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

Kenneth S. Song, Philipp E. Scherer, Zhaolan Tang, Takashi Okamoto, Shengwen Li, Mark Chafel, Caryn Chu, D. Stave Kohtz, Michael P. Lisanti

Research output: Contribution to journalArticle

563 Citations (Scopus)

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, α-sarcoglycan, and β-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.

Original languageEnglish (US)
Pages (from-to)15160-15165
Number of pages6
JournalJournal of Biological Chemistry
Volume271
Issue number25
DOIs
StatePublished - 1996

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Caveolin 3
Sarcolemma
Dystrophin
Cardiac Myocytes
Caveolins
Smooth Muscle Myocytes
Muscle
Glycoproteins
Skeletal Muscle
Cells
Cell membranes
Caveolae
Cell Membrane
Skeletal Myoblasts
Tissue
Caveolin 1
Muscles
Proteins
Skeletal Muscle Fibers
Muscle Cells

ASJC Scopus subject areas

  • Biochemistry

Cite this

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. / Song, Kenneth S.; Scherer, Philipp E.; Tang, Zhaolan; Okamoto, Takashi; Li, Shengwen; Chafel, Mark; Chu, Caryn; Kohtz, D. Stave; Lisanti, Michael P.

In: Journal of Biological Chemistry, Vol. 271, No. 25, 1996, p. 15160-15165.

Research output: Contribution to journalArticle

Song, Kenneth S. ; Scherer, Philipp E. ; Tang, Zhaolan ; Okamoto, Takashi ; Li, Shengwen ; Chafel, Mark ; Chu, Caryn ; Kohtz, D. Stave ; Lisanti, Michael P. / 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. In: Journal of Biological Chemistry. 1996 ; Vol. 271, No. 25. pp. 15160-15165.
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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, α-sarcoglycan, and β-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.",
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AU - Scherer, Philipp E.

AU - Tang, Zhaolan

AU - Okamoto, Takashi

AU - Li, Shengwen

AU - Chafel, Mark

AU - Chu, Caryn

AU - Kohtz, D. Stave

AU - Lisanti, Michael P.

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