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
REVIEW (Open Access)

Nurturing the egg: the essential connection between cumulus cells and the oocyte

Claude Robert A B C *
+ Author Affiliations
- Author Affiliations

A Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation, Université Laval, Québec, QC, Canada.

B Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Université Laval, Québec, QC, Canada.

C Réseau Québécois en Reproduction (RQR), Montréal, QC, Canada.

* Correspondence to: claude.robert@fsaa.ulaval.ca

Reproduction, Fertility and Development 34(2) 149-159 https://doi.org/10.1071/RD21282
Published online: 11 October 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the IETS. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

The determinants of oocyte quality remain uncertain. Under suitable conditions, which have yet to be defined, the gamete grows and acquires the competence to resume meiosis, be fertilised and undergo embryonic development at least beyond genome activation, after which the blastomere is autonomous enough to adapt to the specificity of its environment. This review describes the central role played by the oocyte in reproductive success and how communication between cumulus cells and the oocyte are essential to proper oogenesis and the quality of the resulting gamete. While most attempts to improve oocyte quality have been directed at gonadotrophin-based systemic endocrine signalling, it is proposed that parallel control of fertility may act locally within ovarian follicles through intimate cooperation between somatic cells and the oocyte via the network of transzonal projections. This intercellular communication may prove to be more sensitive to environmental conditions than systemic endocrine signalling, which is essential for many non-reproductive tissues.

Keywords: cell signalling, developmental competence, follicle, folliculogenesis, intercellular communications, oocyte, oogenesis, ovary, transzonal projections.


References

Abbassi, L, El-Hayek, S, Carvalho, KF, et al. (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, et al. (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 |

Allworth, AE, and Albertini, DF (1993). Meiotic maturation in cultured bovine oocytes is accompanied by remodeling of the cumulus cell cytoskeleton. Developmental Biology 158, 101–112.
Meiotic maturation in cultured bovine oocytes is accompanied by remodeling of the cumulus cell cytoskeleton.Crossref | GoogleScholarGoogle Scholar | 8330667PubMed |

Anderson, E, and Albertini, DF (1976). Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. Journal of Cell Biology 71, 680–686.
Gap junctions between the oocyte and companion follicle cells in the mammalian ovary.Crossref | GoogleScholarGoogle Scholar |

Baena, V, and Terasaki, M (2019). Three-dimensional organization of transzonal projections and other cytoplasmic extensions in the mouse ovarian follicle. Scientific Reports 9, 1262.
Three-dimensional organization of transzonal projections and other cytoplasmic extensions in the mouse ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 30718581PubMed |

Bényei, B, Gaspardy, A, Komlosi, I, et al. (2004). Repeatability and heritability of ovulation number and embryos in dam-daughters pairs in superovulated Holstein-Friesian cows. Reproduction in Domestic Animals = Zuchthygiene 39, 99–102.
Repeatability and heritability of ovulation number and embryos in dam-daughters pairs in superovulated Holstein-Friesian cows.Crossref | GoogleScholarGoogle Scholar | 15065991PubMed |

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, et al. (1997). In vitro production of bovine embryos: developmental competence is acquired before maturation. Theriogenology 47, 1061–1075.
In vitro production of bovine embryos: developmental competence is acquired before maturation.Crossref | GoogleScholarGoogle Scholar | 16728056PubMed |

Blondin, P, Bousquet, D, Twagiramungu, H, et al. (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 |

Braw-Tal, R, and Yossefi, S (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. Journal of Reproduction and Fertility 109, 165–171.
Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 9068428PubMed |

Bunel, A, Nivet, AL, Blondin, P, et al. (2014). Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes. Reproduction, Fertility and Development 26, 855–865.
Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar |

Burns, DS, Jimenez-Krassel, F, Ireland, JLH, et al. (2005). Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle-stimulating hormone concentrations. Biology of Reproduction 73, 54–62.
Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle-stimulating hormone concentrations.Crossref | GoogleScholarGoogle Scholar | 15744026PubMed |

