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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Coculture of porcine cumulus–oocyte complexes with porcine luteal cells during IVM: effect on oocyte maturation and embryo development

G. M. Teplitz A B , M. S. Lorenzo A B , A. Maruri B , P. R. Cruzans A B , M. C. Carou https://orcid.org/0000-0001-9657-9464 B and D. M. Lombardo https://orcid.org/0000-0003-0677-7702 B C
+ Author Affiliations
- Author Affiliations

A Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Godoy Cruz 2290 C1425TQB, Buenos Aires, Argentina.

B Universidad de Buenos Aires, Facultad de Ciencias Veterinarias, Instituto de Investigación y Tecnología en Reproducción Animal, Cátedra de Histología y Embriología, Chorroarín 280 C1427CWO, Buenos Aires, Argentina.

C Corresponding author. Email: dlombard@fvet.uba.ar

Reproduction, Fertility and Development 32(16) 1250-1259 https://doi.org/10.1071/RD20117
Submitted: 29 April 2020  Accepted: 12 September 2020   Published: 21 October 2020

Abstract

Coculture with somatic cells is an alternative to improve suboptimal in vitro culture conditions. In pigs, IVF is related to poor male pronuclear formation and high rates of polyspermy. The aim of this study was to assess the effect of a coculture system with porcine luteal cells (PLCs) on the IVM of porcine cumulus–oocyte complexes (COCs). Abattoir-derived ovaries were used to obtain PLCs and COCs. COCs were matured in vitro in TCM-199 with or without the addition of human menopausal gonadotrophin (hMG; C+hMG and C-hMG respectively), in coculture with PLCs from passage 1 (PLC-1) and in PLC-1 conditioned medium (CM). In the coculture system, nuclear maturation rates were significantly higher than in the C-hMG and CM groups, but similar to rates in the C+hMG group. In cumulus cells, PLC-1 coculture decreased viability, early apoptosis and necrosis, and increased late apoptosis compared with C+hMG. PLC-1 coculture also decreased reactive oxygen species levels in cumulus cells. After IVF, monospermic penetration and IVF efficiency increased in the PLC-1 group compared with the C+hMG group. After in vitro culture, higher blastocysts rates were observed in the PLC-1 group. This is the first report of a coculture system of COCs with PLCs. Our model could be an alternative for the conventional maturation medium plus gonadotrophins because of its lower rates of polyspermic penetration and higher blastocysts rates, key issues in porcine in vitro embryo production.

Graphical Abstract Image

Keywords: coculture, embryo development, IVM, luteal cells, pig.


References

Aardema, H., Roelen, B. A. J., van Tol, H. T. A., Oei, C. H. Y., Gadella, B. M., and Vos, P. L. A. M. (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 | 23831113PubMed |

Aigner, B., Renner, S., Kessler, B., Klymiuk, N., Kurome, M., Wünsch, A., and Wolf, E. (2010). Transgenic pigs as models for translational biomedical research. J. Mol. Med. 88, 653–664.
Transgenic pigs as models for translational biomedical research.Crossref | GoogleScholarGoogle Scholar | 20339830PubMed |

Alfaia, C. M., Lopes, P. A., Madeira, M. S., Pestana, J. M., Coelho, D., Toldrá, F., and Prates, J. A. M. (2019). Current feeding strategies to improve pork intramuscular fat content and its nutritional quality. Adv. Food Nutr. Res. 89, 53–94.
Current feeding strategies to improve pork intramuscular fat content and its nutritional quality.Crossref | GoogleScholarGoogle Scholar | 31351530PubMed |

Allen, R. L., and Wright, R. W. (1984). In vitro development of porcine embryos in coculture with endometrial cell monolayers or culture supernatants. J. Anim. Sci. 59, 1657–1661.
In vitro development of porcine embryos in coculture with endometrial cell monolayers or culture supernatants.Crossref | GoogleScholarGoogle Scholar | 6543213PubMed |

