Translocation of caveolin regulates stretch-induced ERK activity in vascular smooth muscle cells

Am J Physiol Heart Circ Physiol. 2004 May;286(5):H1845-52. doi: 10.1152/ajpheart.00593.2003.

Abstract

Mechanical stress contributes to vascular disease related to hypertension. Activation of ERK is key to mediating cellular proliferation and vascular remodeling in response to stretch stress. However, the mechanism by which stretch mediates ERK activation in the vascular tissue is still unclear. Caveolin, a major component of a flasklike invaginated caveolae, acts as an adaptor protein for an integrin-mediated signaling pathway. We found that cyclic stretch transiently induced translocation of caveolin from caveolae to noncaveolar membrane sites in vascular smooth muscle cells (VSMCs). This translocation of caveolin was determined by detergent solubility, sucrose gradient fractionation, and immunocytochemistry. Cyclic stretch induced ERK activation; the activity peaked at 5 min (the early phase), decreased gradually, but persisted up to 120 min (the late phase). Disruption of caveolae by methyl-beta-cyclodextrin, decreasing the caveolar caveolin and accumulating the noncaveolar caveolin, enhanced ERK activation in both the early and late phases. When endogenous caveolins were downregulated, however, the late-phase ERK activation was subsided completely. Caveolin, which was translocated to noncaveolar sites in response to stretch, is associated with beta1-integrins as well as with Fyn and Shc, components required for ERK activation. Taken together, caveolin in caveolae may keep ERK inactive, but when caveolin is translocated to noncaveolar sites in response to stretch stress, caveolin mediates stretch-induced ERK activation through an association with beta1-integrins/Fyn/Shc. We suggest that stretch-induced translocation of caveolin to noncaveolar sites plays an important role in mediating stretch-induced ERK activation in VSMCs.

Publication types

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

MeSH terms

  • Actin Cytoskeleton / physiology
  • Adaptor Proteins, Signal Transducing*
  • Adaptor Proteins, Vesicular Transport / metabolism
  • Animals
  • Biological Transport / physiology
  • Caveolae / metabolism
  • Caveolae / physiology
  • Caveolins / chemistry
  • Caveolins / metabolism*
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Down-Regulation / physiology
  • Enzyme Activation / physiology
  • Integrins / metabolism
  • Mitogen-Activated Protein Kinases / metabolism*
  • Muscle, Smooth, Vascular / cytology
  • Muscle, Smooth, Vascular / enzymology*
  • Myocytes, Smooth Muscle / enzymology*
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-fyn
  • Rats
  • Shc Signaling Adaptor Proteins
  • Signal Transduction / physiology
  • Solubility
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • Stress, Mechanical
  • Tissue Distribution

Substances

  • Adaptor Proteins, Signal Transducing
  • Adaptor Proteins, Vesicular Transport
  • Caveolins
  • Integrins
  • Proto-Oncogene Proteins
  • Shc Signaling Adaptor Proteins
  • Shc1 protein, rat
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • Fyn protein, rat
  • Proto-Oncogene Proteins c-fyn
  • Mitogen-Activated Protein Kinases