Calder, MD, Caveney, AN, Sirard, M-A, et al. (2005). Effect of serum and cumulus cell expansion on marker gene transcripts in bovine cumulus-oocyte complexes during maturation in vitro. Fertility and Sterility 83, 1077–1085.
Effect of serum and cumulus cell expansion on marker gene transcripts in bovine cumulus-oocyte complexes during maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 15831278PubMed |

Caligara, C, Navarro, J, Vargas, G, et al. (2001). The effect of repeated controlled ovarian stimulation in donors. Human Reproduction 16, 2320–2323.
The effect of repeated controlled ovarian stimulation in donors.Crossref | GoogleScholarGoogle Scholar | 11679512PubMed |

Can, A, and Albertini, DF (1997). Stage specific effects of carbendazim (MBC) on meiotic cell cycle progression in mouse oocytes. Molecular Reproduction and Development 46, 351–362.
Stage specific effects of carbendazim (MBC) on meiotic cell cycle progression in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 9041138PubMed |

Carabatsos, MJ, Elvin, J, Matzuk, MM, et al. (1998). Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Developmental Biology 204, 373–384.
Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice.Crossref | GoogleScholarGoogle Scholar | 9882477PubMed |

Combelles, CMH, Carabatsos, MJ, Kumar, TR, et al. (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 |

Conti, M, Hsieh, M, Park, JY, et al. (2006). Role of the epidermal growth factor network in ovarian follicles. Molecular Endocrinology 20, 715–723.
Role of the epidermal growth factor network in ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 16051667PubMed |

Coticchio, G, Guglielmo, MC, Albertini, DF, et al. (2014). Contributions of the actin cytoskeleton to the emergence of polarity during maturation in human oocytes. Molecular Human Reproduction 20, 200–207.
Contributions of the actin cytoskeleton to the emergence of polarity during maturation in human oocytes.Crossref | GoogleScholarGoogle Scholar | 24258450PubMed |

del Collado, M, da Silveira, JC, Sangalli, JR, et al. (2017). Fatty acid binding protein 3 and transzonal projections are involved in lipid accumulation during in vitro maturation of bovine oocytes. Scientific Reports 7, 2645.
Fatty acid binding protein 3 and transzonal projections are involved in lipid accumulation during in vitro maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 28572619PubMed |

Demeestere, I, Centner, J, Gervy, C, et al. (2005). Impact of various endocrine and paracrine factors on in vitro culture of preantral follicles in rodents. Reproduction 130, 147–156.
Impact of various endocrine and paracrine factors on in vitro culture of preantral follicles in rodents.Crossref | GoogleScholarGoogle Scholar | 16049152PubMed |

Dieci, C, Lodde, V, Labreque, R, et al. (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.
Differences in cumulus cell gene expression indicate the benefit of a pre-maturation step to improve in-vitro bovine embryo production.Crossref | GoogleScholarGoogle Scholar | 27559149PubMed |

Dierich, A, Sairam, MR, Monaco, L, et al. (1998). Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proceedings of the National Academy of Sciences of the United States of America 95, 13612–13617.
Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance.Crossref | GoogleScholarGoogle Scholar | 9811848PubMed |

Domhan, S, Ma, L, Tai, A, et al. (2011). Intercellular communication by exchange of cytoplasmic material via tunneling nano-tube like structures in primary human renal epithelial cells. PLoS One 6, e21283.
Intercellular communication by exchange of cytoplasmic material via tunneling nano-tube like structures in primary human renal epithelial cells.Crossref | GoogleScholarGoogle Scholar | 21738629PubMed |

El Fatimy, R, Davidovic, L, Tremblay, S, et al. (2016). Tracking the fragile X mental retardation protein in a highly ordered neuronal ribonucleoparticles population: a link between stalled polyribosomes and RNA granules. PLoS Genetics 12, e1006192.
Tracking the fragile X mental retardation protein in a highly ordered neuronal ribonucleoparticles population: a link between stalled polyribosomes and RNA granules.Crossref | GoogleScholarGoogle Scholar | 27462983PubMed |

