Advertisement

Cell and Tissue Biology

, Volume 5, Issue 3, pp 203–213 | Cite as

Mammalian and human primordial germ cells: Differentiation, identification, migration

Article
  • 140 Downloads

Abstract

In recent years, a large amount of data on gene expression at different stages of primordial germ cell (PGC) development has been acquired. The process of germ line segregation in various species is realized differently, i.e., as preformation or epigenesis. The review surveys the mechanisms of the initial lineage specification of mammalian and human germ cells. The data on PGC identification from their initial detection in the epiblast to gonadal anlagen where they migrate has been analyzed. Information on the PGC markers of the different development, the mechanisms of PGC migration towards genital ridges and the chemokines that direct migration are discussed.

Keywords

primary germ cells markers migration chemokines epiblast 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aizenshtadt, T.B., Tsitologiya oogeneza (Ontogeny Cytology), Moscow: Nauka, 1984.Google Scholar
  2. Allegrucci, C., Thurston, A., Lucas, E., and Young, L., Epigenetics and the Germline, Reproduction, 2005, vol. 129, pp. 137–149.PubMedGoogle Scholar
  3. Alton, M. and Taketo, T., Switch from BAX-Dependent to BAX-Independent Germ Cell Loss during the Development of Fetal Mouse Ovaries, J. Cell. Sci., 2007, vol. 120, pp. 417–424.PubMedGoogle Scholar
  4. Anderson, R., Copeland, T.K., Scholer, H., Heasman, J., and Wylie, C., The Onset of Germ Cell Migration in the Mouse Embryo, Mech. Dev., 2000, vol. 91, pp. 61–68.PubMedGoogle Scholar
  5. Anderson, R., Fassler, R., Georges-Labouesse, E., Hynes, R.O., Bader, B.L., Kreidberg, J.A., Schaible, K., Heasman, J., and Wylie, C., Mouse Primordial Germ Cells Lacking Beta1 Integrins Enter the Germline but Fail to Migrate Normally to the Gonads, Development, 1999, vol. 126, pp. 1655–1664.PubMedGoogle Scholar
  6. Anderson, R., Heasman, J., and Wylie, C., Early Events in the Mammalian Germ Line, Int. Rev. Cyt., 2001, vol. 203, pp. 215–230.Google Scholar
  7. Ara, T., Nakamura, Y., Egawa, T., Sugiyama, T., Abe, K., Kishimoto, T., Matsui, Y., and Nagasawa, T., 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. USA, 2003, vol. 100, pp. 5319–5323.PubMedGoogle Scholar
  8. Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N., and Lovell-Badge, R., Multipotent Cell Lineages in Early Mouse Development Depend on SOX2 Function, Genes Dev,, 2003, vol. 17, pp. 126–140.PubMedGoogle Scholar
  9. Bandyopadhyay, S., Banerjee, S., Pal, A.K., Goswami, S.K., Chakravarty, B., and Kabir, S.N., Primordial Germ Cell Migration in the rat: Preliminary Evidence for a Role of Galactosyltransferase, Biol. Reprod., 2004, vol. 71, pp. 1822–1827.PubMedGoogle Scholar
  10. Bleul, C.C., Fuhlbrigge, R.C., Casasnovas J.M., Aiuti, A., and Springer, T.A., A Highly Efficacious Lymphocyte Chemoattractant, Stromal Cell-Derived Factor 1 (SDF-1), J. Exp. Med., 1996, vol. 184, pp. 1101–1109.PubMedGoogle Scholar
  11. Bortvin, A., Eggan, K., Skaletsky, H., Akutsu, H., Berry, D.L., Yanagimachi, R., Page, D.C. and Jaenisch, R., Incomplete Reactivation of Oct-4-Related Genes in Mouse Embryos Cloned from Somatic Nuclei, Development, 2003, vol. 130, pp. 1673–1680.PubMedGoogle Scholar
