Switching on pluripotency: A perspective on the biological requirement of Nanog

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1575, 2011, Pages 2222-2229

  Theunissen, Thorold W ^a   Silva, José C R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

ES cells; IPS cells; Molecular evolution; Nanog; Pluripotency; Reprogramming

Indexed keywords

HOMEODOMAIN PROTEIN;

CYTOLOGY; EMBRYONIC DEVELOPMENT; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; MOLECULAR ANALYSIS;

ANIMAL; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; REVIEW;

ANIMALS; BIOLOGICAL EVOLUTION; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; MUTATION;

MAMMALIA;

EID: 79960069606     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0003     Document Type: Review

References (61)

1. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. & Smith, A. 2003 Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643-655. (doi:10.1016/S0092-8674(03)00392-1)
2. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M. i, Maeda, M. & Yamanaka, S. 2003 The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642. (doi:10.1016/S0092-8674(03)00393-3)
3. Ying, Q. L., Nichols, J., Chambers, I. & Smith, A. 2003 BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292. (doi:10.1016/ S0092-8674(03)00847-X)
4. Hatano, S. Y., Tada, M., Kimura, H., Yamaguchi, S., Kono, T., Nakano, T., Suemori, H., Nakatsuji, N. & Tada, T. 2005 Pluripotential competence of cells associated with Nanog activity. Mech. Dev. 122, 67-79. (doi:10.1016/j.mod.2004.08.008)
5. Ivanova, N., Dobrin, R., Lu, R., Kotenko, I., Levorse, J., DeCoste, C., Schafer, X., Lun, Y. & Lemischka, I. R. 2006 Dissecting self-renewal in stem cells with RNA interference. Nature 442, 533-538. (doi:10.1038/ nature04915)
6. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Schöler, H. & Smith, A. 1998 Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391. (doi:10.1016/S0092-8674(00)81769-9)
7. Avilion, A. A., Nicolis, S. K., Pevny, L. H., Perez, L., Vivian, N. & Lovell-Badge, R. 2003 Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126-140. (doi:10.1101/gad.224503)
8. Chambers, I. et al. 2007 Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234. (doi:10.1038/nature06403)
9. Wang, J., Theunissen, T. W. & Orkin, S. H. 2007 Site-directed, virus-free, and inducible RNAi in embryonic stem cells. Proc. Natl Acad. Sci. USA 104, 20 850-20855. (doi:10.1073/pnas.0710565105) 10
10. Chazaud, C., Yamanaka, Y., Pawson, T. & Rossant, J. 2006 Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10, 615-624. (doi:10. 1016/j.devcel.2006.02.020)
11. Kurimoto, K., Yabuta, Y., Ohinata, Y., Ono, Y., Uno, K. D., Yamada, R. G., Ueda, H. R. & Saitou, M. 2006 An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res. 34, e42. (doi:10.1093/nar/ gkl050)
12. Silva, J. et al. 2009 Nanog is the gateway to the pluripotent ground state. Cell 138, 722-737. (doi:10.1016/j.cell.2009.07.039)
13. Silva, J. et al. 2003 Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev. Cell 4, 481-495. (doi:10.1016/S1534-5807(03)00068-6)
14. 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. USA 78, 7634-7638. (doi:10.1073/pnas.78.12.7634)
15. Rastan, S. & Robertson, E. J. 1985 X-chromosome deletions in embryo-derived (EK) cell lines associated with lack of X-chromosome inactivation. J. Embryol. Exp. Morphol. 90, 379-388.
16. Navarro, P., Chambers, I., Karwacki-Neisius, V., Chureau, C., Morey, C., Rougeulle, C. & Avner, P. 2008 Molecular coupling of Xist regulation and pluripotency. Science 321, 1693-1695. (doi:10.1126/science.1160952)
17. Navarro, P. & Avner, P. 2009 When X-inactivation meets pluripotency: an intimate rendezvous. FEBS Lett. 583, 1721-1727. (doi:10.1016/j.febslet.2009.03.043)
18. Nichols, J., Silva, J., Roode, M. & Smith, A. 2009 Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136, 3215-3222. (doi:10.1242/dev.038893)