El-Hayek, S, Yang, Q, Abbassi, L, et al. (2018). Mammalian oocytes locally remodel follicular architecture to provide the foundation for germline-soma communication. Current Biology 28, 1124–1131.e3.
Mammalian oocytes locally remodel follicular architecture to provide the foundation for germline-soma communication.Crossref | GoogleScholarGoogle Scholar | 29576478PubMed |

Ellenbogen, A, Shavit, T, and Shalom-Paz, E (2014). IVM results are comparable and may have advantages over standard IVF. Facts, Views & Vision in ObGyn 6, 77–80.

Eppig, JJ, and Schroeder, AC (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biology of Reproduction 41, 268–276.
Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 2508774PubMed |

Eppig, JJ, Wigglesworth, K, Pendola, F, et al. (1997). Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biology of Reproduction 56, 976–984.
Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells.Crossref | GoogleScholarGoogle Scholar | 9096881PubMed |

Fair, T, Hyttel, P, and Greve, T (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Molecular Reproduction and Development 42, 437–442.
Bovine oocyte diameter in relation to maturational competence and transcriptional activity.Crossref | GoogleScholarGoogle Scholar | 8607973PubMed |

Fair, T, Hulshof, SCJ, Hyttel, P, et al. (1997a). Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Molecular Reproduction and Development 46, 208–215.
Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles.Crossref | GoogleScholarGoogle Scholar | 9021752PubMed |

Fair, T, Hulshof, SCJ, Hyttel, P, et al. (1997b). Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anatomy and Embryology 195, 327–336.
Oocyte ultrastructure in bovine primordial to early tertiary follicles.Crossref | GoogleScholarGoogle Scholar | 9108198PubMed |

Gilchrist, RB, Luciano, AM, Richani, D, et al. (2016). Oocyte maturation and quality: role of cyclic nucleotides. Reproduction 152, R143–R157.
Oocyte maturation and quality: role of cyclic nucleotides.Crossref | GoogleScholarGoogle Scholar | 27422885PubMed |

Gougeon, A (1996). Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrine Reviews 17, 121–155.
Regulation of ovarian follicular development in primates: facts and hypotheses.Crossref | GoogleScholarGoogle Scholar | 8706629PubMed |

Graves, KL, Seibert, JT, Keating, AF, et al. (2018). Characterizing the acute heat stress response in gilts: II. Assessing repeatability and association with fertility. Journal of Animal Science 96, 2419–2426.
Characterizing the acute heat stress response in gilts: II. Assessing repeatability and association with fertility.Crossref | GoogleScholarGoogle Scholar | 29788126PubMed |

Guild, GM, Connelly, PS, Shaw, MK, et al. (1997). Actin filament cables in Drosophila nurse cells are composed of modules that slide passively past one another during dumping. Journal of Cell Biology 138, 783–797.
Actin filament cables in Drosophila nurse cells are composed of modules that slide passively past one another during dumping.Crossref | GoogleScholarGoogle Scholar |

Hansen, PJ (2020). The incompletely fulfilled promise of embryo transfer in cattle-why aren’t pregnancy rates greater and what can we do about it? Journal of Animal Science 98, skaa288.
The incompletely fulfilled promise of embryo transfer in cattle-why aren’t pregnancy rates greater and what can we do about it?Crossref | GoogleScholarGoogle Scholar | 33141879PubMed |

Hernandez-Gonzalez, I, Gonzalez-Robayna, I, Shimada, M, et al. (2006). Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process? Molecular Endocrinology 20, 1300–1321.
Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process?Crossref | GoogleScholarGoogle Scholar | 16455817PubMed |

Hertig, AT, and Adams, EC (1967). Studies on the human oocyte and its follicle. I. Ultrastructural and histochemical observations on the primordial follicle stage. Journal of Cell Biology 34, 647–675.
Studies on the human oocyte and its follicle. I. Ultrastructural and histochemical observations on the primordial follicle stage.Crossref | GoogleScholarGoogle Scholar |

