The Chaperonin TRiC/CCT Associates with Prefoldin through a Conserved Electrostatic Interface Essential for Cellular Proteostasis

Cell. 2019 Apr 18;177(3):751-765.e15. doi: 10.1016/j.cell.2019.03.012. Epub 2019 Apr 4.

Abstract

Maintaining proteostasis in eukaryotic protein folding involves cooperation of distinct chaperone systems. To understand how the essential ring-shaped chaperonin TRiC/CCT cooperates with the chaperone prefoldin/GIMc (PFD), we integrate cryoelectron microscopy (cryo-EM), crosslinking-mass-spectrometry and biochemical and cellular approaches to elucidate the structural and functional interplay between TRiC/CCT and PFD. We find these hetero-oligomeric chaperones associate in a defined architecture, through a conserved interface of electrostatic contacts that serves as a pivot point for a TRiC-PFD conformational cycle. PFD alternates between an open "latched" conformation and a closed "engaged" conformation that aligns the PFD-TRiC substrate binding chambers. PFD can act after TRiC bound its substrates to enhance the rate and yield of the folding reaction, suppressing non-productive reaction cycles. Disrupting the TRiC-PFD interaction in vivo is strongly deleterious, leading to accumulation of amyloid aggregates. The supra-chaperone assembly formed by PFD and TRiC is essential to prevent toxic conformations and ensure effective cellular proteostasis.

Keywords: CCT; GIMc; TRiC; XL-MS; chaperone; chaperonin; cryo-EM; prefoldin; proteostasis.

Publication types

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

MeSH terms

  • Actins / chemistry
  • Actins / metabolism
  • Chaperonin Containing TCP-1 / chemistry
  • Chaperonin Containing TCP-1 / genetics
  • Chaperonin Containing TCP-1 / metabolism*
  • Cryoelectron Microscopy
  • Humans
  • Models, Molecular
  • Molecular Chaperones / chemistry
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism*
  • Protein Folding
  • Protein Structure, Quaternary
  • Protein Subunits / chemistry
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Proteostasis / physiology*
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / isolation & purification
  • Saccharomyces cerevisiae / metabolism
  • Static Electricity

Substances

  • Actins
  • Molecular Chaperones
  • Protein Subunits
  • Recombinant Proteins
  • prefoldin
  • Chaperonin Containing TCP-1