Remodelling of Rea1 linker domain drives the removal of assembly factors from pre-ribosomal particles

Nat Commun. 2024 Nov 27;15(1):10309. doi: 10.1038/s41467-024-54698-w.

Abstract

The ribosome maturation factor Rea1 (or Midasin) catalyses the removal of assembly factors from large ribosomal subunit precursors and promotes their export from the nucleus to the cytosol. Rea1 consists of nearly 5000 amino-acid residues and belongs to the AAA+ protein family. It consists of a ring of six AAA+ domains from which the ≈1700 amino-acid residue linker emerges that is subdivided into stem, middle and top domains. A flexible and unstructured D/E rich region connects the linker top to a MIDAS (metal ion dependent adhesion site) domain, which is able to bind the assembly factor substrates. Despite its key importance for ribosome maturation, the mechanism driving assembly factor removal by Rea1 is still poorly understood. Here we demonstrate that the Rea1 linker is essential for assembly factor removal. It rotates and swings towards the AAA+ ring following a complex remodelling scheme involving nucleotide independent as well as nucleotide dependent steps. ATP-hydrolysis is required to engage the linker with the AAA+ ring and ultimately with the AAA+ ring docked MIDAS domain. The interaction between the linker top and the MIDAS domain allows direct force transmission for assembly factor removal.

MeSH terms

  • ATPases Associated with Diverse Cellular Activities / chemistry
  • ATPases Associated with Diverse Cellular Activities / genetics
  • ATPases Associated with Diverse Cellular Activities / metabolism
  • Adenosine Triphosphate / metabolism
  • Models, Molecular
  • Protein Domains*
  • Ribosomal Proteins* / chemistry
  • Ribosomal Proteins* / metabolism
  • Ribosomes / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins* / chemistry
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / isolation & purification
  • Saccharomyces cerevisiae Proteins* / metabolism

Substances

  • Ribosomal Proteins
  • Saccharomyces cerevisiae Proteins
  • MDN1 protein, S cerevisiae
  • Adenosine Triphosphate
  • ATPases Associated with Diverse Cellular Activities