Artificially produced gametes in mice, humans and other species
Katsuhiko Hayashi A G , Cesare Galli B C , Sebastian Diecke D and Thomas B. Hildebrandt E F
+ Author Affiliations
- Author Affiliations
A Department of Stem Cell Biology and Medicine, Graduate School of Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-0054, Japan.
B Avantea, Laboratory of Reproductive Technologies, 26100 Cremona, Italy.
C Fondazione Avantea, 26100 Cremona, Italy.
D Max-Delbrueck-Center for Molecular Medicine, 13092 Berlin, Germany.
E Leibniz Institute for Zoo and Wildlife Research, D-10315 Berlin, Germany.
F Freie Universität Berlin, D-14195 Berlin, Germany.
G Corresponding author. Email: hayashik@hgs.med.kyushu-u.ac.jp
Reproduction, Fertility and Development 33(2) 91-101 https://doi.org/10.1071/RD20265
Published: 8 January 2021
Abstract
The production of gametes from pluripotent stem cells in culture, also known as in vitro gametogenesis, will make an important contribution to reproductive biology and regenerative medicine, both as a unique tool for understanding germ cell development and as an alternative source of gametes for reproduction. In vitro gametogenesis was developed using mouse pluripotent stem cells but is increasingly being applied in other mammalian species, including humans. In principle, the entire process of germ cell development is nearly reconstitutable in culture using mouse pluripotent stem cells, although the fidelity of differentiation processes and the quality of resultant gametes remain to be refined. The methodology in the mouse system is only partially applicable to other species, and thus it must be optimised for each species. In this review, we update the current status of in vitro gametogenesis in mice, humans and other animals, and discuss challenges for further development of this technology.
Keywords: germ cells, in vitro, pluripotent stem cells, reconstitution.
References
Abe, K., Takano, H., and Ito, T. (1982). Response of the epididymal duct in the corpus epididymidis to efferent or epididymal duct ligation in the mouse. J. Reprod. Fertil. 64, 69–72.| Response of the epididymal duct in the corpus epididymidis to efferent or epididymal duct ligation in the mouse.Crossref | GoogleScholarGoogle Scholar | 6275082PubMed |
Aramaki, S., Hayashi, K., Kurimoto, K., Ohta, H., Yabuta, Y., Iwanari, H., Mochizuki, Y., Hamakubo, T., Kato, Y., Shirahige, K., and Saitou, M. (2013). A mesodermal factor, T, specifies mouse germ cell fate by directly activating germline determinants. Dev. Cell 27, 516–529.
| A mesodermal factor, T, specifies mouse germ cell fate by directly activating germline determinants.Crossref | GoogleScholarGoogle Scholar | 24331926PubMed |
Bao, S., Tang, F., Li, X., Hayashi, K., Gillich, A., Lao, K., and Surani, M. A. (2009). Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 461, 1292–1295.
| Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 19816418PubMed |
Ben-Haim, N., Lu, C., Guzman-Ayala, M., Pescatore, L., Mesnard, D., Bischofberger, M., Naef, F., Robertson, E. J., and Constam, D. B. (2006). The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev. Cell 11, 313–323.
| The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4.Crossref | GoogleScholarGoogle Scholar | 16950123PubMed |
Ben-Nun, I. F., Montague, S. C., Houck, M. L., Tran, H. T., Garitaonandia, I., Leonardo, T. R., Wang, Y. C., Charter, S. J., Laurent, L. C., Ryder, O. A., and Loring, J. F. (2011). Induced pluripotent stem cells from highly endangered species. Nat. Methods 8, 829–831.
| Induced pluripotent stem cells from highly endangered species.Crossref | GoogleScholarGoogle Scholar | 21892153PubMed |
Bloise, E., Lin, W., Liu, X., Simbulan, R., Kolahi, K. S., Petraglia, F., Maltepe, E., Donjacour, A., and Rinaudo, P. (2012). Impaired placental nutrient transport in mice generated by in vitro fertilization. Endocrinology 153, 3457–3467.
| Impaired placental nutrient transport in mice generated by in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 22562173PubMed |
Bogliotti, Y. S., Wu, J., Vilarino, M., Okamura, D., Soto, D. A., Zhong, C., Sakurai, M., Sampaio, R. V., Suzuki, K., Izpisua Belmonte, J. C., and Ross, P. J. (2018). Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. Proc. Natl Acad. Sci. USA 115, 2090–2095.
| Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 29440377PubMed |
Bowles, J., Knight, D., Smith, C., Wilhelm, D., Richman, J., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M. J., Rossant, J., Hamada, H., and Koopman, P. (2006). Retinoid signaling determines germ cell fate in mice. Science 312, 596–600.
| Retinoid signaling determines germ cell fate in mice.Crossref | GoogleScholarGoogle Scholar | 16574820PubMed |
Brons, I. G., Smithers, L. E., Trotter, M. W., Rugg-Gunn, P., Sun, B., Chuva de Sousa Lopes, S. M., Howlett, S. K., Clarkson, A., Ahrlund-Richter, L., Pedersen, R. A., and Vallier, L. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191–195.
