Acetylation of the KXGS motifs in tau is a critical determinant in modulation of tau aggregation and clearance

Hum Mol Genet. 2014 Jan 1;23(1):104-16. doi: 10.1093/hmg/ddt402. Epub 2013 Aug 19.

Abstract

The accumulation of hyperphosphorylated tau in neurofibrillary tangles (NFTs) is a neuropathological hallmark of tauopathies, including Alzheimer's disease (AD) and chronic traumatic encephalopathy, but effective therapies directly targeting the tau protein are currently lacking. Herein, we describe a novel mechanism in which the acetylation of tau on KXGS motifs inhibits phosphorylation on this same motif, and also prevents tau aggregation. Using a site-specific antibody to detect acetylation of KXGS motifs, we demonstrate that these sites are hypoacetylated in patients with AD, as well as a mouse model of tauopathy, suggesting that loss of acetylation on KXGS motifs renders tau vulnerable to pathogenic insults. Furthermore, we identify histone deacetylase 6 (HDAC6) as the enzyme responsible for the deacetylation of these residues, and provide proof of concept that acute treatment with a selective and blood-brain barrier-permeable HDAC6 inhibitor enhances acetylation and decreases phosphorylation on tau's KXGS motifs in vivo. As such, we have uncovered a novel therapeutic pathway that can be manipulated to block the formation of pathogenic tau species in disease.

Publication types

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

MeSH terms

  • Acetylation
  • Aged
  • Aged, 80 and over
  • Alzheimer Disease / drug therapy
  • Alzheimer Disease / metabolism*
  • Amino Acid Motifs / drug effects
  • Animals
  • Disease Models, Animal
  • Female
  • HEK293 Cells
  • HeLa Cells
  • Histone Deacetylase 6
  • Histone Deacetylase Inhibitors / pharmacology
  • Histone Deacetylases / metabolism*
  • Humans
  • Hydroxamic Acids / pharmacology
  • Male
  • Mice
  • Phosphorylation
  • Protein Multimerization
  • Pyrimidines / pharmacology
  • tau Proteins / chemistry*
  • tau Proteins / metabolism*

Substances

  • Histone Deacetylase Inhibitors
  • Hydroxamic Acids
  • MAPT protein, human
  • Mapt protein, mouse
  • N-hydroxy-2-(1-phenylcycloproylamino)pyrimidine-5-carboxamide
  • Pyrimidines
  • tau Proteins
  • HDAC6 protein, human
  • Histone Deacetylase 6
  • Histone Deacetylases