crossref | GoogleScholarGoogle Scholar | 25028181PubMed |

Lodde V, Luciano AM, Franciosi F, Labrecque R, Sirard MA (2017) Accumulation of chromatin remodelling enzyme and histone transcripts in bovine oocytes. In ‘Oocytes. Results and problems in cell differentiation’. Vol. 63. (Ed. M Kloc) pp. 223–255. (Springer: Cham, Switzerland)
| Crossref |

Macaulay, AD, Gilbert, I, Caballero, J, Barreto, R, Fournier, E, Tossou, P, Sirard, MA, Clarke, HJ, Khandjian, EW, Richard, FJ, Hyttel, P, and Robert, C (2014). The gametic synapse: RNA transfer to the bovine oocyte. Biology of Reproduction 91, 90.
The gametic synapse: RNA transfer to the bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 25143353PubMed |

Macaulay, AD, Gilbert, I, Scantland, S, Fournier, E, Ashkar, F, Bastien, A, Saadi, HA, Gagné, D, Sirard, MA, Khandjian, EW, Richard, FJ, Hyttel, P, and Robert, C (2016). Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation. Biology of Reproduction 94, 16.
Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation.Crossref | GoogleScholarGoogle Scholar | 26586844PubMed |

Miyara, F, Migne, C, Dumont-Hassan, M, Le Meur, A, Cohen-Bacrie, P, Aubriot, FX, Glissant, A, Nathan, C, Douard, S, Stanovici, A, and Debey, P (2003). Chromatin configuration and transcriptional control in human and mouse oocytes. Molecular Reproduction and Development 64, 458–470.
Chromatin configuration and transcriptional control in human and mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 12589658PubMed |

Modina, S, Luciano, AM, Vassena, R, Baraldi-Scesi, L, Lauria, A, and Gandolfi, F (2001). Oocyte developmental competence after in vitro maturation depends on the persistence of cumulus-oocyte communications which are linked to the intracellular concentration of cAMP. Journal of Anatomy and Embryology 106, 241–248.

Nivet, AL, Bunel, A, Labrecque, R, Belanger, J, Vigneault, C, Blondin, P, and Sirard, MA (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 | 22080141PubMed |

Nogueira, D, Ron-El, R, Friedler, S, Schachter, M, Raziel, A, Cortvrindt, R, and Smitz, J (2006). Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biology of Reproduction 74, 177–184.
Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar | 16207840PubMed |

Park, JY, Su, YQ, Ariga, M, Law, E, Jin, SLC, 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 | 14726596PubMed |

Pontes, JHF, Silva, KCF, Basso, AC, Rigo, AG, Ferreira, CR, Santos, GMG, Sanches, BV, Porcionato, JPF, Vieira, PHS, Faifer, FS, Sterza, FAM, Schenk, JL, and Seneda, MM (2010). Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus-taurus dairy cows using sexed sperm. Theriogenology 74, 1349–1355.
Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus-taurus dairy cows using sexed sperm.Crossref | GoogleScholarGoogle Scholar |

Richani, D, Dunning, KR, Thompson, JG, and Gilchrist, RB (2021). Metabolic co-dependence of the oocyte and cumulus cells: essential role in determining oocyte developmental competence. Human Reproduction Update 27, 27–47.
Metabolic co-dependence of the oocyte and cumulus cells: essential role in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 33020823PubMed |

Rizos, D, Ward, F, Duffy, PAT, Boland, MP, 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. Molecular Reproduction and Development 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 | 11803560PubMed |

Romero, S, Sánchez, F, Lolicato, F, Van Ranst, H, and Smitz, J (2016). Immature oocytes from unprimed juvenile mice become a valuable source for embryo production when using C-type natriuretic peptide as essential component of culture medium. Biology of Reproduction 95, 64.
Immature oocytes from unprimed juvenile mice become a valuable source for embryo production when using C-type natriuretic peptide as essential component of culture medium.Crossref | GoogleScholarGoogle Scholar | 27488026PubMed |

Russell, DL, Gilchrist, RB, Brown, HM, and Thompson, JG (2016). Bidirectional communication between cumulus cells and the oocyte: old hands and new players? Theriogenology 86, 62–68.
Bidirectional communication between cumulus cells and the oocyte: old hands and new players?Crossref | GoogleScholarGoogle Scholar | 27160446PubMed |

Sánchez, F, Romero, S, De Vos, M, Verheyen, G, and Smitz, J (2015). Human cumulus-enclosed germinal vesicle oocytes from early antral follicles reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity. Human Reproduction 30, 1396–1409.
Human cumulus-enclosed germinal vesicle oocytes from early antral follicles reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity.Crossref | GoogleScholarGoogle Scholar | 25904637PubMed |

Sánchez, F, Lolicato, F, Romero, S, De Vos, M, Van Ranst, H, Verheyen, G, Anckaert, E, and Smitz, JEJ (2017). An improved IVM method for cumulus–oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield. Human Reproduction 32, 2056–2068.
An improved IVM method for cumulus–oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield.Crossref | GoogleScholarGoogle Scholar | 28938744PubMed |