| Derivation of pluripotent epiblast stem cells from mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 17597762PubMed |
Chan, Y. S., Goke, J., Ng, J. H., Lu, X., Gonzales, K. A., Tan, C. P., Tng, W. Q., Hong, Z. Z., Lim, Y. S., and Ng, H. H. (2013). Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast. Cell Stem Cell 13, 663–675.
| Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast.Crossref | GoogleScholarGoogle Scholar | 24315441PubMed |
Clark, A. T., Rodriguez, R. T., Bodnar, M. S., Abeyta, M. J., Cedars, M. I., Turek, P. J., Firpo, M. T., and Reijo Pera, R. A. (2004). Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma. Stem Cells 22, 169–179.
| Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma.Crossref | GoogleScholarGoogle Scholar | 14990856PubMed |
de Waal, E., Vrooman, L. A., Fischer, E., Ord, T., Mainigi, M. A., Coutifaris, C., Schultz, R. M., and Bartolomei, M. S. (2015). The cumulative effect of assisted reproduction procedures on placental development and epigenetic perturbations in a mouse model. Hum. Mol. Genet. 24, 6975–6985.
| The cumulative effect of assisted reproduction procedures on placental development and epigenetic perturbations in a mouse model.Crossref | GoogleScholarGoogle Scholar | 26401051PubMed |
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 |
Fang, Z. F., Gai, H., Huang, Y. Z., Li, S. G., Chen, X. J., Shi, J. J., Wu, L., Liu, A., Xu, P., and Sheng, H. Z. (2006). Rabbit embryonic stem cell lines derived from fertilized, parthenogenetic or somatic cell nuclear transfer embryos. Exp. Cell Res. 312, 3669–3682.
| Rabbit embryonic stem cell lines derived from fertilized, parthenogenetic or somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar | 16996056PubMed |
Fawcett, D. W., and Hoffer, A. P. (1979). Failure of exogenous androgen to prevent regression of the initial segments of the rat epididymis after efferent duct ligation or orchidectomy. Biol. Reprod. 20, 162–181.
| Failure of exogenous androgen to prevent regression of the initial segments of the rat epididymis after efferent duct ligation or orchidectomy.Crossref | GoogleScholarGoogle Scholar | 454730PubMed |
Gafni, O., Weinberger, L., Mansour, A. A., Manor, Y. S., Chomsky, E., Ben-Yosef, D., Kalma, Y., Viukov, S., Maza, I., Zviran, A., Rais, Y., Shipony, Z., Mukamel, Z., Krupalnik, V., Zerbib, M., Geula, S., Caspi, I., Schneir, D., Shwartz, T., Gilad, S., Amann-Zalcenstein, D., Benjamin, S., Amit, I., Tanay, A., Massarwa, R., Novershtern, N., and Hanna, J. H. (2013). Derivation of novel human ground state naive pluripotent stem cells. Nature 504, 282–286.
| Derivation of novel human ground state naive pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 24172903PubMed |
Geijsen, N., Horoschak, M., Kim, K., Gribnau, J., Eggan, K., and Daley, G. Q. (2004). Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427, 148–154.
| Derivation of embryonic germ cells and male gametes from embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 14668819PubMed |
Goszczynski, D. E., Cheng, H., Demyda-Peyras, S., Medrano, J. F., Wu, J., and Ross, P. J. (2019). In vitro breeding: application of embryonic stem cells to animal production. Biol. Reprod. 100, 885–895.
| In vitro breeding: application of embryonic stem cells to animal production.Crossref | GoogleScholarGoogle Scholar | 30551176PubMed |
Guo, G., Yang, J., Nichols, J., Hall, J. S., Eyres, I., Mansfield, W., and Smith, A. (2009). Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063–1069.
| Klf4 reverts developmentally programmed restriction of ground state pluripotency.Crossref | GoogleScholarGoogle Scholar | 19224983PubMed |
Hajkova, P., Erhardt, S., Lane, N., Haaf, T., El-Maarri, O., Reik, W., Walter, J., and Surani, M. A. (2002). Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117, 15–23.
| Epigenetic reprogramming in mouse primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 12204247PubMed |
Hajkova, P., Ancelin, K., Waldmann, T., Lacoste, N., Lange, U. C., Cesari, F., Lee, C., Almouzni, G., Schneider, R., and Surani, M. A. (2008). Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452, 877–881.
| Chromatin dynamics during epigenetic reprogramming in the mouse germ line.Crossref | GoogleScholarGoogle Scholar | 18354397PubMed |
Hayashi, K., and Surani, M. A. (2009). Self-renewing epiblast stem cells exhibit continual delineation of germ cells with epigenetic reprogramming in vitro. Development 136, 3549–3556.
