Cross-bridge cycling gives rise to spatiotemporal heterogeneity of dynamic subcellular mechanics in cardiac myocytes probed with atomic force microscopy

Am J Physiol Heart Circ Physiol. 2010 Mar;298(3):H853-60. doi: 10.1152/ajpheart.00427.2009. Epub 2009 Dec 18.

Abstract

To study how the dynamic subcellular mechanical properties of the heart relate to the fundamental underlying process of actin-myosin cross-bridge cycling, we developed a novel atomic force microscope elastography technique for mapping spatiotemporal stiffness of isolated, spontaneously beating neonatal rat cardiomyocytes. Cells were indented repeatedly at a rate close but unequal to their contractile frequency. The resultant changes in pointwise apparent elastic modulus cycled at a predictable envelope frequency between a systolic value of 26.2 +/- 5.1 kPa and a diastolic value of 7.8 +/- 4.1 kPa at a representative depth of 400 nm. In cells probed along their major axis, spatiotemporal changes in systolic stiffness displayed a heterogeneous pattern, reflecting the banded sarcomeric structure of underlying myofibrils. Treatment with blebbistatin eliminated contractile activity and resulted in a uniform apparent modulus of 6.5 +/- 4.8 kPa. This study represents the first quantitative dynamic mechanical mapping of beating cardiomyocytes. The technique provides a means of probing the micromechanical effects of disease processes and pharmacological treatments on beating cardiomyocytes, providing new insights and relating subcellular cardiac structure and function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism*
  • Actins / ultrastructure
  • Animals
  • Biomechanical Phenomena
  • Cells, Cultured
  • Heterocyclic Compounds, 4 or More Rings / pharmacology
  • Microscopy, Atomic Force
  • Models, Biological
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / ultrastructure
  • Myofibrils / metabolism
  • Myofibrils / ultrastructure
  • Myosins / metabolism*
  • Myosins / ultrastructure
  • Rats
  • Rats, Sprague-Dawley
  • Time Factors

Substances

  • Actins
  • Heterocyclic Compounds, 4 or More Rings
  • blebbistatin
  • Myosins