The small GTPase R-Ras regulates organization of actin and drives membrane protrusions through the activity of PLCε

Journal of Cell Science

Volumn 119, Issue 7, 2006, Pages 1307-1319

  Ada Nguema, Aude S ^a   Xenias, Harry ^b   Sheetz, Michael P ^b   Keely, Patricia J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Actin; Ca2+; Cell adhesion; Cell spreading; Integrin; PLC; R Ras

Indexed keywords

ACTIN; CALCIUM ION; PHOSPHOLIPASE C; PHOSPHOLIPASE C EPSILON; RAS PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL SPREADING; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; FILOPODIUM; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; LAMELLIPODIUM; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CALCIUM; CELL ADHESION; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, VIRAL; CERCOPITHECUS AETHIOPS; CHELATING AGENTS; COS CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HUMANS; MAMMARY GLANDS, HUMAN; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PHOSPHOLIPASE C; PRECIPITIN TESTS; PSEUDOPODIA; RAS PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING;

ANIMALIA;

EID: 33646806089     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02835     Document Type: Article

References (80)

1. Arora, P. D., Fan, L., Sodek, J., Kapus, A. and McCulloch, C. A. (2003). Differential binding to dorsal and ventral cell surfaces of fibroblasts: effect on collagen phagocytosis. Exp. Cell Res. 286, 366-380.
2. Arora, P. D., Glogauer, M., Kapus, A., Kwiatkowski, D. J. and McCulloch, C. A. (2004). Gelsolin mediates collagen phagocytosis through a rac-dependent step. Mol. Biol. Cell 15, 588-599.
3. Bader, M. F., Doussau, F., Chasserot-Golaz, S., Vitale, N. and Gasman, S. (2004). Coupling actin and membrane dynamics during calcium-regulated exocytosis: a role for Rho and ARF GTPases. Biochim. Biophys. Acta 1742, 37-49.
4. Bailly, M., Yan, L., Whitesides, G. M., Condeelis, J. S. and Segall, J. E. (1998). Regulation of protrusion shape and adhesion to the substratum during chemotactic responses of mammalian carcinoma cells. Exp. Cell Res. 241, 285-299.
5. Bear, J. E., Svitkina, T. M., Krause, M., Schafer, D. A., Loureiro, J. J., Strasser, G.A., Maly, I. V, Chaga, O. Y., Cooper, J. A., Borisy, G. G. et al. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509-521.
6. Berrier, A. L., Mastrangelo, A. M., Downward, J., Ginsberg, M. and LaFlamme, S.E. (2000). Activated R-ras, Rac1, PI 3-kinase and PKCepsilon can each restore cell spreading inhibited by isolated integrin betal cytoplasmic domains. J. Cell Biol. 151, 1549-1560.
7. Bos, J. L., de Bruyn, K., Enserink, J., Kuiperij, B., Rangarajan, S., Rehmann, H., Riedl, J., de Rooij, J., van Mansfeld, F. and Zwartkruis, F. (2003). The role of Rap1 in integrin-mediated cell adhesion. Biochem. Soc. Trans. 31, 83-86.
8. Caron, E., Self, A. J. and Hall, A. (2000). The GTPase Rap1 controls functional activation of macrophage integrin alphaMbeta2 by LPS and other inflammatory mediators. Curr Biol. 10, 974-978.
9. Chen, C. S., Alonso, J. L., Ostuni, E., Whitesides, G. M. and Ingber, D. E. (2003). Cell shape provides global control of focal adhesion assembly. Biochem. Biophys. Res. Commun. 307,355-361.
10. Clark, G. J., Kinch, M. S., Gilmer, T. M., Burridge, K. and Der, C. J. (1996). Overexpression of the Ras-related TC21/R-Ras2 protein may contribute to the development of human breast cancers. Oncogene 12, 169-176.
11. Cole, A. L., Subbanagounder, G., Mukhopadhyay, S., Berliner, J. A. and Vora, D. K. (2003). Oxidized phospholipid-induced endothelial cell/ monocyte interaction is mediated by a cAMP-dependent R-Ras/PI3-kinase pathway. Arterioscler Thromb. Vasc. Biol. 23, 1384-1390.
12. Cox, E. A., Sastry, S. K. and Huttenlocher, A. (2001). Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol. Biol. Cell 12, 265-277.
13. Czyzyk, J., Brogdon, J. L., Badou, A., Henegariu, O., Preston Hurlburt, P., Flavell, R. and Bottomly, K. (2003). Activation of CD4 T cells by Raf-independent effectors of Ras. Proc. Natl. Acad. Sci. USA 100, 6003-6008.
