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Vertebrate reproductive science and technology
RESEARCH ARTICLE

In vitro growth of immature bovine follicles and oocytes

Evelyn E. Telfer A B D , Kenichiro Sakaguchi A B C , Yvonne L. Clarkson A B and Marie McLaughlin A B
+ Author Affiliations
- Author Affiliations

A Institute of Cell Biology, School of Biological Sciences, The University of Edinburgh, The Hugh Robson Building, 15 George Square, Edinburgh, EH8 9XD, UK.

B Institute of Cell Biology, Genes and Development Group, The University of Edinburgh, The Hugh Robson Building, 15 George Square, Edinburgh, EH8 9XD, UK.

C Laboratory of Theriogenology, Department of Clinical Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido 060-0818, Japan.

D Corresponding author. Email: evelyn.telfer@ed.ac.uk

Reproduction, Fertility and Development 32(2) 1-6 https://doi.org/10.1071/RD19270
Published: 2 December 2019

Abstract

The limitation in the supply of mature, fertilisable oocytes constitutes a major impediment to increasing the success of assisted reproduction, stem cell derivation and cloning in domestic species. Techniques are being developed to grow immature oocytes in vitro that have the potential to increase the supply of oocytes. Mouse oocytes can be cultured from initial stages of development to maturity, and live young have been produced, but for domestic species, such as cows, with long growth periods, in vitro systems that allow complete growth of oocytes contained within primordial follicles to maturity is technically challenging and has not yet been achieved. For cows, several culture systems have been developed that support specific developmental stages, but a multistep culture system will be required for complete growth in vitro. This review highlights the steps that will be required to achieve the goal of growing oocytes in vitro.

Additional keywords: assisted reproductive technology, ART, in vitro maturation, livestock, oogenesis.


References

Abdel-Ghani, M. A., Sakaguchi, K., Kanno, C., Yanagawa, Y., Katagiri, S., and Nagano, M. (2018). Effects of pre-maturational culture duration on developmental competence of bovine small-sized oocytes. J. Reprod. Dev. 64, 365–369.
Effects of pre-maturational culture duration on developmental competence of bovine small-sized oocytes.Crossref | GoogleScholarGoogle Scholar | 29798966PubMed |

Adhikari, D., and Liu, K. (2010). mTOR signaling in the control of activation of primordial follicles. Cell Cycle 9, 1673–1674.
mTOR signaling in the control of activation of primordial follicles.Crossref | GoogleScholarGoogle Scholar | 20404510PubMed |

Albuz, F. K., Sasseville, M., Lane, M., Armstrong, D. T., Thompson, J. G., and Gilchrist, R. B. (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 25, 2999–3011.
Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 20870682PubMed |

Anckaert, E., De Rycke, M., and Smitz, J. (2013). Culture of oocytes and risk of imprinting defects. Hum. Reprod. Update 19, 52–66.
Culture of oocytes and risk of imprinting defects.Crossref | GoogleScholarGoogle Scholar | 23054129PubMed |

Antonino, D. C., Soares, M. M., Junior, J. M., de Alvarenga, P. B., Mohallem, R. F. F., Rocha, C. D., Vieira, L. A., de Souza, A. G., Beletti, M. E., Alves, B. G., Jacomini, J. O., Goulart, L. R., and Alves, K. A. (2019). Three-dimensional levitation culture improves in-vitro growth of secondary follicles in bovine model. Reprod. Biomed. Online 38, 300–311.
Three-dimensional levitation culture improves in-vitro growth of secondary follicles in bovine model.Crossref | GoogleScholarGoogle Scholar | 30639159PubMed |

Araújo, V. R., Gastal, M. O., Wischral, A., Figueiredo, J. R., and Gastal, E. L. (2014). In vitro development of bovine secondary follicles in two- and three-dimensional culture systems using vascular endothelial growth factor, insulin-like growth factor-1, and growth hormone. Theriogenology 82, 1246–1253.
In vitro development of bovine secondary follicles in two- and three-dimensional culture systems using vascular endothelial growth factor, insulin-like growth factor-1, and growth hormone.Crossref | GoogleScholarGoogle Scholar | 25219848PubMed |