  12. Bortvin, A., Goodheart, M., Liao, M., and Page, D.C., Dppa3/Pgc7/Stella Is a Maternal Factor and Is not Required for Germ Cell Specification in Mice, BMC Dev. Biol., 2004, vol. 4, p. 2.PubMedGoogle Scholar
  13. Bowles, J. and Koopman, P., Retinoic Acid, Meiosis and Germ Cell fate in Mammals, Development, 2007, vol. 134, pp. 3401–3411.PubMedGoogle Scholar
  14. Bowles, J. and Koopman, P., Sex Determination in Mammalian Germ Cells: Extrinsic Versus Intrinsic Factors, Reproduction, 2010, vol. 139, pp. 943–958.PubMedGoogle Scholar
  15. Carmeliet, P., Lampugnani, M., Moons, L., Breviario, F., Compernolle, V., Bono, F., Balconi, G., Spagnuolo, R., Oosthuyse, B., Dewerchin, M., Zanetti, A., Angellilo, A., Mattot, V., Nuyens, D., Lutgens, E., Clotman, F., Ruiter, M.C., Groot, A.G., Poelmann, R., Lupu, F., Herbert, J.-M., Collen, D., and Dejana, E., Targeted Deficiency or Cytosolic Truncation of the VE-cadherin gene in mice Impairs VEGF-mediated Endothelial Survival and Angiogenesis, Cell, 1999, vol. 98, pp. 147–157.PubMedGoogle Scholar
  16. Castrillon, D.H., Quade, B.J., Wang, T.Y., Quigley, C., and Crum, C.P., The Human VASA Gene Is Specifically Expressed in the Germ Cell Lineage, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 9585–9590.PubMedGoogle Scholar
  17. Chang, D.H. and Calame, K.L., The Dynamic Expression Pattern of B Lymphocyte Induced Maturation Protein-1 (Blimp-1) during Mouse Embryonic Development, Mech. Dev., 2002, vol. 117, pp. 305–309.PubMedGoogle Scholar
  18. Chiquoine, A.D., The Identification, Origin, and Migration of the Primordial Germ Cells in the Mouse Embryo, Anat.Rec., 1954, vol. 118, pp. 135–146.PubMedGoogle Scholar
  19. Chu, G.C., Dunn, N.R., Anderson, D.C., Oxburgh, L., and Robertson, E.J., Differencial Requirements for Smad4 in TGFbeta-Dependent Patterning of the Early Mouse Embryo, Development, 2004, vol. 131, pp. 3501–3512.PubMedGoogle Scholar
  20. Clark, A.T., Bodnar, M.S., Fox, M., Rodriques, R.T., Abeyta, M.J., Firpo, M.T., and Reijo, Pera, R.A., Spontaneous Differentiation of Germ Cells from Human Embryonic Stem Cells in Vitro, Hum.Mol.Genet., 2004, vol. 13, pp. 727–739.PubMedGoogle Scholar
  21. David, N.B., Sapede, D., Saint-Etienne L., Thisse, C., Thisse, B., Dambly-Chaudiere, C., Rosa, F.M., and Ghysen, A., Molecular Basis of Cell Migration in the Fish Lateral Line: Role of the Chemokine Receptor CXCR4 and of Its Ligand, SDF1, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 16297–16302.PubMedGoogle Scholar
  22. De Felici, M. and Pesce, M., Interactions between Migratory Primordial Germ Cells and Cellular Substrates in the Mouse, in Germline Development. Ciba Symp., 1994, vol. 182, pp. 140–150.Google Scholar
  23. Di Carlo, A. and De Felici, M., A Role of E-Cadherin in Mouse Primordial Germ Cell Development, Dev. Biol., 2000, vol. 226, pp. 209–219.PubMedGoogle Scholar
  24. Dudley, B.M., Runian, C., Takeuchi, Y., Schaible, K., and Molyneaux, K., BMP Signaling Regulates PGC Numbers and Motility in Organ Culture, Mech. Dev., 2007, vol. 124, pp. 68–77.PubMedGoogle Scholar
  25. Durcova-Hills, G., Tokunaga, T., Kurosaka, S., Yamaguchi, M., Takahashi, S., and Imai, H., Immunomagnetic Isolation of Primordial Germ Cells and the Establishment of Embryonic Germ Cell Lines in the Mouse, Cloning, 1999, vol. 1, pp. 217–224.PubMedGoogle Scholar
