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Avian Primordial Germ Cells

  • Takahiro TagamiEmail author
  • Daichi Miyahara
  • Yoshiaki Nakamura
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1001)

Abstract

Germ cells transmit genetic information to the next generation through gametogenesis. Primordial germ cells (PGCs) are the first germ-cell population established during development, and are the common origins of both oocytes and spermatogonia. Unlike in other species, PGCs in birds undergo blood circulation to migrate toward the genital ridge, and are one of the major biological properties of avian PGCs. Germ cells enter meiosis and arrest at prophase I during embryogenesis in females, whereas in males they enter mitotic arrest during embryogenesis and enter meiosis only after birth. In chicken, gonadal sex differentiation occurs as early as embryonic day 6, but meiotic initiation of female germ cells starts from a relatively late stage (embryonic day 15.5). Retinoic acid controls meiotic entry in developing chicken gonads through the expressions of retinaldehyde dehydrogenase 2, a major retinoic acid synthesizing enzyme, and cytochrome P450 family 26, subfamily B member 1, a major retinoic acid-degrading enzyme. The other major biological property of avian PGCs is that they can be propagated in vitro for the long term, and this technique is useful for investigating proliferation mechanisms. The main factor involved in chicken PGC proliferation is fibroblast growth factor 2, which activates the signaling of MEK/ERK and thus promotes the cell cycle and anti-apoptosis. Furthermore, the activation of PI3K/Akt signaling is indispensable for the proliferation and survival of chicken PGCs.

Keywords

Primordial germ cells Germ cell formation Germ cell markers Germ cell migration Germ cell differentiation Gametogenesis Germ cell culture Sexual differentiation Germline chimeras Chicken Quail 

References

  1. Abinawanto, Zhang C, Saito N, et al. Identification of sperm-bearing female-specific chromosome in the sex-reversed chicken. J Exp Zool. 1998;280:65–72.PubMedCrossRefGoogle Scholar
  2. Aoyama H, Asamoto K, Nojyo Y, et al. Monoclonal antibodies specific to quail embryo tissues: their epitopes in the developing quail embryo and their application to identification of quail cells in quail–chick chimeras. J Histochem Cytochem. 1992;40:1769–77.PubMedCrossRefGoogle Scholar
  3. Ara T, Nakamura Y, Egawa T, et al. 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. 2003;100:5319–23.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aramaki S, Sato F, Kato T, et al. Molecular cloning and expression of dead end homologue in chicken primordial germ cells. Cell Tissue Res. 2007;330:45–52.PubMedCrossRefGoogle Scholar
  5. Aramaki S, Kubota K, Soh T, et al. Chicken dead end homologue protein is a nucleoprotein of germ cells including primordial germ cells. J Reprod Dev. 2009;55:214–8.PubMedCrossRefGoogle Scholar
  6. Atsumi Y, Tagami T, Kagami H, et al. Restriction of germline proliferation by soft X-ray irradiation of chicken embryos and its application to chimera production. J Poult Sci. 2008;45:292–7.CrossRefGoogle Scholar
  7. Atsumi Y, Yazawa S, Usui F, et al. Depletion of primordial germ cells (PGCs) by X-irradiation to extraembryonic region of chicken embryos and expression of xenotransplanted quail PGCs. J Poult Sci. 2009;46:136–43.CrossRefGoogle Scholar
  8. Bowles J, Knight D, Smith C, et al. Retinoid signaling determines germ cell fate in mice. Science. 2006;312:596–600.PubMedCrossRefGoogle Scholar
