Translocation of CrkL to Focal Adhesions Mediates Integrin-Induced Migration Downstream of Src Family Kinases

REFERENCES

• Anderson, S. M., E. A. Burton, and B. L. Koch. 1997. Phosphorylation of Cbl following stimulation with interleukin-3 and its association with Grb2, Fyn, and phosphatidylinositol 3-kinase. J. Biol. Chem. 272: 739–745.
   PubMedGoogle Scholar
• Bear, J. E., J. J. Loureiro, I. Libova, R. Fassler, J. Wehland, and F. B. Gertler. 2000. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101: 717–728.
   PubMed Web of Science ®Google Scholar
• Brown, M. C., J. A. Perrotta, and C. E. Turner. 1996. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol. 135: 1109–1123.
   PubMed Web of Science ®Google Scholar
• Brugnera, E., L. Haney, C. Grimsley, M. Lu, S. F. Walk, A. C. Tosello-Trampont, I. G. Macara, H. Madhani, G. R. Fink, and K. S. Ravichandran. 2002. Unconventional Rac-GEF activity is mediated through the Dock180 ELMO complex. Nat. Cell Biol. 4: 574–582.
   PubMed Web of Science ®Google Scholar
• Butler, A. A., V. A. Blakesley, A. Koval, R. deJong, J. Groffen, and D. Le Roith. 1997. In vivo regulation of CrkII and CrkL proto-oncogenes in the uterus by insulin-like growth factor-I. Differential effects on tyrosine phosphorylation and association with paxillin. J. Biol. Chem. 272: 27660–27664.
   PubMedGoogle Scholar
• Cary, L. A., D. C. Han, T. R. Polte, S. K. Hanks, and J. L. Guan. 1998. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J. Cell Biol. 140: 211–221.
   PubMed Web of Science ®Google Scholar
• Cary, L. A., R. A. Klinghoffer, C. Sachsenmaier, and J. A. Cooper. 2002. SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading. Mol. Cell. Biol. 22: 2427–2440.
   PubMed Web of Science ®Google Scholar
• Donaldson, L. W., G. Gish, T. Pawson, L. E. Kay, and J. D. Forman-Kay. 2002. Structure of a regulatory complex involving the Abl SH3 domain, the Crk SH2 domain, and a Crk-derived phosphopeptide. Proc. Natl. Acad. Sci. USA 99: 14053–14058.
   PubMedGoogle Scholar
• Erickson, M. R., B. J. Galletta, and S. M. Abmayr. 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.
   PubMed Web of Science ®Google Scholar
• Feller, S. M. 2001. Crk family adaptors—signalling complex formation and biological roles. Oncogene 20: 6348–6371.
   PubMed Web of Science ®Google Scholar
• Gumienny, T. L., E. Brugnera, A. C. Tosello-Trampont, J. M. Kinchen, L. B. Haney, K. Nishiwaki, S. F. Walk, M. E. Nemergut, I. G. Macara, R. Francis, T. Schedl, Y. Qin, L. Van Aelst, M. O. Hengartner, and K. S. Ravichandran. 2001. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107: 27–41.
   PubMed Web of Science ®Google Scholar
• Guris, D. L., J. Fantes, D. Tara, B. J. Druker, and A. Imamoto. 2001. Mice lacking the homologue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syndrome. Nat. Genet. 27: 293–298.
   PubMedGoogle Scholar
• Hagel, M., E. L. George, A. Kim, R. Tamimi, S. L. Opitz, C. E. Turner, A. Imamoto, and S. M. Thomas. 2002. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 22: 901–915.
   PubMed Web of Science ®Google Scholar
• Hamasaki, K., T. Mimura, N. Morino, H. Furuya, T. Nakamoto, S. Aizawa, C. Morimoto, Y. Yazaki, H. Hirai, and Y. Nojima. 1996. Src kinase plays an essential role in integrin-mediated tyrosine phosphorylation of Crk-associated substrate p130Cas. Biochem. Biophys. Res. Commun. 222: 338–343.
   PubMedGoogle Scholar
• Hasegawa, H., E. Kiyokawa, S. Tanaka, K. Nagashima, N. Gotoh, M. Shibuya, T. Kurata, and M. Matsuda. 1996. DOCK180, a major CRK-binding protein, alters cell morphology upon translocation to the cell membrane. Mol. Cell. Biol. 16: 1770–1776.
