Derivation and Characterization of Rabbit Embryonic Stem Cells: A Review

  • Elen Gócza
  • Zsuzsanna Bősze

Abstract

In the first part of this chapter the different types of pluripotent stem cells are described in general: embryonal carcinoma cells, mouse and human embryonic stem cells, germ cells, epiblast stem cells and induced pluripotent cells. The methods used for isolation of rabbit embryonic stem like cells and rabbit primordial germ cells are detailed in the second part, including the species specific factors playing role in the maintenance of pluripotency. Detection of pluripotency markers both at mRNA and protein levels is an important tool in embryonic stem cell characterization. In vitro differentiation, teratoma formation and chimera forming ability are all inevitable tools to characterize embryonic stem cells. Finally the future potential of a truly validated widely available rabbit embryonic stem cell line is highlighted.

Keywords

Embryonic stem cells pluripotency chimera in vitro differentiation 

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References

  1. Amit M., Carpenter M. K., Inokuma M. S., Chiu C. P., Harris C. P., Waknitz M. A., Itskovitz-Eldor J. and Thomson J. A. (2000) Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 227, 271–278.PubMedCrossRefGoogle Scholar
  2. Besenfelder U. (1998) Generation and application of transgenic rabbits. In Microinjection and transgenesis: strategies and protocol, pp. 561–586. Springer Verlag, Berlin.Google Scholar
  3. Bodo S., Gocza E., Revay T., Hiripi L., Carstea B., Kovacs A., Bodrogi L. and Bosze Z. (2004) Production of transgenic chimeric rabbits and transmission of the transgene through the germ-line. Mol Reprod Dev 68, 435–440.PubMedCrossRefGoogle Scholar
  4. Bosze Z. and Houdebine L. -M. (2006) Application of rabbits in biomedical research: a review. World Rabbit Sci 14, 1–14.Google Scholar
  5. Bradley A., Evans M., Kaufman M. H. and Robertson E. (1984) Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309, 255–256.PubMedCrossRefGoogle Scholar
  6. Brandenberger R., Wei H., Zhang S., Lei S., Murage J., Fisk G. J., Li Y., Xu C., Fang R., Guegler K., Rao M. S., Mandalam R., Lebkowski J. and Stanton L. W. (2004) Transcriptome characterization elucidates signaling networks that control human ES cell growth and differentiation. Nat Biotechnol 22, 707–716.PubMedCrossRefGoogle Scholar
  7. Brevini T. A., Antonini S., Cillo F., Crestan M. and Gandolfi F. (2007a) Porcine embryonic stem cells: facts, challenges and hopes. Theriogenology 68 Suppl 1, S206–213.CrossRefGoogle Scholar
  8. Brevini T. A., Tosetti V., Crestan M., Antonini S. and Gandolfi F. (2007b) Derivation and characterization of pluripotent cell lines from pig embryos of different origins. Theriogenology 67, 54–63.CrossRefGoogle Scholar
  9. Brevini T., Antonini S., Pennerossa G. and Gandolfi F. (2008) Recent progress in embryonic stem cell research and its application in domestic species. Reprod Domest Anim 43, 193–199.PubMedCrossRefGoogle Scholar
  10. Brinster R. L. (1974) The effect of cells transferred into the mouse blastocyst on subsequent development. J Exp Med 140, 1049–1056.PubMedCrossRefGoogle Scholar
  11. Brons I. G., Smithers L. E., Trotter M. W., Rugg-Gunn P., Sun B., Chuva de Sousa Lopes S. M., Howlett S. K., Clarkson A., Ahrlund-Richter L., Pedersen R. A. and Vallier L. (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191–195.PubMedCrossRefGoogle Scholar