19. Messerschmidt, D. M. & Kemler, R. 2010 Nanog is required for primitive endoderm formation through a non-cell autonomous mechanism. Dev. Biol. 344, 129-137. (doi:10.1016/j.ydbio.2010.04.020)
20. Yamanaka, Y., Lanner, F. & Rossant, J. 2010 FGF signaldependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137, 715-724. (doi:10.1242/dev.043471)
21. Kunath, T., Saba-El-Leil, M. K., Almousailleakh, M., Wray, J., Meloche, S. & Smith, A. 2007 FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134, 2895-2902. (doi:10.1242/dev.02880)
22. Silva, J., Barrandon, O., Nichols, J., Kawaguchi, J., Theunissen, T.W. & Smith, A. 2008 Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 6, e253. (doi:10.1371/journal. pbio.0060253)
23. Yamaguchi, S., Kimura, H., Tada, M., Nakatsuji, N. & Tada, T. 2005 Nanog expression in mouse germ cell development. Gene Exp. Patterns 5, 639-646. (doi:10.1016/j.modgep.2005.03.001)
24. Surani, M. A., Hayashi, K. & Hajkova, P. 2007 Genetic and epigenetic regulators of pluripotency. Cell 128, 747-762. (doi:10.1016/j.cell.2007.02.010)
25. Yamaguchi, S., Kurimoto, K., Yabuta, Y., Sasaki, H., Nakatsuji, N., Saitou, M. & Tada, T. 2009 Conditional knockdown of Nanog induces apoptotic cell death in mouse migrating primordial germ cells. Development 136, 4011-4020. (doi:10.1242/dev.041160)
26. Hart, A. H., Hartley, L., Ibrahim, M. & Robb, L. 2004 Identification, cloning and expression analysis of the pluripotency promoting Nanog genes in mouse and human. Dev. Dyn. 230, 187-198. (doi:10.1002/dvdy.20034)
27. Monk, M. & McLaren, A. 1981 X-chromosome activity in foetal germ cells of the mouse. J. Embryol. Exp. Morphol. 63, 75-84.
28. Reik, W., Dean, W. & Walter, J. 2001 Epigenetic reprogramming in mammalian development. Science 293, 1089-1093. (doi:10.1126/science.1063443)
29. Takahashi, K. & Yamanaka, S. 2006 Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676. (doi:10.1016/j.cell.2006.07.024)
30. Silva, J., Chambers, I., Pollard, S. & Smith, A. 2006 Nanog promotes transfer of pluripotency after cell fusion. Nature 441, 997-1001. (doi:10.1038/nature 04914)
31. Okita, K., Ichisaka, T. & Yamanaka, S. 2007 Generation of germline-competent induced pluripotent stem cells. Nature 448, 313-317. (doi:10.1038/nature05934)
32. Wernig, M., Meissner, A., Foreman, R., Brambrink, T., Ku, M., Hochedlinger, K., Bernstein, B. E.& Jaenisch, R. 2007 In vitro reprogramming of fibroblasts into a pluripotent EScell- like state. Nature 448, 318-324. (doi:10.1038/ nature05944)
33. Yu, J. et al. 2007 Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920. (doi:10.1126/science.1151526)
34. Ying, Q. L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P. & Smith, A. 2008 The ground state of embryonic stem cell self-renewal. Nature 453, 519-523. (doi:10.1038/nature06968)
35. Kuroda, T., Tada, M., Kubota, H., Kimura, H., Hatano, S. Y., Suemori, H., Nakatsuji, N. & Tada, T. 2005 Octamer and Sox elements are required for transcriptional cis-regulation of Nanog gene expression. Mol. Cell. Biol. 25, 2475-2485. (doi:10.1128/MCB.25.6. 2475-2485.2005)
36. Rodda, D. J.,Chew, J. L., Lim, L.H., Loh, Y. H., Wang, B., Ng, H. H. & Robson, P. 2005 Transcriptional regulation of nanog by OCT4 and SOX2. J. Biol. Chem. 280, 24731-24737. (doi:10.1074/jbc.M502573200)
37. Sridharan, R., Tchieu, J., Mason, M. J., Yachechko, R., Kuoy, E., Horvath, S., Zhou, Q. & Plath, K. 2009 Role of the murine reprogramming factors in the induction of pluripotency. Cell 136, 364-377. (doi:10.1016/j. cell.2009.01.001)
38. Hanna, J., Saha, K., Pando, B., van Zon, J., Lengner, C. J., Creyghton, M. P., van Oudenaarden, A. & Jaenisch, R. 2009 Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462, 595-601. (doi:10.1038/nature08592)
39. Theunissen, T. W., van Oosten, A. L., Castelo-Branco, G., Hall, J., Smith, A. & Silva, J. C. 2011 Nanog overcomes reprogramming barriers and induces pluripotency in minimal conditions. Curr. Biol. 21, 65-71. (doi:10.1016/j.cub.2010.11.074)
