Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D

Mol Cell Biol. 2002 Nov;22(22):7842-52. doi: 10.1128/MCB.22.22.7842-7852.2002.

Abstract

The FoxO forkhead transcription factors FoxO4 (AFX), FoxO3a (FKHR.L1), and FoxO1a (FKHR) represent important physiological targets of phosphatidylinositol-3 kinase (PI3K)/protein kinase B (PKB) signaling. Overexpression or conditional activation of FoxO factors is able to antagonize many responses to constitutive PI3K/PKB activation including its effect on cellular proliferation. It was previously shown that the FoxO-induced cell cycle arrest is partially mediated by enhanced transcription and protein expression of the cyclin-dependent kinase inhibitor p27(kip1) (R. H. Medema, G. J. Kops, J. L. Bos, and B. M. Burgering, Nature 404:782-787, 2000). Here we have identified a p27(kip1)-independent mechanism that plays an important role in the antiproliferative effect of FoxO factors. Forced expression or conditional activation of FoxO factors leads to reduced protein expression of the D-type cyclins D1 and D2 and is associated with an impaired capacity of CDK4 to phosphorylate and inactivate the S-phase repressor pRb. Downregulation of D-type cyclins involves a transcriptional repression mechanism and does not require p27(kip1) function. Ectopic expression of cyclin D1 can partially overcome FoxO factor-induced cell cycle arrest, demonstrating that downregulation of D-type cyclins represents a physiologically relevant mechanism of FoxO-induced cell cycle inhibition.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Animals
  • Carcinoma
  • Cell Cycle / physiology*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cells, Cultured
  • Colonic Neoplasms
  • Cyclin D
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase Inhibitor p27
  • Cyclin-Dependent Kinases / antagonists & inhibitors
  • Cyclin-Dependent Kinases / metabolism
  • Cyclins / genetics
  • Cyclins / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Down-Regulation / physiology
  • Enzyme Inhibitors / metabolism
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Forkhead Transcription Factors
  • Genes, Reporter
  • Humans
  • Hydroxytestosterones / pharmacology
  • Mice
  • Mice, Transgenic
  • Phosphatidylinositol 3-Kinases / metabolism
  • Promoter Regions, Genetic
  • Protein Binding
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Retinoblastoma Protein / genetics
  • Retinoblastoma Protein / metabolism
  • Retroviridae / genetics
  • Retroviridae / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcription, Genetic
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism

Substances

  • Cdkn1b protein, mouse
  • Cell Cycle Proteins
  • Cyclin D
  • Cyclins
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • FOXO4 protein, human
  • Forkhead Transcription Factors
  • Hydroxytestosterones
  • Proto-Oncogene Proteins
  • Repressor Proteins
  • Retinoblastoma Protein
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Cyclin-Dependent Kinase Inhibitor p27
  • 4,17 beta-dihydroxy-4-androstene-3-one
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • CDK4 protein, human
  • Cdk4 protein, mouse
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinases