Computational simulation of hypertrophic cardiomyopathy mutations in troponin I: influence of increased myofilament calcium sensitivity on isometric force, ATPase and [Ca2+]i

J Biomech. 2007;40(9):2044-52. doi: 10.1016/j.jbiomech.2006.09.026. Epub 2006 Nov 30.

Abstract

Familial hypertrophic cardiomyopathy (FHC) is an inherited disease that is characterized by ventricular hypertrophy, cardiac arrhythmias and increased risk of premature sudden death. FHC is caused by autosomal-dominant mutations in genes for a number of sarcomeric proteins; many mutations in Ca(2+)-regulatory proteins of the cardiac thin filament are associated with increased Ca(2+) sensitivity of myofilament function. Computational simulations were used to investigate the possibility that these mutations could affect the Ca(2+) transient and mechanical response of a myocyte during a single cardiac cycle. We used existing experimental data for specific mutations of cardiac troponin I that exhibit increased Ca(2+) sensitivity in physiological and biophysical assays. The simulated Ca(2+) transients were used as input for a three-dimensional half-sarcomere biomechanical model with filament compliance to predict the resulting force. Mutations with the highest Ca(2+) affinity (lowest K(m)) values, exhibit the largest decrease in peak Ca(2+) assuming a constant influx of Ca(2+) into the cytoplasm; they also prolong Ca(2+) removal but have little effect on diastolic Ca(2+). Biomechanical model results suggest that these cTnI mutants would increase peak force despite the decrease in peak [Ca(2+)](i). There is a corresponding increase in net ATP hydrolysis, with no change in tension cost (ATP hydrolyzed per unit of time-integrated tension). These simulations suggest that myofilament-initiated hypertrophic signaling could be associated with decreased [Ca(2+)](i), increased stress/strain, and/or increased ATP flux.

Publication types

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

MeSH terms

  • Actin Cytoskeleton / enzymology
  • Actin Cytoskeleton / metabolism*
  • Adenosine Triphosphatases / metabolism*
  • Biomechanical Phenomena
  • Calcium / metabolism*
  • Calcium / physiology
  • Cardiomyopathy, Hypertrophic, Familial / enzymology
  • Cardiomyopathy, Hypertrophic, Familial / genetics*
  • Cardiomyopathy, Hypertrophic, Familial / metabolism
  • Cardiomyopathy, Hypertrophic, Familial / physiopathology
  • Computer Simulation*
  • Humans
  • Models, Biological
  • Myocardial Contraction / genetics
  • Signal Transduction / genetics
  • Troponin I / genetics*
  • Troponin I / physiology

Substances

  • Troponin I
  • Adenosine Triphosphatases
  • Calcium