  9. Castrillon DH, Quade BJ, Wang TY, et al. The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci U S A. 2000;97:9585–90.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chambers I, Silva J, Colby D, et al. Nanog safeguards pluripotency and mediates germline development. Nature. 2007;450:1230–4.PubMedCrossRefGoogle Scholar
  11. Chang IK, Tajima A, Chikamune T, et al. Proliferation of chick primordial germ cells cultured on stroma cells from the germinal ridge. Cell Biol Int. 1995;19:143–9.PubMedCrossRefGoogle Scholar
  12. Chang IK, Jeong DK, Hong YH, et al. Production of germline chimeric chickens by transfer of cultured primordial germ cells. Cell Biol Int. 1997;21:485–9.CrossRefGoogle Scholar
  13. Choi JW, Kim S, Kim TM, et al. Basic fibroblast growth factor activates MEK/ERK cell signaling pathway and stimulates the proliferation of chicken primordial germ cells. PLoS One. 2010;5(9):e12968.PubMedPubMedCentralCrossRefGoogle Scholar
  14. De Melo Bernardo A, Sprenkels K, Rodrigues G, et al. Chicken primordial germ cells use the anterior vitelline veins to enter the embryonic circulation. Biol Open. 2012;1:1146–52.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Didier E, Didier P, Fargeix N, et al. Expression and distribution of carbohydrate sequences in chick germ cells: a comparative study with lectins and the NC-1/HNK-1 monoclonal antibody. Int J Dev Biol. 1990;34:421–31.PubMedGoogle Scholar
  16. Doitsidou M, Reichman-Fried M, Stebler J, et al. Guidance of primordial germ cell migration by the chemokine SDF-1. Cell. 2002;111:647–59.PubMedCrossRefGoogle Scholar
  17. Donovan PJ. Growth factor regulation of mouse primordial germ cell development. Curr Top Dev Biol. 1994;29:189–225.PubMedCrossRefGoogle Scholar
  18. Eberhart CG, Maines JZ, Wasserman SA. Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature. 1996;381:783–5.PubMedCrossRefGoogle Scholar
  19. Eddy EM. Germ plasm and the differentiation of the germ cell line. Int Rev Cytol. 1975;43:229–80.PubMedCrossRefGoogle Scholar
  20. Ephrussi A, Lehmann R. Induction of germ cell formation by oskar. Nature. 1992;358:387–92.PubMedCrossRefGoogle Scholar
  21. Eyal-Giladi H, Ginsburg M, Farbarov A. Avian primordial germ cells are of epiblastic origin. J Embryol Exp Morphol. 1981;65:139–47.PubMedGoogle Scholar
  22. Eyal-Giladi H, Kochav S. From cleavage to primitive streak formation: a complementary normal table and a new look at the first stage of the development of the chicken I. General morphology. Dev Biol. 1976;49:321–37.PubMedCrossRefGoogle Scholar
  23. Fujiwara Y, Komiya T, Kawabata H, et al. Isolation of a DEAD-Family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci U S A. 1994;91:12258–62.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Ghabrial A, Schupbach T. Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat Cell Biol. 1999;1:354–7.PubMedCrossRefGoogle Scholar
  25. Ginsburg M, Eyal-Giladi H. Primordial germ cells of the young chick blastoderm originate from the central zone of the area pellucida irrespective of the embryo-forming process. Development. 1987;101:209–19.PubMedGoogle Scholar
  26. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol. 1951;88:49–92.PubMedCrossRefGoogle Scholar
  27. Hayashi K, Ogushi S, Kurimoto K, et al. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science. 2012;338:971–5.PubMedCrossRefGoogle Scholar
  28. Hayashi K, Ohta H, Kurimoto K, et al. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011;146:519–32.PubMedCrossRefGoogle Scholar
  29. Hen G, Friedman-Einat M, Sela-Donenfeld D. Primordial germ cells in the dorsal mesentery of the chicken embryo demonstrate left–right asymmetry and polarized distribution of the EMA1 epitope. J Anat. 2014;224:556–63.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Houston DW, King ML. A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development. 2000;127:447–56.PubMedGoogle Scholar
