HspB1 and Hsc70 chaperones engage distinct tau species and have different inhibitory effects on amyloid formation

J Biol Chem. 2018 Feb 23;293(8):2687-2700. doi: 10.1074/jbc.M117.803411. Epub 2018 Jan 3.

Abstract

The microtubule-associated protein tau forms insoluble, amyloid-type aggregates in various dementias, most notably Alzheimer's disease. Cellular chaperone proteins play important roles in maintaining protein solubility and preventing aggregation in the crowded cellular environment. Although tau is known to interact with numerous chaperones, it remains unclear how these chaperones function mechanistically to prevent tau aggregation and how chaperones from different classes compare in terms of mechanism. Here, we focused on the small heat shock protein HspB1 (also known as Hsp27) and the constitutive chaperone Hsc70 (also known as HspA8) and report how each chaperone interacts with tau to prevent its fibril formation. Using fluorescence and NMR spectroscopy, we show that the two chaperones inhibit tau fibril formation by distinct mechanisms. HspB1 delayed tau fibril formation by weakly interacting with early species in the aggregation process, whereas Hsc70 was highly efficient at preventing tau fibril elongation, possibly by capping the ends of tau fibrils. Both chaperones recognized aggregation-prone motifs within the microtubule-binding repeat region of tau. However, HspB1 binding remained transient in both aggregation-promoting and non-aggregating conditions, whereas Hsc70 binding was significantly tighter under aggregation-promoting conditions. These differences highlight the fact that chaperones from different families play distinct but complementary roles in the prevention of pathological protein aggregation.

Keywords: 70 kilodalton heat shock protein (Hsp70); aggregation; amyloid; chaperone; small heat shock protein (sHsp); tau.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Substitution
  • Amyloid / chemistry
  • Amyloid / drug effects
  • Amyloid / metabolism*
  • Amyloid / ultrastructure
  • Anticoagulants / pharmacology
  • Cryoelectron Microscopy
  • Dimerization
  • Down-Regulation* / drug effects
  • HSC70 Heat-Shock Proteins / chemistry
  • HSC70 Heat-Shock Proteins / genetics
  • HSC70 Heat-Shock Proteins / metabolism*
  • HSC70 Heat-Shock Proteins / ultrastructure
  • HSP27 Heat-Shock Proteins / chemistry
  • HSP27 Heat-Shock Proteins / genetics
  • HSP27 Heat-Shock Proteins / metabolism*
  • HSP27 Heat-Shock Proteins / ultrastructure
  • Heat-Shock Proteins
  • Heparin / pharmacology
  • Humans
  • Kinetics
  • Models, Molecular*
  • Molecular Chaperones
  • Mutation
  • Protein Aggregation, Pathological / metabolism*
  • Protein Aggregation, Pathological / pathology
  • Protein Aggregation, Pathological / prevention & control
  • Protein Interaction Domains and Motifs
  • Protein Isoforms / chemistry
  • Protein Isoforms / metabolism
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Solubility
  • tau Proteins / chemistry
  • tau Proteins / genetics
  • tau Proteins / metabolism*
  • tau Proteins / ultrastructure

Substances

  • Amyloid
  • Anticoagulants
  • HSC70 Heat-Shock Proteins
  • HSP27 Heat-Shock Proteins
  • HSPA8 protein, human
  • HSPB1 protein, human
  • Heat-Shock Proteins
  • Molecular Chaperones
  • Protein Isoforms
  • Recombinant Fusion Proteins
  • tau Proteins
  • Heparin