Araújo, V. R., Gastal, M. O., Wischral, A., Figueiredo, J. R., and Gastal, E. L. (2015). Long-term in vitro culture of bovine preantral follicles: effect of base medium and medium replacement methods. Anim. Reprod. Sci. 161, 23–31.
Long-term in vitro culture of bovine preantral follicles: effect of base medium and medium replacement methods.Crossref | GoogleScholarGoogle Scholar | 26304751PubMed |

Banwell, K. M., and Thompson, J. G. (2008). In vitro maturation of mammalian oocytes: outcomes and consequences. Semin. Reprod. Med. 26, 162–174.
In vitro maturation of mammalian oocytes: outcomes and consequences.Crossref | GoogleScholarGoogle Scholar | 18302108PubMed |

Blondin, P. (2017). Logistics of large scale commercial IVF embryo production. Reprod. Fertil. Dev. 29, 32–36.
Logistics of large scale commercial IVF embryo production.Crossref | GoogleScholarGoogle Scholar |

Castrillon, D. H., Miao, L., Kollipara, R., Horner, J. W., and DePinho, R. A. (2003). Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301, 215–218.
Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a.Crossref | GoogleScholarGoogle Scholar | 12855809PubMed |

da Cunha, E. V., de Souza, G. B., Passos, J. R. S., Silva, A. W. B., Dau, A. M., Saraiva, M. V. A., Lobo, R. N. B., and Silva, J. R. V. (2017). Effects of bone morphogenetic protein 4 (BMP4) on in vitro development and survival of bovine preantral follicles enclosed in fragments ovarian tissue. Zygote 25, 256–264.
Effects of bone morphogenetic protein 4 (BMP4) on in vitro development and survival of bovine preantral follicles enclosed in fragments ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 28300526PubMed |

da Cunha, E. V., Melo, L. R. F., Sousa, G. B., Araújo, V. R., Vasconcelos, G. L., Silva, A. W. B., and Silva, J. R. V. (2018). Effect of bone morphogenetic proteins 2 and 4 on survival and development of bovine secondary follicles cultured in vitro. Theriogenology 110, 44–51.
Effect of bone morphogenetic proteins 2 and 4 on survival and development of bovine secondary follicles cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 29331831PubMed |

Dupont, J., and Scaramuzzi, R. J. (2016). Insulin signalling and glucose transport in the ovary and ovarian function during the ovarian cycle. Biochem. J. 473, 1483–1501.
Insulin signalling and glucose transport in the ovary and ovarian function during the ovarian cycle.Crossref | GoogleScholarGoogle Scholar | 27234585PubMed |

Ealy, A. D., Wooldridge, L. K., and McCoski, S. R. (2019). Board invited review: post-transfer consequences of in vitro-produced embryos in cattle. J. Anim. Sci. 97, 2555–2568.
Board invited review: post-transfer consequences of in vitro-produced embryos in cattle.Crossref | GoogleScholarGoogle Scholar | 30968113PubMed |

Eppig, J. J., and O’Brien, M. J. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54, 197–207.
Development in vitro of mouse oocytes from primordial follicles.Crossref | GoogleScholarGoogle Scholar | 8838017PubMed |

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

Fortune, J. E., Kito, S., Wandji, S. A., and Srsen, V. (1998). Activation of bovine and baboon primordial follicles in vitro. Theriogenology 49, 441–449.
Activation of bovine and baboon primordial follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 10732025PubMed |

Gigli, I., Byrd, D. D., and Fortune, J. E. (2006). Effects of oxygen tension and supplements to the culture medium on activation and development of bovine follicles in vitro. Theriogenology 66, 344–353.
Effects of oxygen tension and supplements to the culture medium on activation and development of bovine follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 16442155PubMed |

Gosden, R. G., and Telfer, E. E. (1987). Scaling of follicular sizes in mammalian ovaries. J. Zool. (Lond.) 211, 157–168.
Scaling of follicular sizes in mammalian ovaries.Crossref | GoogleScholarGoogle Scholar |

