Reconstitution of Gametogenesis In Vitro: Meiosis Is the Biggest Obstacle

Yuan-Chao Sun; Shun-Feng Cheng; Rui Sun; Yong Zhao; Wei Shen

doi:10.1016/j.jgg.2013.12.008

Volume 41 Issue 3

Mar. 2014

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2014 > 41(3): 87-95

PDF( 400 KB)

Reconstitution of Gametogenesis In Vitro: Meiosis Is the Biggest Obstacle

doi: 10.1016/j.jgg.2013.12.008

a
Key Laboratory of Animal Reproduction and Germplasm Enhancement in Universities of Shandong, Qingdao Agricultural University, Qingdao 266109, China
b
National Laboratory for Physical Sciences at Microscale, School of Life Sciences, University of Science and Technology of China, Hefei 230027, China

More Information

Corresponding author: E-mail address: shenwei427@163.com (Wei Shen)
Received Date: 2013-10-11
Accepted Date: 2013-12-20
Rev Recd Date: 2013-12-08

Available Online: 2014-02-22

Publish Date: 2014-03-20

Abstract

Abstract

Germ-line cells are responsible for transmitting genetic and epigenetic information across generations, and ensuring the creation of new individuals from one generation to the next. Gametogenesis process requires several rigorous steps, including primordial germ cell (PGC) specification, proliferation, migration to the gonadal ridges and differentiation into mature gametes such as sperms and oocytes. But this process is not clearly explored because a small number of PGCs are deeply embedded in the developing embryo. In the attempt to establish an in vitro model for understanding gametogenesis process well, several groups have made considerable progress in differentiating embryonic stem cells (ESCs) and adult stem cells (ASCs) into germ-like cells over the past ten years. These stem cell-derived germ cells appear to be capable of undergoing meiosis and generating both male and female gametes. But most of gametes turn out to be not fully functional due to their abnormal meiosis process compared to endogenous germ cells. Therefore, a robust system of differentiating stem cells into germ cells would enable us to investigate the genetic, epigenetic and environmental factors associated with germ cell development. Here, we review the stem cell-derived germ cell development, and discuss the potential and challenges in the differentiation of functional germ cells from stem cells.
- Stem cells,
- Germ cells,
- Gametogenesis,
- Differentiation,
- Meiosis

FullText(HTML)

References(70)

