Regulation of skeletal muscle stiffness and elasticity by titin isoforms: A test of the segmental extension model of resting tension

Kuan Wang, Roger Mccarter, John Wright, Jennate Beverly, Ruben Ramirez-Mitchell

Research output: Contribution to journalArticle

239 Citations (Scopus)

Abstract

To explore the role of titin filaments in muscle elasticity, we measured the resting tension-sarcomere length curves of six rabbit skeletal muscles that express three size classes of titin isoform. The stress-strain curves of the split fibers of these muscles displayed a similar multiphasic shape, with an exponential increase in tension at low sarcomere strain followed by a leveling of tension and a decrease in stiffness at and beyond an elastic limit (yield point) at higher sarcomere strain. Significantly, positive correlations exist between the size of the expressed titin isoform, the sarcomere length at the onset of exponential resting tension, and the yield point of each muscle. Immunoelectron microscopic studies of an epitope in the extensible segment of titin revealed a transition in the elastic behavior of the titin filaments near the yield point sarcomere length of these muscles, providing direct evidence of titin's involvement in the genesis of resting tension. Our data led to the formulation of a segmental extension model of resting tension that recognizes the interplay of three major factors in shaping the stress-strain curves: the net contour length of an extensible segment of titin filaments (between the Z line and the ends of the thick filaments), the intrinsic molecular elasticity of titin, and the strength of titin thick filament anchorage. Our data further suggest that skeletal muscle cells may control and modulate stiffness and elastic limit coordinately by selective expression of specific titin isoforms.

Original languageEnglish
Pages (from-to)7101-7105
Number of pages5
JournalProceedings of the National Academy of Sciences of the United States of America
Volume88
Issue number16
DOIs
Publication statusPublished - 1991
Externally publishedYes

Keywords

  • Cardiac muscle
  • Connectin
  • Elastic filaments
  • Elastic limit
  • Sarcomere matrix

ASJC Scopus subject areas

  • General

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