14. Dubin-Thaler, B. J., Giannone, G., Dobereiner, H. G. and Sheetz, M. P. (2004). Nanometer analysis of cell spreading on matrix-coated surfaces reveals two distinct cell states and STEPs. Biophys. J. 86, 1794-1806.
15. Dunn, G. A., Zicha, D. and Fraylich, P. E. (1997). Rapid, microtubule-dependent fluctuations of the cell margin. J. Cell Sci. 110, 3091-3098.
16. Engler, A., Bacakova, L., Newman, C., Hategan, A., Griffin, M. and Discher, D. (2004). Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86, 617-628.
17. Giannone, G., Dubin-Thaler, B. J., Dobereiner, H. G., Kieffer, N., Bresnick, A. R. and Sheetz, M. P. (2004). Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443.
18. Hansen, M., Prior, I. A., Hughes, P. E., Oertli, B., Chou, F. L., Willumsen, B. M., Hancock, J. F. and Ginsberg, M. H. (2003). C-terminal sequences in R-Ras are involved in integrin regulation and in plasma membrane microdomain distribution. Biochem. Biophys. Res. Commun. 311, 829-838.
19. Itano, N., Okamoto, S., Zhang, D., Lipton, S. A. and Ruoslahti, E. (2003). Cell spreading controls endoplasmic and nuclear calcium: a physical gene regulation pathway from the cell surface to the nucleus. Proc. Natl. Acad. Sci. USA 100, 5181-5186.
20. Ivins, J. K., Yurchenco, P. D. and Lander, A. D. (2000). Regulation of neurite outgrowth by integrin activation. A Neurosci. 20, 6551-6560.
21. Jeong, H. W., Nam, J. O. and Kim, I. S. (2005). The COOH-terminal end of R-Ras alters the motility and morphology of breast epithelial cells through Rho/Rho-kinase. Cancer Res. 65, 507-515.
22. Jin, T. G., Satoh, T., Liao, Y., Song, C., Gao, X., Kariya, K., Hu, C. D. and Kataoka, T. (2001). Role of the CDC25 homology domain of phospholipase Cepsilon in amplification of Rap1 -dependent signaling. J. Biol. Chem. 276, 30301-30307.
23. Jones, N. P., Peak, J., Brader, S., Eccles, S. A. and Katan, M. (2005). PLCgammal is essential for early events in integrin signalling required for cell motility. J. Cell Sci. 118, 2695-2706.
24. Jones, S. L., Wang, J., Turck, C. W. and Brown, E. J. (1998). A role for the actin-bundling protein L-plastin in the regulation of leukocyte integrin function. Proc. Natl. Acad. Sci. USA 95, 9331-9336.
25. Keely, P. and Parise, L. (1996). The α2β1 integrin is a necessary co-receptor for collagen-induced activation of Syk and the subsequent phosphorylation of phospholipase Cγ2 in platelets. J. Biol. Chem. 271, 26668-26676.
26. Keely, P. J., Rusyn, E. V., Cox, A. D. and Parise, L. V. (1999). R-Ras signals through specific integrin alpha cytoplasmic domains to promote migration and invasion of breast epithelial cells. J. Cell Biol. 145, 1077-1088.
27. Kelley, G. G., Reks, S. E., Ondrako, J. M. and Smrcka, A. V. (2001). Phospholipase C(epsilon): a novel Ras effector. EMBO J. 20, 743-754.
28. Kelley, G. G., Reks, S. E. and Smrcka, A. V. (2004). Hormonal regulation of phospholipase Cepsilon through distinct and overlapping pathways involving G12 and Ras family G-proteins. Biochem. J. 378, 129-139.
29. 2+ leak across the endoplasmic reticular membrane. J. Biol. Chem. 278, 13672-13679.
30. Kucik, D. F., Dustin, M. L., Miller, J. M. and Brown, E. J. (1996). Adhesion-activating phorbol ester increases the mobility of leukocyte integrin LFA-1 in cultured lymphocytes. J. Clin. Invest. 97, 2139-2144.
31. Kwong, L., Wozniak, M., Colins, A. S., Wilson, S. D. and Keely, P. J. (2003). R-Ras promotes focal adhesion formation through focal adhesion kinase and p130cas by a novel mechanism that differs from integrins. Mol. Cell. Biol. 23, 933-949.
32. Lader, A. S., Kwiatkowski, D. J. and Cantiello, H. F. (1999). Role of gelsolin in the actin filament regulation of cardiac L-type calcium channels. Am. J. Physiol. 277, C1277-C1283.
33. 2+ regulation of gelsolin by its C-terminal tail. J. Biol. Chem. 275, 27746-27752.
34. Lopez, I., Mak, E. C., Ding, J., Hamm, H. E. and Lomasney, J. W. (2001). A novel bifunctional phospholipase c that is regulated by Galpha 12 and stimulates the Ras/mitogen-activated protein kinase pathway. J. Biol. Chem. 276, 2758-2765.