  12. Catunda A. P., Gocza E., Carstea B. V., Hiripi L., Hayes H., Rogel-Gaillard C., Bertaud M. and Bosze Z. (2008) Characterization, Chromosomal Assignment, and Role of LIFR in Early Embryogenesis and Stem Cell Establishment of Rabbits. Cloning Stem Cells 10, 523–534.PubMedCrossRefGoogle Scholar
  13. Chen Y., He Z. X., Liu A., Wang K., Mao W. W., Chu J. X., Lu Y., Fang Z. F., Shi Y. T., Yang Q. Z., Chen da Y., Wang M. K., Li J. S., Huang S. L., Kong X. Y., Shi Y. Z., Wang Z. Q., Xia J. H., Long Z. G., Xue Z. G., Ding W. X. and Sheng H. Z. (2003) Embryonic stem cells generated by nuclear transfer of human somatic nuclei into rabbit oocytes. Cell Res 13, 251–263.PubMedCrossRefGoogle Scholar
  14. Choo A., Padmanabhan J., Chin A., Fong W. J. and Oh S. K. (2006) Immortalized feeders for the scale-up of human embryonic stem cells in feeder and feeder-free conditions. J Biotechnol 122, 130–141.PubMedCrossRefGoogle Scholar
  15. Cole R. J., Edwards R. G., and Paul J. (1966) Cytodifferentiation and embryogenesis in cell colonies and tissue cultures derived from ova and blastocyst of the rabbit. Dev Biol 13, 385–407.PubMedCrossRefGoogle Scholar
  16. Daheron L., Opitz S. L., Zaehres H., Lensch W. M., Andrews P. W., Itskovitz-Eldor J. and Daley G. Q. (2004) LIF/STAT3 signaling fails to maintain self-renewal of human embryonic stem cells. Stem Cells 22, 770–778.PubMedCrossRefGoogle Scholar
  17. Demers S. P., Yoo J. G., Lian L., Therrien J. and Smith L. C. (2007) Rat embryonic stem-like (ES-like) cells can contribute to extraembryonic tissues in vivo. Cloning Stem Cells 9, 512–522.PubMedCrossRefGoogle Scholar
  18. Doetschman T., Gregg R. G., Maeda N., Hooper M. L., Melton D. W., Thompson S. and Smithies O. (1987) Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 330, 576–578.PubMedCrossRefGoogle Scholar
  19. Du F., Giles J. R., Foote R. H., Graves K. H., Yang X. and Moreadith R. W. (1995) Nuclear transfer of putative rabbit embryonic stem cells leads to normal blastocyst development. J Reprod Fertil 104, 219–223.PubMedGoogle Scholar
  20. Evans M. J. and Kaufman M. H. (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154–156.PubMedCrossRefGoogle Scholar
  21. Fang Z. F., Gai H., Huang Y. Z., Li S. G., Chen X. J., Shi J. J., Wu L., Liu A., Xu P. and Sheng H. Z. (2006) Rabbit embryonic stem cell lines derived from fertilized, parthenogenetic or somatic cell nuclear transfer embryos. Exp Cell Res 312, 3669–3682.PubMedCrossRefGoogle Scholar
  22. Ginis I., Luo Y., Miura T., Thies S., Brandenberger R., Gerecht-Nir S., Amit M., Hoke A., Carpenter M. K., Itskovitz-Eldor J. and Rao M. S. (2004) Differences between human and mouse embryonic stem cells. Dev Biol 269, 360–380.PubMedCrossRefGoogle Scholar
  23. Graves K. H. and Moreadith R. W. (1993) Derivation and characterization of putative pluripo-tential embryonic stem cells from preimplantation rabbit embryos. Mol Reprod Dev 36, 424–433.PubMedCrossRefGoogle Scholar
  24. Guan K., Nayernia K., Maier L. S., Wagner S., Dressel R., Lee J. H., Nolte J., Wolf F., Li M., Engel W. and Hasenfuss G. (2006) Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440, 1199–1203.PubMedCrossRefGoogle Scholar
  25. He S., Pant D., Schiffmacher A., Bischoff S., Melican D., Gavin W. and Keefer C. (2006) Developmental expression of pluripotency determining factors in caprine embryos: novel pattern of NANOG protein localization in the nucleolus. Mol Reprod Dev 73, 1512–1522.PubMedCrossRefGoogle Scholar
  26. Hiripi L., Makovics F., Halter R., Baranyi M., Paul D., Carnwath J. W., Bosze Z. and Niemann H. (2003) Expression of active human blood clotting factor VIII in mammary gland of transgenic rabbits. DNA Cell Biol 22, 41–45.PubMedCrossRefGoogle Scholar
