IL-1 beta breaks tolerance through expansion of CD25+ effector T cells

J Immunol. 2006 Jun 15;176(12):7278-87. doi: 10.4049/jimmunol.176.12.7278.

Abstract

IL-1 is a key proinflammatory driver of several autoimmune diseases including juvenile inflammatory arthritis, diseases with mutations in the NALP/cryopyrin complex and Crohn's disease, and is genetically or clinically associated with many others. IL-1 is a pleiotropic proinflammatory cytokine; however the mechanisms by which increased IL-1 signaling promotes autoreactive T cell activity are not clear. Here we show that autoimmune-prone NOD and IL-1 receptor antagonist-deficient C57BL/6 mice both produce high levels of IL-1, which drives autoreactive effector cell expansion. IL-1beta drives proliferation and cytokine production by CD4(+)CD25(+)FoxP3(-) effector/memory T cells, attenuates CD4(+)CD25(+)FoxP3(+) regulatory T cell function, and allows escape of CD4(+)CD25(-) autoreactive effectors from suppression. Thus, inflammation or constitutive overexpression of IL-1beta in a genetically predisposed host can promote autoreactive effector T cell expansion and function, which attenuates the ability of regulatory T cells to maintain tolerance to self.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Division / genetics
  • Cell Division / immunology
  • Cell Proliferation*
  • Cells, Cultured
  • Clonal Anergy / genetics
  • Clonal Anergy / immunology
  • Diabetes Mellitus, Type 1 / genetics
  • Diabetes Mellitus, Type 1 / immunology
  • Forkhead Transcription Factors / biosynthesis
  • Genetic Predisposition to Disease
  • Immunologic Memory / genetics
  • Interferon-gamma / biosynthesis
  • Interleukin-1 / biosynthesis
  • Interleukin-1 / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred NOD
  • Mice, Knockout
  • Mice, SCID
  • Receptors, Interleukin-2 / biosynthesis*
  • Receptors, Interleukin-2 / deficiency
  • Receptors, Interleukin-2 / genetics
  • Self Tolerance / genetics
  • Self Tolerance / immunology*
  • T-Lymphocytes, Regulatory / cytology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism*

Substances

  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Interleukin-1
  • Receptors, Interleukin-2
  • Interferon-gamma