Skip to main content

Embryonic Stem Cells and Fetal Development Models

  • Chapter
  • First Online:
Fetal Stem Cells in Regenerative Medicine

Abstract

Pluripotent stem cells possess the unique capacity to proliferate indefinitely in culture and to differentiate into cells of the three germ layers, the endoderm, ectoderm and mesoderm. These important features render pluripotent stem cells ideal for both, basic studies in developmental biology and biomedical research in farm animals. Pluripotent cells can serve as a valuable tool for complex genetic modifications with the goal to improve production traits, disease resistance or for the creation of human disease models. The domestic pig shares many genetic, anatomical and physiological similarities with humans and thus has emerged as a particularly suitable model for the creation of human disease models and the development of novel stem cell therapies. Porcine germ line competent pluripotent stem cell lines have not yet been established, neither from early embryos (embryonic stem cells), nor from fetuses (fetal stem cells) or adult tissue (adult stem cells). Here, we review the progress made in the derivation and characterization of pluripotent stem cell lines from pigs.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Ahn KS, Won JY, Heo SY, Kang JH, Yang HS, Shim H. Transgenesis and nuclear transfer using porcine embryonic germ cells. Cloning Stem Cells. 2007;9:461–8.

    Article  CAS  PubMed  Google Scholar 

  2. Alberio R, Croxall N, Allegrucci C. Pig epiblast stem cells depend on activin/nodal signaling for pluripotency and self-renewal. Stem Cells Dev. 2010;6:484–95.

    Google Scholar 

  3. Anderson R, Copeland TK, Schöler H, Heasman J, Wylie C. The onset of germ cell migration in the mouse embryo. Mech Dev. 2000;91:61–8.

    Article  CAS  PubMed  Google Scholar 

  4. Anderson RA, McLaughlin M, Woods DC, Tilly JL, Telfer EE. Evaluation of oogonial stem cells and neo-oogenesis in girls and women with Turner syndrome: a pilot study. Hum Reprod. 2013;28(Suppl):52.

    Article  Google Scholar 

  5. Bai Y, Yu M, Hu Y, Qiu P, Liu W, Zheng W, Peng S, Hua J. Location and characterization of female germline stem cells (FGSCs) in juvenile porcine ovary. Cell Prolif. 2013;46:516–28.

    Article  CAS  PubMed  Google Scholar 

  6. Blomberg LA, Schreier LL, Talbot NC. Expression analysis of pluripotency factors in the undifferentiated porcine inner cell mass and epiblast during in vitro culture. Mol Reprod Dev. 2008;75:450–63.

    Article  CAS  PubMed  Google Scholar 

  7. Boiani M, Schöler HR. Regulatory networks in embryo-derived pluripotent stem cells. Nat Rev Mol Cell Biol. 2005;6:872–84.

    Article  CAS  PubMed  Google Scholar 

  8. Boroviak T, Nichols J. The birth of embryonic pluripotency. Philos Trans R Soc Lond B Biol Sci. 2014;369(1657):pii:20130541.

    Article  CAS  Google Scholar 

  9. Brevini TA, Antonini S, Cillo F, Crestan M, Gandolfi F. Porcine embryonic stem cells: facts, challenges and hopes. Theriogenology. 2007;68 Suppl 1:S206–13.

    Article  CAS  PubMed  Google Scholar 

  10. Brevini TA, Antonini S, Pennarossa G, Gandolfi F. Recent progress in embryonic stem cell research and its application in domestic species. Reprod Domest Anim. 2008;43 Suppl 2:193–9.

    Article  PubMed  Google Scholar 

  11. Brevini TA, Pennarossa G, Gandolfi F. No shortcuts to pig embryonic stem cells. Theriogenology. 2010;74:544–50.

    Article  CAS  PubMed  Google Scholar 

  12. Brevini TA, Tosetti V, Crestan M, Antonini S, Gandolfi F. Derivation and characterization of pluripotent cell lines from pig embryos of different origins. Theriogenology. 2007;67:54–63.

