Checkpoint-Independent Regulation of Origin Firing by Mrc1 through Interaction with Hsk1 Kinase

Mol Cell Biol. 2017 Mar 17;37(7):e00355-16. doi: 10.1128/MCB.00355-16. Print 2017 Apr 1.

Abstract

Mrc1 is a conserved checkpoint mediator protein that transduces the replication stress signal to the downstream effector kinase. The loss of mrc1 checkpoint activity results in the aberrant activation of late/dormant origins in the presence of hydroxyurea. Mrc1 was also suggested to regulate orders of early origin firing in a checkpoint-independent manner, but its mechanism was unknown. Here we identify HBS (Hsk1 bypass segment) on Mrc1. An ΔHBS mutant does not activate late/dormant origin firing in the presence of hydroxyurea but causes the precocious and enhanced activation of weak early-firing origins during normal S-phase progression and bypasses the requirement for Hsk1 for growth. This may be caused by the disruption of intramolecular binding between HBS and NTHBS (N-terminal target of HBS). Hsk1 binds to Mrc1 through HBS and phosphorylates a segment adjacent to NTHBS, disrupting the intramolecular interaction. We propose that Mrc1 exerts a "brake" on initiation (through intramolecular interactions) and that this brake can be released (upon the loss of intramolecular interactions) by either the Hsk1-mediated phosphorylation of Mrc1 or the deletion of HBS (or a phosphomimic mutation of putative Hsk1 target serine/threonine), which can bypass the function of Hsk1 for growth. The brake mechanism may explain the checkpoint-independent regulation of early origin firing in fission yeast.

Keywords: DNA replication timing; Hsk1; Mrc1; intramolecular interaction; replication checkpoint.

MeSH terms

  • Amino Acid Sequence
  • Cell Cycle Checkpoints* / drug effects
  • Cell Cycle Proteins / metabolism*
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Hydroxyurea / pharmacology
  • Models, Biological
  • Mutation / genetics
  • Peptides / pharmacology
  • Phosphorylation / drug effects
  • Protein Binding / drug effects
  • Protein Serine-Threonine Kinases / metabolism*
  • Replication Origin* / drug effects
  • Schizosaccharomyces / drug effects
  • Schizosaccharomyces / growth & development
  • Schizosaccharomyces / metabolism*
  • Schizosaccharomyces pombe Proteins / chemistry
  • Schizosaccharomyces pombe Proteins / genetics
  • Schizosaccharomyces pombe Proteins / metabolism*
  • Signal Transduction / drug effects

Substances

  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • MRC1 protein, S pombe
  • Peptides
  • Schizosaccharomyces pombe Proteins
  • HSK1 protein, S pombe
  • Protein Serine-Threonine Kinases
  • Hydroxyurea