Ras signaling directs endothelial specification of VEGFR2+ vascular progenitor cells

Journal of Cell Biology

Volumn 181, Issue 1, 2008, Pages 131-141

  Kawasaki, Kyoko ^a   Watabe, Tetsuro ^a   Sase, Hitoshi ^a   Hirashima, Masanori ^b   Koide, Hiroshi ^c   Morishita, Yasuyuki ^a   Yuki, Keiko ^a   Sasaoka, Toshikuni ^d   Suda, Toshio ^b   Katsuki, Motoya ^d   Miyazono, Kohei ^a   Miyazawa, Keiji ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c KANAZAWA UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE METHYL ESTER; PLATELET DERIVED GROWTH FACTOR BB; RAS PROTEIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYO CULTURE; ENDOTHELIUM CELL; EX VIVO STUDY; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; ANTIGENS, CD31; CELL DIFFERENTIATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; ENZYME INHIBITORS; METHIONINE; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS P21(RAS); SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

MUS;

EID: 42049112366     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200709127     Document Type: Article

References (42)

1. Arbiser, J.L., A.M. Moses, C.A. Fernandez, N. Ghiso, Y. Cao, N. Klauber, D. Frank, M. Brownlee, E. Flynn, S. Parangi, et al. 1997. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc. Natl. Acad. Sci. USA. 94: 861-866.
2. Corson, L.B., Y. Yamanaka, M.K. Lai, and J. Rossant. 2003. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development. 130: 4527-4537.
3. Coultas, L., K. Chawengsaksophak, and J. Rossant. 2005. Endothelial cells and VEGF in vascular development. Nature. 438: 937-945
4. Doanes, A.M., D.D. Hegland, R. Sethi, I. Kovesdi, T.J. Bruder, and T. Finkel. 1999. VEGF stimulates MAPK through a pathway that is unique for receptor tyrosine kinases. Biochem. Biophys. Res. Commun. 255: 545-548.
5. Ema, M., P. Faloon, J.W. Zhang, M. Hirashima, T. Reid, L.W. Stanford, S. Orkin, K. Choi, and J. Rossant. 2003. Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev. 17: 380-393.
6. Ema, M., S. Takahashi, and J. Rossant. 2006. Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors. Blood. 107: 111-117.
7. Esteban, L.M., C. Vicario-Abejon, P. Fernandez-Salguero, A. Fernandez-Medarde, N. Swaminathan, K. Yienger, E. Lopez, M. Malumbres, R. McKay, M.J. Ward, et al. 2001. Targeted genomic disruption of H-ras and N-ras, individually or in combination, reveals the dispensability of both loci for mouse growth and development. Mol. Cell. Biol. 21: 1444-1452.
8. Ferguson, J.E. III, W.R. Kelley, and C. Patterson. 2005. Mechanisms of endothelial differentiation in embryonic vasculogenesis. Arterioscler. Thromb. Vasc. Biol. 25: 2246-2254.
9. Grugel, S., G. Finkenzeller, K. Weindel, B. Barleon, and D. Marmé. 1995. Both v-Ha-Ras ad v-Raf stimulate expression of the vascular endothelial growth factor in NIH 3T3 cells. J. Biol. Chem. 270: 25915-25919.
10. Hirashima, M., H. Kataoka, S. Nishikawa, N. Matsuyoshi, and S.I. Nishikawa. 1999. Maturation of embryonic stem cells into endothelial cells in an in vitro model of angiogenesis. Blood. 93: 1253-1263.
11. Hiratsuka, S., Y. Kataoka, K. Nakao, K. Nakamura, S. Morikawa, S. Tanaka, M. Katsuki, Y. Maru, and M. Shibuya. 2005. Vascular endothelial growth factor A (VEGF-A) is involved in guidance of VEGF receptor-positive cells to the anterior portion of early embryos. Mol. Cell. Biol. 25: 355-363.
12. Hogan, B., R. Beddington, F. Constantini, and E. Lacy. 1994. Manipulating the Mouse Embryo. A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York. 487pp.
13. Hood, J.D., R. Frausto, B.W. Kiosses, A.M. Schwartz, and A.D. Cheresh. 2003. Differential αv integrin-mediated Ras-Erk signaling during two pathways of angiogenesis. J. Cell Biol. 162: 933-943.
14. Huber, T.L., V. Kouskoff, H. Joerg Fehling, J. Palis, and G. Keller. 2004. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 432: 625-630.
15. Ise, K., K. Nakamura, K. Nakao, S. Shimizu, H. Harada, T. Ichise, J. Miyoshi, Y. Gondo, T. Ishikawa, A. Aiba, and M. Katsuki. 2000. Targeted deletion of the H-ras gene decreases tumor formation in mouse skin carcinogenesis. Oncogene. 19: 2951-2956.
16. Joneson, T., A.M. White, H.M. Wigler, and D. Bar-Sagi. 1996. Stimulation of membrane ruffling and MAP kinase activation by distinct effectors of RAS. Science. 271: 810-812.
17. Kano, M.R., Y. Morishita, C. Iwata, S. Iwasaka, T. Watabe, Y. Ouchi, K. Miyazono, and K. Miyazawa. 2005. VEGF-A and FGF-2 synergistically promote neoangiogenesis through enhancement of endogenous PDGF-BPDGFRb signaling. J. Cell Sci. 118: 3759-3768.
18. Klint, P., S. Kanda, Y. Kloog, and L. Claesson-Welsh. 1999. Contribution of Src and Ras pathways in FGF-2 induced endothelial cell differentiation. Oncogene. 18: 3354-3364.
