RhoGDI: Multiple functions in the regulation of Rho family GTPase activities

Biochemical Journal

Volumn 390, Issue 1, 2005, Pages 1-9

  Dovas, Athanassios ^a   Couchman, John R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Effector; Membrane domain; Protein complex; Rho GDP dissociation inhibitor (RhoGDI); Rho GTPase; Targeting

Indexed keywords

BIOCHEMISTRY; BIOLOGICAL MEMBRANES; CELLS;

GTPASE-RHOGDI COMPLEXES; GTPASES; PROTEIN COMPLEX; TARGETING;

ENZYMES;

CYCLIC AMP DEPENDENT PROTEIN KINASE; EZRIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; MOESIN; PHOSPHOLIPASE C BETA2; PROTEIN CDC42; PROTEIN KINASE C; RADIXIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CYTOKINESIS; DOWN REGULATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE EXPRESSION; GOLGI COMPLEX; MEMBRANE BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; GENE EXPRESSION REGULATION; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PROTEIN CONFORMATION; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 23944518413     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20050104     Document Type: Review

References (80)

1. Nobes, C. D. and Hall, A. (1995) Rho, Rac and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibres, lamellipodia and filopodia. Cell 81, 53-62
2. Etienne-Manneville, S. and Hall, A. (2002) RhoGTPases in cell biology. Nature (London) 420, 629-635
3. Bishop, A. L. and Hall, A. (2000) RhoGTPases and their effector proteins. Biochem. J. 348, 241-255
4. Schmidt, A. and Hall, A. (2002) Guanine nucleotide exchange proteins for Rho GTPases: turning on the switch. Genes Dev. 16, 1587-1609
5. Moon, S. Y. and Zheng, Y. (2003) Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13, 13-22
6. Sasaki, T. and Takai, Y. (1998) The Rho small G protein family - RhoGDI system as a temporal and spatial determinant for cytoskeletal control. Biochem. Biophys. Res. Commun. 245, 641-645
7. Olofsson, B. (1999) Rho guanine dissociation inhibitors: pivotal molecules in cellular signalling. Cell. Signal. 11, 545-554
8. Masuda, T., Tanaka, K., Nonaka, H., Yamochi, W., Maeda, A. and Takai, Y. (1994) Molecular cloning and characterisation of yeast rho GDP dissociation inhibitor. J. Biol. Chem. 269, 19713-19718
9. Yap, S. F., Chen, W. and Lim, L. (1999) Molecular characterisation of the Caenorhabditis elegans Rho GDP-dissociation inhibitor. Eur. J. Biochem. 266, 1090-1100
10. Imai, K., Kijima, T., Noda, Y., Sutoh, K., Yoda, K. and Adachi, H. (2002) A Rho GDP-dissociation inhibitor is involved in cytokinesis in Dictyostelium. Biochem. Biophys. Res. Commun. 296, 305-312
11. Rivero, F., Illenberger, D., Somesh, B. P., Dislich, H., Adam, N. and Meyer, A. K. (2002) Defects in cytokinesis, actin reorganisation and the contractile vacuole in cells deficient in RhoGDI. EMBO J. 21, 4539-4549
12. Bischoff, F., Vahlkamp, L., Molendijk, A. and Palme, K. (2000) Localization of AtROP4 and AtROP6 and interaction with the guanine nucleotide dissociation inhibitor AtRhoGDI1 from Arabidopsis. Plant Mol. Biol. 42, 515-530
13. Nancy, V., Callebaut, I., El Marjou, A. and de Gunzburg, J. (2002) The δ subunit of the retinal rod cGMP phosphodiesterase regulates the membrane association of Ras and Rap GTPases. J. Biol. Chem. 277, 15076-15084
14. Michaelson, D., Silletti, J., Murphy, G., D'Eustachio, P., Rush, M. and Philips, M. R. (2001) Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J. Cell Biol. 152, 111-126
15. Platko, J. V., Leonard, D. A., Adra, C. N., Shaw, R. J., Cerione, R. A. and Lim, B. (1995) A single residue can modify target-binding affinity and activity of the functional domain of the Rho-subfamily GDP dissociation inhibitors. Proc. Natl. Acad. Sci. U.S.A. 92, 2974-2978
16. Gorvel, J.-P., Chang, T.-C., Boretto, J., Azuma, T. and Chavrier, P. (1998) Differential properties of D4/LyGDI versus RhoGDI: phosphorylation and rho GTPase selectivity. FEBS Lett. 422, 269-273
17. Zalcman, G., Closson, V., Camonis, J., Honore, N., Rousseau-Merck, M. F., Tavitian, A. and Olofsson, B. (1996) RhoGDI-3 is a new GDP dissociation inhibitor (GDI). Identification of a non-cytosolic GDI protein interacting with the small GTP-binding proteins RhoB and RhoG. J. Biol. Chem. 271, 30366-30374
18. Adra, C. N., Manor, D., Ko, J. L., Zhu, S., Horiuchi, T., Van Aelst, L., Cerione, R. A. and Lim, B. (1997) RhoGDIγ: A GDP-dissociation inhibitor for Rho proteins with preferential expression in brain and pancreas. Proc. Natl. Acad. Sci. U.S.A. 94, 4279-4284
19. Togawa, A., Miyoshi, J., Ishizaki, H., Tanaka, M., Takakura, A., Nishioka, H., Yoshida, H., Doi, T., Mizoguchi, A., Matsuura, N. et al. (1999) Progressive impairment of kidneys and reproductive organs in mice lacking RhoGDIα. Oncogene 18, 5373-5380
20. Brunet, N., Morin, A. and Olofsson, B. (2002) RhoGDI-3 regulates RhoG and targets this protein to the Golgi complex through its unique N-terminal domain. Traffic 3, 342-358
21. Guillemot, J. C., Kruskal, B. A., Adra, C. N., Zhu, S., Ko, J. L., Burch, P., Nocka, K., Sootoo, K., Simons, E. and Lim, B. (1996) Targeted disruption of guanosine diphosphate-dissociation inhibitor for Rho-related proteins, GDID4: normal hematopoietic differentiation but subtle defect in superoxide production by macrophages derived from embryonal stem cell differentiation. Blood 88, 2722-2731
22. Yin, L., Schwartzberg, P., Scharton-Kersten, T. M., Staudt, L. and Lenardo, M. (1997) Immune responses in mice deficient in Ly-GDI, a lymphoid-specific regulator of Rho GTPases. Mol. Immunol. 34, 481-491
23. Koch, G., Tanaka, K., Masuda, T., Yamochi, W., Nonaka, H. and Takai, Y. (1997) Association of the Rho family small GTP-binding proteins with Rho GDP dissociation inhibitor in Saccharomyces cerevisiae. Oncogene 15, 417-422
24. Anastasiadis, P. Z., Moon, S. Y., Thoreson, M. A., Mariner, D. J., Crawford, H. C., Zheng, Y. and Reynolds, A. B. (2000) Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2, 637-644
25. Degani, S., Balzac, F., Brancaccio, M., Guazzone, S., Retta, S. F., Silengo, L., Eva, A. and Tarone, G. (2002) The integrin cytoplasmic domain-associated protein ICAP-1 binds and regulates Rho family GTPases during cell spreading. J. Cell Biol. 156, 377-387
26. Keep, N. H., Barnes, M., Barsukov, I., Badii, R., Lian, L.-Y., Segal, A. W., Moody, P. C. E. and Roberts, G. C. K. (1997) A modulator of rho family G proteins, rhoGDI, binds these G proteins via an immunoglobulin-like domain and a flexible N-terminal arm. Structure 5, 623-633
27. Gosser, Y. Q., Nomanbhoy, T. K., Aghazadeh, B., Manor, D., Combs, C., Cerione, R. A. and Rosen, M. K. (1997) C-terminal binding domain of RhoGDP-dissociation inhibitor directs N-terminal inhibitory peptide to GTPases. Nature (London) 387, 814-819
28. Golovanov, A. P., Chuang, T.-H., DerMardirossian, C., Barsukov, I., Hawkins, D., Badii, R., Bokoch, G. M., Lian, L.-Y. and Roberts, G. C. K. (2001) Structure-activity relationships in flexible protein domains: Regulation of rho GTPases by RhoGDI and D4 GDI. J. Mol. Biol. 305, 121-135
29. Longenecker, K., Read, P., Derewenda, U., Dauter, Z., Liu, X., Garrard, S., Walker, L., Somlyo, A. V., Nakamoto, R. K., Somlyo, A. P. and Derewenda, Z. S. (1999) How RhoGDI binds Rho. Acta Crytallogr, Sect. D: Biol. Crystallogr. 55, 1503-1515
30. Hoffman, G. R., Nassar, N. and Cerione, R. A. (2000) Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 100, 345-356
31. Grizot, S., Fauré, J., Fieschi, F., Vignais, P. V., Dagher, M.-C. and Pebay-Peyroula, E. (2001) Crystal structure of the Rac1-RhoGDI complex involved in NADPH oxidase activation. Biochemistry 40, 10007-10013
32. Schefzek, K., Stephan, I., Jensen, O. N., Illenberger, D. and Gierschik, P. (2000) The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI. Nat. Struct. Biol. 7, 122-126
33. Li, R. and Zheng, Y. (1997) Residues of the Rho family GTPases that specify sensitivity to Dbl-like guanine nucleotide exchange factors. J. Biol. Chem. 272, 4671-4679
34. Golovanov, A. P., Hawkins, D., Barsukov, I., Badii, R., Bokoch, G. K., Lian, L.-Y. and Roberts, G. C. K. (2001) Structural consequences of site-directed mutagenesis in flexible protein domains. NMR characterization of the L(55,56)S mutant of RhoGDI. Eur. J. Biochem. 268, 2253-2260
35. Nomanbhoy, T. K., Erickson, J. W. and Cerione, R. C. (1999) Kinetics of Cdc42 membrane extraction by rho-GDI monitored by real-time fluorescence resonance energy transfer. Biochemistry 38, 17440-1750
36. Lang, P., Gesbert, F., Delespine-Carmagnat, M., Stancou, R., Pouchelet, M. and Bertoglio, J. (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15, 510-519
37. Forget, M. A., Desrosiers, R. R., Gingras, D. and Beliveau, R. (2002) Phosphorylation states of Cdc42 and RhoA regulate their interactions with Rho GDP dissociation inhibitor and their extraction from biological membranes. Biochem. J. 361, 243-254
38. Ellerbroek, S. M., Wennerberg, K. and Burridge, K. (2003) Serine phosphorylation negatively regulates RhoA in vivo. J. Biol. Chem. 278, 19023-19031
39. Tu, S., Wu, W. J., Wang, J. and Cerione, R. A. (2003) Epidermal growth factor-dependent regulation of Cdc42 is mediated by the Src tyrosine kinase. J. Biol. Chem. 278, 49293-49300
40. Bourmeyster, N. and Vignais, P. V. (1996) Phosphorylation of RhoGDI stabilizes the RhoA-RhoGDI complex in neutrophil cytosol. Biochem. Biophys. Res. Commun. 218, 54-60
41. Unwin, R. D., Sternberg, D. W., Lu, Y., Pierce, A., Gilliland, D. G. and Whetton, A. D. (2005) Global effects of BCR/ABL and TEL/PDGFRbeta expression on the proteome and phosphoproteome: Identification of the Rho pathway as a target of BCR/ABL. J. Biol. Chem. 280, 6316-6326
42. Mehta, D., Rahman, A. and Malik, A. B. (2001) Protein kinase Cα signals Rho-guanine nucleotide dissociation inhibitor phosphorylation and Rho activation and regulates the endothelial cell barrier function. J. Biol. Chem. 276, 22614-22620
43. Price, L. S., Langeslag, M., Klooster, J. P., Hordijk, P. L., Jalink, K. and Collard, J. G. (2003) Calcium signalling regulates translocation and activation of Rac. J. Biol. Chem. 278, 39413-39421
44. DerMardirossian, C., Schnelzer, A. and Bokoch, G. M. (2004) Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Mol. Cell 15, 117-127
45. Bretscher, A., Edwards, K. and Fehon, R. G. (2002) ERM proteins and Merlin: Integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586-599
46. Takahashi, K., Sasaki, T., Mammoto, A., Takaishi, K., Kaneyama, T., Tsukita, Sa., Tsukita, Sh. and Takai, Y. (1997) Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J. Biol. Chem. 272, 23371-23375
47. Hirao, M., Sato, N., Kondo, T., Yonemura, S., Monden, M., Sasaki, T., Takai, Y., Tsukita, Sh. and Tsukita, Sa. (1996) Regulation mechanism of ERM (Ezrin/Radixin/ Moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signalling pathway. J. Cell Biol. 135, 37-51
48. Allenspach, E. J., Cullinan, P., Tong, J., Tang, Q., Tesciuba, A. G., Cannon, J. L., Takahashi, S. M., Morgan, R., Burkhardt, J. K. and Sperling, A. I. (2001) ERM-dependent movement of CD43 defines a novel protein complex distal to the immunological synapse. Immunity 15, 739-750
49. Ota, T., Maeda, M., Suto, S. and Tatsuka, M. (2004) LyGDI functions in cancer metastasis by anchoring Rho proteins to the cell membrane. Mol. Carcinog. 39, 206-220
50. Yamashita, T. and Tohyama, M. (2003) The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat. Neurosci. 6, 461-467
51. Fauré, J. and Dagher, M. C. (2001) Interactions between Rho GTPases and Rho GDP dissociation inhibitor. Biochimie 83, 409-414
52. Kim, O., Yang, J. and Qiu, Y. (2002) Selective activation of the small GTPase RhoA by tyrosine kinase Etk through its pleckstrin homology domain. J. Biol. Chem. 277, 30066-30071
53. Jamney, P. A. and Lindberg, U. (2004) Cytoskeletal regulation: rich in lipids. Nat. Rev. Mol. Cell. Biol. 5, 658-666
54. Chuang, T.-S., Bohl, B. P. and Bokoch, G. M. (1993) Biologically active lipids are regulators of Rac-GDI complexation. J. Biol. Chem. 268, 26206-26211
55. Fauré, J., Vignais, P. V. and Dagher, M. C. (1999) Phosphoinositide-dependent activation of RhoA involves partial opening of the RhoA/Rho-GDI complex. Eur. J. Biochem. 262, 879-889
56. Yonemura, S., Matsui, T., Tsukita, Sh. and Tsukita, Sa. (2002) Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115, 2569-2580
57. Fievet, B. T., Gautreau, A., Roy, C., Del Maestro, L., Mangeat, P., Louvard, D. and Arpin, M. (2004) Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164, 653-659
58. Gibson, R. M. and Wilson-Delfosse, A. L. (2001) RhoGDI-binding defective mutant of Cdc42 targets to membranes and activates filopodia formation but does not cycle with the cytosol of mammalian cells. Biochem. J. 359, 285-294
59. Gibson, R. M., Gandhi, P. N., Tong, X., Miyoshi, J., Takai, Y., Konieczkowski, M., Sedor, J. R. and Wilson-Delfosse, A. L. (2004) An activating mutant of Cdc42 that fails to interact with Rho GDP-dissociation inhibitor localizes to the plasma membrane and mediates actin reorganization. Exp. Cell Res. 301, 211-222
60. Gandhi, P. N., Gibson, R. M., Tong, X., Miyoshi, J., Takai, Y., Konieczowski, M., Sedor, J. R. and Wilson-Delfosse, A. L. (2003) An activating mutant of Rac1 that fails to interact with Rho GDP-dissociation inhibitor stimulates membrane ruffling in mammalian cells. Biochem. J. 378, 409-419
61. Pfeffer, S. and Aivazian, D. (2004) Targeting Rab GTPases to distinct membrane compartments. Nat. Rev. Mol. Cell Biol. 5, 886-896
62. Lin, Q., Fuji, R. N., Yang, W. and Cerione, R. C. (2003) RhoGDI is required for Cdc42-mediated cellular transformation. Curr. Biol. 13, 1469-1479
63. Hancock, J. F. and Hall, A. (1993) A novel role for RhoGDI as an inhibitor of GAP proteins. EMBO J. 12, 1915-1921
64. O'Sullivan, A. J., Brown, A. M., Freeman, H. N. M. and Gomperts, B. D. (1996) Purification and identification of FOAD-II, a cytosolic protein that regulates secretion in streptolysin-O permeabilized mast cells, as a Rac/RhoGDI complex. Mol. Biol. Cell 7, 397-408
65. Abo, A., Pick, E., Hall, A., Totty, N., Teahn, C. G. and Segal, A. W. (1991) Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature (London) 353, 668-670
66. Di-Poï, N., Fauré, J., Grizot, S., Molná, G., Pick, E. and Dagher, M. C. (2001) Mechanism of NADPH oxidase activation by the Rac/Rho-GDI complex. Biochemistry 40, 10014-10022
67. 2 by the Rho GTPases Cdc42Hs and Rac1. EMBO J. 17, 6241-6249
68. Tolias, K. F., Couvillon, A. D., Cantley, L. C. and Carpenter, C. L. (1998) Characterization of a Rac1- and RhoGDI-associated lipid kinase signalling complex. Mol. Cell. Biol. 18, 762-770
69. Hansen, M. D. H. and Nelson, W. J. (2001) Serum-activated assembly and membrane translocation of an endogenous Rac1:effector complex. Curr. Biol. 11, 356-360
70. del Pozo, M. A., Price, L. S., Alderson, N. B., Ren, X.-D. and Schwartz, M. A. (2000) Adhesion to extracellular matrix regulates coupling of the small GTPase Rac to its effector PAK. EMBO J. 19, 2008-2014
71. del Pozo, M. A., Kiosses, W. B., Alderson, N. B., Meller, N., Hahn, K. M. and Schwartz, M. A. (2002) Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat. Cell Biol. 4, 232-239
72. del Pozo, M. A., Alderson, N. B., Kiosses, W. B., Chiang, H.-H., Anderson, R. G. W. and Schwartz, M. A. (2004) Integrins regulate Rac targeting by internalisation of membrane domains. Science (Washington, D.C.) 303, 839-842
73. Robinson, J. M. and Badwey, J. A. (2002) Rapid association of cytoskeletal remodelling proteins with the developing phagosomes of human neutrophils. Histochem. Cell Biol. 118, 117-125
74. Caron, E. and Hall, A. (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science (Washington, D.C.) 282, 1717-1721
75. Garin, J., Diez, R., Kieffer, S., Dermine, J.-F., Duclos, S., Gagnon, E., Sadoul, R., Rondeau, C. and Desjardins, M. (2001) The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152, 165-180
76. Cougoule, C., Wiedermann, A., Lim, J. and Caron, E. (2004) Phagocytosis, an alternative model system for the study of cell adhesion. Semin. Cell Devel. Biol. 15, 679-689
77. Dvorsky, R. and Ahmadian, M. R. (2004) Always look on the bright site of Rho: structural implications for a conserved intermolecular interface. EMBO Rep. 5, 1130-1136
78. Robbe, K., Otto-Bruc, A., Chardin, P. and Anthonny, B. (2003) Dissociation of GDP dissociation inhibitor and membrane translocation are required for efficient activation of Rac by the Dbl homology - pleckstrin homology region of Tiam. J. Biol. Chem. 278, 4756-4762
79. Groysman, M., Hornstein, I., Alcover, A. and Katzav, S. (2002) Vav1 and Ly-GDI two regulators of Rho GTPases, function cooperatively as signal transducers in T cell antigen receptor-induced pathways. J. Biol. Chem. 277, 50121-50130
80. Holinstat, M., Mehta, D., Kozasa, T., Minshtall, R. D. and Malik, A. B. (2003) Protein kinase Cα-induced p115RhoGEF phosphorylation signals endothelial cytoskeletal rearrangement. J. Biol. Chem. 278, 28793-28798