  31. Huettner AF. The origin of the germ cells in Drosophila melanogaster. J Morphol. 1923;2:385–422.CrossRefGoogle Scholar
  32. Hughes GC. The population of germ cells in the developing female chick. J Embryol Exp Morphol. 1963;11:513–36.PubMedGoogle Scholar
  33. Illmensee K, Mahowald AP. Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci U S A. 1974;71:1016–20.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Illmensee K, Mahowald AP. The autonomous function of germ plasm in a somatic region of the Drosophila egg. Exp Cell Res. 1976;97:127–40.PubMedCrossRefGoogle Scholar
  35. Illmensee K, Mahowald AP, Loomis MR. The ontogeny of germ plasm during oogenesis in Drosophila. Dev Biol. 1976;49:40–65.PubMedCrossRefGoogle Scholar
  36. Intarapat S, Stern CD. Chick stem cells: current progress and future prospects. Stem Cell Res. 2013;11:1378–92.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Ishiguro S, Minematsu T, Naito M, et al. Migratory ability of chicken primordial germ cells transferred into quail embryos. J Reprod Dev. 2009;55:183–6.PubMedCrossRefGoogle Scholar
  38. Jung JG, Kim DK, Park TS, et al. Development of novel markers for the characterization of chicken primordial germ cells. Stem Cells. 2005;23:689–98.PubMedCrossRefGoogle Scholar
  39. Kagami H, Clark ME, Verrinder Gibbins AM, et al. Sexual differentiation of chimeric chickens containing ZZ and ZW cells in the germline. Mol Reprod Dev. 1995;42:379–87.PubMedCrossRefGoogle Scholar
  40. Kagami H, Tagami T, Matsubara Y, et al. The developmental origin of primordial germ cells and the transmission of the donor-derived gametes in mixed-sex germline chimeras to the offspring in the chicken. Mol Reprod Dev. 1997;48:501–10.PubMedCrossRefGoogle Scholar
  41. Kang SJ, Choi JW, Kim SY, et al. Reproduction of wild birds via interspecies germ cell transplantation. Biol Reprod. 2008;79:931–7.PubMedCrossRefGoogle Scholar
  42. Karagenç L, Ginsburg M, Eyal-Giladi H, et al. Origin of primordial germ cells in the prestreak chick embryo. Dev Genet. 1996;19:290–301.PubMedCrossRefGoogle Scholar
  43. Karashima T, Sugimoto A, Yamamoto M. Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development. 2000;127:1069–79.PubMedGoogle Scholar
  44. Kimura T, Tomooka M, Yamano N, et al. AKT signaling promotes derivation of embryonic germ cells from primordial germ cells. Development. 2008;135:869–79.PubMedCrossRefGoogle Scholar
  45. Kito G, Aramaki S, Tanaka K, et al. Temporal and spatial differential expression of chicken germline-specific proteins cDAZL, CDH and CVH during gametogenesis. J Reprod Dev. 2010;56:341–6.PubMedCrossRefGoogle Scholar
  46. Knaut H, Werz C, Geisler R, et al. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature. 2003;421:279–82.PubMedCrossRefGoogle Scholar
  47. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, et al. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 2010;24:887–92.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kuwana T, Hashimoto K, Nakanishi A, et al. Long-term culture of avian embryonic cells in vitro. Int J Dev Biol. 1996;4:1061–4.Google Scholar
  49. Lasko PF, Ashburner M. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature. 1988;335:611–7.PubMedCrossRefGoogle Scholar
  50. Macdonald J, Glover JD, Taylor L, et al. Characterisation and germline transmission of cultured avian primordial germ cells. PLoS One. 2010;5(11):e15518.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Maeda S, Ohsako S, Kurohmaru M, et al. Analysis for the stage specific antigen of the primordial germ cells in the chick embryo. J Vet Med Sci. 1994;56:315–20.PubMedCrossRefGoogle Scholar
