Allosteric landscapes of eukaryotic cytoplasmic Hsp70s are shaped by evolutionary tuning of key interfaces

Proc Natl Acad Sci U S A. 2018 Nov 20;115(47):11970-11975. doi: 10.1073/pnas.1811105115. Epub 2018 Nov 5.

Abstract

The 70-kDa heat shock proteins (Hsp70s) are molecular chaperones that perform a wide range of critical cellular functions. They assist in the folding of newly synthesized proteins, facilitate assembly of specific protein complexes, shepherd proteins across membranes, and prevent protein misfolding and aggregation. Hsp70s perform these functions by a conserved mechanism that relies on allosteric cycles of nucleotide-modulated binding and release of client proteins. Current models for Hsp70 allostery have come from extensive study of the bacterial Hsp70, DnaK. Extending our understanding to eukaryotic Hsp70s is extremely important not only in providing a likely common mechanistic framework but also because of their central roles in cellular physiology. In this study, we examined the allosteric behaviors of the eukaryotic cytoplasmic Hsp70s, HspA1 and Hsc70, and found significant differences from that of DnaK. We found that HspA1 and Hsc70 favor a state in which the nucleotide-binding domain (NBD) and substrate-binding domain (SBD) are intimately docked significantly more as compared to DnaK. Past work established that the NBD-SBD interface and the helical lid-β-SBD interface govern the allosteric landscape of DnaK. Here, we identified sites on these interfaces that differ between eukaryotic cytoplasmic Hsp70s and DnaK. Our mutational analysis has revealed key evolutionary variations that account for the population shifts between the docked and undocked conformations. These results underline the tunability of Hsp70 functions by modulation of allosteric interfaces through evolutionary diversification and also suggest sites where the binding of small-molecule modulators could influence Hsp70 function.

Keywords: Hsp70; allostery; chaperone; methyl-TROSY NMR.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Allosteric Regulation / genetics
  • Allosteric Site / genetics
  • Animals
  • Computational Biology / methods
  • Cytoplasm / metabolism
  • Cytosol / metabolism
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / metabolism
  • Eukaryota / genetics
  • Eukaryota / metabolism
  • Eukaryotic Cells / metabolism
  • Evolution, Molecular
  • HSC70 Heat-Shock Proteins / metabolism*
  • HSP70 Heat-Shock Proteins / metabolism*
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism
  • Humans
  • Models, Molecular
  • Protein Conformation
  • Protein Domains

Substances

  • Escherichia coli Proteins
  • HSC70 Heat-Shock Proteins
  • HSP70 Heat-Shock Proteins
  • HSPA1A protein, human
  • Heat-Shock Proteins
  • dnaK protein, E coli