Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo

Development

Volumn 136, Issue 19, 2009, Pages 3215-3222

  Nichols, Jennifer ^a   Silva, Jose ^a   Roode, Mila ^a   Smith, Austin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Blastocyst; Epiblast; Erk; Hypoblast; Mouse; Pluripotency

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NANOG; 2 (2 CHLORO 4 IODOANILINO) N CYCLOPROPYLMETHOXY 3,4 DIFLUOROBENZAMIDE; 2-(2-CHLORO-4-IODOPHENYLAMINO)-N-CYCLOPROPYLMETHOXY-3,4-DIFLUOROBENZAMIDE; 3 [4 METHYL 2 (2 OXO 3 INDOLINYLMETHYLIDENYL) 3 PYRROLYL]PROPIONIC ACID; BENZAMIDE DERIVATIVE; LEUKEMIA INHIBITORY FACTOR; LIF PROTEIN, MOUSE; PROTEIN KINASE INHIBITOR; PYRROLE DERIVATIVE;

ANIMAL CELL; ARTICLE; BLASTOCYTE; CELL COUNT; CELL DIVISION; CELL EXPANSION; CELL SURVIVAL; ECTODERM; EMBRYO; ENZYME INHIBITION; GENE REPRESSION; GENE SILENCING; INNER CELL MASS; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CBA MOUSE; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; EMBRYO CULTURE; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENZYMOLOGY; FEMALE; GERM LAYER; MALE; METABOLISM; PHYSIOLOGY; PREGNANCY; RAT;

CHIMAERIFORMES; RATTUS;

ANIMALS; BENZAMIDES; BLASTOCYST INNER CELL MASS; CELL DIFFERENTIATION; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GERM LAYERS; LEUKEMIA INHIBITORY FACTOR; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; PLURIPOTENT STEM CELLS; PREGNANCY; PROTEIN KINASE INHIBITORS; PYRROLES; RATS;

EID: 70349934958     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.038893     Document Type: Article

References (58)

