Chemical Genetics Identifies c-Src as an Activator of Primitive Ectoderm Formation in Murine Embryonic Stem Cells

Science Signaling

Volumn 2, Issue 92, 2009, Pages

  Meyn III, Malcolm A ^a   Smithgall, Thomas E ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMATOPOIETIC CELL KINASE; PROTEIN KINASE FYN; PROTEIN KINASE LCK; PROTEIN KINASE YES; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CELL DIFFERENTIATION; CELL FATE; CELL GROWTH; CHEMICAL GENETICS; ECTODERM; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; IMMUNOBLOTTING; MOUSE; MOUSE EMBRYO; MUTANT; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; CELL LINEAGE; CELL PROLIFERATION; CHEMICAL MODEL; CONFORMATION; CYTOLOGY; GENETIC PROCEDURES; METABOLISM; MUTATION; STEM CELL;

MURINAE;

ANIMALS; CATALYSIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; ECTODERM; EMBRYONIC STEM CELLS; GENETIC TECHNIQUES; MICE; MODELS, CHEMICAL; MOLECULAR CONFORMATION; MUTATION; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; STEM CELLS;

EID: 73349084621     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000311     Document Type: Article

References (54)

1. M. J. Evans, M. H. Kaufman, Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156 (1981). (Pubitemid 11050741)
2. G. R. Martin, 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 (1981).
3. N. Liu, M. Lu, X. Tian, Z. Han, Molecular mechanisms involved in self-renewal and pluripotency of embryonic stem cells. J. Cell. Physiol. 211, 279-286 (2007). (Pubitemid 46580081)
4. C. Annerén, Tyrosine kinase signalling in embryonic stem cells. Clin. Sci. (Lond) 115, 43-55 (2008). (Pubitemid 351930792)
5. T. J. Yeatman, A renaissance for SRC. Nat. Rev. Cancer 4, 470-480 (2004).
6. G. Manning, D. B. Whyte, R. Martinez, T. Hunter, S. Sudarsanam, The protein kinase complement of the human genome. Science 298, 1912-1934 (2002). (Pubitemid 35425239)
7. M. A. Meyn III, S. J. Schreiner, T. P. Dumitrescu, G. J. Nau, T. E. Smithgall, SRC family kinase activity is required for murine embryonic stem cell growth and differentiation. Mol. Pharmacol. 68, 1320-1330 (2005).
8. R. L. Williams,D. J.Hilton, S. Pease, T.A. Willson,C. L. Stewart,D. P.Gearing,E. F.Wagner, D. Metcalf, N. A. Nicola, N. M. Gough, Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336, 684-687 (1988). (Pubitemid 19007951)
9. D. C. Weinstein, J. Marden, F. Carnevali, A. Hemmati-Brivanlou, FGF-mediated mesoderm induction involves the Src-family kinase Laloo. Nature 394, 904-908 (1998). (Pubitemid 28410914)
10. D. C. Weinstein, A. Hemmati-Brivanlou, Src family kinase function during early Xenopus development. Dev. Dyn. 220, 163-168 (2001). (Pubitemid 32107817)
11. M. Ernst, D. P. Gearing, A. R. Dunn, Functional and biochemical association of Hck with the LIF/IL-6 receptor signal transducing subunit gp130 in embryonic stem cells. EMBO J. 13, 1574-1584 (1994). (Pubitemid 24114708)
12. M. Ernst, U. Novak, S. E. Nicholson, J. E. Layton, A. R. Dunn, The carboxyl-terminal domains of gp130-related cytokine receptors are necessary for suppressing embryonic stem cell differentiation. Involvement of STAT3. J. Biol. Chem. 274, 9729-9737 (1999). (Pubitemid 129517950)
13. C. Annerén, C. A. Cowan, D. A. Melton, The Src family of tyrosine kinases is important for embryonic stem cell self-renewal. J. Biol. Chem. 279, 31590-31598 (2004).
14. F. Sicheri, I. Moarefi, J. Kuriyan, Crystal structure of the Src family tyrosine kinase Hck. Nature 385, 602-609 (1997).