    Article  PubMed  Google Scholar 

  13. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A. 1994;91:11298–302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL, Smith A. Capture of authentic embryonic stem cells from rat blastocysts. Cell. 2008;135:1287–98.

    Article  CAS  PubMed  Google Scholar 

  15. Bui HT, Van Thuan N, Kwon DN, Choi YJ, Kang MH, Han JW, Kim T, Kim JH. Identification and characterization of putative stem cells in the adult pig ovary. Development. 2014;141:2235–44.

    Article  CAS  PubMed  Google Scholar 

  16. Chen LR, Shiue YL, Bertolini L, Medrano JF, BonDurant RH, Anderson GB. Establishment of pluripotent cell lines from porcine preimplantation embryos. Theriogenology. 1999;52:195–212.

    Article  CAS  PubMed  Google Scholar 

  17. Cong Y, Ma J, Sun R, Wang J, Xue B, Wang J, Xie B, Wang J, Hu K, Liu Z. Derivation of putative porcine embryonic germ cells and analysis of their multi-lineage differentiation potential. J Genet Genomics. 2013;40:453–64.

    Article  CAS  PubMed  Google Scholar 

  18. De Felici M, Barrios F. Seeking the origin of female germline stem cells in the mammalian ovary. Reproduction. 2013;146:R125–30.

    Article  PubMed  CAS  Google Scholar 

  19. Dirami G, Ravindranath N, Pursel V, Dym M. Effects of stem cell factor and granulocyte macrophage-colony stimulating factor on survival of porcine type A spermatogonia cultured in KSOM. Biol Reprod. 1999;61:225–30.

    Article  CAS  PubMed  Google Scholar 

  20. Dong X, Tsung H, Mu Y, Liu L, Chen H, Zhang L, Wang H, Feng S. Generation of chimeric piglets by injection of embryonic germ cells from inbred Wuzhishan miniature pigs into blastocysts. Xenotransplantation. 2013;21:140–8.

    Article  PubMed  Google Scholar 

  21. Durcova-Hills G, Prelle K, Muller S, Stojkovic M, Motlik J, Wolf E, Brem G. Primary culture of porcine PGCs requires LIF and porcine membrane-bound stem cell factor. Zygote. 1998;6:271–5.

    Article  CAS  PubMed  Google Scholar 

  22. Durcova-Hills G, Tokunaga T, Kurosaka S, Yamaguchi M, Takahashi S, Imai H. Immunomagnetic isolation of primordial germ cells and the establishment of embryonic germ cell lines in the mouse. Cloning. 1999;1:217–24.

    Article  CAS  PubMed  Google Scholar 

  23. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154–6.

    Article  CAS  PubMed  Google Scholar 

  24. Evans MJ, Notarianni E, Laurie S, Moor RM. Derivation and preliminary characterization of pluripotent cell lines from porcine and bovine blastocysts. Theriogenology. 1990;33:125–8.

    Article  Google Scholar 

  25. Garcia T, Hofmann MC. Isolation of undifferentiated and early differentiating type A spermatogonia from Pou5f1-GFP reporter mice. Methods Mol Biol. 2012;825:31–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Geijsen N, Hochedlinger K. gPS navigates germ cells to pluripotency. Cell Stem Cell. 2009;5:3–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Gheorghisan-Galateanu AA, Hinescu ME, Enciu AM. Ovarian adult stem cells: hope or pitfall? J Ovarian Res. 2014;7:71.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Giuili G, Tomljenovic A, Labrecque N, Oulad-Abdelghani M, Rassoulzadegan M, Cuzin F. Murine spermatogonial stem cells: targeted transgene expression and purification in an active state. EMBO Rep. 2002;3:753–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Goel S, Fujihara M, Tsuchiya K, Takagi Y, Minami N, Yamada M, Imai H. Multipotential ability of primitive germ cells from neonatal pig testis cultured in vitro. Reprod Fertil Dev. 2009;21:696–708.

    Article  CAS  PubMed  Google Scholar 

  30. Goel S, Sugimoto M, Minami N, Yamada M, Kume S, Imai H. Identification, isolation, and in vitro culture of porcine gonocytes. Biol Reprod. 2007;77:127–37.

