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Mol. Cell. Biol. 20 (7): 2475-2487

Copyright © 2000 by the American Society for Microbiology. All rights reserved.

Molecular and Cellular Biology, April 2000, p. 2475-2487, Vol. 20, No. 7
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

H-ras but Not K-ras Traffics to the Plasma Membrane through the Exocytic Pathway

Ann Apolloni,1 Ian A. Prior,1 Margaret Lindsay,2 Robert G. Parton,2 and John F. Hancock1,*

Queensland Cancer Fund Laboratory of Experimental Oncology, Department of Pathology, University of Queensland Medical School,1 and Centre for Microscopy and Microanalysis, Centre for Molecular and Cellular Biology, Department of Physiology and Pharmacology, University of Queensland,2 Brisbane 4069, Australia

Received 12 August 1999/Returned for modification 7 October 1999/Accepted 9 January 2000

Ras proteins must be localized to the inner surface of the plasma membrane to be biologically active. The motifs that effect Ras plasma membrane targeting consist of a C-terminal CAAX motif plus a second signal comprising palmitoylation of adjacent cysteine residues or the presence of a polybasic domain. In this study, we examined how Ras proteins access the cell surface after processing of the CAAX motif is completed in the endoplasmic reticulum (ER). We show that palmitoylated CAAX proteins, in addition to being localized at the plasma membrane, are found throughout the exocytic pathway and accumulate in the Golgi region when cells are incubated at 15°C. In contrast, polybasic CAAX proteins are found only at the cell surface and not in the exocytic pathway. CAAX proteins which lack a second signal for plasma membrane targeting accumulate in the ER and Golgi. Brefeldin A (BFA) significantly inhibits the plasma membrane accumulation of newly synthesized, palmitoylated CAAX proteins without inhibiting their palmitoylation. BFA has no effect on the trafficking of polybasic CAAX proteins. We conclude that H-ras and K-ras traffic to the cell surface through different routes and that the polybasic domain is a sorting signal diverting K-Ras out of the classical exocytic pathway proximal to the Golgi. Farnesylated Ras proteins that lack a polybasic domain reach the Golgi but require palmitoylation in order to traffic further to the cell surface. These data also indicate that a Ras palmitoyltransferase is present in an early compartment of the exocytic pathway.

* Corresponding author. Mailing address: Queensland Cancer Fund Laboratory of Experimental Oncology, Department of Pathology, University of Queensland Medical School, Herston Rd., Brisbane 4069, Australia. Phone: 617 3365 5288. Fax: 617 3365 5511. E-mail: j.hancock{at}mailbox.uq.edu.au.

Molecular and Cellular Biology, April 2000, p. 2475-2487, Vol. 20, No. 7
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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n-6 and n-3 polyunsaturated fatty acids differentially modulate oncogenic Ras activation in colonocytes.
E. D. Collett, L. A. Davidson, Y.-Y. Fan, J. R. Lupton, and R. S. Chapkin (2001)
Am J Physiol Cell Physiol 280, C1066-C1075
   Abstract »    Full Text »    PDF »
A Ras by Any Other Name.
D. Bar-Sagi (2001)
Mol. Cell. Biol. 21, 1441-1443
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Targeted Genomic Disruption of H-ras and N-ras, Individually or in Combination, Reveals the Dispensability of Both Loci for Mouse Growth and Development.
L. M. Esteban, C. Vicario-Abejón, P. Fernández-Salguero, A. Fernández-Medarde, N. Swaminathan, K. Yienger, E. Lopez, M. Malumbres, R. McKay, J. M. Ward, et al. (2001)
Mol. Cell. Biol. 21, 1444-1452
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Differential Localization of Rho GTPases in Live Cells: Regulation by Hypervariable Regions and RhoGDI Binding.
D. Michaelson, J. Silletti, G. Murphy, P. D'Eustachio, M. Rush, and M. R. Philips (2001)
J. Cell Biol. 152, 111-126
   Abstract »    Full Text »    PDF »
Compartmentalization of Ras proteins.
I. Prior and J. Hancock (2001)
J. Cell Sci. 114, 1603-1608
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Small GTP-Binding Proteins.
Y. Takai, T. Sasaki, and T. Matozaki (2001)
Physiol Rev 81, 153-208
   Abstract »    Full Text »    PDF »
Association of Prenylated Proteins with the Plasma Membrane and the Inner Nuclear Membrane Is Mediated by the Same Membrane-targeting Motifs.
H. Hofemeister, K. Weber, and R. Stick (2000)
Mol. Biol. Cell 11, 3233-3246
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The C-terminal Polylysine Region and Methylation of K-Ras Are Critical for the Interaction between K-Ras and Microtubules.
Z. Chen, J. C. Otto, M. O. Bergo, S. G. Young, and P. J. Casey (2000)
J. Biol. Chem. 275, 41251-41257