  52. Matsui Y, Takehara A, Tokitake Y, et al. The majority of early primordial germ cells acquire pluripotency by AKT activation. Development. 2014;141:4457–67.PubMedCrossRefGoogle Scholar
  53. Matsui Y, Zsebo K, Hogan BL. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell. 1992;70:841–7.PubMedCrossRefGoogle Scholar
  54. Mendez C, Carrasco E, Pedernera E. Adenohypophysis regulates cell proliferation in the gonads of the developing chick embryo. J Exp Zool A Comp Exp Biol. 2005;303:179–85.PubMedCrossRefGoogle Scholar
  55. Menke DB, Koubova J, Page DC. Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave. Dev Biol. 2003;262:303–12.PubMedCrossRefGoogle Scholar
  56. Meyer DB. The intra-embryonic migration of primordial germ cells in staged chick embryos. Anat Rec. 1961;139:314–5.Google Scholar
  57. Meyer DB. The migration of primordial germ cells in the chick embryo. Dev Biol. 1964;10:154–90.PubMedCrossRefGoogle Scholar
  58. Mintz B, Russell ES. Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool. 1957;134:207–37.PubMedCrossRefGoogle Scholar
  59. Miyahara D, Mori T, Makino R, et al. Culture conditions for maintain propagation, long-term survival and germline transmission of chicken primordial germ cell-like cells. J Poult Sci. 2014;51:87–95.CrossRefGoogle Scholar
  60. Miyahara D, Oishi I, Makino R, et al. Chicken stem cell factor enhances primordial germ cell proliferation cooperatively with fibroblast growth factor 2. J Reprod Dev. 2016;61:143–9.CrossRefGoogle Scholar
  61. Molyneaux KA, Zinszner H, Kunwar PS, et al. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development. 2003;130:4279–86.PubMedCrossRefGoogle Scholar
  62. Mozdziak PE, Angerman-Stewart J, Rushton B, et al. Isolation of chicken primordial germ cells using fluorescence-activated cell sorting. Poult Sci. 2005;84:594–600.PubMedCrossRefGoogle Scholar
  63. Nakamura Y, Yamamoto Y, Usui F, et al. Migration and proliferation of primordial germ cells in the early chicken embryo. Poult Sci. 2007;86:2182–93.PubMedCrossRefGoogle Scholar
  64. Naito M, Matsubara Y, Harumi T, et al. Differentiation of donor primordial germ cells into functional gametes in the gonads of mixed-sex germline chimaeric chickens produced by transfer of primordial germ cells isolated from embryonic blood. J Reprod Fertil. 1999;117:291–8.PubMedCrossRefGoogle Scholar
  65. Naito M, Harumi T, Kuwana T. Long-term culture of chicken primordial germ cells isolated from embryonic blood and production of germline chimaeric chickens. Anim Reprod Sci. 2015;153:50–61.PubMedCrossRefGoogle Scholar
  66. Nieuwkoop PD, Sutasurya LA. The migration of the primordial germ cells. In: Nieuwkoop PD, Sutasurya LA, editors. Primordial germ cells in the chordates. London: Cambridge University Press; 1979. p. 113–27.Google Scholar
  67. Ohinata Y, Payer B, O’Carroll D, et al. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature. 2005;436:207–13.PubMedCrossRefGoogle Scholar
  68. Olsen LC, Aasland R, Fjose A. A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev. 1997;66:95–105.PubMedCrossRefGoogle Scholar
  69. Ono T, Machida Y. Immunomagnetic purification of viable primordial germ cells of Japanese quail (Coturnix japonica). Comp Biochem Physiol A Mol Integr Physiol. 1999;122:255–9.PubMedCrossRefGoogle Scholar
  70. Ono T, Yokoi R, Aoyama H. Transfer of male or female primordial germ cells of quail into chick embryonic gonads. Exp Anim. 1996;45:347–52.PubMedCrossRefGoogle Scholar
