Collagen IV regulates Caco-2 cell spreading and p130Cas phosphorylation by FAK-dependent and FAK-independent pathways

Biological Chemistry

Volumn 389, Issue 1, 2008, Pages 47-55

  Sanders, Matthew A ^a,b   Basson, Marc D ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cell spreading; Focal adhesion kinase; Intestinal epithelial cell; p130 Cas; SH3 domain; Type IV collagen

Indexed keywords

COLLAGEN TYPE 4; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; PROTEIN P130; PROTEIN SH3; SMALL INTERFERING RNA;

ARTICLE; CELL ADHESION; CELL SPREADING; CELL STRAIN CACO 2; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

CACO-2 CELLS; CELL ADHESION; CELL PROLIFERATION; COLLAGEN TYPE IV; CRK-ASSOCIATED SUBSTRATE PROTEIN; CULTURE MEDIA; FOCAL ADHESION KINASE 2; HUMANS; PHOSPHORYLATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION;

RATTUS;

EID: 37349026319     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2008.008     Document Type: Article

References (43)

1. Armulik, A., Velling, T., and Johansson, S. (2004). The integrin β1 subunit transmembrane domain regulates phosphatidylinositol 3-kinase-dependent tyrosine phosphorylation of Crk-associated substrate. Mol. Biol. Cell 15, 2558-2567.
2. Astier, A., Avraham, H., Manie, S.N., Groopman, J., Canty, T., Avraham, S., and Freedman, A.S. (1997). The related adhesion focal tyrosine kinase is tyrosine-phosphorylated after β1-integrin stimulation in B cells and binds to p130cas. J. Biol. Chem. 272, 228-232.
3. Basson, M.D. (1998). Role of integrins in enterocyte migration. Clin. Exp. Pharmacol. Physiol. 25, 280-285.
4. Basson, M.D. (2001). In vitro evidence for matrix regulation of intestinal epithelial biology during mucosal healing. Life Sci. 69, 3005-3018.
5. Beaulieu, J.F. (1992). Differential expression of the VLA family of integrins along the crypt-villus axis in the human small intestine. J. Cell Sci. 102, 427-436.
6. Beaulieu, J.F. (1997). Extracellular matrix components and integrins in relationship to human intestinal epithelial cell differentiation. Prog. Histochem. Cytochem. 31, 1-78.
7. Cary, L.A., Chang, J.F., and Guan, J.L. (1996). Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J. Cell Sci. 109, 1787-1794.
8. Cary, L.A., Han, D.C., Polte, T.R., Hanks, S.K., and Guan, J.L. (1998). Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J. Cell Biol. 140, 211-221.
9. Cohen, L.A. and Guan, J.L. (2005). Mechanisms of focal adhesion kinase regulation. Curr. Cancer Drug Targets 5, 629-643.
10. Cukierman, E., Pankov, R., Stevens, D.R., and Yamada, K.M. (2001). Taking cell-matrix adhesions to the third dimension. Science 294, 1708-1712.
11. Dignass, A.U. (2001). Mechanisms and modulation of intestinal epithelial repair. Inflamm. Bowel Dis. 7, 68-77.
12. Goldberg, G.S., Alexander, D.B., Pellicena, P., Zhang, Z.Y., Tsuda, H., and Miller, W.T. (2003). Src phosphorylates Cas on tyrosine 253 to promote migration of transformed cells. J. Biol. Chem. 278, 46533-46540.
13. Harte, M.T., Hildebrand, J.D., Burnham, M.R., Bouton, A.H., and Parsons, J.T. (1996). p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase. J. Biol. Chem. 271, 13649-13655.
14. Hildebrand, J.D., Taylor, J.M., and Parsons, J.T. (1996). An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol. Cell Biol. 16, 3169-3178.
15. Huang, J., Hamasaki, H., Nakamoto, T., Honda, H., Hirai, H., Saito, M., Takato, T., and Sakai, R. (2002). Differential regulation of cell migration, actin stress fiber organization, and cell transformation by functional domains of Crk-associated substrate. J. Biol. Chem. 277, 27265-27272.
16. Ilic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., and Yamamoto, T. (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
17. Keogh, R.J., Houliston, R.A., and Wheeler-Jones, C.P. (2002). Human endothelial Pyk2 is expressed in two isoforms and associates with paxillin and p130Cas. Biochem. Biophys. Res. Commun. 290, 1470-1477.
18. Cas to the guanine nucleotide exchange factor C3G. J. Biol. Chem. 273, 25673-25679.
19. Lakkakorpi, P.T., Nakamura, I., Nagy, R.M., Parsons, J.T., Rodan, G.A., and Duong, L.T. (1999). Stable association of PYK2 and p130(Cas) in osteoclasts and their co-localization in the sealing zone. J. Biol. Chem. 274, 4900-4907.
20. Lamorte, L., Rodrigues, S., Sangwan, V., Turner, C.E., and Park, M. (2003). Crk associates with a multimolecular Paxillin/GIT2/β-PIX complex and promotes Rac-dependent relocalization of Paxillin to focal contacts. Mol. Biol. Cell 14, 2818-2831.