Ando, H., Goto, M., Iwase, A., Kikkawa, F., Shibata, D., and Naruse, K. (2007). Sequential co-culture of preimplantation embryos with oviductal epithelial cells first is more effective than that with endometrial epithelial cells first in human. Fertil. Steril. 88, S315–S316.
Sequential co-culture of preimplantation embryos with oviductal epithelial cells first is more effective than that with endometrial epithelial cells first in human.Crossref | GoogleScholarGoogle Scholar |

Anguita, B., Vandaele, L., Mateusen, B., Maes, D., and Van Soom, A. (2007). Developmental competence of bovine oocytes is not related to apoptosis incidence in oocytes, cumulus cells and blastocysts. Theriogenology 67, 537–549.
Developmental competence of bovine oocytes is not related to apoptosis incidence in oocytes, cumulus cells and blastocysts.Crossref | GoogleScholarGoogle Scholar | 17007918PubMed |

Anguita, B., Paramio, M. T., Morató, R., Romaguera, R., Jiménez-Macedo, A. R., Mogas, T., and Izquierdo, D. (2009). Effect of the apoptosis rate observed in oocytes and cumulus cells on embryo development in prepubertal goats. Anim. Reprod. Sci. 116, 95–106.
Effect of the apoptosis rate observed in oocytes and cumulus cells on embryo development in prepubertal goats.Crossref | GoogleScholarGoogle Scholar | 19217225PubMed |

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 | 21228216PubMed |

Barros, R. G., Lima, P. F., Soares, A. C. S., Sanches, L., Price, C. A., and Buratini, J. (2019). Fibroblast growth factor 2 regulates cumulus differentiation under the control of the oocyte. J. Assist. Reprod. Genet. 36, 905–913.
Fibroblast growth factor 2 regulates cumulus differentiation under the control of the oocyte.Crossref | GoogleScholarGoogle Scholar | 30887159PubMed |

Batista, M., Torres, A., Diniz, P., Mateus, L., and Lopes-da-Costa, L. (2012). Development of a bovine luteal cell in vitro culture system suitable for co-culture with early embryos. In Vitro Cell. Dev. Biol. Anim. 48, 583–592.
Development of a bovine luteal cell in vitro culture system suitable for co-culture with early embryos.Crossref | GoogleScholarGoogle Scholar | 23054443PubMed |

Bongso, A., Ng, S.-C., and Ratnam, S. (1990). Co-cultures: their relevance to assisted reproduction. Hum. Reprod. 5, 893–900.
Co-cultures: their relevance to assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 2081801PubMed |

Chen, X. Y., Li, Q. W., Zhang, S. S., Han, Z. S., Zhao, R., Wu, S. Y., and Wang, J. (2007). Effects of ovarian cortex cell co-culture during in vitro maturation on porcine oocytes maturation, fertilization and embryo development. Anim. Reprod. Sci. 99, 306–316.
Effects of ovarian cortex cell co-culture during in vitro maturation on porcine oocytes maturation, fertilization and embryo development.Crossref | GoogleScholarGoogle Scholar | 16782288PubMed |

Coy, P., Grullon, L., Canovas, S., Romar, R., Matas, C., and Aviles, M. (2008). Hardening of the zona pellucida of unfertilized eggs can reduce polyspermic fertilization in the pig and cow. Reproduction 135, 19–27.
Hardening of the zona pellucida of unfertilized eggs can reduce polyspermic fertilization in the pig and cow.Crossref | GoogleScholarGoogle Scholar | 18159080PubMed |

da Silveira, J. C., Veeramachaneni, D. N. R., Winger, Q. A., Carnevale, E. M., and Bouma, G. J. (2012). Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol. Reprod. 86, 71.
Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 22116803PubMed |

Desai, N., and Goldfarb, J. (1998). Co-cultured human embryos may be subjected to widely different microenvironments: pattern of growth factor/cytokine release by Vero cells during the co-culture interval. Hum. Reprod. 13, 1600–1605.
Co-cultured human embryos may be subjected to widely different microenvironments: pattern of growth factor/cytokine release by Vero cells during the co-culture interval.Crossref | GoogleScholarGoogle Scholar | 9688399PubMed |