    Article  CAS  PubMed  Google Scholar 

  31. Habermann FA, Wuensch A, Sinowatz F, Wolf E. Reporter genes for embryogenesis research in livestock species. Theriogenology. 2007;68 Suppl 1:S116–24.

    Article  CAS  PubMed  Google Scholar 

  32. Hadjantonakis AK, Gertsenstein M, Ikawa M, Okabe M, Nagy A. Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech Dev. 1998;76:79–90.

    Article  CAS  PubMed  Google Scholar 

  33. Hall V. Porcine embryonic stem cells: a possible source for cell replacement therapy. Stem Cell Rev. 2008;4:275–82.

    Article  PubMed  Google Scholar 

  34. Hall VJ. Early development of the porcine embryo: the importance of cell signalling in development of pluripotent cell lines. Reprod Fertil Dev. 2012;25:94–102.

    Article  PubMed  Google Scholar 

  35. Hall VJ, Christensen J, Gao Y, Schmidt MH, Hyttel P. Porcine pluripotency cell signaling develops from the inner cell mass to the epiblast during early development. Dev Dyn. 2009;238:2014–24.

    Article  CAS  PubMed  Google Scholar 

  36. Hall VJ, Jacobsen JV, Rasmussen MA, Hyttel P. Ultrastructural and molecular distinctions between the porcine inner cell mass and epiblast reveal unique pluripotent cell states. Dev Dyn. 2010;239:2911–20.

    Article  CAS  PubMed  Google Scholar 

  37. Hammond SS, Martin A. Tools for the genetic analysis of germ cells. Genesis. 2009;47:617–27.

    Article  CAS  PubMed  Google Scholar 

  38. Han DW, Tapia N, Joo JY, Greber B, Araúzo-Bravo MJ, Bernemann C, Ko K, Wu G, Stehling M, Do JT, Schöler HR. Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell. 2010;143:617–27.

    Article  CAS  PubMed  Google Scholar 

  39. Hochereau-de Reviers MT, Perreau C. In vitro culture of embryonic disc cells from porcine blastocysts. Reprod Nutr Dev. 1993;33:475–83.

    Article  CAS  PubMed  Google Scholar 

  40. Irie N, Tang WW, Surani AM. Germ cell specification and pluripotency in mammals: a perspective from early embryogenesis. Reprod Med Biol. 2014;13:203–15.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, Tschudy KS, Tilly JC, Cortes ML, Forkert R, Spitzer T, Iacomini J, Scadden DT, Tilly JL. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122:303–15.

    Article  CAS  PubMed  Google Scholar 

  42. Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428:145–50. Erratum in: Nature. 2004;430:1062.

    Article  CAS  PubMed  Google Scholar 

  43. Kanatsu-Shinohara M, Lee J, Inoue K, Ogonuki N, Miki H, Toyokuni S, Ikawa M, Nakamura T, Ogura A, Shinohara T. Pluripotency of a single spermatogonial stem cell in mice. Biol Reprod. 2008;78:681–7.

    Article  CAS  PubMed  Google Scholar 

  44. Kanatsu-Shinohara M, Muneto T, Lee J, Takenaka M, Chuma S, Nakatsuji N, Horiuchi T, Shinohara T. Long-term culture of male germline stem cells from hamster testes. Biol Reprod. 2008;78:611–7.

    Article  CAS  PubMed  Google Scholar 

  45. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, Shinohara T. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod. 2003;69:612–6.

    Article  CAS  PubMed  Google Scholar 

  46. Keefer CL, Pant D, Blomberg L, Talbot NC. Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Anim Reprod Sci. 2007;98:147–68.

    Article  CAS  PubMed  Google Scholar 

  47. Kim HS, Son HY, Kim S, Lee GS, Park CH, Kang SK, Lee BC, Hwang WS, Lee CK. Isolation and initial culture of porcine inner cell masses derived from in vitro-produced blastocysts. Zygote. 2007;15:55–63.

