Skip to main content

The Formation and Migration of Primordial Germ Cells in Mouse and Man

  • Chapter
  • First Online:
Molecular Mechanisms of Cell Differentiation in Gonad Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 58))

Abstract

In most multicellular organisms, including mammals, germ cells are at the origin of new organisms and ensure the continuation of the genetic and epigenetic information across the generations.

In the mammalian germ line, the primordial germ cells (PGCs) are the precursors of the primary oocytes and prospermatogonia of fetal ovaries and testes, respectively. In mammals such as the primates, in which the formation of the primary oocytes is largely asynchronous and occurs during a relatively long period, PGCs after the arrival into the XX gonadal ridges are termed oogonia which then become primary oocytes when entering into meiotic prophase I. In the fetal testes, germ cells derived from the PGCs after gonad colonization are termed prospermatogonia or gonocytes.

One of the most fascinating aspect of the mammalian germline development is that it is probably the first cell lineage to be established in the embryo by epigenetic mechanisms and that these inductive events happen in extraembryonic tissues much earlier that gonad develop inside the embryo proper. Moreover, such events prepare the germ cells for totipotency through genetic and epigenetic regulations of their genome function. How this occurs remained a mystery until short time ago.

In this chapter, I will report and discuss the most recent advances in the cellular and molecular mechanisms underlying the formation in extraembryonic tissues and migration of PGCs toward the gonadal ridges made primarily by studies carried out in the mouse with some perspective in the human. Established concepts about these processes will be only summarized when necessary since they are widely described and discussed in many excellent reviews; most of them are cited in the text below.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aeckerle N, Drummer C, Debowski K et al (2014) Primordial germ cell development in the marmoset monkey as revealed by pluripotency factor expression: suggestion of a novel model of embryonic germ cell translocation. Mol Hum Reprod 21:66–80

    Article  PubMed  PubMed Central  Google Scholar 

  • Almstrup K, Nielsen JE, Mlynarska O et al (2010) Carcinoma in situ testis displays permissive chromatin modifications similar to immature foetal germ cells. Br J Cancer 103:1269–1276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez-Buylla A, Merchant-Larios H (1986) Mouse primordial germ cells use fibronectin as a substrate for migration. Exp Cell Res 165:362–368

    Article  CAS  PubMed  Google Scholar 

  • Anderson R, Fässler R, Georges-Labouesse E et al (1999) Mouse primordial germ cells lacking beta1 integrins enter the germline but fail to migrate normally to the gonads. Development 126:1655–1664

    CAS  PubMed  Google Scholar 

  • Anderson R, Copeland TK, Schöler H et al (2000) The onset of germ cell migration in the mouse embryo. Mech Dev 91:61–68

    Article  CAS  PubMed  Google Scholar 

  • Ara T, Nakamura Y, Egawa T et al (2003) Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci U S A 100:5319–5323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aramaki S, Hayashi K, Kurimoto K et al (2013) A mesodermal factor, T, specifies mouse germ cell fate by directly activating germline determinants. Dev Cell 27:516–529

    Article  CAS  PubMed  Google Scholar 

  • Avilion AA, Nicolis SK, Pevny LH et al (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:126–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartkova J, Moudry P, Hodny Z et al (2011) Heterochromatin marks HP1γ, HP1α and H3K9me3, and DNA damage response activation in human testis development and germ cell tumours. Int J Androl 34:103–113

    Article  Google Scholar 

  • Bendel-Stenzel MR, Gomperts M, Anderson R et al (2000) The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 91:143–152

    Article  CAS  PubMed  Google Scholar 

  • Bendsen E, Byskov AG, Andersen CY et al (2006) Number of germ cells and somatic cells in human foetal ovaries during the first weeks after sex differentiation. Hum Rep 21:30–35

    Article  CAS  Google Scholar 

  • Bortvin A, Goodheart M, Liao M et al (2004) Dppa3/Pgc7/stella is a maternal factor and is not required for germ cell specification in mice. BMC Dev Biol 2004(4):2–6

