Ubp-M serine 552 phosphorylation by cyclin-dependent kinase 1 regulates cell cycle progression

Cell Cycle. 2013 Oct 1;12(19):3219-27. doi: 10.4161/cc.26278. Epub 2013 Sep 4.

Abstract

In eukaryotic cells, genomic DNA is organized into a chromatin structure, which not only serves as the template for DNA-based nuclear processes, but also as a platform integrating intracellular and extracellular signals. Although much effort has been spent to characterize chromatin modifying/remodeling activities, little is known about cell signaling pathways targeting these chromatin modulators. Here, we report that cyclin-dependent kinase 1 (CDK1) phosphorylates the histone H2A deubiquitinase Ubp-M at serine 552 (S552P), and, importantly, this phosphorylation is required for cell cycle progression. Mass spectrometry analysis confirmed Ubp-M is phosphorylated at serine 552, and in vitro and in vivo assays demonstrated that CDK1/cyclin B kinase is responsible for Ubp-M S552P. Interestingly, Ubp-M S552P is not required for Ubp-M tetramer formation, deubiquitination activity, substrate specificity, or regulation of gene expression. However, Ubp-M S552P is required for cell proliferation and cell cycle G 2/M phase progression. Ubp-M S552P reduces Ubp-M interaction with nuclear export protein CRM1 and facilitates Ubp-M nuclear localization. Therefore, these studies confirm that Ubp-M is phosphorylated at S552 and identify CDK1 as the enzyme responsible for the phosphorylation. Importantly, this study specifically links Ubp-M S552P to cell cycle G 2/M phase progression.

Keywords: CDK1; CRM1; G2/M phase; H2A deubiquitination; Ubp-M; cell cycle; gene expression; phosphorylation.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • CDC2 Protein Kinase / metabolism*
  • Cell Cycle Checkpoints
  • Cell Division
  • Cell Proliferation
  • Exportin 1 Protein
  • G2 Phase
  • HeLa Cells
  • Humans
  • Karyopherins / metabolism
  • Phosphorylation
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Serine / metabolism
  • Ubiquitin Thiolesterase / chemistry
  • Ubiquitin Thiolesterase / genetics
  • Ubiquitin Thiolesterase / metabolism*

Substances

  • Karyopherins
  • Receptors, Cytoplasmic and Nuclear
  • Recombinant Fusion Proteins
  • USP16 protein, human
  • Serine
  • CDC2 Protein Kinase
  • Ubiquitin Thiolesterase