MCM2-7 ring closure involves the Mcm5 C-terminus and triggers Mcm4 ATP hydrolysis

Nat Commun. 2025 Jan 2;16(1):14. doi: 10.1038/s41467-024-55479-1.

Abstract

The eukaryotic helicase MCM2-7, is loaded by ORC, Cdc6 and Cdt1 as a double-hexamer onto replication origins. The insertion of DNA into the helicase leads to partial MCM2-7 ring closure, while ATP hydrolysis is essential for consecutive steps in pre-replicative complex (pre-RC) assembly. Currently it is unknown how MCM2-7 ring closure and ATP-hydrolysis are controlled. A cryo-EM structure of an ORC-Cdc6-Cdt1-MCM2-7 intermediate shows a remodelled, fully-closed Mcm2/Mcm5 interface. The Mcm5 C-terminus (C5) contacts Orc3 and specifically recognises this closed ring. Interestingly, we found that normal helicase loading triggers Mcm4 ATP-hydrolysis, which in turn leads to reorganisation of the MCM2-7 complex and Cdt1 release. However, defective MCM2-7 ring closure, due to mutations at the Mcm2/Mcm5 interface, leads to MCM2-7 ring splitting and complex disassembly. As such we identify Mcm4 as the key ATPase in regulating pre-RC formation. Crucially, a stable Mcm2/Mcm5 interface is essential for productive ATP-hydrolysis-dependent remodelling of the helicase.

MeSH terms

  • Adenosine Triphosphate* / metabolism
  • Cell Cycle Proteins* / chemistry
  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • Cryoelectron Microscopy
  • DNA Helicases / chemistry
  • DNA Helicases / genetics
  • DNA Helicases / metabolism
  • DNA Replication
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Hydrolysis
  • Minichromosome Maintenance Complex Component 4 / genetics
  • Minichromosome Maintenance Complex Component 4 / metabolism
  • Minichromosome Maintenance Proteins / chemistry
  • Minichromosome Maintenance Proteins / genetics
  • Minichromosome Maintenance Proteins / metabolism
  • Origin Recognition Complex / chemistry
  • Origin Recognition Complex / genetics
  • Origin Recognition Complex / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins* / chemistry
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism

Substances

  • Adenosine Triphosphate
  • Cell Cycle Proteins
  • Saccharomyces cerevisiae Proteins
  • Minichromosome Maintenance Proteins
  • MCM5 protein, S cerevisiae
  • MCM4 protein, S cerevisiae
  • Origin Recognition Complex
  • Minichromosome Maintenance Complex Component 4
  • MCM2 protein, S cerevisiae
  • TAH11 protein, S cerevisiae
  • DNA Helicases
  • DNA-Binding Proteins