Ca2+-dependent rapid Ca2+ sensitization of contraction in arterial smooth muscle

Circ Res. 2007 Jan 5;100(1):121-9. doi: 10.1161/01.RES.0000253902.90489.df. Epub 2006 Dec 7.

Abstract

Ca(2+) ion is a universal intracellular messenger that regulates numerous biological functions. In smooth muscle, Ca(2+) with calmodulin activates myosin light chain (MLC) kinase to initiate a rapid MLC phosphorylation and contraction. To test the hypothesis that regulation of MLC phosphatase is involved in the rapid development of MLC phosphorylation and contraction during Ca(2+) transient, we compared Ca(2+) signal, MLC phosphorylation, and 2 modes of inhibition of MLC phosphatase, phosphorylation of CPI-17 Thr38 and MYPT1 Thr853, during alpha(1) agonist-induced contraction with/without various inhibitors in intact rabbit femoral artery. Phenylephrine rapidly induced CPI-17 phosphorylation from a negligible amount to a peak value of 0.38+/-0.04 mol of Pi/mol within 7 seconds following stimulation, similar to the rapid time course of Ca(2+) rise and MLC phosphorylation. This rapid CPI-17 phosphorylation was dramatically inhibited by either blocking Ca(2+) release from the sarcoplasmic reticulum or by pretreatment with protein kinase C inhibitors, suggesting an involvement of Ca(2+)-dependent protein kinase C. This was followed by a slow Ca(2+)-independent and Rho-kinase/protein kinase C-dependent phosphorylation of CPI-17. In contrast, MYPT1 phosphorylation had only a slow component that increased from 0.29+/-0.09 at rest to the peak of 0.68+/-0.14 mol of Pi/mol at 1 minute, similar to the time course of contraction. Thus, there are 2 components of the Ca(2+) sensitization through inhibition of MLC phosphatase. Our results support the hypothesis that the initial rapid Ca(2+) rise induces a rapid inhibition of MLC phosphatase coincident with the Ca(2+)-induced MLC kinase activation to synergistically initiate a rapid MLC phosphorylation and contraction in arteries with abundant CPI-17 content.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adrenergic alpha-Agonists / pharmacology
  • Animals
  • Calcium / metabolism*
  • Calcium Channel Blockers / pharmacology
  • Calcium Signaling
  • Femoral Artery / drug effects
  • Femoral Artery / metabolism
  • Femoral Artery / physiology*
  • In Vitro Techniques
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Muscle Proteins / metabolism
  • Muscle, Smooth, Vascular / physiology*
  • Myosin Light Chains / metabolism
  • Myosin-Light-Chain Phosphatase / metabolism
  • Phenylephrine / pharmacology
  • Phosphoprotein Phosphatases / metabolism
  • Phosphoproteins / metabolism
  • Phosphorylation / drug effects
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase Inhibitors / pharmacology
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Protein Subunits / metabolism
  • Rabbits
  • Time Factors
  • Vasoconstriction / drug effects
  • Vasoconstriction / physiology*
  • Vasoconstrictor Agents / pharmacology
  • rho-Associated Kinases

Substances

  • Adrenergic alpha-Agonists
  • CPI-17 protein, Oryctolagus cuniculus
  • Calcium Channel Blockers
  • Intracellular Signaling Peptides and Proteins
  • Muscle Proteins
  • Myosin Light Chains
  • Phosphoproteins
  • Protein Kinase Inhibitors
  • Protein Subunits
  • Vasoconstrictor Agents
  • Phenylephrine
  • Protein Serine-Threonine Kinases
  • rho-Associated Kinases
  • Protein Kinase C
  • Phosphoprotein Phosphatases
  • Myosin-Light-Chain Phosphatase
  • Calcium