A novel role for Lsc/p115 RhoGEF and LARG in regulating RhoA activity downstream of adhesion to fibronectin

Journal of Cell Science

Volumn 120, Issue 22, 2007, Pages 3989-3998

  Dubash, Adi D ^a   Wennerberg, Krister ^a   García Mata, Rafael ^a   Menold, Marisa M ^a   Arthur, William T ^a   Burridge, Keith ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Cell spreading; Extracellular matrix; Fibronectin; Focal adhesions; Guanine nucleotide exchange factors; Leukemia associated RhoGEF; Lsc; p115 RhoGEF; RhoA; Stress fibers

Indexed keywords

FIBRONECTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; PROTEIN DBL; PROTEIN ECT2; PROTEIN LEUKEMIA ASSOCIATED RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN LSC; PROTEIN P115; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL SPREADING; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FOCAL ADHESION; GENE OVEREXPRESSION; MUTANT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRESS FIBER;

ANIMALS; CELL ADHESION; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESIONS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICE; MUTANT PROTEINS; NIH 3T3 CELLS; PROTEIN TRANSPORT; RATS; RECEPTORS, G-PROTEIN-COUPLED; RHOA GTP-BINDING PROTEIN; STRESS FIBERS;

EID: 37249071435     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.003806     Document Type: Article

References (49)

