Integrin-specific signaling pathways controlling focal adhesion formation and cell migration

Journal of Cell Biology

Volumn 161, Issue 1, 2003, Pages 155-167

  Mostafavi Pour, Zohreh ^a   Askari, Janet A ^a   Parkinson, Scott J ^b   Parker, Peter J ^b   Ng, Tony T C ^c,d   Humphries, Martin J ^a,e  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d ST THOMAS HOSPITAL   (United Kingdom)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cytoskeleton; Fibronectin; PKC; Syndecan; Vinculin

Indexed keywords

FIBRONECTIN; INTEGRIN; PROTEIN KINASE C ALPHA; PROTEIN KINASE C DELTA; PROTEIN KINASE C ZETA; PROTEOGLYCAN; RECEPTOR; SYNDECAN; SYNDECAN 4; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 4; VERY LATE ACTIVATION ANTIGEN 5;

ARTICLE; CELL ADHESION; CELL ASSAY; CELL MIGRATION; CELL SURFACE; CELLULAR PARAMETERS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MELANOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

CELL ADHESION; CELL MOVEMENT; EUKARYOTIC CELLS; FLUORESCENT ANTIBODY TECHNIQUE; FOCAL ADHESIONS; HUMANS; INTEGRIN ALPHA4BETA1; INTEGRIN ALPHA5BETA1; INTEGRINS; MEMBRANE GLYCOPROTEINS; MUTATION; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN KINASE C-DELTA; PROTEOGLYCANS; SIGNAL TRANSDUCTION; SYNDECAN-4; TUMOR CELLS, CULTURED;

EID: 0037437153     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200210176     Document Type: Article

References (70)