Downs, S. M. (1989). Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol. Reprod. 41, 371–379.
Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro.Crossref | GoogleScholarGoogle Scholar | 2508778PubMed |

Dressing, G. E., Goldberg, J. E., Charles, N. J., Schwertfeger, K. L., and Lange, C. A. (2011). Membrane progesterone receptor expression in mammalian tissues: a review of regulation and physiological implications. Steroids 76, 11–17.
Membrane progesterone receptor expression in mammalian tissues: a review of regulation and physiological implications.Crossref | GoogleScholarGoogle Scholar | 20869977PubMed |

Fleury, C., Mignotte, B., and Vayssière, J. L. (2002). Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84, 131–141.
Mitochondrial reactive oxygen species in cell death signaling.Crossref | GoogleScholarGoogle Scholar | 12022944PubMed |

Fukaya, T., Chida, S., Murakami, T., and Yajima, A. (1996). Is direct cell-to-cell contact needed to improve embryonic development in co-culture? Tohoku J. Exp. Med. 180, 225–232.
Is direct cell-to-cell contact needed to improve embryonic development in co-culture?Crossref | GoogleScholarGoogle Scholar | 9058507PubMed |

Funahashi, H., and Day, B. N. (1997). Advances in in vitro production of pig embryos. J. Reprod. Fertil. Suppl. 52, 271–283.
| 9602735PubMed |

Funahashi, H., and Nagai, T. (2001). Regulation of in vitro penetration of frozen–thawed boar spermatozoa by caffeine and adenosine. Mol. Reprod. Dev. 58, 424–431.
Regulation of in vitro penetration of frozen–thawed boar spermatozoa by caffeine and adenosine.Crossref | GoogleScholarGoogle Scholar | 11241779PubMed |

Funsho Fagbohun, C., and Downs, S. M. (1990). Maturation of the mouse oocyte–cumulus cell complex: stimulation by lectins. Biol. Reprod. 42, 413–423.
Maturation of the mouse oocyte–cumulus cell complex: stimulation by lectins.Crossref | GoogleScholarGoogle Scholar |

Gerrits, R. J., Lunney, J. K., Johnson, L. A., Pursel, V. G., Kraeling, R. R., Rohrer, G. A., and Dobrinsky, J. R. (2005). Perspectives for artificial insemination and genomics to improve global swine populations. Theriogenology 63, 283–299.
Perspectives for artificial insemination and genomics to improve global swine populations.Crossref | GoogleScholarGoogle Scholar | 15626400PubMed |

Gilula, N. B., Epstein, M. L., and Beers, W. H. (1978). Cell-to-cell communication and ovulation. A study of the cumulus–oocyte complex. J. Cell Biol. 78, 58–75.
Cell-to-cell communication and ovulation. A study of the cumulus–oocyte complex.Crossref | GoogleScholarGoogle Scholar | 670298PubMed |

Grupen, C. G. (2014). The evolution of porcine embryo in vitro production. Theriogenology 81, 24–37.
The evolution of porcine embryo in vitro production.Crossref | GoogleScholarGoogle Scholar | 24274407PubMed |

Grupen, C. G., and Armstrong, D. T. (2010). Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM. Reprod. Fertil. Dev. 22, 1100–1109.
Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM.Crossref | GoogleScholarGoogle Scholar | 20797348PubMed |

Hao, Y., Mathialagan, N., Walters, E., Mao, J., Lai, L., Becker, D., Li, W., Critser, J., and Prather, R. S. (2006). Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol. Reprod. 75, 726–733.
Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 16870945PubMed |

Hussein, T. S., Froiland, D. A., Amato, F., Thompson, J. G., and Gilchrist, R. B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257–5268.
Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins.Crossref | GoogleScholarGoogle Scholar | 16263764PubMed |