  26. Eddy, E.M., Germ Plasm and the Differentiation of the Germ Cell Line, Int. Rev. Cytol., 1975, vol. 43, pp. 229–280.PubMedGoogle Scholar
  27. El, Ouali, H., Leheup, B.P., Gelly, J.L., and Grirnon, G., Laminin Ultrastructural Immunolocalization in Rat Testis during Ontogenesis, Histochemistry, 1991, vol. 95, pp. 241–246.PubMedGoogle Scholar
  28. Epifano, O. and Dean, J., Genetic Control of Early Folliculogenesis in Mice, Trends Endocrinol. Metab., 2002, vol. 13, pp. 169–173.PubMedGoogle Scholar
  29. Extavour, C.G. and Akam, M., Mechanisms of Germ Cells Specification Across the Metazoans: Epigenesis and Preformation, Development, 2003, vol. 130, pp. 5869–5884.PubMedGoogle Scholar
  30. Farini, D., La Sala, G., Tedesco, M., and De Felici, M., Chemoattractant Action and Molecular Signaling Pathways of Kit Ligand on Mouse Primordial Germ Cells, Dev. Biol., 2007, vol. 306, pp. 572–583.PubMedGoogle Scholar
  31. Fukuda, T., Ultrastructure of Primordial Germ Cells in Human Embryo, Virch. Arch. Cell Pathol., 1976, vol. 20, pp. 85–89.Google Scholar
  32. Garsia-Castro, M., Anderson, R., Heasman, J., and Wylie, C., Interactions between Germ Cells and Extracellular Matrix Glycoproteins during Migration and Gonad Assembly in the Mouse Embryo, J. Cell Biol., 1997, vol. 138, pp. 471–480.Google Scholar
  33. Geijsen, N., Horoschak, M., Kim, K., Gribnau, J., Eggan, K., and Daley, G.Q., Derivation of Embryonic Germ Cells and male Gametes from Embryonic Germ Cells, Nature, 2004, vol. 427, pp. 148–154.PubMedGoogle Scholar
  34. Gelly, J.-L., Richoux, J.P., and Grignon, G., Immunolocalization of Albumin and Transferrin in Germ Cells and Sertoli Cells during Rat Gonadal Morphogenesis and Postnatal Development of the Testis, Cell Tiss. Res., 1994, vol. 276, pp. 347–351.Google Scholar
  35. Ginsburg, V., Snow, M.H., and McLaren, A., Primordial Germ Cells in the Mouse Embryo during Gastrulation, Development, 1990, vol. 110, pp. 521–528.PubMedGoogle Scholar
  36. Gomperts, M., Garsia-Castro, M., Wylie., and Heasman, J., Interactions between Primordial Germ Cells Play a Role in Their Migration in Mouse Embryos, Development, 1994, vol. 120, pp. 135–141.PubMedGoogle Scholar
  37. Gu, Y., Runyan, C., Shoemaker, A., Surani, A., and Wylie, C., Steel Factor Controls Primordial Germ Cell Survival and Motility from the Time of Their Specification in the Allantois, and Provides a Continuous Niche Throughout Their Migration, Development, 2009, vol. 136, pp. 1295–1303.PubMedGoogle Scholar
  38. Haston, K.M., Tung, J.Y., and Reijo, Pera, R.A., Dazl Functions in Maintenance of Pluripotency and Genetic and Epigenetic Programs of Differentiation in Mouse Primordial Germ Cells in vivo and in vitro, PLoS ONE, 2009, vol. 4, pp. e5654.PubMedGoogle Scholar
  39. Hayashi, K., de, Sousa, Lopes, S.M., and Surani, M.A., Germ Cell Specification in Mice, Science, 2007, vol. 316, pp. 394–396.PubMedGoogle Scholar
  40. Hayashi, K., Kobayashi, T., Umino, T., Goitsuka, R., Matsui, Y., and Kitamura, D., SMAD1 Signaling Is Critical for Initial Commitment of Germ Cell Lineage from Mouse Epiblast, Mech. Dev., 2002, vol. 118, pp. 99–109.PubMedGoogle Scholar
