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Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1

Cell. 2011 Sep 2;146(5):772-84. doi: 10.1016/j.cell.2011.07.033. Epub 2011 Aug 25.

Abstract

T cell differentiation into distinct functional effector and inhibitory subsets is regulated, in part, by the cytokine environment present at the time of antigen recognition. Here, we show that hypoxia-inducible factor 1 (HIF-1), a key metabolic sensor, regulates the balance between regulatory T cell (T(reg)) and T(H)17 differentiation. HIF-1 enhances T(H)17 development through direct transcriptional activation of RORγt and via tertiary complex formation with RORγt and p300 recruitment to the IL-17 promoter, thereby regulating T(H)17 signature genes. Concurrently, HIF-1 attenuates T(reg) development by binding Foxp3 and targeting it for proteasomal degradation. Importantly, this regulation occurs under both normoxic and hypoxic conditions. Mice with HIF-1α-deficient T cells are resistant to induction of T(H)17-dependent experimental autoimmune encephalitis associated with diminished T(H)17 and increased T(reg) cells. These findings highlight the importance of metabolic cues in T cell fate determination and suggest that metabolic modulation could ameliorate certain T cell-based immune pathologies.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Encephalomyelitis, Autoimmune, Experimental / metabolism
  • Forkhead Transcription Factors / metabolism
  • Humans
  • Hypoxia-Inducible Factor 1 / metabolism
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Interleukin-17 / genetics
  • Interleukin-17 / immunology
  • Jurkat Cells
  • Mice
  • Molecular Sequence Data
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / genetics
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism
  • STAT3 Transcription Factor / metabolism
  • Sequence Alignment
  • T-Lymphocytes, Regulatory / cytology*
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • Th17 Cells / cytology*
  • Th17 Cells / immunology
  • Th17 Cells / metabolism
  • p300-CBP Transcription Factors / metabolism

Substances

  • Forkhead Transcription Factors
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Interleukin-17
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • STAT3 Transcription Factor
  • p300-CBP Transcription Factors