EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLCγ signaling pathway

Journal of Cell Science

Volumn 111, Issue 5, 1998, Pages 615-624

  Xie, Heng ^a   Pallero, Manuel A ^a   Gupta, Kiran ^a   Chang, Philip ^a   Ware, Margaret F ^b   Witke, Walter ^c,d   Kwiatkowski, David J ^c   Lauffenburger, Douglas A ^b   Murphy Ullrich, Joanne E ^a   Wells, Alan ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b USA   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Adhesion; Cell matrix interaction; EGF receptor; Focal contact; Migration

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GELSOLIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C;

ARTICLE; CELL ADHESION; CELL MOTILITY; FIBROBLAST; PRIORITY JOURNAL;

ADHESIONS; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL ADHESION; CELL LINE; CELL MOVEMENT; FIBROBLASTS; GELSOLIN; HETEROZYGOTE; HOMOZYGOTE; ISOENZYMES; MICE; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 0031939434     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Arora, P. D. and McCulloch, C. A. G. (1996) Dependence of fibroblast migration on actin severing activity of gelsolin, J. Cell Biol. 271, 20516-20523.
2. Bornfeldt, K. E., Raines, E. W., Nakano. T., Graves, L. M., Krebs, E. G. and Ross, R. (1994). Insulin-like growth factor-1 and platelet-derived growth factor-BB induce directed migration of human arterial smooth muscle cells via signalling pathways that are distinct from those of proliteration, J. Clin, Invest. 93, 1266-1274.
3. Bornfeldt, K. E., Raines, E. W., Graves, L. M., Skinner. M. R., Krebs. E. G. and Ross, R. (1995). Platelet-derived growth factor. Distinct signal transduction pathways associated with migration versus proliferation. Ann NY Acad. Sci. 766, 416-430.
4. Barridge, K., Fath, K., Kelly, T., Nuckolls, G. and Turner. C. (1988) Focal adhesions: transmembrane junctions between the extracellular matrix and cytoskeleton. Annu. Rev. Cell Biol. 4, 487-525.
5. Burridge, K. and Chrzanowska-Wodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518.
6. Chen, P., Gupta, K. and Wells, A. (1994a). Cell movement elicited by epidermal growth factor receptor requires kinase and autophosphorylation but is separable from mitogenesis. J. Cell Biol. 124, 547-555.
7. Chen, P., Xie, H., Sekar, M. C., Gupta, K. B. and Wells, A. (1994b). Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but MAP kinase activity is not sufficient for induced cell movement. J. Cell Biol. 127, 847-857.
8. Chen, P., Murphy-Ullrich, J. and Wells, A. (1996). A role for gelsolin in actuating EGF receptor-mediated cell motility. J. Cell Biol. 134, 689-698.
9. Clark, R. A. F. (1996). The Molecular and Cellular Biology of Wound Repair, Plenum Press, NY.
10. Cobb, M. H., Hepler, J. E., Cheng, M. and Robbins, D. (1994) The mitogen-activated protein kinases, ERKI and ERK2, Semin. Cancer Biol. 5, 261-268.
11. Couchman, J. R., Rees, D. A., Green, M. R. and Smith, C. G. (1982). Fibronectin has a dual role in locomotion and anchorage of primary chick fibroblasts and can promote entry into the division cycle. J. Cell Biol. 93, 402-410.
12. Crowley, E. and Horwitz, A. F. (1995). Tyrosine phosphorylation and cytoskeletal tension regulate release of fibroblast adhesions. J. Cell Biol. 131, 525-537.
13. Decker, S. J. (1993). Transmembrane signaling by epidermal growth factor receptors lacking autophosphorylation sites. J. Biol. Chem. 268, 9176-9179.
14. Dedhar, S. and Hannigan, G. E. (1996). Integrin cytoplasmic interactions and bidirectional transmembrane signalling, Curr. Opin. Cell Biol. 8, 657-669.
15. Derman, M. P., Chen, J. Y., Spokes, K. C., Songyang, Z. and Cantley, L. G. (1996). An 11-amino acid sequence from c-met initiates epithelial chemotaxis via phosphatidylinositol 3-kinase and phospholipase C. J. Biol. Chem. 271, 4251-4255.