    Article  CAS  PubMed  Google Scholar 

  48. Kim S, Kim JH, Lee E, Jeong YW, Hossein MS, Park SM, Park SW, Lee JY, Jeong YI, Kim HS, Kim YW, Hyun SH, Hwang WS. Establishment and characterization of embryonic stem-like cells from porcine somatic cell nuclear transfer blastocysts. Zygote. 2010;18:93–101.

    Article  CAS  PubMed  Google Scholar 

  49. King GJ, Atkinson BA, Robertson HA. Implantation and early placentation in domestic ungulates. J Reprod Fertil Suppl. 1981;31:17–30.

    Google Scholar 

  50. Knowles BB, Aden DP, Solter D. Monoclonal antibody detecting a stage-specific embryonic antigen (SSEA-1) on preimplantation mouse embryos and teratocarcinoma cells. Curr Top Microbiol Immunol. 1978;81:51–3.

    CAS  PubMed  Google Scholar 

  51. Ko K, Tapia N, Wu G, Kim JB, Bravo MJ, Sasse P, Glaser T, Ruau D, Han DW, Greber B, Hausdörfer K, Sebastiano V, Stehling M, Fleischmann BK, Brüstle O, Zenke M, Schöler HR. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell. 2009;5:87–96.

    Article  CAS  PubMed  Google Scholar 

  52. Kues WA, Niemann H. The contribution of farm animals to human health. Trends Biotechnol. 2004;22:286–94.

    Article  CAS  PubMed  Google Scholar 

  53. Kues WA, Herrmann D, Barg-Kues B, Haridoss S, Nowak-Imialek M, Buchholz T, Streeck M, Grebe A, Grabundzija I, Merkert S, Martin U, Hall VJ, Rasmussen MA, Ivics Z, Hyttel P, Niemann H. Derivation and characterization of sleeping beauty transposon-mediated porcine induced pluripotent stem cells. Stem Cells Dev. 2013;22:124–35.

    Article  CAS  PubMed  Google Scholar 

  54. Kuijk EW, Colenbrander B, Roelen BA. The effects of growth factors on in vitro-cultured porcine testicular cells. Reproduction. 2009;138:721–31.

    Article  CAS  PubMed  Google Scholar 

  55. Lee CK, Piedrahita JA. Effects of growth factors and feeder cells on porcine primordial germ cells in vitro. Cloning. 2000;2:197–205.

    Article  CAS  PubMed  Google Scholar 

  56. Lee H-J, Selesniemi K, Niikura Y, Niikura T, Klein R, Dombkowski DM, Tilly JL. Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure. J Clin Oncol. 2007;25:3198–204.

    Article  CAS  PubMed  Google Scholar 

  57. Leitch HG, Blair K, Mansfield W, Ayetey H, Humphreys P, Nichols J, Surani MA, Smith A. Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development. 2010;137:2279–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Li M, Zhang D, Hou Y, Jiao L, Zheng X, Wang WH. Isolation and culture of embryonic stem cells from porcine blastocysts. Mol Reprod Dev. 2003;65:429–34.

    Article  CAS  PubMed  Google Scholar 

  59. Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, Yan Y, Maxson RE, Schulze EN, Song H, Hsieh CL, Pera MF, Ying QL. Germline competent embryonic stem cells derived from rat blastocysts. Cell. 2008;135:1299–310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Luo J, Megee S, Rathi R, Dobrinski I. Protein gene product 9.5 is a spermatogonia-specific marker in the pig testis: application to enrichment and culture of porcine spermatogonia. Mol Reprod Dev. 2006;73:1531–40.

    Article  CAS  PubMed  Google Scholar 

  61. Martin G. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981;78:7634–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Matsui Y. Developmental fates of the mouse germ cell line. Int J Dev Biol. 1998;42:1037–42.

    CAS  PubMed  Google Scholar 

  63. 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 

  64. McClellan K, Gosden R, Taketo T. Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary. Dev Biol. 2003;258:334–48.

    Article  CAS  PubMed  Google Scholar 

  65. McLaren A. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol. 2000;163:3–9.

    Article  CAS  PubMed  Google Scholar 

  66. Miyoshi K, Taguchi Y, Sendai Y, Hoshi H, Sato E. Establishment of a porcine cell line from in vitro-produced blastocysts and transfer of the cells into enucleated oocytes. Biol Reprod. 2000;62:1640–6.