| Self-renewing epiblast stem cells exhibit continual delineation of germ cells with epigenetic reprogramming in vitro.Crossref | GoogleScholarGoogle Scholar | 19793888PubMed |
Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S., and Saitou, M. (2011). Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146, 519–532.
| Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 21820164PubMed |
Hayashi, K., Ogushi, S., Kurimoto, K., Shimamoto, S., Ohta, H., and Saitou, M. (2012). Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338, 971–975.
| Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice.Crossref | GoogleScholarGoogle Scholar | 23042295PubMed |
Hikabe, O., Hamazaki, N., Nagamatsu, G., Obata, Y., Hirao, Y., Hamada, N., Shimamoto, S., Imamura, T., Nakashima, K., Saitou, M., and Hayashi, K. (2016). Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature 539, 299–303.
| Reconstitution in vitro of the entire cycle of the mouse female germ line.Crossref | GoogleScholarGoogle Scholar | 27750280PubMed |
Hildebrandt, T. B., Hermes, R., Colleoni, S., Diecke, S., Holtze, S., Renfree, M. B., Stejskal, J., Hayashi, K., Drukker, M., Loi, P., Goritz, F., Lazzari, G., and Galli, C. (2018). Embryos and embryonic stem cells from the white rhinoceros. Nat. Commun. 9, 2589.
| Embryos and embryonic stem cells from the white rhinoceros.Crossref | GoogleScholarGoogle Scholar | 29973581PubMed |
Honda, A., Hirose, M., Hatori, M., Matoba, S., Miyoshi, H., Inoue, K., and Ogura, A. (2010). Generation of induced pluripotent stem cells in rabbits: potential experimental models for human regenerative medicine. J. Biol. Chem. 285, 31362–31369.
| Generation of induced pluripotent stem cells in rabbits: potential experimental models for human regenerative medicine.Crossref | GoogleScholarGoogle Scholar | 20670936PubMed |
Honda, A., Choijookhuu, N., Izu, H., Kawano, Y., Inokuchi, M., Honsho, K., Lee, A. R., Nabekura, H., Ohta, H., Tsukiyama, T., Ohinata, Y., Kuroiwa, A., Hishikawa, Y., Saitou, M., Jogahara, T., and Koshimoto, C. (2017). Flexible adaptation of male germ cells from female iPSCs of endangered Tokudaia osimensis. Sci. Adv. 3, e1602179.
| Flexible adaptation of male germ cells from female iPSCs of endangered Tokudaia osimensis.Crossref | GoogleScholarGoogle Scholar | 28508054PubMed |
Hou, Z., An, L., Han, J., Yuan, Y., Chen, D., and Tian, J. (2018). Revolutionize livestock breeding in the future: an animal embryo-stem cell breeding system in a dish. J. Anim. Sci. Biotechnol. 9, 90.
| Revolutionize livestock breeding in the future: an animal embryo-stem cell breeding system in a dish.Crossref | GoogleScholarGoogle Scholar | 30568797PubMed |
Hübner, K., Fuhrmann, G., Christenson, L. K., Kehler, J., Reinbold, R., De La Fuente, R., Wood, J., Strauss, J. F., Boiani, M., and Scholer, H. R. (2003). Derivation of oocytes from mouse embryonic stem cells. Science 300, 1251–1256.
| Derivation of oocytes from mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 12730498PubMed |
Irie, N., Weinberger, L., Tang, W. W., Kobayashi, T., Viukov, S., Manor, Y. S., Dietmann, S., Hanna, J. H., and Surani, M. A. (2015). SOX17 is a critical specifier of human primordial germ cell fate. Cell 160, 253–268.
| SOX17 is a critical specifier of human primordial germ cell fate.Crossref | GoogleScholarGoogle Scholar | 25543152PubMed |
Ishikura, Y., Yabuta, Y., Ohta, H., Hayashi, K., Nakamura, T., Okamoto, I., Yamamoto, T., Kurimoto, K., Shirane, K., Sasaki, H., and Saitou, M. (2016). In vitro derivation and propagation of spermatogonial stem cell activity from mouse pluripotent stem cells. Cell Rep. 17, 2789–2804.
| In vitro derivation and propagation of spermatogonial stem cell activity from mouse pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 27926879PubMed |
Kalkan, T., and Smith, A. (2014). Mapping the route from naive pluripotency to lineage specification. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130540.
| Mapping the route from naive pluripotency to lineage specification.Crossref | GoogleScholarGoogle Scholar | 25349449PubMed |
Kalkan, T., Olova, N., Roode, M., Mulas, C., Lee, H. J., Nett, I., Marks, H., Walker, R., Stunnenberg, H. G., Lilley, K. S., Nichols, J., Reik, W., Bertone, P., and Smith, A. (2017). Tracking the embryonic stem cell transition from ground state pluripotency. Development 144, 1221–1234.