Holm, P, and Callesen, H (1998). In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application. Reproduction Nutrition Development 38, 579–594.
In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application.Crossref | GoogleScholarGoogle Scholar |

Kidder, GM, and Mhawi, AA (2002). Gap junctions and ovarian folliculogenesis. Reproduction 123, 613–620.
Gap junctions and ovarian folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 12006089PubMed |

Kölle, S, Dubois, CS, Caillaud, M, et al. (2007). Equine zona protein synthesis and ZP structure during folliculogenesis, oocyte maturation, and embryogenesis. Molecular Reproduction and Development 74, 851–859.
Equine zona protein synthesis and ZP structure during folliculogenesis, oocyte maturation, and embryogenesis.Crossref | GoogleScholarGoogle Scholar | 17252540PubMed |

Kreeger, PK, Fernandes, NN, Woodruff, TK, et al. (2005). Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biology of Reproduction 73, 942–950.
Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose.Crossref | GoogleScholarGoogle Scholar | 15987824PubMed |

Kumar, TR, Wang, Y, Lu, N, et al. (1997). Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nature Genetics 15, 201–204.
Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility.Crossref | GoogleScholarGoogle Scholar | 9020850PubMed |

Lawson, DW, and Borgerhoff Mulder, M (2016). The offspring quantity–quality trade-off and human fertility variation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 371, 20150145.
The offspring quantity–quality trade-off and human fertility variation.Crossref | GoogleScholarGoogle Scholar | 27022072PubMed |

Li, R, and Albertini, DF (2013). The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nature Reviews Molecular Cell Biology 14, 141–152.
The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte.Crossref | GoogleScholarGoogle Scholar | 23429793PubMed |

Liu, Y-X, and Hsueh, AJW (1986). Synergism between granulosa and theca-interstitial cells in estrogen biosynthesis by gonadotropin-treated rat ovaries: studies on the two-cell, two-gonadotropin hypothesis using steroid antisera. Biology of Reproduction 35, 27–36.
Synergism between granulosa and theca-interstitial cells in estrogen biosynthesis by gonadotropin-treated rat ovaries: studies on the two-cell, two-gonadotropin hypothesis using steroid antisera.Crossref | GoogleScholarGoogle Scholar | 3091103PubMed |

Lodde, V, Modina, S, Galbusera, C, et al. (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.
Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence.Crossref | GoogleScholarGoogle Scholar | 17075796PubMed |

Lodde, V, Modina, S, Maddox-Hyttel, P, et al. (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 |

Lonergan, P, Monaghan, P, Rizos, D, et al. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Molecular Reproduction and Development 37, 48–53.
Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro.Crossref | GoogleScholarGoogle Scholar | 8129930PubMed |

Luciano, AM, Lodde, V, Beretta, MS, et al. (2005). Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus–oocyte complexes: role of cumulus cells, cyclic adenosine 3′,5′-monophosphate, and glutathione. Molecular Reproduction and Development 71, 389–397.
Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus–oocyte complexes: role of cumulus cells, cyclic adenosine 3′,5′-monophosphate, and glutathione.Crossref | GoogleScholarGoogle Scholar | 15803456PubMed |

Luciano, AM, Franciosi, F, Modina, SC, et al. (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 |

Lynch, M, Ackerman, MS, Gout, J-F, et al. (2016). Genetic drift, selection and the evolution of the mutation rate. Nature Reviews Genetics 17, 704–714.
Genetic drift, selection and the evolution of the mutation rate.Crossref | GoogleScholarGoogle Scholar | 27739533PubMed |

Macaulay, AD, Gilbert, I, Caballero, J, et al. (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, et al. (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 |

McLaughlin, M, and Telfer, EE (2010). Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two-step serum-free culture system. Reproduction 139, 971–978.
Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two-step serum-free culture system.Crossref | GoogleScholarGoogle Scholar | 20207724PubMed |