    Article  CAS  PubMed  Google Scholar 

  67. Montiel E, Guillomot M, Rojas M, Bustos-Obregón E, Flechon J. Primordial germ cell characterization by immunohistochemistry of vasa-homologue protein in preimplantational rabbit embryos. Int J Dev Biol. 2001;45(S1):141–2.

    Google Scholar 

  68. Moore H, Udayashankar R, Aflatoonian B. Stem cells for reproductive medicine. Mol Cell Endocrinol. 2008;288:104–10.

    Article  CAS  PubMed  Google Scholar 

  69. Mueller S, Prelle K, Rieger N, Petznek H, Lassnig C, Luksch U, Aigner B, Baetscher M, Wolf E, Mueller M, Brem G. Chimeric pigs following blastocyst injection of transgenic porcine primordial germ cells. Mol Reprod Dev. 1999;54:244–54.

    Article  CAS  PubMed  Google Scholar 

  70. Ng HH, Surani MA. The transcriptional and signalling networks of pluripotency. Nat Cell Biol. 2011;13:490–6.

    Article  CAS  PubMed  Google Scholar 

  71. Niemann H. Pigs as model systems for biomedical research. In: Rodriguez-Martinez H, Soede NM, Flowers WL, editors. Control of pig reproduction IX. Leicestershire: Context Products Ltd.; 2013. p. 267–86.

    Google Scholar 

  72. Notarianni E, Galli C, Laurie S, Moor RM, Evans MJ. Derivation of pluripotent, embryonic cell lines from the pig and sheep. J Reprod Fertil Suppl. 1991;43:255–60.

    CAS  PubMed  Google Scholar 

  73. Notarianni E, Laurie S, Moor RM, Evans MJ. Maintenance and differentiation in culture of pluripotential embryonic cell lines from pig blastocysts. J Reprod Fertil Suppl. 1990;41:51–6.

    CAS  PubMed  Google Scholar 

  74. Nowak-Imialek M, Kues WA, Petersen B, Lucas-Hahn A, Herrmann D, Haridoss S, Oropeza M, Lemme E, Schöler HR, Carnwath JW, Niemann H. Oct4-enhanced green fluorescent protein transgenic pigs: a new large animal model for reprogramming studies. Stem Cells Dev. 2011;20:1563–75.

    Article  CAS  PubMed  Google Scholar 

  75. Nowak-Imialek M, Kues WA, Rudolph C, Schlegelberger B, Taylor U, Carnwath JW, Niemann H. Preferential loss of porcine chromosomes in reprogrammed interspecies cell hybrids. Cell Reprogram. 2010;12:55–65.

    Article  CAS  PubMed  Google Scholar 

  76. Nowak-Imialek M, Niemann H. Pluripotent cells in farm animals: state of the art and future perspectives. Reprod Fertil Dev. 2012;25:103–28.

    Article  PubMed  Google Scholar 

  77. Ohinata Y, Payer B, O'Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature. 2005;436:207–13.

    Article  CAS  PubMed  Google Scholar 

  78. Ohinata Y, Sano M, Shigeta M, Yamanaka K, Saitou M. A comprehensive, non-invasive visualization of primordial germ cell development in mice by the Prdm1-mVenus and Dppa3-ECFP double transgenic reporter. Reproduction. 2008;136:503–14.

    Article  CAS  PubMed  Google Scholar 

  79. Ohmura M, Yoshida S, Ide Y, Nagamatsu G, Suda T, Ohbo K. Spatial analysis of germ stem cell development in Oct-4/EGFP transgenic mice. Arch Histol Cytol. 2004;67:285–96.

    Article  CAS  PubMed  Google Scholar 

  80. Pacchiarotti J, Maki C, Ramos T, Marh J, Howerton K, Wong J, Pham J, Anorve S, Chow YC, Izadyar F. Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation. 2010;79:159–70.

