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Avian Primordial Germ Cells

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Avian Reproduction

Part of the book series: Advances in Experimental Medicine and Biology ((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.

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References

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bowles J, Knight D, Smith C, et al. Retinoid signaling determines germ cell fate in mice. Science. 2006;312:596–600.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chambers I, Silva J, Colby D, et al. Nanog safeguards pluripotency and mediates germline development. Nature. 2007;450:1230–4.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Donovan PJ. Growth factor regulation of mouse primordial germ cell development. Curr Top Dev Biol. 1994;29:189–225.

    Article  CAS  PubMed  Google Scholar 

  • Eberhart CG, Maines JZ, Wasserman SA. Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature. 1996;381:783–5.

    Article  CAS  PubMed  Google Scholar 

  • Eddy EM. Germ plasm and the differentiation of the germ cell line. Int Rev Cytol. 1975;43:229–80.

    Article  CAS  PubMed  Google Scholar 

  • Ephrussi A, Lehmann R. Induction of germ cell formation by oskar. Nature. 1992;358:387–92.

    Article  CAS  PubMed  Google Scholar 

  • Eyal-Giladi H, Ginsburg M, Farbarov A. Avian primordial germ cells are of epiblastic origin. J Embryol Exp Morphol. 1981;65:139–47.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghabrial A, Schupbach T. Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat Cell Biol. 1999;1:354–7.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol. 1951;88:49–92.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Huettner AF. The origin of the germ cells in Drosophila melanogaster. J Morphol. 1923;2:385–422.

    Article  Google Scholar 

  • Hughes GC. The population of germ cells in the developing female chick. J Embryol Exp Morphol. 1963;11:513–36.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Illmensee K, Mahowald AP, Loomis MR. The ontogeny of germ plasm during oogenesis in Drosophila. Dev Biol. 1976;49:40–65.

    Article  CAS  PubMed  Google Scholar 

  • Intarapat S, Stern CD. Chick stem cells: current progress and future prospects. Stem Cell Res. 2013;11:1378–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Kang SJ, Choi JW, Kim SY, et al. Reproduction of wild birds via interspecies germ cell transplantation. Biol Reprod. 2008;79:931–7.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Kuramochi-Miyagawa S, Watanabe T, Gotoh K, et al. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 2010;24:887–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Lasko PF, Ashburner M. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature. 1988;335:611–7.

    Article  CAS  PubMed  Google Scholar 

  • Macdonald J, Glover JD, Taylor L, et al. Characterisation and germline transmission of cultured avian primordial germ cells. PLoS One. 2010;5(11):e15518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Matsui Y, Zsebo K, Hogan BL. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell. 1992;70:841–7.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Meyer DB. The intra-embryonic migration of primordial germ cells in staged chick embryos. Anat Rec. 1961;139:314–5.

    Google Scholar 

  • Meyer DB. The migration of primordial germ cells in the chick embryo. Dev Biol. 1964;10:154–90.

    Article  CAS  PubMed  Google Scholar 

  • Mintz B, Russell ES. Gene-induced embryological modifications of primordial germ cells in the mouse. J Exp Zool. 1957;134:207–37.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Olsen LC, Aasland R, Fjose A. A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev. 1997;66:95–105.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Ono T, Yokoi R, Maeda S, et al. Settlement of quail primordial germ cells in chicken gonads. Anim Sci Technol. 1998;69:546–55.

    CAS  Google Scholar 

  • Pardanaud L, Buck C, Dieterlen-Liever F. Early germ cell segregation and distribution in the quail blastodisc. Cell Differ. 1987;22:47–60.

    Article  CAS  PubMed  Google Scholar 

  • Resnick JL, Bixler LS, Cheng L, et al. Long-term proliferation of mouse primordial germ cells in culture. Nature. 1992;359:550–1.

    Article  CAS  PubMed  Google Scholar 

  • Romanoff AL. The urogenital system. In: Romanoff AL, editor. The avian embryo. New York: Macmillan; 1960. p. 783–862.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruggiu M, Speed R, Taggart M, et al. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature. 1997;389:73–7.

    Article  CAS  PubMed  Google Scholar 

  • Saitou M, Barton SC, Surani MA. A molecular programme for the specification of germ cell fate in mice. Nature. 2002;41:293–300.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Swartz WJ, Domm LV. A study on division of primordial germ cells in the early chick embryo. Am J Anat. 1972;135:51–70.

    Article  CAS  PubMed  Google Scholar 

  • Swartz WJ. Acid and alkaline phosphatase activity in migrating primordial germ cells of the early chick embryo. Anat Rec. 1982;202:379–85.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Swift CH. Origin and early history of the primordial germ-cells in the chick. Am J Anat. 1914;15:483–516.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Vallier L, Mendjan S, Brown S, et al. Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development. 2009;136:1339–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van de Lavoir MC, Diamond JH, Leighton PA, et al. Germline transmission of genetically modified primordial germ cells. Nature. 2006;441:766–9.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Venkatarama T, Lai F, Luo X, et al. Repression of zygotic gene expression in the Xenopus germline. Development. 2010;137:651–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waldeyer W. Eierstock und Ei. Ein Beitrag zur Anatomie und Entwicklungsgeschichte der Sexualorgane. Leipzig: W. Engelmann; 1870.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson A, Lehmann R. Germ cell development in Drosophila. Annu Rev Cell Dev Biol. 1996;12:365–91.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Tagami, T., Miyahara, D., Nakamura, Y. (2017). Avian Primordial Germ Cells. In: Sasanami, T. (eds) Avian Reproduction. Advances in Experimental Medicine and Biology, vol 1001. Springer, Singapore. https://doi.org/10.1007/978-981-10-3975-1_1

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