| Tracking the embryonic stem cell transition from ground state pluripotency.Crossref | GoogleScholarGoogle Scholar | 28174249PubMed |
Kanatsu-Shinohara, M., Ogonuki, N., Inoue, K., Miki, H., Ogura, A., Toyokuni, S., and Shinohara, T. (2003). Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol. Reprod. 69, 612–616.
| Long-term proliferation in culture and germline transmission of mouse male germline stem cells.Crossref | GoogleScholarGoogle Scholar | 12700182PubMed |
Kee, K., Gonsalves, J. M., Clark, A. T., and Pera, R. A. (2006). Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev. 15, 831–837.
| Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 17253946PubMed |
Kerr, J. B., and de Kretser, D. M. (1974). Proceedings: the role of the Sertoli cell in phagocytosis of the residual bodies of spermatids. J. Reprod. Fertil. 36, 439–440.
| Proceedings: the role of the Sertoli cell in phagocytosis of the residual bodies of spermatids.Crossref | GoogleScholarGoogle Scholar | 4819326PubMed |
Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M. J., Ji, H., Ehrlich, L. I., Yabuuchi, A., Takeuchi, A., Cunniff, K. C., Hongguang, H., McKinney-Freeman, S., Naveiras, O., Yoon, T. J., Irizarry, R. A., Jung, N., Seita, J., Hanna, J., Murakami, P., Jaenisch, R., Weissleder, R., Orkin, S. H., Weissman, I. L., Feinberg, A. P., and Daley, G. Q. (2010). Epigenetic memory in induced pluripotent stem cells. Nature 467, 285–290.
| Epigenetic memory in induced pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 20644535PubMed |
Kobayashi, H., Sakurai, T., Miura, F., Imai, M., Mochiduki, K., Yanagisawa, E., Sakashita, A., Wakai, T., Suzuki, Y., Ito, T., Matsui, Y., and Kono, T. (2013). High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome Res. 23, 616–627.
| High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice.Crossref | GoogleScholarGoogle Scholar | 23410886PubMed |
Kobayashi, T., Zhang, H., Tang, W. W. C., Irie, N., Withey, S., Klisch, D., Sybirna, A., Dietmann, S., Contreras, D. A., Webb, R., Allegrucci, C., Alberio, R., and Surani, M. A. (2017). Principles of early human development and germ cell program from conserved model systems. Nature 546, 416–420.
| Principles of early human development and germ cell program from conserved model systems.Crossref | GoogleScholarGoogle Scholar | 28607482PubMed |
Kojima, Y., Sasaki, K., Yokobayashi, S., Sakai, Y., Nakamura, T., Yabuta, Y., Nakaki, F., Nagaoka, S., Woltjen, K., Hotta, A., Yamamoto, T., and Saitou, M. (2017). Evolutionarily distinctive transcriptional and signaling programs drive human germ cell lineage specification from pluripotent stem cells. Cell Stem Cell 21, 517–532e515.
| Evolutionarily distinctive transcriptional and signaling programs drive human germ cell lineage specification from pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 28985527PubMed |
Korody, M. L., Pivaroff, C., Nguyen, T. D., Peterson, S. E., Ryder, O. A., and Loring, J. F. (2017). Four new induced pluripotent stem cell lines produced from northern white rhinoceros with non-integrating reprogramming factors. bioRxiv , 202499.
Koubova, J., Menke, D. B., Zhou, Q., Capel, B., Griswold, M. D., and Page, D. C. (2006). Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl Acad. Sci. USA 103, 2474–2479.
| Retinoic acid regulates sex-specific timing of meiotic initiation in mice.Crossref | GoogleScholarGoogle Scholar | 16461896PubMed |
Kubo, N., Toh, H., Shirane, K., Shirakawa, T., Kobayashi, H., Sato, T., Sone, H., Sato, Y., Tomizawa, S., Tsurusaki, Y., Shibata, H., Saitsu, H., Suzuki, Y., Matsumoto, N., Suyama, M., Kono, T., Ohbo, K., and Sasaki, H. (2015). DNA methylation and gene expression dynamics during spermatogonial stem cell differentiation in the early postnatal mouse testis. BMC Genomics 16, 624.
| DNA methylation and gene expression dynamics during spermatogonial stem cell differentiation in the early postnatal mouse testis.Crossref | GoogleScholarGoogle Scholar | 26290333PubMed |
Kurimoto, K., Yabuta, Y., Ohinata, Y., Shigeta, M., Yamanaka, K., and Saitou, M. (2008). Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev. 22, 1617–1635.
| Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice.Crossref | GoogleScholarGoogle Scholar | 18559478PubMed |
Kurimoto, K., Yabuta, Y., Hayashi, K., Ohta, H., Kiyonari, H., Mitani, T., Moritoki, Y., Kohri, K., Kimura, H., Yamamoto, T., Katou, Y., Shirahige, K., and Saitou, M. (2015). Quantitative dynamics of chromatin remodeling during germ cell specification from mouse embryonic stem cells. Cell Stem Cell 16, 517–532.
