Adaptor protein Crk is required for ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells

Molecular Biology of the Cell

Volumn 13, Issue 12, 2002, Pages 4231-4242

  Nagashima, Ken Ichiro ^a   Endo, Akira ^a   Ogita, Hisakazu ^a   Kawana, Akiko ^a   Yamagishi, Akiko ^a   Kitabatake, Akira ^b   Matsuda, Michiyuki ^c   Mochizuki, Naoki ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; EPHRIN; PROTEIN CRK; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; RAP PROTEIN; UNCLASSIFIED DRUG; BCAR1 PROTEIN, HUMAN; CRK ASSOCIATED SUBSTRATE PROTEIN; EPHRIN B1; ONCOPROTEIN; PHOSPHOPROTEIN; PROTEIN; PROTEIN P130; RECOMBINANT PROTEIN;

ANGIOGENESIS; AORTA; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FLUORESCENCE; HUMAN; HUMAN CELL; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; RNA ANALYSIS; BIOLOGICAL MODEL; CELL CULTURE; CELL LINE; CELL MEMBRANE; CELL MOTION; CYTOLOGY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; IMMUNOBLOTTING; METABOLISM; PHYSIOLOGY; PLASMID; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; SERODIAGNOSIS; TIME; VASCULAR ENDOTHELIUM;

AORTA; CELL LINE; CELL MEMBRANE; CELL MOVEMENT; CELLS, CULTURED; CRK-ASSOCIATED SUBSTRATE PROTEIN; ENDOTHELIUM, VASCULAR; EPHRIN-B1; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PHOSPHOPROTEINS; PLASMIDS; PRECIPITIN TESTS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CRK; RECOMBINANT PROTEINS; RETINOBLASTOMA-LIKE PROTEIN P130; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION;

EID: 0036911338     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-04-0181     Document Type: Article

References (53)