Janowski, D., Salilew-Wondim, D., Torner, H., Tesfaye, D., Ghanem, N., Tomek, W., El-Sayed, A., Schellander, K., and Hölker, M. (2012). Incidence of apoptosis and transcript abundance in bovine follicular cells is associated with the quality of the enclosed oocyte. Theriogenology 78, 656–669.e5.
Incidence of apoptosis and transcript abundance in bovine follicular cells is associated with the quality of the enclosed oocyte.Crossref | GoogleScholarGoogle Scholar | 22578626PubMed |

Joo, B. S., Kim, M. K., Na, Y. J., Moon, H. S., Lee, K. S., and Kim, H. D. (2001). The mechanism of action of coculture on embryo development in the mouse model: direct embryo-to-cell contact and the removal of deleterious components. Fertil. Steril. 75, 193–199.
The mechanism of action of coculture on embryo development in the mouse model: direct embryo-to-cell contact and the removal of deleterious components.Crossref | GoogleScholarGoogle Scholar | 11163837PubMed |

Kątska-Książkiewicz, L. (2006). Pig embryo production by in vitro maturation and fertilization of ovarian oocytes. A review. J. Anim. Feed Sci. 15, 525–542.
Pig embryo production by in vitro maturation and fertilization of ovarian oocytes. A review.Crossref | GoogleScholarGoogle Scholar |

Kawashima, I., Liu, Z., Mullany, L. K., Mihara, T., Richards, J. S., and Shimada, M. (2012). EGF-like factors induce expansion of the cumulus cell–oocyte complexes by activating calpain-mediated cell movement. Endocrinology 153, 3949–3959.
EGF-like factors induce expansion of the cumulus cell–oocyte complexes by activating calpain-mediated cell movement.Crossref | GoogleScholarGoogle Scholar | 22673225PubMed |

Kidson, A., Schoevers, E., Langendijk, P., Verheijden, J., Colenbrander, B., and Bevers, M. (2003). The effect of oviductal epithelial cell co-culture during in vitro maturation on sow oocyte morphology, fertilization and embryo development. Theriogenology 59, 1889–1903.
The effect of oviductal epithelial cell co-culture during in vitro maturation on sow oocyte morphology, fertilization and embryo development.Crossref | GoogleScholarGoogle Scholar | 12600727PubMed |

LeBel, C. P., Ischiropoulos, H., and Bondy, S. C. (1992). Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5, 227–231.
Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1322737PubMed |

Lee, K. S., Joo, B. S., Na, Y. J., Yoon, M. S., Choi, O. H., and Kim, W. W. (2001). Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J. Assist. Reprod. Genet. 18, 490–498.
Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET.Crossref | GoogleScholarGoogle Scholar | 11665664PubMed |

Lonergan, P., and Fair, T. (2016). Maturation of oocytes in vitro. Annu. Rev. Anim. Biosci. 4, 255–268.
Maturation of oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 26566159PubMed |

Lopera-Vásquez, R., Hamdi, M., Fernandez-Fuertes, B., Maillo, V., Beltrán-Breña, P., Calle, A., Redruello, A., López-Martín, S., Gutierrez-Adán, A., Yañez-Mó, M., Ramirez, M. A., and Rizos, D. (2016). Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One 11, e0148083.
Extracellular vesicles from BOEC in in vitro embryo development and quality.Crossref | GoogleScholarGoogle Scholar | 26845570PubMed |

Lorenzo, M. S., Maruri, A., Cruzanso, P. R., Teplitz, G. M., Fello, M. F., and Lombardo, D. M. (2019). The antioxidant dimethylthiourea improves IVF efficiency and decreases cumulus cell apoptosis in pigs. Reprod. Fertil. Dev. 31, 1607–1615.
The antioxidant dimethylthiourea improves IVF efficiency and decreases cumulus cell apoptosis in pigs.Crossref | GoogleScholarGoogle Scholar | 31242959PubMed |

