Single-molecule imaging reveals the mechanism of bidirectional replication initiation in metazoa

Cell. 2024 Jul 25;187(15):3992-4009.e25. doi: 10.1016/j.cell.2024.05.024. Epub 2024 Jun 11.

Abstract

Metazoan genomes are copied bidirectionally from thousands of replication origins. Replication initiation entails the assembly and activation of two CMG helicases (Cdc45⋅Mcm2-7⋅GINS) at each origin. This requires several replication firing factors (including TopBP1, RecQL4, and DONSON) whose exact roles are still under debate. How two helicases are correctly assembled and activated at each origin is a long-standing question. By visualizing the recruitment of GINS, Cdc45, TopBP1, RecQL4, and DONSON in real time, we uncovered that replication initiation is surprisingly dynamic. First, TopBP1 transiently binds to the origin and dissociates before the start of DNA synthesis. Second, two Cdc45 are recruited together, even though Cdc45 alone cannot dimerize. Next, two copies of DONSON and two GINS simultaneously arrive at the origin, completing the assembly of two CMG helicases. Finally, RecQL4 is recruited to the CMG⋅DONSON⋅DONSON⋅CMG complex and promotes DONSON dissociation and CMG activation via its ATPase activity.

Keywords: Cdc45; DONSON; GINS; KEHRMIT; RecQL4; TopBP1; origin firing; replication initiation.

MeSH terms

  • Animals
  • Cell Cycle Proteins* / metabolism
  • DNA Helicases / metabolism
  • DNA Replication*
  • DNA-Binding Proteins / metabolism
  • Humans
  • RecQ Helicases / metabolism
  • Replication Origin
  • Single Molecule Imaging*

Substances

  • Cell Cycle Proteins
  • DNA Helicases
  • RecQ Helicases
  • DNA-Binding Proteins
  • RECQL4 protein, human
  • CDC45 protein, human