1. Baciu, P.C., and P.F. Goetinck. 1995. Protein kinase C regulates the recruitment of syndecan-4 into focal contacts. Mol. Biol. Cell. 6:1503-1513.
2. Ballestrem, C., B. Wehrle-Haller, B. Hinz, and B.A. Imhof. 2000. Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration. Mol. Biol. Cell. 11:2999-3012.
3. Barkalow, F.J., and J.E. Schwarzbauer. 1991. Localization of the major heparinbinding site in fibronectin. J. Biol. Chem. 266:7812-7818.
4. Bass, M.D., and M.J. Humphries. 2002. The cytoplasmic interactions of syndecan-4 orchestrate adhesion receptor and growth factor receptor signalling. Biochem. J. 368:1-15.
5. Bloom, L., K.C. Ingham, and R.O. Hynes. 1999. Fibronectin regulates assembly of actin filaments and focal contacts in cultured cells via the heparin-binding site in repeat III13. Mol. Biol. Cell. 10:1521-1536.
6. Bornancin, F., and P.J. Parker. 1997. Phosphorylation of protein kinase C-α on serine 657 controls the accumulation of active enzyme and contributes to its phosphatase-resistant state. J. Biol. Chem. 272:3544-3549.
7. Bouvard, D., C. Brakebusch, E. Gustafsson, A. Aszodi, T. Bengtsson, A. Berna, and R. Fassler. 2001. Functional consequences of integrin gene mutations in mice. Circ. Res. 89:211-223.
8. Bretscher, A., K. Edwards, and R.G. Fehon. 2002. ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3:586-599.
9. Buchanan, F.G., C.M. Elliot, M. Gibbs, and J.H. Exton. 2000. Translocation of the Rac1 guanine nucleotide exchange factor Tiam1 induced by platelet-derived growth factor and lysophosphatidic acid. J. Biol. Chem. 275:9742-9748.
10. Burridge, K., and M. Chrzanowska-Wodnicka. 1996. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12:463-519.
11. Chan, B.M.C., P.D. Kassner, J.A. Schiro, H.R. Byers, T.S. Kupper, and M.E. Hemler. 1992. Distinct cellular functions mediated by different VLA integrin α subunit cytoplasmic domains. Cell. 68:1051-1060.
12. Choquet, D., D.P. Felsenfeld, and M.P. Sheetz. 1997. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell. 88:39-48.
13. Echtermeyer, F., P.C. Baciu, S. Saoncella, Y. Ge, and P.F. Goetinck. 1999. Syndecan-4 core protein is sufficient for the assembly of focal adhesions and stress fibers. J. Cell Sci. 112:3433-3441.
14. Gautreau, A., D. Louvard, and M. Arpin. 2002. ERM proteins and NF2 tumor suppressor: the Yin and Yang of cortical actin organization and cell growth signaling. Curr. Opin. Cell Biol. 14:104-109.
15. Gilmore, A.P., and K. Burridge. 1996. Regulation of vinculin binding to talin and actin by phosphatidylinositol-4,5-bisphosphate. Nature. 381:531-535.
16. Hamada, K., T. Shimizu, T. Matsui, S. Tsukita, S. Tsukita, and T. Hakoshima. 2000. Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J. 19:4449-4462.
17. Han, J., S. Liu, D.M. Rose, D.D. Schlaepfer, H. McDonald, and M.H. Ginsberg. 2001. Phosphorylation of the integrin alpha 4 cytoplasmic domain regulates paxillin binding. J. Biol. Chem. 276:40903-40909.
18. Horowitz, A., and M. Simons. 1998. Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Cα. J. Biol. Chem. 273:25548-25551.
19. Huhtala, P., M.J. Humphries, J.B. McCarthy, P.M. Tremble, Z. Werb, and C.H. Damsky. 1995. Cooperative signaling by α5β1 and α4β1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin. J. Cell Biol. 129:867-879.
20. Humphries, M.J., S.K. Akiyama, A. Komoriya, K. Olden, and K.M. Yamada. 1986. Identification of an alternatively spliced site in human plasma fibronectin that mediates cell type-specific adhesion. J. Cell Biol. 103:2637-2647.
21. Humphries, M.J., A. Komoriya, S.K. Akiyama, K. Olden, and K.M. Yamada. 1987. Identification of two distinct regions of the type III connecting segment of human plasma fibronectin that promote cell type-specific adhesion. J. Biol. Chem. 262:6886-6892.
22. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687.
23. Iida, J., A.M. Meijne, T.R. Oegema, T.A. Yednock, N.L. Kovach, L.T. Furcht, and J.B. McCarthy. 1998. A role of chondroitin sulfate glycosaminoglycan binding site in α4β1 integrin-mediated melanoma cell adhesion. J. Biol. Chem. 273:5955-5962.
24. Imamura, H., K. Takaishi, K. Nakano, A. Kodama, H. Oishi, H. Shiozaki, M. Monden, T. Sasaki, and Y. Takai. 1998. Rho and Rab small G proteins coordinately reorganize stress fibers and focal adhesions in MDCK cells. Mol. Biol. Cell. 9:2561-2575.
25. Ishiguro, K., K. Kadomatsu, T. Kojima, H. Muramatsu, S. Tsuzuki, E. Nakamura, K. Kusugami, H. Saito, and T. Muramatsu. 2000. Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J. Biol. Chem. 275:5249-5252.