Luo, Y., Lin, L., Bolund, L., Jensen, T. G., and Brandt Sørensen, C. (2012). Genetically modified pigs for biomedical research. J. Inherit. Metab. Dis. 35, 695–713.
Genetically modified pigs for biomedical research.Crossref | GoogleScholarGoogle Scholar | 22453682PubMed |

Martino, N. A., Dell’Aquila, M. E., Cardone, R. A., Somoskoi, B., Lacalandra, G. M., and Cseh, S. (2013). Vitrification preserves chromatin integrity, bioenergy potential and oxidative parameters in mouse embryos. Reprod. Biol. Endocrinol. 11, 27.
Vitrification preserves chromatin integrity, bioenergy potential and oxidative parameters in mouse embryos.Crossref | GoogleScholarGoogle Scholar | 23552480PubMed |

Maruri, A., Cruzans, P. R., Lorenzo, M. S., Tello, M. F., Teplitz, G. M., Carou, M. C., and Lombardo, D. M. (2018). Embryotrophic effect of a short-term embryo coculture with bovine luteal cells. Theriogenology 119, 143–149.
Embryotrophic effect of a short-term embryo coculture with bovine luteal cells.Crossref | GoogleScholarGoogle Scholar | 30006130PubMed |

Mattioli, M., Galeati, G., and Seren, E. (1988a). Effect of follicle somatic cells during pig oocyte maturation on egg penetrability and male pronucleus formation. Gamete Res. 20, 177–183.
Effect of follicle somatic cells during pig oocyte maturation on egg penetrability and male pronucleus formation.Crossref | GoogleScholarGoogle Scholar | 3235035PubMed |

Mattioli, M., Galeati, G., Bacci, M. L., and Seren, E. (1988b). Follicular factors influence oocyte fertilizability by modulating the intercellular cooperation between cumulus cells and oocyte. Gamete Res. 21, 223–232.
Follicular factors influence oocyte fertilizability by modulating the intercellular cooperation between cumulus cells and oocyte.Crossref | GoogleScholarGoogle Scholar | 3246367PubMed |

Moussa, M., Shu, J., Zhang, X. H., and Zeng, F. (2015). Maternal control of oocyte quality in cattle ‘a review’. Anim. Reprod. Sci. 155, 11–27.
Maternal control of oocyte quality in cattle ‘a review’.Crossref | GoogleScholarGoogle Scholar | 25726438PubMed |

Ng, Y. H., Rome, S., Jalabert, A., Forterre, A., Singh, H., Hincks, C. L., and Salamonsen, L. A. (2013). Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo–endometrial cross talk at implantation. PLoS One 8, e58502.
Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo–endometrial cross talk at implantation.Crossref | GoogleScholarGoogle Scholar | 23516492PubMed |

Orsi, N. M., and Reisch, J. B. (2007). Mammalian embryo co-culture: trials and tribulations of a misunderstood method. Theriogenology 67, 441–458.
Mammalian embryo co-culture: trials and tribulations of a misunderstood method.Crossref | GoogleScholarGoogle Scholar | 17118433PubMed |

Picton, H., Briggs, D., and Gosden, R. (1998). The molecular basis of oocyte growth and development. Mol. Cell. Endocrinol. 145, 27–37.
The molecular basis of oocyte growth and development.Crossref | GoogleScholarGoogle Scholar | 9922096PubMed |

Piehl, L. L., Fischman, M. L., Hellman, U., Cisale, H., and Miranda, P. V. (2013). Boar seminal plasma exosomes: effect on sperm function and protein identification by sequencing. Theriogenology 79, 1071–1082.
Boar seminal plasma exosomes: effect on sperm function and protein identification by sequencing.Crossref | GoogleScholarGoogle Scholar | 23489476PubMed |

Rękawiecki, R., Kowalik, M. K., and Kotwica, J. (2011). Nuclear progesterone receptor isoforms and their functions in the female reproductive tract. Pol. J. Vet. Sci. 14, 149–158.
Nuclear progesterone receptor isoforms and their functions in the female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 21528728PubMed |