15. X. Zhu, J. L. Kim, J. R. Newcomb, P. E. Rose, D. R. Stover, L. M. Toledo, H. Zhao, K. A. Morgenstern, Structural analysis of the lymphocyte-specific kinase Lck in complex with non-selective and Src family selective kinase inhibitors. Structure 7, 651-661 (1999).
16. W. Xu, S. C. Harrison, M. J. Eck, Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602 (1997).
17. T. Kinoshita, M. Matsubara, H. Ishiguro, K. Okita, T. Tada, Structure of human Fyn kinase domain complexed with staurosporine. Biochem. Biophys. Res. Commun. 346, 840-844 (2006).
18. T. Schindler, F. Sicheri, A. Pico, A. Gazit, A. Levitzki, J. Kuriyan, Crystal structure of Hck in complex with a Src family-selective tyrosine kinase inhibitor. Mol. Cell 3, 639-648 (1999).
19. S. D. Briggs, T. E. Smithgall, SH2-kinase linker mutations release Hck tyrosine kinase and transforming activities in Rat-2 fibroblasts. J. Biol. Chem. 274, 26579-26583 (1999).
20. L. Tatton, G. M. Morley, R. Chopra, A. Khwaja, The Src-selective kinase inhibitor PP1 also inhibits Kit and Bcr-Abl tyrosine kinases. J. Biol. Chem. 278, 4847-4853 (2003).
21. M. B. Wilson, S. J. Schreiner, H. J. Choi, J. Kamens, T. E. Smithgall, Selective pyrrolopyrimidine inhibitors reveal a necessary role for Src family kinases in Bcr-Abl signal transduction and oncogenesis. Oncogene 21, 8075-8088 (2002).
22. D. J. Calderwood, D. N. Johnston, R. Munschauer, P. Rafferty, Pyrrolo[2,3-d]pyrimidines containing diverse N-7 substituents as potent inhibitors of Lck. Bioorg. Med. Chem. Lett. 12, 1683-1686 (2002).
23. S. R. Cherry, D. Biniszkiewicz, L. van Parijs, D. Baltimore, R. Jaenisch, Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol. Cell. Biol. 20, 7419-7426 (2000).
24. G. Chapman, J. L. Remiszewski, G. C. Webb, T. C. Schulz, C. D. Bottema, P. D. Rathjen, The mouse homeobox gene, Gbx2: Genomic organization and expression in pluripotent cells in vitro and in vivo. Genomics 46, 223-233 (1997).
25. H. R. Schöler, G. R. Dressler, R. Balling, H. Rohdewohld, P. Gruss, Oct-4: A germlinespecific transcription factor mapping to the mouse t-complex. EMBO J. 9, 2185-2195 (1990).
26. I. Chambers, D. Colby,M. Robertson, J. Nichols, S. Lee, S. Tweedie, A.Smith, Functional expression cloning ofNanog, a pluripotency sustaining factor in embryonic stemcells.Cell 113, 643-655 (2003).
27. K. Mitsui, Y. Tokuzawa, H. Itoh, K. Segawa, M. Murakami, K. Takahashi, M. Maruyama, M. Maeda, S. Yamanaka, The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642 (2003).
28. M. B. Rogers, B. A. Hosler, L. J. Gudas, Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 113, 815-824 (1991).
29. J. Jiang, Y. S. Chan, Y. H. Loh, J. Cai, G. Q. Tong, C. A. Lim, P. Robson, S. Zhong, H. H. Ng, A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat. Cell Biol. 10, 353-360 (2008).
30. N. B. Ivanova, J. T. Dimos, C. Schaniel, J. A. Hackney, K. A. Moore, I. R. Lemischka, A stem cell molecular signature. Science 298, 601-604 (2002).
31. O. Haub, M. Goldfarb, Expression of the fibroblast growth factor-5 gene in the mouse embryo. Development 112, 397-406 (1991).
32. B. G. Herrmann, Expression pattern of the Brachyury gene in whole-mount TWis/TWis mutant embryos. Development 113, 913-917 (1991).
33. C. C. Lu, J. Brennan, E. J. Robertson, From fertilization to gastrulation: Axis formation in the mouse embryo. Curr. Opin. Genet. Dev. 11, 384-392 (2001).
34. J. Rathjen, J. A. Lake, M. D. Bettess, J. M. Washington, G. Chapman, P. D. Rathjen, 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 (1999).
35. I. G. Brons, L. E. Smithers, M. W. Trotter, P. Rugg-Gunn, B. Sun, S. M. Chuva de Sousa Lopes, S. K. Howlett, A. Clarkson, L. Ahrlund-Richter, R. A. Pedersen, L. Vallier, Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195 (2007).