   PubMed Web of Science ®Google Scholar
• Heaney, C., K. Kolibaba, A. Bhat, T. Oda, S. Ohno, S. Fanning, and B. J. Druker. 1997. Direct binding of CRKL to BCR-ABL is not required for BCR-ABL transformation. Blood 89: 297–306.
   PubMed Web of Science ®Google Scholar
• Hemmeryckx, B., A. van Wijk, A. Reichert, V. Kaartinen, R. de Jong, P. K. Pattengale, I. Gonzalez-Gomez, J. Groffen, and N. Heisterkamp. 2001. Crkl enhances leukemogenesis in BCR/ABL P190 transgenic mice. Cancer Res. 61: 1398–1405.
   PubMedGoogle Scholar
• Honda, H., T. Nakamoto, R. Sakai, and H. Hirai. 1999. p130(Cas), an assembling molecule of actin filaments, promotes cell movement, cell migration, and cell spreading in fibroblasts. Biochem. Biophys. Res. Commun. 262: 25–30.
   PubMedGoogle Scholar
• Honda, H., H. Oda, T. Nakamoto, Z. Honda, R. Sakai, T. Suzuki, T. Saito, K. Nakamura, K. Nakao, T. Ishikawa, M. Katsuki, Y. Yazaki, and H. Hirai. 1998. Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas. Nat. Genet. 19: 361–365.
   PubMed Web of Science ®Google Scholar
• Imaizumi, T., K. Araki, K. Miura, M. Araki, M. Suzuki, H. Terasaki, and K. Yamamura. 1999. Mutant mice lacking Crk-II caused by the gene trap insertional mutagenesis: Crk-II is not essential for embryonic development. Biochem. Biophys. Res. Commun. 266: 569–574.
   PubMedGoogle Scholar
• Imamoto, A., and P. Soriano. 1993. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell 73: 1117–1124.
   PubMed Web of Science ®Google Scholar
• Itoh, R. E., K. Kurokawa, Y. Ohba, H. Yoshizaki, N. Mochizuki, and M. Matsuda. 2002. Activation of Rac and Cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell. Biol. 22: 6582–6591.
   PubMed Web of Science ®Google Scholar
• Kinsella, T. M., and G. P. Nolan. 1996. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7: 1405–1413.
   PubMed Web of Science ®Google Scholar
• Kiyokawa, E., Y. Hashimoto, S. Kobayashi, H. Sugimura, T. Kurata, and M. Matsuda. 1998. Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12: 3331–3336.
   PubMed Web of Science ®Google Scholar
• Klinghoffer, R. A., C. Sachsenmaier, J. A. Cooper, and P. Soriano. 1999. Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18: 2459–2471.
   PubMed Web of Science ®Google Scholar
• Kobayashi, S., T. Shirai, E. Kiyokawa, N. Mochizuki, M. Matsuda, and Y. Fukui. 2001. Membrane recruitment of DOCK180 by binding to PtdIns(3,4,5)P3. Biochem. J. 354: 73–78.
   PubMedGoogle Scholar
• Li, L., M. Okura, and A. Imamoto. 2002. Focal adhesions require catalytic activity of Src family kinases to mediate integrin-matrix adhesion. Mol. Cell. Biol. 22: 1203–1217.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mayer, B. J., M. Hamaguchi, and H. Hanafusa. 1988. A novel viral oncogene with structural similarity to phospholipase C. Nature 332: 272–275.
   PubMed Web of Science ®Google Scholar
• Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18: 3587–3596.
   PubMed Web of Science ®Google Scholar
• Nakamoto, T., R. Sakai, H. Honda, S. Ogawa, H. Ueno, T. Suzuki, S.-I. Aizawa, Y. Yazaki, and H. Hirai. 1997. Requirements for localization of p130 cas to focal adhesions. Mol. Cell. Biol. 17: 3884–3897.
   PubMedGoogle Scholar
• Nolan, K. M., K. Barrett, Y. Lu, K. Q. Hu, S. Vincent, and J. Settleman. 1998. Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes. Genes Dev. 12: 3337–3342.
   PubMed Web of Science ®Google Scholar
• Reddien, P. W., and H. R. Horvitz. 2000. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2: 131–136.
   PubMed Web of Science ®Google Scholar
• Reichman, C. T., B. J. Mayer, S. Keshav, and H. Hanafusa. 1992. The product of the cellular crk gene consists primarily of SH2 and SH3 regions. Cell Growth Differ. 3: 451–460.
