An inhibitor of the proteasomal deubiquitinating enzyme USP14 induces tau elimination in cultured neurons

J Biol Chem. 2017 Nov 24;292(47):19209-19225. doi: 10.1074/jbc.M117.815126. Epub 2017 Sep 26.

Abstract

The ubiquitin-proteasome system (UPS) is responsible for most selective protein degradation in eukaryotes and regulates numerous cellular processes, including cell cycle control and protein quality control. A component of this system, the deubiquitinating enzyme USP14, associates with the proteasome where it can rescue substrates from degradation by removal of the ubiquitin tag. We previously found that a small-molecule inhibitor of USP14, known as IU1, can increase the rate of degradation of a subset of proteasome substrates. We report here the synthesis and characterization of 87 variants of IU1, which resulted in the identification of a 10-fold more potent USP14 inhibitor that retains specificity for USP14. The capacity of this compound, IU1-47, to enhance protein degradation in cells was tested using as a reporter the microtubule-associated protein tau, which has been implicated in many neurodegenerative diseases. Using primary neuronal cultures, IU1-47 was found to accelerate the rate of degradation of wild-type tau, the pathological tau mutants P301L and P301S, and the A152T tau variant. We also report that a specific residue in tau, lysine 174, is critical for the IU1-47-mediated tau degradation by the proteasome. Finally, we show that IU1-47 stimulates autophagic flux in primary neurons. In summary, these findings provide a powerful research tool for investigating the complex biology of USP14.

Keywords: IU1; IU1-47; neurodegenerative disease; proteasome; small molecule; tauopathy; ubiquitin.

MeSH terms

  • Animals
  • Cells, Cultured
  • Cytoplasm / metabolism
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / drug effects
  • Embryo, Mammalian / metabolism*
  • Enzyme Inhibitors / chemical synthesis
  • Enzyme Inhibitors / pharmacology*
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / metabolism*
  • Proteasome Endopeptidase Complex / metabolism
  • Proteolysis
  • Pyrroles / chemical synthesis
  • Pyrroles / pharmacology*
  • Rats, Sprague-Dawley
  • Ubiquitin / metabolism
  • Ubiquitin Thiolesterase / physiology*
  • Ubiquitination
  • tau Proteins / metabolism*

Substances

  • Enzyme Inhibitors
  • IU1-47
  • Pyrroles
  • Ubiquitin
  • Usp14 protein, mouse
  • tau Proteins
  • Ubiquitin Thiolesterase
  • Proteasome Endopeptidase Complex