    Article  Google Scholar 

  • Buehr M, McLaren A, Bartley A et al (1993) Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev Dyn 198:182–189

    Article  CAS  PubMed  Google Scholar 

  • Campolo F, Gori M, Favaro R et al (2013) Essential role of Sox2 for the establishment and maintenance of the germ cell line. Stem Cells 31:1408–1421

    Article  CAS  PubMed  Google Scholar 

  • Chambers I, Silva J, Colby D et al (2007) Nanog safeguards pluripotency and mediates germline development. Nature 450:1230–1234

    Article  CAS  PubMed  Google Scholar 

  • Chawengsaksophak K, Svingen T, Ng ET (2012) Loss of Wnt5a disrupts primordial germ cell migration and male sexual development in mice. Biol Reprod 86:1–12

    Article  PubMed  CAS  Google Scholar 

  • Chen SR, Zheng QS, Zhang Y et al (2013) Disruption of genital ridge development causes aberrant primordial germ cell proliferation but does not affect their directional migration. BMC Biol. doi:10.1186/1741-7007-11-22

    Google Scholar 

  • Chiquoine AD (1954) The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat Rec 118:135–146

    Article  CAS  PubMed  Google Scholar 

  • Chuva de Sousa Lopes SM, van den Driesche S, Carvalho RLC et al (2005) Altered primordial germ cell migration in the absence of transforming growth factor β signaling via ALK5. Dev Biol 5:194–203

    Article  CAS  Google Scholar 

  • Ciccarone F, Klinger FG, Catizone A et al (2012) Poly (ADP-rybosil)ation acts in DNA demethylation of mouse primordial germ cells also with DNA damage independent roles. PlosONE 7:e46927

    Article  CAS  Google Scholar 

  • Covello KL, Kehler J, Yu H et al (2006) HIF-2α regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20:557–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Felici M (2011) Nuclear reprogramming in mouse primordial germ cells: epigenetic contribution. Stem Cells Int. doi:10.4061/2011/425863

    PubMed  PubMed Central  Google Scholar 

  • De Felici M (2013) Origin, migration, and proliferation of human primordial germ cells. In: Coticchio G et al (eds) Oogenesis. Springer, London, pp 19–37. doi:10.1007/978-0-85729-826-3_2

    Chapter  Google Scholar 

  • De Felici M, Dolci S (1989) In vitro adhesion of mouse fetal germ cells to extracellular matrix components. Cell Differ Dev 26:87–96

    Article  PubMed  Google Scholar 

  • De Felici M, Farini D (2012) The control of cell cycle in mouse primordial germ cells: old and new players. Curr Pharm Des 18:233–244

    Article  PubMed  Google Scholar 

  • De Felici M, Pesce M, Giustiniani Q et al (1998) In vitro adhesiveness of mouse primordial germ cells to cellular and extracellular matrix component substrata. Microsc Res Tech 43:258–264

    Article  PubMed  Google Scholar 

  • De Miguel MP, Cheng L, Holland EC et al (2002) Dissection of the c-Kit signaling pathway in mouse primordial germ cells by retroviral-mediated gene transfer. Proc Natl Acad Sci U S A 99:10458–10463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Di Carlo A, De Felici M (2000) A role for E-cadherin in mouse primordial germ cell development. Dev Biol 226:209–219

    Article  PubMed  CAS  Google Scholar 

  • Ding J, Jiang D, Kurczy M et al (2008) Inhibition of HMG CoA reductase reveals an unexpected role for cholesterol during PGC migration in the mouse. BMC Dev Biol. doi:10.1186/1471-213X-8-120

    Google Scholar 

  • Downs KM, Inman KE, Jin DX et al (2009) The Allontoic Core Domain (ACD): new insights into development of the murine allantois and its relation to the primitive streak. Dev Dyn 238:532–553

