Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2016 (2016), Article ID 1741072, 8 pages
http://dx.doi.org/10.1155/2016/1741072
Review Article

Primordial Germ Cells: Current Knowledge and Perspectives

1Center for Molecular Medicine and Stem Cell Research, Faculty of Medical Sciences, University of Kragujevac, 69 Svetozara Markovica Street, 34000 Kragujevac, Serbia
2Institute of Genetic Medicine, Newcastle University, The International Centre for Life, Central Parkway, Newcastle upon Tyne NE1 3BZ, UK
3Spebo Medical, Norvezanska 16, 16 000 Leskovac, Serbia

Received 15 April 2015; Accepted 17 May 2015

Academic Editor: Irma Virant-Klun

Copyright © 2016 Aleksandar Nikolic et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Bahamondes and M. Y. Makuch, “Infertility care and the introduction of new reproductive technologies in poor resource settings,” Reproductive Biology and Endocrinology, vol. 12, no. 1, article 87, 2014. View at Publisher · View at Google Scholar
  2. M. C. Inhrorn and P. Patrizio, “Infertility around the globe: new thinking on gender, reproductive technologies and global movements in the 21st century,” Human Reproduction Update, 2015. View at Publisher · View at Google Scholar
  3. J. Boivin, L. Bunting, J. A. Collins, and K. G. Nygren, “International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care,” Human Reproduction, vol. 22, no. 6, pp. 1506–1512, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Bhartiya, I. Hinduja, H. Patel, and R. Bhilawadikar, “Making gametes from pluripotent stem cells—a promising role for very small embryonic-like stem cells,” Reproductive Biology and Endocrinology, vol. 12, article 114, 2014. View at Publisher · View at Google Scholar
  5. N. E. Skakkebæk, E. Rajpert-De Meyts, and K. M. Main, “Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects,” Human Reproduction, vol. 16, no. 5, pp. 972–978, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Saitou and M. Yamaji, “Primordial germ cells in mice,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 11, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. Ohinata, H. Ohta, M. Shigeta, K. Yamanaka, T. Wakayama, and M. Saitou, “A signaling principle for the specification of the germ cell lineage in mice,” Cell, vol. 137, no. 3, pp. 571–584, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Saitou, B. Payer, U. C. Lange, S. Erhardt, S. C. Barton, and M. A. Surani, “Specification of germ cell fate in mice,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 358, no. 1436, pp. 1363–1370, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. D. H. Castrillon, B. J. Quade, T. Y. Wang, C. Quigley, and C. P. Crum, “The human VASA gene is specifically expressed in the germ cell lineage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 17, pp. 9585–9590, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. E. E. Saffman and P. Lasko, “Germline development in vertebrates and invertebrates,” Cellular and Molecular Life Sciences, vol. 55, no. 8-9, pp. 1141–1163, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Gomperts, M. Garcia-Castro, C. Wylie, and J. Heasman, “Interactions between primordial germ cells play a role in their migration in mouse embryos,” Development, vol. 120, no. 1, pp. 135–141, 1994. View at Google Scholar · View at Scopus
  12. G. Seydoux and M. A. Dunn, “Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster,” Development, vol. 124, no. 11, pp. 2191–2201, 1997. View at Google Scholar · View at Scopus
  13. R. E. Boswell and A. P. Mahowald, “tudor, a gene required for assembly of the germ plasma in Drosophila melanogaster,” Cell, vol. 43, no. 1, pp. 97–104, 1985. View at Publisher · View at Google Scholar · View at Scopus
  14. E. E. Capowski, P. Martin, C. Garvin, and S. Strome, “Identification of grandchildless loci whose products are required for normal germ-line development in the nematode Caenorhabditis elegans,” Genetics, vol. 129, no. 4, pp. 1061–1072, 1991. View at Google Scholar · View at Scopus
