Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis

EMBO J. 2006 Mar 8;25(5):1126-36. doi: 10.1038/sj.emboj.7601002. Epub 2006 Feb 16.

Abstract

Replication licensing is carefully regulated to restrict replication to once in a cell cycle. In higher eukaryotes, regulation of the licensing factor Cdt1 by proteolysis and Geminin is essential to prevent re-replication. We show here that the N-terminal 100 amino acids of human Cdt1 are recognized for proteolysis by two distinct E3 ubiquitin ligases during S-G2 phases. Six highly conserved amino acids within the 10 first amino acids of Cdt1 are essential for DDB1-Cul4-mediated proteolysis. This region is also involved in proteolysis following DNA damage. The second E3 is SCF-Skp2, which recognizes the Cy-motif-mediated Cyclin E/A-cyclin-dependent kinase-phosphorylated region. Consistently, in HeLa cells cosilenced of Skp2 and Cul4, Cdt1 remained stable in S-G2 phases. The Cul4-containing E3 is active during ongoing replication, while SCF-Skp2 operates both in S and G2 phases. PCNA binds to Cdt1 through the six conserved N-terminal amino acids. PCNA is essential for Cul4- but not Skp2-directed degradation during DNA replication and following ultraviolet-irradiation. Our data unravel multiple distinct pathways regulating Cdt1 to block re-replication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Cycle Proteins / antagonists & inhibitors
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Cycle Proteins / pharmacology
  • Cells, Cultured
  • Cullin Proteins / antagonists & inhibitors
  • Cullin Proteins / genetics
  • Cullin Proteins / metabolism*
  • Cyclin A / metabolism
  • Cyclin E / metabolism
  • DNA Damage
  • DNA Replication / radiation effects
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Fibroblasts / metabolism
  • Geminin
  • Gene Silencing
  • HeLa Cells
  • Humans
  • Kidney / embryology
  • Kidney / metabolism
  • Mice
  • Peptide Hydrolases / chemistry*
  • Phosphorylation
  • Proliferating Cell Nuclear Antigen / metabolism
  • RNA, Small Interfering / pharmacology
  • S-Phase Kinase-Associated Proteins / antagonists & inhibitors
  • S-Phase Kinase-Associated Proteins / genetics
  • S-Phase Kinase-Associated Proteins / metabolism*
  • SKP Cullin F-Box Protein Ligases / antagonists & inhibitors
  • SKP Cullin F-Box Protein Ligases / genetics
  • SKP Cullin F-Box Protein Ligases / metabolism*
  • Ubiquitin / metabolism
  • Ultraviolet Rays

Substances

  • CDT1 protein, human
  • CUL4A protein, human
  • Cell Cycle Proteins
  • Cullin Proteins
  • Cyclin A
  • Cyclin E
  • DDB1 protein, human
  • DNA-Binding Proteins
  • GMNN protein, human
  • Geminin
  • Proliferating Cell Nuclear Antigen
  • RNA, Small Interfering
  • S-Phase Kinase-Associated Proteins
  • Ubiquitin
  • SKP Cullin F-Box Protein Ligases
  • Peptide Hydrolases