21. Liu, Y., Loijens, J.C., Martin, K.H., Karginov, A.V., and Parsons, J.T. (2002). The association of ASAP1, an ADP ribosylation factor-GTPase activating protein, with focal adhesion kinase contributes to the process of focal adhesion assembly. Mol. Biol. Cell 13, 2147-2156.
22. Lussier, C., Basora, N., Bouatrouss, Y., and Beaulieu, J.F. (2000). Integrins as mediators of epithelial cell-matrix interactions in the human small intestinal mucosa. Microsc. Res. Tech. 51, 169-178.
23. Madri, J.A., Pratt, B.M., and Yannariello-Brown, J. (1988). Matrix-driven cell size change modulates aortic endothelial cell proliferation and sheet migration. Am. J. Pathol. 132, 18-27.
24. Mitra, S.K., Hanson, D.A., and Schlaepfer, D.D. (2005). Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68.
25. Nakamoto, T., Sakai, R., Honda, H., Ogawa, S., Ueno, H., Suzuki, T., Aizawa, S., Yazaki, Y., and Hirai, H. (1997). Requirements for localization of p130cas to focal adhesions. Mol. Cell. Biol. 17, 3884-3897.
26. Parsons, J.T. (2003). Focal adhesion kinase: the first ten years. J. Cell Sci. 116, 1409-1416.
27. Peterson, M.D. and Mooseker, M.S. (1993). An in vitro model for the analysis of intestinal brush border assembly. I. Ultrastructural analysis of cell contact-induced brush border assembly in Caco-2BBe cells. J. Cell Sci. 105, 445-460.
28. Peterson, M.D., Bement, W.M., and Mooseker, M.S. (1993). An in vitro model for the analysis of intestinal brush border assembly. II. Changes in expression and localization of brush border proteins during cell contact-induced brush border assembly in Caco-2BBe cells. J. Cell Sci. 105, 461-472.
29. Petit, V., Boyer, B., Lentz, D., Turner, C.E., Thiery, J.P., and Valles, A.M. (2000). Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J. Cell Biol. 148, 957-970.
30. Podolsky, D.K. (1999). Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: the best offense is a good defense. Am. J. Physiol. 277, G495-499.
31. Polte, T.R. and Hanks, S.K. (1995). Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc. Natl. Acad. Sci. USA 92, 10678-10682.
32. 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.
33. Sanders, M.A. and Basson, M.D. (2000). Collagen IV-dependent ERK activation in human Caco-2 intestinal epithelial cells requires focal adhesion kinase. J. Biol. Chem. 275, 38040-38047.
34. Sanders, M.A. and Basson, M.D. (2004). Collagen IV regulates Caco-2 migration and ERK activation via α1β1- and α2β1-integrin- dependent Src kinase activation. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G547-557.
35. Sanders, M.A. and Basson, M.D. (2005). p130cas but not paxillin is essential for Caco-2 intestinal epithelial cell spreading and migration on collagen IV. J. Biol. Chem. 280, 23516-23522.
36. Shin, N.Y., Dise, R.S., Schneider-Mergener, J., Ritchie, M.D., Kilkenny, D.M., and Hanks, S.K. (2004). Subsets of the major tyrosine phosphorylation sites in Crk-associated substrate (CAS) are sufficient to promote cell migration. J. Biol. Chem. 279, 38331-38337.
37. Sieg, D.J., Ilic, D., Jones, K.C., Damsky, C.H., Hunter, T., and Schlaepfer, D.D. (1998). Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK-cell migration. EMBO J. 17, 5933-5947.
38. Taylor, J.M., Hildebrand, J.D., Mack, C.P., Cox, M.E., and Parsons, J.T. (1998). Characterization of graf, the GTPase-activating protein for rho associated with focal adhesion kinase. Phosphorylation and possible regulation by mitogen-activated protein kinase. J. Biol. Chem. 273, 8063-8070.
39. Taylor, J.M., Macklem, M.M., and Parsons, J.T. (1999). Cytoskeletal changes induced by GRAF, the GTPase regulator associated with focal adhesion kinase, are mediated by Rho. J. Cell Sci. 112, 231-242.
40. Wang, J.Y. (2005). Polyamines regulate expression of E-cadherin and play an important role in control of intestinal epithelial barrier function. Inflammopharmacology 13, 91-101.
41. Yano, H., Uchida, H., Iwasaki, T., Mukai, M., Akedo, H., Nakamura, K., Hashimoto, S., and Sabe, H. (2000). Paxillin α 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.
42. Yano, H., Mazaki, Y., Kurokawa, K., Hanks, S.K., Matsuda, M., and Sabe, H. (2004). Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J. Cell Biol. 166, 283-295.
43. Yu, C.F., Sanders, M.A., and Basson, M.D. (2000). Human caco-2 motility redistributes FAK and paxillin and activates p38 MAPK in a matrix-dependent manner. Am. J. Physiol. Gastrointest. Liver Physiol. 278, G952-966.