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(Received for publication, October 16, 1996, and in revised form, December 9, 1996)
From the Department of Pathology, Harvard Medical School, Beth
Israel Deaconess Medical Center, Boston, Massachusetts 02215 and the
Regulated signal transduction in discrete
microdomains of the cell surface is an attractive hypothesis for
achieving spatial and temporal specificity in signaling. A procedure
for purifying caveolae separately from other similarly buoyant
microdomains including those rich in
glycosylphosphatidylinositol-anchored proteins has been developed
(Schnitzer, J. E., McIntosh, D. P., Dvorak, A. M., Liu, J., and Oh, P. (1995) Science 269, 1435-1439) and used here to show that
caveolae contain many signaling molecules including select kinases
(platelet-derived growth factor (PDGF) receptors, protein kinase C,
phosphatidylinositol 3-kinase, and Src-like kinases), phospholipase C,
sphingomyelin, and even phosphoinositides. More importantly, two
different techniques reveal that caveolae function as signal
transducing subcompartments of the plasma membrane. PDGF rapidly
induces phosphorylation of endothelial cell plasmalemmal proteins
residing in caveolae as detected by membrane subfractionation and
confocal immunofluorescence microscopy. This PDGF signaling cascade is
halted when the caveolar compartment is disassembled by filipin.
Finally, in vitro kinase assays show that caveolae contain
most of the intrinsic tyrosine kinase activity of the plasma membrane.
As signal transducing organelles, caveolae organize a distinct set of
signaling molecules to permit direct regionalized signal transduction
within their boundaries.
Volume 272, Number 11,
Issue of March 14, 1997
pp. 7211-7222
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
and
Department of Environmental Health, Harvard School of
Public Health, Boston, Massachusetts 02115
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M. Isshiki, J. Ando, R. Korenaga, H. Kogo, T. Fujimoto, T. Fujita, and A. Kamiya Endothelial Ca2+ waves preferentially originate at specific loci in caveolin-rich cell edges PNAS, April 28, 1998; 95(9): 5009 - 5014. [Abstract] [Full Text] [PDF]
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P. Oh, D. P. McIntosh, and J. E. Schnitzer Dynamin at the Neck of Caveolae Mediates Their Budding to Form Transport Vesicles by GTP-driven Fission from the Plasma Membrane of Endothelium J. Cell Biol., April 6, 1998; 141(1): 101 - 114. [Abstract] [Full Text] [PDF]
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T. Okamoto, A. Schlegel, P. E. Scherer, and M. P. Lisanti Caveolins, a Family of Scaffolding Proteins for Organizing "Preassembled Signaling Complexes" at the Plasma Membrane J. Biol. Chem., March 6, 1998; 273(10): 5419 - 5422. [Full Text] [PDF]
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G. Civenni, S. T. Test, U. Brodbeck, and P. Butikofer In Vitro Incorporation of GPI-Anchored Proteins Into Human Erythrocytes and Their Fate in the Membrane Blood, March 1, 1998; 91(5): 1784 - 1792. [Abstract] [Full Text] [PDF]
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S. Esser, K. Wolburg, H. Wolburg, G. Breier, T. Kurzchalia, and W. Risau Vascular Endothelial Growth Factor Induces Endothelial Fenestrations In Vitro J. Cell Biol., February 23, 1998; 140(4): 947 - 959. [Abstract] [Full Text] [PDF]
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J. P. Deans, S. M. Robbins, M. J. Polyak, and J. A. Savage Rapid Redistribution of CD20 to a Low Density Detergent-insoluble Membrane Compartment J. Biol. Chem., January 2, 1998; 273(1): 344 - 348. [Abstract] [Full Text] [PDF]
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R. Brown Sphingolipid organization in biomembranes: what physical studies of model membranes reveal J. Cell Sci., January 1, 1998; 111(1): 1 - 9. [Abstract] [PDF]
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N. Oka, M. Yamamoto, C. Schwencke, J.-i. Kawabe, T. Ebina, S. Ohno, J. Couet, M. P. Lisanti, and Y. Ishikawa Caveolin Interaction with Protein Kinase C. ISOENZYME-DEPENDENT REGULATION OF KINASE ACTIVITY BY THE CAVEOLIN SCAFFOLDING DOMAIN PEPTIDE J. Biol. Chem., December 26, 1997; 272(52): 33416 - 33421. [Abstract] [Full Text] [PDF]
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T. P. Stauffer and T. Meyer Compartmentalized IgE Receptor-mediated Signal Transduction in Living Cells J. Cell Biol., December 15, 1997; 139(6): 1447 - 1454. [Abstract] [Full Text] [PDF]
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C. C. Mastick and A. R. Saltiel Insulin-stimulated Tyrosine Phosphorylation of Caveolin Is Specific for the Differentiated Adipocyte Phenotype in 3T3-L1 Cells J. Biol. Chem., August 15, 1997; 272(33): 20706 - 20714. [Abstract] [Full Text] [PDF]
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A. Pol, A. Lu, M. Pons, S. Peiro, and C. Enrich Epidermal Growth Factor-mediated Caveolin Recruitment to Early Endosomes and MAPK Activation. ROLE OF CHOLESTEROL AND ACTIN CYTOSKELETON J. Biol. Chem., September 22, 2000; 275(39): 30566 - 30572. [Abstract] [Full Text] [PDF]
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L. P. Henderson, L. Lin, A. Prasad, C. A. Paul, T. Y. Chang, and R. A. Maue Embryonic Striatal Neurons from Niemann-Pick Type C Mice Exhibit Defects in Cholesterol Metabolism and Neurotrophin Responsiveness J. Biol. Chem., June 23, 2000; 275(26): 20179 - 20187. [Abstract] [Full Text] [PDF]
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A. Ros-Baro, C. Lopez-Iglesias, S. Peiro, D. Bellido, M. Palacin, A. Zorzano, and M. Camps Lipid rafts are required for GLUT4 internalization in adipose cells PNAS, October 9, 2001; 98(21): 12050 - 12055. [Abstract] [Full Text] [PDF]
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S. V. Matveev and E. J. Smart Heterologous desensitization of EGF receptors and PDGF receptors by sequestration in caveolae Am J Physiol Cell Physiol, April 1, 2002; 282(4): C935 - C946. [Abstract] [Full Text] [PDF]
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