Bidirectional substrate shuttling between the 26S proteasome and the Cdc48 ATPase promotes protein degradation

Mol Cell. 2024 Apr 4;84(7):1290-1303.e7. doi: 10.1016/j.molcel.2024.01.029. Epub 2024 Feb 23.

Abstract

Most eukaryotic proteins are degraded by the 26S proteasome after modification with a polyubiquitin chain. Substrates lacking unstructured segments cannot be degraded directly and require prior unfolding by the Cdc48 ATPase (p97 or VCP in mammals) in complex with its ubiquitin-binding partner Ufd1-Npl4 (UN). Here, we use purified yeast components to reconstitute Cdc48-dependent degradation of well-folded model substrates by the proteasome. We show that a minimal system consists of the 26S proteasome, the Cdc48-UN ATPase complex, the proteasome cofactor Rad23, and the Cdc48 cofactors Ubx5 and Shp1. Rad23 and Ubx5 stimulate polyubiquitin binding to the 26S proteasome and the Cdc48-UN complex, respectively, allowing these machines to compete for substrates before and after their unfolding. Shp1 stimulates protein unfolding by the Cdc48-UN complex rather than substrate recruitment. Experiments in yeast cells confirm that many proteins undergo bidirectional substrate shuttling between the 26S proteasome and Cdc48 ATPase before being degraded.

Keywords: AAA ATPase; Cdc48; ERAD; p97; proteasome; protein degradation; protein unfolding; shuttling factor; ubiquitin.

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Polyubiquitin / metabolism
  • Proteasome Endopeptidase Complex* / metabolism
  • Proteolysis
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Ubiquitin / metabolism
  • Valosin Containing Protein / genetics
  • Valosin Containing Protein / metabolism

Substances

  • Adenosine Triphosphatases
  • ATP dependent 26S protease
  • Cell Cycle Proteins
  • Polyubiquitin
  • Proteasome Endopeptidase Complex
  • Saccharomyces cerevisiae Proteins
  • Ubiquitin
  • Valosin Containing Protein