Disruption of Ca2+-dependent cell-matrix adhesion enhances c-Src kinase activity, but causes dissociation of the c-Src/FAK complex and dephosphorylation of tyrosine-577 of FAK in carcinoma cells

Experimental Cell Research

Volumn 293, Issue 1, 2004, Pages 1-13

  Lin, Eva H ^a   Hui, Angela Y ^a   Meens, Jalna A ^a   Tremblay, Eric A ^a   Schaefer, Erik ^b   Elliott, Bruce E ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b BioSource International   (United States)

Author keywords

Anchorage independent growth; c Src; Cell matrix adhesion; FAK; Fibronectin; Signaling

Indexed keywords

CALCIUM; FIBRONECTIN; FOCAL ADHESION KINASE; POLYSTYRENE; TYROSINE; FOCAL ADHESION KINASE 1; PHENYLALANINE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE C SRC; PROTEIN-TYROSINE KINASE C-SRC; PTK2 PROTEIN, MOUSE;

ADHERENT CELL; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BREAST CARCINOMA; BREAST EPITHELIUM; CARCINOMA CELL; CELL ADHESION; CELL DISRUPTION; CELL SPREADING; CELL SUSPENSION; CORRELATION ANALYSIS; DEPHOSPHORYLATION; EMBRYO; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; MOUSE; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; AMINO ACID SUBSTITUTION; ANIMAL; CARCINOMA; CELL MEMBRANE; CHEMISTRY; ENZYME ACTIVATION; EXPERIMENTAL NEOPLASM; GENETICS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; TUMOR CELL LINE;

AMINO ACID SUBSTITUTION; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CARCINOMA; CELL LINE, TUMOR; CELL-MATRIX JUNCTIONS; ENZYME ACTIVATION; FIBRONECTINS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; MAMMARY NEOPLASMS, ANIMAL; MICE; PHENYLALANINE; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TYROSINE;

EID: 0347320586     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.09.008     Document Type: Article

References (58)

