Titin based viscosity in ventricular physiology: an integrative investigation of PEVK-actin interactions

J Mol Cell Cardiol. 2011 Sep;51(3):428-34. doi: 10.1016/j.yjmcc.2011.06.006. Epub 2011 Jun 16.

Abstract

Viscosity is proposed to modulate diastolic function, but only limited understanding of the source(s) of viscosity exists. In vitro experiments have shown that the proline-glutamic acid-valine-lysine (PEVK) rich element of titin interacts with actin, causing a viscous force in the sarcomere. It is unknown whether this mechanism contributes to viscosity in vivo. We tested the hypothesis that PEVK-actin interaction causes cardiac viscosity and is important in vivo via an integrative physiological study on a unique PEVK knockout (KO) model. Both skinned cardiomyocytes and papillary muscle fibers were isolated from wildtype (WT) and PEVK KO mice and passive viscosity was examined using stretch-hold-release and sinusoidal analysis. Viscosity was reduced by ~60% in KO myocytes and ~50% in muscle fibers at room temperature. The PEVK-actin interaction was not modulated by temperature or diastolic calcium, but was increased by lattice compression. Stretch-hold and sinusoidal frequency protocols on intact isolated mouse hearts showed a smaller, 30-40% reduction in viscosity, possibly due to actomyosin interactions, and showed that microtubules did not contribute to viscosity. Transmitral Doppler echocardiography similarly revealed a 40% decrease in LV chamber viscosity in the PEVK KO in vivo. This integrative study is the first to quantify the influence of a specific molecular (PEVK-actin) viscosity in vivo and shows that PEVK-actin interactions are an important physiological source of viscosity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism*
  • Actomyosin / antagonists & inhibitors
  • Animals
  • Connectin
  • Heart Ventricles / metabolism*
  • Heterocyclic Compounds, 4 or More Rings / pharmacology
  • Male
  • Mice
  • Mice, Knockout
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Myocardium / metabolism
  • Protein Binding / genetics
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Sarcomeres / genetics
  • Sarcomeres / metabolism
  • Viscosity / drug effects

Substances

  • Actins
  • Connectin
  • Heterocyclic Compounds, 4 or More Rings
  • Muscle Proteins
  • blebbistatin
  • Actomyosin
  • Protein Kinases