1. Arthur, W. T. and Burridge, K. (2001). RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol. Biol. Cell 12, 2711-2720.
2. Arthur, W. T., Petch, L. A. and Burridge, K. (2000). Integrin engagement suppresses RhoA activity via a c-Srr-dependent mechanism. Curr. Biol. 10, 719-722.
3. Arthur, W. T., Ellerbroek, S. M., Der, C. J., Burridge, K. and Wennerberg, K. (2002). XPLN, a guanine nucleotide exchange factor for RhoA and RhoB, but not RhoC. J. Biol. Chem. 277, 42964-42972.
4. Aukhil, I., Joshi, P., Yan, Y. and Erickson, H. P. (1993). Cell- and heparin-binding domains of the hexabrachion arm identified by tenascin expression proteins. J. Biol. Chem. 268, 2542-2553.
5. Bass, M. D. and Humphries, M. J. (2002). Cytoplasmic interactions of syndecan-4 orchestrate adhesion receptor and growth factor receptor signalling. Biochem. J. 368, 1-15.
6. Bass, M. D., Roach, K. A., Morgan, M. R., Mostafavi-Pour, Z., Schoen, T., Muramatsu, T., Mayer, U., Ballestrem, C., Spatz, J. P. and Humphries, M. J. (2007). Syndecan4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J. Cell Biol. 177, 527-538.
7. Bhattacharyya, R. and Wedegaertner, P. B. (2003a). Characterization of Gα 13-dependent plasma membrane recruitment of p115RhoGEF. Biochem. J. 371, 709-720.
8. Bhattacharyya, R. and Wedegaertner, P. B. (2003b). Mutation of an N-terminal acidic-rich region of p1l5-RhoGEF dissociates α13 binding and α13-promoted plasma membrane recruitment. FEBS Lett. 540, 211-216.
9. Boudreau, N. J. and Jones, P. L. (1999). Extracellular matrix and integrin signalling: the shape of things to come. Biochem. J. 339, 481-488.
10. Bourguignon, L. Y., Singleton, P. A., Zhu, H. and Diedrich, F. (2003). Hyaluronan-mediated CD44 interaction with RhoGEF and Rho kinase promotes Grb2-associated binder-1 phosphorylation and phosphatidylinositol 3-kinase signaling leading to cytokine (macrophage-colony stimulating factor) production and breast tumor progression. J. Biol. Chem. 278, 29420-29434.
11. 2+ signaling, and cytoskeleton modification in head and neck squamous cell carcinoma cells. J. Biol. Chem. 281, 14026-14040.
12. Burridge, K. and Wennerberg, K. (2004). Rho and Rac take center stage. Cell 116, 167-179.
13. Chikumi, H., Fukuhara, S. and Gutkind, J. S. (2002). Regulation of G protein-linked guanine nucleotide exchange factors for Rho, PDZ-RhoGEF, and LARG by tyrosine phosphorylation: evidence of a role for focal adhesion kinase. J. Biol. Chem. 277, 12463-12473.
14. Chikumi, H., Barac, A., Behbahani, B., Gao, Y., Teramoto, H., Zheng, Y. and Gutkind, J. S. (2004). Homo- and hetero-oligomerization of PDZ-RhoGEF, LARG and p115RhoGEF by their C-terminal region regulates their in vivo Rho GEF activity and transforming potential. Oncogene 23, 233-240.
15. Defilippi, P., Olivo, C., Venturino, M., Dolce, L., Silengo, L. and Tarone, G. (1999). Actin cytoskeleton organization in response to integrin-mediated adhesion. Microsc. Res. Tech. 47, 67-78.
16. Disatnik, M. H., Boutet, S. C., Lee, C. H., Mochly-Rosen, D. and Rando, T. A. (2002). Sequential activation of individual PKC isozymes in integrin-mediated muscle cell spreading: a role for MARCKS in an integrin signaling pathway. J. Cell Sci. 115, 2151-2163.
17. Dovas, A., Yoneda, A. and Couchman, J. R. (2006). PKCα-dependent activation of RhoA by syndecan-4 during focal adhesion formation. J. Cell Sci. 119, 2837-2846.
18. Engvall, E. and Ruoslahti, E. (1977). Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer 20, 1-5.
19. Francis, S. A., Shen, X., Young, J. B., Kaul, P. and Lerner, D. J. (2006). Rho GEF Lsc is required for normal polarization, migration, and adhesion of formyl-peptide-stimulated neutrophils. Blood 107, 1627-1635.
20. Fukuhara, S., Chikumi, H. and Gutkind, J. S. (2001). RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho? Oncogene 20, 1661-1668.
21. Garcia-Mata, R., Wennerberg, K., Arthur, W. T., Noren, N. K., Ellerbroek, S. M. and Burridge, K. (2006). Analysis of activated GAPs and GEFs in cell lysates. Meth. Enzymol. 406, 425-437.
22. Hashimoto-Uoshima, M., Yang Y. Z., Schneider, G. and Aukhil, I. (1997). The alternatively spliced domains EIIIB and EIIIA of human fibronectin affect cell adhesion and spreading. J. Cell Sci. 110, 2271-2280.
23. Holinstat, M., Mehta, D., Kozasa, T., Minshall, R. D. and Malik, A. B. (2003). Protein kinase Cα-induced p115RhoGEF phosphorylation signals endothelial cytoskeletal rearrangement. J. Biol. Chem. 278, 28793-28798.
24. Hornstein, I., Alcover, A. and Katzav, S. (2004). Vav proteins, masters of the world of cytoskeleton organization. Cell. Signal. 16, 1-11.
25. Hotulainen, P. and Lappalainen, P. (2006). Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173, 383-394.
26. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
27. Krendel, M., Zenke, F. T. and Bokoch, G. M. (2002). Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4, 294-301.
28. Kristelly, R., Gao, G. and Tesmer, J. J. (2004). Structural determinants of RhoA binding and nucleotide exchange in leukemia-associated Rho guanine-nucleotide exchange factor. J. Biol. Chem. 279, 47352-47362.
29. Liu, B. P. and Burridge, K. (2000). Vav2 activates Rac1, Cdc42, and RhoA downstream from growth factor receptors but not beta1 integrins. Mol. Cell. Biol. 20, 7160-7169.
30. Meller, N., Merlot, S. and Guda, C. (2005). CZH proteins: a new family of Rho-GEFs. J. Cell Sci. 118, 4937-4946.
31. Moon, S. Y. and Zheng, Y. (2003). Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13, 13-22.
32. Nobes, C. D. and Hall, A. (1995). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
33. Noren, N. K., Arthur, W. T. and Burridge, K. (2003). Cadherin engagement inhibits RhoA via p190RhoGAP. J. Biol. Chem. 278, 13615-13618.
34. Pankov, R. and Yamada, K. M. (2002). Fibronectin at a glance. J. Cell Sci. 115, 3861-3863.
35. Price, L. S., Leng, J., Schwartz, M. A. and Bokoch, G. M. (1998). Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 9, 1863-1871.
36. Ren, X. D., Kiosses, W. B. and Schwartz, M. A. (1999). Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578-585.
37. Reuther, G. W., Lambert, Q. T., Booden, M. A., Wennerberg, K., Becknell, B., Marcucci, G., Sondek, J., Caligiuri, M. A. and Der, C. J. (2001). Leukemia-associated Rho guanine nucleotide exchange factor, a Dbl family protein found mutated in leukemia, causes transformation by activation of RhoA. J. Biol. Chem. 276, 27145-27151.
38. Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
39. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
40. Rossman, K. L. and Sondek, J. (2005). Larger than Dbl: new structural insights into RhoA activation. Trends Biochem. Sci. 30, 163-165.
41. Rossman, K L., Der, C. J. and Sondek, J. (2005). GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180.
42. Saoncella, S., Echtermeyer, F., Denhez, F., Nowlen, J. K., Mosher, D. F., Robinson, S. D., Hynes, R. O. and Goetinck, P. F. (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.
43. Suzuki, N., Nakamura, S., Mano, H. and Kozasa, T. (2003). Gα: 12 activates Rho GTPase through tyrosine-phosphorylated leukemia-associated RhoGEF Proc. Natl. Acad. Sci. USA 100, 733-738.
44. Swiercz, J. M., Kuner, R., Behrens, J. and Offermanns, S. (2002). Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35, 51-63.
45. Taya, S., Inagaki, N., Sengiku, H., Makino, H., Iwamatsu, A., Urakawa, I., Nagao, K., Kataoka, S. and Kaibuchi, K. (2001). Direct interaction of insulin-like growth factor-1 receptor with leukemia-associated RhoGEF. J. Cell Biol. 155, 809-820.
46. Wang, R., Clark, R. A., Mosher, D. F. and Ren, X. D. (2005). Fibronectin's central cell-binding domain supports focal adhesion formation and Rho signal transduction. J. Biol. Chem. 280, 28803-28810.
47. Worthylake, D. K., Rossman, K. L. and Sondek, J. (2000). Crystal structure of Rac1 in complex with the guanine nucleotide exchange region of Tiam1. Nature 408, 682-688.
48. Zhai, J., Lin, H., Nie, Z., Wu, J., Canete-Soler, R., Schlaepfer, W. W. and Schlaepfer, D. D. (2003). Direct interaction of focal adhesion kinase with p190RhoGEF. J. Biol. Chem. 278, 24865-24873.
49. Zhang, X. F., Schaefer, A. W., Burnette, D. T., Schoonderwoert, V. T. and Forscher, P. (2003). Rho-dependent contractile responses in the neuronal growth cone are independent of classical peripheral retrograde actin flow. Neuron 40, 931-944.