  41. Houston, D.W. and King, M.L., Germ Plasma and Molecular Determinants of Germ Cell Fate, Curr. Top. Dev. Biol., 2000, vol. 50, pp. 155–181.PubMedGoogle Scholar
  42. Hoyer, P.E., Byskov, A.G., and Mollgard, K., Stem Cell Factor and C-Kit in Human Primordial Germ Cells and Fetal Ovaries, Mol. Cell. Endocrinol., 2005, vol. 234, pp. 1–10.PubMedGoogle Scholar
  43. Kee, K., Gonsalves, J.M., Clark, A.T., and Reijo, Pera, R.A., Bone Morphogenetic Proteins Induce Germ Cell Differentiation from Human Embryonic Stem Cells, Stem Cells Dev., 2006, vol. 15, pp. 831–837.PubMedGoogle Scholar
  44. Kerr, C.L. and Cheng, L., The Dazzle in Germ Cell Differentiation, J. Mol. Cell Biol., 2010, vol. 2, pp. 26–29.PubMedGoogle Scholar
  45. Kierszenbaum, A. and Tres, L., Primordial Germ Cell-Somatic Cell Partnership: A Balancing Cell Signaling Act, Mol. Repr. Dev., 2001, vol. 60, pp. 277–280.Google Scholar
  46. Knaut, H., Werz, C., and Geisler, R., The Tubingen 2000 Screen Consortium, Nusslein-Volhard, C., A Zebrafish Homologue of the Chemokine Receptor Cxcr4 Is a Germ-Cell Guidance Receptor, Nature, 2003, vol. 421, pp. 279–282.PubMedGoogle Scholar
  47. Kunwar, P.S., Siekhaus, D.E., and Lehmann, R., In vivo Migration: a Germ Cell Perspective, Annu. Rev. Cell. Biol., 2006, vol. 22, pp. 237–265.Google Scholar
  48. Kurimoto, K., Yabuta, Y., Ohinata, Y., Shigeta, M., Yamanaka, K., and Saitou, M., Complex Genome-Wide Transcription Dynamics by Blimp1 for the Specification of the Germ Cell Lineage in Mice, Genes Dev,, 2008, vol. 22, pp. 1617–1635.PubMedGoogle Scholar
  49. Lange, U.C., Adams, D.J., Lee, C., Barton, S., Schneider, R., Bradley, A., and Surani, M.A., Normal Germ Line Establishment in Mice Carrying a Deletion of the Ifitm/Fragilis Gene Family Cluster, Mol. Cell. Biol., 2008, vol. 28, pp. 4688–4696.PubMedGoogle Scholar
  50. Lawson, K.A. and Hage, W.J., Clonal Analysis of the Origin of Primordial Germ Cells in the Mouse, Ciba Found. Symp., 1994, vol. 182, pp. 68–84, discussion 84–91.PubMedGoogle Scholar
  51. Lin, L. and DePhilip, R., Sex-Dependent Expression of Placental (P) Cadherin during Mouse Gonadogenesis, Anat. Res., 1996, vol. 246, pp. 535–544.Google Scholar
  52. Lin, Y. and Page, D.C., Dazl Deficiency Leads to Embryonic Arrest of Germ Cell Development in XY C57BL/6 Mice, Dev. Biol., 2005, vol. 288, pp. 309–316.PubMedGoogle Scholar
  53. Lu, M., Grove, E.A., and Miller, R.J., Abnormal Development of the Hippocampal Dentate Gyrus in Mice Lacking the CXCR4 Chemokine Receptor, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 7090–7095.PubMedGoogle Scholar
  54. Müller A., Homey, B., Soto, H., Ge, N., Carton, D., Buchanan, M.E., McClanahan, T., Murphy, E., Yuan, W., Wagner, S.N., Barrera, J.L., Mohar, A., Verastegui, E., and Zlotnik, A., Involvement of Chemokine Receptors in Breast Cancer Metastasis, Nature, 2001, vol. 410, pp. 50–56.PubMedGoogle Scholar
  55. Mahabir, E. and Holtz, W., Migration of Primordial Germ Cells during Embryonic Development in Pigs, Reprod. Domest. Anim., 1999, vol. 34, pp. 35.Google Scholar
  56. Mahakali, Zama, A., Hudson, F.P., and Bedell, M.A., Analysis of Hypomorphic KitlSl Mutants Suggests Different Requirements for KITL in Proliferation and Migration of Mouse Primordial Germ Cells, Biol. Reprod., 2005, vol. 73, pp. 639–647.Google Scholar
