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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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K. Gaus, E. Gratton, E. P. W. Kable, A. S. Jones, I. Gelissen, L. Kritharides, and W. Jessup (2003)
PNAS 100, 15554-15559
   Abstract »    Full Text »    PDF »
High Affinity for Farnesyltransferase and Alternative Prenylation Contribute Individually to K-Ras4B Resistance to Farnesyltransferase Inhibitors.
J. J. Fiordalisi, R. L. Johnson II, C. A. Weinbaum, K. Sakabe, Z. Chen, P. J. Casey, and A. D. Cox (2003)
J. Biol. Chem. 278, 41718-41727
   Abstract »    Full Text »    PDF »
Activation of mast cells by incorporation of cholesterol into rafts.
T. Baumruker, R. Csonga, E. Pursch, A. Pfeffer, N. Urtz, S. Sutton, E. Bofill-Cardona, M. Cooke, and E. Prieschl (2003)
Int. Immunol. 15, 1207-1218
   Abstract »    Full Text »    PDF »
Caveolin Interacts with the Angiotensin II Type 1 Receptor during Exocytic Transport but Not at the Plasma Membrane.
B. D. Wyse, I. A. Prior, H. Qian, I. C. Morrow, S. Nixon, C. Muncke, T. V. Kurzchalia, W. G. Thomas, R. G. Parton, and J. F. Hancock (2003)
J. Biol. Chem. 278, 23738-23746
   Abstract »    Full Text »    PDF »
Distinct Rates of Palmitate Turnover on Membrane-bound Cellular and Oncogenic H-Ras.
T. L. Baker, H. Zheng, J. Walker, J. L. Coloff, and J. E. Buss (2003)
J. Biol. Chem. 278, 19292-19300
   Abstract »    Full Text »    PDF »
Observing Cell Surface Signaling Domains Using Electron Microscopy.
I. A. Prior, R. G. Parton, and J. F. Hancock (2003)
Sci. STKE 2003, pl9
   Abstract »    Full Text »    PDF »

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