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Semin Reprod Med 2013; 31(01): 014-023
DOI: 10.1055/s-0032-1331793
DOI: 10.1055/s-0032-1331793
Germ Cell Differentiation from Pluripotent Cells
Further Information
Publication History
Publication Date:
17 January 2013 (online)
Abstract
Infertility is a medical condition with an increasing impact in Western societies with causes linked to toxins, genetics, and aging (primarily delay of motherhood). Within the different pathologies that can lead to infertility, poor quality or reduced quantity of gametes plays an important role. Gamete donation and therefore demand on donated sperm and eggs in fertility clinics is increasing. It is hoped that a better understanding of the conditions related to poor gamete quality may allow scientists to design rational treatments. However, to date, relatively little is known about human germ cell development in large part due to the inaccessibility of human development to molecular genetic analysis. It is hoped that pluripotent human embryonic stem cells and induced pluripotent stem cells may provide an accessible in vitro model to study germline development; these cells are able to differentiate to cells of all three primary embryonic germ layers, as well as to germ cells in vitro. We review the state of the art in germline differentiation from pluripotent stem cells.
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References
- 1 Ziebe S, Loft A, Petersen JH , et al. Embryo quality and developmental potential is compromised by age. Acta Obstet Gynecol Scand 2001; 80 (2) 169-174
- 2 Adamson GD, de Mouzon J, Lancaster P, Nygren KG, Sullivan E, Zegers-Hochschild F. International Committee for Monitoring Assisted Reproductive Technology. World collaborative report on in vitro fertilization, 2000. Fertil Steril 2006; 85 (6) 1586-1622
- 3 Ginsburg M, Snow MH, McLaren A. Primordial germ cells in the mouse embryo during gastrulation. Development 1990; 110 (2) 521-528
- 4 Hayashi K, de Sousa Lopes SM, Surani MA. Germ cell specification in mice. Science 2007; 316 (5823) 394-396
- 5 Lawson KA, Hage WJ. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found Symp 1994; 182: 68-84 ; discussion 84–91
- 6 Saitou M, Barton SC, Surani MA. A molecular programme for the specification of germ cell fate in mice. Nature 2002; 418 (6895) 293-300
- 7 Marques-Mari AI, Lacham-Kaplan O, Medrano JV, Pellicer A, Simón C. Differentiation of germ cells and gametes from stem cells. Hum Reprod Update 2009; 15 (3) 379-390
- 8 Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292 (5819) 154-156
- 9 Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 1981; 78 (12) 7634-7638
- 10 Thomson JA, Itskovitz-Eldor J, Shapiro SS , et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282 (5391) 1145-1147
- 11 Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126 (4) 663-676
- 12 Fujiwara T, Dunn NR, Hogan BL. Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse. Proc Natl Acad Sci U S A 2001; 98 (24) 13739-13744
- 13 Ying Y, Liu XM, Marble A, Lawson KA, Zhao GQ. Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol Endocrinol 2000; 14 (7) 1053-1063
- 14 Ying Y, Qi X, Zhao GQ. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci U S A 2001; 98 (14) 7858-7862
- 15 Vincent SD, Dunn NR, Sciammas R , et al. The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development 2005; 132 (6) 1315-1325
- 16 Ohinata Y, Payer B, O'Carroll D , et al. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 2005; 436 (7048) 207-213
- 17 Wylie CC, Stott D, Donovan PJ. Primordial germ cell migration. Dev Biol (N Y 1985) 1986; 2: 433-448
- 18 Goto T, Adjaye J, Rodeck CH, Monk M. Identification of genes expressed in human primordial germ cells at the time of entry of the female germ line into meiosis. Mol Hum Reprod 1999; 5 (9) 851-860
- 19 Fujimoto T, Miyayama Y, Fuyuta M. The origin, migration and fine morphology of human primordial germ cells. Anat Rec 1977; 188 (3) 315-330