  57. Mardanpour, P., Guan, K., Nolte, J., Lee, J.H., Hasenfuss, G., Engel, W., and Nayernia, K., Potency of Germ Cells and its Relevance for Regenerative Medicine, J. Anat., 2008, vol. 213, pp. 26–29.PubMedGoogle Scholar
  58. Massague, J., Seoane, J., and Wotton, D., Smad Transcription Factors, Genes Dev., 2005, vol. 19, pp. 2783–2810.PubMedGoogle Scholar
  59. Matova, N. and Cooley, L., Comparative Aspects of Animal Oogenesis, Dev. Biol., 2001, vol. 231, pp. 291–320.PubMedGoogle Scholar
  60. Matsui, Y., The Molecular Mechanisms Regulating Germ Cell Development and Potential, J. Androl., 2010, vol. 31, pp. 61–65.PubMedGoogle Scholar
  61. Matsui, Y., Zsebo, K.M., and Hogan, B.L., Embryonic Expression of a Haemotopoietic Growth Factor Encoded by the Sl Locus and the Ligand for C-kit, Nature, 1990, vol. 347, pp. 667–669.PubMedGoogle Scholar
  62. McLaren, A., Mammalian Germ Cells: Birth, Sex, and Immortality, Cell Struct. Funct., 2001, vol. 26, pp. 119–122.PubMedGoogle Scholar
  63. McLaren, A., Primordial Germ Cells in the Mouse, Dev. Biol., 2003, vol. 262, pp. 1–15.PubMedGoogle Scholar
  64. Mithraprabhu, S., and Loveland, K.L., Control of KIT Signalling in Male Germ Cells: What Can We Learn from Other Systems? Reproduction, 2009, vol. 138, pp. 743–757.PubMedGoogle Scholar
  65. Mochizuki, K., Nishimiya-Fujisawa, C., and Fujisawa, T., Universal Occurrence of the vasa-Related Genes among Metazoans and Their Germline Expression in Hydra, Dev. Genes Evol., 2001, vol. 211, pp. 299–308.PubMedGoogle Scholar
  66. Molyneaux, K.A., Stallock, J., Schaible, K., and Wylie, C., Time-Lapse Analysis of Living Mouse Germ Cell Migration, Dev. Biol., 2001, vol. 240, pp. 488–498.PubMedGoogle Scholar
  67. Molyneaux, K.A., Zinszner, H., Kunwar, P.S., Schaible, K., Stebler, J., Sunshine, M.J., O’Brien, W., Raz, E., Littman, D., Wylie, C., and Lehmann, R., The Chemokine SDF1/CXCL12 and Its Receptor CXCR4 Regulate Mouse Germ Cell Migration and Survival, Development, 2003, vol. 130, pp. 4279–4286.PubMedGoogle Scholar
  68. Nakamura, A., and Seydoux, G., Less is More: Specification of the Germline by Transcriptional Repression, Development, 2008, vol. 135, pp. 3817–3827.PubMedGoogle Scholar
  69. Nussbaum, M., Zur Differenzierung des Geschlechts im Tierreich, Arch. Mikr. Anat., 1880, vol. 18, pp. 1–121.Google Scholar
  70. Ohinata, Y., Ohta, H., Shigeta, M., Yamanaka, K., Wakayama, T., and Saitou, M., A Signaling Principle for the Specification of the Germ Cell Lineage in Mice, Cell, 2009, vol. 137, pp. 571–584.PubMedGoogle Scholar
  71. Ohinata, Y., Payer, B., O’Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S.C., Obukhanych, T. Nussenzweig, M., Tarakhovsky, A., Saitou, M., and Surani, A., Blimp1 Is a Critical Determinant of the Germ Cell Lineage in Mice, Nature, 2005, vol. 436, pp. 207–213.PubMedGoogle Scholar
  72. Okamura, D., Hayashi, K., and Matsui, Y., Mouse Epiblasts Change Responsiveness to BMP4 Signal Required for PGC Formation through Functions of Extraembryonic Ectoderm, Mol. Reprod. Dev., 2005, vol. 70, pp. 20–29.PubMedGoogle Scholar
  73. Okamura, D., Kimura, T., Nakano, T., and Matsui, Y., Cadherin-Mediated Cell Interaction Regulates Germ Cell Determination in Mice, Development, 2003, vol. 130, pp. 6423–6430.PubMedGoogle Scholar