| Quantitative dynamics of chromatin remodeling during germ cell specification from mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 25800778PubMed |
Lawson, K. A., and Hage, W. J. (1994). Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182, 68–84.
| Clonal analysis of the origin of primordial germ cells in the mouse.Crossref | GoogleScholarGoogle Scholar | 7835158PubMed |
Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V., Korving, J. P., and Hogan, B. L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424–436.
| Bmp4 is required for the generation of primordial germ cells in the mouse embryo.Crossref | GoogleScholarGoogle Scholar | 10049358PubMed |
Lee, J., Kanatsu-Shinohara, M., Ogonuki, N., Miki, H., Inoue, K., Morimoto, T., Morimoto, H., Ogura, A., and Shinohara, T. (2009). Heritable imprinting defect caused by epigenetic abnormalities in mouse spermatogonial stem cells. Biol. Reprod. 80, 518–527.
| Heritable imprinting defect caused by epigenetic abnormalities in mouse spermatogonial stem cells.Crossref | GoogleScholarGoogle Scholar | 19020300PubMed |
Lillehammer, M., Meuwissen, T. H., and Sonesson, A. K. (2013). Genomic selection for two traits in a maternal pig breeding scheme. J. Anim. Sci. 91, 3079–3087.
| Genomic selection for two traits in a maternal pig breeding scheme.Crossref | GoogleScholarGoogle Scholar | 23658351PubMed |
Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R., and Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22, 361–365.
| Requirement for Wnt3 in vertebrate axis formation.Crossref | GoogleScholarGoogle Scholar | 10431240PubMed |
Maeda, Y., Shiratsuchi, A., Namiki, M., and Nakanishi, Y. (2002). Inhibition of sperm production in mice by annexin V microinjected into seminiferous tubules: possible etiology of phagocytic clearance of apoptotic spermatogenic cells and male infertility. Cell Death Differ. 9, 742–749.
| Inhibition of sperm production in mice by annexin V microinjected into seminiferous tubules: possible etiology of phagocytic clearance of apoptotic spermatogenic cells and male infertility.Crossref | GoogleScholarGoogle Scholar | 12058279PubMed |
Malki, S., van der Heijden, G. W., O’Donnell, K. A., Martin, S. L., and Bortvin, A. (2014). A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev. Cell 29, 521–533.
| A role for retrotransposon LINE-1 in fetal oocyte attrition in mice.Crossref | GoogleScholarGoogle Scholar | 24882376PubMed |
McLaren, A., and Southee, D. (1997). Entry of mouse embryonic germ cells into meiosis. Dev. Biol. 187, 107–113.
| Entry of mouse embryonic germ cells into meiosis.Crossref | GoogleScholarGoogle Scholar | 9224678PubMed |
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 |
Meuwissen, T. H., Hayes, B. J., and Goddard, M. E. (2001). Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 1819–1829.
| 11290733PubMed |
Morohaku, K., Tanimoto, R., Sasaki, K., Kawahara-Miki, R., Kono, T., Hayashi, K., Hirao, Y., and Obata, Y. (2016). Complete in vitro generation of fertile oocytes from mouse primordial germ cells. Proc. Natl Acad. Sci. USA 113, 9021–9026.
| Complete in vitro generation of fertile oocytes from mouse primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 27457928PubMed |
Murakami, K., Gunesdogan, U., Zylicz, J. J., Tang, W. W. C., Sengupta, R., Kobayashi, T., Kim, S., Butler, R., Dietmann, S., and Surani, M. A. (2016). NANOG alone induces germ cells in primed epiblast in vitro by activation of enhancers. Nature 529, 403–407.
| NANOG alone induces germ cells in primed epiblast in vitro by activation of enhancers.Crossref | GoogleScholarGoogle Scholar | 26751055PubMed |
Nakaki, F., Hayashi, K., Ohta, H., Kurimoto, K., Yabuta, Y., and Saitou, M. (2013). Induction of mouse germ-cell fate by transcription factors in vitro. Nature 501, 222–226.
| Induction of mouse germ-cell fate by transcription factors in vitro.Crossref | GoogleScholarGoogle Scholar | 23913270PubMed |
Nakamura, T., Okamoto, I., Sasaki, K., Yabuta, Y., Iwatani, C., Tsuchiya, H., Seita, Y., Nakamura, S., Yamamoto, T., and Saitou, M. (2016). A developmental coordinate of pluripotency among mice, monkeys and humans. Nature 537, 57–62.
| A developmental coordinate of pluripotency among mice, monkeys and humans.Crossref | GoogleScholarGoogle Scholar | 27556940PubMed |
Navara, C. S., Hornecker, J., Grow, D., Chaudhari, S., Hornsby, P. J., Ichida, J. K., Eggan, K., and McCarrey, J. R. (2013). Derivation of induced pluripotent stem cells from the baboon: a nonhuman primate model for preclinical testing of stem cell therapies. Cell. Reprogram. 15, 495–502.
