Identification of Rap 1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G

Molecular and Cellular Biology

Volumn 15, Issue 12, 1995, Pages 6746-6753

  Gotoh, Takaya ^a,b   Hattori, Seisuke ^a   Nakamura, Shun ^a   Kitayama, Hitoshi ^c   Noda, Makoto ^c   Takai, Yoshimi ^d   Kaibuchi, Kozo ^e   Matsui, Hideki ^b,g   Hatase, Osamu ^b   Takahashi, Hidehiro ^f   Kurata, Takeshi ^f   Matsuda, Michiyuki ^f  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b KAGAWA UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^e NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^f NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^g OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATE; RAS PROTEIN;

ANIMAL CELL; ARTICLE; AUTOGRAPHA CALIFORNICA; CELL MEMBRANE; CELL STRAIN 3T3; CELL STRAIN COS1; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME SPECIFICITY; GENE EXPRESSION; GENE TARGETING; MOUSE; NONHUMAN; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANIMAL; BASE SEQUENCE; BINDING SITES; CELL CYCLE PROTEINS; CELL LINE; DNA PRIMERS; GTP-BINDING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); GUANOSINE DIPHOSPHATE; KINETICS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEIN PHOSPHATASE; POLYMERASE CHAIN REACTION; PROTEINS; PROTO-ONCOGENE PROTEINS; RAP GTP-BINDING PROTEINS; RAS GUANINE NUCLEOTIDE EXCHANGE FACTORS; RAS-GRF1; RECOMBINANT PROTEINS; SON OF SEVENLESS PROTEINS; SPODOPTERA; SUBSTRATE SPECIFICITY; SUPPORT, NON-U.S. GOV'T; TRANSFECTION;

EID: 0028881018     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.15.12.6746     Document Type: Article

References (70)