Modina, S, Borromeo, V, Luciano, AM, et al. (2007). Relationship between growth hormone concentrations in bovine oocytes and follicular fluid and oocyte developmental competence. European Journal of Histochemistry 51, 173–180.
| 17921112PubMed |

Motta, PM, Makabe, S, Naguro, T, et al. (1994). Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy. Archives of Histology and Cytology 57, 369–394.
Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy.Crossref | GoogleScholarGoogle Scholar | 7880591PubMed |

Muzio MR, Cascella M (2021) ‘‘Histology, Axon’, in StatPearls’. (StatPearls Publishing: Treasure Island, FL, USA). Available at http://www.ncbi.nlm.nih.gov/books/NBK554388/ [Accessed: 20 July 2021]

Nawaz, M, and Fatima, F (2017). Extracellular vesicles, tunneling nanotubes, and cellular interplay: synergies and missing links. Frontiers in Molecular Biosciences 4, 50.
Extracellular vesicles, tunneling nanotubes, and cellular interplay: synergies and missing links.Crossref | GoogleScholarGoogle Scholar | 28770210PubMed |

Nivet, A-L, Bunel, A, Labrecque, R, et al. (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 |

Numabe, T, Oikawa, T, Kikuchi, T, et al. (2000). Birth weight and birth rate of heavy calves conceived by transfer of in vitro or in vivo produced bovine embryos. Animal Reproduction Science 64, 13–20.
Birth weight and birth rate of heavy calves conceived by transfer of in vitro or in vivo produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 11078963PubMed |

O’Doherty, EM, Wade, MG, Hill, JL, et al. (1997). Effects of culturing bovine oocytes either singly or in groups on development to blastocysts. Theriogenology 48, 161–169.
Effects of culturing bovine oocytes either singly or in groups on development to blastocysts.Crossref | GoogleScholarGoogle Scholar | 16728116PubMed |

Pangas, SA, Saudye, H, Shea, LD, et al. (2003). Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes. Tissue Engineering 9, 1013–1021.
Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 14633385PubMed |

Paul, LT, Atilan, O, and Tulay, P (2019). The effect of repeated controlled ovarian stimulation cycles on the gamete and embryo development. Zygote 27, 347–349.
The effect of repeated controlled ovarian stimulation cycles on the gamete and embryo development.Crossref | GoogleScholarGoogle Scholar | 31405397PubMed |

Peñalver Bernabé, B, Thiele, I, Galdones, E, et al. (2019). Dynamic genome-scale cell-specific metabolic models reveal novel inter-cellular and intra-cellular metabolic communications during ovarian follicle development. BMC Bioinformatics 20, 307.
Dynamic genome-scale cell-specific metabolic models reveal novel inter-cellular and intra-cellular metabolic communications during ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 31182013PubMed |

Philpott, CC, Ringuette, MJ, and Dean, J (1987). Oocyte-specific expression and developmental regulation of ZP3, the sperm receptor of the mouse zona pellucida. Developmental Biology 121, 568–575.
Oocyte-specific expression and developmental regulation of ZP3, the sperm receptor of the mouse zona pellucida.Crossref | GoogleScholarGoogle Scholar | 2884155PubMed |

Plancha, CE, Sanfins, A, Rodrigues, P, et al. (2005). Cell polarity during folliculogenesis and oogenesis. Reproductive Biomedicine Online 10, 478–484.
Cell polarity during folliculogenesis and oogenesis.Crossref | GoogleScholarGoogle Scholar | 15901455PubMed |

Plourde, D, Vigneault, C, Lemay, A, et al. (2012). Contribution of oocyte source and culture conditions to phenotypic and transcriptomic variation in commercially produced bovine blastocysts. Theriogenology 78, 116–131.e3.
Contribution of oocyte source and culture conditions to phenotypic and transcriptomic variation in commercially produced bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 22494684PubMed |