  15. L. B. Christerson and D. M. McKearin, “orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis,” Genes and Development, vol. 8, no. 5, pp. 614–628, 1994. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Tilgner, S. P. Atkinson, A. Golebiewska, M. Stojković, M. Lako, and L. Armstrong, “Isolation of primordial germ cells from differentiating human embryonic stem cells,” Stem Cells, vol. 26, no. 12, pp. 3075–3085, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Ginsburg, M. H. L. Snow, and A. McLaren, “Primordial germ cells in the mouse embryo during gastrulation,” Development, vol. 110, no. 2, pp. 521–528, 1990. View at Google Scholar · View at Scopus
  18. A. D. Chiquoine, “The identification, origin, and migration of the primordial germ cells in the mouse embryo,” The Anatomical Record, vol. 118, no. 2, pp. 135–146, 1954. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Moore, R. Udayashankar, and B. Aflatoonian, “Stem cells for reproductive medicine,” Molecular and Cellular Endocrinology, vol. 288, no. 1-2, pp. 104–110, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Anderson, T. K. Copeland, H. Schöler, J. Heasman, and C. Wylie, “The onset of germ cell migration in the mouse embryo,” Mechanisms of Development, vol. 91, no. 1-2, pp. 61–68, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Saitou, S. C. Barton, and M. A. Surani, “A molecular programme for the specification of germ cell fate in mice,” Nature, vol. 418, no. 6895, pp. 293–300, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. G. R. MacGregor, B. P. Zambrowicz, and P. Soriano, “Tissue non-specific alkaline phosphatase is expressed in both embryonic and extraembryonic lineages during mouse embryogenesis but is not required for migration of primordial germ cells,” Development, vol. 121, no. 5, pp. 1487–1496, 1995. View at Google Scholar · View at Scopus
  23. Y. I. I. Yeom, G. Fuhrmann, C. E. Ovitt et al., “Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells,” Development, vol. 122, no. 3, pp. 881–894, 1996. View at Google Scholar · View at Scopus
  24. Y. Ohinata, B. Payer, D. O'Carroll et al., “Blimp1 is a critical determinant of the germ cell lineage in mice,” Nature, vol. 436, no. 7048, pp. 207–213, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Yamaji, Y. Seki, K. Kurimoto et al., “Critical function of Prdm14 for the establishment of the germ cell lineage in mice,” Nature Genetics, vol. 40, no. 8, pp. 1016–1022, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. U. Günesdogan, E. Magnúsdóttir, and M. A. Surani, “Primoridal germ cell specification: a context-dependent cellular differentiation event,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 369, no. 1657, 2013. View at Publisher · View at Google Scholar
  27. K. Kurimoto, Y. Yabuta, Y. Ohinata, M. Shigeta, K. Yamanaka, and M. Saitou, “Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice,” Genes and Development, vol. 22, no. 12, pp. 1617–1635, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Yabuta, K. Kurimoto, Y. Ohinata, Y. Seki, and M. Saitou, “Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling,” Biology of Reproduction, vol. 75, no. 5, pp. 705–716, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Sato, T. Kimura, K. Kurokawa et al., “Identification of PGC7, a new gene expressed specifically in preimplantation embryos and germ cells,” Mechanisms of Development, vol. 113, no. 1, pp. 91–94, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Saga, “Mouse germ cell development during embryogenesis,” Current Opinion in Genetics and Development, vol. 18, no. 4, pp. 337–341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Saitou, B. Payer, D. O'Carroll, Y. Ohinata, and M. A. Surani, “Blimp1 and the emergence of the germ line during development in the mouse,” Cell Cycle, vol. 4, no. 12, pp. 1736–1740, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Saitou, “Germ cell specification in mice,” Current Opinion in Genetics and Development, vol. 19, no. 4, pp. 386–395, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. L. C. Fuentealba, E. Eivers, A. Ikeda et al., “Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal,” Cell, vol. 131, no. 5, pp. 980–993, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. K. A. Molyneaux, J. Stallock, K. Schaible, and C. Wylie, “Time-lapse analysis of living mouse germ cell migration,” Developmental Biology, vol. 240, no. 2, pp. 488–498, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. P. P. L. Tam and M. H. L. Snow, “Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos,” Journal of Embryology and Experimental Morphology, vol. 64, pp. 133–147, 1981. View at Google Scholar · View at Scopus