1. Beranger, F., B. Goud, A. Tavitian, and J. de Gunzburg. 1991. Association of the Ras-antagonistic Rap1/Krev-1 proteins with the Golgi complex. Proc. Natl. Acad. Sci. USA 88:1606-1610.
2. Birge, R. B., J. E. Fajardo, B. J. Mayer, and H. Hanafusa. 1992. Tyrosinephosphorylated epidermal growth factor receptor and cellular p130 provide high affinity binding substrates to analyze Crk-phosphotyrosine-dependent interactions in vitro. J. Biol. Chem. 267:10588-10595.
3. Birge, R. B., J. E. Fajardo, C. Reichman, S. E. Shoelson, Z. Songyang, L. C. Cantley, and H. Hanafusa. 1993. Identification and characterization of a high-affinity interaction between v-Crk and tyrosinc-phosphorylated paxillin in CT10-transformed fibroblasts. Mol. Cell. Biol. 13:4648-4656.
4. Birge, R. B., and H. Hanafusa. 1993. Closing in on SH2 specificity. Science 262:1522-1524.
5. Bonfini, L., C. A. Karlovich, C. Dasgupta, and U. Banerjee. 1992. The Son of sevenless gene product: a putative activator of Ras. Science 255:603-606.
6. Bowtell, D., P. Fu, M. Simon, and P. Senior. 1992. Identification of murine homologues of the Drosophila Son of sevenless gene: potential activators of ras. Proc. Natl. Acad. Sci. USA 89:6511-6515.
7. Broek, D., T. Toda, T. Michaeli, L. Levin, C. Birchmeier, M. Zoller, S. Powers, and M. Wigler. 1987. The S. cerevisiae CDC25 gene product regulates the R4S/adenylate cyclase pathway. Cell 48:789-799.
8. ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell 73:611-620.
9. Campa, M. J., K. J. Chang, V. Molina, B. R. Reep, and E. G. Lapetina. 1991. Inhibition of ras-induced germinal vesicle breakdown in Xenopus oocytes by rap-1B. Biochem. Biophys. Res. Commun. 174:1-5.
10. Cen, H., A. G. Papageorge, R. Zippel, D. R. Lowy, and K. Zhang. 1992. Isolation of multiple mouse cDNAs with coding homology to Saccharomyces cerevisiae CDC2S: identification of a region related to Bcr, Vav, Dbl and CDC24. EMBO J. 11:4007-4015.
11. Cook, S. J., B. Rubinfeld, I. Albert, and F. McCormick. 1993. RapV12 antagonizes Ras-dependent activation of ERK1 and ERK2 by LPA and EGF in Rat-1 fibroblasts. EMBO J. 12:3475-3485.
12. Egan, S. E., B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. A. Weinberg. 1993. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation [see comments]. Nature (London) 363:45-51.
13. Frech, M., J. John, V. Pizon, P. Chardin, A. Tavitian, R. Clark, F. McCormick, and A. Wittinghofer. 1990. Inhibition of GTPase activating protein stimulation of Ras-p21 GTPase by the Krev-1 gene product. Science 249: 169-171.
14. Fukumoto, Y., K. Kaibuchi, N. Oku, Y. Hori, and Y. Takai. 1990. Activation of the c-fos serum-response element by the activated c-Ha-ras protein in a manner independent of protein kinase C and cAMP-dependent protein kinase. J. Biol. Chem. 265:774-780.
15. Gale, N. W., S. Kaplan, E. J. Lowenstein, J. Schlessinger, and D. Bar-Sagi. 1993. Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature (London) 363:88-92.
16. Hata, Y., K. Kaibuchi, S. Kawamura, M. Hiroyoshi, H. Shirataki, and Y. Takai. 1991. Enhancement of the actions of smg p21 GDP/GTP exchange protein by the protein kinase A-catalyzed phosphorylation of smg p21. J. Biol. Chem. 266:6571-6577.
17. Hata, Y., A. Kikuchi, T. Sasaki, M. D. Schaber, J. B. Gibbs, and Y. Takai. 1990. Inhibition of the ras p21 GTPase-activating protein-stimulated GTPase activity of c-Ha-ras p21 by smg p21 having the same putative effector domain as ras p21s. J. Biol. Chem. 265:7104-7107.
18. Hiraoka, K., K. Kaibuchi, S. Ando, T. Musha, K. Takaishi, T. Mizuno, M. Asada, L. Menard, E. Tomhave, and J. Didsbury. 1992. Both stimulatory and inhibitory GDP/GTP exchange proteins, smg GDS and rho GDI, are active on multiple small GTP-binding proteins. Biochem. Biophys. Res. Commun. 182:921-930.
19. Jacquet, E., M. Vanoni, C. Ferrari, L. Alberghina, E. Martegani, and A. Parmeggiani. 1992. A mouse CDC25-like product enhances the formation of the active GTP complex of human ras p21 and Saccharomyces cerevisiae RAS2 proteins. J. Biol. Chem. 267:24181-24183.
20. Karlovich, C. A., L. Bonnni, L. McCollan, R. D. Roge, A. Daga, M. P. Czech, and U. Banerjee. 1995. In vivo functional analysis of the Ras exchange factor Son of sevenless. Science 268:576-579.
21. Kawamura, M., K. Kaibuchi, K. Kishi, and Y. Takai. 1993. Translocation of Ki-ras p21 between membrane and cytoplasm by smg GDS. Biochem. Biophys. Res. Commun. 190:832-841.
22. Kawata, M., Y. Matsui, J. Kondo, T. Hishida, Y. Teranishi, and Y. Takai. 1988. A novel small molecular weight GTP-binding protein with the same putative effector domain as the ras proteins in bovine brain membranes. Purification, determination of primary structure, and characterization. J. Biol. Chem. 263:18965-18971.