  71. Ono T, Yokoi R, Maeda S, et al. Settlement of quail primordial germ cells in chicken gonads. Anim Sci Technol. 1998;69:546–55.Google Scholar
  72. Pardanaud L, Buck C, Dieterlen-Liever F. Early germ cell segregation and distribution in the quail blastodisc. Cell Differ. 1987;22:47–60.PubMedCrossRefGoogle Scholar
  73. Resnick JL, Bixler LS, Cheng L, et al. Long-term proliferation of mouse primordial germ cells in culture. Nature. 1992;359:550–1.PubMedCrossRefGoogle Scholar
  74. Romanoff AL. The urogenital system. In: Romanoff AL, editor. The avian embryo. New York: Macmillan; 1960. p. 783–862.Google Scholar
  75. Roussell DL, Bennett KL. glh-1, a germ-line putative RNA helicase from Caenorhabditis, has four zinc fingers. Proc Natl Acad Sci U S A. 1993;90:9300–4.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Ruggiu M, Speed R, Taggart M, et al. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature. 1997;389:73–7.PubMedCrossRefGoogle Scholar
  77. Saitou M, Barton SC, Surani MA. A molecular programme for the specification of germ cell fate in mice. Nature. 2002;41:293–300.CrossRefGoogle Scholar
  78. Sengoku T, Nureki O, Nakamura A, et al. Structural basis for RNA unwinding by the DEAD-box protein Drosophila vasa. Cell. 2006;125:287–300.PubMedCrossRefGoogle Scholar
  79. Smith CA, Roeszler KN, Bowles J, et al. Onset of meiosis in the chicken embryo; evidence of a role for retinoic acid. BMC Dev Biol. 2008;8:85.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Srihawong T, Kuwana T, Siripattarapravat K, et al. Chicken primordial germ cell motility in response to stem cell factor sensing. Int J Dev Biol. 2015;59:453–60.PubMedCrossRefGoogle Scholar
  81. Stebler J, Spieler D, Slanchev K, et al. Primordial germ cell migration in the chicken and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev Biol. 2004;272:351–61.PubMedCrossRefGoogle Scholar
  82. Swartz WJ, Domm LV. A study on division of primordial germ cells in the early chick embryo. Am J Anat. 1972;135:51–70.PubMedCrossRefGoogle Scholar
  83. Swartz WJ. Acid and alkaline phosphatase activity in migrating primordial germ cells of the early chick embryo. Anat Rec. 1982;202:379–85.PubMedCrossRefGoogle Scholar
  84. Swindell EC, Thaller C, Sockanathan S, et al. Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev Biol. 1999;216:282–96.PubMedCrossRefGoogle Scholar
  85. Swift CH. Origin and early history of the primordial germ-cells in the chick. Am J Anat. 1914;15:483–516.CrossRefGoogle Scholar
  86. Tagami T, Matsubara Y, Hanada H, et al. Differentiation of female chicken primordial germ cells into spermatozoa in male gonads. Dev Growth Differ. 1997;39:267–71.PubMedCrossRefGoogle Scholar
  87. Tagami T, Kagami H. Developmental origin of avian primordial germ cells and its unique differentiation in the gonads of mixed-sex chimeras. Mol Reprod Dev. 1998;50:370–6.PubMedCrossRefGoogle Scholar
  88. Tagami T, Kagami H, Matsubara Y, et al. Differentiation of female primordial germ cells in the male testes of chicken (Gallus Gallus Domesticus). Mol Reprod Dev. 2007;74:68–75.PubMedCrossRefGoogle Scholar
  89. Tajima A, Hayashi H, Kamizumi A, et al. Study on the concentration of circulating primordial germ cells (cPGCs) in early chick embryos. J Exp Zool. 1999;284:759–64.PubMedCrossRefGoogle Scholar
  90. Tajima A, Naito M, Yasuda Y, Kuwana T. Production of germ line chimera by transfer of primordial germ cells in the domestic chicken (Gallus domesticus). Theriogenology. 1993;40:509–19.PubMedCrossRefGoogle Scholar
  91. Takagi S, Ono T, Tsukada A, et al. Fertilization and blastoderm development of quail oocytes after intracytoplasmic injection of chicken sperm bearing the W chromosome. Poult Sci. 2007;86:937–43.PubMedCrossRefGoogle Scholar