  36. K. Tilgner, S. P. Atkinson, S. Yung et al., “Expression of GFP under the control of the RNA helicase VASA permits fluorescence-activated cell sorting isolation of human primordial germ cells,” Stem Cells, vol. 28, no. 1, pp. 84–92, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. D. B. Menke, J. Koubova, and D. C. Page, “Sexual differentiation of germ cells in XX mouse gonads occurs in an anterior-to-posterior wave,” Developmental Biology, vol. 262, no. 2, pp. 303–312, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. P. F. Lasko and M. Ashburner, “Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development,” Genes and Development, vol. 4, no. 6, pp. 905–921, 1990. View at Publisher · View at Google Scholar · View at Scopus
  39. M. R. Bendel-Stenzel, M. Gomperts, R. Anderson, J. Heasman, and C. Wylie, “The role of cadherins during primordial germ cell migration and early gonad formation in the mouse,” Mechanisms of Development, vol. 91, no. 1-2, pp. 143–152, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Anderson, R. Fässler, E. Georges-Labouesse et al., “Mouse primordial germ cells lacking β1 integrins enter the germline but fail to migrate normally to the gonads,” Development, vol. 126, no. 8, pp. 1655–1664, 1999. View at Google Scholar · View at Scopus
  41. S.-R. Chen, Q.-S. Zheng, Y. Zhang, F. Gao, and Y.-X. Liu, “Disruption of genital ridge development causes aberrant primordial germ cell proliferation but does not affect their directional migration,” BMC Biology, vol. 11, article 22, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Chuma, M. Kanatsu-Shinohara, K. Inoue et al., “Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis,” Development, vol. 132, no. 1, pp. 117–122, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Hayashi, S. M. C. D. S. Lopes, and M. A. Surani, “Germ cell specification in mice,” Science, vol. 316, no. 5823, pp. 394–396, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Lin and D. C. Page, “Dazl deficiency leads to embryonic arrest of germ cell development in XY C57BL/6 mice,” Developmental Biology, vol. 288, no. 2, pp. 309–316, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Reynolds, B. Collier, V. Bingham, N. K. Gray, and H. J. Cooke, “Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl,” RNA, vol. 13, no. 7, pp. 974–981, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. N. Reynolds, B. Collier, K. Maratou et al., “Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells,” Human Molecular Genetics, vol. 14, no. 24, pp. 3899–3909, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Zeng, Y. Lu, X. Liao et al., “DAZL binds to 3′UTR of Tex19.1 mRNAs and regulates Tex19.1 expression,” Molecular Biology Reports, vol. 36, no. 8, pp. 2399–2403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Ruggiu, R. Speed, M. Taggart et al., “The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis,” Nature, vol. 389, no. 6646, pp. 73–77, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Tsui, T. Dai, S. T. Warren, E. C. Salido, and P. H. Yen, “Association of the mouse infertility factor DAZL1 with actively translating polyribosomes,” Biology of Reproduction, vol. 62, no. 6, pp. 1655–1660, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. H. J. Cooke, M. Lee, S. Kerr, and M. Ruggiu, “A murine homologue of the human DAZ gene is autosomal and expressed only in male and female gonads,” Human Molecular Genetics, vol. 5, no. 4, pp. 513–516, 1996. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Chen, M. Welling, D. Bloch et al., “DAZL limits pluripotency, differentiation, and apoptosis in developing primordial germ cells,” Stem Cell Reports, vol. 3, no. 5, pp. 892–904, 2014. View at Publisher · View at Google Scholar
  52. M. E. Gill, Y.-C. Hu, Y. Lin, and D. C. Page, “Licensing of gametogenesis, dependent on RNA binding protein DAZL, as a gateway to sexual differentiation of fetal germ cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 18, pp. 7443–7448, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. A. McLaren, “Primordial germ cells in the mouse,” Developmental Biology, vol. 262, no. 1, pp. 1–15, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. C. Hu, P. K. Nicholls, Y. Q. Soh et al., “Licensing of primordial germ cells for gametogenesis depends on genital ridge signaling,” PLoS Genetics, vol. 11, no. 3, Article ID e1005019, 2015. View at Publisher · View at Google Scholar