1. Arman, E., Krausz-Haffner, R., Chen, Y., Heath, J. K. and Lonai, P. (1998). Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. USA 95, 5082-5087.
2. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I., Arthur, J. S., Alessi, D. R. and Cohen, P. (2007). The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297-315.
3. Batlle-Morera, L., Smith, A. and Nichols, J. (2008). Parameters influencing derivation of embryonic stem cells from murine embryos. Genesis 46, 758-767.
4. Bradley, A., Evans, M. J., Kaufman, M. H. and Robertson, E. (1984). Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309, 255-256.
5. 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. et al. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195.
6. Brook, F. A. and Gardner, R. L. (1997). The origin and efficient derivation of embryonic stem cells in the mouse. Proc. Natl. Acad. Sci. USA 94, 5709-5712.
7. Buehr, M. and Smith, A. (2003). Genesis of embryonic stem cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1397-1402; discussion 1402.
8. 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.
9. 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.
10. Burdon, T., Stracey, C., Chambers, I., Nichols, J. and Smith, A. (1999). Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev. Biol. 210, 30-43.
11. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. and Smith, A. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643-655.
12. Champlin, A. K., Dorr, D. L. and Gates, A. H. (1973). Determining the stage of the estrous cycle in the mouse by the appearance of the vagina. Biol. Reprod. 8, 491-494.
13. 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.
14. Chen, S., Do, J. T., Zhang, Q., Yao, S., Yan, F., Peters, E. C., Scholer, H. R., Schultz, P. G. and Ding, S. (2006). Self-renewal of embryonic stem cells by a small molecule. Proc. Natl. Acad. Sci. USA 103, 17266-17271.
15. Cheng, A. M., Saxton, T. M., Sakai, R., Kulkarni, S., Mbamalu, G., Vogel, W., Tortorice, C. G., Cardiff, R. D., Cross, J. C., Muller, W. J. et al. (1998). Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation. Cell 95, 793-803.
16. Evans, M. J. and Kaufman, M. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156.
17. Gardner, R. L. (1985). Regeneration of endoderm from primitive ectoderm in the mouse embryo: fact or artifact? J. Embryol. Exp. Morphol. 80, 303-326.
18. Gardner, R. L. and Brook, F. A. (1997). Reflections on the biology of embryonic stem cells. Int. J. Dev. Biol. 41, 235-243.
19. Guo, G., Yang, J., Nichols, J., Hall, J. S., Eyres, I., Mansfield, W. and Smith, A. (2009). Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063-1069.
20. Hart, A. H., Hartley, L., Ibrahim, M. and Robb, L. (2004). Identification, cloning and expression analysis of the pluripotency promoting Nanog genes in mouse and human. Dev. Dyn. 230, 187-198.
21. Holdener, B. C., Faust, C., Rosenthal, N. S. and Magnuson, T. (1994). msd is required for mesoderm induction in mice. Development 120, 1335-1346.
22. Kawase, E., Suemori, H., Takahashi, N., Okazaki, K., Hashimoto, K. and Nakatsuji, N. (1994). Strain difference in establishment of mouse embryonic stem (ES) cell lines. Int. J. Dev. Biol. 38, 385-390.
23. Kunath, T., Saba-El-Leil, M. K., Almousailleakh, M., Wray, J., Meloche, S. and 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.
24. Li, P., Tong, C., Mehrian-Shai, R., Jia, L., Wu, N., Yan, Y., Maxson, R. E., Schulze, E. N., Song, H., Hsieh, C. L. et al. (2008). Germline competent embryonic stem cells derived from rat blastocysts. Cell 135, 1299-1310.
25. Lu, C. W., Yabuuchi, A., Chen, L., Viswanathan, S., Kim, K. and Daley, G. Q. (2008). Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat. Genet. 40, 921-926.
26. Mak, W., Nesterova, T. B., de Napoles, M., Appanah, R., Yamanaka, S., Otte, A. P. and Brockdorff, N. (2004). Reactivation of the paternal X chromosome in early mouse embryos. Science 303, 666-669.
27. 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.
28. 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.
29. Morrisey, E. E., Ip, H. S., Lu, M. M. and Parmacek, M. S. (1996). GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev. Biol. 177, 309-322.
30. Nichols, J. and Ying, Q. L. (2006). Derivation and propagation of embryonic stem cells in serum- and feeder-free culture. Methods Mol. Biol. 329, 91-98.
31. Nichols, J. and Smith, A. (2009). Naive and primed pluripotent states. Cell Stem Cell 4, 487-492.
32. Nichols, J., Davidson, D., Taga, T., Yoshida, K., Chambers, I. and Smith, A. G. (1996). Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech. Dev. 57, 123-131.
33. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Scholer, H. and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct-4. Cell 95, 379-391.
34. Nichols, J., Jones, K., Phillips, J. M., Newland, S. A., Roode, M., Mansfield, W., Smith, A. and Cooke, A. (2009). Validated germline-competent embryonic stem cell lines from nonobese diabetic mice. Nat. Med. 15, 814-818.
35. Nishioka, N., Inoue, K., Adachi, K., Kiyonari, H., Ota, M., Ralston, A., Yabuta, N., Hirahara, S., Stephenson, R. O., Ogonuki, N. et al. (2009). The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398-410.
36. Okamoto, I., Otte, A. P., Allis, C. D., Reinberg, D. and Heard, E. (2004). Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303, 644-649.
37. Palmieri, S. L., Peter, W., Hess, H. and Scholer, H. R. (1994). Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation. Dev. Biol. 166, 259-267.
38. Quinn, P., Barros, C. and Whittingham, D. G. (1982). Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. J. Reprod. Fertil. 66, 161-168.
39. Rappolee, D. A., Basilico, C., Patel, Y. and Werb, Z. (1994). Expression and function of FGF-4 in peri-implantation development in the mouse embryo. Development 120, 2259-2269.
40. 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.
41. Silva, J. M., Marran, K., Parker, J. S., Silva, J., Golding, M., Schlabach, M. R., Elledge, S. J., Hannon, G. J. and Chang, K. (2008). Profiling essential genes in human mammary cells by multiplex RNAi screening. Science 319, 617-620.
42. Silva, S. S., Rowntree, R. K., Mekhoubad, S. and Lee, J. T. (2008). X-chromosome inactivation and epigenetic fluidity in human embryonic stem cells. Proc. Natl. Acad. Sci. USA 105, 4820-4825.
43. Silva, J., Nichols, J., Theunissen, T. W., Guo, G., van Oosten, A. L., Barrandon, O., Wray, J., Yamanaka, S., Chambers, I. and Smith, A. (2009). Nanog is the gateway to the pluripotent ground state. Cell doi:10.1016/j.cell.2009.07.039.
44. Smith, A. G. (2001). Embryonic stem cells. In Stem Cell Biology, vol. 40 (ed. D. R. Marshak, R. L. Gardner and D. Gottlieb), pp. 205-230. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
45. Smith, A. G., Heath, J. K., Donaldson, D. D., Wong, G. G., Moreau, J., Stahl, M. and Rogers, D. (1988). Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336, 688-690.
46. Solter, D. and Knowles, B. (1975). Immunosurgery of mouse blastocyst. Proc. Natl. Acad. Sci. USA 72, 5099-5102.
47. 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.
48. Tanaka, S., Kunath, T., Hadjantonakis, A.-K., Nagy, A. and Rossant, J. (1998). Promotion of trophoblast stem cell proliferation by FGF-4. Science 282, 2072-2075.
49. 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.
50. Umehara, H., Kimura, T., Ohtsuka, S., Nakamura, T., Kitajima, K., Ikawa, M., Okabe, M., Niwa, H. and Nakano, T. (2007). Efficient derivation of embryonic stem cells by inhibition of glycogen synthase kinase-3. Stem Cells 25, 2705-2711.
51. Voss, A. K., Thomas, T., Petrou, P., Anastassiadis, K., Scholer, H. and Gruss, P. (2000). Taube nuss is a novel gene essential for the survival of pluripotent cells of early mouse embryos. Development 127, 5449-5461.
52. Williams, R. L., Hilton, D. J., Pease, S., Willson, T. A., Stewart, C. L., Gearing, D. P., Wagner, E. F., Metcalf, D., Nicola, N. A. and Gough, N. M. (1988). Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336, 684-687.
53. Yagi, R., Kohn, M. J., Karavanova, I., Kaneko, K. J., Vullhorst, D., DePamphilis, M. L. and Buonanno, A. (2007). Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134, 3827-3836.
54. Ying, Q. L. and Smith, A. G. (2003). Defined conditions for neural commitment and differentiation. Methods Enzymol. 365, 327-341.
55. Ying, Q. L., Nichols, J., Chambers, I. and 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.
56. Ying, Q. L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P. and Smith, A. (2008). The ground state of embryonic stem cell self-renewal. Nature 453, 519-523.
57. Zhen, Y., Sorensen, V., Jin, Y., Suo, Z. and Wiedlocha, A. (2007). Indirubin-3′-monoxime inhibits autophosphorylation of FGFR1 and stimulates ERK1/2 activity via p38 MAPK. Oncogene 26, 6372-6385.
58. Zwaka, T. P. and Thomson, J. A. (2005). A germ cell origin of embryonic stem cells? Development 132, 227-233.