23. Kim, S., A. Mizoguchi, A. Kikuchi, and Y. Takai. 1990. Tissue and subcellular distributions of the smg-21/rap 1/Krev-1 proteins which are partly distinct from those of c-ras p21s. Mol. Cell. Biol. 10:2645-2652.
24. Kitayama, H., T. Matsuzaki, Y. Ikawa, and M. Noda. 1990. Genetic analysis of the Kirsten-ras-revertant 1 gene: potentiation of its tumor suppressor activity by specific point mutations. Proc. Natl. Acad. Sci. USA 87:4284-4288.
25. Kitayama, H., Y. Sugimoto, T. Matsuzaki, Y. Ikawa, and M. Noda. 1989. A ras-related gene with transformation suppressor activity. Cell 56:77-84.
26. Knudsen, B. S., S. M. Feller, and H. Hanafusa. 1994. Four proline-rich sequences of the guanine-nucleotide exchange factor C3G bind with unique specificity to the first Src homology 3 domain of Crk. J. Biol. Chem. 269: 32767.
27. Koch, C. A., D. Anderson, M. F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252:668-674.
28. Lehmann, J. M., G. Riethmuller, and J. P. Johnson. 1990. Nck, a melanoma cDNA encoding a cytoplasmic protein consisting of the src homology units SH2 and SH3. Nucleic Acids Res. 18:1048.
29. Li, N., A. Batzer, R. Daly, V. Yajnik, E. Skolnik, P. Chardin, D. Bar-Sagi, B. Margolis, and J. Schlessinger. 1993. Guanine-nuclcotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature (London) 363:85-88.
30. Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E. Y. Skolnik, D. Bar-Sagi, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70:431-442.
31. Martegani, E., M. Vanoni, R. Zippel, P. Coccetti, R. Brambilla, C. Ferrari, E. Sturani, and L. Alberghina. 1992. Cloning by functional complementation of a mouse cDNA encoding a homologue of CDC25, a Saccharomyces cerevisiae RAS activator. EMBO J. 11:2151-2157.
32. Matsuda, M., Y. Hashimoto, K. Muroya, H. Hasegawa, T. Kurata, S. Tanaka, S. Nakamura, and S. Hattori. 1994. CRK protein binds to two guanine nucleotide-releasing proteins for the Ras family and modulates nerve growth factor-induced activation of Ras in PC12 cells. Mol. Cell. Biol. 14:5495-5500.
33. gag-crk, to a broad range of phosphotyrosine-containing proteins. Science 248:1537-1539.
34. Matsuda, M., S. Tanaka, S. Nagata, A. Kojima, T. Kurata, and M. Shibuya. 1992. Two species of human CRK cDNA encode proteins with distinct biological activities. Mol. Cell. Biol. 12:3482-3489.
35. Matsui, Y., A. Kikuchi, M. Kawata, J. Kondo, Y. Teranishi, and Y. Takai. 1990. Molecular cloning of smg p21B and identification oismg p21 purified from bovine brain and human platelets as smg p21B. Biochem. Biophys. Res. Commun. 166:1010-1016.
36. Matsuura, Y., R. D. Possee, H. A. Uverton, and D. H. L. Bishop. 1987. Baculovirus expression vector: the requirements for high level expression of proteins, including glycoproteins. J. Gen. Virol. 68:1233-1250.
37. Matuoka, K., M. Shibata, A. Yamakawa, and T. Takenawa. 1992. Cloning of ASH, a ubiquitous protein composed of one Src homology region (SH) 2 and two SH3 domains, from human and rat cDNA libraries. Proc. Natl. Acad. Sci. USA 89:9015-9019.
38. Mayer, B. J., M. Hamaguchi, and H. Hanafusa. 1988. A novel viral oncogene with structural similarity to phospholipase C. Nature (London) 332:272-275.
39. Mayer, B. J., H. Hirai, and R. Sakai. 1995. Evidence that SH2 domains promote processive phosphorylation by protein-tyrosine kinases. Curr. Biol. 5:296-305.
40. Mayer, B. J., R. Ren, K. L. Clark, and D. Baltimore. 1993. A putative modular domain present in diverse signaling proteins. Cell 73:629-630.
41. McCoy, M. S., C. I. Bargmann, and R. A. Weinberg. 1984. Human colon carcinoma Ki-rai2 oncogene and its corresponding proto-oncogene. Mol. Cell. Biol. 4:1577-1582.
42. Mistou, M. Y., E. Jacquet, P. Poullet, H. Rensland, P. Gideon, I. Schlichting, A. Wittinghofer, and A. Parmeggiani. 1992. Mutations of Ha-ras p21 that define important regions for the molecular mechanism of the SDC25 C-domain, a guanine nucleotide dissociation stimulator. EMBO J. 11:2391-2397.
43. Mizuno, T., K. Kaihuchi, T. Yamamoto, M. Kawamura, T. Sakoda, H. Fujioka, Y. Matsuura, and Y. Takai. 1991. A stimulatory GDP/GTP exchange protein for smg p21 is active on the post-translationally processed form of c-Ki-ras p21 and rhoA p21. Proc. Natl. Acad. Sci. USA 88:6442-6446.
44. Mosteller, R. D., J. Han, and D. Broek. 1994. Identification of residues of the H-ras protein critical for functional interaction with guanine nucleotide exchange factors. Mol. Cell. Biol. 14:1104-1112.
45. ras in rat pheochromocytoma PC12 cells. Oncogene 7:277-281.
46. Nakanishi, H., K. Kaibuchi, S. Orita, N. Ueno, and Y. Takai. 1994. Different functions of Smgm GDP dissociation stimulator and mammalian counterpart of yeast Crfc25. J. Biol. Chem. 269:15085-15091.