36. P. J. Tesar, J.G.Chenoweth,F. A.Brook, T. J.Davies,E. P.Evans,D. L.Mack,R. L.Gardner, R. D. McKay, New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199 (2007).
37. P. W. Zandstra, H. V. Le, G. Q. Daley, L. G. Griffith, D. A. Lauffenburger, Leukemia inhibitory factor (LIF) concentration modulates embryonic stem cell self-renewal and differentiation independently of proliferation. Biotechnol. Bioeng. 69, 607-617 (2000).
38. G. M. Keller, In vitro differentiation of embryonic stem cells. Curr. Opin. Cell Biol. 7, 862-869 (1995).
39. A. Leahy, J. W. Xiong, F. Kuhnert, H. Stuhlmann, Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation. J. Exp. Zool. 284, 67-81 (1999).
40. E. Coucouvanis, G. R. Martin, Signals for death and survival: A two-step mechanism for cavitation in the vertebrate embryo. Cell 83, 279-287 (1995).
41. J. Lake, J.Rathjen, J. Remiszewski, P. D.Rathjen, Reversible programming of pluripotent cell differentiation. J. Cell Sci. 113, 555-566 (2000).
42. Y. Toyooka, D. Shimosato, K. Murakami, K. Takahashi, H. Niwa, Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 135, 909-918 (2008).
43. R. L. Gardner, Regeneration of endoderm from primitive ectoderm in the mouse embryo: Fact or artifact? J. Embryol. Exp. Morphol. 88, 303-326 (1985).
44. N. E. Kremer, G. D'Arcangelo, S. M. Thomas, M. DeMarco, J. S. Brugge, S. Halegoua, Signal transduction by nerve growth factor and fibroblast growth factor in PC12 cells requires a sequence of src and ras actions. J. Cell Biol. 115, 809-819 (1991).
45. F. Jin, A. B. Reynolds, M. D. Hines, P. J. Jensen, K. R. Johnson, M. J. Wheelock, Src induces morphological changes in A431 cells that resemble epidermal differentiation through an SH3- and Ras-independent pathway. J. Cell Sci. 112, 2913-2924 (1999).
46. S. M. Thomas, J. S. Brugge, Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13, 513-609 (1997).
47. T. C. Doetschman, H. Eistetter, M. Katz, W. Schmidt, R. Kemler, 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 (1985).
48. H. Niwa, T. Burdon, I. Chambers, A. Smith, Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev. 12, 2048-2060 (1998). (Pubitemid 28323878)
49. J. A. Rogers, R. D. Read, J. Li, K. L. Peters, T. E. Smithgall, Autophosphorylation of the Fes tyrosine kinase. Evidence for an intermolecular mechanism involving two kinase domain tyrosine residues. J. Biol. Chem. 271, 17519-17525 (1996).
50. C. M. Ward, P. L. Stern, The human cytomegalovirus immediate-early promoter is transcriptionally active in undifferentiated mouse embryonic stem cells. Stem Cells 20, 472-475 (2002).
51. E. Willems, I. Mateizel, C. Kemp, G. Cauffman, K. Sermon, L. Leyns, Selection of reference genes in mouse embryos and in differentiating human and mouse ES cells. Int. J. Dev. Biol. 50, 627-635 (2006).
52. C. L. Murphy, J. M. Polak, Differentiating embryonic stem cells: GAPDH, but neither HPRT nor b-tubulin is suitable as an internal standard for measuring RNA levels. Tissue Eng. 8, 551-559 (2002).
53. M. W. Pfaffl, G. W. Horgan, L. Dempfle, Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in realtime PCR. Nucleic Acids Res. 30, e36 (2002).
54. This work was supported by NIH grants K01CA111633 (to M.A.M.) and R01 GM077629 (to T.E.S.). We thank M. Tsang of the Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, for critical reading of this manuscript. The pan-SFK inhibitor A-419259 was provided by D. Calderwood, Abbott Bioresearch, Inc., Worcester, MA.