1. Bar-Sagi, D., and Hall, A. (2000). Ras, and Rho GTPases, a family reunion. Cell 103, 227-238.
2. Birge, R.B., Fajardo, J.E., Reichman, C., Shoelson, S.E., Songyang, Z., Cantley, L.C., and Hanafusa, H. (1993). Identification and characterization of a high-affinity interaction between v-Crk and tyrosinephosphorylated paxillin in CT10-transformed fibroblasts. Mol. Cell. Biol. 13, 4648-4656.
3. Brückner, K., Pasquale, E.B., and Klein, R. (1997). Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 275, 1640-1643.
4. Carmeliet, P., and Jain, R.K. (2000). Angiogenesis in cancer and other diseases. Nature 407, 249-257.
5. 2 by LPS and other inflammatory mediators. Curr. Biol. 10, 974-978.
6. Cheresh, D.A., Leng, J., and Klemke, R.L. (1999). Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells. J. Cell Biol. 146, 1107-1116.
7. Cook, S.J., Rubinfeld, B., Albert, I., and McCormick, F. (1993). RapV12 antagonizes Ras-dependent activation of ERK1 and ERK2 by LPA and EGF in Rat-1 fibroblasts. EMBO J. 12, 3475-3485.
8. Cowan, C.A., and Henkemeyer, M. (2001). The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413, 174-179.
9. Dodelet, V.C., and Pasquale, E.B. (2000). Eph receptors and ephrin ligands: Embryogenesis to tumorigenesis. Oncogene 19, 5614-5619.
10. Dodelet, V.C., Pazzagli, C., Zisch, A.H., Hauser, C.A., and Pasquale, E.B. (1999). A novel signaling intermediate, SHEP1, directly couples Eph receptors to R-Ras and Rap1A. J. Biol. Chem. 274, 31941-31946.
11. Elowe, S., Holland, S.J., Kulkarni, S., and Pawson, T. (2001). Down-regulation of the Ras-mitogen-activated protein kinase pathway by the EphB2 receptor tyrosine kinase is required for ephrin-induced neurite retraction. Mol. Cell. Biol. 21, 7429-7441.
12. Endo, A., Nagashima, K., Kurose, H., Mochizuki S., Matsuda, M., and Mochizuki, N. (2002). Sphingosine 1-phosphate induces membrane ruffling and increases motility of human umbilical vein endothelial cells via vascular endothelial growth factor receptor and CrkII. J. Biol. Chem. 277, 23747-23754.
13. Eph Nomenclature Committee. (1997). Unified nomenclature for Eph family receptors and their ligands, the ephrins. Eph Nomenclature Committee letter. Cell 90, 403-404.
14. Erickson, M.R., Galletta, B.J., and Abmayr, S.M. (1997). Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure, and cytoskeletal organization. J. Cell Biol. 138, 589-603.
15. Fradkov, A.F., Chen, Y., Ding, L., Barsova, E.V., Matz, M.V., and Lukyanov, S.A. (2000). Novel fluorescent protein from Discosoma coral and its mutants possesses a unique far-red fluorescence. FEBS Lett. 479, 127-130.
16. Gale, N.W., Baluk, P., Pan, L., Kwan, M., Holash, J., DeChiara, T.M., McDonald, D.M., and Yancopoulos, G.D. (2001). Ephrin-B2 selectively marks arterial vessels and neovascularization sites in the adult, with expression in both endothelial and smooth-muscle cells. Dev. Biol. 230, 151-160.
17. Geiger, B., Bershadsky, A., Pankov, R., and Yamada, K.M. (2001). Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell. Biol. 2, 793-805.
18. Harborth, J., Elbashir, S.M., Bechert, K., Tuschl, T., and Weber, K. (2001). Identification of essential genes in cultured mammalian cells using small interfering RNAs. J. Cell Sci. 114, 4557-4565.
19. Hock, B., Böhme, B., Karn, T., Feller, S., Rübsamen-Waigmann, H., and Strebhardt, K. (1998). Tyrosine-614, the major autophosphorylation site of the receptor tyrosine kinase HEK2, functions as multi-docking site for SH2-domain mediated interactions. Oncogene 17, 255-260.
20. Holder, N., and Klein R. (1999). Eph receptors and ephrins: Effectors of morphogenesis. Development 126, 2033-2044.
21. Ichiba, T., Hashimoto, Y., Nakaya, M., Kuraishi, Y., Tanaka, S., Kurata, T., Mochizuki, N., and Matsuda, M. (1999). Activation of C3G guanine nucleotide exchange factor for Rap1 by phosphorylation of tyrosine 504. J. Biol. Chem. 274, 14376-14381.
22. Ichiba, T., Kuraishi, Y., Sakai, O., Nagata, S., Groffen, J., Kurata, T., Hattori, S., and Matsuda, M. (1997). Enhancement of guanine-nucleotide exchange activity of C3G for Rap1 by the expression of Crk, CrkL, and Grb2. J. Biol. Chem. 272, 22215-22220.
23. Kitayama, H., Sugimoto, Y., Matsuzaki, T., Ikawa, Y., and Noda, M. (1989). A ras-related gene with transformation suppressor activity. Cell 56, 77-84.
24. Kiyokawa, E., Hashimoto, Y., Kobayashi, S., Sugimura, H., Kurata, T., and Matsuda, M. (1998). Activation of Racl by a Crk SH3- binding protein, DOCK180. Genes Dev. 12, 3331-3336.
25. Kiyokawa, E., Mochizuki, N., Kurata, T., and Matsuda, M. (1997). Role of Crk oncogene product in physiologic signaling. Crit. Rev. Oncog. 8, 329-342.
