Drosophila model of myosin myopathy rescued by overexpression of a TRIM-protein family member

Proc Natl Acad Sci U S A. 2018 Jul 10;115(28):E6566-E6575. doi: 10.1073/pnas.1800727115. Epub 2018 Jun 26.

Abstract

Myosin is a molecular motor indispensable for body movement and heart contractility. Apart from pure cardiomyopathy, mutations in MYH7 encoding slow/β-cardiac myosin heavy chain also cause skeletal muscle disease with or without cardiac involvement. Mutations within the α-helical rod domain of MYH7 are mainly associated with Laing distal myopathy. To investigate the mechanisms underlying the pathology of the recurrent causative MYH7 mutation (K1729del), we have developed a Drosophila melanogaster model of Laing distal myopathy by genomic engineering of the Drosophila Mhc locus. Homozygous MhcK1728del animals die during larval/pupal stages, and both homozygous and heterozygous larvae display reduced muscle function. Flies expressing only MhcK1728del in indirect flight and jump muscles, and heterozygous MhcK1728del animals, were flightless, with reduced movement and decreased lifespan. Sarcomeres of MhcK1728del mutant indirect flight muscles and larval body wall muscles were disrupted with clearly disorganized muscle filaments. Homozygous MhcK1728del larvae also demonstrated structural and functional impairments in heart muscle, which were not observed in heterozygous animals, indicating a dose-dependent effect of the mutated allele. The impaired jump and flight ability and the myopathy of indirect flight and leg muscles associated with MhcK1728del were fully suppressed by expression of Abba/Thin, an E3-ligase that is essential for maintaining sarcomere integrity. This model of Laing distal myopathy in Drosophila recapitulates certain morphological phenotypic features seen in Laing distal myopathy patients with the recurrent K1729del mutation. Our observations that Abba/Thin modulates these phenotypes suggest that manipulation of Abba/Thin activity levels may be beneficial in Laing distal myopathy.

Keywords: Abba/Thin; Drosophila; Laing distal myopathy; myosin; myosin myopathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Disease Models, Animal
  • Distal Myopathies* / genetics
  • Distal Myopathies* / metabolism
  • Distal Myopathies* / pathology
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster
  • Genetic Loci*
  • Homozygote
  • Humans
  • Mutation*
  • Myocardium / metabolism*
  • Myocardium / pathology
  • Myosin Heavy Chains* / genetics
  • Myosin Heavy Chains* / metabolism
  • Tripartite Motif Proteins* / biosynthesis
  • Tripartite Motif Proteins* / genetics

Substances

  • Drosophila Proteins
  • Tripartite Motif Proteins
  • Myosin Heavy Chains