    Article  PubMed  PubMed Central  Google Scholar 

  • Farini D, La Sala G, Tedesco M et al (2007) Chemoattractant action and molecular signaling pathways of Kit ligand on mouse primordial germ cells. Dev Biol 306:572–583

    Article  CAS  PubMed  Google Scholar 

  • Felix W (1911) Die Entwicklung der Harn- und Geschlechtsorgane. In: Keibel F, Mall FP (eds) Handbuch der Entwicklungageschichte des Menshen, vol 2. Hirzel, Leipzig, pp 732–795

    Google Scholar 

  • Ffrench-Constant F, Hollingsworth A, Heasman J et al (1991) Response to fibronectin of mouse primordial germ cells before, during and after migration. Development 113:1365–1373

    CAS  PubMed  Google Scholar 

  • Freeman B (2003) The active migration of germ cells in the embryos of mice and men is a myth. Reproduction 125:635–643

    Article  CAS  PubMed  Google Scholar 

  • Fujimoto T, Miyayama Y, Fuyuta M (1977) The origin, migration and fine morphology of human primordial germ cells. Anat Rec 188:315–329

    Article  CAS  PubMed  Google Scholar 

  • Fuss A (1911) Uber extraregionare Geschlechtszellen bei einem menschlichen Embryo von 4 Wochen. Anat Am 39:407–409

    Google Scholar 

  • Fuss A (1912) Uber die Geschlechtszellen des Menschen und der Saugetiere. Anat Entw Mech 81:1–23

    Article  Google Scholar 

  • García-Castro MI, Anderson R, Janet Heasman J et al (1997) Interactions between germ cells and extracellular matrix glycoproteins during migration and gonad assembly in the mouse embryo. J Cell Biol 138:471–480

    Article  PubMed  PubMed Central  Google Scholar 

  • Ginsburg M, Snow MH, McLaren A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110:521–528

    CAS  PubMed  Google Scholar 

  • Gkountela S, Li Z, Vincent JJ et al (2013) The ontogeny of cKIT+ human primordial germ cells proves to be a resource for human germ line reprogramming, imprint erasure and in vitro differentiation. Nat Cell Biol 15:113–122

    Article  CAS  PubMed  Google Scholar 

  • Gkountela S, Zhang KX, Shafiq TA et al (2015) DNA demethylation dynamics in the human prenatal germline. Cell 161:1425–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomperts M, Garcia-Castro M, Wylie C et al (1994) Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120:135–141

    CAS  PubMed  Google Scholar 

  • Goto T, Salpekar A, Monk M (2001) Expression of testis specific member of the olfactory receptor gene family in human primordial germ cells. Mol Hum Reprod 7:553–558

    Article  CAS  PubMed  Google Scholar 

  • Gu Y, Runyan C, Shoemaker A et al (2011) Membrane-bound steel factor maintains a high local concentration for mouse primordial germ cell motility, and defines the region of their migration. PLoS One 6(10):e25984. doi:10.1371/journal.pone.0025984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo F, Yan L, Guo H et al (2015) The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 161:1437–1452

    Article  CAS  PubMed  Google Scholar 

  • Hara K, Kanai-Azuma M, Uemura M et al (2009) Evidence for crucial role of hindgut expansion in directing proper migration of primordial germ cells in mouse early embryogenesis. Dev Biol 330:427–439

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Chuva de Sousa Lopes SM, Surani MA (2007) Germ cell specification in mice. Science 316:394–396

    Article  CAS  PubMed  Google Scholar 

  • Hu Y-C, Okumura LM, Page DC (2013) Gata4 is required for formation of the genital ridge in mice. PLoS Genet 9(7):e1003629. doi:10.1371/journal.pgen.1003629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irie N, Tang WWC, Surani MA (2015a) Germ cell specification and pluripotency in mammals: a perspective from early embryogenesis. Reprod Med Biol 13:203–215