    Article  CAS  PubMed  Google Scholar 

  81. Pan Y. A new tool to generate transgenic rats using female germline stem cells from post-natal ovaries. Mol Hum Reprod. 2014;20:283–5.

    Article  PubMed  Google Scholar 

  82. Parte S, Bhartiya D, Telang J, Daithankar V, Salvi V, Zaveri K, Hinduja I. Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells Dev. 2011;20:1451–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Payer B, Chuva de Sousa Lopes SM, Barton SC, Lee C, Saitou M, Surani MA. Generation of stella-GFP transgenic mice: a novel tool to study germ cell development. Genesis. 2006;44:75–83.

    Article  CAS  PubMed  Google Scholar 

  84. Pesce M, Wang X, Wolgemuth DJ, Schöler H. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech Dev. 1998;71:89–98.

    Article  CAS  PubMed  Google Scholar 

  85. Petkov SG, Anderson GB. Culture of porcine embryonic germ cells in serum-supplemented and serum-free conditions: the effects of serum and growth factors on primary and long-term culture. Cloning Stem Cells. 2008;10:263–76.

    Article  CAS  PubMed  Google Scholar 

  86. Petkov SG, Marks H, Klein T, Garcia RS, Gao Y, Stunnenberg H, Hyttel P. In vitro culture and characterization of putative porcine embryonic germ cells derived from domestic breeds and Yucatan mini pig embryos at days 20–24 of gestation. Stem Cell Res. 2011;6:226–37.

    Article  CAS  PubMed  Google Scholar 

  87. Petkov SG, Reh WA, Anderson GB. Methylation changes in porcine primordial germ cells. Mol Reprod Dev. 2009;76:22–30. Erratum in: Mol Reprod Dev. 2009:76:522.

    Article  CAS  PubMed  Google Scholar 

  88. Petkov SG, Hyttel P, Niemann H. The small molecule inhibitors PD0325091 and CHIR99021 reduce expression of pluripotency-related genes in putative porcine induced pluripotent stem cells. Cell Reprogram. 2014;16:235–40.

    Article  CAS  PubMed  Google Scholar 

  89. Piedrahita JA, Anderson GB, Bondurant RH. Influence of feeder layer type on the efficiency of isolation of porcine embryo-derived cell lines. Theriogenology. 1990;34:865–77.

    Article  CAS  PubMed  Google Scholar 

  90. Piedrahita JA, Anderson GB, Bondurant RH. On the isolation of embryonic stem cells: comparative behavior of murine, porcine and ovine embryos. Theriogenology. 1990;34:879–901.

    Article  CAS  PubMed  Google Scholar 

  91. Piedrahita JA, Anderson GB, Martin GR, Bondurant RH, Pashen RL. Isolation of embryonic stem cell-like colonies from porcine embryos. Theriogenology. 1988;29:286.

    Article  Google Scholar 

  92. Piedrahita JA, Moore K, Oetama B, Lee CK, Scales N, Ramsoondar J, Bazer FW, Ott T. Generation of transgenic porcine chimeras using primordial germ cell-derived colonies. Biol Reprod. 1998;58:1321–9.

    Article  CAS  PubMed  Google Scholar 

  93. Prelle K, Zink N, Wolf E. Pluripotent stem cells—model of embryonic development, tool for gene targeting, and basis of cell therapy. Anat Histol Embryol. 2002;3:169–86.

    Article  Google Scholar 

  94. Rao M. Conserved and divergent paths that regulate self-renewal in mouse and human embryonic stem cells. Dev Biol. 2004;275:269–86.

    Article  CAS  PubMed  Google Scholar 

  95. Rui R, Qiu Y, Hu Y, Fan B. Establishment of porcine transgenic embryonic germ cell lines expressing enhanced green fluorescent protein. Theriogenology. 2006;65:713–20.

    Article  CAS  PubMed  Google Scholar 

  96. Rui R, Shim H, Moyer AL, Anderson DL, Penedo CT, Rowe JD, BonDurant RH, Anderson GB. Attempts to enhance production of porcine chimeras from embryonic germ cells and preimplantation embryos. Theriogenology. 2004;61:1225–35.