Sanchez, F, Le, AH, Ho, VNA, Romero, S, Van Ranst, H, De Vos, M, Gilchrist, RB, Ho, TM, Vuong, LN, and Smitz, J (2019). Biphasic in vitro maturation (CAPA-IVM) specifically improves the developmental capacity of oocytes from small antral follicles. Journal of Assisted Reproduction and Genetics 36, 2135–2144.
Biphasic in vitro maturation (CAPA-IVM) specifically improves the developmental capacity of oocytes from small antral follicles.Crossref | GoogleScholarGoogle Scholar | 31399916PubMed |

Santiquet, NW, Greene, AF, Becker, J, Barfield, JP, Schoolcraft, WB, and Krisher, RL (2017). A pre-in vitro maturation medium containing cumulus oocyte complex ligand-receptor signaling molecules maintains meiotic arrest, supports the cumulus oocyte complex and improves oocyte developmental competence. Molecular Human Reproduction 23, 594–606.
A pre-in vitro maturation medium containing cumulus oocyte complex ligand-receptor signaling molecules maintains meiotic arrest, supports the cumulus oocyte complex and improves oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 28586460PubMed |

Sirard, MA (2016). Somatic environment and germinal differentiation in antral follicle: the effect of FSH withdrawal and basal LH on oocyte competence acquisition in cattle. Theriogenology 86, 54–61.
Somatic environment and germinal differentiation in antral follicle: the effect of FSH withdrawal and basal LH on oocyte competence acquisition in cattle.Crossref | GoogleScholarGoogle Scholar | 27158126PubMed |

Sirard, MA, 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 |

Soares, ACS, Lodde, V, Barros, RG, Price, CA, Luciano, AM, and Buratini, J (2017). 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. Reproduction, Fertility and Development 29, 2217–2224.
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.Crossref | GoogleScholarGoogle Scholar |

Soares A, Lodde V, Bragança L, Marques K, Luciano A, Buratini J (2018) Effects of ovarian synchronization associated with a two-step IVM strategy on in vitro embryo production in cattle. In ‘IRRS international ruminant reproduction symposium’, 16–20 September 2018. pp. 1152–1152. (Animal Reproduction: Foz do Iguau, Brazil)

Soares, ACS, Marques, KNG, Bragança, LGM, Lodde, V, Luciano, AM, and Buratini, J (2020a). Synchronization of germinal vesicle maturity improves efficacy of in vitro embryo production in Holstein cows. Theriogenology 154, 53–58.
Synchronization of germinal vesicle maturity improves efficacy of in vitro embryo production in Holstein cows.Crossref | GoogleScholarGoogle Scholar | 32480064PubMed |

Soares, ACS, Sakoda, JN, Gama, IL, Bayeux, BM, Lodde, V, Luciano, AM, and Buratini, J (2020b). Characterization and control of oocyte large-scale chromatin configuration in different cattle breeds. Theriogenology 141, 146–152.
Characterization and control of oocyte large-scale chromatin configuration in different cattle breeds.Crossref | GoogleScholarGoogle Scholar | 31541784PubMed |

Sutton, ML, Gilchrist, RB, and Thompson, JG (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Human Reproduction Update 9, 35–48.
Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity.Crossref | GoogleScholarGoogle Scholar | 12638780PubMed |

Sutton-McDowall, ML, Gilchrist, RB, and Thompson, JG (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
The pivotal role of glucose metabolism in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 20089664PubMed |

Thomas, RE, Thompson, JG, Armstrong, DT, and Gilchrist, RB (2004). Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biology of Reproduction 71, 1142–1149.
Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity.Crossref | GoogleScholarGoogle Scholar | 15189837PubMed |

Vanhoutte, L, De Sutter, P, Nogueira, D, Gerris, J, Dhont, M, and Van der Elst, J (2007). Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor. Human Reproduction 22, 1239–1246.
Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor.Crossref | GoogleScholarGoogle Scholar | 17303631PubMed |

Viana, J (2020). 2019 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsletter 38, .

Vuong, LN, Le, AH, Ho, VNA, Pham, TD, Sanchez, F, Romero, S, De Vos, M, Ho, TM, Gilchrist, RB, and Smitz, J (2020). Live births after oocyte in vitro maturation with a prematuration step in women with polycystic ovary syndrome. Journal of Assisted Reproduction and Genetics 37, 347–357.
Live births after oocyte in vitro maturation with a prematuration step in women with polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 31902102PubMed |

Webb, R, and Buratini, J (2016). Global challenges for the 21st century: the role and strategy of the agri-food sector. Animal Reproduction 13, 133–142.
Global challenges for the 21st century: the role and strategy of the agri-food sector.Crossref | GoogleScholarGoogle Scholar |

Zhang, M, Su, Y-Q, Sugiura, K, Xia, G, and Eppig, JJ (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 | 20947764PubMed |

Zhang, M, Su, Y-Q, Sugiura, K, Wigglesworth, K, Xia, G, and Eppig, JJ (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 | 21914782PubMed |

Zuccotti, M, Piccinelli, A, Rossi, PG, Garagna, S, and Redi, CA (1995). Chromatin organization during mouse oocyte growth. Molecular Reproduction and Development 41, 479–485.
Chromatin organization during mouse oocyte growth.Crossref | GoogleScholarGoogle Scholar | 7576615PubMed |