Molecular Insights into the Differential Effects of Acetylation on the Aggregation of Tau Microtubule-Binding Repeats

J Chem Inf Model. 2024 Apr 22;64(8):3386-3399. doi: 10.1021/acs.jcim.3c01929. Epub 2024 Mar 15.

Abstract

Aggregation of tau protein into intracellular fibrillary inclusions is characterized as the hallmark of tauopathies, including Alzheimer's disease and chronic traumatic encephalopathy. The microtubule-binding (MTB) domain of tau, containing either three or four repeats with sequence similarities, plays an important role in determining tau's aggregation. Previous studies have reported that abnormal acetylation of lysine residues displays a distinct effect on the formation of pathological tau aggregates. However, the underlying molecular mechanism remains mostly elusive. In this study, we performed extensive replica exchange molecular dynamics (REMD) simulations of 144 μs in total to systematically investigate the dimerization of four tau MTB repeats and explore the impacts of Lys280 (K280) or Lys321 (K321) acetylation on the conformational ensembles of the R2 or R3 dimer. Our results show that R3 is the most prone to aggregation among the four repeats, followed by R2 and R4, while R1 displays the weakest aggregation propensity with a disordered structure. Acetylation of K280 could promote the aggregation of R2 peptides by increasing the formation of β-sheet structures and strengthening the interchain interaction. However, K321 acetylation decreases the β-sheet content of the R3 dimer, reduces the ability of R3 peptides to form long β-strands, and promotes the stable helix structure formation. The salt bridge and Y310-Y310 π-π stacking interactions of the R3 dimer are greatly weakened by K321 acetylation, resulting in the inhibition of dimerization. This study uncovers the structural ensembles of tau MTB repeats and provides mechanistic insights into the influences of acetylation on tau aggregation, which may deepen the understanding of the pathogenesis of tauopathies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Humans
  • Microtubules* / metabolism
  • Molecular Dynamics Simulation*
  • Protein Aggregates*
  • Protein Binding
  • Protein Conformation
  • Protein Multimerization
  • tau Proteins* / chemistry
  • tau Proteins* / metabolism

Substances

  • tau Proteins
  • Protein Aggregates