BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Embryo-derived stem cells -a system is emerging

  • Binas, B. (Division of Molecular and Life Sciences, Hanyang University)
  • Published : 2009.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

In mammals, major progress has recently been made with the dissection of early embryonic cell specification, the isolation of stem cells from early embryos, and the production of embryonic-like stem cells from adult cells. These studies have overcome long-standing species barriers for stem cell isolation, have revealed a deeper than expected similarity of embryo cell types across species, and have led to a better understanding of the lineage identities of embryo-derived stem cells, most notably of mouse and human embryonic stem (ES) cells. Thus, it has now become possible to propose a species-overarching classification of embryo stem cells, which are defined here as pre- to early post-implantation conceptus-derived stem cell types that maintain embryonic lineage identities in vitro. The present article gives an overview of these cells and discusses their relationships with each other and the conceptus. Consequently, it is debated whether further embryo stem cell types await isolation, and the study of the earliest extraembryonically committed stem cells is identified as a promising new research field.

Keywords

References

  1. Gilbert, S. F. (2006) Developmental Biology, 8th ed., Sinauer Associates, Inc, Sunderland, Ma., USA
  2. Nagy, A., Gertsenstein, M., Vintersten, K. and Behringer, R. (2003) Manipulating the Mouse Embryo, 3rd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA
  3. Smith, A. G. (2006) A glossary for stem-cell biology. Nature 441, 1060 https://doi.org/10.1038/nature04954
  4. Jaenisch, R. and Young, R. (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132, 567-582 https://doi.org/10.1016/j.cell.2008.01.015
  5. Gurdon, J. B. and Melton, D. A. (2008) Nuclear reprogramming in cells. Science 322, 1811-1815 https://doi.org/10.1126/science.1160810
  6. Chazaud, C., Yamanaka, Y., Pawson, T. and Rossant, J. (2006) Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10, 615-624 https://doi.org/10.1016/j.devcel.2006.02.020
  7. Kurimoto, K., Yabuta, Y., Ohinata, Y., Ono, Y., Uno, K. D., Yamada, R. G., Ueda H. R. and Saitou M. (2006) An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res. 34, e42 https://doi.org/10.1093/nar/gkl050
  8. Plusa, B., Piliszek, A., Frankenberg, S., Artus, J. and Hadjantonakis, A.K. (2008) Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081-3091 https://doi.org/10.1242/dev.021519
  9. Gerbe, F., Cox, B., Rossant, J. and Chazaud, C. (2008) Dynamic expression of Lrp2 pathway members reveals progressive epithelial differentiation of primitive endoderm in mouse blastocyst. Dev. Biol. 313, 594-602 https://doi.org/10.1016/j.ydbio.2007.10.048
  10. Pelton, T. A., Sharma, S., Schulz, T. C., Rathjen, J. and Rathjen, P. D. (2002) Transient pluripotent cell populations during primitive ectoderm formation: correlation of in vivo and in vitro pluripotent cell development. J. Cell Sci. 115, 329-339
  11. Evans, M. J. and Kaufman, M. (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156 https://doi.org/10.1038/292154a0
  12. 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 https://doi.org/10.1073/pnas.78.12.7634
  13. Poueymirou, W. T., Auerbach, W., Frendewey, D., Hickey, J. F., Escaravage, J. M., Esau, L., Dore, A. T., Stevens, S., Adams, N. C., Dominguez, M. G., Gale, N. W., Yancopoulos, G. D., DeChiara, T. M. and Valenzuela, D, M. (2007) F0 generation mice fully derived from gene-targeted embryonic stem cells allowing immediate phenotypic analyses. Nat. Biotechnol. 25, 91-99 https://doi.org/10.1038/nbt1263
  14. Beddington, R. S. and Robertson, E. J. (1989) An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105, 733-737
  15. Doetschman, T. C., Eistetter, H., Katz, M., Schmidt, W. and Kemler, R. (1985) The in vitro development of blastocyst- derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87, 27-45