References

[1]	Anderson, R.A., Fulton, N., Cowan, G. et al. Conserved and divergent patterns of expression of DAZL, VASA and OCT4 in the germ cells of the human fetal ovary and testis BMC Dev. Biol., 7 (2007),p. 136
[2]	Araki, R., Uda, M., Hoki, Y. et al. Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells Nature, 494 (2013),pp. 100-104
[3]	Baltus, A.E., Menke, D.B., Hu, Y.C. et al. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication Nat. Genet., 38 (2006),pp. 1430-1434
[4]	Boheler, K.R., Czyz, J., Tweedie, D. et al. Differentiation of pluripotent embryonic stem cells into cardiomyocytes Circ. Res., 91 (2002),pp. 189-201
[5]	Bucay, N., Yebra, M., Cirulli, V. et al. A Novel Approach for the Derivation of Putative Primordial GermCells and Sertoli Cells from Human Embryonic Stem Cells Stem Cells., 27 (2009),pp. 68-77
[6]	Clark, A.T., Bodnar, M.S., Fox, M. et al. Spontaneous differentiation of germ cells from human embryonic stem cells in vitro Hum Mol Genet., 13 (2004),pp. 727-739
[7]	Danner, S., Kajahn, J., Geismann, C. et al. Derivation of oocyte-like cells from a clonal pancreatic stem cell line Mol. Hum. Reprod., 13 (2007),pp. 11-20
[8]	De Miguel, M.P., Cheng, L., Holland, E.C. et al. Dissection of the c-Kit signaling pathway in mouse primordial germ cells by retroviralmediated gene transfer Proc. Natl. Acad. Sci. USA, 99 (2002),pp. 10458-10463
[9]	Dokshin, G.A., Baltus, A.E., Eppig, J.J. et al. Oocyte differentiation is genetically dissociable from meiosis in mice Nat. Genet., 45 (2013),pp. 877-883
[10]	Dudley, B.M., Runyan, C., Takeuchi, Y. et al. BMP signaling regulates PGC numbers and motility in organ culture Mech. Dev., 124 (2007),pp. 68-77
[11]	Dyce, P.W., Shen, W., Huynh, E. et al. Analysis of oocyte-like cells differentiated from porcine fetal skin-derived stem cells Stem Cells Dev., 20 (2011),pp. 809-819
[12]	Dyce, P.W., Liu, J., Tayade, C. et al. PLoS ONE, 6 (2011),p. e20339
[13]	Dyce, P.W., Wen, L., Li, J. Nat. Cell Biol., 8 (2006),pp. 384-390
[14]	Dyce, P.W., Zhu, H., Craig, J. et al. Stem cells with multilineage potential derived from porcine skin Biochem. Biophys. Res. Commun., 316 (2004),pp. 651-658
[15]	Enders, G.C., May, J.J. Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice Dev. Biol., 163 (1994),pp. 331-340
[16]	Fuchs, E., Segre, J.A. Stem cells: a new lease on life Cell, 100 (2000),pp. 143-155
[17]	Gardner, R.L., Beddington, R.S. Multi-lineage 'stem' cells in the mammalian embryo J. Cell Sci., 10 (1988),pp. 11-27
[18]	Geijsen, N., Horoschak, M., Kim, K. et al. Derivation of embryonic germ cells and male gametes from embryonicstem cells Nature, 427 (2004),pp. 148-154
[19]	Ginsburg, M., Snow, M.H., McLaren, A. Primordial germ cells in the mouse embryo during gastrulation Development, 110 (1990),pp. 521-528
[20]	Gill, M.E., Hu, Y.C., Lin, Y. et al. Licensing of gametogenesis, dependent on RNA binding protein DAZL, as a gateway to sexual differentiation of fetal germ cells Proc. Natl. Acad. Sci. USA, 108 (2011),pp. 7443-7448
[21]	Grove, J.E., Bruscia, E., Krause, D.S. Plasticity of bone marrow-derived stem cells Stem Cells, 22 (2004),pp. 487-500
[22]	Hayashi, K., Ohta, H., Kurimoto, K. et al. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells Cell, 146 (2011),pp. 519-532
[23]	Hayashi, K., Ogushi, S., Kurimoto, K. et al. Science, 338 (2012),pp. 971-975
[24]	Hilscher, B., Hilscher, W., Bülthoff-Ohnolz, B. et al. Kinetics of gametogenesis. I. Comparative histological and autoradiographic studies of oocytes and transitional prospermatogonia during oogenesis and prespermatogenesis Cell Tissue Res., 154 (1974),pp. 443-470
[25]	Hübner, K., Fuhrmann, G., Christenson, L.K. et al. Derivation of oocytes from mouse embryonic stem cells Science, 300 (2003),pp. 1251-1256
[26]	Imamura, M., Aoi, T., Tokumasu, A. et al. Induction of primordial germ cells from mouse induced pluripotent stem cells derived from adult hepatocytes Mol Reprod Dev., 77 (2010),pp. 802-811
[27]	Jiang, Y., Jahagirdar, B.N., Reinhardt, R.L. et al. Pluripotency of mesenchymal stem cells derived from adult marrow Nature, 418 (2002),pp. 41-49
[28]	Kang, L., Wang, J., Zhang, Y. et al. iPS cells can support full-term development of tetraploid blastocyst-complemented embryos Cell Stem Cell, 5 (2009),pp. 135-138
[29]	Kee, K., Angeles, V.T., Flores, M. et al. Nature, 462 (2009),pp. 222-225
[30]	Kerkis, A., Fonseca, S.A., Serafim, R.C. et al. Cloning Stem Cell, 9 (2007),pp. 535-548
[31]	Kocer, A., Reichmann, J., Best, D. et al. Germ cell sex determination in mammals Mol. Hum. Reprod., 15 (2009),pp. 205-213
[32]	Koubova, J., Menke, D.B., Zhou, Q. et al. Retinoic acid regulates sex-specific timing of meiotic initiation in mice Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 2474-2479
[33]	Kruse, C., Birth, M., Rohwedel, J. et al. Pluripotency of adult stem cells derived from human and rat pancreas Appl. Phys. A, 79 (2004),pp. 1617-1624
[34]	Kues, W.A., Petersen, B., Mysegades, W. et al. Isolation of murine and porcine fetal stem cells from somatic tissue Biol. Reprod., 72 (2005),pp. 1020-1028