  55. B. Aflatoonian and H. D. Moore, “Germ cells from mouse and human embryonic stem cells,” Reproduction, vol. 132, no. 5, pp. 699–707, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. R. L. Brinster, “Germline stem cell transplantation and transgenesis,” Science, vol. 296, no. 5576, pp. 2174–2176, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. A. McLaren, “Mammalian germ cells: birth, sex, and immortality,” Cell Structure and Function, vol. 26, no. 3, pp. 119–122, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. K. A. Lawson, N. R. Dunn, B. A. J. Roelen et al., “Bmp4 is required for the generation of primordial germ cells in the mouse embryo,” Genes & Development, vol. 13, no. 4, pp. 424–436, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. P. P. L. Tam and D. A. F. Loebel, “Gene function in mouse embryogenesis: get set for gastrulation,” Nature Reviews Genetics, vol. 8, no. 5, pp. 368–381, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Hübner, G. Fuhrmann, L. K. Christenson et al., “Derivation of oocytes from mouse embryonic stem cells,” Science, vol. 300, no. 5623, pp. 1251–1256, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. Li, X. Wang, X. Feng et al., “Generation of male germ cells from mouse induced pluripotent stem cells in vitro,” Stem Cell Research, vol. 12, no. 2, pp. 517–530, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Hayashi, H. Ohta, K. Kurimoto, S. Aramaki, and M. Saitou, “Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells,” Cell, vol. 146, no. 4, pp. 519–532, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. W. Wei, T. Qing, X. Ye et al., “Primordial germ cell specification from embryonic stem cells,” PLoS ONE, vol. 3, no. 12, Article ID e4013, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Matoba and A. Ogura, “Generation of functional oocytes and spermatids from fetal primordial germ cells after ectopic transplantation in adult mice,” Biology of Reproduction, vol. 84, no. 4, pp. 631–638, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Hashimoto, M. Noguchi, and N. Nakatsuji, “Mouse offspring derived from fetal ovaries or reaggregates which were cultured and transplanted into adult females,” Development Growth and Differentiation, vol. 34, no. 2, pp. 233–238, 1992. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Hayashi, S. Ogushi, K. Kurimoto, S. Shimamoto, H. Ohta, and M. Saitou, “Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice,” Science, vol. 338, no. 6109, pp. 971–975, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. K. Hayashi and M. Saitou, “Generation of eggs from mouse embryonic stem cells and induced pluripotent stem cells,” Nature Protocols, vol. 8, no. 8, pp. 1513–1524, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. N. Irie, L. Weinberger, W. W. Tang et al., “SOX17 is a critical specifier of human primordial germ cell fate,” Cell, vol. 160, no. 1-2, pp. 253–268, 2015. View at Publisher · View at Google Scholar
  69. C. Ramathal, J. Durruthy-Durruthy, M. Sukhwani et al., “Fate of iPSCs derived from azoospermic and fertile men following Xenotransplantation to murine seminiferous tubules,” Cell Reports, vol. 7, no. 4, pp. 1284–1297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. L. Leng, Y. Tan, F. Gong et al., “Differentiation of primordial germ cells from induced pluripotent stem cells of primary ovarian insufficiency,” Human Reproduction, vol. 30, no. 3, pp. 737–748, 2015. View at Publisher · View at Google Scholar
  71. H. Cai, X. Xia, L. Wang et al., “In vitro and in vivo differentiation of induced pluripotent stem cells into male germ cells,” Biochemical and Biophysical Research Communications, vol. 433, no. 3, pp. 286–291, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. K. Okita, T. Ichisaka, and S. Yamanaka, “Generation of germline-competent induced pluripotent stem cells,” Nature, vol. 448, no. 7151, pp. 313–317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Imamura, T. Aoi, A. Tokumasu et al., “Induction of primordial germ cells from mouse induced pluripotent stem cells derived from adult hepatocytes,” Molecular Reproduction and Development, vol. 77, no. 9, pp. 802–811, 2010. View at Publisher · View at Google Scholar · View at Scopus