  16. Hamazaki, T., Oka, M., Yamanaka, S. and Terada, N. (2004) Aggregation of embryonic stem cells induces Nanog repression and primitive endoderm differentiation. J. Cell Sci. 117, 5681-5686 https://doi.org/10.1242/jcs.01489
  17. Schenke-Layland, K., Angelis, E., Rhodes, K. E., Heydarkhan-Hagvall, S., Mikkola, H. K. and Maclellan, W. R. (2007) Collagen IV induces trophoectoderm differentiation of mouse embryonic stem cells. Stem Cells 25, 1529-1538 https://doi.org/10.1634/stemcells.2006-0729
  18. Stewart, C. L., Kaspar, P., Brunet, L. J., Bhatt, H., Gadi, I., Kontgen, F. and Abbondanzo, S. J. (1992) Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76-79 https://doi.org/10.1038/359076a0
  19. Ware, C. B., Horowitz, M. C., Renshaw, B. R., Hunt, J. S., Liggit, D., Koblar, S. A., Gliniak, B. C., McKenna, H. J., Papayannopoulou, T., Thoma, B., Cheng, L., Donovan, P., Peschon, J., Bartlett, P., Willis, C., Wright, B., Carpenter, M., Davison, B. and Gearing, D. (1995). Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 121, 1283-1299
  20. Li, P., Tong, C., Mehrian-Shai, R., Jia, L., Wu, N., Yan, Y., Maxson, R. E., Schulze, E. N., Song, H., Hsieh, C. L., Pera, M. F. and Ying, Q. L. (2008) Germline competent embryonic stem cells derived from rat blastocysts. Cell 135,1299-1310 https://doi.org/10.1016/j.cell.2008.12.006
  21. Buehr, M., Meek, S., Blair, K., Yang, J., Ure, J., Silva, J., McLay, R., Hall, J., Ying, Q. L. and Smith, A. (2008) Capture of authentic embryonic stem cells from rat blastocysts. Cell 135, 1287-1298 https://doi.org/10.1016/j.cell.2008.12.007
  22. Gardner, R. L. and Brook, F. A. (1997) Reflections on the biology of embryonic stem (ES) cells. Int. J. Dev. Biol. 41, 235-243
  23. Evans, M. and Hunter, S. (2002) Source and nature of embryonic stem cells. C. R. Biol. 325, 1003-1007 https://doi.org/10.1016/S1631-0691(02)01527-5
  24. Brook, F. A. and Gardner, R. L. (1997) The origin and efficient derivation of embryonic stem cells in the mouse. Proc. Natl. Acad. Sci. U.S.A. 94, 5709-5712 https://doi.org/10.1073/pnas.94.11.5709
  25. Nichols, J., Chambers, I., Taga, T. and Smith, A. (2001) Physiological rationale for responsiveness of mouse embryonic stem cells to gp130 cytokines. Development 128, 2333-2339
  26. Rathjen, J., Lake, J. A., Bettess, M. D., Washington, J. M., Chapman, G. and Rathjen, P. D. (1999) Formation of a primitive ectoderm like cell population, EPL cells, from ES cells in response to biologically derived factors. J. Cell Sci. 112, 601-612
  27. Coucouvanis, E. and Martin, G. R. (1995) Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83, 279-287 https://doi.org/10.1016/0092-8674(95)90169-8
  28. 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 https://doi.org/10.1126/science.282.5391.1145
  29. 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 https://doi.org/10.1038/nature05950
  30. 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 https://doi.org/10.1038/nature05972
  31. Li, W., Wei, W., Zhu, S., Zhu, J., Shi, Y., Lin, T., Hao, E., Hayek, A., Deng, H. and Ding, S. (2009) Generation of rat and human induced pluripotent stem cells by combining genetic reprogramming and chemical inhibitors. Cell Stem Cell 4, 16-19 https://doi.org/10.1016/j.stem.2008.11.014
  32. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. and Rossant, J. (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075 https://doi.org/10.1126/science.282.5396.2072
  33. Buehr, M., Nichols, J., Stenhouse, F., Mountford, P., Greenhalgh, C. J., Kantachuvesiri, S., Brooker, G., Mullins, J. and Smith, A. G. (2003) Rapid loss of Oct-4 and pluripotency in cultured rodent blastocysts and derivative cell lines. Biol. Reprod. 68, 222-229 https://doi.org/10.1095/biolreprod.102.006197
  34. Takahashi, Y., Dominici, M., Swift, J., Nagy, C. and Ihle, J. N. (2006) Trophoblast stem cells rescue placental defect in SOCS3-deficient mice. J. Biol. Chem. 281, 11444-11445 https://doi.org/10.1074/jbc.C600015200
  35. Kunath, T., Arnaud, D., Uy, G. D., Okamoto, I., Chureau, C., Yamanaka, Y., Heard, E., Gardner, R. L., Avner, P. and Rossant, J. (2005) Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development 132, 1649-1661 https://doi.org/10.1242/dev.01715
