Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells

J Cell Biol. 1993 Aug;122(4):789-807. doi: 10.1083/jcb.122.4.789.

Abstract

GPI-linked protein molecules become Triton-insoluble during polarized sorting to the apical cell surface of epithelial cells. These insoluble complexes, enriched in cholesterol, glycolipids, and GPI-linked proteins, have been isolated by flotation on sucrose density gradients and are thought to contain the putative GPI-sorting machinery. As the cellular origin and molecular protein components of this complex remain unknown, we have begun to characterize these low-density insoluble complexes isolated from MDCK cells. We find that these complexes, which represent 0.4-0.8% of the plasma membrane, ultrastructurally resemble caveolae and are over 150-fold enriched in a model GPI-anchored protein and caveolin, a caveolar marker protein. However, they exclude many other plasma membrane associated molecules and organelle-specific marker enzymes, suggesting that they represent microdomains of the plasma membrane. In addition to caveolin, these insoluble complexes contain a subset of hydrophobic plasma membrane proteins and cytoplasmically-oriented signaling molecules, including: (a) GTP-binding proteins--both small and heterotrimeric; (b) annex II--an apical calcium-regulated phospholipid binding protein with a demonstrated role in exocytic fusion events; (c) c-Yes--an apically localized member of the Src family of non-receptor type protein-tyrosine kinases; and (d) an unidentified serine-kinase activity. As we demonstrate that caveolin is both a transmembrane molecule and a major phospho-acceptor component of these complexes, we propose that caveolin could function as a transmembrane adaptor molecule that couples luminal GPI-linked proteins with cytoplasmically oriented signaling molecules during GPI-membrane trafficking or GPI-mediated signal transduction events. In addition, our results have implications for understanding v-Src transformation and the actions of cholera and pertussis toxins on hetero-trimeric G proteins.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Caveolin 1
  • Caveolins*
  • Cell Fractionation
  • Cell Line
  • Cell Membrane / physiology
  • Cell Polarity
  • Detergents
  • Dogs
  • Fibroblasts / chemistry
  • Fibroblasts / ultrastructure
  • GTP-Binding Proteins / metabolism
  • Glycosylphosphatidylinositols / physiology*
  • In Vitro Techniques
  • Membrane Glycoproteins / physiology*
  • Membrane Proteins / chemistry
  • Membrane Proteins / metabolism*
  • Phosphoproteins / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-yes
  • Rats
  • Signal Transduction
  • Solubility
  • Thyroid Gland / metabolism
  • src-Family Kinases*

Substances

  • Cav1 protein, rat
  • Caveolin 1
  • Caveolins
  • Detergents
  • Glycosylphosphatidylinositols
  • Membrane Glycoproteins
  • Membrane Proteins
  • Phosphoproteins
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-yes
  • src-Family Kinases
  • GTP-Binding Proteins