Limits of titin extension in single cardiac myofibrils

J Muscle Res Cell Motil. 1996 Aug;17(4):425-38. doi: 10.1007/BF00123359.

Abstract

Passive force and dynamic stiffness were measured in relaxed, single myofibrils from rabbit ventricle over a wide range of sarcomere lengths, from approximately 2-5 microns. Myofibril stretch up to sarcomere lengths of approximately 3 microns resulted in a steady increase in both force and stiffness. The shape of the length-force and the length-stiffness curves remained fully reproducible for repeated extensions to a sarcomere length of approximately 2.7 microns. Above this length, myofibrillar viscoelastic properties were apparently changed irreversibly, likely due to structural alterations within the titin (connectin) filaments. Stretch beyond approximately 3 microns sarcomere length resulted in a markedly reduced slope of the passive force curve, while the stiffness curve became flat. Thus, cardiac sarcomeres apparently reach a strain limit near a length of 3 microns. Above the strain limit, both curve types frequently showed a series of inflections, which we assumed to result from the disruption of titin-thick filament bonds and consequent addition of previously bound A-band titin segments to the elastic I-band titin portion. Indeed, we confirmed in immunofluorescence microscopic studies, using a monoclonal antibody against titin near the A/I junction, that upon sarcomere stretch beyond the strain limit length, the previously stationary antibody epitopes suddenly moved into the I-band, indicating A-band titin release. Altogether, the passive force/stiffness-length relation of cardiac myofibrils was qualitatively similar to, but quantitatively different from, that reported for skeletal myofibrils. From these results, we inferred that cardiac myofibrils have an approximately two times greater relative I-band titin extensibility than skeletal myofibrils. This could hint at differences in the maximum passive force-bearing capacity of titin filaments in the two muscle types.

MeSH terms

  • Animals
  • Calmodulin-Binding Proteins / chemistry*
  • Carrier Proteins / chemistry*
  • Connectin
  • Electrophoresis, Polyacrylamide Gel
  • Fluorescent Antibody Technique
  • Membrane Proteins / chemistry*
  • Microscopy, Phase-Contrast
  • Muscle Proteins / chemistry*
  • Myocardium / chemistry*
  • Protein Kinases / chemistry*
  • Rabbits

Substances

  • Calmodulin-Binding Proteins
  • Carrier Proteins
  • Connectin
  • Membrane Proteins
  • Muscle Proteins
  • Protein Kinases