- 20 Matsui Y, Zsebo KM, Hogan BL. Embryonic expression of a haematopoietic growth factor encoded by the Sl locus and the ligand for c-kit. Nature 1990; 347 (6294) 667-669
- 21 Donovan PJ, Stott D, Cairns LA, Heasman J, Wylie CC. Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 1986; 44 (6) 831-838
- 22 Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP. The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci U S A 2000; 97 (17) 9585-9590
- 23 Noce T, Okamoto-Ito S, Tsunekawa N. Vasa homolog genes in mammalian germ cell development. Cell Struct Funct 2001; 26 (3) 131-136
- 24 Tanaka SS, Toyooka Y, Akasu R , et al. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 2000; 14 (7) 841-853
- 25 Byskov AG. Differentiation of mammalian embryonic gonad. Physiol Rev 1986; 66 (1) 71-117
- 26 Sinclair AH, Berta P, Palmer MS , et al. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990; 346 (6281) 240-244
- 27 McLaren A. Somatic and germ-cell sex in mammals. Philos Trans R Soc Lond B Biol Sci 1988; 322 (1208) 3-9
- 28 Koopman P, Münsterberg A, Capel B, Vivian N, Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 1990; 348 (6300) 450-452
- 29 Burgoyne PS. Role of mammalian Y chromosome in sex determination. Philos Trans R Soc Lond B Biol Sci 1988; 322 (1208) 63-72
- 30 Upadhyay S, Zamboni L. Preliminary observations on the role of the mesonephros in the development of the adrenal cortex. Anat Rec 1982; 202 (1) 105-111
- 31 McLaren A. Sex reversal in the mouse. Differentiation 1983; 23 (Suppl): S93-S98
- 32 McLaren A, Southee D. Entry of mouse embryonic germ cells into meiosis. Dev Biol 1997; 187 (1) 107-113
- 33 McLaren A. Meiosis and differentiation of mouse germ cells. Symp Soc Exp Biol 1984; 38: 7-23
- 34 Bowles J, Knight D, Smith C , et al. Retinoid signaling determines germ cell fate in mice. Science 2006; 312 (5773) 596-600
- 35 Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A 2006; 103 (8) 2474-2479
- 36 Schöler HR, Ruppert S, Suzuki N, Chowdhury K, Gruss P. New type of POU domain in germ line-specific protein Oct-4. Nature 1990; 344 (6265) 435-439
- 37 Pesce M, Wang X, Wolgemuth DJ, Schöler H. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech Dev 1998; 71 (1-2) 89-98
- 38 Heyting C, Dettmers RJ, Dietrich AJ, Redeker EJ, Vink AC. Two major components of synaptonemal complexes are specific for meiotic prophase nuclei. Chromosoma 1988; 96 (4) 325-332
- 39 Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 1994; 107 (Pt 10) 2749-2760
- 40 Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, Morita T. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1998; 1 (5) 707-718
- 41 Pittman DL, Cobb J, Schimenti KJ , et al. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1998; 1 (5) 697-705
- 42 Reynolds N, Collier B, Bingham V, Gray NK, Cooke HJ. Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl. RNA 2007; 13 (7) 974-981
- 43 Bellvé AR, Millette CF, Bhatnagar YM, O'Brien DA. Dissociation of the mouse testis and characterization of isolated spermatogenic cells. J Histochem Cytochem 1977; 25 (7) 480-494
- 44 McLaren A. Germ cells and germ cell sex. Philos Trans R Soc Lond B Biol Sci 1995; 350 (1333) 229-233
- 45 Bestor TH. The DNA methyltransferases of mammals. Hum Mol Genet 2000; 9 (16) 2395-2402
- 46 Bestor T, Laudano A, Mattaliano R, Ingram V. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J Mol Biol 1988; 203 (4) 971-983
- 47 Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998; 19 (3) 219-220
- 48 Lyle R. Gametic imprinting in development and disease. J Endocrinol 1997; 155 (1) 1-12
- 49 Miozzo M, Simoni G. The role of imprinted genes in fetal growth. Biol Neonate 2002; 81 (4) 217-228
- 50 Surani MA. Reprogramming of genome function through epigenetic inheritance. Nature 2001; 414 (6859) 122-128
- 51 Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293 (5532) 1089-1093