1. Boyer B., Valles A.M., Edme N. Induction and regulation of epithelial-mesenchymal transitions. Biochem. Pharmacol. 60:2000;1091-1099.
2. Humphries M.J., Mould A.P. Structure. An anthropomorphic integrin. Science. 294:2001;316-317.
3. Loftus J.C., Liddington R.C. New insights into integrin-ligand interaction. J. Clin. Invest. 100:1997;S77-S81.
4. Yamada K.M., Geiger B. Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9:1997;76-85.
5. Thomas S.M., Brugge J.S. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13:1997;513-609.
6. Cas to SH2 and SH3 domains of Src kinase. J. Biol. Chem. 271:1996;8959-8965.
7. Turner C.E. Paxillin and focal adhesion signalling. Nat. Cell Biol. 2:2000;E231-E236.
8. c-src protein kinase is an early event in colonic carcinogenesis. Proc. Natl. Acad. Sci. U. S. A. 87:1990;558-562.
9. Cartwright C.A., Coad C.A., Egbert B.M. Elevated c-Src tyrosine kinase activity in premalignant epithelia of ulcerative colitis. J. Clin. Invest. 93:1994;509-515.
10. c-src in progressive stages of human colorectal cancer. J. Clin. Invest. 91:1993;53-60.
11. van Oijen M.G., Rijksen G., ten Broek F.W., Slootweg P.J. Overexpression of c-Src in areas of hyperproliferation in head and neck cancer, premalignant lesions and benign mucosal disorders. J. Oral Pathol. Med. 27:1998;147-152.
12. Lutz M.P., Esser I.B., Flossmann-Kast B.B., Vogelmann R., Luhrs H., Friess H., Buchler M.W., Adler G. Overexpression and activation of the tyrosine kinase Src in human pancreatic carcinoma. Biochem. Biophys. Res. Commun. 243:1998;503-508.
13. Verbeek B.S., Vroom T.M., Adriaansen-Slot S.S., Ottenhoff-Kalff A.E., Geertzema J.G., Hennipman A., Rijksen G. c-Src protein expression is increased in human breast cancer. An immunohistochemical and biochemical analysis. J. Pathol. 180:1996;383-388.
14. Guy C.T., Muthuswamy S.K., Cardiff R.D., Soriano P., Muller W.J. Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice. Genes Dev. 8:1994;23-32.
15. Webster M.A., Cardiff R.D., Muller W.J. Induction of mammary epithelial hyperplasias and mammary tumors in transgenic mice expressing a murine mammary tumor virus/activated c-Src fusion gene. Proc. Natl. Acad. Sci. U. S. A. 92:1995;7849-7853.
16. Bjorge J.D., Jakymiw A., Fujita D.J. Selected glimpses into the activation and function of Src kinase. Oncogene. 19:2000;5620-5635.
17. Jones R.J., Brunton V.G., Frame M.C. Adhesion-linked kinases in cancer; emphasis on Src, focal adhesion kinase and PI 3-kinase. Eur. J. Cancer. 36:2000;1595-1606.
18. Turner C.E., Glenney J.R.J., Burridge K. Paxillin: a new vinculin-binding protein present in focal adhesions. J. Cell Biol. 111:1990;1059-1068.
19. Lock P., Abram C.L., Gibson T., Courtneidge S.A. A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J. 17:1998;4346-4357.
20. Calalb M.B., Polte T.R., Hanks S.K. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol. 15:1995;954-963.
21. Calalb M.B., Zhang X., Polte T.R., Hanks S.K. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228:1996;662-668.
22. Verbeek B.S., Vroom T.M., Rijksen G. Overexpression of c-Src enhances cell-matrix adhesion and cell migration in PDGF-stimulated NIH3T3 fibroblasts. Exp. Cell Res. 248:1999;531-537.
23. Kaplan K.B., Swedlow J.R., Morgan D.O., Varmus H.E. c-Src enhances the spreading of src-/- fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 9:1995;1505-1517.
24. Fincham V.J., Frame M.C. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J. 17:1998;81-92.
25. FAK) in invasive human tumors. Cancer Res. 55:1995;2752-2755.
26. FAK. Nature. 380:1996;538-540.
27. Gilmore A.P., Romer L.H. Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol. Biol. Cell. 7:1996;1209-1224.
28. Hauck C.R., Sieg D.J., Hsia D.A., Loftus J.C., Gaarde W.A., Monia B.P., Schlaepfer D.D. Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res. 61:2001;7079-7090.
29. Cary L.A., Klinghoffer R.A., Sachsenmaier C., Cooper J.A. SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading. Mol. Cell. Biol. 22:2002;2427-2440.
30. Rahimi N., Hung W., Saulnier R., Tremblay E., Elliott B. c-Src kinase activity is required for hepatocyte growth factor-induced motility and anchorage-independent growth of mammary carcinoma cells. J. Biol. Chem. 273:1998;33714-33721.
31. Saulnier R., Bhardwaj B., Klassen J., Leopold D., Rahimi N., Tremblay E., Mosher D., Elliott B. Fibronectin fibrils and growth factors stimulate anchorage-independent growth of a murine mammary carcinoma. Exp. Cell Res. 222:1996;360-369.