| Derivation of induced pluripotent stem cells from the baboon: a nonhuman primate model for preclinical testing of stem cell therapies.Crossref | GoogleScholarGoogle Scholar | 24182315PubMed |
Ohinata, Y., Payer, B., O’Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S. C., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A., Saitou, M., and Surani, M. A. (2005). Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436, 207–213.
| Blimp1 is a critical determinant of the germ cell lineage in mice.Crossref | GoogleScholarGoogle Scholar | 15937476PubMed |
Ohinata, Y., Ohta, H., Shigeta, M., Yamanaka, K., Wakayama, T., and Saitou, M. (2009). A signaling principle for the specification of the germ cell lineage in mice. Cell 137, 571–584.
| A signaling principle for the specification of the germ cell lineage in mice.Crossref | GoogleScholarGoogle Scholar | 19410550PubMed |
Ohta, H., Kurimoto, K., Okamoto, I., Nakamura, T., Yabuta, Y., Miyauchi, H., Yamamoto, T., Okuno, Y., Hagiwara, M., Shirane, K., Sasaki, H., and Saitou, M. (2017). In vitro expansion of mouse primordial germ cell-like cells recapitulates an epigenetic blank slate. EMBO J. 36, 1888–1907.
| In vitro expansion of mouse primordial germ cell-like cells recapitulates an epigenetic blank slate.Crossref | GoogleScholarGoogle Scholar | 28559416PubMed |
Park, T. S., Galic, Z., Conway, A. E., Lindgren, A., van Handel, B. J., Magnusson, M., Richter, L., Teitell, M. A., Mikkola, H. K., Lowry, W. E., Plath, K., and Clark, A. T. (2009). Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells. Stem Cells 27, 783–795.
| Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells.Crossref | GoogleScholarGoogle Scholar | 19350678PubMed |
Pepling, M. E., and Spradling, A. C. (2001). Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev. Biol. 234, 339–351.
| Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles.Crossref | GoogleScholarGoogle Scholar | 11397004PubMed |
Pineau, C., Le Magueresse, B., Courtens, J. L., and Jegou, B. (1991). Study in vitro of the phagocytic function of Sertoli cells in the rat. Cell Tissue Res. 264, 589–598.
| Study in vitro of the phagocytic function of Sertoli cells in the rat.Crossref | GoogleScholarGoogle Scholar | 1907888PubMed |
Sasaki, K., Yokobayashi, S., Nakamura, T., Okamoto, I., Yabuta, Y., Kurimoto, K., Ohta, H., Moritoki, Y., Iwatani, C., Tsuchiya, H., Nakamura, S., Sekiguchi, K., Sakuma, T., Yamamoto, T., Mori, T., Woltjen, K., Nakagawa, M., Yamamoto, T., Takahashi, K., Yamanaka, S., and Saitou, M. (2015). Robust in vitro induction of human germ cell fate from pluripotent stem cells. Cell Stem Cell 17, 178–194.
| Robust in vitro induction of human germ cell fate from pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 26189426PubMed |
Sasaki, K., Nakamura, T., Okamoto, I., Yabuta, Y., Iwatani, C., Tsuchiya, H., Seita, Y., Nakamura, S., Shiraki, N., Takakuwa, T., Yamamoto, T., and Saitou, M. (2016). The germ cell fate of cynomolgus monkeys is specified in the nascent amnion. Dev. Cell 39, 169–185.
| The germ cell fate of cynomolgus monkeys is specified in the nascent amnion.Crossref | GoogleScholarGoogle Scholar | 27720607PubMed |
Seisenberger, S., Andrews, S., Krueger, F., Arand, J., Walter, J., Santos, F., Popp, C., Thienpont, B., Dean, W., and Reik, W. (2012). The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 48, 849–862.
| The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 23219530PubMed |
Seki, Y., Hayashi, K., Itoh, K., Mizugaki, M., Saitou, M., and Matsui, Y. (2005). Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278, 440–458.
| Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice.Crossref | GoogleScholarGoogle Scholar | 15680362PubMed |
Shirane, K., Toh, H., Kobayashi, H., Miura, F., Chiba, H., Ito, T., Kono, T., and Sasaki, H. (2013). Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet. 9, e1003439.
| Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases.Crossref | GoogleScholarGoogle Scholar | 23637617PubMed |
Shirane, K., Kurimoto, K., Yabuta, Y., Yamaji, M., Satoh, J., Ito, S., Watanabe, A., Hayashi, K., Saitou, M., and Sasaki, H. (2016). Global landscape and regulatory principles of DNA methylation reprogramming for germ cell specification by mouse pluripotent stem cells. Dev. Cell 39, 87–103.
| Global landscape and regulatory principles of DNA methylation reprogramming for germ cell specification by mouse pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 27642137PubMed |
Showell, C., Binder, O., and Conlon, F. L. (2004). T-box genes in early embryogenesis. Dev. Dyn. 229, 201–218.
