Muscle-specific stress fibers give rise to sarcomeres in cardiomyocytes

Elife. 2018 Dec 12:7:e42144. doi: 10.7554/eLife.42144.

Abstract

The sarcomere is the contractile unit within cardiomyocytes driving heart muscle contraction. We sought to test the mechanisms regulating actin and myosin filament assembly during sarcomere formation. Therefore, we developed an assay using human cardiomyocytes to monitor sarcomere assembly. We report a population of muscle stress fibers, similar to actin arcs in non-muscle cells, which are essential sarcomere precursors. We show sarcomeric actin filaments arise directly from muscle stress fibers. This requires formins (e.g., FHOD3), non-muscle myosin IIA and non-muscle myosin IIB. Furthermore, we show short cardiac myosin II filaments grow to form ~1.5 μm long filaments that then 'stitch' together to form the stack of filaments at the core of the sarcomere (i.e., the A-band). A-band assembly is dependent on the proper organization of actin filaments and, as such, is also dependent on FHOD3 and myosin IIB. We use this experimental paradigm to present evidence for a unifying model of sarcomere assembly.

Keywords: actin; cardiomyocytes; cell biology; formins; human; myosin; sarcomeres.

Publication types

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

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / metabolism
  • Cell Line
  • Cell Line, Tumor
  • Formins
  • HeLa Cells
  • Humans
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism
  • Microscopy, Confocal
  • Molecular Motor Proteins / genetics
  • Molecular Motor Proteins / metabolism
  • Muscle Fibers, Skeletal / cytology
  • Muscle Fibers, Skeletal / metabolism*
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / metabolism*
  • Myosin Heavy Chains / genetics
  • Myosin Heavy Chains / metabolism
  • Nonmuscle Myosin Type IIB / genetics
  • Nonmuscle Myosin Type IIB / metabolism
  • RNA Interference
  • Sarcomeres / metabolism*
  • Stress Fibers / metabolism*

Substances

  • Actins
  • FHOD3 protein, human
  • Formins
  • MYH9 protein, human
  • Microfilament Proteins
  • Molecular Motor Proteins
  • Nonmuscle Myosin Type IIB
  • nonmuscle myosin type IIB heavy chain
  • Myosin Heavy Chains