  27. Hogan B., Fellous M., Avner P. and Jacob F. (1977) Isolation of a human teratoma cell line which expresses F9 antigen. Nature 270, 515–518.PubMedCrossRefGoogle Scholar
  28. Honda A., Hirose M., Inoue K., Ogonuki N., Miki H., Shimozawa N., Hatori M., Shimizu N., Murata T., Hirose M., Katayama K., Wakisaka N., Miyoshi H., Yokoyama K. K., Sankai T. and Ogura A. (2008) Stable embryonic stem cell lines in rabbits: potential small animal models for human research. Reprod Biomed Online 17, 706–715.PubMedCrossRefGoogle Scholar
  29. Humphrey R. K., Beattie G. M., Lopez A. D., Bucay N., King C. C., Firpo M. T., Rose-John S. and Hayek A. (2004) Maintenance of pluripotency in human embryonic stem cells is STAT3 independent. Stem Cells 22, 522–530.PubMedCrossRefGoogle Scholar
  30. Jin D. I., Kim D. K., Im K. S. and Choi W. S. (2000) Successful pregnancy after transfer of rabbit blastocysts grown in vitro from single-cell zygotes. Theriogenology 54, 1109–1116.PubMedCrossRefGoogle Scholar
  31. Kahan B. W. and Ephrussi B. (1970) Developmental potentialities of clonal in vitro cultures of mouse testicular teratoma. J Natl Cancer Inst 44, 1015–1036.PubMedGoogle Scholar
  32. Kakegawa R., Teramura T., Takehara T., Anzai M., Mitani T., Matsumoto K., Saeki K., Sagawa N., Fukuda K. and Hosoi Y. (2008) Isolation and culture of rabbit primordial germ cells. J Reprod Dev 54, 352–357.PubMedCrossRefGoogle Scholar
  33. Kanatsu-Shinohara M., Inoue K., Lee J., Yoshimoto M., Ogonuki N., Miki H., Baba S., Kato T., Kazuki Y., Toyokuni S., Toyoshima M., Niwa O., Oshimura M., Heike T., Nakahata T., Ishino F., Ogura A. and Shinohara T. (2004) Generation of pluripotent stem cells from neonatal mouse testis. Cell 119, 1001–1012.PubMedCrossRefGoogle Scholar
  34. Keefer C. L., Pant D., Blomberg L. and Talbot N. C. (2007) Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Anim Reprod Sci 98, 147–168.PubMedCrossRefGoogle Scholar
  35. Kirchhof N., Carnwath J. W., Lemme E., Anastassiadis K., Scholer H. and Niemann H. (2000) Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 63, 1698–1705.PubMedCrossRefGoogle Scholar
  36. Kleinsmith L. J. and Pierce G. B., Jr. (1964) Multipotentiality of single embryonal carcinoma cells. Cancer Res 24, 1544–1551.PubMedGoogle Scholar
  37. Koestenbauer S., Zech N. H., Juch H., Vanderzwalmen P., Schoonjans L. and Dohr G. (2006) Embryonic stem cells: similarities and differences between human and murine embryonic stem cells. Am J Reprod Immunol 55, 169–180.PubMedCrossRefGoogle Scholar
  38. Labosky P. A., Barlow D. P. and Hogan B. L. (1994) Mouse embryonic germ (EG) cell lines: transmission through the germline and differences in the methylation imprint of insulinlike growth factor 2 receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. Development 120, 3197–3204.PubMedGoogle Scholar
  39. Laslett A. L., Filipczyk A. A. and Pera M. F. (2003) Characterization and culture of human embryonic stem cells. Trends Cardiovasc Med 13, 295–301.PubMedCrossRefGoogle Scholar
  40. Lerou P. H., Yabuuchi A., Huo H., Takeuchi A., Shea J., Cimini T., Ince T. A., Ginsburg E., Racowsky C. and Daley G. Q. (2008) Human embryonic stem cell derivation from poor-quality embryos. Nat Biotechnol 26, 212–214.PubMedCrossRefGoogle Scholar
  41. Levenstein M. E., Ludwig T. E., Xu R. H., Llanas R. A., VanDenHeuvel-Kramer K., Manning D. and Thomson J. A. (2006) Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells 24, 568–574.PubMedCrossRefGoogle Scholar