    Article  PubMed  Google Scholar 

  97. Shim H, Gutiérrez-Adán A, Chen LR, BonDurant RH, Behboodi E, Anderson GB. Isolation of pluripotent stem cells from cultured porcine primordial germ cells. Biol Reprod. 1997;57:1089–95.

    Article  CAS  PubMed  Google Scholar 

  98. Shim SW, Han DW, Yang JH, Lee BY, Kim SB, Shim H, Lee HT. Derivation of embryonic germ cells from post migratory primordial germ cells, and methylation analysis of their imprinted genes by bisulfite genomic sequencing. Mol Cells. 2008;25:358–67.

    CAS  PubMed  Google Scholar 

  99. Sommer JR, Jackson LR, Simpson SG, Collins EB, Piedrahita JA, Petters RM. Transgenic Stra8-EYFP pigs: a model for developing male germ cell technologies. Transgenic Res. 2012;21:383–92.

    Article  CAS  PubMed  Google Scholar 

  100. Stewart CL, Gadi I, Bhatt H. Stem cells from primordial germ cells can reenter the germ line. Dev Biol. 1994;161:626–8.

    Article  CAS  PubMed  Google Scholar 

  101. Strojek RM, Reed MA, Hoover JL, Wagner TE. A method for cultivating morphologically undifferentiated embryonic stem cells from porcine blastocysts. Theriogenology. 1990;33:901–13.

    Article  CAS  PubMed  Google Scholar 

  102. Suzuki H, Dann CT, Rajkovic A. Generation of a germ cell-specific mouse transgenic CHERRY reporter, Sohlh1-mCherryFlag. Genesis. 2013;51:50–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Talbot NC, Rexroad Jr CE, Pursel VG, Powell AM, Nel ND. Culturing the epiblast cells of the pig blastocyst. In Vitro Cell Dev Biol Anim. 1993;29A:543–54.

    Article  CAS  PubMed  Google Scholar 

  104. Tegelenbosch RA, de Rooij DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101F1 hybrid mouse. Mutat Res. 1993;290:193–200.

    Article  CAS  PubMed  Google Scholar 

  105. Telugu BP, Ezashi T, Roberts RM. The promise of stem cell research in pigs and other ungulate species. Stem Cell Rev. 2010;6:31–41.

    Article  PubMed  Google Scholar 

  106. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–7. Erratum in: Science. 282:1827.

    Article  CAS  PubMed  Google Scholar 

  107. Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA, Hearn JP. Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci U S A. 1995;92:7844–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Tsung HC, Du ZW, Rui R, Li XL, Bao LP, Wu J, Bao SM, Yao Z. The culture and establishment of embryonic germ (EG) cell lines from Chinese mini swine. Cell Res. 2003;13:195–202.

    Article  CAS  PubMed  Google Scholar 

  109. Vackova I, Madrova J. Porcine embryonic stem-like cells, an animal model for human stem cell therapy. Hum Reprod. 2006;21 Suppl 1:163.

    Article  Google Scholar 

  110. Vackova I, Ungrova A, Lopes F. Putative embryonic stem cell lines from pig embryos. J Reprod Dev. 2007;53:1137–49.

    Article  PubMed  Google Scholar 

  111. van Dissel-Emiliani FM, de Rooij DG, Meistrich ML. Isolation of rat gonocytes by velocity sedimentation at unit gravity. J Reprod Fertil. 1989;86:759–66.

    Article  PubMed  Google Scholar 

  112. Vassiliev I, Vassilieva S, Beebe LF, Harrison SJ, McIlfatrick SM, Nottle MB. In vitro and in vivo characterization of putative porcine embryonic stem cells. Cell Reprogram. 2010;12:223–30.

    Article  CAS  PubMed  Google Scholar 

  113. Vassiliev I, Vassilieva S, Beebe LF, McIlfatrick SM, Harrison SJ, Nottle MB. Development of culture conditions for the isolation of pluripotent porcine embryonal outgrowths from in vitro produced and in vivo derived embryos. J Reprod Dev. 2010;56:546–51.

