Cyclin E-CDK2 protein phosphorylates plant homeodomain finger protein 8 (PHF8) and regulates its function in the cell cycle

J Biol Chem. 2015 Feb 13;290(7):4075-85. doi: 10.1074/jbc.M114.602532. Epub 2014 Dec 29.

Abstract

Cyclin E-CDK2 is a key regulator in G1/S transition. Previously, we identified a number of CDK2-interacting proteins, including PHF8 (plant homeodomain finger protein 8). In this report, we confirmed that PHF8 is a novel cyclin E-CDK2 substrate. By taking the approach of mass spectrometry, we identified that PHF8 Ser-844 is phosphorylated by cyclin E-CDK2. Immunoblotting analysis indicated that WT PHF8 demethylates histone H3K9me2 more efficiently than the cyclin E-CDK2 phosphorylation-deficient PHF8-S844A mutant. Furthermore, flow cytometry analysis showed that WT PHF8 promotes S phase progression more robustly than PHF8-S844A. Real-time PCR results demonstrated that PHF8 increases transcription of cyclin E, E2F3, and E2F7 to significantly higher levels compared with PHF8-S844A. Further analysis by ChIP assay indicated that PHF8 binds to the cyclin E promoter stronger than PHF8-S844A and reduces the H3K9me2 level at the cyclin E promoter more efficiently than PHF8-S844A. In addition, we found that cyclin E-CDK2-mediated phosphorylation of PHF8 Ser-844 promotes PHF8-dependent rRNA transcription in luciferase reporter assays and real-time PCR. Taken together, these results indicate that cyclin E-CDK2 phosphorylates PHF8 to stimulate its demethylase activity to promote rRNA transcription and cell cycle progression.

Keywords: Cell Cycle; Cell Signaling; Cyclin; Cyclin E-CDK2, PHF8, Phosphorylation, rRNA Transcription; Cyclin-dependent Kinase (CDK); Phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blotting, Western
  • Cell Proliferation
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • Cyclin E / genetics
  • Cyclin E / metabolism*
  • Cyclin-Dependent Kinase 2 / genetics
  • Cyclin-Dependent Kinase 2 / metabolism*
  • DNA Methylation
  • DNA, Ribosomal / genetics
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Gene Expression Regulation*
  • HeLa Cells
  • Histone Demethylases / antagonists & inhibitors
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism*
  • Histones / metabolism*
  • Humans
  • Immunoprecipitation
  • Oncogene Proteins / genetics
  • Oncogene Proteins / metabolism*
  • Phosphorylation
  • RNA, Messenger / genetics
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • S Phase / physiology*
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • CCNE1 protein, human
  • Cyclin E
  • DNA, Ribosomal
  • Histones
  • Oncogene Proteins
  • RNA, Messenger
  • RNA, Small Interfering
  • Transcription Factors
  • Histone Demethylases
  • PHF8 protein, human
  • CDK2 protein, human
  • Cyclin-Dependent Kinase 2