What we can learn from the bovine embryo and mouse models to enable in vitro gametogenesis in cattle
Anna C. Denicol A *A
Abstract
The development of in vitro gametogenesis (IVG) in the mouse opened up unforeseen possibilities for assisted reproduction. The development of this technology to be used in cattle production could accelerate the rate of genetic selection by dramatically reducing the generation interval, while decreasing the environmental impact of livestock production as the need to grow animals in the process of genetic selection would be reduced or even eliminated. Although several steps of the process of IVG such as in vitro oocyte maturation and fertilization, and embryo production are already routinely performed in cattle, other steps of the system such as in vitro follicle and oocyte development are still rudimentary. The stable derivation of bovine pluripotent stem cells is the starting point without which IVG cannot be realized. However, producing a primordial germ cell and taking this cell through oogenesis and folliculogenesis in a dish will require a more detailed understanding of the milestones that need to be accomplished in vivo before they can be recapitulated in vitro. In particular, understanding the regulatory circuitry of germ cell specification in the embryo, the timing and events related to development of the germ cell program, and the factors necessary to make a competent egg, will need to be uncovered. Here, we review the process of IVG and provide a brief description of the current advances and bottlenecks related to in vitro oogenesis and folliculogenesis in cattle. Finally, we provide a brief comparison between mice and cows in this regard.
Keywords: bovine, cattle, embryo, embryonic stem cell, fetus, folliculogenesis, gametogenesis, oocyte, stem cell.
References
Adhikari D, Liu K (2009) Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocrine Reviews 30(5), 438-464.
| Crossref | Google Scholar | PubMed |
Alberio R, Kobayashi T, Surani MA (2021) Conserved features of non-primate bilaminar disc embryos and the germline. Stem Cell Reports 16(5), 1078-1092.
| Crossref | Google Scholar | PubMed |
Bogliotti YS, Wu J, Vilarino M, Okamura D, Soto DA, Zhong C, Sakurai M, Sampaio RV, Suzuki K, Izpisua Belmonte JC, Ross PJ (2018) Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. Proceedings of the National Academy of Sciences of the United States of America 115(9), 2090-2095.
| Crossref | Google Scholar |
Botigelli RC, Guiltinan C, Arcanjo RB, Denicol AC (2023) In vitro gametogenesis from embryonic stem cells in livestock species: recent advances, opportunities, and challenges to overcome. Journal of Animal Science 101, skad137.
| Crossref | Google Scholar |
Bromfield JJ, Sheldon IM (2013) Lipopolysaccharide reduces the primordial follicle pool in the bovine ovarian cortex ex vivo and in the murine ovary in vivo. Biology of Reproduction 88(4), 98.
| Crossref | Google Scholar | PubMed |
Candelaria JI, Botigelli RC, Guiltinan C, Shikanov A, Denicol AC (2024) Three-dimensional culture in a bioengineered matrix and somatic cell complementation to improve growth and survival of bovine preantral follicles. BioRxiv [Preprint].
| Crossref | Google Scholar |
Correia HHV, Lima LF, Sousa FGC, Ferreira ACA, Cadenas J, Paes VM, Alves BG, Shikanov A, Figueiredo JR (2020) Activation of goat primordial follicles in vitro: influence of alginate and ovarian tissue. Reproduction in Domestic Animals 55(1), 105-109.
| Crossref | Google Scholar | PubMed |
Fair T (2010) Mammalian oocyte development: checkpoints for competence. Reproduction, Fertility and Development 22(1), 13-20.
| Crossref | Google Scholar | PubMed |
Ferreira ACA, Sá NAR, Cadenas J, Correia HHV, Guerreiro DD, Alves BG, Lima LF, Celestino JJH, Rodrigues APPR, Gastal EL, Figueiredo JR (2020) Pituitary porcine FSH, and recombinant bovine and human FSH differentially affect growth and relative abundances of mRNA transcripts of preantral and early developing antral follicles in goats. Animal Reproduction Science 219, 106461.
| Crossref | Google Scholar | PubMed |
Fortune JE, Yang MY, Allen JJ, Herrick SL (2013) Triennial reproduction symposium: the ovarian follicular reserve in cattle: what regulates its formation and size? Journal of Animal Science 91(7), 3041-3050.