Gougeon, A., and Busso, D. (2000). Morphologic and functional determinants of primordial and primary follicles in the monkey ovary. Mol. Cell. Endocrinol. 163, 33–42.
Morphologic and functional determinants of primordial and primary follicles in the monkey ovary.Crossref | GoogleScholarGoogle Scholar | 10963871PubMed |

Gutierrez, C. G., Ralph, J. H., Telfer, E. E., Wilmut, I., and Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62, 1322–1328.
Growth and antrum formation of bovine preantral follicles in long-term culture in vitro.Crossref | GoogleScholarGoogle Scholar | 10775183PubMed |

Hashimoto, S., Yamanaka, M., Yamochi, T., Iwata, H., Kawahara-Miki, R., Inoue, M., and Morimoto, Y. (2019). Mitochondrial function in immature bovine oocytes is improved by an increase of cellular cyclic AMP. Sci. Rep. 9, 5167.
Mitochondrial function in immature bovine oocytes is improved by an increase of cellular cyclic AMP.Crossref | GoogleScholarGoogle Scholar | 30914704PubMed |

Heinzmann, J., Mattern, F., Aldag, P., Bernal-Ulloa, S. M., Schneider, T., Haaf, T., and Niemann, H. (2015). Extended in vitro maturation affects gene expression and DNA methylation in bovine oocytes. Mol. Hum. Reprod. 21, 770–782.
Extended in vitro maturation affects gene expression and DNA methylation in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 26155800PubMed |

Hirao, Y., Itoh, T., Shimizu, M., Iga, K., Aoyagi, K., Kobayashi, M., Kacchi, M., Hoshi, H., and Takenouchi, N. (2004). In vitro growth and development of bovine oocyte–granulosa cell complexes on the flat substratum: effects of high polyvinylpyrrolidone concentration in culture medium. Biol. Reprod. 70, 83–91.
In vitro growth and development of bovine oocyte–granulosa cell complexes on the flat substratum: effects of high polyvinylpyrrolidone concentration in culture medium.Crossref | GoogleScholarGoogle Scholar | 12954724PubMed |

Jimenez, C. R., Araújo, V. R., Penitente-Filho, J. M., de Azevedo, J. L., Silveira, R. G., and Torres, C. A. (2016). The base medium affects ultrastructure and survival of bovine preantral follicles cultured in vitro. Theriogenology 85, 1019–1029.
The base medium affects ultrastructure and survival of bovine preantral follicles cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 26711701PubMed |

Jorssen, E. P., Langbeen, A., Fransen, E., Martinez, E. L., Leroy, J. L., and Bols, P. E. (2014). Monitoring preantral follicle survival and growth in bovine ovarian biopsies by repeated use of neutral red and cultured in vitro under low and high oxygen tension. Theriogenology 82, 387–395.
Monitoring preantral follicle survival and growth in bovine ovarian biopsies by repeated use of neutral red and cultured in vitro under low and high oxygen tension.Crossref | GoogleScholarGoogle Scholar | 24877724PubMed |

Luciano, A. M., and Sirard, M. A. (2018). Successful in vitro maturation of oocytes: a matter of follicular differentiation. Biol. Reprod. 98, 162–169.
Successful in vitro maturation of oocytes: a matter of follicular differentiation.Crossref | GoogleScholarGoogle Scholar | 29165545PubMed |

Maidarti, M., Clarkson, Y. L., McLaughlin, M., Anderson, R. A., and Telfer, E. E. (2019). Inhibition of PTEN activates bovine non-growing follicles in vitro but increases DNA damage and reduces DNA repair response. Hum. Reprod. 34, 297–307.
Inhibition of PTEN activates bovine non-growing follicles in vitro but increases DNA damage and reduces DNA repair response.Crossref | GoogleScholarGoogle Scholar | 30521029PubMed |

Matoba, S., Bender, K., Fahey, A. G., Mamo, S., Brennan, L., Lonergan, P., and Fair, T. (2014). Predictive value of bovine follicular components as markers of oocyte developmental potential. Reprod. Fertil. Dev. 26, 337–345.
Predictive value of bovine follicular components as markers of oocyte developmental potential.Crossref | GoogleScholarGoogle Scholar | 23514964PubMed |