35. Lub, M., van Kooyk, Y., van Vliet, S. J. and Figdor, C. G. (1997). Dual role of the actin cytoskeleton in regulating cell adhesion mediated by the integrin lymphocyte function-associated molecule-1. Mol. Biol, Cell 8, 341-351.
36. Mallavarapu, A. and Mitchison, T. (1999). Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J. Cell Biol. 146, 1097-1106.
37. McGough, A. M., Staiger, C. J., Min, J. K. and Simonetti, K. D. (2003). The gelsolin family of actin regulatory proteins: modular structures, versatile functions. FEBS Lett. 552,75-81.
38. McNamee, H. P., Ingber, D. E. and Schwartz, M. A. (1993). Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J. Cell Biol. 121, 673-678.
39. McNamee, H. P., Liley, H. G. and Ingber, D. E. (1996). Integrin-dependent control of inositol lipid synthesis in vascular endothelial cells and smooth muscle cells. Exp. Cell Res. 224, 116-122.
40. Mejillano, M. R., Kojima, S., Applewhite, D. A., Gertler, F. B., Svitkina, T. M. and Borisy, G. G. (2004). Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363-373.
41. Mouneimne, G., Soon, L., DesMarais, V., Sidani, M., Song, X., Yip, S. C., Ghosh, M., Eddy, R., Backer, J. M. and Condeelis, J. (2004). Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation. J. Cell Biol. 166, 697-708.
42. Ohba, Y., Ikuta, K., Ogura, A., Matsuda, J., Mochizuki, N., Nagashima, K., Kurokawa, K., Mayer, B. J., Maki, K., Miyazaki, J. et al. (2001). Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 20, 3333-3341.
43. Pantaloni, D., Le Clainche, C. and Carlier, M. F. (2001). Mechanism of actin-based motility. Science 292, 1502-1506.
44. 2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J. Physiol. 547, 333-348.
45. 2+ signalling in human neutrophils. Biochem. Soc. Trans. 24, 70S.
46. 2+ changes in neutrophils during engagement of Cd11b/CD18 integrin visualised using confocal laser scanning reconstruction. J. Cell Sci. 109, 1689-1694.
47. 2+ triggers rapid spreading of human neutrophils adherent via integrin engagement. J. Cell Sci. 111, 2209-2215.
48. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
49. Price, L. S., Langeslag, M., Klooster, J. P. t., Hordijk, P. L., Jalink, K. and Collard, J. G. (2003). Calcium signaling regulates translocation and activation of rac. J Biol. Chem. 278, 39413-39421.
50. Rangarajan, S., Enserink, J. M., Kuiperij, H. B., de Rooij, J., Price, L. S., Schwede, F. and Bos, J. L. (2003). Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J. Cell Biol, 160, 487-493.
51. Raucher, D. and Sheetz, M. P. (2000). Cell spreading and lamellipodial extension rate is regulated by membrane tension. J. Cell Biol. 148, 127-136.
52. Raucher, D. and Sheetz, M. P. (2001). Phospholipase C activation by anesthetics decreases membrane-cytoskeleton adhesion. J. Cell Sci. 114, 3759-3766.
53. Raucher, D., Stauffer, T., Chen, W., Shen, K., Guo, S., York, J. D., Sheetz, M. P. and Meyer, T. (2000). Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228.
54. Sampath, R., Gallagher, P. J. and Pavalko, F. M. (1998). Cytoskeletal interactions with the leukocyte integrin beta2 cytoplasmic tail. Activation-dependent regulation of associations with talin and alpha-actinin. J. Biol. Chem. 273, 33588-33594.
55. Schmidt, M., Evellin, S., Weernink, P. A., von Dorp, F., Rehmann, H., Lomasney, J. W. and Jakobs, K. H. (2001). A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat. Cell Biol. 3, 1020-1024.
56. Sechi, A. S. and Wehland, J. (2000). The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci. 113, 3685-3695.
57. Self, A. J., Caron, E., Paterson, H. F. and Hall, A. (2001). Analysis of R-Ras signalling pathways. J. Cell Sci. 114, 1357-1366.
58. Sethi, T., Ginsberg, M. H., Downward, J. and Hughes, P. E. (1999). The small GTP-binding protein R-Ras can influence integrin activation by antagonizing a Ras/Raf-initiated integrin suppression pathway. Mol. Biol. Cell 10, 1799-1809.
59. Shears, S. (1997). Measurement of inositol phosphate turnover in intact cells and cell-free systems. In Signalling by Inositides (ed. S. Shears), pp. 33. Oxford, New York: IRL Press at Oxford University Press.