  92. Tam PP, Zhou SX. 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. 1996;178:124–32.PubMedCrossRefGoogle Scholar
  93. Technau GM, Campos-Ortega JA. Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster Part III. Commitment and proliferative capabilities of pole cells and midgut progenitors. Rouxs Arch Dev Biol. 1986;195:489–98.PubMedCrossRefGoogle Scholar
  94. Tsunekawa N, Naito M, Sakai Y, et al. Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development. 2000;127:2741–50.PubMedGoogle Scholar
  95. Urven LE, Erickson CA, Abbott UK, et al. Analysis of germline development in the chicken embryo using an anti mouse EC cell antibody. Development. 1988;103:299–304.PubMedGoogle Scholar
  96. Vallier L, Mendjan S, Brown S, et al. Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development. 2009;136:1339–49.PubMedPubMedCentralCrossRefGoogle Scholar
  97. van de Lavoir MC, Diamond JH, Leighton PA, et al. Germline transmission of genetically modified primordial germ cells. Nature. 2006;441:766–9.PubMedCrossRefGoogle Scholar
  98. Van Limborgh J. Le premier indice de la différenciation sexuelle des gonades chez l’embryon de poulet. Arch Anat Microsc Morphol Exp. 1968;57:79–90.PubMedGoogle Scholar
  99. Venkatarama T, Lai F, Luo X, et al. Repression of zygotic gene expression in the Xenopus germline. Development. 2010;137:651–60.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Waldeyer W. Eierstock und Ei. Ein Beitrag zur Anatomie und Entwicklungsgeschichte der Sexualorgane. Leipzig: W. Engelmann; 1870.Google Scholar
  101. Weidinger G, Stebler J, Slanchev K, et al. Dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol. 2003;13:1429–34.PubMedCrossRefGoogle Scholar
  102. Whyte J, Glover JD, Woodcock M, et al. FGF, Insulin, and SMAD signaling cooperate for avian primordial germ cell self-renewal. Stem Cell Reports. 2015;5:1171–82.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Williamson A, Lehmann R. Germ cell development in Drosophila. Annu Rev Cell Dev Biol. 1996;12:365–91.PubMedCrossRefGoogle Scholar
  104. Xu RH, Sampsell-Barron TL, Gu F, et al. NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell. 2008;7:196–206.CrossRefGoogle Scholar
  105. Yasuda Y, Tajima A, Fujimoto T, et al. A method to obtain avian germ-line chimaeras using isolated primordial germ cells. J Reprod Fertil. 1992;96:521–8.PubMedCrossRefGoogle Scholar
  106. Yamaguchi S, Kurimoto K, Yabuta Y, et al. Conditional knockdown of Nanog induces apoptotic cell death in mouse migrating primordial germ cells. Development. 2009;136:4011–20.PubMedCrossRefGoogle Scholar
  107. Yoon C, Kawakami K, Hopkins N. Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development. 1997;124:3157–65.PubMedGoogle Scholar
  108. Yoshinaga K, Fujimoto T, Nakamura M, et al. Selective binding sites of primordial germ cells in chick and quail embryos. Anat Rec. 1992;233:625–32.PubMedCrossRefGoogle Scholar
  109. Yoshizaki G, Sakatani S, Tominaga H, et al. Cloning and characterization of vasa-like gene in rainbow trout and its expression in the germ cell lineage. Mol Reprod Dev. 2000;55:364–71.PubMedCrossRefGoogle Scholar
  110. Youngren KK, Coveney D, Peng X, et al. The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature. 2005;435:360–4.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Takahiro Tagami
    • 1
    Email author
  • Daichi Miyahara
    • 1
    • 2
  • Yoshiaki Nakamura
    • 3
  1. 1.Institute of Livestock Grassland Science, NAROIbarakiJapan
  2. 2.Shinshu UniversityUedaJapan
  3. 3.National Institute for Basic BiologyOkazakiJapan

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