Early adhesion induces interaction of FAK and Fyn in lipid domains and activates raft-dependent Akt signaling in SW480 colon cancer cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 12, 2008, Pages 2323-2331

  Baillat, Gilbert ^a   Siret, Carole ^a   Delamarre, Estelle ^a   Luis, Jose ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Akt 1; Early adhesion; FAK; Lipid domain; SFK; Signal transduction

Indexed keywords

COMPLEMENTARY DNA; FOCAL ADHESION KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE;

ARTICLE; AUTOPHOSPHORYLATION; CANCER CELL; CELL ADHESION; COLON CANCER; COLON CARCINOGENESIS; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; LIPID RAFT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; BETA-CYCLODEXTRINS; BLOTTING, WESTERN; CAVEOLAE; CELL ADHESION; CHOLESTEROL; COLONIC NEOPLASMS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; IMMUNOPRECIPITATION; INTEGRINS; MEMBRANE MICRODOMAINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-FYN; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANSFECTION; TUMOR CELLS, CULTURED; TYROSINE;

EID: 55049119303     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.08.008     Document Type: Article

References (40)

1. Calalb M.B., Polte T.R., and 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
2. Schlaepfer D.D., and Hunter T. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16 (1996) 5623-5633
3. Schlaepfer D.D., and Mitra S.K. Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 14 (2004) 92-101
4. Parsons J.T. Focal adhesion kinase: the first ten years. J. Cell Sci. 116 (2003) 1409-1416
5. Klinghoffer R.A., Sachsenmaier C., Cooper J.A., and Soriano P. Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18 (1999) 2459-2471
6. Frame M.C. Src in cancer: deregulation and consequences for cell behaviour. Biochim. Biophys. Acta 1602 (2002) 114-130
7. Liang X., Nazarian A., Erdjument-Bromage H., Bornmann W., Tempst P., and Resh M.D. Heterogeneous fatty acylation of Src family kinases with polyunsaturated fatty acids regulates raft localization and signal transduction. J. Biol. Chem. 276 (2001) 30987-30994
8. Galbiati F., Razani B., and Lisanti M.P. Emerging themes in lipid rafts and caveolae. Cell 106 (2001) 403-411
9. Kusumi A., and Suzuki K. Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim. Biophys. Acta 1746 (2005) 234-251
10. Mitra S.K., and Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18 (2006) 516-523
11. Fantini J., Abadie B., Tirard A., Remy L., Ripert J.P., el Battari A., and Marvaldi J. Spontaneous and induced dome formation by two clonal cell populations derived from a human adenocarcinoma cell line, HT29. J. Cell Sci. 83 (1986) 235-249
12. Kadi A., Pichard V., Lehmann M., Briand C., Braguer D., Marvaldi J., Rognoni J.B., and Luis J. Effect of microtubule disruption on cell adhesion and spreading. Biochem. Biophys. Res. Commun. 246 (1998) 690-695
13. Remacle-Bonnet M., Garrouste F., Baillat G., Andre F., Marvaldi J., and Pommier G. Membrane rafts segregate pro- from anti-apoptotic insulin-like growth factor-I receptor signaling in colon carcinoma cells stimulated by members of the tumor necrosis factor superfamily. Am. J. Pathol. 167 (2005) 761-773
14. Calalb M.B., Zhang X., Polte T.R., and Hanks S.K. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228 (1996) 662-668
15. Munoz P., Navarro M.C., Pavon E.J., Salmeron J., Malavasi F., Sancho J., and Zubiaur M. CD38 signaling in T cells is initiated within a subset of membrane rafts containing Lck and the CD3-{zeta} subunit of the T cell antigen receptor. J. Biol. Chem. 278 (2003) 50791-50802
16. Talamonti M.S., Roh M.S., Curley S.A., and Gallick G.E. Increase in activity and level of pp60c-src in progressive stages of human colorectal cancer. Clin. Invest. 91 (1993) 53-60
17. Cobb B.S., Schaller M.D., Leu T.H., and Parsons J.T. Stable association of pp60src and pp59fyn with the focal adhesion-associated protein tyrosine kinase, pp125FAK. Mol. Cell. Biol. 14 (1994) 147-155
18. Webb D.J., Donais K., Whitmore L.A., Thomas S.M., Turner C.E., Parsons J.T., and Horwitz A.F. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6 (2004) 154-161
19. Schlaepfer D.D., and Hunter T. Focal adhesion kinase overexpression enhances Ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J. Biol. Chem. 272 (1997) 13189-13195