McLaughlin, M., and Telfer, E. E. (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 |

McLaughlin, M., Bromfield, J. J., Albertini, D. F., and Telfer, E. E. (2010). Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol. Hum. Reprod. 16, 644–653.
Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles.Crossref | GoogleScholarGoogle Scholar | 20203128PubMed |

McLaughlin, M., Albertini, D. F., Wallace, W. H. B., Anderson, R. A., and Telfer, E. E. (2018). Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. Mol. Hum. Reprod. 24, 135–142.
Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system.Crossref | GoogleScholarGoogle Scholar | 29390119PubMed |

Moore, S. G., and Hasler, J. F. (2017). A 100-year review: reproductive technologies in dairy science. J. Dairy Sci. 100, 10314–10331.
A 100-year review: reproductive technologies in dairy science.Crossref | GoogleScholarGoogle Scholar | 29153167PubMed |

Nagano, M. (2019). Acquisition of developmental competence and in vitro growth culture of bovine oocytes. J. Reprod. Dev. 65, 195–201.
Acquisition of developmental competence and in vitro growth culture of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 30799320PubMed |

O’Brien, M. J., Pendola, J. K., and Eppig, J. J. (2003). A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68, 1682–1686.
A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence.Crossref | GoogleScholarGoogle Scholar | 12606400PubMed |

Oliveira, S. A., Calsavara, V. F., and Cortes, G. C. (2016). Final oocyte maturation in assisted reproduction with human chorionic gonadotropin and gonadotropin-releasing hormone agonist (dual trigger). JBRA Assist. Reprod. 20, 246–250.
Final oocyte maturation in assisted reproduction with human chorionic gonadotropin and gonadotropin-releasing hormone agonist (dual trigger).Crossref | GoogleScholarGoogle Scholar | 28050961PubMed |

Otoi, T., Yamamoto, K., Koyama, N., Tachikawa, S., and Suzuki, T. (1997). Bovine oocyte diameter in relation to developmental competence. Theriogenology 48, 769–774.
Bovine oocyte diameter in relation to developmental competence.Crossref | GoogleScholarGoogle Scholar | 16728170PubMed |

Paes, V. M., Vieira, L. A., Correia, H. H. V., Sa, N. A. R., Moura, A. A. A., Sales, A. D., Rodrigues, A. P. R., Magalhaes-Padilha, D. M., Santos, F. W., Apgar, G. A., Campello, C. C., Camargo, L. S. A., and Figueiredo, J. R. (2016). Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus–oocyte complex. Theriogenology 86, 994–1003.
Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus–oocyte complex.Crossref | GoogleScholarGoogle Scholar | 27125691PubMed |

Passos, M. J., Vasconcelos, G. L., Silva, A. W., Brito, I. R., Saraiva, M. V., Magalhaes, D. M., Costa, J. J., Donato, M. A., Ribeiro, R. P., Cunha, E. V., Peixoto, C. A., Campello, C. C., Figueiredo, J. R., van den Hurk, R., and Silva, J. R. (2013). Accelerated growth of bovine preantral follicles in vitro after stimulation with both FSH and BMP-15 is accompanied by ultrastructural changes and increased atresia. Theriogenology 79, 1269–1277.
Accelerated growth of bovine preantral follicles in vitro after stimulation with both FSH and BMP-15 is accompanied by ultrastructural changes and increased atresia.Crossref | GoogleScholarGoogle Scholar | 23582608PubMed |

Paulino, L. R. F. M., Cunha, E. V., Barbalho Silva, A. W., Souza, G. B., Lopes, E. P. F., Donato, M. A. M., Peixoto, C. A., Matos-Brito, B. G., van den Hurk, R., and Silva, J. R. V. (2018). Effects of tumour necrosis factor-alpha and interleukin-1 beta on in vitro development of bovine secondary follicles. Reprod. Domest. Anim. 53, 997–1005.
Effects of tumour necrosis factor-alpha and interleukin-1 beta on in vitro development of bovine secondary follicles.Crossref | GoogleScholarGoogle Scholar |