| T-box genes in early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 14699590PubMed |
Sitzenstock, F., Ytournel, F., Sharifi, A. R., Cavero, D., Taubert, H., Preisinger, R., and Simianer, H. (2013). Efficiency of genomic selection in an established commercial layer breeding program. Genet. Sel. Evol. 45, 29.
| Efficiency of genomic selection in an established commercial layer breeding program.Crossref | GoogleScholarGoogle Scholar | 23902427PubMed |
Skory, R. M., Xu, Y., Shea, L. D., and Woodruff, T. K. (2015). Engineering the ovarian cycle using in vitro follicle culture. Hum. Reprod. 30, 1386–1395.
| Engineering the ovarian cycle using in vitro follicle culture.Crossref | GoogleScholarGoogle Scholar | 25784584PubMed |
Smallwood, S. A., Tomizawa, S., Krueger, F., Ruf, N., Carli, N., Segonds-Pichon, A., Sato, S., Hata, K., Andrews, S. R., and Kelsey, G. (2011). Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 43, 811–814.
| Dynamic CpG island methylation landscape in oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 21706000PubMed |
Stanton, M. M., Tzatzalos, E., Donne, M., Kolundzic, N., Helgason, I., and Ilic, D. (2019). Prospects for the use of induced pluripotent stem cells in animal conservation and environmental protection. Stem Cells Transl. Med. 8, 7–13.
| Prospects for the use of induced pluripotent stem cells in animal conservation and environmental protection.Crossref | GoogleScholarGoogle Scholar | 30251393PubMed |
Sugawa, F., Arauzo-Bravo, M. J., Yoon, J., Kim, K. P., Aramaki, S., Wu, G., Stehling, M., Psathaki, O. E., Hubner, K., and Scholer, H. R. (2015). Human primordial germ cell commitment in vitro associates with a unique PRDM14 expression profile. EMBO J. 34, 1009–1024.
| Human primordial germ cell commitment in vitro associates with a unique PRDM14 expression profile.Crossref | GoogleScholarGoogle Scholar | 25750208PubMed |
Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676.
| Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors.Crossref | GoogleScholarGoogle Scholar | 16904174PubMed |
Takashima, Y., Guo, G., Loos, R., Nichols, J., Ficz, G., Krueger, F., Oxley, D., Santos, F., Clarke, J., Mansfield, W., Reik, W., Bertone, P., and Smith, A. (2014). Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158, 1254–1269.
| Resetting transcription factor control circuitry toward ground-state pluripotency in human.Crossref | GoogleScholarGoogle Scholar | 25215486PubMed |
Tam, P. P., and Zhou, S. X. (1996). The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178, 124–132.
| The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo.Crossref | GoogleScholarGoogle Scholar | 8812114PubMed |
Tang, W. W., Dietmann, S., Irie, N., Leitch, H. G., Floros, V. I., Bradshaw, C. R., Hackett, J. A., Chinnery, P. F., and Surani, M. A. (2015). A unique gene regulatory network resets the human germline epigenome for development. Cell 161, 1453–1467.
| A unique gene regulatory network resets the human germline epigenome for development.Crossref | GoogleScholarGoogle Scholar | 26046444PubMed |
Telfer, E. E., and Zelinski, M. B. (2013). Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil. Steril. 99, 1523–1533.
| Ovarian follicle culture: advances and challenges for human and nonhuman primates.Crossref | GoogleScholarGoogle Scholar | 23635350PubMed |
Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L., and McKay, R. D. (2007). New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196–199.
| New cell lines from mouse epiblast share defining features with human embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 17597760PubMed |
Theunissen, T. W., Powell, B. E., Wang, H., Mitalipova, M., Faddah, D. A., Reddy, J., Fan, Z. P., Maetzel, D., Ganz, K., Shi, L., Lungjangwa, T., Imsoonthornruksa, S., Stelzer, Y., Rangarajan, S., D’Alessio, A., Zhang, J., Gao, Q., Dawlaty, M. M., Young, R. A., Gray, N. S., and Jaenisch, R. (2014). Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 15, 471–487.
| Systematic identification of culture conditions for induction and maintenance of naive human pluripotency.Crossref | GoogleScholarGoogle Scholar | 25090446PubMed |
Toyooka, Y., Tsunekawa, N., Akasu, R., and Noce, T. (2003). Embryonic stem cells can form germ cells in vitro. Proc. Natl Acad. Sci. USA 100, 11457–11462.
| Embryonic stem cells can form germ cells in vitro.Crossref | GoogleScholarGoogle Scholar | 14504407PubMed |
van Leeuwen, J., Rawson, P., Berg, D. K., Wells, D. N., and Pfeffer, P. L. (2020). On the enigmatic disappearance of Rauber’s layer. Proc. Natl Acad. Sci. USA 117, 16409–16417.
| On the enigmatic disappearance of Rauber’s layer.Crossref | GoogleScholarGoogle Scholar | 32601185PubMed |
Verma, R., Holland, M. K., Temple-Smith, P., and Verma, P. J. (2012). Inducing pluripotency in somatic cells from the snow leopard (Panthera uncia), an endangered felid. Theriogenology 77, 220–228.e2.