| Crossref | Google Scholar | PubMed |
Gill ME, Hu YC, Lin Y, Page DC (2011) Licensing of gametogenesis, dependent on RNA binding protein DAZL, as a gateway to sexual differentiation of fetal germ cells. Proceedings of the National Academy of Sciences of the United States of America 108(18), 7443-7448.
| Crossref | Google Scholar | PubMed |
Ginther OJ (2016) The theory of follicle selection in cattle. Domestic Animal Endocrinology 57, 85-99.
| Crossref | Google Scholar | PubMed |
Goszczynski DE, Cheng H, Demyda-Peyrás S, Medrano JF, Wu J, Ross PJ (2019) In vitro breeding: application of embryonic stem cells to animal production. Biology of Reproduction 100(4), 885-895.
| Crossref | Google Scholar | PubMed |
Green LJ, Zhou H, Padmanabhan V, Shikanov A (2019) Adipose-derived stem cells promote survival, growth, and maturation of early-stage murine follicles. Stem Cell Research & Therapy 10(1), 102.
| Crossref | Google Scholar | PubMed |
Hayashi K, Saitou M (2013) Generation of eggs from mouse embryonic stem cells and induced pluripotent stem cells. Nature Protocols 8(8), 1513-1524.
| Crossref | Google Scholar | PubMed |
Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, Shimamoto S, Imamura T, Nakashima K, Saitou M, Hayashi K (2016) Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature 539(7628), 299-303.
| Crossref | Google Scholar |
Irie N, Kobayashi T, Azim Surani M (2024) Human primordial germ cell-like cell induction from pluripotent stem cells by SOX17 and PRDM1 expression. Methods in Molecular Biology 2770, 87-97.
| Crossref | Google Scholar | PubMed |
Kobayashi T, Zhang H, Tang WWC, Irie N, Withey S, Klisch D, Sybirna A, Dietmann S, Contreras DA, Webb R, Allegrucci C, Alberio R, Surani MA (2017) Principles of early human development and germ cell program from conserved model systems. Nature 546(7658), 416-420.
| Crossref | Google Scholar | PubMed |
Kobayashi T, Castillo-Venzor A, Penfold CA, Morgan M, Mizuno N, Tang WWC, Osada Y, Hirao M, Yoshida F, Sato H, Nakauchi H, Hirabayashi M, Surani MA (2021) Tracing the emergence of primordial germ cells from bilaminar disc rabbit embryos and pluripotent stem cells. Cell Reports 37(2), 109812.
| Crossref | Google Scholar | PubMed |
Latorraca LB, Galvão A, Rabaglino MB, D’Augero JM, Kelsey G, Fair T (2024) Single-Cell profiling reveals transcriptome dynamics during bovine oocyte growth. BMC Genomics 25(1), 335.
| Crossref | Google Scholar |
Lodde V, Modina S, Galbusera C, Franciosi F, 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(6), 740-749.
| Crossref | Google Scholar | PubMed |
Lodde V, Modina S, Maddox-Hyttel P, Franciosi F, Lauria A, 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(5), 915-924.
| Crossref | Google Scholar | PubMed |
Lussier JG, Matton P, Dufour JJ (1987) Growth rates of follicles in the ovary of the cow. Journal of Reproduction and Fertility 81(2), 301-307.
| Crossref | Google Scholar | PubMed |
Maddox-Hyttel P, Alexopoulos NI, Vajta G, Lewis I, Rogers P, Cann L, Callesen H, Tveden-Nyborg P, Trounson A (2003) Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125(4), 607-623.
| Crossref | Google Scholar | PubMed |
Martinez CA, Rizos D, Rodriguez-Martinez H, Funahashi H (2023) Oocyte-cumulus cells crosstalk: new comparative insights. Theriogenology 205, 87-93.
| Crossref | Google Scholar | PubMed |
Matzuk MM, Burns KH, Viveiros MM, Eppig JJ (2002) Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296(5576), 2178-2180.