60. Small, J. V., Stradal, T., Vignal, E. and Rottner, K. (2002). The lamellipodium: where motility begins. Trends Cell. Biol. 12, 112-120.
61. Song, C., Hu, C. D., Masago, M., Kariyai, K., Yamawaki-Kataoka, Y., Shibatohge, M., Wu, D., Satoh, T. and Kataoka, T. (2001). Regulation of a novel human phospholipase C, PLCepsilon, through membrane targeting by Ras. J. Biol. Chem. 276, 2752-2757.
62. Song, C., Satoh, T., Edamatsu, H., Wu, D., Tadano, M., Gao, X. and Kataoka, T. (2002). Differential roles of Ras and Rap1 in growth factor-dependent activation of phospholipase C epsilon. Oncogene 21, 8105-8113.
63. Spaargaren, M., Martin, G. A., McCormick, F., Fernandez-Sarabia, M. J. and Bischoff, J. R. (1994). The Ras-related protein R-ras interacts directly with Raf-1 in a GTP-dependent manner. Biochem. J. 300, 303-307.
64. Spoonster, J. R., Masiero, L., Savage, S. A., Probst, J. and Kohn, E. C. (1997). Regulation of cell spreading during differentiation in the muscarinic M5 receptor tumor-suppressor model. Int. J. Cancer 72, 362-368.
65. Stope, M. B., Vom Dorp, F., Szatkowski, D., Bohm, A., Keiper, M., Nolte, J., Oude Weernink, P. A., Rosskopf, D., Evellin, S., Jakobs, K. H. et al. (2004). Rap2B-dependent stimulation of phospholipase C-epsilon by epidermal growth factor receptor mediated by c-Src phosphorylation of RasGRP3. Mol. Cell. Biol. 24, 4664-4676.
66. Sun, H. Q., Yamamoto, M., Mejillano, M. and Yin, H. L. (1999). Gelsolin, a multifunctional actin regulatory protein. J. Biol. Chem. 274, 33179-33182.
67. Svitkina, T. M., Bulanova, E. A., Chaga, O. Y., Vignjevic, D. M., Kojima, S., Vasiliev, J. M. and Borisy, G. G. (2003). Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160, 409-421.
68. Takenawa, T. and Itoh, T. (2001). Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim. Biophys. Acta 1533, 190-206.
69. Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K. and Chen, C. S. (2003). Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad Sci. USA 100, 1484-1489.
70. van Kooyk, Y. and Figdor, C. G. (2000). Avidity regulation of integrins: the driving force in leukocyte adhesion. Curr. Opin. Cell Biol. 12, 542-547.
71. van Kooyk, Y., van Vliet, S. J. and Figdor, C. G. (1999). The actin cytoskeleton regulates LFA-1 ligand binding through avidity rather than affinity changes. J. Biol. Chem. 274, 26869-26877.
72. Vignjevic, D., Yarar, D., Welch, M. D., Peloquin, J., Svitkina, T. and Borisy, G. G. (2003). Formation of filopodia-like bundles in vitro from a dendritic network. J. Cell Biol. 160, 951-962.
73. Wakatsuki, T., Schwab, B., Thompson, N. C. and Elson, E. L. (2001). Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J. Cell Sci. 114, 1025-1036.
74. Wozniak, M. A., Kwong, L., Chodniewicz, D., Klemke, R. L. and Keely, P. J. (2005). R-Ras controls membrane protrusion and cell migration through the spatial regulation of Rac and Rho. Mol. Biol. Cell 16, 84-96.
75. Yauch, R. L., Felsenfeld, D. P., Kraeft, S. K., Chen, L. B., Sheetz, M. P. and Hemler, M. E. (1997). Mutational evidence for control of cell adhesion through integrin diffusion/clustering, independent of ligand binding. J. Exp. Med. 186, 1347-1355.
76. Yin, H. L. and Janmey, P. A. (2003). Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65, 761-789.
77. Yue, L., Bao, Z. and Li, J. (2000a). Expression of MacMARCKS restores cell adhesion to ICAM- 1 -coated surface. Cell Adhes. Commun. 7, 359-366.
78. Yue, L., Lu, S., Garces, J., Jin, T. and Li, J. (2000b). Protein kinase C-regulated dynamitin-macrophage-enriched myristoylated alanine-rice C kinase substrate interaction is involved in macrophage cell spreading. J. Biol. Chem. 275, 23948-23956.
79. Zhang, Z., Vuori, K., Wang, H., Reed, J. C. and Ruoslahti, E. (1996). Integrin activation by R-ras. Cell 85, 61-69.
80. Zhou, X. and Li, J. (2000). Macrophage-enriched myristoylated alanine-rich C kinase substrate and its phosphorylation is required for the phorbol ester-stimulated diffusion of beta 2 integrin molecules. J. Biol. Chem. 275, 20217-20222.