20. Stupack D.G., and Cheresh D.A. Get a ligand, get a life: integrins, signaling and cell survival. J. Cell Sci. 115 (2002) 3729-3738
21. Chen H.C., Appeddu P.A., Isoda H., and Guan J.L. Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J. Biol. Chem. 271 (1996) 26329-26334
22. Adam R.M., Mukhopadhyay N.K., Kim J., Di Vizio D., Cinar B., Boucher K., Solomon K.R., and Freeman M.R. Cholesterol sensitivity of endogenous and myristoylated Akt. Cancer Res. 67 (2007) 6238-6246
23. Windham T.C., Parikh N.U., Siwak D.R., Summy J.M., McConkey D.J., Kraker A.J., and Gallick G.E. Src activation regulates anoikis in human colon tumor cell lines. Oncogene 21 (2002) 7797-7807
24. Hakomori S.I. Cell adhesion/recognition and signal transduction through glycosphingolipid microdomain. Glycoconj. J. 17 (2000) 143-151
25. Iwabuchi K., Yamamura S., Prinetti A., Handa K., and Hakomori S.I. GM3-enriched Microdomain involved in cell adhesion and signal transduction through carbohydrate-carbohydrate interaction in mouse melanoma B16 cells. J. Biol. Chem. 273 (1998) 9130-9138
26. Le Y., Honczarenko M., Glodek A.M., Ho D.K., and Silberstein L.E. CXC chemokine ligand 12-induced focal adhesion kinase activation and segregation into membrane domains is modulated by regulator of G protein signaling 1 in Pro-B cells. J. Immunol. 174 (2005) 2582-2590
27. Gaus K., Le Lay S., Balasubramanian N., and Schwartz M.A. Integrin-mediated adhesion regulates membrane order. J. Cell Biol. 174 (2006) 725-734
28. Xu L.H., Yang X., Craven R.J., and Cance W.G. The COOH-terminal domain of the focal adhesion kinase induces loss of adhesion and cell death in human tumor cells. Cell Growth Differ. 9 (1998) 999-1005
29. Wei W.C., Hsu Y.C., Chiu W.T., Wang C.Z., Wu C.M., Wang Y.K., Shen M.R., and Tang M.J. Low substratum rigidity of collagen gel promotes ERK phosphorylation via lipid raft to augment cell migration. J. Cell. Biochem. 103 (2007) 1111-1124
30. Lenne P.F., Wawrezinieck L., Conchonaud F., Wurtz O., Boned A., Guo X.J., Rigneault H., He H.T., and Marguet D. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25 (2006) 3245-3256
31. Sandilands E., Brunton V.G., and Frame M.C. The membrane targeting and spatial activation of Src, Yes and Fyn is influenced by palmitoylation and distinct RhoB/RhoD endosome requirements. J. Cell Sci. 120 (2007) 2555-2564
32. Shima T., Nada S., and Okada M. Transmembrane phosphoprotein Cbp senses cell adhesion signaling mediated by Src family kinase in lipid rafts. Proc. Natl. Acad. Sci. 100 (2003) 14897-14902
33. Kostic A., and Sheetz M.P. Fibronectin rigidity response through Fyn and p130Cas recruitment to the leading edge. Mol. Biol. Cell. 17 (2006) 2684-2695
34. Peres C., Yart A., Perret B., Salles J.P., and Raynal P. Modulation of phosphoinositide 3-kinase activation by cholesterol level suggests a novel positive role for lipid rafts in lysophosphatidic acid signalling. FEBS Lett. 534 (2003) 164-168
35. Decker L., and Ffrench-Constant C. Lipid rafts and integrin activation regulate oligodendrocyte survival. J. Neurosci. 24 (2004) 3816-3825
36. Arcaro A., Aubert M., Espinosa del Hierro M.E., Khanzada U.K., Angelidou S., Tetley T.D., Bittermann A.G., Frame M.C., and Seckl M.J. Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signalling. Cell Signal. 19 (2007) 1081-1092
37. Müller E.J., Williamson L., Kolly C., and Suter M.M. Outside-in signaling through integrins and cadherins: a central mechanism to control epidermal growth and differentiation?. J. Invest. Dermatol. 128 (2008) 501-516
38. Bouchard V., Demers M.J., Thibodeau S., Laquerre V., Fujita N., Tsuruo T., Beaulieu J.F., Gauthier R., Vézina A., Villeneuve L., and Vachon P.H. Fak/Src signaling in human intestinal epithelial cell survival and anoikis: differentiation state-specific uncoupling with the PI3-K/Akt-1 and MEK/Erk pathways. J. Cell. Physiol. 212 (2007) 717-728
39. Basson M.D. An intracellular signal pathway that regulates cancer cell adhesion in response to extracellular forces. Cancer Res. 68 (2008) 2-4
40. Katz B.Z., Miyamoto S., Teramoto H., Zohar M., Krylov D., Vinson C., Gutkind J.S., and Yamada K.M. Direct transmembrane clustering and cytoplasmic dimerization of focal adhesion kinase initiates its tyrosine phosphorylation. Biochim. Biophys. Acta 1592 (2002) 141-152