    Article  CAS  PubMed  Google Scholar 

  114. Virant-Klun I, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P, Malicev E, Meden-Vrtovec H. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation. 2008;76:843–56.

    Article  CAS  PubMed  Google Scholar 

  115. Wheeler MB. Development and validation of swine embryonic stem cells: a review. Reprod Fertil Dev. 1994;6:563–8.

    Article  CAS  PubMed  Google Scholar 

  116. White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18:413–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Wianny F, Perreau C, Hochereau de Reviers MT. Proliferation and differentiation of porcine inner cell mass and epiblast in vitro. Biol Reprod. 1997;57:756–64.

    Article  CAS  PubMed  Google Scholar 

  118. Wolff EF, Libfraind LL, Weitzel P, Woods DC, Feng Y, Tilly JL, DeCherney AH, Tisdale JF. Oogonial stem cells generate mature oocytes in an autologous Rhesus macaque transplantation model. Reprod Sci. 2014;21(Suppl):119A.

    Google Scholar 

  119. Wu Z, Falciatori I, Molyneux LA, Richardson TE, Chapman KM, Hamra FK. Spermatogonial culture medium: an effective and efficient nutrient mixture for culturing rat spermatogonial stem cells. Biol Reprod. 2009;81:77–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Yeom YI, Fuhrmann G, Ovitt CE, Brehm A, Ohbo K, Gross M, Hübner K, Schöler HR. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development. 1996;122:881–94.

    CAS  PubMed  Google Scholar 

  121. Yin M, Fang Z, Jiang W, Xing F, Jiang M, Kong P, Li Y, Zhou X, Tang L, Li S, Chen X. The Oct4 promoter-EGFP transgenic rabbit: a new model for monitoring the pluripotency of rabbit stem cells. Int J Dev Biol. 2013;57:845–52.

    Article  CAS  PubMed  Google Scholar 

  122. Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, Yamamoto M, Suda T, Nabeshima Y. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol. 2004;269:447–58.

    Article  CAS  PubMed  Google Scholar 

  123. Yoshimizu T, Sugiyama N, De Felice M, Yeom YI, Ohbo K, Masuko K, Obinata M, Abe K, Schöler HR, Matsui Y. Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. Dev Growth Differ. 1999;41:675–84.

    Article  CAS  PubMed  Google Scholar 

  124. Youn H, Kim SH, Choi KA, Kim S. Characterization of Oct4-GFP spermatogonial stem cell line and its application in the reprogramming studies. J Cell Biochem. 2013;114:920–8.

    Article  CAS  PubMed  Google Scholar 

  125. Zheng Y, Tian X, Zhang Y, Qin J, An J, Zeng W. In vitro propagation of male germline stem cells from piglets. J Assist Reprod Genet. 2013;30:945–52.

    Article  PubMed  PubMed Central  Google Scholar 

  126. Zhou L, Wang L, Kang JX, Xie W, Li X, Wu C, Xu B, Wu J. Production of fat-1 transgenic rats using a post-natal female germline stem cell line. Mol Hum Reprod. 2014;20:271–81.

    Article  CAS  PubMed  Google Scholar 

  127. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, Small C, Griswold MD. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A-sufficient postnatal murine testes. Biol Reprod. 2008;79:35–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, Xiang J, Shi L, Yu Q, Zhang Y, Hou R, Wu J. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol. 2009;11:631–6.

    Article  CAS  PubMed  Google Scholar 

  129. Zuckerman S. The number of oocytes in the mature ovary. Recent Prog Horm Res. 1951;6:63–108.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heiner Niemann D.V.M., Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media New York

About this chapter

Cite this chapter

Nowak-Imialek, M., Niemann, H. (2016). Embryonic Stem Cells and Fetal Development Models. In: Fauza, D., Bani, M. (eds) Fetal Stem Cells in Regenerative Medicine. Stem Cell Biology and Regenerative Medicine. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3483-6_5

Download citation

Publish with us

Policies and ethics