   PubMedGoogle Scholar
• Ruest, P. J., N.-Y. Shin, T. R. Polte, X. Zhang, and S. K. Hanks. 2001. Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 21: 7641–7652.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Sakai, R., T. Nakamoto, K. Ozawa, S. Aizawa, and H. Hirai. 1997. Characterization of the kinase activity essential for tyrosine phosphorylation of p130Cas in fibroblasts. Oncogene 14: 1419–1426.
   PubMedGoogle Scholar
• Salgia, R., E. Pisick, M. Sattler, J. L. Li, N. Uemura, W. K. Wong, S. A. Burky, H. Hirai, L. B. Chen, and J. D. Griffin. 1996. p130CAS forms a signaling complex with the adapter protein CRKL in hematopoietic cells transformed by the BCR/ABL oncogene. J. Biol. Chem. 271: 25198–25203.
   PubMed Web of Science ®Google Scholar
• Salgia, R., N. Uemura, K. Okuda, J. L. Li, E. Pisick, M. Sattler, R. de Jong, B. Druker, N. Heisterkamp, L. B. Chen, et al. 1995. CRKL links p210BCR/ABL with paxillin in chronic myelogenous leukemia cells. J. Biol. Chem. 270: 29145–29150.
   PubMed Web of Science ®Google Scholar
• Schaller, M. D., J. D. Hildebrand, J. D. Shannon, J. W. Fox, R. R. Vines, and J. T. Parsons. 1994. Autophosphorylation of the focal adhesion kinase, pp125 FAK , directs SH2-dependent binding of pp60 src . Mol. Cell. Biol. 14: 1680–1688.
   PubMed Web of Science ®Google Scholar
• Senechal, K., C. Heaney, B. Druker, and C. L. Sawyers. 1998. Structural requirements for function of the Crkl adapter protein in fibroblasts and hematopoietic cells. Mol. Cell. Biol. 18: 5082–5090.
   PubMedGoogle Scholar
• Sieg, D. J. 1999. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 112: 2677–2691.
   PubMed Web of Science ®Google Scholar
• Sieg, D. J., C. R. Hauck, D. Ilic, C. K. Klingbeil, E. Schaefer, C. H. Damsky, and D. D. Schlaepfer. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2: 249–256.
   PubMed Web of Science ®Google Scholar
• Tachibana, K., T. Urano, H. Fujita, Y. Ohashi, K. Kamiguchi, S. Iwata, H. Hirai, and C. Morimoto. 1997. Tyrosine phosphorylation of Crk-associated substrates by focal adhesion kinase. A putative mechanism for the integrin-mediated tyrosine phosphorylation of Crk-associated substrates. J. Biol. Chem. 272: 29083–29090.
   PubMed Web of Science ®Google Scholar
• ten Hoeve, J., C. Morris, N. Heisterkamp, and J. Groffen. 1993. Isolation and chromosomal localization of CRKL, a human crk-like gene. Oncogene 8: 2469–2474.
   PubMed Web of Science ®Google Scholar
• Thomas, S. M., P. Soriano, and A. Imamoto. 1995. Specific and redundant roles of Src and Fyn in organizing the cytoskeleton. Nature 376: 267–271.
   PubMed Web of Science ®Google Scholar
• Vuori, K., H. Hirai, S. Aizawa, and E. Ruoslahti. 1996. Introduction of p130 cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell. Biol. 16: 2606–2613.
   PubMed Web of Science ®Google Scholar
• Wu, Y. C., and H. R. Horvitz. 1998. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392: 501–504.
   PubMedGoogle Scholar
• Wu, Y. C., M. C. Tsai, L. C. Cheng, C. J. Chou, and N. Y. Weng. 2001. C. elegans CED-12 acts in the conserved crkII/DOCK180/Rac pathway to control cell migration and cell corpse engulfment. Dev. Cell 1: 491–502.
   PubMed Web of Science ®Google Scholar
• Zhou, Z., E. Caron, E. Hartwieg, A. Hall, and H. R. Horvitz. 2001. The C. elegans PH domain protein CED-12 regulates cytoskeletal reorganization via a Rho/Rac GTPase signaling pathway. Dev. Cell 1: 477–489.
   PubMed Web of Science ®Google Scholar
• Zwartkruis, F. J., R. M. Wolthuis, N. M. Nabben, B. Franke, and J. L. Bos. 1998. Extracellular signal-regulated activation of Rap1 fails to interfere in Ras effector signalling. EMBO J. 17: 5905–5912.
   PubMed Web of Science ®Google Scholar