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J. Cell Biol. 160 (2): 165-170

Copyright © 2003 by the Rockefeller University Press.


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Direct visualization of Ras proteins in spatially distinct cell surface microdomains

Ian A. Prior1, Cornelia Muncke1, Robert G. Parton2, and John F. Hancock1

1 Department of Pathology and Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4006, Australia
2 Institute for Molecular Bioscience, Centre for Microscopy and Microanalysis and School of Biomedical Sciences, University of Queensland, Brisbane, Queensland 4072, Australia

Address correspondence to John F. Hancock, Dept. of Pathology, University of Queensland Medical School, Herston Rd., Herston, Brisbane, Queensland 4006, Australia. Tel.: 61-7-3365-5288. Fax: 61-7-3365-5511. E-mail: j.hancock{at}mailbox.uq.edu.au; or Robert G. Parton, Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland 4072, Australia. Tel.: 61-7-3365-6468. Fax: 61-7-3365-4422 E-mail: r.parton{at}imb.uq.edu.au

Abstract: Localization of signaling complexes to specific microdomains coordinates signal transduction at the plasma membrane. Using immunogold electron microscopy of plasma membrane sheets coupled with spatial point pattern analysis, we have visualized morphologically featureless microdomains, including lipid rafts, in situ and at high resolution. We find that an inner-plasma membrane lipid raft marker displays cholesterol-dependent clustering in microdomains with a mean diameter of 44 nm that occupy 35% of the cell surface. Cross-linking an outer-leaflet raft protein results in the redistribution of inner leaflet rafts, but they retain their modular structure. Analysis of Ras microlocalization shows that inactive H-ras is distributed between lipid rafts and a cholesterol-independent microdomain. Conversely, activated H-ras and K-ras reside predominantly in nonoverlapping, cholesterol-independent microdomains. Galectin-1 stabilizes the association of activated H-ras with these nonraft microdomains, whereas K-ras clustering is supported by farnesylation, but not geranylgeranylation. These results illustrate that the inner plasma membrane comprises a complex mosaic of discrete microdomains. Differential spatial localization within this framework can likely account for the distinct signal outputs from the highly homologous Ras proteins.

Key Words: cholesterol; lipid rafts; immunogold; electron microscopy; statistical analysis


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Mol. Biol. Cell 16, 2704-2718
   Abstract »    Full Text »    PDF »
PIP2 signaling in lipid domains: a critical re-evaluation.
J. van Rheenen, E. Mulugeta Achame, H. Janssen, J. Calafat, and K. Jalink (2005)
EMBO J. 24, 1664-1673
   Abstract »    Full Text »    PDF »
Single-molecule diffusion measurements of H-Ras at the plasma membrane of live cells reveal microdomain localization upon activation.
P. H. M. Lommerse, B. E. Snaar-Jagalska, H. P. Spaink, and T. Schmidt (2005)
J. Cell Sci. 118, 1799-1809
   Abstract »    Full Text »    PDF »
Galectin-1 Sensitizes Resting Human T Lymphocytes to Fas (CD95)-mediated Cell Death via Mitochondrial Hyperpolarization, Budding, and Fission.
P. Matarrese, A. Tinari, E. Mormone, G. A. Bianco, M. A. Toscano, B. Ascione, G. A. Rabinovich, and W. Malorni (2005)
J. Biol. Chem. 280, 6969-6985
   Abstract »    Full Text »    PDF »
Glioma Formation in Neurofibromatosis 1 Reflects Preferential Activation of K-RAS in Astrocytes.
B. Dasgupta, W. Li, A. Perry, and D. H. Gutmann (2005)
Cancer Res. 65, 236-245
   Abstract »    Full Text »    PDF »
Analysis of Detergent-Resistant Membranes in Arabidopsis. Evidence for Plasma Membrane Lipid Rafts.
G. H.H. Borner, D. J. Sherrier, T. Weimar, L. V. Michaelson, N. D. Hawkins, A. MacAskill, J. A. Napier, M. H. Beale, K. S. Lilley, and P. Dupree (2005)
Plant Physiology 137, 104-116
   Abstract »    Full Text »    PDF »
Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane.
S. Schuck and K. Simons (2004)
J. Cell Sci. 117, 5955-5964
   Abstract »    Full Text »    PDF »
Galectin-3 Augments K-Ras Activation and Triggers a Ras Signal That Attenuates ERK but Not Phosphoinositide 3-Kinase Activity.
G. Elad-Sfadia, R. Haklai, E. Balan, and Y. Kloog (2004)
J. Biol. Chem. 279, 34922-34930
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Three Separable Domains Regulate GTP-Dependent Association of H-ras with the Plasma Membrane.
B. Rotblat, I. A. Prior, C. Muncke, R. G. Parton, Y. Kloog, Y. I. Henis, and J. F. Hancock (2004)
Mol. Cell. Biol. 24, 6799-6810
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Accumulation of Glycosphingolipids in Niemann-Pick C Disease Disrupts Endosomal Transport.
D. t. Vruchte, E. Lloyd-Evans, R. J. Veldman, D. C. A. Neville, R. A. Dwek, F. M. Platt, W. J. van Blitterswijk, and D. J. Sillence (2004)
J. Biol. Chem. 279, 26167-26175
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Shear-Dependent Capping of L-Selectin and P-Selectin Glycoprotein Ligand 1 by E-Selectin Signals Activation of High-Avidity {beta}2-Integrin on Neutrophils.
C. E. Green, D. N. Pearson, R. T. Camphausen, D. E. Staunton, and S. I. Simon (2004)
J. Immunol. 172, 7780-7790
   Abstract »    Full Text »    PDF »
Markers for Detergent-resistant Lipid Rafts Occupy Distinct and Dynamic Domains in Native Membranes.
B. S. Wilson, S. L. Steinberg, K. Liederman, J. R. Pfeiffer, Z. Surviladze, J. Zhang, L. E. Samelson, L.-h. Yang, P. G. Kotula, and J. M. Oliver (2004)
Mol. Biol. Cell 15, 2580-2592
   Abstract »    Full Text »    PDF »

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