  74. Ovitt C.E. and Scholer, H.R., The Molecular Biology of Oct-4 in the Early Mouse Embryo, Mol. Hum. Reprod., 1998, vol. 4, pp. 1021–1031.PubMedGoogle Scholar
  75. Pereda, J. and Motta, P.M., An Unique Fibrillar Coat on the Surface of Migrating Human Primordial Germ Cells, Arch. Histol. Cytol., 1991, vol. 54, pp. 419–425.PubMedGoogle Scholar
  76. Pesce, M. and Scholer, H., Oct-4: Gatekeeper in the Beginnings of Mammalian Development, Stem Cells, 2001, vol. 19, pp. 271–278.PubMedGoogle Scholar
  77. Raz, E. and Mahabaleshwar, H., Chemokine Signaling in Embryonic Cell Migration: A Fisheye View, Development, 2009, vol. 136, pp. 1223–1229.PubMedGoogle Scholar
  78. Reynolds, N., Collier, B., Maratou, K., Bingham, V., Speed, R.M., Taggart, M., Semple, C.A., Gray, N.K., and Cooke, H.J., Dazl Binds in vivo to Specific Transcripts and Can Regulate the Pre-meiotic Translation of Mvh in Germ Cells, Hum. Mol. Genet., 2005, vol. 14, pp. 3899–3009.PubMedGoogle Scholar
  79. Robertson, E.J., Charatsi, I., Joyner, C.J., Koonce, C.H., Morgan, M., Islam, A., Paterson, C., Lejsek, E., Arnold, S.J., Kallies, A., et al., Blimp1 Regulates Development of the Posterior Forelimb, Caudal Pharyngeal Arches, Heart and Sensory Vibrissae in Mice, Development, 2007, vol. 134, pp. 4335–4345.PubMedGoogle Scholar
  80. Runyan, C., Schaible, K., Molyneaux, K., Wang, Z., Levin, L., and Wylie, C., Steel Factor Controls Midline Cell Death of Primordial Germ Cells and Is Essential for Their Normal Proliferation and Migration, Development, 2006, vol. 133, pp. 4861–4869.PubMedGoogle Scholar
  81. Saitou, M., Barton, S.C., and Surani, M.A., A Molecular Programme for the Specification of Germ Cell Fate in Mice, Nature, 2002, vol. 418, pp. 293–300.PubMedGoogle Scholar
  82. Saitou, M., Specification of the Germ Cell Lineage in Mice, Front. Biosci., 2009, vol. 14, pp. 1068–1087.PubMedGoogle Scholar
  83. Sato, M., Kimura, T., Kurokawa, K., Fujita, Y., Abe, K., Masuhara, M., Yasunaga, T., Ryo, A., Yamamoto, M., and Nakano, T., Identification of PGC7, a New Gene Expressed Specifically in Preimplantation Embryos and Germ Cells, Mech. Dev., 2002, vol. 113, pp. 91–94.PubMedGoogle Scholar
  84. Seki, Y., Yamaji, M., Yabuta, Y., Sano, M., Shigeta, M., Matsui, Y., Saga, Y., Tachibana, M., Shinkai, Y., and Saitou, M., Cellular Dynamics Associated with the Genome-Wide Epigenetic Reprogramming in Migrating Primordial Germ Cells in Mice, Development, 2007, vol. 134, pp. 2627–2638.PubMedGoogle Scholar
  85. Semenova-Tyan-Shanskaya, A.G., and Knorre, A.G., Genital Primordium (Gonoblast), Its Origin and Evolution, Arkh. Anat., 1972, vol. 63, no. 8, pp. 29–48.Google Scholar
  86. Semenova-Tyan-Shanskaya, A.G., Primary Germ Cells of Embryos of Higher Vertebrates and Man at Early Development Stages, Arkh. Anat., 1971, vol. 60, no. 6, pp. 106–116.Google Scholar
  87. Seydoux, G. and Braun, R.E., Cell Pathway to Totipotency: Lesson from Germ Cells, Cell, 2006, vol. 127, pp. 891–904.PubMedGoogle Scholar
  88. Stallock J., Molyneaux, K., Schaible, K., Knudson, C.M., and Wylie, C., The Proapoptotic Gene Bax is Required for the Death of Ectopic Primordial Germ Cells during Their Migration in the Mouse Embryo, Development, 2003, vol. 130, pp. 6589–6597.PubMedGoogle Scholar