32. Hanke J.H., Gardner J.P., Dow R.L., Changelian P.S., Brissette W.H., Weringer E.J., Pollok B.A., Connelly P.A. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271:1996;695-701.
33. Klinghoffer R.A., Sachsenmaier C., Cooper J.A., Soriano P. Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18:1999;2459-2471.
34. Rahimi N., Tremblay E., McAdam L., Park M., Schwall R., Elliott B. Identification of a hepatocyte growth factor autocrine loop in a murine mammary carcinoma. Cell Growth Differ. 7:1996;263-270.
35. Doppler W., Groner B., Ball R.K. Prolactin and glucocorticoid hormones synergistically induce expression of transfected rat beta-casein gene promoter constructs in a mammary epithelial cell line. Proc. Natl. Acad. Sci. U. S. A. 86:1989;104-108.
36. Hung W., Elliott B. Co-operative effect of c-Src tyrosine kinase and Stat3 in activation of hepatocyte growth factor expression in mammary carcinoma cells. J. Biol. Chem. 276:2001;12395-12403.
37. Cobb B.S., Parsons J.T. Regulation of the cellular Src protein tyrosine kinase: interactions of the carboxyl terminal sequences residing between the kinase domain and tyrosine-527. Oncogene. 8:1993;2897-2903.
38. Superti-Furga G. Regulation of the Src protein tyrosine kinase. FEBS Lett. 369:1995;62-66.
39. c-src. Exp. Cell Res. 260:2000;189-198.
40. Miyamoto S., Teramoto H., Gutkind J.S., Yamada K.M. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J. Cell Biol. 135:1996;1633-1642.
41. Miyamoto S., Teramoto H., Coso O.A., Gutkind J.S., Burbelo P.D., Akiyama S.K., Yamada K.M. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131:1995;791-805.
42. Bourguignon L.Y., Zhu H., Shao L., Chen Y.W. CD44 interaction with c-Src kinase promotes cortactin-mediated cytoskeleton function and hyaluronic acid-dependent ovarian tumor cell migration. J. Biol. Chem. 276:2001;7327-7336.
43. Brunton V.G., Ozanne B.W., Paraskeva C., Frame M.C. A role for epidermal growth factor receptor, c-Src and focal adhesion kinase in an in vitro model for the progression of colon cancer. Oncogene. 14:1997;283-293.
44. Poullet P., Gautreau A., Kadare G., Girault J.A., Louvard D., Arpin M. Ezrin interacts with focal adhesion kinase and induces its activation independently of cell-matrix adhesion. J. Biol. Chem. 276:2001;37686-37691.
45. McLean G.W., Fincham V.J., Frame M.C. v-Src induces tyrosine phosphorylation of focal adhesion kinase independently of tyrosine 397 and formation of a complex with Src. J. Biol. Chem. 275:2000;23333-23339.
46. Cheng A., Bal G.S., Kennedy B.P., Tremblay M.L. Attenuation of adhesion-dependent signaling and cell spreading in transformed fibroblasts lacking protein tyrosine phosphatase-1B. J. Biol. Chem. 276:2001;25848-25855.
47. Aplin A.E., Howe A., Alahari S.K., Juliano R.L. Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol. Rev. 50:1998;197-263.
48. Bibbins K.B., Boeuf H., Varmus H.E. Binding of the Src SH2 domain to phosphopeptides is determined by residues in both the SH2 domain and the phosphopeptides. Mol. Cell. Biol. 13:1993;7278-7287.
49. Xu W., Harrison S.C., Eck M.J. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 385:1997;595-602.
50. Schlessinger J. SH2/SH3 signaling proteins. Curr. Opin. Genet. Dev. 4:1994;25-30.
51. Ponzetto C., Bardelli A., Zhen Z., Maina F., dalla Zonca P., Giordano S.A.U., Panayotou G., Comoglio P.M. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell. 77:1994;261-271.
52. Fixman E., Fournier T., Kamikura D., Naujokas M., Park M. Pathways downstream of Shc and Grb2 are required for cell transformation by the Tpr-Met oncoprotein. J. Biol. Chem. 271:1996;13116-13122.
53. Frame M.C. Src in cancer: deregulation and consequences for cell behaviour. Biochim. Biophys. Acta. 1602:2002;114-130.
54. Avizienyte E., Wyke A.W., Jones R.J., McLean G.W., Westhoff M.A., Brunton V.G., Frame M.C. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat. Cell Biol. 4:2002;632-638.
55. Irby R.B., Mao W., Coppola D., Kang J., Loubeau J.M., Trudeau W., Karl R., Fujita D.J., Jove R., Yeatman T.J. Activating SRC mutation in a subset of advanced human colon cancers. Nat. Genet. 21:1999;187-190.
56. Werb Z., Sympson C.J., Alexander C.M., Thomasset N., Lund L.R., MacAuley A., Ashkenas J., Bissell M.J. Extracellular matrix remodeling and the regulation of epithelial-stromal interactions during differentiation and involution. Kidney Int. 49(Suppl. 54):1996;S68-S74.
57. Lochter A., Galosy S., Muschler J., Freedman N., Werb Z., Bissell M.J. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell Biol. 139:1997;1861-1872.
58. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer. 2:2002;161-174.