    Article  Google Scholar 

  • Irie N, Weinberger L, Tang WWC et al (2015b) SOX17 is a critical specifier of human primordial germ cell fate. Cell 160:253–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kehler J, Tolkunova E, Koschorz B et al (2004) Oct4 is required for primordial germ cell survival. EMBO Rep 5:1078–1083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuwana T, Fujimoto T (1983) Active locomotion of human primordial germ cells in vitro. Anat Rec 205:21–26

    Article  CAS  PubMed  Google Scholar 

  • Laird DJ, Altshuler-Keylin S, Kissner MD et al (2011) ROR2 enhances polarity and directional migration of primordial germ cells. PLoS Genet 7:e1002428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lange UC, Saitou M, Western PS (2003) The fragilis interferon-inducible gene family of transmembrane proteins is associated with germ cell specification in mice. BMC Dev Biol 3:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lange UC, Adams DJ, Lee C et al (2008) Normal germ line establishment in mice carrying a deletion of the Ifitm/Fragilis gene family cluster. Mol Cell Biol 28:4688–4696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawson KA, Hage WJ (1994) Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found Symp 182:68–84

    CAS  PubMed  Google Scholar 

  • Lawson KA, Dunn NR, Roelen BA et al (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahakali Zama A, Hudson FP, Bedell MA (2005) Analysis of hypomorphic KitlSl mutants suggests different requirements for KITL in proliferation and migration of mouse primordial germ cells. Biol Reprod 73:639–647

    Article  PubMed  CAS  Google Scholar 

  • Makabe S, Nottola SA, Motta PM (1989) Life history of the human female germ cell: ultrastructural aspects. In: Van Blerkom J, Motta PM (eds) Ultrastructure of human gametogenesis and early embryogenesis. Kluwer Academic, Boston, pp 33–60

    Chapter  Google Scholar 

  • Mamsen LS, Brochner CB, Byskov AG et al (2012) The migration and loss of human primordial germ stem cells from the hind gut epithelium towards the gonadal ridge. Int J Dev Biol 56:771–778

    Article  CAS  PubMed  Google Scholar 

  • Mattiske D, Kume T, Hogan BL (2006) The mouse forkhead gene Foxc1 is required for primordial germ cell migration and antral follicle development. Dev Biol 290:447–458

    Article  CAS  PubMed  Google Scholar 

  • McCoshen JA, McCallion DJ (1975) A study of the primordial germ cells during their migratory phase in Steel mutant mice. Experientia 31:589–590

    Article  CAS  PubMed  Google Scholar 

  • McKay DG, Hertig AT, Adams EC et al (1953) Histochemical observations on the germ cells of human embryos. Anat Rec 17:201–219

    Article  Google Scholar 

  • Mikedis MM, Downs KM (2012) STELLA-positive subregions of the primitive streak cooperate to build the posterior region of the murine conceptus. Dev Biol 363:201–218

    Article  CAS  PubMed  Google Scholar 

  • Mikedis MM, Downs KM (2013) Widespread but tissue-specific patterns of interferon-induced transmembrane protein 3 (IFITM3, FRAGILIS, MIL-1) in the mouse gastrula. Gene Expr Patterns 13:225–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mintz B, Russell ES (1957) Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool 134:207–237

    Article  CAS  PubMed  Google Scholar 

  • Møllgard HK, Jespersen A, Lutterodt MC et al (2010) Human primordial germ cells migrate along nerve fibers and Schwann cells from the dorsal hind gut mesentery to the gonadal ridge. Mol Hum Reprod 16:621–631

    Article  PubMed  CAS  Google Scholar 

  • Molyneaux K, Wylie C (2004) Primordial germ cell migration. Int J Dev Biol 48:537–554

    Article  CAS  PubMed  Google Scholar 

  • Molyneaux KA, Stallock J, Schaible K et al (2001) Time-lapse analysis of living mouse germ cell migration. Dev Biol 240:488–498