  42. Li C., Yang Y., Gu J., Ma Y. and Jin Y. (2008) Derivation and transcriptional profiling analysis of pluripotent stem cell lines from rat blastocysts. Cell Res 19, 173–186.CrossRefGoogle Scholar
  43. Li T., Wang S., Xie Y., Lu Y., Zhang X., Wang L., Yang S., Wolf D., Zhou Q. and Ji W. (2005) Homologous feeder cells support undifferentiated growth and pluripotency in monkey embryonic stem cells. Stem Cells 23, 1192–1199.PubMedCrossRefGoogle Scholar
  44. Lowry N., Goderie S. K., Adamo M., Lederman P., Charniga C., Gill J., Silver J. and Temple S. (2008) Multipotent embryonic spinal cord stem cells expanded by endothelial factors and Shh/ RA promote functional recovery after spinal cord injury. Exp Neurol 209, 510–522.PubMedCrossRefGoogle Scholar
  45. Ludwig T. E., Levenstein M. E., Jones J. M., Berggren W. T., Mitchen E. R., Frane J. L., Crandall L. J., Daigh C. A., Conard K. R., Piekarczyk M. S., Llanas R. A. and Thomson J. A. (2006) Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24, 185–187.PubMedCrossRefGoogle Scholar
  46. Maherali N., Sridharan R., Xie W., Utikal J., Eminli S., Arnold K., Stadtfeld M., Yachechko R., Tchieu J., Jaenisch R., Plath K. and Hochedlinger K. (2007) Directly reprogrammed fibrob-lasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1, 55–70.PubMedCrossRefGoogle Scholar
  47. Martin G. R. (1981) 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 78, 7634–7638.PubMedCrossRefGoogle Scholar
  48. Matsui Y., Zsebo K. and Hogan B. L. (1992) Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70, 841–847.PubMedCrossRefGoogle Scholar
  49. Moore K. and Piedrahita J. A. (1997) The effects of human leukemia inhibitory factor (hLIF) and culture medium on in vitro differentiation of cultured porcine inner cell mass (pICM). In Vitro Cell Dev Biol Anim 33, 62–71.PubMedCrossRefGoogle Scholar
  50. Niwa H., Miyazaki J. and Smith A. G. (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24, 372–376.PubMedCrossRefGoogle Scholar
  51. Notarianni E., Galli C., Laurie S., Moor R. M. and Evans M. J. (1991) Derivation of pluripotent, embryonic cell lines from the pig and sheep. J Reprod Fertil Suppl 43, 255–260.PubMedGoogle Scholar
  52. Oka M., Tagoku K., Russell T. L., Nakano Y., Hamazaki T., Meyer E. M., Yokota T. and Terada N. (2002) CD9 is associated with leukemia inhibitory factor-mediated maintenance of embryonic stem cells. Mol Biol Cell 13, 1274–1281.PubMedCrossRefGoogle Scholar
  53. Okita K., Ichisaka T. and Yamanaka S. (2007) Generation of germline-competent induced pluri-potent stem cells. Nature 448, 313–317.PubMedCrossRefGoogle Scholar
  54. Pant D. and Keefer C. (2006) Gene expression in cultures of inner cell masses isolated from in vitro produced and in vivo derived bovine blastocysts. Reprod Fertil Dev 18, 110–110.CrossRefGoogle Scholar
  55. Park I. H., Arora N., Huo H., Maherali N., Ahfeldt T., Shimamura A., Lensch M. W., Cowan C., Hochedlinger K. and Daley G. Q. (2008) Disease-specific induced pluripotent stem cells. Cell 134, 877–886.PubMedCrossRefGoogle Scholar
  56. Pesce M. and Scholer H. R. (2001) Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 19, 271–278.PubMedCrossRefGoogle Scholar
  57. Piedrahita J. A., Anderson G. B. and Bondurant R. H. (1990a) Influence of feeder layer type on the efficiency of isolation of porcine embryo-derived cell lines. Theriogenology 34, 865–877.CrossRefGoogle Scholar
  58. Piedrahita J. A., Anderson G. B. and Bondurant R. H. (1990b) On the isolation of embryonic stem cells: comparative behavior of murine, porcine and ovine embryos. Theriogenology 34, 879–901.CrossRefGoogle Scholar
