Knockdown of genes involved in axonal transport enhances the toxicity of human neuromuscular disease-linked MATR3 mutations in Drosophila

FEBS Lett. 2020 Sep;594(17):2800-2818. doi: 10.1002/1873-3468.13858. Epub 2020 Jun 28.

Abstract

Mutations in the nuclear matrix protein Matrin 3 (MATR3) have been identified in amyotrophic lateral sclerosis and myopathy. To investigate the mechanisms underlying MATR3 mutations in neuromuscular diseases and efficiently screen for modifiers of MATR3 toxicity, we generated transgenic MATR3 flies. Our findings indicate that expression of wild-type or mutant MATR3 in motor neurons reduces climbing ability and lifespan of flies, while their expression in indirect flight muscles (IFM) results in abnormal wing positioning and muscle degeneration. In both motor neurons and IFM, mutant MATR3 expression results in more severe phenotypes than wild-type MATR3, demonstrating that the disease-linked mutations confer pathogenicity. We conducted a targeted candidate screen for modifiers of the MATR3 abnormal wing phenotype and identified multiple enhancers involved in axonal transport. Knockdown of these genes enhanced protein levels and insolubility of mutant MATR3. These results suggest that accumulation of mutant MATR3 contributes to toxicity and implicate axonal transport dysfunction in disease pathogenesis.

Keywords: Drosophila; MATR3; amyotrophic lateral sclerosis; genetic screen; multisystem proteinopathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyotrophic Lateral Sclerosis / genetics*
  • Amyotrophic Lateral Sclerosis / metabolism
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Animals, Genetically Modified
  • Axonal Transport / genetics*
  • Brain / metabolism
  • Brain / pathology
  • Disease Models, Animal
  • Drosophila Proteins / antagonists & inhibitors
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / metabolism
  • Epistasis, Genetic
  • Flight, Animal / physiology
  • Gene Expression
  • Humans
  • Longevity / genetics
  • Motor Neurons / metabolism*
  • Motor Neurons / pathology
  • Muscles / metabolism
  • Muscles / pathology
  • Muscular Diseases / genetics*
  • Muscular Diseases / metabolism
  • Muscular Diseases / pathology
  • Nuclear Matrix-Associated Proteins / genetics*
  • Nuclear Matrix-Associated Proteins / metabolism
  • Phenotype
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism
  • Transgenes
  • Wings, Animal / metabolism
  • Wings, Animal / pathology

Substances

  • Drosophila Proteins
  • MATR3 protein, human
  • Nuclear Matrix-Associated Proteins
  • RNA, Messenger
  • RNA, Small Interfering
  • RNA-Binding Proteins