16. Dudley, D. T., Pang, L., Decker, S. J., Bridges, A. J. and Saltiel, A. R. (1995). A synthetic inhibitor of the mitogen-activated protein kinase cascade, Proc. Nat. Acad. Sci. USA 92, 7686-7689.
17. Dunlevy, J. R. and Couchman, J. R. (1993). Controlled induction of focal adhesion disassembly and migration in primary fibroblasts, J. Cell Sci. 105, 489-500.
18. Hendey, B. and Maxfied, F. R. (1993). Regulation of neutrophil motility and adhesion by intracellular calcium transients, Blood Cells 19, 143-161.
19. Herman, B., Harrington, M. A., Olashaw, N. E. and WJ, P. (1986) Identification of the cellular mechanisms responsible for platelet-derived growth factor induced alterations in cytoplasmic vinculin distribution, J. Cell. Physiol. 126. 115-125.
20. Herman, B., Roe, M. W., Harris, C., Wray, B. and Clemmons, D. (1987) Platelet-derived growth factor-induced alterations in vinculin distribution in porcine vascular smooth muscle cells. Cell Motil. Cytoskel. 8, 91-105.
21. Hinrichsen, R. D. (1993). Calcium and calmodulin in the control of cellular behavior and motility. Biochem. Biophys. Acta 1155, 277-293.
22. Hotchin, N. A. and Hall, A. (1995). The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases, J. Cell Biol. 131, 1857-1865.
23. Hughes, P. E., Renshaw, M. W., Pfaff, M., Forsyth, J., Keivens, V. M., Schwartz, M. A. and Ginsberg, M. H. (1997). Suppression of integrin activation: a novel function of a ras/raf-initiated MAP kinase pathway. Cell 88, 521-530.
24. Janmey, P. A. and Stossel, T. P. (1987) Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate. Nature 325, 362-364.
25. Janmey, P. A. (1994). Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu. Rev. Physiol. 56, 169-91.
26. Jay, P. Y., Pham, P. A., Wong, S. A. and Elson, E. L. (1995). A mechanical function of myosin II in cell motility, J. Cell Sci. 108, 387-393.
27. Klemke, R. L., Cai. S., Giannini, A. L., Gallagher, P. J., deLanerolle. P. and Cheresh. D. A. (1997). Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137, 481-492.
28. Kundra, V., Kscobedo, J. A., Kazlauskas. A., Kim. H. K., Rhee. S. G., Williams, L. T. and Zetter, B. R. (1994). Regulation of chemotasis by the platelet-densed growth factor receptor-β. Nature 367, 474-476.
29. Lauffenburger. D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
30. 2+- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 377, 75-79.
31. Lu, P. J., Shieh. W. R., Rhee. S. G., Yin. H. L. and Chen. C. S. (1996). Lipid products of phosphoinositide 3-kinase bind human protilin with high affinity, Biochemistry 35, 14027-14034.
32. Manske, M. and Bade, E. G. (1994). Growth factor-induced cell migration: biology and methods of analysis. Int. Rev. Cytol. 155, 49-96.
33. FAK) and promotes migration and invasion by oral squamous cell carcinoma cells. J. Biol. Chem. 269, 31807-31813.
34. Milasincic. D. J., Calera, M. R., Farmer, S. R. and Pilch, P. F. (1996) Stimulation of C2C12 myoblast growth by basic fibroblast growth factor and insulin-like growth factor 1 can occur via mitogen-activated protein kinase-dcpendcnt and -independent pathways. Mol. Cell Biol. 16, 5964-5973.
35. Mitchison, T. J. and Cramer, L. P. (1996) Actin-based cell motilily and cell locomotion. Cell 84, 371 -379.
36. Murphy-Ullrich, J. E., Gurusiddappa, S., Frazier, W. A. and Hook, M. (1993). Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity. J. Biol. Chem. 268, 26784-26789.
37. Murphy-Ullrich, J. E., Pallero, M. A., Boerth, N., Greenwood, J. A., Lincoln, T. M. and Cornwell, T. L. (1996). Cyclic GMP-dependent protein kinasc is required for thrombospondin and tenascin mediated focal adhesion disassembly. J. Cell Sci. 109, 2499-2508.
38. Palecek, S. P., Schmidt, C. K., Lauffenburger, D. A. and Horwitz, A. F. (1996). Integrin dynamics on the uropodal region of migrating fibroblasts. J. Cell Sci. 109, 941-952.