    Article  CAS  PubMed  Google Scholar 

  • Molyneaux KA, Zinszner H, Kunwar PS et al (2003) The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 18:4279–4286

    Article  CAS  Google Scholar 

  • Motta PM, Nottola SA, Makabe S et al (2000) Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod 15:129–147

    Article  PubMed  Google Scholar 

  • Ohinata Y, Payer B, O’Carroll D et al (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207–213

    Article  CAS  PubMed  Google Scholar 

  • Ohinata Y, Ohta H, Shigeta M et al (2009) A signaling principle for the specification of the germ cell lineage in mice. Cell 137:571–584

    Article  CAS  PubMed  Google Scholar 

  • Ohno R, Megumi Nakayama M, Naruse C et al (2013) A replication-dependent passive mechanism modulates DNA demethylation in mouse primordial germ cells. Development 140:2892–2903

    Article  CAS  PubMed  Google Scholar 

  • Okamura D, Kimura T, Nakano T et al (2003) Cadherin-mediated cell interaction regulates germ cell determination in mice. Development 130:6423–6430

    Article  CAS  PubMed  Google Scholar 

  • Okamura D, Tokitake Y, Niwa H et al (2008) Requirement of Oct3/4 function for germ cell specification. Dev Biol 317:576–584

    Article  CAS  PubMed  Google Scholar 

  • Pereda J, Zorn T, Soto-Suazo M (2006) Migration of human and mouse primordial germ cells and colonization of the developing ovary: an ultrastructural and cytochemical study. Microsc Res Tech 69:386–395

    Article  PubMed  Google Scholar 

  • Person AD, Beiraghi S, Sieben CM et al (2010) WNT5A mutations in patients with autosomal dominant Robinow syndrome. Dev Dyn 239:327–337

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pesce M, Farrace MG, Piacentini M et al (1993) Stem cell factor and leukemia inhibitory factor promote primordial germ cell survival by suppressing programmed cell death (apoptosis). Development 118:1089–1094

    CAS  PubMed  Google Scholar 

  • Pesce M, Di Carlo A, De Felici M (1997) The c-kit receptor is involved in the adhesion of mouse primordial germ cells to somatic cells in culture. Mech Dev 68:37–44

    Article  CAS  PubMed  Google Scholar 

  • Pesce M, Klinger FG, De Felici M (2002) Derivation in culture of primordial germ cells from cells of the mouse epiblast: phenotypic induction and growth control by Bmp4 signalling. Mech Dev 12:15–24

    Article  Google Scholar 

  • Runyan C, Schaible K, Molyneaux K et al (2006) Steel factor controls midline cell death of primordial germ cells and is essential for their normal proliferation and migration. Development 133:4861–4869

    Article  CAS  PubMed  Google Scholar 

  • Saitou M, Yamaji M (2012) Primordial germ cells in mice. Cold Spring Harb Perspect Biol (4):a008375

    Google Scholar 

  • Saitou M, Barton SC, Surani MA (2002) A molecular programme for the specification of germ cell fate in mice. Nature 418:293–300

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Yokobayashi S, Nakamura T et al (2015) Robust in vitro induction of human germ cell fate from pluripotent stem cells. Cell Stem Cell. doi:10.1016/j.stem.2015.06.014

    PubMed  Google Scholar 

  • Scaldaferri ML, Klinger FG, Farini D et al (2015) Hematopoietic activity in putative mouse primordial germ cell populations. Mech Dev 136:53–63

    Article  CAS  PubMed  Google Scholar 

  • Soto-Suazo M, Abrahamsohn PA, Pereda J et al (1999) Distribution and space-time relationship of proteoglycans in the extracellular matrix of the migratory pathway of primordial germ cells in mouse embryos. Tissue Cell 31:291–300