  89. Stebler, J., Spieler, D., Slanchev, K., Molyneaux, K.A., Richter, U., Cojocaru, V., Tarabykin, V., Wylie, C., Kessel, M., and Raz, E., Primordial Germ Cell Migration in the Chick and Mouse Embryo: the Role of the Chemokine SDF1/CXCL12, Dev. Biol., 2004, vol. 272, pp. 351–361.PubMedGoogle Scholar
  90. Surani, M.A., Ancelin, K., Hajkova, P., Lange, U.C., Payer, B., Western, P., and Saitou, M., Mechanism of Mouse Germ Cell Specification: a Genetic Program Regulating Epigenetic Reprogramming, Gold Spring Harb. Symp. Quant. Biol., 2004, vol. 69, pp. 1–9.Google Scholar
  91. Surani, M.A., Hayashi, K., and Hajkova, P., Genetic and Epigenetic Regulators of Pluripotency, Cell, 2007, vol. 128, pp. 747–762.PubMedGoogle Scholar
  92. Suzuki, H., Tsuda, M., Kiso, M., and Saga, Y., Nanos3 Maintains the Germ Cell Lineage in the Mouse by Suppressing both Bax-Dependent and -Independent Apoptotic Pathways, Dev. Biol., 2008, vol. 318, pp. 133–142.PubMedGoogle Scholar
  93. Takahashi, K. and Yamanaka, S., Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors, Cell, 2006, vol. 126, pp. 663–676.PubMedGoogle Scholar
  94. Takeuchi, T., Tanigawa, Y., Minamide, R., Ikenishi, K., and Komiya, T., Analysis of SDF-1/CXCR4 Signaling in Primordial Germ Cell Migration and Survival or Differentiation in Xenopus laevis, Mech. Dev., 2010, vol. 127, pp. 146–158.PubMedGoogle Scholar
  95. Takeuchi, Y., Molyneaux, K., Runian, C., Schaible, K., and Wylie, C., The Roles of FGF Signaling in Germ Cell Migration in the Mouse, Development, 2005, vol. 132, pp. 5399–5409.PubMedGoogle Scholar
  96. Takeva, Z., The Primary Germ Cells and Formation of Indifferent Gonad in Man, Dokl. Bolg. Acad. Sci., 1997, vol. 50, pp. 97–98.Google Scholar
  97. Tam, P.P. and Zhou, S.X., 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, vol. 178, pp. 124–132.PubMedGoogle Scholar
  98. Tanaka, S.S. and Matsui, Y., Developmentally Regulated Expression of Mil-1 and Mil-2, Mouse Interferon-Induced Transmembrane Protein Like Genes, during Formation and Differentiation of Primordial Germ Cells, Mech. Dev., 2002, vol. 119(Suppl. 1), pp. S261–S267.PubMedGoogle Scholar
  99. Tanaka, S.S., Yamaguchi, Y.L., Tsoi, B., Lickert, H., and Tam, P.P., IFITM/Mil/Fragilis Family Proteins IFITM1 and IFITM3 Play Distinct Roles in Mouse Primordial Germ Cell Homing and Repulsion, Dev. Cell., 2005, vol. 9, pp. 745–756.PubMedGoogle Scholar
  100. Teramura, T., Takehara, T., Kawata, N., Fujinami, N., Mitani, T., Takenoshita, M., Matsumoto, K., Saeki, K., Iritani, A., Sagawa, N., and Hosoi, Y., Primate Embryonic stem Cells Proceed to Early Gametogenesis in vitro, Cloning Stem Cells, 2007, vol. 9, pp. 144–156.PubMedGoogle Scholar
  101. Tres, L.L., Rosselot, C., and Kierszenbaum, A.L., Primordial Germ Cells: What Does It Take to Be Alive? Mol. Reprod. Dev., 2004, vol. 68, pp. 1–4.PubMedGoogle Scholar
  102. Tsuda, M., Sasaoka, Y., Kiso, M., Abe, K., Haraguchi, S., Kobayashi, S., and Saga, Y., Conserved Role of Nanos Proteins in Germ Cell Development, Science, 2003, vol. 301, pp. 1239–1241.PubMedGoogle Scholar
  103. Vincent, S.D., Dunn, N.R., Sciammas, R., Shapiro-Shalef, M., Davis, M.M., Calame, K., Bikoff, E.K., and Robertson, E.J., 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, vol. 132, pp. 1315–1325.PubMedGoogle Scholar
