Tyrosine phosphorylation of the CrkII adaptor protein modulates cell migration

Journal of Cell Science

Volumn 116, Issue 15, 2003, Pages 3145-3155

  Takino, Takahisa ^a   Tamura, Masahito ^a   Miyamori, Hisashi ^b   Araki, Masaru ^a   Matsumoto, Kazue ^a   Sato, Hiroshi ^b   Yamada, Kenneth M ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b KANAZAWA UNIVERSITY   (Japan)

Author keywords

Cell migration; CrkII; Phosphatase; PTP1B; Tyrosine phosphorylation

Indexed keywords

ADAPTOR PROTEIN; FIBRONECTIN; FOCAL ADHESION KINASE; MUTANT PROTEIN; PAXILLIN; PHENYLALANINE; PROTEIN P130; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; BINDING AFFINITY; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

CELL MOVEMENT; CELLS, CULTURED; CRK-ASSOCIATED SUBSTRATE PROTEIN; CYTOSKELETAL PROTEINS; FIBRONECTINS; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MUTATION; PAXILLIN; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-TYROSINE-PHOSPHATASE; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CRK; RECOMBINANT PROTEINS; RETINOBLASTOMA-LIKE PROTEIN P130; RNA, SMALL INTERFERING; TYROSINE;

EID: 0042887439     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00632     Document Type: Article

References (35)