  36. Tesar, P. J. (2005) Derivation of germ-line-competent embryonic stem cell lines from preblastocyst mouse embryos. Proc. Natl. Acad. Sci. U.S.A. 102, 8239-8244 https://doi.org/10.1073/pnas.0503231102
  37. Nagy, A., Gocza, E., Diaz, E. M., Prideaux, V.R., Ivanyi, E., Markkula, M. and Rossant, J. (1990) Embryonic stem cells alone are able to support fetal development in the mouse. Development 110, 815-821
  38. Hubner, K., Fuhrmann, G., Christenson, L. K., Kehler, J., Reinbold, R., de La Fuente, R., Wood, J., Strauss, J. F., 3rd, Boiani, M. and Sch$\"{o}$ler, H. R. (2003) Derivation of oocytes from mouse embryonic stem cells. Science 300, 1251-1256 https://doi.org/10.1126/science.1083452
  39. Dietrich, J. E. and Hiiragi, T. (2007) Stochastic patterning in the mouse pre-implantation embryo. Development 134, 4219-4231 https://doi.org/10.1242/dev.003798
  40. Strumpf, D., Mao, C.A., Yamanaka, Y., Ralston, A., Chawengsaksophak, K., Beck, F. and Rossant, J. (2005) Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093-2102 https://doi.org/10.1242/dev.01801
  41. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe- Nebenius, D., Chambers, I., Schöler, H. and Smith, A. (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391 https://doi.org/10.1016/S0092-8674(00)81769-9
  42. Niwa, H., Toyooka, Y., Shimosato, D., Strumpf, D., Takahashi, K., Yagi, R. and Rossant, J. (2005) Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123, 917-929 https://doi.org/10.1016/j.cell.2005.08.040
  43. 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 https://doi.org/10.1038/74199
  44. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M. and Yamanaka, S. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642 https://doi.org/10.1016/S0092-8674(03)00393-3
  45. Fujikura, J., Yamato, E., Yonemura, S., Hosoda, K., Masui, S., Nakao, K., Miyazaki, Ji, J. and Niwa, H. (2002) Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev. 16, 784-789 https://doi.org/10.1101/gad.968802
  46. Singh, A. M., Hamazaki, T., Hankowski, K. E. and Terada, N. (2007) A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25, 2534-2542 https://doi.org/10.1634/stemcells.2007-0126
  47. Graf, T. and Stadtfeld, M. (2008) Heterogeneity of embryonic and adult stem cells. Cell Stem Cell 3, 480-483 https://doi.org/10.1016/j.stem.2008.10.007
  48. Hattori, N., Nishino, K., Ko, Y. G., Hattori, N., Ohgane, J., Tanaka, S. and Shiota, K. (2004) Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. J. Biol. Chem. 279, 17063-17069 https://doi.org/10.1074/jbc.M309002200
  49. Hattori, N., Imao, Y., Nishino, K., Hattori, N., Ohgane, J., Yagi, S., Tanaka, S. and Shiota, K. (2007) Epigenetic regulation of Nanog gene in embryonic stem and trophoblast stem cells. Genes Cells 12, 387-396 https://doi.org/10.1111/j.1365-2443.2007.01058.x
  50. Fandrich, F., Lin, X., Chai, G. X., Schulze, M., Ganten, D., Bader, M., Holle, J., Huang, D. S., Parwaresch, R., Zavazava, N. and Binas, B. (2002) Preimplantation-stage stem cells induce long-term allogeneic graft acceptance without supplementary host conditioning. Nat. Med. 8, 171-178 https://doi.org/10.1038/nm0202-171
  51. Brenin, D., Look, J., Bader, M., Hubner, N., Levan, G. and Iannaccone, P. (1997) Rat embryonic stem cells: a progress report. Transplant Proc. 29, 1761-1765 https://doi.org/10.1016/S0041-1345(97)00046-8
  52. Chou, Y. F., Chen, H. H., Eijpe, M., Yabuuchi, A.,Chenoweth, J. G., Tesar, P., Lu, J., McKay, R. D. and Geijsen, N. (2008) The growth factor environment defines distinct pluripotent ground states in novel blastocystderived stem cells. Cell 135, 449-461 https://doi.org/10.1016/j.cell.2008.08.035
  53. Silva, J., Barrandon, O., Nichols, J., Kawaguchi, J., Theunissen, T. W. and Smith, A. (2008) Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 6, e253 https://doi.org/10.1371/journal.pbio.0060253

Cited by

  1. Average cell size is a factor reflecting the interaction of CHO cells during their proliferation vol.5, pp.6, 2011, https://doi.org/10.1134/S1990519X11060113