39. Palecek, S. P., Loftus, J. C., Ginsburg, M. H., Lauffenburger, D. A. and Horwitz, A. F. (1997). Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness, Nature 385, 537-540.
40. Regen, C. M. and Horwitz, A. F. (1992). Dynamics of β1 integrin-mediated adhesive contacts in motile fibroblasts. J. Cell Biol. 119, 1347-1359.
41. Siegal, G. P., Wang, M.-H., Rinehart, C. A., Kennedy, J. W., Goodly, L. J., Miller, Y., Kaufman, D. G. and Singh, R. K. (1993). Development of a novel human extracellular matrix for quantitation of the invasiveness of human cells. Cancer Lett. 69, 123-132.
42. Singh, S. S., Chauhan. A., Murakami, N. and Chauhan, V. P. (1996) Profilin and gelsolin stimulate phosphatidylinositol 3-kinase activity. Biochemistry 35, 16544-16549.
43. Smith, R. J., Sam, L. M., Justen, J. M., Bundy. G. L., Bala, G. A. and Bleasdale, J. E. (1990). Receptor-coupled signal transduction in human polymorphonuclcar neutrophils: effects of a novel inhibitor of phospholipase C-dependent processes on cell responsiveness, J. Pharmacol. Exp. Ther 253, 688-697.
44. Stossel, T. P. (1993). On the crawling of animal cells, Science 260, 1086-1094.
45. Tidball, J. G. and Spencer, M. J. (1993). PDGF stimulation induces phosphorylation of talin and eytoskeletal reorganisation in skeletal muscle. J. Cell Biol. 123, 627-635.
46. Usami, S., Chen. H. H., Zhao. Y., Chien. S. and Skalak, R. (1993). Design and construction of a linear shear stress flow chamber Annu. Biomed. Eng. 21, 77-83.
47. VanEpps-Fung, M., Hardy. R. W., Williford, J., Gupta. K. and Wells, A. (1996). EGF induces glucose storage in transgenic 3T3-L1 adipocytes overexpressing EGF receptors. Diabetes 45, 1619-1625
48. Varner, J. A., Emerson, D. A. and Juliano. R. L. (1995). Integrin alpha 5 beta I expression negatively regulates cell growth: reversal by attachment to fibronectin. Mol. Biol. Cell 6, 725-740.
49. Volberg, T., Geiger, B., Kam, Z., Pankov, R., Simcha, I., Sabany, H., C , J. L., Adamson, E. and Ben-Ze'ev, A. (1995). Focal adhesion formation by F9 embryonal carcinoma cells after vinculin gene disruption. J. Cell Biol. 108, 2253-2260.
50. Waskiewicz, A. J. and Cooper, J. A. (1995). Mitogen and stress resp pathways: MAP kinase cascades and phosphatase regulation in mamals and yeast. Curr. Opin. Cell Biol 7, 798-805.
51. Wells, A. and Bishop, J. M. (1988). Genetic determinants of neopla transformation by the retroviral oncogene v-erbB. Proc. Nat. Acad. Sci. USA 85, 7597-7601.
52. Wells, A., Welsh, J. B., Lazar, C. S., Wiley, H. S., Gill, G. N. and Rosenfeld M. G. (1990). Ligand-induced transformation by a non internalizing EGF receptor. Science 247, 962-964.
53. Welsh, J. B., Gill, G. N., Rosenfeld, M. G. and Wells, A. (1991) A negative feedback loop attenuates EGF-induccd morphological changes. J. Cell Biol. 114, 533-543.
54. Wennstrom, S., Siegbahn, A., Yokote, K., Arvidsson. A. K., Heldin, C. Mori, S. and Claesson-Welsh, L. (1994). Membrane ruffling chemotaxis transduced by the PBDFß-receptor require the binding site phosphatidylinositol 3′ kinase. Oncogene 9, 651-660.
55. Witke, W., Sharpe, A. H., Hartwig, J. H., Azuma, T., Stossel, T. P. Kwiatkowski, D. J. (1995). Hcmostatic. inflammatory, and fibrob responses are blunted in mice lacking gelsolin. Cell 81, 41-51.
56. Woods, A., McCarthy, J. B., Furcht, L. T. and Couchman, J. R. (1993) synthetic peptide from the COOH-terminal heparin-binding domain fibronectin promotes focal adhesion formation. Mol. Biol. Cell 4, 605
57. Wright, J. D., Reuter, C. W. M. and Weber, M. J. (1995). An incom program of cellular tyrosine phosphorylations induced by kinase-def epidermal growth factor receptors. J. Biol. Chem. 270, 12085-12093.
58. Zimmerman, A. and Keller, H. (1992). Effects of staurosporine, K 252a other structurally related protein kinase inhibitors on shape and locom of Walker carcinosarcoma cells Brit. J. Cancer 66, 1077-1082.