The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2

J Immunol. 2002 May 15;168(10):5024-31. doi: 10.4049/jimmunol.168.10.5024.

Abstract

The cytokine IL-2 plays a very important role in the proliferation and survival of activated T cells. These effects of IL-2 are dependent on signaling through the phosphatidylinositol 3-kinase (PI3K) pathway. We and others have shown that PI3K, through activation of protein kinase B/Akt, inhibits transcriptional activation by a number of forkhead transcription factors (FoxO1, FoxO3, and FoxO4). In this study we have investigated the role of these forkhead transcription factors in the IL-2-induced T cell proliferation and survival. We show that IL-2 regulates phosphorylation of FoxO3 in a PI3K-dependent fashion. Phosphorylation and inactivation of FoxO3 appears to play an important role in IL-2-mediated T cell survival, because mere activation of FoxO3 is sufficient to trigger apoptosis in T cells. Indeed, active FoxO3 can induce expression of IL-2-regulated genes, such as the cdk inhibitor p27(Kip1) and the proapoptotic Bcl-2 family member Bim. Furthermore, we show that IL-2 triggers a rapid, PI3K-dependent, phosphorylation of FoxO1a in primary T cells. Thus, we propose that inactivation of FoxO transcription factors by IL-2 plays a critical role in T cell proliferation and survival.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Apoptosis / immunology
  • Apoptosis Regulatory Proteins
  • Bcl-2-Like Protein 11
  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism*
  • Cell Cycle Proteins / genetics*
  • Cell Cycle Proteins / metabolism*
  • Cell Line
  • Cell Survival / genetics
  • Cell Survival / immunology
  • Cells, Cultured
  • Cyclin-Dependent Kinase Inhibitor p27
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology*
  • Forkhead Box Protein O1
  • Forkhead Transcription Factors
  • Gene Silencing / immunology
  • Humans
  • Interleukin-2 / physiology*
  • Lymphocyte Activation / genetics
  • Membrane Proteins*
  • Mice
  • Phosphatidylinositol 3-Kinases / physiology
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / physiology
  • Proto-Oncogene Proteins c-akt
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / enzymology
  • T-Lymphocytes / immunology
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / metabolism
  • Transcription Factors / physiology*
  • Transcription, Genetic / immunology*
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism*

Substances

  • Apoptosis Regulatory Proteins
  • BCL2L11 protein, human
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • Carrier Proteins
  • Cdkn1b protein, mouse
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • FOXO1 protein, human
  • FOXO4 protein, human
  • Forkhead Box Protein O1
  • Forkhead Transcription Factors
  • Interleukin-2
  • Membrane Proteins
  • Proto-Oncogene Proteins
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Cyclin-Dependent Kinase Inhibitor p27
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt