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J. Cell Biol. 152 (1): 111-126

Copyright © 2001 by the Rockefeller University Press.

Original Article

Differential Localization of Rho Gtpases in Live Cells

Regulation by Hypervariable Regions and Rhogdi Binding

David Michaelsona,b, Joseph Sillettia,b, Gretchen Murphyc, Peter D'Eustachioc, Mark Rushc, , and Mark R. Philipsa,b

a Department of Medicine, New York University School of Medicine, New York, New York 10016
b Department of Cell Biology, New York University School of Medicine, New York, New York 10016
c Department of Biochemistry, New York University School of Medicine, New York, New York 10016
Departments of Medicine and Cell Biology, MSB251, New York University School of Medicine, 550 First Ave., New York, NY 10016.(212) 263-0759(212) 263-7404

philim01{at}med.nyu.edu

Abstract: Determinants of membrane targeting of Rho proteins were investigated in live cells with green fluorescent fusion proteins expressed with or without Rho-guanine nucleotide dissociation inhibitor (GDI){alpha}. The hypervariable region determined to which membrane compartment each protein was targeted. Targeting was regulated by binding to RhoGDI{alpha} in the case of RhoA, Rac1, Rac2, and Cdc42hs but not RhoB or TC10. Although RhoB localized to the plasma membrane (PM), Golgi, and motile peri-Golgi vesicles, TC10 localized to PMs and endosomes. Inhibition of palmitoylation mislocalized H-Ras, RhoB, and TC10 to the endoplasmic reticulum. Although overexpressed Cdc42hs and Rac2 were observed predominantly on endomembrane, Rac1 was predominantly at the PM. RhoA was cytosolic even when expressed at levels in vast excess of RhoGDI{alpha}. Oncogenic Dbl stimulated translocation of green fluorescent protein (GFP)-Rac1, GFP-Cdc42hs, and GFP-RhoA to lamellipodia. RhoGDI binding to GFP-Cdc42hs was not affected by substituting farnesylation for geranylgeranylation. A palmitoylation site inserted into RhoA blocked RhoGDI{alpha} binding. Mutations that render RhoA, Cdc42hs, or Rac1, either constitutively active or dominant negative abrogated binding to RhoGDI{alpha} and redirected expression to both PMs and internal membranes. Thus, despite the common essential feature of the CAAX (prenylation, AAX tripeptide proteolysis, and carboxyl methylation) motif, the subcellular localizations of Rho GTPases, like their functions, are diverse and dynamic.

Key Words: Rho • Rac • Cdc42hs • RhoGDI • green fluorescent protein

The online version of this article contains supplemental material.

Abbreviations used in this paper: 2BP, 2-bromopalmitate; BFA, brefeldin A; CCD, charge-coupled device; GDI, guanine nucleotide dissociation inhibitor; GEF, guanine nucleotide exchange factor; GFP, green fluorescent protein; GST, glutathione S-transferase; LAMP, lysosome-associated membrane protein; PAE, porcine aortic endothelial; pcCMT, prenylcysteine-directed COOH methyltransferase; PM, plasma membrane; SRF, serum response factor.

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   Abstract »    Full Text »    PDF »
Isoform-Specific Membrane Targeting Mechanism of Rac during Fc{gamma}R-Mediated Phagocytosis: Positive Charge-Dependent and Independent Targeting Mechanism of Rac to the Phagosome.
T. Ueyama, M. Eto, K. Kami, T. Tatsuno, T. Kobayashi, Y. Shirai, M. R. Lennartz, R. Takeya, H. Sumimoto, and N. Saito (2005)
J. Immunol. 175, 2381-2390
   Abstract »    Full Text »    PDF »
Depalmitoylated Ras traffics to and from the Golgi complex via a nonvesicular pathway.
J. S. Goodwin, K. R. Drake, C. Rogers, L. Wright, J. Lippincott-Schwartz, M. R. Philips, and A. K. Kenworthy (2005)
J. Cell Biol. 170, 261-272
   Abstract »    Full Text »    PDF »
Critical and Distinct Roles of Amino- and Carboxyl-terminal Sequences in Regulation of the Biological Activity of the Chp Atypical Rho GTPase.
E. J. Chenette, A. Abo, and C. J. Der (2005)
J. Biol. Chem. 280, 13784-13792
   Abstract »    Full Text »    PDF »
Postprenylation CAAX Processing Is Required for Proper Localization of Ras but Not Rho GTPases.
D. Michaelson, W. Ali, V. K. Chiu, M. Bergo, J. Silletti, L. Wright, S. G. Young, and M. Philips (2005)
Mol. Biol. Cell 16, 1606-1616
   Abstract »    Full Text »    PDF »
An Acylation Cycle Regulates Localization and Activity of Palmitoylated Ras Isoforms.
O. Rocks, A. Peyker, M. Kahms, P. J. Verveer, C. Koerner, M. Lumbierres, J. Kuhlmann, H. Waldmann, A. Wittinghofer, and P. I. H. Bastiaens (2005)
Science 307, 1746-1752
   Abstract »    Full Text »    PDF »
Uncoupling of Inhibitory and Shuttling Functions of Rho GDP Dissociation Inhibitors.
E. Dransart, A. Morin, J. Cherfils, and B. Olofsson (2005)
J. Biol. Chem. 280, 4674-4683
   Abstract »    Full Text »    PDF »
Regulation of Cystic Fibrosis Transmembrane Regulator Trafficking and Protein Expression by a Rho Family Small GTPase TC10.
J. Cheng, H. Wang, and W. B. Guggino (2005)
J. Biol. Chem. 280, 3731-3739
   Abstract »    Full Text »    PDF »
Rac GTPase Isoform-specific Regulation of NADPH Oxidase and Chemotaxis in Murine Neutrophils in Vivo: ROLE OF THE C-TERMINAL POLYBASIC DOMAIN.
A. Yamauchi, C. C. Marchal, J. Molitoris, N. Pech, U. Knaus, J. Towe, S. J. Atkinson, and M. C. Dinauer (2005)
J. Biol. Chem. 280, 953-964
   Abstract »    Full Text »    PDF »
Clostridium difficile Toxin A Induces Expression of the Stress-induced Early Gene Product RhoB.
R. Gerhard, H. Tatge, H. Genth, T. Thum, J. Borlak, G. Fritz, and I. Just (2005)
J. Biol. Chem. 280, 1499-1505
   Abstract »    Full Text »    PDF »
Rac1 is the small GTPase responsible for regulating the neutrophil chemotaxis compass.
C. X. Sun, G. P. Downey, F. Zhu, A. L. Y. Koh, H. Thang, and M. Glogauer (2004)
Blood 104, 3758-3765
   Abstract »    Full Text »    PDF »
Cyclin B1 Is a Critical Target of RhoB in the Cell Suicide Program Triggered by Farnesyl Transferase Inhibition.
U. Kamasani, M. Huang, J. B. DuHadaway, E. V. Prochownik, P. S. Donover, and G. C. Prendergast (2004)
Cancer Res. 64, 8389-8396
   Abstract »    Full Text »    PDF »
Rac2-Deficient Murine Macrophages Have Selective Defects in Superoxide Production and Phagocytosis of Opsonized Particles.
A. Yamauchi, C. Kim, S. Li, C. C. Marchal, J. Towe, S. J. Atkinson, and M. C. Dinauer (2004)
J. Immunol. 173, 5971-5979
   Abstract »    Full Text »    PDF »
Rac1 Mediates Collapse of Microvilli on Chemokine-Activated T Lymphocytes.
R. Nijhara, P. B. van Hennik, M. L Gignac, M. J. Kruhlak, P. L. Hordijk, J. Delon, and S. Shaw (2004)
J. Immunol. 173, 4985-4993
   Abstract »    Full Text »    PDF »

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