Pontes, J. H., Nonato-Junior, I., Sanches, B. V., Ereno-Junior, J. C., Uvo, S., Barreiros, T. R., Oliveira, J. A., Hasler, J. F., and Seneda, M. M. (2009). Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology 71, 690–697.
Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows.Crossref | GoogleScholarGoogle Scholar | 18995895PubMed |

Reddy, P., Liu, L., Adhikari, D., Jagarlamudi, K., Rajareddy, S., Shen, Y., Du, C., Tang, W., Hamalainen, T., Peng, S. L., Lan, Z. J., Cooney, A. J., Huhtaniemi, I., and Liu, K. (2008). Oocyte-specific deletion of PTEN causes premature activation of the primordial follicle pool. Science 319, 611–613.
Oocyte-specific deletion of PTEN causes premature activation of the primordial follicle pool.Crossref | GoogleScholarGoogle Scholar | 18239123PubMed |

Rossetto, R., Saraiva, M. V., dos Santos, R. R., da Silva, C. M., Faustino, L. R., Chaves, R. N., Brito, I. R., Rodrigues, G. Q., Lima, I. M., Donato, M. A., Peixoto, C. A., and de Figueiredo, J. R. (2013). Effect of medium composition on the in vitro culture of bovine pre-antral follicles: morphology and viability do not guarantee functionality. Zygote 21, 125–128.
Effect of medium composition on the in vitro culture of bovine pre-antral follicles: morphology and viability do not guarantee functionality.Crossref | GoogleScholarGoogle Scholar | 22717039PubMed |

Rossi, R. O., da Cunha, E. V., Portela, A. M., Passos, J. R., Costa, J. J., Silva, A. W., Saraiva, M. V., Peixoto, C. A., Donato, M. A., van den Hurk, R., and Silva, J. R. (2016). Influence of BMP-2 on early follicular development and mRNA expression of oocyte specific genes in bovine preantral follicles cultured in vitro. Histol. Histopathol. 31, 339–348.
| 26435174PubMed |

Salilew-Wondim, D., Fournier, E., Hoelker, M., Saeed-Zidane, M., Tholen, E., Looft, C., Neuhoff, C., Besenfelder, U., Havlicek, V., Rings, F., Gagne, D., Sirard, M. A., Robert, C., Shojaei Saadi, H. A., Gad, A., Schellander, K., and Tesfaye, D. (2015). Genome-wide DNA methylation patterns of bovine blastocysts developed in vivo from embryos completed different stages of development in vitro. PLoS One 10, e0140467.
Genome-wide DNA methylation patterns of bovine blastocysts developed in vivo from embryos completed different stages of development in vitro.Crossref | GoogleScholarGoogle Scholar | 26536655PubMed |

Scaramuzzi, R. J., Martensz, N. D., and Van Look, P. F. (1980). Ovarian morphology and the concentration of steroids, and of gonadotrophins during the breeding season in ewes actively immunized against oestradiol-17 beta or oestrone. J. Reprod. Fertil. 59, 303–310.
Ovarian morphology and the concentration of steroids, and of gonadotrophins during the breeding season in ewes actively immunized against oestradiol-17 beta or oestrone.Crossref | GoogleScholarGoogle Scholar | 6776269PubMed |

Sirard, M. A., and Blondin, P. (1996). Oocyte maturation and IVF in cattle. Anim. Reprod. Sci. 42, 417–426.
Oocyte maturation and IVF in cattle.Crossref | GoogleScholarGoogle Scholar |

Tang, K., Yang, W. C., Li, X., Wu, C. J., Sang, L., and Yang, L. G. (2012). GDF-9 and bFGF enhance the effect of FSH on the survival, activation, and growth of cattle primordial follicles. Anim. Reprod. Sci. 131, 129–134.
GDF-9 and bFGF enhance the effect of FSH on the survival, activation, and growth of cattle primordial follicles.Crossref | GoogleScholarGoogle Scholar | 22516229PubMed |

