The unstructured linker of Mlh1 contains a motif required for endonuclease function which is mutated in cancers

Proc Natl Acad Sci U S A. 2022 Oct 18;119(42):e2212870119. doi: 10.1073/pnas.2212870119. Epub 2022 Oct 10.

Abstract

Eukaryotic DNA mismatch repair (MMR) depends on recruitment of the Mlh1-Pms1 endonuclease (human MLH1-PMS2) to mispaired DNA. Both Mlh1 and Pms1 contain a long unstructured linker that connects the N- and carboxyl-terminal domains. Here, we demonstrated the Mlh1 linker contains a conserved motif (Saccharomyces cerevisiae residues 391-415) required for MMR. The Mlh1-R401A,D403A-Pms1 linker motif mutant protein was defective for MMR and endonuclease activity in vitro, even though the conserved motif could be >750 Å from the carboxyl-terminal endonuclease active site or the N-terminal adenosine triphosphate (ATP)-binding site. Peptides encoding this motif inhibited wild-type Mlh1-Pms1 endonuclease activity. The motif functioned in vivo at different sites within the Mlh1 linker and within the Pms1 linker. Motif mutations in human cancers caused a loss-of-function phenotype when modeled in S. cerevisiae. These results suggest that the Mlh1 motif promotes the PCNA-activated endonuclease activity of Mlh1-Pms1 via interactions with DNA, PCNA, RFC, or other domains of the Mlh1-Pms1 complex.

Keywords: DNA mismatch repair; DNA replication; Msh2–Msh6; intrinsically disordered protein.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Triphosphate / metabolism
  • DNA / metabolism
  • DNA Mismatch Repair / genetics
  • DNA-Binding Proteins / metabolism
  • Endonucleases / genetics
  • Endonucleases / metabolism
  • Humans
  • Mismatch Repair Endonuclease PMS2 / genetics
  • MutL Protein Homolog 1 / genetics
  • MutL Protein Homolog 1 / metabolism
  • MutL Proteins
  • MutS Homolog 2 Protein / metabolism
  • Mutant Proteins / metabolism
  • Neoplasms*
  • Proliferating Cell Nuclear Antigen / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins* / metabolism

Substances

  • DNA-Binding Proteins
  • MLH1 protein, S cerevisiae
  • MLH1 protein, human
  • Mutant Proteins
  • PMS1 protein, S cerevisiae
  • Proliferating Cell Nuclear Antigen
  • Saccharomyces cerevisiae Proteins
  • Adenosine Triphosphate
  • DNA
  • Endonucleases
  • Mismatch Repair Endonuclease PMS2
  • MutL Protein Homolog 1
  • MutL Proteins
  • MutS Homolog 2 Protein