| Crossref | Google Scholar | PubMed |
McDonnell SP, Candelaria JI, Morton AJ, Denicol AC (2022) Isolation of small preantral follicles from the bovine ovary using a combination of fragmentation, homogenization, and serial filtration. Journal of Visualized Experiments 187, e64423.
| Crossref | Google Scholar | PubMed |
Morton AJ, Candelaria JI, McDonnell SP, Zgodzay DP, Denicol AC (2023) Review: roles of follicle-stimulating hormone in preantral folliculogenesis of domestic animals: what can we learn from model species and where do we go from here? Animal 17(Suppl 1), 100743.
| Crossref | Google Scholar |
Pillai VV, Koganti PP, Kei TG, Gurung S, Butler WR, Selvaraj V (2021) Efficient induction and sustenance of pluripotent stem cells from bovine somatic cells. Biology Open 10(10), bio058756.
| Crossref | Google Scholar |
Richard S, Zhou Y, Jasoni CL, Pankhurst MW (2024) Ovarian follicle size or growth rate can both be determinants of ovulatory follicle selection in mice. Biology of Reproduction 110(1), 130-139.
| Crossref | Google Scholar |
Shirasawa A, Hayashi M, Shono M, Ideta A, Yoshino T, Hayashi K (2024) Efficient derivation of embryonic stem cells and primordial germ cell-like cells in cattle. Journal of Reproduction and Development 70(2), 82-95.
| Crossref | Google Scholar | PubMed |
Silva AFB, Lima LF, Sousa RP, Silva RF, Neves GCS, Carvalho MAM, Ferreira ACA, Oliveira AC, Alves BG, Rodrigues APR, Gastal EL, Bordignon V, Figueiredo JR (2024) Stem cell-conditioned medium improves methylation patterns and quality of caprine preantral follicles. Reproduction 168(3), e230483.
| Crossref | Google Scholar |
Sternlicht AL, Schultz RM (1981) Biochemical studies of mammalian oogenesis: kinetics of accumulation of total and poly(A)-containing RNA during growth of the mouse oocyte. Journal of Experimental Zoology 215(2), 191-200.
| Crossref | Google Scholar | PubMed |
Stoop H, Honecker F, Cools M, de Krijger R, Bokemeyer C, Looijenga LHJ (2005) Differentiation and development of human female germ cells during prenatal gonadogenesis: an immunohistochemical study. Human Reproduction 20(6), 1466-1476.
| Crossref | Google Scholar | PubMed |
Su Y, Wang L, Fan Z, Liu Y, Zhu J, Kaback D, Oudiz J, Patrick T, Yee SP, Tian XC, Polejaeva I, Tang Y (2021) Establishment of bovine-induced pluripotent stem cells. International Journal of Molecular Sciences 22(19), 10489.
| Crossref | Google Scholar | PubMed |
Viana J (2022) 2022 statistics of embryo production and transfer in domestic farm animals: the main trends or the world embryo industry still stand. Embryo Transfer Newsletter 41(4), 20-38.
| Google Scholar |
Vijayakumar S, Sala R, Kang G, Chen A, Pablo MA, Adebayo AI, Cipriano A, Fowler JL, Gomes DL, Ang LT, Loh KM, Sebastiano V (2023) Monolayer platform to generate and purify primordial germ-like cells in vitro provides insights into human germline specification. Nature Communications 14(1), 5690.
| Crossref | Google Scholar | PubMed |
Wrobel KH, Süß F (1998) Identification and temporospatial distribution of bovine primordial germ cells prior to gonadal sexual differentiation. Anatomy and Embryology 197, 451-467.
| Crossref | Google Scholar | PubMed |
Yang MY, Fortune JE (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. Biology of Reproduction 78(6), 1153-1161.
| Crossref | Google Scholar | PubMed |
Yoshino T, Suzuki T, Nagamatsu G, Yabukami H, Ikegaya M, Kishima M, Kita H, Imamura T, Nakashima K, Nishinakamura R, Tachibana M, Inoue M, Shima Y, Morohashi KI, Hayashi K (2021) Generation of ovarian follicles from mouse pluripotent stem cells. Science 373(6552), eabe0237.
| Crossref | Google Scholar |