Identification of the hyaluronic acid pathway as a therapeutic target for facioscapulohumeral muscular dystrophy

Sci Adv. 2019 Dec 11;5(12):eaaw7099. doi: 10.1126/sciadv.aaw7099. eCollection 2019 Dec.

Abstract

Facioscapulohumeral muscular dystrophy (FSHD) is linked to epigenetic derepression of the germline/embryonic transcription factor DUX4 in skeletal muscle. However, the etiology of muscle pathology is not fully understood, as DUX4 misexpression is not tightly correlated with disease severity. Using a DUX4-inducible cell model, we show that multiple DUX4-induced molecular pathologies that have been observed in patient-derived disease models are mediated by the signaling molecule hyaluronic acid (HA), which accumulates following DUX4 induction. These pathologies include formation of RNA granules, FUS aggregation, DNA damage, caspase activation, and cell death. We also observe previously unidentified pathologies including mislocalization of mitochondria and the DUX4- and HA-binding protein C1QBP. These pathologies are prevented by 4-methylumbelliferone, an inhibitor of HA biosynthesis. Critically, 4-methylumbelliferone does not disrupt DUX4-C1QBP binding and has only a limited effect on DUX4 transcriptional activity, establishing that HA signaling has a central function in pathology and is a target for FSHD therapeutics.

Publication types

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

MeSH terms

  • Carrier Proteins / genetics*
  • Cell Death / genetics
  • Cell Line
  • DNA Damage / genetics
  • Epigenesis, Genetic / genetics
  • Gene Expression Regulation / drug effects
  • Germ-Line Mutation / genetics
  • Homeodomain Proteins / genetics*
  • Humans
  • Hyaluronic Acid / genetics
  • Hyaluronic Acid / metabolism*
  • Hymecromone / pharmacology
  • Mitochondrial Proteins / genetics*
  • Muscle Fibers, Skeletal / drug effects
  • Muscular Dystrophy, Facioscapulohumeral / drug therapy
  • Muscular Dystrophy, Facioscapulohumeral / genetics*
  • Muscular Dystrophy, Facioscapulohumeral / metabolism
  • Muscular Dystrophy, Facioscapulohumeral / pathology
  • Myoblasts / metabolism
  • Myoblasts / pathology
  • Protein Aggregation, Pathological / genetics*
  • Protein Aggregation, Pathological / pathology
  • Protein Binding / drug effects
  • RNA-Binding Protein FUS / genetics
  • Signal Transduction / drug effects

Substances

  • C1QBP protein, human
  • Carrier Proteins
  • DUX4L1 protein, human
  • FUS protein, human
  • Homeodomain Proteins
  • Mitochondrial Proteins
  • RNA-Binding Protein FUS
  • Hymecromone
  • Hyaluronic Acid