A farnesyltransferase inhibitor activates lysosomes and reduces tau pathology in mice with tauopathy

Sci Transl Med. 2019 Mar 27;11(485):eaat3005. doi: 10.1126/scitranslmed.aat3005.

Abstract

Tau inclusions are a shared feature of many neurodegenerative diseases, among them frontotemporal dementia caused by tau mutations. Treatment approaches for these conditions include targeting posttranslational modifications of tau proteins, maintaining a steady-state amount of tau, and preventing its tendency to aggregate. We discovered a new regulatory pathway for tau degradation that operates through the farnesylated protein, Rhes, a GTPase in the Ras family. Here, we show that treatment with the farnesyltransferase inhibitor lonafarnib reduced Rhes and decreased brain atrophy, tau inclusions, tau sumoylation, and tau ubiquitination in the rTg4510 mouse model of tauopathy. In addition, lonafarnib treatment attenuated behavioral abnormalities in rTg4510 mice and reduced microgliosis in mouse brain. Direct reduction of Rhes in the rTg4510 mouse by siRNA reproduced the results observed with lonafarnib treatment. The mechanism of lonafarnib action mediated by Rhes to reduce tau pathology was shown to operate through activation of lysosomes. We finally showed in mouse brain and in human induced pluripotent stem cell-derived neurons a normal developmental increase in Rhes that was initially suppressed by tau mutations. The known safety of lonafarnib revealed in human clinical trials for cancer suggests that this drug could be repurposed for treating tauopathies.

Publication types

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

MeSH terms

  • Animals
  • Brain / drug effects
  • Brain / metabolism
  • Brain / pathology
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Farnesyltranstransferase / antagonists & inhibitors*
  • Female
  • GTP-Binding Proteins / antagonists & inhibitors
  • GTP-Binding Proteins / genetics
  • GTP-Binding Proteins / metabolism
  • Humans
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism
  • Lysosomes / drug effects
  • Lysosomes / metabolism
  • Male
  • Mice
  • Mice, Transgenic
  • Mutation
  • Neurons / drug effects
  • Neurons / metabolism
  • Piperidines / pharmacology
  • Proteolysis / drug effects
  • Pyridines / pharmacology
  • RNA, Small Interfering / genetics
  • Tauopathies / drug therapy*
  • Tauopathies / metabolism*
  • Tauopathies / pathology
  • Translational Research, Biomedical
  • tau Proteins / genetics
  • tau Proteins / metabolism

Substances

  • Enzyme Inhibitors
  • MAPT protein, human
  • Mapt protein, mouse
  • Piperidines
  • Pyridines
  • RNA, Small Interfering
  • tau Proteins
  • Farnesyltranstransferase
  • GTP-Binding Proteins
  • Rasd2 protein, mouse
  • lonafarnib