Cellular Models of Aggregation-dependent Template-directed Proteolysis to Characterize Tau Aggregation Inhibitors for Treatment of Alzheimer Disease

J Biol Chem. 2015 Apr 24;290(17):10862-75. doi: 10.1074/jbc.M114.616029. Epub 2015 Mar 10.

Abstract

Alzheimer disease (AD) is a degenerative tauopathy characterized by aggregation of Tau protein through the repeat domain to form intraneuronal paired helical filaments (PHFs). We report two cell models in which we control the inherent toxicity of the core Tau fragment. These models demonstrate the properties of prion-like recruitment of full-length Tau into an aggregation pathway in which template-directed, endogenous truncation propagates aggregation through the core Tau binding domain. We use these in combination with dissolution of native PHFs to quantify the activity of Tau aggregation inhibitors (TAIs). We report the synthesis of novel stable crystalline leucomethylthioninium salts (LMTX®), which overcome the pharmacokinetic limitations of methylthioninium chloride. LMTX®, as either a dihydromesylate or a dihydrobromide salt, retains TAI activity in vitro and disrupts PHFs isolated from AD brain tissues at 0.16 μM. The Ki value for intracellular TAI activity, which we have been able to determine for the first time, is 0.12 μM. These values are close to the steady state trough brain concentration of methylthioninium ion (0.18 μM) that is required to arrest progression of AD on clinical and imaging end points and the minimum brain concentration (0.13 μM) required to reverse behavioral deficits and pathology in Tau transgenic mice.

Keywords: Alzheimer Disease; Cell Biology; LMTX; Methylthioninium; Prion-like Processing; Protein Aggregation; Tau Protein (Tau); Tauopathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / drug therapy*
  • Alzheimer Disease / metabolism*
  • Animals
  • Brain / drug effects
  • Brain / metabolism
  • Cell Line
  • Humans
  • Methylene Blue / analogs & derivatives
  • Methylene Blue / chemical synthesis
  • Methylene Blue / chemistry
  • Methylene Blue / pharmacology
  • Mice
  • Mice, Transgenic
  • Models, Biological
  • Protein Aggregates / drug effects
  • Protein Aggregation, Pathological / drug therapy*
  • Protein Aggregation, Pathological / metabolism*
  • Protein Interaction Domains and Motifs
  • Proteolysis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • tau Proteins / chemistry*
  • tau Proteins / metabolism*

Substances

  • MAPT protein, human
  • Protein Aggregates
  • Recombinant Proteins
  • tau Proteins
  • hydromethylthionine
  • Methylene Blue