  59. Rao B. M. and Zandstra P. W. (2005) Culture development for human embryonic stem cell propagation: molecular aspects and challenges. Curr Opin Biotechnol 16, 568–576.PubMedCrossRefGoogle Scholar
  60. Raz R., Lee C. K., Cannizzaro L. A., d'Eustachio P. and Levy D. E. (1999) Essential role of STAT3 for embryonic stem cell pluripotency. Proc Natl Acad Sci U S A 96, 2846–2851.PubMedCrossRefGoogle Scholar
  61. Resnick J. L., Bixler L. S., Cheng L. and Donovan P. J. (1992) Long-term proliferation of mouse primordial germ cells in culture. Nature 359, 550–551.PubMedCrossRefGoogle Scholar
  62. Rossant J. (2008) Stem cells and early lineage development. Cell 132, 527–531.PubMedCrossRefGoogle Scholar
  63. Schoonjans L., Albright G. M., Li J. L., Collen D. and Moreadith R. W. (1996) Pluripotential rabbit embryonic stem (ES) cells are capable of forming overt coat color chimeras following injection into blastocysts. Mol Reprod Dev 45, 439–443.PubMedCrossRefGoogle Scholar
  64. Shamblott M. J., Axelman J., Wang S., Bugg E. M., Littlefield J. W., Donovan P. J., Blumenthal P. D., Huggins G. R. and Gearhart J. D. (1998) Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci U S A 95, 13726–13731.PubMedCrossRefGoogle Scholar
  65. Shiomi M. and Fan J. (2008) Unstable coronary plaques and cardiac events in myocardial infarction-prone Watanabe heritable hyperlipidemic rabbits: questions and quandaries. Curr Opin Lipidol 19, 631–636.PubMedCrossRefGoogle Scholar
  66. Stacey G. N., Cobo F., Nieto A., Talavera P., Healy L. and Concha A. (2006) The development of ‘feeder’ cells for the preparation of clinical grade hES cell lines: challenges and solutions. J Biotechnol 125, 583–588.PubMedCrossRefGoogle Scholar
  67. Steer H. W. (1970) The trophoblastic knobs of the preimplanted rabbit blastocyst: a light and electron microscopic study. J Anat 107, 315–325.PubMedGoogle Scholar
  68. Stewart C. L. (1994) Leukaemia inhibitory factor and the regulation of pre-implantation development of the mammalian embryo. Mol Reprod Dev 39, 233–238.PubMedCrossRefGoogle Scholar
  69. Sumi T., Fujimoto Y., Nakatsuji N. and Suemori H. (2004) STAT3 is dispensable for maintenance of self-renewal in nonhuman primate embryonic stem cells. Stem Cells 22, 861–872.PubMedCrossRefGoogle Scholar
  70. Takahashi K. and Yamanaka S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676.PubMedCrossRefGoogle Scholar
  71. Talbot N. C., Rexroad C. E., Jr., Pursel V. G., Powell A. M. and Nel N. D. (1993) Culturing the epiblast cells of the pig blastocyst. In Vitro Cell Dev Biol Anim 29A, 543–554.PubMedCrossRefGoogle Scholar
  72. Talbot N. C., Powell A. M. and Rexroad C. E., Jr. (1995) In vitro pluripotency of epiblasts derived from bovine blastocysts. Mol Reprod Dev 42, 35–52.PubMedCrossRefGoogle Scholar
  73. Talbot N. C., Powell A. M. and Garrett W. M. (2002) Spontaneous differentiation of porcine and bovine embryonic stem cells (epiblast) into astrocytes or neurons. In Vitro Cell Dev Biol Anim 38, 191–197.PubMedCrossRefGoogle Scholar
  74. Tesar P. J., Chenoweth J. G., Brook F. A., Davies T. J., Evans E. P., Mack D. L., Gardner R. L. and McKay R. D. (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196–199.PubMedCrossRefGoogle Scholar
  75. Thomas K. R. and Capecchi M. R. (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503–512.PubMedCrossRefGoogle Scholar
  76. Thomson J. A., Kalishman J., Golos T. G., Durning M., Harris C. P., Becker R. A. and Hearn J. P. (1995) Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci U S A 92, 7844–7848.PubMedCrossRefGoogle Scholar