- 52 Rideout III WM, Eggan K, Jaenisch R. Nuclear cloning and epigenetic reprogramming of the genome. Science 2001; 293 (5532) 1093-1098
- 53 Maatouk DM, Resnick JL. Continuing primordial germ cell differentiation in the mouse embryo is a cell-intrinsic program sensitive to DNA methylation. Dev Biol 2003; 258 (1) 201-208
- 54 Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 2000; 9 (19) 2885-2894
- 55 Ueda T, Abe K, Miura A , et al. The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 2000; 5 (8) 649-659
- 56 Everman DB, Cassidy SB. Genetics of childhood disorders: XII. Genomic imprinting: breaking the rules. J Am Acad Child Adolesc Psychiatry 2000; 39 (3) 386-389
- 57 Tycko B, Morison IM. Physiological functions of imprinted genes. J Cell Physiol 2002; 192 (3) 245-258
- 58 Nayernia K, Nolte J, Michelmann HW , et al. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell 2006; 11 (1) 125-132
- 59 Hübner K, Fuhrmann G, Christenson LK , et al. Derivation of oocytes from mouse embryonic stem cells. Science 2003; 300 (5623) 1251-1256
- 60 Toyooka Y, Tsunekawa N, Akasu R, Noce T. Embryonic stem cells can form germ cells in vitro. Proc Natl Acad Sci U S A 2003; 100 (20) 11457-11462
- 61 Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 2004; 427 (6970) 148-154
- 62 Kerkis A, Fonseca SA, Serafim RC , et al. In vitro differentiation of male mouse embryonic stem cells into both presumptive sperm cells and oocytes. Cloning Stem Cells 2007; 9 (4) 535-548
- 63 Lacham-Kaplan O, Chy H, Trounson A. Testicular cell conditioned medium supports differentiation of embryonic stem cells into ovarian structures containing oocytes. Stem Cells 2006; 24 (2) 266-273
- 64 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 2007; 75 (10) 902-911
- 65 Novak I, Lightfoot DA, Wang H, Eriksson A, Mahdy E, Höög C. Mouse embryonic stem cells form follicle-like ovarian structures but do not progress through meiosis. Stem Cells 2006; 24 (8) 1931-1936
- 66 Clark AT, Bodnar MS, Fox MS , et al. Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet 2004; 13 (7) 727-739
- 67 Tilgner K, Atkinson SP, Golebiewska A, Stojkovic M, Lako M, Armstrong L. Isolation of primordial germ cells from differentiating human embryonic stem cells. Stem Cells 2008; 26 (12) 3075-3085
- 68 Park TS, Galic Z, Conway AE , 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 2009; 27 (4) 783-795
- 69 Bucay N, Yebra M, Cirulli V , et al. A novel approach for the derivation of putative primordial germ cells and Sertoli cells from human embryonic stem cells. Stem Cells 2009; 27 (1) 68-77
- 70 Kee K, Gonsalves JM, Clark AT, Pera RA. Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev 2006; 15 (6) 831-837
- 71 Kee K, Angeles VT, Flores M, Nguyen HN, Reijo Pera RA. Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 2009; 462 (7270) 222-225
- 72 Panula S, Medrano JV, Kee K , et al. Human germ cell differentiation from fetal- and adult-derived induced pluripotent stem cells. Hum Mol Genet 2011; 20 (4) 752-762
- 73 Medrano JV, Ramathal C, Nguyen HN, Simon C, Reijo Pera RA. Divergent RNA-binding proteins, DAZL and VASA, induce meiotic progression in human germ cells derived in vitro. Stem Cells 2012; 30 (3) 441-451
- 74 Eguizabal C, Montserrat N, Vassena R , et al. Complete meiosis from human induced pluripotent stem cells. Stem Cells 2011; 29 (8) 1186-1195
- 75 Handel MA, Schimenti JC. Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 2010; 11 (2) 124-136
- 76 Burgoyne PS, Mahadevaiah SK, Turner JM. The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 2009; 10 (3) 207-216
- 77 Sun SC, Kim NH. Spindle assembly checkpoint and its regulators in meiosis. Hum Reprod Update 2012; 18 (1) 60-72
- 78 Kassir Y, Adir N, Boger-Nadjar E , et al. Transcriptional regulation of meiosis in budding yeast. Int Rev Cytol 2003; 224: 111-171
- 79 Gill ME, Hu YC, Lin Y, Page DC. Licensing of gametogenesis, dependent on RNA binding protein DAZL, as a gateway to sexual differentiation of fetal germ cells. Proc Natl Acad Sci U S A 2011; 108 (18) 7443-7448
