The nebulin SH3 domain is dispensable for normal skeletal muscle structure but is required for effective active load bearing in mouse

J Cell Sci. 2013 Dec 1;126(Pt 23):5477-89. doi: 10.1242/jcs.137026. Epub 2013 Sep 17.

Abstract

Nemaline myopathy (NM) is a congenital myopathy with an estimated incidence of 150,000 live births. It is caused by mutations in thin filament components, including nebulin, which accounts for about 50% of the cases. The identification of NM cases with nonsense mutations resulting in loss of the extreme C-terminal SH3 domain of nebulin suggests an important role of the nebulin SH3 domain, which is further supported by the recent demonstration of its role in IGF-1-induced sarcomeric actin filament formation through targeting of N-WASP to the Z-line. To provide further insights into the functional significance of the nebulin SH3 domain in the Z-disk and to understand the mechanisms by which truncations of nebulin lead to NM, we took two approaches: (1) an affinity-based proteomic screening to identify novel interaction partners of the nebulin SH3 domain; and (2) generation and characterization of a novel knockin mouse model with a premature stop codon in the nebulin gene, eliminating its C-terminal SH3 domain (NebΔSH3 mouse). Surprisingly, detailed analyses of NebΔSH3 mice revealed no structural or histological skeletal muscle abnormalities and no changes in gene expression or localization of interaction partners of the nebulin SH3 domain, including myopalladin, palladin, zyxin and N-WASP. Also, no significant effect on peak isometric stress production, passive tensile stress or Young's modulus was found. However, NebΔSH3 muscle displayed a slightly altered force-frequency relationship and was significantly more susceptible to eccentric contraction-induced injury, suggesting that the nebulin SH3 domain protects against eccentric contraction-induced injury and possibly plays a role in fine-tuning the excitation-contraction coupling mechanism.

Keywords: Nebulin; Nemaline myopathy; Sarcomere; Skeletal muscle; Z-line.

Publication types

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

MeSH terms

  • Animals
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism
  • Elastic Modulus / physiology
  • Excitation Contraction Coupling / physiology
  • Female
  • Gene Expression
  • Humans
  • Isometric Contraction / physiology
  • Male
  • Mice
  • Muscle Proteins / chemistry
  • Muscle Proteins / deficiency
  • Muscle Proteins / genetics*
  • Muscle Proteins / metabolism
  • Muscle, Skeletal / metabolism*
  • Muscle, Skeletal / pathology
  • Myopathies, Nemaline / genetics
  • Myopathies, Nemaline / metabolism
  • Myopathies, Nemaline / pathology
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • Tensile Strength / physiology
  • Weight-Bearing / physiology
  • Wiskott-Aldrich Syndrome Protein, Neuronal / genetics
  • Wiskott-Aldrich Syndrome Protein, Neuronal / metabolism
  • Zyxin / genetics
  • Zyxin / metabolism

Substances

  • Cytoskeletal Proteins
  • Muscle Proteins
  • Phosphoproteins
  • Wasl protein, mouse
  • Wiskott-Aldrich Syndrome Protein, Neuronal
  • Zyx protein, mouse
  • Zyxin
  • palladin protein, mouse
  • nebulin