SUV39 SET domains mediate crosstalk of heterochromatic histone marks

Elife. 2021 Sep 15:10:e62682. doi: 10.7554/eLife.62682.

Abstract

The SUV39 class of methyltransferase enzymes deposits histone H3 lysine 9 di- and trimethylation (H3K9me2/3), the hallmark of constitutive heterochromatin. How these enzymes are regulated to mark specific genomic regions as heterochromatic is poorly understood. Clr4 is the sole H3K9me2/3 methyltransferase in the fission yeast Schizosaccharomyces pombe, and recent evidence suggests that ubiquitination of lysine 14 on histone H3 (H3K14ub) plays a key role in H3K9 methylation. However, the molecular mechanism of this regulation and its role in heterochromatin formation remain to be determined. Our structure-function approach shows that the H3K14ub substrate binds specifically and tightly to the catalytic domain of Clr4, and thereby stimulates the enzyme by over 250-fold. Mutations that disrupt this mechanism lead to a loss of H3K9me2/3 and abolish heterochromatin silencing similar to clr4 deletion. Comparison with mammalian SET domain proteins suggests that the Clr4 SET domain harbors a conserved sensor for H3K14ub, which mediates licensing of heterochromatin formation.

Keywords: S. pombe; chromosomes; enzyme kinetics; gene expression; heterochromatin; methyltransferase; posttranslational modifications; protein complex; ubiquitin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Catalytic Domain / genetics
  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • DNA Methylation / genetics
  • Heterochromatin* / chemistry
  • Heterochromatin* / genetics
  • Heterochromatin* / metabolism
  • Histone Code / genetics*
  • Histone-Lysine N-Methyltransferase* / genetics
  • Histone-Lysine N-Methyltransferase* / metabolism
  • Histones* / chemistry
  • Histones* / genetics
  • Histones* / metabolism
  • Lysine / metabolism
  • Schizosaccharomyces pombe Proteins* / genetics
  • Schizosaccharomyces pombe Proteins* / metabolism
  • Ubiquitination / genetics

Substances

  • Cell Cycle Proteins
  • Heterochromatin
  • Histones
  • Schizosaccharomyces pombe Proteins
  • Histone-Lysine N-Methyltransferase
  • clr4 protein, S pombe
  • Lysine