| Inducing pluripotency in somatic cells from the snow leopard (Panthera uncia), an endangered felid.Crossref | GoogleScholarGoogle Scholar | 22079579PubMed |
Wang, S., Tang, X., Niu, Y., Chen, H., Li, B., Li, T., Zhang, X., Hu, Z., Zhou, Q., and Ji, W. (2007). Generation and characterization of rabbit embryonic stem cells. Stem Cells 25, 481–489.
| Generation and characterization of rabbit embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 17038672PubMed |
Weber, S., Eckert, D., Nettersheim, D., Gillis, A. J., Schafer, S., Kuckenberg, P., Ehlermann, J., Werling, U., Biermann, K., Looijenga, L. H., and Schorle, H. (2010). Critical function of AP-2 gamma/TCFAP2C in mouse embryonic germ cell maintenance. Biol. Reprod. 82, 214–223.
| Critical function of AP-2 gamma/TCFAP2C in mouse embryonic germ cell maintenance.Crossref | GoogleScholarGoogle Scholar | 19776388PubMed |
Wiggans, G. R., Cole, J. B., Hubbard, S. M., and Sonstegard, T. S. (2017). Genomic selection in dairy cattle: the USDA experience. Annu. Rev. Anim. Biosci. 5, 309–327.
| Genomic selection in dairy cattle: the USDA experience.Crossref | GoogleScholarGoogle Scholar | 27860491PubMed |
Yamaji, M., Seki, Y., Kurimoto, K., Yabuta, Y., Yuasa, M., Shigeta, M., Yamanaka, K., Ohinata, Y., and Saitou, M. (2008). Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40, 1016–1022.
| Critical function of Prdm14 for the establishment of the germ cell lineage in mice.Crossref | GoogleScholarGoogle Scholar | 18622394PubMed |
Yamashiro, C., Sasaki, K., Yabuta, Y., Kojima, Y., Nakamura, T., Okamoto, I., Yokobayashi, S., Murase, Y., Ishikura, Y., Shirane, K., Sasaki, H., Yamamoto, T., and Saitou, M. (2018). Generation of human oogonia from induced pluripotent stem cells in vitro. Science 362, 356–360.
| Generation of human oogonia from induced pluripotent stem cells in vitro.Crossref | GoogleScholarGoogle Scholar | 30237246PubMed |
Yin, H., Kristensen, S. G., Jiang, H., Rasmussen, A., and Andersen, C. Y. (2016). Survival and growth of isolated pre-antral follicles from human ovarian medulla tissue during long-term 3D culture. Hum. Reprod. 31, 1531–1539.
| Survival and growth of isolated pre-antral follicles from human ovarian medulla tissue during long-term 3D culture.Crossref | GoogleScholarGoogle Scholar | 27112699PubMed |
Ying, Q. L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., and Smith, A. (2008). The ground state of embryonic stem cell self-renewal. Nature 453, 519–523.
| The ground state of embryonic stem cell self-renewal.Crossref | GoogleScholarGoogle Scholar | 18497825PubMed |
Young, M. A., Larson, D. E., Sun, C. W., George, D. R., Ding, L., Miller, C. A., Lin, L., Pawlik, K. M., Chen, K., Fan, X., Schmidt, H., Kalicki-Veizer, J., Cook, L. L., Swift, G. W., Demeter, R. T., Wendl, M. C., Sands, M. S., Mardis, E. R., Wilson, R. K., Townes, T. M., and Ley, T. J. (2012). Background mutations in parental cells account for most of the genetic heterogeneity of induced pluripotent stem cells. Cell Stem Cell 10, 570–582.
| Background mutations in parental cells account for most of the genetic heterogeneity of induced pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 22542160PubMed |
Yu, R. R., Cheng, A. T., Lagenaur, L. A., Huang, W., Weiss, D. E., Treece, J., Sanders-Beer, B. E., Hamer, D. H., Lee, P. P., Xu, Q., and Liu, Y. (2009). A Chinese rhesus macaque (Macaca mulatta) model for vaginal Lactobacillus colonization and live microbicide development. J. Med. Primatol. 38, 125–136.
| A Chinese rhesus macaque (Macaca mulatta) model for vaginal Lactobacillus colonization and live microbicide development.Crossref | GoogleScholarGoogle Scholar | 19367737PubMed |
Zhou, Q., Wang, M., Yuan, Y., Wang, X., Fu, R., Wan, H., Xie, M., Liu, M., Guo, X., Zheng, Y., Feng, G., Shi, Q., Zhao, X. Y., Sha, J., and Zhou, Q. (2016). Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell 18, 330–340.
| Complete meiosis from embryonic stem cell-derived germ cells in vitro.Crossref | GoogleScholarGoogle Scholar | 26923202PubMed |