26. Ivaska, J., R.D. Whelan, R. Watson, and P.J. Parker. 2002. PKC epsilon controls the traffic of beta1 integrins in motile cells. EMBO J. 21:3608-3619.
27. Izzard, C.S., R. Radinsky, and L.A. Culp. 1986. Substratum contacts and cytoskeletal reorganization of BALB/c3T3 cells on a cell-binding fragment and heparin-binding fragments of plasma fibronectin. Exp. Cell Res. 165:320-336.
28. Kassner, P.D., R. Alon, T.A. Springer, and M.E. Hemler. 1995. Specialized functional properties of the integrin α4 cytoplasmic domain. Mol. Biol. Cell. 6:661-674.
29. Kozlowski, J.M., I.R. Hart, I.J. Fidler, and N. Hanna. 1984. A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice. J. Natl. Cancer Inst. 72:913-917.
30. Kunkel, T.A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA. 82:488-492.
31. Lee, D., E.-S. Oh, A. Woods, J.R. Couchman, and W. Lee. 1998. Solution structure of a syndecan-4 cytoplasmic domain and its interaction with phosphatidylinositol-4,5-bisphosphate. J. Biol. Chem. 273:13022-13029.
32. Legg, J.W., C.A. Lewis, M. Parsons, T. Ng, and C.M. Isacke. 2002. A novel PKCregulated mechanism controls CD44 ezrin association and directional cell motility. Nat. Cell Biol. 4:399-407.
33. Liu, S., and M.H. Ginsberg. 2000. Paxillin binding to a conserved sequence motif in the α4 integrin cytoplasmic domain. J. Biol. Chem. 275:22736-22742.
34. Liu, S., S.M. Thomas, D.G. Woodside, D.M. Rose, W.B. Kiosses, M. Pfaff, and M.H. Ginsberg. 1999. Binding of paxillin to α4 integrins modifies integrindependent biological responses. Nature. 402:676-681.
35. Longley, R.L., A. Woods, A. Fleetwood, G.J. Cowling, J.T. Gallagher, and J.R. Couchman. 1999. Control of morphology, cytoskeleton and migration by syndecan-4. J. Cell. Sci. 112:3421-3431.
36. Makarem, R., P. Newham, J.A. Askari, L.J. Green, J. Clements, M. Edwards, M.J. Humphries, and A.P. Mould. 1994. Competitive binding of vascular cell adhesion molecule-1 and the HepII/IIICS domain of fibronectin to the integrin α4β1. J. Biol. Chem. 269:4005-4011.
37. Manser, E., T.H. Loo, C.G. Koh, Z.S. Zhao, X.Q. Chen, L. Tan, I. Tan, T. Leung, and L. Lim. 1998. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell. 1:183-192.
38. Martel, V., C. Racaud-Sultan, S. Dupe, C. Marie, F. Paulhe, A. Galmiche, M.R. Block, and C. Albiges-Rizo. 2001. Conformation, localization, and integrin binding of talin depend on its interaction with phosphoinositides. J. Biol. Chem. 276:21217-21227.
39. McCarthy, J.B., M.K. Chelberg, D.J. Mickelson, and L.T. Furcht. 1988. Localization and chemical synthesis of fibronectin peptides with melanoma adhesion and heparin binding activities. Biochemistry. 27:1380-1388.
40. McCarthy, J.B., A.P.N. Skubitz, Z. Qi, X.-Y. Yi, D.J. Mickelson, D.J. Klein, and L.T. Furcht. 1990. RGD-independent cell adhesion to the carboxy-terminal heparin-binding fragment of fibronectin involves heparin-dependent and -independent activities. J. Cell Biol. 110:777-787.
41. McNamee, H.P., D.E. Ingber, and M.A. Schwartz. 1993. Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J. Cell Biol. 121:673-678.
42. Mostafavi-Pour, Z., J.A. Askari, J.D. Whittard, and M.J. Humphries. 2001. Identification of a novel heparin binding site in the alternatively spliced IIICS region of fibronectin: roles of integrins and proteoglycans in cell adhesion to fibronectin splice variants. Matrix Biol. 20:63-73.
43. Mould, A.P., and M.J. Humphries. 1991. Identification of a novel recognition sequence for the integrin α4β1 in the COOH-terminal heparin-binding domain of fibronectin. EMBO J. 10:4089-4095.
44. Mould, A.P., L.A. Wheldon, A. Komoriya, E.A. Wayner, K.M. Yamada, and M.J. Humphries. 1990. Affinity chromatographic isolation of the melanoma adhesion receptor for the IIICS region of fibronectin and its identification as the integrin α4β1. J. Biol. Chem. 265:4020-4024.
45. Mould, A.P., A. Komoriya, K.M. Yamada, and M.J. Humphries. 1991. The CS5 peptide is a second site in the IIICS region of fibronectin recognized by the integrin α4β1. Inhibition of α4β1 function by RGD peptide homologues. J. Biol. Chem. 266:3579-3585.
46. Mould, A.P., J.A. Askari, S.E. Craig, A.N. Garratt, J. Clements, and M.J. Humphries. 1994. Integrin α4β1-mediated melanoma cell adhesion and migration on vascular cell adhesion molecule-1 (VCAM-1) and the alternatively spliced IIICS region of fibronectin. J. Biol. Chem. 269:27224-27230.