26. Klemke, R.L., Leng, J., Molander, R., Brooks, P.C., Vuori, K., and Cheresh, D.A. (1998). CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 140, 961-972.
27. Lauffenburger, D.A., and Horwitz, A.F. (1996). Cell migration: A physically integrated molecular process. Cell 84, 359-369.
28. Li, L., Okura, M., and Imamoto, A. (2002). Focal adhesions require catalytic activity of SRC family kinases to mediate integrin-matrix adhesion. Mol. Cell. Biol. 22, 1203-1217.
29. Lu, Q., Sun, E.E., Klein, R.S., and Flanagan, J.G. (2001). Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction. Cell 105, 69-79.
30. Matsuda, M., Tanaka, S., Nagata, S., Kojima, A., Kurata, T., and Shibuya, M. (1992). Two species of human CRK cDNA encode proteins with distinct biological activities. Mol. Cell. Biol. 12, 3482- 3489.
31. Miao, H., Wei, B., Prehl, D.M., Li, Q., Alexandrou, T., Schelling, J.R., Rhim, J.S., Sedor, J.R., Burnett, E., and Wang, B. (2001). Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat. Cell. Biol. 3, 527-530.
32. Mochizuki, N., Ohba, Y., Kiyokawa, E., Kurata, T., Murakami, T., Ozaki, T., Kitabatake, A., Nagashima, K., and Matsuda, M. (1999). Activation of the ERK/MAPK pathway by an isoform of rap1GAP associated with Gαi. Nature 400, 891-894.
33. Mochizuki, N., Yamashita, S., Kurokawa, K., Ohba, Y., Nagai, T., Miyawaki, A., and Matsuda, M. (2001). Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068.
34. Niwa, H., Yamamura, K., and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
35. Ohba, Y., et al. (2001). Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 20, 3333-3341.
36. Reddien, P.W., and Horvitz, H.R. (2000). CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2, 131-136.
37. Reedquist, K.A., Ross, E., Koop, E.A., Wolthuis, R.M., Zwartkruis, F.J., van Kooyk, Y., Salmon, M., Buckley, C.D., and Bos, J.L. (2000). The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J. Cell Biol. 148, 1151-1158.
38. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674.
39. Rottner, K., Hall, A., and Small, J.V. (1999). Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol. 9, 640-648.
40. Sakai, R., Iwamatsu, A., Hirano, N., Ogawa, S., Tanaka, T., Mano, H., Yazaki, Y., and Hirai, H. (1994). A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner. EMBO J. 13, 3748- 3756.
41. Sakakibara, A., and Hattori, S. (2000) Chat, a Cas/HEF-associated adaptor protein that integrates multiple signaling pathways. J. Biol. Chem. 275, 6404-6410.
42. Schaller, M.D., and Parsons, J.T. (1995). pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15, 2635-2645.
43. Shin, D., Garcia-Cardena, G., Hayashi, S., Gerety, S., Asahara, T., Stavrakis, G., Isner, J., Folkman, J., Gimbrone, Jr., M.A., and Anderson, D.J. (2001). Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev. Biol. 230, 139-150.
44. Stein, E., Cerretti, D.P., and Daniel, T.O. (1996). Ligand activation of ELK receptor tyrosine kinase promotes its association with Grb10 and Grb2 in vascular endothelial cells. J. Biol. Chem. 271, 23588-23593.
45. Vuori, K., Hirai, H., Aizawa, S., and Ruoslahti, E. (1996). Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion: A zole for Src family kinases. Mol. Cell. Biol. 16, 2606-2613.
46. Wang, H.U., Chen, Z.F., and Anderson, D.J. (1998). Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93, 741-753.
47. Wu, Y.C., and Horvitz, H.R. (1998). C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392, 501-504.
48. Xing, L., Ge, C., Zeltser, R., Maskevitch, G., Mayer, B.J., and Alexandropoulos, K. (2000). c-Src signaling induced by the adapters Sin, and Cas is mediated by Rap1 GTPase. Mol. Cell Biol. 20, 7363-7377.
49. Yancopoulos, G.D., Davis, S., Gale, N.W., Rudge, J.S., Wirgand, S.J., and Holash, J. (2000). Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248.
50. Yancopoulos, G.D., Klagsbrun, M., and Folkman, J. (1998). Vasculogenesis, angiogenesis, and growth factors: Ephrins enter the fray at the border. Cell 93, 661-664.
51. Yano, H., Uchida, H., Iwasaki, T., Mukai, M., Akedo, H., Nakamura, K., Hashimoto, S., and Sabe, H. (2000). Paxillin alpha and Crk- associated substrate exert opposing effects on cell migration and contact inhibition of growth through tyrosine phosphorylation. Proc. Natl. Acad. Sci. USA 97, 9076-9081.
52. Yu, H.H., Zisch, A.H., Dodelet, V.C., and Pasquale, E.B. (2001). Multiple signaling interactions of Abl and Arg kinases with the EphB2 receptor. Oncogene 20, 3995-4006.
53. Zisch, A.H., Pazzagli, C., Freeman, A.L., Schneller, M., Hadman, M., Smith, J.W., Ruoslahti, E., and Pasquale, E.B. (2000). Replacing two conserved tyrosines of the Eph32 receptor with glutamic acid prevents binding of SH2 domains without abrogating kinase activity and biological responses. Oncogene 19, 177-187.