Rocha-Frigoni, N. A. S., Leão, B. C. S., Nogueira, E., Accorsi, M. F., and Mingoti, G. Z. (2014). Reduced levels of intracellular reactive oxygen species and apoptotic status are not correlated with increases in cryotolerance of bovine embryos produced in vitro in the presence of antioxidants. Reprod. Fertil. Dev. 26, 797–805.
Reduced levels of intracellular reactive oxygen species and apoptotic status are not correlated with increases in cryotolerance of bovine embryos produced in vitro in the presence of antioxidants.Crossref | GoogleScholarGoogle Scholar |

Romar, R., Coy, P., Campos, I., Gadea, J., Matas, C., and Ruiz, S. (2001). Effect of co-culture of porcine sperm and oocytes with porcine oviductal epithelial cells on in vitro fertilization. Anim. Reprod. Sci. 68, 85–98.
Effect of co-culture of porcine sperm and oocytes with porcine oviductal epithelial cells on in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 11600277PubMed |

Rothchild, I. (1981). The regulation of the mammalian corpus luteum. Recent Prog. Horm. Res. 37, 183–298.
| 7025133PubMed |

Saeed-Zidane, M., Linden, L., Salilew-Wondim, D., Held, E., Neuhoff, C., Tholen, E., Hoelker, M., Schellander, K., and Tesfaye, D. (2017). Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress. PLoS One 12, e0187569.
Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 29117219PubMed |

Salehnia, M., and Zavareh, S. (2013). The effects of progesterone on oocyte maturation and embryo development. Int. J. Fertil. Steril. 7, 74–81.
| 24520467PubMed |

Sinha, A., Principe, S., Alfaro, J., Ignatchenko, A., Ignatchenko, V., and Kislinger, T. (2018). Proteomic profiling of secreted proteins, exosomes, and microvesicles in cell culture conditioned media. Methods Mol. Biol. 1722, 91–102.
Proteomic profiling of secreted proteins, exosomes, and microvesicles in cell culture conditioned media.Crossref | GoogleScholarGoogle Scholar | 29264800PubMed |

Siqueira, L. C., Barreta, M. H., Gasperin, B., Bohrer, R., Oliveira, J. F., Santos, J. T., Buratini, J., and Gonçalves, P. B. (2012). Angiotensin II, progesterone, and prostaglandins are sequential steps in the pathway to bovine oocyte nuclear maturation. Theriogenology 77, 1779–1787.
Angiotensin II, progesterone, and prostaglandins are sequential steps in the pathway to bovine oocyte nuclear maturation.Crossref | GoogleScholarGoogle Scholar | 22365701PubMed |

Son, Y. J., Lee, S. E., Hyun, H., Shin, M. Y., Park, Y. G., Jeong, S. G., Kim, E. Y., and Park, S.-P. (2017). Fibroblast growth factor 10 markedly improves in vitro maturation of porcine cumulus–oocyte complexes. Mol. Reprod. Dev. 84, 67–75.
Fibroblast growth factor 10 markedly improves in vitro maturation of porcine cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 27862569PubMed |

Tanghe, S., Van Soom, A., Nauynck, H., Coryn, M., and De Kruif, A. (2002). Minireview: functions of the cumulus oophurus during oocyte maturation, ovulation and fertilization. Mol. Reprod. Dev. 61, 414–424.
Minireview: functions of the cumulus oophurus during oocyte maturation, ovulation and fertilization.Crossref | GoogleScholarGoogle Scholar | 11835587PubMed |

Teilmann, S. C., Clement, C. A., Thorup, J., Byskov, A. G., and Christensen, S. T. (2006). Expression and localization of the progesterone receptor in mouse and human reproductive organs. J. Endocrinol. 191, 525–535.
Expression and localization of the progesterone receptor in mouse and human reproductive organs.Crossref | GoogleScholarGoogle Scholar | 17170211PubMed |

