HIRA, the human homologue of yeast Hir1p and Hir2p, is a novel cyclin-cdk2 substrate whose expression blocks S-phase progression

Mol Cell Biol. 2001 Mar;21(5):1854-65. doi: 10.1128/MCB.21.5.1854-1865.2001.

Abstract

Substrates of cyclin-cdk2 kinases contain two distinct primary sequence motifs: a cyclin-binding RXL motif and one or more phosphoacceptor sites (consensus S/TPXK/R or S/TP). To identify novel cyclin-cdk2 substrates, we searched the database for proteins containing both of these motifs. One such protein is human HIRA, the homologue of two cell cycle-regulated repressors of histone gene expression in Saccharomyces cerevisiae, Hir1p and Hir2p. Here we demonstrate that human HIRA is an in vivo substrate of a cyclin-cdk2 kinase. First, HIRA bound to and was phosphorylated by cyclin A- and E-cdk2 in vitro in an RXL-dependent manner. Second, HIRA was phosphorylated in vivo on two consensus cyclin-cdk2 phosphoacceptor sites and at least one of these, threonine 555, was phosphorylated by cyclin A-cdk2 in vitro. Third, phosphorylation of HIRA in vivo was blocked by cyclin-cdk2 inhibitor p21(cip1). Fourth, HIRA became phosphorylated on threonine 555 in S phase when cyclin-cdk2 kinases are active. Fifth, HIRA was localized preferentially to the nucleus, where active cyclin A- and E-cdk2 are located. Finally, ectopic expression of HIRA in cells caused arrest in S phase and this is consistent with the notion that it is a cyclin-cdk2 substrate that has a role in control of the cell cycle.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Blotting, Western
  • CDC2-CDC28 Kinases*
  • Cell Cycle
  • Cell Cycle Proteins*
  • Cell Line
  • Cell Nucleus / metabolism
  • Cell Separation
  • Cyclin A / metabolism*
  • Cyclin E / metabolism*
  • Cyclin-Dependent Kinase 2
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclin-Dependent Kinases / metabolism*
  • Cyclins / metabolism
  • Flow Cytometry
  • Glutathione Transferase / metabolism
  • Histone Chaperones
  • Humans
  • Mass Spectrometry
  • Microscopy, Fluorescence
  • Molecular Sequence Data
  • Nuclear Proteins / chemistry*
  • Nuclear Proteins / metabolism
  • Nuclear Proteins / physiology*
  • Peptides / chemistry
  • Phosphorylation
  • Plasmids / metabolism
  • Precipitin Tests
  • Protein Binding
  • Protein Serine-Threonine Kinases / metabolism*
  • Recombinant Fusion Proteins / metabolism
  • Repressor Proteins / chemistry
  • S Phase
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins*
  • Sequence Homology, Amino Acid
  • Threonine / chemistry
  • Transcription Factors / chemistry*
  • Transcription Factors / metabolism
  • Transcription Factors / physiology*
  • Transfection

Substances

  • CDKN1A protein, human
  • Cell Cycle Proteins
  • Cyclin A
  • Cyclin E
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins
  • HIR1 protein, S cerevisiae
  • HIR2 protein, S cerevisiae
  • HIRA protein, human
  • Histone Chaperones
  • Nuclear Proteins
  • Peptides
  • Recombinant Fusion Proteins
  • Repressor Proteins
  • Saccharomyces cerevisiae Proteins
  • Transcription Factors
  • Threonine
  • Glutathione Transferase
  • Protein Serine-Threonine Kinases
  • CDC2-CDC28 Kinases
  • CDK2 protein, human
  • Cyclin-Dependent Kinase 2
  • Cyclin-Dependent Kinases