1. Abassi, Y. A. and Vuori, K. (2002). Tyrosine 221 in CrkII regulates adhesion-dependent membrane localization of Crk and Rac and activation of Rac signaling. EMBO J. 17, 4571-4582.
2. Akagi, T., Shishido, T., Murata, K. and Hanafusa, H. (2000). v-Crk activates the phosphoinositide 3-kinase/Akt pathway in transformation. Proc. Natl. Acad. Sci. USA 97, 7290-7295.
3. Altun-Gultekin, Z. F., Chandriani, S., Bougeret, C., Ishizaki, T., Narumiya, S., de Graaf, P., van Bergen en Henegouwen, P., Hanafusa, H., Wagner, J. A. and Birge, R. B. (1998). Activation of Rho-dependent cell spreading and focal adhesion biogenesis by the v-Crk adaptor protein. Mol. Cell. Biol. 18, 3044-3058.
4. Arregui, C. O., Balsamo, J. and Lilien, J. (1998). Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J. Cell Biol. 143, 861-873.
5. Birge, R. B., Fajardo, J. E., Mayer, B. J. and Hanafusa, H. (1992). Tyrosine-phosphorylated 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.
6. Bjorge, J. D., Pang, A. and Fujita, D. J. (2000). Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J. Biol. Chem. 275, 41439-41446.
7. Byon, J. C., Kenner, K. A., Kusari, A. B. and Kusari, J. (1997). Regulation of growth factor-induced signaling by protein-tyrosine-phosphatases. Proc. Soc. Exp. Biol. Med. 216, 1-20.
8. Cheng, A., Bal, G. S., Kennedy, B. P. and Tremblay, M. L. (2001). Attenuation of adhesion-dependent signaling and cell spreading in transformed fibroblasts lacking protein tyrosine phosphatase-1B. J. Biol. Chem. 276, 25848-25855.
9. Dickens, M., Rogers, J. S., Cavanagh, J., Raitano, A., Xia, Z., Halpem, J. R., Greenberg, M. E., Sawyers, C. L. and Davis, R. (1997). A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277, 693-696.
10. Escalante, M., Courtney, J., Chin, W. G., Teng, K. K., Kim, J. I., Fajardo, J. E., Mayer, B. J., Hempstead, B. L. and Birge, R. B. (2000). Phosphorylation of c-Crk II on the negative regulatory Tyr222 mediates nerve growth factor-induced cell spreading and morphogenesis. J. Biol. Chem. 275, 24787-24797.
11. Feller, S. M., Posern, G., Voss, J., Kardinal, C., Sakkab, D., Zheng, J. and Knudsen, B. S. (1998). Physiological signals and oncogenesis mediated through Crk family adapter proteins. J. Cell. Physiol. 177, 535-552.
12. Frangioni, J. V., Beahm, P. H., Shifrin, V., Jost, C. A. and Neel, B. G. (1992). The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 68, 545-560.
13. Giradin, S. E. and Yaniv, M. (2001). A deirect interaction between JNK1 and CrkII is critical for Rac1-induced JNK activation. EMBO J. 20, 3437-3446.
14. Haj, F. G., Markova, B., Klaman, L. D., Bohmer, F. D. and Neel, B. G. (2003). Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatase-1B. J. Biol. Chem. 278, 739-744.
15. Harding, T. C., Xue, L., Bienemann, A., Haywood, D., Dickens, M., Tolkovsky, A. M. and Uney, J. B. (2001). Inhibition of JNK by overexpression of the JNK binding domain of JIP-1 prevents apoptosis in sympathetic neurons. J. Biol. Chem. 276, 4531-4534.
16. Hashimoto, Y., Katayama, H., Kiyokawa, E., Ota, S., Kurata, T., Gotoh, N., Otsuka, N., Shibata, M. and Matsuda, M. (1998). Phosphorylation of CrkII adaptor protein at tyrosine 221 by epidermal growth factor receptor. J. Biol. Chem. 273, 17186-17191.
17. Ito, M., Yoshioka, K., Akechi, M., Yamashita, S., Takamatsu, N., Sugiyama, K., Hibi, M., Nakabeppu, Y., Shiba, T. and Yamamoto, K. (1999). JSAP1, a novel Jun N-terminal protein kinase (JNK)-binding protein that functions as a scaffold factor in the JNK signaling pathway. Mol. Cell. Biol. 19, 7539-7548.
18. Kain, K. H. and Klemke, R. L. (2001). Inhibition of cell migration by Ab1 family tyrosine kinases through uncoupling of Crk-CAS complexes. J. Biol. Chem. 276, 16185-16192.
19. Kiyokawa, E., Hashimoto, Y., Kobayashi, S., Sugimura, H., Kurata, T. and Matsuda, M. (1998a). Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12, 3331-3336.
20. Kiyokawa, E., Hashimoto, Y., Kurata, T., Sugimura, H. and Matsuda, M. (1998b). Evidence that DOCK180 up-regulates signals from the CrkII-p130(Cas) complex. J. Biol. Chem. 273, 24479-24484.
21. 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.
22. Levchenko, A., Bruck, J. and Sternberg, P. W. (2000). Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc. Natl. Acad. Sci. USA 97, 5818-5823.
23. Liu, F., Hill, D. E. and Chernoff, J. (1996). Direct binding of the proline-rich region of protein tyrosine phosphatase 1B to the Src homology 3 domain of p130(Cas). J. Biol. Chem. 271, 31290-31295.
24. Liu, F., Sells, M. A. and Chernoff, J. (1998). Protein tyrosine phosphatase 1B negatively regulates integrin signaling. Curr. Biol. 8, 173-176.
25. Matsuda, M. and Kurata, T. (1996). Emerging components of the Crk oncogene product: the first identified adaptor protein. Cell. Signal. 8, 335-340.
26. Mayer, B. J., Hamaguchi, A and Hanafusa, H. (1988). A novel viral oncogene with structural similarity to phospholipase C. Nature 332, 272-275.
27. Ohba, Y., Ikuta, K., Ogura, A., Matsuda, J., Mochizuki, N., Nagashima, K., Kurokawa, K., Mayer, B. J., Maki, K., Miyazaki, J. et al. (2001). Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 20, 3333-3341.
28. Okada, S., Matsuda, M., Anafi, M., Pawson, T. and Pessin, J. E. (1998). Insulin regulates the dynamic balance between Ras and Rap1 signaling by coordinating the assembly states of the Grb2-SOS and CrkII-C3G complexes. EMBO J. 17, 2554-2565.
29. Rosen, M. K., Yamazaki, T., Gish, G. D., Kay, C. M., Pawson, T. and Kay, L. E. (1995). Direct demonstration of an intramolecular SH2-phosphotyrosine interaction in the Crk protein. Nature 374, 477-479.
30. Smith, J. J., Richardson, A., Kopf, J., Yoshida, M., Hollingsworth, R. E. and Kornbluth, S. (2002). Apoptotic regulation by the Crk adapter protein mediated by interactions with Wee1 and Crm1/Exportin. Mol. Cell. Biol. 22, 1412-1423.
31. Takino, T., Nakada, M., Miyamori, H., Yamashita, J., Yamada, K. M. and Sato, H. (2003). CrkI apaptor protein modulates cell migration and invasion in glioblastoma. Cancer Res. 63, 2335-2337.
32. Tamura, M., Gu, J., Matsumoto, K., Aota, S., Parsons, R. and Yamada, K. M. (1998). Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280, 1614-1617.
33. Tamura, M., Gu, J., Danen, E. H., Takino, T., Miyamoto, S. and Yamada, K. M. (1999a). PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 274, 20693-20703.
34. Tamura, M., Gu, J., Takino, T. and Yamada, K. M. (1999b). Tumor suppressor PTEN inhibition of cell invasion, migration, and growth: differential involvement of focal adhesion kinase and p130Cas. Cancer Res. 59, 442-449.
35. 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.