Titin force in muscle cells alters lattice order, thick and thin filament protein formation

Proc Natl Acad Sci U S A. 2022 Nov 29;119(48):e2209441119. doi: 10.1073/pnas.2209441119. Epub 2022 Nov 21.

Abstract

Skeletal muscle force production is increased at longer compared to shorter muscle lengths because of length-dependent priming of thick filament proteins in the contractile unit before contraction. Using small-angle X-ray diffraction in combination with a mouse model that specifically cleaves the stretch-sensitive titin protein, we found that titin cleavage diminished the length-dependent priming of the thick filament. Strikingly, a titin-sensitive, length-dependent priming was also present in thin filaments, which seems only possible via bridge proteins between thick and thin filaments in resting muscle, potentially myosin-binding protein C. We further show that these bridges can be forcibly ruptured via high-speed stretches. Our results advance a paradigm shift to the fundamental regulation of length-dependent priming, with titin as the key driver.

Keywords: X-ray diffraction; elasticity; length-dependent activation; mouse; ultrastructure.

Publication types

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

MeSH terms

  • Actin Cytoskeleton* / metabolism
  • Animals
  • Connectin / metabolism
  • Mice
  • Muscle Contraction / physiology
  • Muscle, Skeletal / metabolism
  • Protein Kinases / metabolism
  • Sarcomeres* / metabolism

Substances

  • Connectin
  • titin protein, mouse
  • Protein Kinases