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Science 307 (5716): 1746-1752

Copyright © 2005 by the American Association for the Advancement of Science

An Acylation Cycle Regulates Localization and Activity of Palmitoylated Ras Isoforms

Oliver Rocks,1,3 Anna Peyker,3 Martin Kahms,1 Peter J. Verveer,3 Carolin Koerner,1 Maria Lumbierres,2 Jürgen Kuhlmann,1 Herbert Waldmann,2 Alfred Wittinghofer,1* Philippe I. H. Bastiaens3*

Abstract: We show that the specific subcellular distribution of H- and Nras guanosine triphosphate–binding proteins is generated by a constitutive de/reacylation cycle that operates on palmitoylated proteins, driving their rapid exchange between the plasma membrane (PM) and the Golgi apparatus. Depalmitoylation redistributes farnesylated Ras in all membranes, followed by repalmitoylation and trapping of Ras at the Golgi, from where it is redirected to the PM via the secretory pathway. This continuous cycle prevents Ras from nonspecific residence on endomembranes, thereby maintaining the specific intracellular compartmentalization. The de/reacylation cycle also initiates Ras activation at the Golgi by transport of PM-localized Ras guanosine triphosphate. Different de/repalmitoylation kinetics account for isoform-specific activation responses to growth factors.

1 Department of Structural Biology, Max Planck Institute for Molecular Physiology, Otto-Hahn-Straße 11, 44227 Dortmund, Germany.
2 Department of Chemical Biology, Max Planck Institute for Molecular Physiology, Otto-Hahn-Straße 11, 44227 Dortmund, Germany.
3 European Molecular Biology Laboratory, Meyerhofstraße 1, 69117 Heidelberg, Germany.

* To whom correspondence should be addressed. E-mail: alfred.wittinghofer{at} (A.W.) and bastiaen{at} (P.I.H.B.)

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Plasma Membrane Localization of Ras Requires Class C Vps Proteins and Functional Mitochondria in Saccharomyces cerevisiae.
G. Wang and R. J. Deschenes (2006)
Mol. Cell. Biol. 26, 3243-3255
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TRAF6 activation of PI 3-kinase-dependent cytoskeletal changes is cooperative with Ras and is mediated by an interaction with cytoplasmic Src.
K. Z. Q. Wang, N. Wara-Aswapati, J. A. Boch, Y. Yoshida, C.-D. Hu, D. L. Galson, and P. E. Auron (2006)
J. Cell Sci. 119, 1579-1591
   Abstract »    Full Text »    PDF »
Ras and Its Signals Diffuse through the Cell on Randomly Moving Nanoparticles.
B. Rotblat, O. Yizhar, R. Haklai, U. Ashery, and Y. Kloog (2006)
Cancer Res. 66, 1974-1981
   Abstract »    Full Text »    PDF »
Palmitoylations on Murine Coronavirus Spike Proteins Are Essential for Virion Assembly and Infectivity.
E. B. Thorp, J. A. Boscarino, H. L. Logan, J. T. Goletz, and T. M. Gallagher (2006)
J. Virol. 80, 1280-1289
   Abstract »    Full Text »    PDF »
Receptor palmitoylation and ubiquitination regulate anthrax toxin endocytosis.
L. Abrami, S. H. Leppla, and F. G. van der Goot (2006)
J. Cell Biol. 172, 309-320
   Abstract »    Full Text »    PDF »
Palmitoyl-protein thioesterase-1 deficiency mediates the activation of the unfolded protein response and neuronal apoptosis in INCL.
Z. Zhang, Y.-C. Lee, S.-J. Kim, M. S. Choi, P.-C. Tsai, Y. Xu, Y.-J. Xiao, P. Zhang, A. Heffer, and A. B. Mukherjee (2006)
Hum. Mol. Genet. 15, 337-346
   Abstract »    Full Text »    PDF »
K-ras4B and Prenylated Proteins Lacking "Second Signals" Associate Dynamically with Cellular Membranes.
J. R. Silvius, P. Bhagatji, R. Leventis, and D. Terrone (2006)
Mol. Biol. Cell 17, 192-202
   Abstract »    Full Text »    PDF »
Imaging Signal Transduction in Living Cells with Fluorescent Proteins.
M. R. Philips (2005)
Sci. STKE 2005, tr28
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