Ratchet-like polypeptide translocation mechanism of the AAA+ disaggregase Hsp104

Science. 2017 Jul 21;357(6348):273-279. doi: 10.1126/science.aan1052. Epub 2017 Jun 15.

Abstract

Hsp100 polypeptide translocases are conserved members of the AAA+ family (adenosine triphosphatases associated with diverse cellular activities) that maintain proteostasis by unfolding aberrant and toxic proteins for refolding or proteolytic degradation. The Hsp104 disaggregase from Saccharomyces cerevisiae solubilizes stress-induced amorphous aggregates and amyloids. The structural basis for substrate recognition and translocation is unknown. Using a model substrate (casein), we report cryo-electron microscopy structures at near-atomic resolution of Hsp104 in different translocation states. Substrate interactions are mediated by conserved, pore-loop tyrosines that contact an 80-angstrom-long unfolded polypeptide along the axial channel. Two protomers undergo a ratchet-like conformational change that advances pore loop-substrate interactions by two amino acids. These changes are coupled to activation of specific nucleotide hydrolysis sites and, when transmitted around the hexamer, reveal a processive rotary translocation mechanism and substrate-responsive flexibility during Hsp104-catalyzed disaggregation.

Publication types

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

MeSH terms

  • Caseins / metabolism
  • Cryoelectron Microscopy
  • Heat-Shock Proteins / chemistry*
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism
  • Heat-Shock Proteins / ultrastructure
  • Hydrolysis
  • Nucleotides / chemistry
  • Nucleotides / metabolism
  • Peptides / chemistry
  • Peptides / genetics
  • Peptides / metabolism
  • Promoter Regions, Genetic
  • Protein Domains
  • Protein Transport
  • Saccharomyces cerevisiae / enzymology*
  • Saccharomyces cerevisiae Proteins / chemistry*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Saccharomyces cerevisiae Proteins / ultrastructure
  • Substrate Specificity
  • Tyrosine / genetics
  • Tyrosine / metabolism

Substances

  • Caseins
  • Heat-Shock Proteins
  • Nucleotides
  • Peptides
  • Saccharomyces cerevisiae Proteins
  • HsP104 protein, S cerevisiae
  • Tyrosine