Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins

J Biol Chem. 1996 Jun 21;271(25):15160-5. doi: 10.1074/jbc.271.25.15160.

Abstract

Caveolae are microdomains of the plasma membrane that have been implicated in signal transduction. Caveolin, a 21-24-kDa integral membrane protein, is a principal component of the caveolae membrane. Recently, we and others have identified a family of caveolin-related proteins; caveolin has been retermed caveolin-1. Caveolin-3 is most closely related to caveolin-1, but caveolin-3 mRNA is expressed only in muscle tissue types. Here, we examine (i) the expression of caveolin-3 protein in muscle tissue types and (ii) its localization within skeletal muscle fibers by immunofluorescence microscopy and subcellular fractionation. For this purpose, we generated a novel monoclonal antibody (mAb) probe that recognizes the unique N-terminal region of caveolin-3, but not other members of the caveolin gene family. A survey of tissues and muscle cell types by Western blot analysis reveals that the caveolin-3 protein is selectively expressed only in heart and skeletal muscle tissues, cardiac myocytes, and smooth muscle cells. Immunolocalization of caveolin-3 in skeletal muscle fibers demonstrates that caveolin-3 is localized to the sarcolemma (muscle cell plasma membrane) and coincides with the distribution of another muscle-specific plasma membrane marker protein, dystrophin. In addition, caveolin-3 protein expression is dramatically induced during the differentiation of C2C12 skeletal myoblasts in culture. Using differentiated C2C12 skeletal myoblasts as a model system, we observe that caveolin-3 co-fractionates with cytoplasmic signaling molecules (G-proteins and Src-like kinases) and members of the dystrophin complex (dystrophin, alpha-sarcoglycan, and beta-dystroglycan), but is clearly separated from the bulk of cellular proteins. Caveolin-3 co-immunoprecipitates with antibodies directed against dystrophin, suggesting that they are physically associated as a discrete complex. These results are consistent with previous immunoelectron microscopic studies demonstrating that dystrophin is localized to plasma membrane caveolae in smooth muscle cells.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antibodies, Monoclonal
  • Aorta
  • Blotting, Western
  • Caveolin 3
  • Caveolins*
  • Cell Line
  • Chlorocebus aethiops
  • Cytoskeletal Proteins / isolation & purification
  • Cytoskeletal Proteins / metabolism*
  • Dystroglycans
  • Dystrophin / isolation & purification
  • Dystrophin / metabolism*
  • Epitopes
  • Female
  • Immunohistochemistry
  • Membrane Glycoproteins / isolation & purification
  • Membrane Glycoproteins / metabolism*
  • Membrane Proteins / biosynthesis*
  • Membrane Proteins / isolation & purification
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Molecular Sequence Data
  • Muscle Proteins / biosynthesis
  • Muscle, Skeletal / metabolism*
  • Muscle, Smooth, Vascular / metabolism*
  • Myocardium / metabolism*
  • Rats
  • Sarcoglycans
  • Sarcolemma / metabolism*
  • Transfection

Substances

  • Antibodies, Monoclonal
  • Cav3 protein, mouse
  • Cav3 protein, rat
  • Caveolin 3
  • Caveolins
  • Cytoskeletal Proteins
  • Dystrophin
  • Epitopes
  • Membrane Glycoproteins
  • Membrane Proteins
  • Muscle Proteins
  • Sarcoglycans
  • Dystroglycans