The deubiquitinating enzyme Usp14 controls ciliogenesis and Hedgehog signaling

Hum Mol Genet. 2019 Mar 1;28(5):764-777. doi: 10.1093/hmg/ddy380.

Abstract

Primary cilia are hair-like organelles that play crucial roles in vertebrate development, organogenesis and when dysfunctional result in pleiotropic human genetic disorders called ciliopathies, characterized by overlapping phenotypes, such as renal and hepatic cysts, skeletal defects, retinal degeneration and central nervous system malformations. Primary cilia act as communication hubs to transfer extracellular signals into intracellular responses and are essential for Hedgehog (Hh) signal transduction in mammals. Despite the renewed interest in this ancient organelle of growing biomedical importance, the molecular mechanisms that trigger cilia formation, extension and ciliary signal transduction are still not fully understood. Here we provide, for the first time, evidence that the deubiquitinase ubiquitin-specific protease-14 (Usp14), a major regulator of the ubiquitin proteasome system (UPS), controls ciliogenesis, cilia elongation and Hh signal transduction. Moreover, we show that pharmacological inhibition of Usp14 positively affects Hh signal transduction in a model of autosomal dominant polycystic kidney disease. These findings provide new insight into the spectrum of action of UPS in cilia biology and may provide novel opportunities for therapeutic intervention in human conditions associated with ciliary dysfunction.

Publication types

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

MeSH terms

  • Animals
  • Biomarkers
  • Cell Line
  • Cilia / metabolism*
  • Deubiquitinating Enzymes / genetics
  • Deubiquitinating Enzymes / metabolism
  • Fibroblasts
  • Fluorescent Antibody Technique
  • Gene Expression Regulation
  • Hedgehog Proteins / metabolism*
  • Mice
  • Mutation
  • Organogenesis / genetics*
  • Protein Transport
  • Signal Transduction*
  • TRPP Cation Channels / genetics
  • TRPP Cation Channels / metabolism
  • Ubiquitin Thiolesterase / genetics*
  • Ubiquitin Thiolesterase / metabolism*

Substances

  • Biomarkers
  • Hedgehog Proteins
  • TRPP Cation Channels
  • Usp14 protein, mouse
  • polycystic kidney disease 1 protein
  • Deubiquitinating Enzymes
  • Ubiquitin Thiolesterase