Smooth muscle archvillin: a novel regulator of signaling and contractility in vascular smooth muscle

J Cell Sci. 2004 Oct 1;117(Pt 21):5043-57. doi: 10.1242/jcs.01378. Epub 2004 Sep 21.

Abstract

The mechanisms by which protein kinase C (PKC) and extracellular-signal-regulated kinases (ERK1/2) govern smooth-muscle contractility remain unclear. Calponin (CaP), an actin-binding protein and PKC substrate, mediates signaling through ERK1/2. We report here that CaP sequences containing the CaP homology (CH) domain bind to the C-terminal 251 amino acids of smooth-muscle archvillin (SmAV), a new splice variant of supervillin, which is a known actin- and myosin-II-binding protein. The CaP-SmAV interaction is demonstrated by reciprocal yeast two-hybrid and blot-overlay assays and by colocalization in COS-7 cells. In differentiated smooth muscle, endogenous SmAV and CaP co-fractionate and co-translocate to the cell cortex after stimulation by agonist. Antisense knockdown of SmAV in tissue inhibits both the activation of ERK1/2 and contractions stimulated by either agonist or PKC activation. This ERK1/2 signaling and contractile defect is similar to that observed in CaP knockdown experiments. In A7r5 smooth-muscle cells, PKC activation by phorbol esters induces the reorganization of endogenous, membrane-localized SmAV and microfilament-associated CaP into podosome-like structures that also contain F-actin, nonmuscle myosin IIB and ERK1/2. These results indicate that SmAV contributes to the regulation of contractility through a CaP-mediated signaling pathway, involving PKC activation and phosphorylation of ERK1/2.

Publication types

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

MeSH terms

  • Alternative Splicing
  • Amino Acid Sequence
  • Animals
  • Aorta / metabolism
  • Blotting, Western
  • COS Cells
  • Calcium-Binding Proteins / metabolism
  • Calponins
  • DNA, Complementary / metabolism
  • Enzyme Activation
  • Ferrets
  • Glutathione Transferase / metabolism
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology*
  • Microfilament Proteins / metabolism
  • Microfilament Proteins / physiology*
  • Microscopy, Fluorescence
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Models, Genetic
  • Molecular Sequence Data
  • Muscle, Smooth / metabolism*
  • Oligonucleotides, Antisense / pharmacology
  • Phosphorylation
  • Protein Binding
  • Protein Kinase C / metabolism
  • Protein Structure, Tertiary
  • Recombinant Proteins / chemistry
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Homology, Amino Acid
  • Signal Transduction
  • Subcellular Fractions / metabolism
  • Time Factors
  • Transfection
  • Two-Hybrid System Techniques

Substances

  • Calcium-Binding Proteins
  • DNA, Complementary
  • Membrane Proteins
  • Microfilament Proteins
  • Oligonucleotides, Antisense
  • Recombinant Proteins
  • Svil protein, mouse
  • Glutathione Transferase
  • Protein Kinase C
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3