- 80 Papaioannou MD, Nef S. microRNAs in the testis: building up male fertility. J Androl 2010; 31 (1) 26-33
- 81 Buchold GM, Coarfa C, Kim J, Milosavljevic A, Gunaratne PH, Matzuk MM. Analysis of microRNA expression in the prepubertal testis. PLoS ONE 2010; 5 (12) e15317
- 82 Han J, Pedersen JS, Kwon SC , et al. Posttranscriptional crossregulation between Drosha and DGCR8. Cell 2009; 136 (1) 75-84
- 83 Hayashi K, Chuva de Sousa Lopes SM, Kaneda M , et al. MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS ONE 2008; 3 (3) e1738
- 84 West JA, Viswanathan SR, Yabuuchi A , et al. A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 2009; 460 (7257) 909-913
- 85 Zhong X, Li N, Liang S, Huang Q, Coukos G, Zhang L. Identification of microRNAs regulating reprogramming factor LIN28 in embryonic stem cells and cancer cells. J Biol Chem 2010; 285 (53) 41961-41971
- 86 Western PS, van den Bergen JA, Miles DC, Sinclair AH. Male fetal germ cell differentiation involves complex repression of the regulatory network controlling pluripotency. FASEB J 2010; 24 (8) 3026-3035
- 87 Yan N, Lu Y, Sun H , et al. A microarray for microRNA profiling in mouse testis tissues. Reproduction 2007; 134 (1) 73-79
- 88 Marcon E, Babak T, Chua G, Hughes T, Moens PB. miRNA and piRNA localization in the male mammalian meiotic nucleus. Chromosome Res 2008; 16 (2) 243-260
- 89 Bouhallier F, Allioli N, Lavial F , et al. Role of miR-34c microRNA in the late steps of spermatogenesis. RNA 2010; 16 (4) 720-731
- 90 Luo L, Ye L, Liu G , et al. Microarray-based approach identifies differentially expressed microRNAs in porcine sexually immature and mature testes. PLoS ONE 2010; 5 (8) e11744
- 91 Juliano C, Wessel G. Developmental biology. Versatile germline genes. Science 2010; 329 (5992) 640-641
- 92 Xu EY, Moore FL, Pera RA. A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in metazoans. Proc Natl Acad Sci U S A 2001; 98 (13) 7414-7419
- 93 Ruggiu M, Speed R, Taggart M , et al. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 1997; 389 (6646) 73-77
- 94 Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP. The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci U S A 2000; 97 (17) 9585-9590
- 95 Gruidl ME, Smith PA, Kuznicki KA , et al. Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans . Proc Natl Acad Sci U S A 1996; 93 (24) 13837-13842
- 96 Komiya T, Itoh K, Ikenishi K, Furusawa M. Isolation and characterization of a novel gene of the DEAD box protein family which is specifically expressed in germ cells of Xenopus laevis. . Dev Biol 1994; 162 (2) 354-363
- 97 Lasko PF, Ashburner M. The product of the Drosophila gene Vasa is very similar to eukaryotic initiation factor-4A. Nature 1988; 335 (6191) 611-617
- 98 Tanaka SS, Toyooka Y, Akasu R , et al. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 2000; 14 (7) 841-853
- 99 Mohr S, Stryker JM, Lambowitz AM. A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 2002; 109 (6) 769-779
- 100 Reynolds N, Collier B, Maratou K , et al. Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells. Hum Mol Genet 2005; 14 (24) 3899-3909
- 101 Becalska AN, Gavis ER. Lighting up mRNA localization in Drosophila oogenesis. Development 2009; 136 (15) 2493-2503
- 102 Saga Y. Sexual development of mouse germ cells: Nanos2 promotes the male germ cell fate by suppressing the female pathway. Dev Growth Differ 2008; 50 (Suppl. 01) S141-S147
- 103 Liu N, Han H, Lasko P. Vasa promotes Drosophila germline stem cell differentiation by activating mei-P26 translation by directly interacting with a (U)-rich motif in its 3′ UTR. Genes Dev 2009; 23 (23) 2742-2752
- 104 Peters L, Meister G. Argonaute proteins: mediators of RNA silencing. Mol Cell 2007; 26 (5) 611-623
- 105 Kuramochi-Miyagawa S, Watanabe T, Gotoh K , et al. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev 2010; 24 (9) 887-892