Telfer, E. E., Binnie, J. P., McCaffery, F. H., and Campbell, B. K. (2000). In vitro development of oocytes from porcine and bovine primary follicles. Mol. Cell. Endocrinol. 163, 117–123.
In vitro development of oocytes from porcine and bovine primary follicles.Crossref | GoogleScholarGoogle Scholar | 10963883PubMed |

Telfer, E. E., McLaughlin, M., Ding, C., and Thong, K. J. (2008). A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum. Reprod. 23, 1151–1158.
A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin.Crossref | GoogleScholarGoogle Scholar | 18326514PubMed |

Thomas, F. H., Campbell, B. K., Armstrong, D. G., and Telfer, E. E. (2007). Effects of IGF-I bioavailability on bovine preantral follicular development in vitro. Reproduction 133, 1121–1128.
Effects of IGF-I bioavailability on bovine preantral follicular development in vitro.Crossref | GoogleScholarGoogle Scholar | 17636166PubMed |

Vasconcelos, G. L., Saraiva, M. V., Costa, J. J., Passos, M. J., Silva, A. W., Rossi, R. O., Portela, A. M., Duarte, A. B., Magalhaes-Padilha, D. M., Campelo, C. C., Figueiredo, J. R., van den Hurk, R., and Silva, J. R. (2013). Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles. Reprod. Fertil. Dev. 25, 1194–1203.
Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 23241220PubMed |

Walters, K. A., Armstrong, D. G., and Telfer, E. E. (2007). Bovine mural granulosa cells, and not the oocyte, are the major source of proteases capable of IGFBP-2 degradation. Anim. Reprod. Sci. 98, 365–370.
Bovine mural granulosa cells, and not the oocyte, are the major source of proteases capable of IGFBP-2 degradation.Crossref | GoogleScholarGoogle Scholar | 16713142PubMed |

Wandji, S. A., Eppig, J. J., and Fortune, J. E. (1996). FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45, 817–832.
FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 16727844PubMed |

Yang, M. Y., and Fortune, J. E. (2006). Testosterone stimulates the primary to secondary follicle transition in bovine follicles in vitro. Biol. Reprod. 75, 924–932.
Testosterone stimulates the primary to secondary follicle transition in bovine follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 16943368PubMed |

Yang, M. Y., and Fortune, J. E. (2007). Vascular endothelial growth factor stimulates the primary to secondary follicle transition in bovine follicles in vitro. Mol. Reprod. Dev. 74, 1095–1104.
Vascular endothelial growth factor stimulates the primary to secondary follicle transition in bovine follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 17290425PubMed |

Yang, M. Y., and Fortune, J. E. (2008). The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biol. Reprod. 78, 1153–1161.
The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes.Crossref | GoogleScholarGoogle Scholar | 18305225PubMed |

Yang, M. Y., Cushman, R. A., and Fortune, J. E. (2017). Anti-Müllerian hormone inhibits activation and growth of bovine ovarian follicles in vitro and is localized to growing follicles. Mol. Hum. Reprod. 23, 282–291.
Anti-Müllerian hormone inhibits activation and growth of bovine ovarian follicles in vitro and is localized to growing follicles.Crossref | GoogleScholarGoogle Scholar | 28333275PubMed |

Zhang, H., and Liu, K. (2015). Cellular and molecular regulation of the activation of mammalian primordial follicles: somatic cells initiate follicle activation in adulthood. Hum. Reprod. Update 21, 779–786.
Cellular and molecular regulation of the activation of mammalian primordial follicles: somatic cells initiate follicle activation in adulthood.Crossref | GoogleScholarGoogle Scholar | 26231759PubMed |

Zoheir, K. M., Harisa, G. I., Allam, A. A., Yang, L., Li, X., Liang, A., Abd-Rabou, A. A., and Harrath, A. H. (2017). Effect of alpha lipoic acid on in vitro development of bovine secondary preantral follicles. Theriogenology 88, 124–130.
Effect of alpha lipoic acid on in vitro development of bovine secondary preantral follicles.Crossref | GoogleScholarGoogle Scholar | 27743686PubMed |