Teplitz, G. M., Maruri, A., Cruzans, P. R., Carou, M. C., and Lombardo, D. M. (2016). Culture of porcine luteal cells as a substrate for in vitro maturation of porcine cumulus oocyte complexes. Establishment and characterization. Spermova 6, 140–143.
Culture of porcine luteal cells as a substrate for in vitro maturation of porcine cumulus oocyte complexes. Establishment and characterization.Crossref | GoogleScholarGoogle Scholar |

Thibodeaux, J. K., Broussard, J. R., Godke, R. A., and Hansel, W. (1994). Stimulation of progesterone production in bovine luteal cells by co-incubation with bovine blastocyst-stage embryos or trophoblastic vesicles. J. Reprod. Fertil. 101, 657–662.
Stimulation of progesterone production in bovine luteal cells by co-incubation with bovine blastocyst-stage embryos or trophoblastic vesicles.Crossref | GoogleScholarGoogle Scholar | 7966022PubMed |

Wang, W. H., Macháty, Z., Abeydeera, L. R., Prather, R. S., and Day, B. N. (1999). Time course of cortical and zona reaction of pig oocytes upon intracellular calcium increase induced by thimerosal. Zygote 7, 79–86.
Time course of cortical and zona reaction of pig oocytes upon intracellular calcium increase induced by thimerosal.Crossref | GoogleScholarGoogle Scholar | 10216920PubMed |

Warzych, E., Pers-Kamszyc, E., Krzywac, A., Dudzinska, S., and Lechniak, D. (2013). Apoptotix index within cumulus cells is a questionable marker of meiotic competence of bovine oocytes matured in vitro. Reprod. Biol. 13, 82–87.
Apoptotix index within cumulus cells is a questionable marker of meiotic competence of bovine oocytes matured in vitro.Crossref | GoogleScholarGoogle Scholar | 23522075PubMed |

Wiltbank, M. C. (1994). Cell types and hormonal mechanisms associated with mid-cycle corpus luteum function. J. Anim. Sci. 72, 1873–1883.
Cell types and hormonal mechanisms associated with mid-cycle corpus luteum function.Crossref | GoogleScholarGoogle Scholar | 7928767PubMed |

Xia, P., Wang, Z., Yang, Z., Tan, J., and Qin, P. (2001). Ultrastructural study of polyspermy during early embryo development in pigs, observed by scanning electron microscope and transmission electron microscope. Cell Tissue Res. 303, 271–275.
Ultrastructural study of polyspermy during early embryo development in pigs, observed by scanning electron microscope and transmission electron microscope.Crossref | GoogleScholarGoogle Scholar | 11291773PubMed |

Yoon, J. D., Jeon, Y., Cai, L., Hwang, S. U., Kim, E., Lee, E., Kim, D. Y., and Hyun, S. H. (2015). Effects of coculture with cumulus-derived somatic cells on in vitro maturation of porcine oocytes. Theriogenology 83, 294–305.
Effects of coculture with cumulus-derived somatic cells on in vitro maturation of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 25442018PubMed |

Yuan, Y. Q., Van Soom, A., Leroy, J. L., Dewulf, J., Van Zeveren, A., de Kruif, A., and Peelman, L. J. (2005). Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology 63, 2147–2163.
Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence.Crossref | GoogleScholarGoogle Scholar | 15826680PubMed |

Zeyneloglu, H. B., and Kahraman, S. (2009). The use of coculture in assisted reproductive technology: does it have any impact? Curr. Opin. Obstet. Gynecol. 21, 253–259.
The use of coculture in assisted reproductive technology: does it have any impact?Crossref | GoogleScholarGoogle Scholar | 19352179PubMed |

Zhang, J. Y., Jiang, Y., Lin, T., Kang, J. W., Lee, J. E., and Jin, D. I. (2015). Lysophosphatidic acid improves porcine oocyte maturation and embryo development in vitro. Mol. Reprod. Dev. 82, 66–77.
Lysophosphatidic acid improves porcine oocyte maturation and embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 25564987PubMed |