47. Nassar, N., G. Horn, C. Herrmann, A. Sherer, F. McCormick, and A. Wittinghofer. 1995. The 2.2 Å crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf-1 in complex with RaplA and a GTP analogue. Nature (London) 375:554-560.
48. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-200.
49. Noda, M., H. Kitayama, T. Matsuzaki, Y. Sugimoto, H. Okayama, R. H. Bassin, and Y. Ikawa. 1989. Detection of genes with a potential for suppressing the transformed phenotype associated with activated ras genes. Proc. Natl. Acad. Sci. USA 86:162-166.
50. Noda, M., Z. Selinger, E. M. Scolnick, and R. H. Bassin. 1983. Flat revertants isolated from Kirsten sarcoma virus-transformed cells are resistant to the action of specific oncogenes. Proc. Natl. Acad. Sci. USA 80:5602-5606.
51. Pawson, T., and G. D. Gish. 1992. SH2 and SH3 domains: from structure to function. Cell 71:359-362.
52. Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Carallo, G. Forni, I. Nicoletti, T. Pawson, and P. G. Pelicci. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93-104.
53. Pizon, V., P. Chardin, I. Lerosey, B. Olofsson, and A. Tavitian. 1988. Human cDNAs rap1 and rap2 homologous to the Drosophila gene Dras3 encode proteins closely related to ras in the 'effector' region. Oncogene 3:201-204.
54. Ren, R., B. J. Mayer, P. Cicchetti, and D. Baltimore. 1993. Identification of a ten-amino acid proline-rich SH3 binding site. Science 259:1157-1161.
55. Rozakis-Adcock, M., R. Fernley, J. Wade, T. Pawson, and D. Bowtell. 1993. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1. Nature (London) 363:83-85.
56. Sakai, R., A. Iwamatsu, N. Hirano, S. Ogawa, T. Tanaka, H. Mano, Y. Yazaki, and H. Hirai. 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.
57. Sakoda, T., K. Kaibuchi, K. Kishi, S. Kishida, K. Doi, M. Hoshino, S. Hattori, and Y. Takai. 1992. smg/rap 1/Krev-1 p21s inhibit the signal pathway to the c-fos promoter/enhancer from c-Ki-ras p21 but not from c-raf-1 kinase in NIH3T3 cells. Oncogene 7:1705-1711.
58. Sawasdikosoi, S., K. S. Ravichandran, K. K. Lee, J. H. Chang, and S. J. Burakoff. 1995. Crk interacts with tyrosine-phosphorylated p116 upon T cell activation. J. Biol. Chem. 270:2893-2896.
59. Schaller, M. D., and J. T. Parsons. 1995. pp125(FAK)-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for crk. Mol. Cell. Biol. 15:2635-2645.
60. Schlessinger, J. 1993. How receptor tyrosine kinases activate Ras. Trends Biochem. Sci. 18:273-275.
61. Schlessinger, J. 1994. SH2/SH3 signaling proteins. Curr. Opin. Genet. Dev. 4:25-30.
62. Shou, C., C. L. Farnsworth, B. G. Neel, and L. A. Feig. 1992. Molecular cloning of cDNAs encoding a guanine-nucleotide-releasing factor for Ras p21. Nature (London) 358:351-354.
63. Simon, M. A., D. D. Bowtell, G. S. Dodson, T. R. Laverty. and G. M. Rubin. 1991. Rasl and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67: 701-716.
64. Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Fajardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, and L. C. Cantley. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.
65. Songyang, Z., S. E. Shoelson, J. McGlade, P. Olivier, T. Pawson, X. R. Bustelo, M. Barbacid, H. Sabe, H. Hanafusa, T. Yi, R. Ren, D. Baltimore, S. Ratnofskj, R. A. Feldman, and L. C. Cantley. 1994. Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14:2777-2785.
66. Tanaka, S., S. Hattori, T. Kurata, K. Nagashima, Y. Fukui, S. Nakamura, and M. Matsuda. 1993. Both the SH2 and SH3 domains of human CRK protein are required for neuronal differentiation of PC12 cells. Mol. Cell. Biol. 13:4409-4415.
67. Tanaka, S., T. Morishita, Y. Hashimoto, S. Hattori, S. Nakamura, M. Shibuya, K. Matuoka, T. Takenawa, T. Kurata, K. Nagashima, and M. Matsuda. 1994. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins. Proc. Natl. Acad. Sci. USA 91:3443-3447.
68. Verrotti, A. C., J, B. Crechet, F. Di Blasi, G. Seidita, M. G. Mirisola, C. Kavounis, V. Nastopoulos, E. Burderi, E. De Vendittis, and A. Parmeggiani. 1992. RAS residues that are distant from the GDP binding site play a critical role in dissociation factor-stimulated release of GDP. EMBO J. 11:2855-2862.
69. Yoshida, Y., M. Kawata, Y. Miura, T. Musha, T. Sasaki, A. Kikuchi, and Y. Takai. 1992. Microinjection of smg/rap 1/Krev-1 p21 into Swiss 3T3 cells induces DNA synthesis and morphological changes. Mol. Cell. Biol. 12: 3407-3414.
70. Zhang, K., M. Noda, W. C. Vass, A. G. Papageorge, and D. R. Lowy. 1990. Identification of small clusters of divergent amino acids that mediate the opposing effects of ras and Krev-1. Science 249:162-165.