Increased Rho activation and PKC-mediated smooth muscle contractility in the absence of caveolin-1

Am J Physiol Cell Physiol. 2006 Dec;291(6):C1326-35. doi: 10.1152/ajpcell.00046.2006.

Abstract

Caveolae are omega-shaped membrane invaginations that are abundant in smooth muscle cells. Since many receptors and signaling proteins co-localize with caveolae, these have been proposed to integrate important signaling pathways. The aim of this study was to test whether RhoA/Rho-kinase and protein kinase C (PKC)-mediated Ca(2+) sensitization depends on caveolae using caveolin (Cav)-1-deficient (KO) and wild-type (WT) mice. In WT smooth muscle, caveolae were detected and Cav-1, -2 and -3 proteins were expressed. Relative mRNA expression levels were approximately 15:1:1 for Cav-1, -2, and -3, respectively. Caveolae were absent in KO and reduced levels of Cav-2 and Cav-3 proteins were seen. In intact ileum longitudinal muscle, no differences in the responses to 5-HT or the muscarinic agonist carbachol were found, whereas contraction elicited by endothelin-1 was reduced. Rho activation by GTPgammaS was increased in KO compared with WT as shown using a pull-down assay. Following alpha-toxin permeabilization, no difference in Ca(2+) sensitivity or in Ca(2+) sensitization was detected. In KO femoral arteries, phorbol 12,13-dibutyrate (PDBu)-induced and PKC-mediated contraction was increased. This was associated with increased alpha(1)-adrenergic contraction. Following inhibition of PKC, alpha(1)-adrenergic contraction was normalized. PDBu-induced Ca(2+) sensitization was not increased in permeabilized femoral arteries. In conclusion, Rho activation, but not Ca(2+) sensitization, depends on caveolae in the ileum. Moreover, PKC driven arterial contraction is increased in the absence of caveolin-1. This depends on an intact plasma membrane and is not associated with altered Ca(2+) sensitivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic alpha-Agonists / metabolism
  • Animals
  • Calcium / metabolism
  • Caveolae / metabolism
  • Caveolin 1 / genetics
  • Caveolin 1 / metabolism*
  • Caveolin 2 / genetics
  • Caveolin 2 / metabolism
  • Caveolin 3 / genetics
  • Caveolin 3 / metabolism
  • Enzyme Activation
  • Enzyme Inhibitors / metabolism
  • Femoral Artery / cytology
  • Femoral Artery / metabolism
  • Humans
  • Ileum / cytology
  • Ileum / metabolism
  • Imidazoles / metabolism
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle Contraction / physiology*
  • Muscle, Smooth / cytology
  • Muscle, Smooth / physiology*
  • Myocytes, Smooth Muscle / metabolism
  • Myocytes, Smooth Muscle / ultrastructure
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism*
  • Protein Serine-Threonine Kinases / metabolism
  • Type C Phospholipases / metabolism
  • rho-Associated Kinases
  • rhoA GTP-Binding Protein / metabolism*

Substances

  • Adrenergic alpha-Agonists
  • Caveolin 1
  • Caveolin 2
  • Caveolin 3
  • Enzyme Inhibitors
  • Imidazoles
  • Intracellular Signaling Peptides and Proteins
  • Protein Serine-Threonine Kinases
  • rho-Associated Kinases
  • Protein Kinase C
  • Type C Phospholipases
  • rhoA GTP-Binding Protein
  • cirazoline
  • Calcium