47. Mould, A.P., J.A. Askari, S. Aota, S. Yamada, K.M. Yamada, A. Irie, Y. Takada, H.J. Mardon, and M.J. Humphries. 1997. Defining the topology of integrin α5β1-fibronectin interactions using inhibitory anti-α5 and anti-β1 monoclonal antibodies: Evidence that the synergy sequence of fibronectin is recognized by the amino-terminal repeats of the α5 subunit. J. Biol. Chem. 272:17283-17292.
48. Murakami, M., A. Horowitz, S. Tang, J.A. Ware, and M. Simons. 2002. Protein kinase C (PKC) δ regulates PKCα activity in a syndecan-4-dependent manner. J. Biol. Chem. 277:20367-20371.
49. Ng, T., D. Shima, A. Squire, P.I.H. Bastiaens, S. Gschmeissner, M.J. Humphries, and P.J. Parker. 1999a. PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18:3909-3923.
50. Ng, T., A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, et al. 1999b. Imaging protein kinase Cα activation in cells. Science. 283:2085-2089.
51. Ng, T., M. Parsons, W.E. Hughes, J. Monypenny, D. Zicha, A. Gautreau, M. Arpin, S. Gschmeissner, P.J. Verveer, P.I. Bastiaens, and P.J. Parker. 2001. Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J. 20:2723-2741.
52. Oh, E.-S., A. Woods, and J.R. Couchman. 1997a. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J. Biol. Chem. 272:8133-8136.
53. Oh, E.-S., A. Woods, and J.R. Couchman. 1997b. Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C. J. Biol. Chem. 272:11805-11811.
54. Oh, E.-S., A. Woods, S.-T. Lim, A.W. Theibert, and J.R. Couchman. 1998. Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol-4,5-bisphosphate coordinately regulate protein kinase C activity. J. Biol. Chem. 273:10624-10629.
55. Parekh, D.B., W. Ziegler, and P.J. Parker. 2000. Multiple pathways control protein kinase C phosphorylation. EMBO J. 19:496-503.
56. Parsons, M., M.D. Keppler, A. Kline, A. Messent, M.J. Humphries, R. Gilchrist, I.R. Hart, C. Quittau-Prevostel, W.E. Hughes, P.J. Parker, and T. Ng. 2002. Site-directed perturbation of PKC-integrin interaction blocks carcinoma cell chemotaxis. Mol. Cell. Biol. 22:5897-5911.
57. Podar, K., Y.T. Tai, B.K. Lin, R.P. Narsimhan, M. Sattler, T. Kijima, R. Salgia, D. Gupta, D. Chauhan, and K.C. Anderson. 2002. Vascular endothelial growth factor-induced migration of multiple myeloma cells is associated with β1 integrin- and PI3-kinase-dependent PKCα activation. J. Biol. Chem. 277:7875-7881.
58. Saoncella, S., F. Echtermeyer, F. Denhez, J.K. Nowlen, D.F. Mosher, S.D. Robinson, R.O. Hynes, and P.F. Goetinck. 1999. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl. Acad. Sci. USA. 96:2805-2810.
59. Schoenwaelder, S.M., and K. Burridge. 1999. Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 11:274-286.
60. Sharma, A., J.A. Askari, M.J. Humphries, E.Y. Jones, and D.I. Stuart. 1999. Crystal structure of a heparin and integrin-binding segment of human fibronectin. EMBO J. 18:1468-1479.
61. Shin, J., W. Lee, D. Lee, B.-K. Koo, I. Han, Y. Lim, A. Woods, J.R. Couchman, and E.-S. Oh. 2001. Solution structure of the dimeric cytoplasmic domain of syndecan-4. Biochemistry. 40:8471-8478.
62. Srivastava, J., K.J. Procyk, X. Iturrioz, and P.J. Parker. 2002. Phosphorylation is required for PMA- and cell-cycle-induced degradation of protein kinase Cδ. Biochem. J. 368:349-355. First published on September 4, 2002; 10.1042/BJ20020737.
63. Turner, C.E. 2000. Paxillin interactions. J. Cell Sci. 113:41394-4140.
64. Wang, F., V.M. Weaver, O.W. Petersen, C.A. Larabell, S. Dedhar, P. Briand, R. Lupu, and M.J. Bissell. 1998. Reciprocal interactions between β1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc. Natl. Acad. Sci. USA. 95:14821-14826.
65. Wayner, E.A., A. Garcia-Pardo, M.J. Humphries, J.A. McDonald, and W.G. Carter. 1989. Identification and characterization of the T lymphocyte adhesion receptor for an alternative cell attachment domain (CS-1) in plasma fibronectin. J. Cell Biol. 109:1321-1330.
66. Woods, A., and J.R. Couchman. 1992. Protein kinase C involvement in focal adhesion formation. J. Cell Sci. 101:277-290.
67. Woods, A., and J.R. Couchman. 1994. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol. Biol. Cell. 5:183-192.
68. Woods, A., and J.R. Couchman. 2001. Syndecan-4 and focal adhesion function. Curr. Opin. Cell. Biol. 13:578-583.
69. Woods, A., J.R. Couchman, S. Johansson, and M. Höök. 1986. Adhesion and cytoskeletal organization of fibroblasts in response to fibronectin fragments. EMBO J. 5:665-670.
70. Yamada, K.M., and B. Geiger. 1997. Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9:76-85.