[35]	Lacham-Kaplan, O., Chy, H., Trounson, A. Testicular cell conditioned medium supports differentiation of embryonic stem cells into ovarian structures containing oocytes Stem Cells, 24 (2006),pp. 266-273
[36]	Lev, S., Blechman, J.M., Givol, D. et al. Steel factor and c-kit protooncogene: genetic lessons in signal transduction Crit. Rev. Oncog., 5 (1994),pp. 141-168
[37]	Lin, Y., Gill, M.E., Koubova, J. et al. Germ cell-intrinsic and -extrinsic factors govern meiotic initiation in mouse embryos Science, 322 (2008),pp. 1685-1687
[38]	Linher, K., Dyce, P., Li, J. PLoS ONE, 4 (2009),p. e8263
[39]	Lue, Y., Erkkila, K., Liu, P.Y. et al. Fate of bone marrow stem cells transplanted into the testis: potential implication for men with testicular failure Am J Pathol., 170 (2007),pp. 899-908
[40]	McLaren, A. Development of the mammalian gonad: the fate of the supporting cell lineage Bioessays, 13 (1991),pp. 151-156
[41]	McLaren, A. Meiosis and differentiation of mouse germ cells Symp. Soc. Exp. Biol., 38 (1984),pp. 7-23
[42]	Monk, M., McLaren, A. X-chromosome activity in foetal germ cells of the mouse J. Embryol. Exp. Morphol., 63 (1981),pp. 75-84
[43]	Nayernia, K., Lee, J.H., Drusenheimer, N. et al. Derivation of male germ cells from bonemarrow stem cells Lab. Invest., 86 (2006),pp. 654-663
[44]	Nayernia, K., Nolte, J., Michelmann, H.W. et al. Dev. Cell, 11 (2006),pp. 125-132
[45]	Novak, I., Lightfoot, D.A., Wang, H. et al. Mouse embryonic stem cells form follicle-like ovarian structures but do not progress through meiosis Stem Cells, 24 (2006),pp. 1931-1936
[46]	Panula, S., Medrano, J.V., Kee, K. et al. Human germ cell differentiation from fetal- and adult-derived induced pluripotent stem cells Hum. Mol. Genet., 20 (2010),pp. 752-762
[47]	Park, B.W., Shen, W., Linher-Melville, K. et al. Stem Cells Dev., 22 (2013),pp. 939-950
[48]	Park, T.S., Galic, Z., Conway, A.E. et al. 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 (2009),pp. 783-795
[49]	Qing, T., Shi, Y., Qin, H. et al. Induction of oocyte-like cells from mouse embryonic stem cells by co-culture with ovarian granulosa cells Differentiation, 75 (2007),pp. 902-911
[50]	Ramiya, V.K., Maraist, M., Arfors, K.E. et al. Nat. Med., 6 (2000),pp. 278-282
[51]	Reijo, R., Lee, T.Y., Salo, P. et al. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene Nat. Genet., 10 (1995),pp. 383-393
[52]	Salvador, L.M., Silva, C.P., Kostetskii, I. et al. The promoter of the oocyte-specific gene, Gdf9, is active in population of cultured mouse embryonic stem cells with an oocyte-like phenotype Methods., 45 (2008),pp. 172-181
[53]	Sharpe, R.
[54]	Shen, W., Park, B.W., Toms, D. et al. Midkine promotes proliferation of primordial germ cell by inhibiting the expression of the deleted in azoospermia-like gene Endocrinology, 153 (2012),pp. 3482-3492
[55]	Takahashi, K., Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell, 126 (2006),pp. 663-676
[56]	Tam, P.P., Snow, M.H. Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos J. Embryol. Exp. Morphol., 64 (1981),pp. 133-147
[57]	Theise, N.D. Gastrointestinal stem cells. III. Emergent themes of liver stem cell biology: niche, quiescence, self-renewal, and plasticity Am. J. Physiol. Gastrointest. Liver Physiol., 290 (2006),pp. G189-G193
[58]	Tilgner, K., Atkinson, S.P., Golebiewska, A. et al. Isolation of primordial germ cells from differentiating human embryonic stem cells Stem Cell., 26 (2008),pp. 3075-3085
[59]	Toyota, Y., Tsunekawa, N., Akasu, R. et al. Proc. Natl. Acad. Sci. USA, 100 (2003),pp. 11457-11462
[60]	Toyota, Y., Tsunekawa, N., Takahashi, Y. et al. Expression and intracellular localization of Vasa-homologue protein during germ cell development Mech. Dev., 93 (2000),pp. 139-149
[61]	Watt, F.M., Hogan, B.L. Out of Eden: stem cells and their niches Science, 287 (2000),pp. 1427-1430
[62]	West, J.A., Park, I.H., Daley, G.Q. et al. In vitro generation of germ cells from murine embryonic stem cells Nat Protoc., 1 (2006),pp. 2026-2036
[63]	Ying, Y., Zhao, G.Q. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse Dev. Biol., 232 (2001),pp. 484-492
[64]	Young, J.C., Dias, V.L., Loveland, K.L. Defining the window of germline genesis in vitro from murine embryonic stem cells Biol. Reprod., 82 (2010),pp. 390-401
[65]	Yokobayashi, S., Liang, C.Y., Kohler, H. et al. PRC1 coordinates timing of sexual differentiation of female primordial germ cells Nature, 495 (2013),pp. 236-240
[66]	Yu, Z., Ji, P., Cao, J. et al. Dazl promotes germ cell differentiation from embryonic stem cells J. Mol. Cell Biol., 1 (2009),pp. 93-103
[67]	Zhao, T., Zhang, Z.N., Rong, Z. et al. Immunogenicity of induced pluripotent stem cells Nature, 474 (2011),pp. 212-215
[68]	Zhao, X.Y., Li, W., Lv, Z. et al. iPS cells produce viable mice through tetraploid complementation Nature, 461 (2009),pp. 86-90
[69]	Zhou, Q., Li, Y., Nie, R. et al. Biol. Reprod., 78 (2008),pp. 537-545
[70]	Zhu, Y., Hu, H.L., Li, P. et al. Asian J. Androl., 14 (2012),pp. 574-579