    Article  CAS  PubMed  Google Scholar 

  • Soto-Suazo M, Abrahamsohn PA, Pereda J et al (2002) Modulation of hyaluronan in the migratory pathway of mouse primordial germ cells. Histochem Cell Biol 117:265–723

    Article  CAS  PubMed  Google Scholar 

  • Soto-Suazo M, San Martin S, Zorn TM (2004) Collagen and tenascin-C expression along the migration pathway of mouse primordial germ cells. Histochem Cell Biol 121(2):149–153

    Article  CAS  PubMed  Google Scholar 

  • Stallock J, Molyneaux K, Schaible K et al (2003) The pro-apoptotic gene Bax is required for the death of ectopic primordial germ cells during their migration in the mouse embryo. Development 30:6589–6597

    Article  CAS  Google Scholar 

  • Sugawa F, Araúzo-Bravo MJ, Yoon J et al (2015) Human primordial germ cell commitment in vitro associates with a unique PRDM14 expression profile. EMBO J 34:1009–1024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tam PPL, Loebel DAF (2009) Specifying mouse embryonic germ cells. Cell 137:398–400

    Article  CAS  PubMed  Google Scholar 

  • Tanaka SS, Yamaguchi YL, Tsoi B et al (2005) IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. Dev Cell 9:745–756

    Article  CAS  PubMed  Google Scholar 

  • Tanaka SS, Yamaguchi YL, Steiner KA et al (2010) Loss of Lhx1 activity impacts on the localization of primordial germ cells in the mouse. Dev Dyn 239:2851–2859

    Article  CAS  PubMed  Google Scholar 

  • Tanaka SS, Nakane A, Yamaguchi YL et al (2013) Dullard/Ctdnep1 modulates WNT signalling activity for the formation of primordial germ cells in the mouse embryo. PLoS One 8:e77428. doi:10.1371/journal.pone.0057428

    Article  Google Scholar 

  • Tang WW, Dietmann S, Irie N et al (2015) A unique gene regulatory network resets the human germline epigenome for development. Cell 161:1453–1467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber S, Eckert D, Nettersheim D et al (2010) Critical function of AP-2 gamma/TCFAP2C in mouse embryonic germ cell maintenance. Biol Reprod 82:214–223

    Article  CAS  PubMed  Google Scholar 

  • Wermann H, Stoop H, Gillis AJ et al (2010) Global DNA methylation in fetal human germ cells and germ cell tumours: association with differentiation and cisplatin resistance. J Pathol 221:433–442

    CAS  PubMed  Google Scholar 

  • West JA, Viswanathan SR, Yabuuchi A et al (2009) A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460:909–913

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi S, Kurimoto K, Yabuta Y et al (2009) Conditional knockdown of Nanog induces apoptotic cell death in mouse migrating primordial germ cells. Development 136:4011–4020

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi YL, Tanaka SS, Kumagai M et al (2015) Sall4 is essential for mouse primordial germ cell specification by suppressing somatic cell program genes. Stem Cells 33:289–300

    Article  CAS  PubMed  Google Scholar 

  • Yamaji M, Seki Y, Kurimoto K (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40:1016–1022

    Article  CAS  PubMed  Google Scholar 

  • Ying Y, Zhao GQ (2001) Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev Biol 232:484–492

    Article  CAS  PubMed  Google Scholar 

  • Ying Y, Liu XM, Marble A et al (2000) Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol Endocrinol 14:1053–1063

    Article  CAS  PubMed  Google Scholar 

  • Ying Y, Qi X, Zhao GQ (2001) Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci U S A 98:7858–7862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Massimo De Felici .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

De Felici, M. (2016). The Formation and Migration of Primordial Germ Cells in Mouse and Man. In: Piprek, R. (eds) Molecular Mechanisms of Cell Differentiation in Gonad Development. Results and Problems in Cell Differentiation, vol 58. Springer, Cham. https://doi.org/10.1007/978-3-319-31973-5_2

Download citation

Publish with us

Policies and ethics