19. Lamalice, L., F. Houle, G. Jourdan, and J. Hout. 2004. Phosphorylation of tyrosine 1214 on VEGFR2 is required for VEGF-induced activation of cdc42 upstream of SAPK/p38. Oncogene. 23: 434-445.
20. Lerner, E.C., Y. Qian, A.M. Blaskovich, D.R. Fossum, A. Vogt, J. Sun, D.A. Cox, J.C. Der, D.A. Hamilton, and M.S. Sebti. 1995. Ras CAAX peptidomimetic FTI-277 selectively blocks oncogenic Ras signaling by inducing cytoplasmic accumulation of inactive Ras-Raf complexes. J. Biol. Chem. 270: 26802-26806.
21. Marshall, C.J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 80: 179-185.
22. Masui, S., D. Shimosato, Y. Toyooka, R. Yagi, K. Takahashi, and H. Niwa. 2005. An efficient system to establish multiple embryonic stem cell lines carrying an inducible expression unit. Nucleic Acids Res. 33: e43.
23. Matsumoto, T., S. Bohman, J. Dixelius, T. Berge, A. Dimberg, P. Magnusson, L. Wang, C. Wikner, H.J. Qi, C. Wernstedt, et al. 2005. VEGF receptor-2 Y951 signaling and a role for the adaptor molecule TSAd in tumor angiogenesis. EMBO J. 24: 2342-2353.
24. Mishima, K., T. Watabe, A. Saito, Y. Yoshimatsu, N. Imaizumi, S. Masui, M. Hirashima, T. Morisada, Y. Oike, M. Araie, et al. 2007. Prox1 induces lymphatic endothelial differentiation via integrin a9 and other signaling cascades. Mol. Biol. Cell. 18: 1421-1429.
25. + progenitor: contribution to muscle lineage. Genesis. 35: 153-159.
26. Rak, J., Y. Mitsuhashi, L. Bayko, J. Filmus, S. Shirasawa, T. Sasazuki, and S.R. Kerbel. 1995. Mutant ras oncogenes upregulate VEGF/VPF expression: Implications for induction and inhibition of tumor angiogenesis. Cancer Res. 55: 4575-4580.
27. -/- embryonic stem cells and embryos. Proc. Natl. Acad. Sci. USA. 96: 2159-2164.
28. Shalaby, F., J. Rossant, P.T. Yamaguchi, M. Gertsenstein, F.X. Wu, L.M. Breitman, and C.A. Schuh. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 376: 62-66.
29. Shalaby, F., J. Ho, L.W. Stanford, D.K. Fischer, C.A. Schuh, L. Schwartz, A. Bernstein, and J. Rossant. 1997. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell. 89: 981-990.
30. Shibuya, M., and L. Claesson-Welsh. 2006. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp. Cell Res. 312: 549-560.
31. Spiekermann, K., F. Faber, R. Voswinckel, and W. Hiddemann. 2002. The protein tyrosine kinase inhibitor SU5614 inhibits VEGF-induced endothelial cell sprouting and induces growth arrest and apoptosis by inhibition of c-kit in AML cells. Exp. Hematol. 30: 767-773.
32. Sternberg, P.W., and M. Han. 1998. Genetics of RAS signaling in C. elegans. Trends Genet. 14: 466-472.
33. Suzuki, H., T. Watabe, M. Kato, K. Miyazawa, and K. Miyazono. 2005. Roles of vascular endothelial growth factor receptor 3 signaling in differentiation of mouse embryonic stem cell-derived vascular progenitor cells into endothelial cells. Blood. 105: 2372-2379.
34. Takahashi, T., H. Ueno, and M. Shibuya. 1999. VEGF activates proteins kinase C-dependent, but Ras-independent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene. 18: 2221-2230.
35. Takahashi, T., S. Yamaguchi, K. Chida, and M. Shibuya. 2001. A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-γ and DNA synthesis in vascular endothelial cells. EMBO J. 20: 2768-2778.
36. Wassarman, D.A., M. Therrien, and M.G. Rubin. 1995. The Ras signaling pathway in Drosophila. Curr. Opin. Genet. Dev. 5: 44-50.
37. Watabe, T., A. Nishihara, K. Mishima, J. Yamashita, K. Shimizu, K. Miyazawa, S. Nishikawa, and K. Miyazono. 2003. TGF-β receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J. Cell Biol. 163: 1303-1311.
38. Yamamoto, K., T. Takahashi, T. Asahara, N. Ohura, T. Sokabe, A. Kamiya, and J. Ando. 2003. Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J. Appl. Physiol. 95: 2081-2088.
39. Yamamoto, K., T. Sokabe, T. Watabe, K. Miyazono, J.K. Yamashita, S. Obi, N. Ohura, A. Matsushita, A. Kamiya, and J. Ando. 2005. Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am. J. Physiol. Heart Circ. Physiol. 288: H1915-H1924.
40. Yamashita, J., H. Itoh, M. Hirashima, M. Ogawa, S. Nishikawa, T. Yurugi, M. Naito, K. Nakao, and S. Nishikawa. 2000. Flk-1 positive cells derived from embryonic stem cells serves as vascular progenitors. Nature. 408: 92-96.
41. Yashima, R., M. Abe, K. Tanaka, H. Ueno, K. Shitara, S. Takenoshita, and Y. Sato. 2001. Heterogeneity of the signal transduction pathways for VEGF-induced MAPKs activation in human vascular endothelial cells. J. Cell. Physiol. 188: 201-210.
42. Yoshida-Koide, U., T. Matsuda, K. Saikawa, Y. Nakanuma, T. Yokota, M. Asashima, and H. Koide. 2004. Involvement of Ras in extraembryonic endoderm differentiation of embryonic stem cells. Biochem. Biophys. Res. Commun. 313: 475-481