  104. Waldeyer, W., Eierstock und Ei, Leipzig: Engelmann Verl., 1870.Google Scholar
  105. Wartenberg, H., Germ Cell Migration Induced and Guided by Somatic Cell Interaction, Bibl. Anat., 1983, vol. 24, pp. 93–110.PubMedGoogle Scholar
  106. Weismann, A., Das Keimplasma, Eine Theorie der Vererbung, Jena: G. Fischer Verl., 1892.Google Scholar
  107. Weismann, A., Die Kontinuitat des Keimplasmas als Grundlage Einer Theorie der Vererbung, Jena: G.Fischer Verl., 1885.Google Scholar
  108. West, F.D., Roche-Rios, M.I., Abraham, S., Rao, R.R., Natrajan, M.S., Bacanamwo, M., and Stice, S.L., KIT Ligand and bone Morphogenetic Protein Signaling Enhances Human Embryonic stem Cell to Germ-like Cell Differentiation, Hum.Reprod., 2010, vol. 25, pp. 168–178.PubMedGoogle Scholar
  109. West, J.A., Viswanathan, S.R., Yabuuchi, A., Cunniff, K., Takeuchi, A., Park, I.H., Sero, J.E., Zhu, H., Perez-Atayde, A., Frazier, A.L., Surani, M.A., and Daley, G.Q., A Role for Lin28 in Primordial Germ-Cell Development and Germ-Cell Malignancy, Nature, 2009, vol. 460, pp. 909–913.PubMedGoogle Scholar
  110. Wylie, C., Germ Cells, Cell, 1999, vol. 96, pp. 165–174.PubMedGoogle Scholar
  111. Yabuta, Y., Kurimoto, K., Ohinata, Y., Seki, Y., and Saitou, M., Gene Expression Dynamics during Germline Specification in Mice Identified by Quantitative Single-Cell Gene Expression Profiling, Biol. Reprod., 2006, vol. 75, pp. 705–716.PubMedGoogle Scholar
  112. Yamaji, M., Seki, Y., Kurimoto, K., Yabuta, Y., Yuasa, M., Shigeta, M., Yamanaka, K., Ohinata, Y., and Saitou, M., Critical Function of Prdm14 for the Establishment of the Germ Cell Lineage in Mice, Nat. Genet., 2008, vol. 40, pp. 1016–1022.PubMedGoogle Scholar
  113. Yamaji, M., Tanaka, T., Shigeta, M., Chuma, S., Saga, Y., and Saitou, M., Functional Reconstruction of Nanos3 Expression in the Germ Cell Lineage by a Novel Transgenic Reporter Reveals Distinct Subcellular Localizations of Nanos3, Reproduction, 2010, vol. 139, pp. 381–393.PubMedGoogle Scholar
  114. Yeom, Y.I., Fuhrmann, G., Ovitt, C.E., Brehm, A., Ohbo, K., Gross, M., Hubner, K., and Scholer, H.R., Germline Regulatory Element of Oct-4 Specific for the Totipotent Cycle of Embryonal Cells, Development, 1996, vol. 122, pp. 881–894.PubMedGoogle Scholar
  115. Ying, Y. and Zhao, G.-Q., Cooperation of Endoderm-Derived BMP2 and Extraembrionic Ectoderm-Derived BMP4 in Primordial Germ Cell Generation in Mouse, Dev. Biol., 2001, vol. 232, pp. 484–492.PubMedGoogle Scholar
  116. Zeelenberg, I.S., Ruuls-Van, Stalle, L., and Roos, E., The Chemokine Receptor CXCR4 is Required for Outgrowth of Colon Carcinoma Micrometastases, Cancer Res., 2003, vol. 63, pp. 3833–3839.PubMedGoogle Scholar
  117. Zeeman, A.-M., Stoop, H., Boter, M., Gillis, Ad, J.M., Castrillon, D.H., Oosterhuis, J.W., and Looijenga, L.H.J., VASA Is a Specific Marker for Both Normal and Malignant Human Germ Cells, Lab. Invest., 2002, vol. 82, pp. 159–166.PubMedGoogle Scholar
  118. Zhao, G.-Q. and Garbers, D.L., Male Germ Cell Specification and Differentiation, Developmental Cell, 2002, vol. 2, pp. 537–547.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  1. 1.State Academy of PediatricsSt. PetersburgRussia

Personalised recommendations