Reynaud, K, Cortvrindt, R, Smitz, J, et al. (2001). Alterations in ovarian function of mice with reduced amounts of KIT receptor. Reproduction 121, 229–237.
Alterations in ovarian function of mice with reduced amounts of KIT receptor.Crossref | GoogleScholarGoogle Scholar | 11226047PubMed |

Richards, JS (2007). Genetics of ovulation. Seminars in Reproductive Medicine 25, 235–242.
Genetics of ovulation.Crossref | GoogleScholarGoogle Scholar | 17594604PubMed |

Rieger, D, and Loskutoff, NM (1994). Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. Reproduction 100, 257–262.
Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro.Crossref | GoogleScholarGoogle Scholar |

Rieger, D, Loskutoff, NM, and Betteridge, KJ (1992). Developmentally related changes in the metabolism of glucose and glutamine by cattle embryos produced and co-cultured in vitro. Reproduction 95, 585–595.
Developmentally related changes in the metabolism of glucose and glutamine by cattle embryos produced and co-cultured in vitro.Crossref | GoogleScholarGoogle Scholar |

Rizos, D, Ward, F, Duffy, P, et al. (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 |

Romano, JE, Bryan, K, Ramos, RS, et al. (2016). Effect of early pregnancy diagnosis by per rectum amniotic sac palpation on pregnancy loss, calving rates, and abnormalities in newborn dairy calves. Theriogenology 85, 419–427.
Effect of early pregnancy diagnosis by per rectum amniotic sac palpation on pregnancy loss, calving rates, and abnormalities in newborn dairy calves.Crossref | GoogleScholarGoogle Scholar | 26443235PubMed |

Rubelt, F, Busse, CE, Bukhari, SAC, et al. (2017). Adaptive immune receptor repertoire community recommendations for sharing immune-repertoire sequencing data. Nature Immunology 18, 1274–1278.
Adaptive immune receptor repertoire community recommendations for sharing immune-repertoire sequencing data.Crossref | GoogleScholarGoogle Scholar | 29144493PubMed |

Santiquet, N, Robert, C, and Richard, FJ (2013). The dynamics of connexin expression, degradation and localisation are regulated by gonadotropins during the early stages of in vitro maturation of swine oocytes. PLoS One 8, e68456.
The dynamics of connexin expression, degradation and localisation are regulated by gonadotropins during the early stages of in vitro maturation of swine oocytes.Crossref | GoogleScholarGoogle Scholar | 23861906PubMed |

Santiquet, NW, Greene, AF, Becker, J, et al. (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 |

Scantland, S, Tessaro, I, Macabelli, CH, et al. (2014). The adenosine salvage pathway as an alternative to mitochondrial production of ATP in maturing mammalian oocytes. Biology of Reproduction 91, 75.
The adenosine salvage pathway as an alternative to mitochondrial production of ATP in maturing mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 25078684PubMed |

Sinowatz, F, Kölle, S, and Töpfer-Petersen, E (2001). Biosynthesis and expression of zona pellucida glycoproteins in mammals. Cells Tissues Organs 168, 24–35.
Biosynthesis and expression of zona pellucida glycoproteins in mammals.Crossref | GoogleScholarGoogle Scholar | 11114584PubMed |

Sood, P, Zachut, M, Dekel, I, et al. (2017). Preovulatory follicle characteristics and oocyte competence in repeat breeder dairy cows. Journal of Dairy Science 100, 9372–9381.
Preovulatory follicle characteristics and oocyte competence in repeat breeder dairy cows.Crossref | GoogleScholarGoogle Scholar | 28888606PubMed |

Spracklen, AJ, and Tootle, TL (2013). The utility of stage-specific mid-to-late Drosophila follicle isolation. Journal of Visualized Experiments: JoVE 82, 50493.
The utility of stage-specific mid-to-late Drosophila follicle isolation.Crossref | GoogleScholarGoogle Scholar |

