The Transcriptional Regulator Id2 Is Critical for Adipose-Resident Regulatory T Cell Differentiation, Survival, and Function

J Immunol. 2019 Aug 1;203(3):658-664. doi: 10.4049/jimmunol.1900358. Epub 2019 Jun 14.

Abstract

Adipose regulatory T cells (aTregs) have emerged as critical cells for the control of local and systemic inflammation. In this study, we show a distinctive role for the transcriptional regulator Id2 in the differentiation, survival, and function of aTregs in mice. Id2 was highly expressed in aTregs compared with high Id3 expression in lymphoid regulatory T cells (Tregs). Treg-specific deletion of Id2 resulted in a substantial decrease in aTregs, whereas Tregs in the spleen and lymph nodes were unaffected. Additionally, loss of Id2 resulted in decreased expression of aTreg-associated markers, including ST2, CCR2, KLRG1, and GATA3. Gene expression analysis revealed that Id2 expression was essential for the survival of aTregs, and loss of Id2 increased cell death in aTregs due to increased Fas expression. Id2-mediated aTreg depletion resulted in increased systemic inflammation, increased inflammatory macrophages and CD8+ effector T cells, and loss of glucose tolerance under standard diet conditions. Thus, we reveal an unexpected and novel function for Id2 in mediating differentiation, survival, and function of aTregs that when lost result in increased metabolic perturbation.

Publication types

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

MeSH terms

  • Adipose Tissue / cytology*
  • Animals
  • CD4 Lymphocyte Count
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Death / genetics
  • Cell Differentiation / genetics
  • Cell Survival / genetics
  • GATA3 Transcription Factor / metabolism
  • Inflammation / immunology
  • Inhibitor of Differentiation Protein 2 / genetics*
  • Inhibitor of Differentiation Protein 2 / metabolism*
  • Inhibitor of Differentiation Proteins / metabolism
  • Interleukin-1 Receptor-Like 1 Protein / metabolism
  • Lectins, C-Type / metabolism
  • Macrophages / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Receptors, CCR2 / metabolism
  • Receptors, Immunologic / metabolism
  • T-Lymphocytes, Regulatory / cytology*
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism*
  • fas Receptor / metabolism

Substances

  • Ccr2 protein, mouse
  • Fas protein, mouse
  • GATA3 Transcription Factor
  • Gata3 protein, mouse
  • Idb2 protein, mouse
  • Il1rl1 protein, mouse
  • Inhibitor of Differentiation Protein 2
  • Inhibitor of Differentiation Proteins
  • Interleukin-1 Receptor-Like 1 Protein
  • Klrg1 protein, mouse
  • Lectins, C-Type
  • Receptors, CCR2
  • Receptors, Immunologic
  • fas Receptor
  • Idb3 protein, mouse