  77. Thomson J. A., Kalishman J., Golos T. G., Durning M., Harris C. P. and Hearn J. P. (1996) Pluripotent cell lines derived from common marmoset (Callithrix jacchus) blastocysts. Biol Reprod 55, 254–259.PubMedCrossRefGoogle Scholar
  78. Thomson J. A., Itskovitz-Eldor J., Shapiro S. S., Waknitz M. A., Swiergiel J. J., Marshall V. S. and Jones J. M. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282, 1145–1147.PubMedCrossRefGoogle Scholar
  79. Turnpenny L., Brickwood S., Spalluto C. M., Piper K., Cameron I. T., Wilson D. I. and Hanley N. A. (2003) Derivation of human embryonic germ cells: an alternative source of pluripotent stem cells. Stem Cells 21, 598–609.PubMedCrossRefGoogle Scholar
  80. van de Lavoir M. C., Diamond J. H., Leighton P. A., Mather-Love C., Heyer B. S., Bradshaw R., Kerchner A., Hooi L. T., Gessaro T. M., Swanberg S. E., Delany M. E. and Etches R. J. (2006) Germline transmission of genetically modified primordial germ cells. Nature 441, 766–769.PubMedCrossRefGoogle Scholar
  81. van Eijk M. J., van Rooijen M. A., Modina S., Scesi L., Folkers G., van Tol H. T., Bevers M. M., Fisher S. R., Lewin H. A., Rakacolli D., Galli C., de Vaureix C., Trounson A. O., Mummery C. L. and Gandolfi F. (1999) Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol Reprod 60, 1093–1103.PubMedCrossRefGoogle Scholar
  82. Vassilieva S., Guan K., Pich U. and Wobus A. (2000) Establishment of SSEA-1- and Oct-4-expressing rat embryonic stem-like cell lines and effects of cytokines of the IL-6 family on clonal growth. Exp Cell Res 258, 361–373.PubMedCrossRefGoogle Scholar
  83. Wang S., Tang X., Niu Y., Chen H., Li B., Li T., Zhang X., Hu Z., Zhou Q. and Ji W. (2007) Generation and characterization of rabbit embryonic stem cells. Stem Cells 25, 481–489.PubMedCrossRefGoogle Scholar
  84. Wernig M., Meissner A., Foreman R., Brambrink T., Ku M., Hochedlinger K., Bernstein B. E. and Jaenisch R. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448, 318–324.PubMedCrossRefGoogle Scholar
  85. Wheeler M. (1994) Development and validation of swine embryonic stem cells: a review. Reprod Fertil Dev 6, 563–568.PubMedCrossRefGoogle Scholar
  86. Wobus A. M. and Boheler K. R. (2005) Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 85, 635–678.PubMedCrossRefGoogle Scholar
  87. Xu R. H., Peck R. M., Li D. S., Feng X., Ludwig T. and Thomson J. A. (2005) Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Meth 2, 185–190.CrossRefGoogle Scholar
  88. Yamagata K., Nakanishi T., Ikawa M., Yamaguchi R., Moss S. B. and Okabe M. (2002) Sperm from the calmegin-deficient mouse have normal abilities for binding and fusion to the egg plasma membrane. Dev Biol 250, 348–357.PubMedGoogle Scholar
  89. Yu J. and Thomson J. A. (2008) Pluripotent stem cell lines. Genes Dev 22, 1987–1997.PubMedCrossRefGoogle Scholar
  90. Yu J., Vodyanik M. A., He P., Slukvin, II and Thomson J. A. (2006) Human embryonic stem cells reprogram myeloid precursors following cell-cell fusion. Stem Cells 24, 168–176.PubMedCrossRefGoogle Scholar
  91. Yu J., Vodyanik M. A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J. L., Tian S., Nie J., Jonsdottir G. A., Ruotti V., Stewart R., Slukvin, II and Thomson J. A. (2007) Induced pluri-potent stem cell lines derived from human somatic cells. Science 318, 1917–1920.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media B.V. 2009

Authors and Affiliations

  • Elen Gócza
    • 1
  • Zsuzsanna Bősze
    • 1
  1. 1.Agricultural Biotechnology CenterHungary

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