Stimpfel, M, Jancar, N, Vrtacnik-Bokal, E, et al. (2019). Conventional IVF improves blastocyst rate and quality compared to ICSI when used in patients with mild or moderate teratozoospermia. Systems Biology in Reproductive Medicine 65, 458–464.
Conventional IVF improves blastocyst rate and quality compared to ICSI when used in patients with mild or moderate teratozoospermia.Crossref | GoogleScholarGoogle Scholar | 31522570PubMed |

Su, Y-Q, Wu, X, O’Brien, MJ, et al. (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. Developmental Biology 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 | 15531364PubMed |

Sugiura, K, Su, Y-Q, Li, Q, et al. (2010). Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15. Molecular Endocrinology 24, 2303–2314.
Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15.Crossref | GoogleScholarGoogle Scholar | 21047911PubMed |

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 |

Telfer, EE, and Andersen, CY (2021). In vitro growth and maturation of primordial follicles and immature oocytes. Fertility and Sterility 115, 1116–1125.
In vitro growth and maturation of primordial follicles and immature oocytes.Crossref | GoogleScholarGoogle Scholar | 33823993PubMed |

Truong, T, and Gardner, DK (2017). Antioxidants improve IVF outcome and subsequent embryo development in the mouse. Human Reproduction 32, 2404–2413.
Antioxidants improve IVF outcome and subsequent embryo development in the mouse.Crossref | GoogleScholarGoogle Scholar | 29136144PubMed |

Tutt, DAR, Silvestri, G, Serrano-Albal, M, et al. (2021). Analysis of bovine blastocysts indicates ovarian stimulation does not induce chromosome errors, nor discordance between inner-cell mass and trophectoderm lineages. Theriogenology 161, 108–119.
Analysis of bovine blastocysts indicates ovarian stimulation does not induce chromosome errors, nor discordance between inner-cell mass and trophectoderm lineages.Crossref | GoogleScholarGoogle Scholar | 33307428PubMed |

Van Blerkom, J (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.
Mitochondrial function in the human oocyte and embryo and their role in developmental competence.Crossref | GoogleScholarGoogle Scholar | 20933103PubMed |

van Wagtendonk-de Leeuw, AM, Mullaart, E, de Roos, APW, et al. (2000). Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring. Theriogenology 53, 575–597.
Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring.Crossref | GoogleScholarGoogle Scholar | 10735051PubMed |

Wang, X, Catt, S, Pangestu, M, et al. (2011). Successful in vitro culture of pre-antral follicles derived from vitrified murine ovarian tissue: oocyte maturation, fertilization, and live births. Reproduction 141, 183–191.
Successful in vitro culture of pre-antral follicles derived from vitrified murine ovarian tissue: oocyte maturation, fertilization, and live births.Crossref | GoogleScholarGoogle Scholar | 21075829PubMed |

Xiao, S, Zhang, J, Romero, MM, et al. (2015). In vitro follicle growth supports human oocyte meiotic maturation. Scientific Reports 5, 17323.
In vitro follicle growth supports human oocyte meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 26612176PubMed |

Xiao, S, Coppeta, JR, Rogers, HB, et al. (2017). A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. Nature Communications 8, 14584.
A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle.Crossref | GoogleScholarGoogle Scholar | 28350383PubMed |

Yin, C, Liu, J, Chang, Z, et al. (2020). Heat exposure impairs porcine oocyte quality with suppressed actin expression in cumulus cells and disrupted F-actin formation in transzonal projections. Journal of Animal Science and Biotechnology 11, 71.
Heat exposure impairs porcine oocyte quality with suppressed actin expression in cumulus cells and disrupted F-actin formation in transzonal projections.Crossref | GoogleScholarGoogle Scholar | 32647569PubMed |

Zeng, H-t, Ren, Z, Guzman, L, et al. (2013). Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Human Reproduction 28, 1536–1545.
Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence.Crossref | GoogleScholarGoogle Scholar | 23559189PubMed |