40. Wang, J., Rao, S., Chu, J., Shen, X., Levasseur, D. N., Theunissen, T. W. & Orkin, S. H. 2006 A protein interaction network for pluripotency of embryonic stem cells. Nature 444, 364-368. (doi:10.1038/ nature05284)
41. Orkin, S. H., Wang, J., Kim, J., Chu, J., Rao, S., Theunissen, T. W., Shen, X. & Levasseur, D. N. 2008 The transcriptional network controlling pluripotency in ES cells. Cold Spring Harb. Symp. Quant. Biol. 73, 195-202. (doi:10.1101/sqb.2008.72.001)
42. Kim, J., Chu, J., Shen, X., Wang, J. & Orkin, S. H. 2008 An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132, 1049-1061. (doi:10.1016/j.cell.2008.02.039)
43. Boyer, L. A. et al. 2005 Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956. (doi:10.1016/j.cell.2005.08.020)
44. Loh, Y. H. et al. 2006 The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38, 431-440. (doi:10.1038/ ng1760)
45. Liang, J. et al. 2008 Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol. 10, 731-739. (doi:10.1038/ncb1736)
46. Nichols, J., Jones, K., Phillips, J. M., Newland, S. A., Roode, M., Mansfield, W., Smith, A. & Cooke, A. 2009 Validated germline-competent embryonic stem cell lines from nonobese diabetic mice. Nat. Med. 15, 814-818. (doi:10.1038/nm.1996)
47. Buehr, M. et al. 2008 Capture of authentic embryonic stem cells from rat blastocysts. Cell 135, 1287-1298. (doi:10.1016/j.cell.2008.12.007)
48. Li, P. et al. 2008 Germline competent embryonic stem cells derived from rat blastocysts. Cell 135, 1299-1310. (doi:10.1016/j.cell.2008.12.006)
49. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. & Jones, J. M. 1998 Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147. (doi:10.1126/science.282.5391.1145)
50. Silva, S. S., Rowntree, R. K., Mekhoubad, S. & Lee, J. T. 2008 X-chromosome inactivation and epigenetic fluidity in human embryonic stem cells. Proc. Natl Acad. Sci. USA 105, 4820-4825. (doi:10.1073/pnas.0712136105)
51. Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L. & McKay, R. D. G. 2007 New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199. (doi:10.1038/nature05972)
52. Brons, I. G. et al. 2007 Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195. (doi:10.1038/nature05950)
53. Guo, G., Yang, J., Nichols, J., Hall, J. S., Eyres, I., Mansfield, W. & Smith, A. 2009 Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063-1069. (doi:10.1242/dev.030957)
54. Hanna, J. et al. 2009 Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell 4, 513-524. (doi:10.1016/j.stem.2009.04.015)
55. Greber, B. et al. 2010 Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 6, 215-226. (doi:10.1016/j.stem.2010.01.003)
56. Hanna, J., Cheng, A. W., Saha, K., Kim, J., Lengner, C. J., Soldner, F., Cassady, J. P., Muffat, J., Carey, B. W. & Jaenisch, R. 2010 Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc. Natl Acad. Sci. USA. (doi:10.1073/pnas.1004584107)
57. Kim, Y. & Nirenberg, M. 1989 Drosophila NK-homeobox genes. Proc. Natl Acad. Sci. USA 86, 7716-7720. (doi:10.1073/pnas.86.20.7716)
58. Mullin, N. P., Yates, A., Rowe, A. J., Nijmeijer, B., Colby, D., Barlow, P. N., Walkinshaw, M. D. & Chambers, I. 2008 The pluripotency rheostat Nanog functions as a dimer. Biochem. J. 411, 227-231. (doi:10.1042/BJ20080134)
59. Wang, J., Levasseur, D. N. & Orkin, S. H. 2008 Requirement of Nanog dimerization for stem cell self-renewal and pluripotency. Proc. Natl Acad. Sci. USA 105, 6326-6331. (doi:10.1073/pnas.0802288105)
60. Lavial, F. et al. 2007 The Oct4 homologue PouV and Nanog regulate pluripotency in chicken embryonic stem cells. Development 134, 3549-3563. (doi:10.1242/ dev.006569)
61. Dixon, J. E. et al. 2010 Axolotl Nanog activity in mouse embryonic stem cells demonstrates that ground state pluripotency is conserved from urodele amphibians to mammals. Development 137, 2973-2980. (doi:10.1242/ dev.049262)