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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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   Abstract »    Full Text »    PDF »
Differences on the Inhibitory Specificities of H-Ras, K-Ras, and N-Ras (N17) Dominant Negative Mutants Are Related to Their Membrane Microlocalization.
D. Matallanas, I. Arozarena, M. T. Berciano, D. S. Aaronson, A. Pellicer, M. Lafarga, and P. Crespo (2003)
J. Biol. Chem. 278, 4572-4581
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The Exocytotic Trafficking of TC10 Occurs through both Classical and Nonclassical Secretory Transport Pathways in 3T3L1 Adipocytes.
R. T. Watson, M. Furukawa, S.-H. Chiang, D. Boeglin, M. Kanzaki, A. R. Saltiel, and J. E. Pessin (2003)
Mol. Cell. Biol. 23, 961-974
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Elevated Phospholipase D Activity in H-Ras- but Not K-Ras-Transformed Cells by the Synergistic Action of RalA and ARF6.
L. Xu, P. Frankel, D. Jackson, T. Rotunda, R. L. Boshans, C. D'Souza-Schorey, and D. A. Foster (2003)
Mol. Cell. Biol. 23, 645-654
   Abstract »    Full Text »    PDF »
Specificity of Plasma Membrane Targeting by the Rous Sarcoma Virus Gag Protein.
L. Z. Scheifele, J. D. Rhoads, and L. J. Parent (2003)
J. Virol. 77, 470-480
   Abstract »    Full Text »    PDF »
Plasma membrane localization of the Yck2p yeast casein kinase 1 isoform requires the C-terminal extension and secretory pathway function.
P. Babu, J. D. Bryan, H. R. Panek, S. L. Jordan, B. M. Forbrich, S. C. Kelley, R. T. Colvin, and L. C. Robinson (2002)
J. Cell Sci. 115, 4957-4968
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Flotillin-1/Reggie-2 Traffics to Surface Raft Domains via a Novel Golgi-independent Pathway: IDENTIFICATION OF A NOVEL MEMBRANE TARGETING DOMAIN AND A ROLE FOR PALMITOYLATION.
I. C. Morrow, S. Rea, S. Martin, I. A. Prior, R. Prohaska, J. F. Hancock, D. E. James, and R. G. Parton (2002)
J. Biol. Chem. 277, 48834-48841
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Erf4p and Erf2p Form an Endoplasmic Reticulum-associated Complex Involved in the Plasma Membrane Localization of Yeast Ras Proteins.
L. Zhao, S. Lobo, X. Dong, A. D. Ault, and R. J. Deschenes (2002)
J. Biol. Chem. 277, 49352-49359
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Preferential DNA Damage and Poor Repair Determine ras Gene Mutational Hotspot in Human Cancer.
Z. Feng, W. Hu, J. X. Chen, A. Pao, H. Li, W. Rom, M.-C. Hung, and M.-s. Tang (2002)
J Natl Cancer Inst 94, 1527-1536
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A Cell-Specific, Prenylation-Independent Mechanism Regulates Targeting of Type II RACs.
M. Lavy, K. Bracha-Drori, H. Sternberg, and S. Yalovsky (2002)
PLANT CELL 14, 2431-2450
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Insider Information: How Palmitoylation of Ras Makes It a Signaling Double Agent.
L. G. Berthiaume (2002)
Sci. STKE 2002, pe41
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A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65.
J. Kanaani, A. E.-D. El-Husseini, A. Aguilera-Moreno, J. M. Diacovo, D. S. Bredt, and S. Baekkeskov (2002)
J. Cell Biol. 158, 1229-1238
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SNAP-25 Traffics to the Plasma Membrane by a Syntaxin-independent Mechanism.
S. S. Loranger and M. E. Linder (2002)
J. Biol. Chem. 277, 34303-34309
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Membrane Trafficking of Heterotrimeric G Proteins via the Endoplasmic Reticulum and Golgi.
D. Michaelson, I. Ahearn, M. Bergo, S. Young, and M. Philips (2002)
Mol. Biol. Cell 13, 3294-3302
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The Arabidopsis AtSTE24 Is a CAAX Protease with Broad Substrate Specificity.
K. Bracha, M. Lavy, and S. Yalovsky (2002)
J. Biol. Chem. 277, 29856-29864
   Abstract »    Full Text »    PDF »

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