IFN-beta inhibits human Th17 cell differentiation

J Immunol. 2009 Oct 15;183(8):5418-27. doi: 10.4049/jimmunol.0803227. Epub 2009 Sep 25.

Abstract

IFN-beta-1a has been used over the past 15 years as a primary therapy for relapsing-remitting multiple sclerosis (MS). However, the immunomodulatory mechanisms that provide a therapeutic effect against this CNS inflammatory disease are not yet completely elucidated. The effect of IFN-beta-1a on Th17 cells, which play a critical role in the development of the autoimmune response, has not been extensively studied in humans. We have investigated the effect of IFN-beta-1a on dendritic cells (DCs) and naive CD4(+)CD45RA(+) T cells derived from untreated MS patients and healthy controls in the context of Th17 cell differentiation. We report that IFN-beta-1a treatment down-regulated the expression of IL-1beta and IL-23p19 in DCs, whereas it induced the gene expression of IL-12p35 and IL-27p28. We propose that IFN-beta-1a-mediated up-regulation of the suppressor of cytokine signaling 3 expression, induced via STAT3 phosphorylation, mediates IL-1beta and IL-23 down-regulation, while IFN-beta-1a-induced STAT1 phosphorylation induces IL-27p28 expression. CD4(+)CD45RA(+) naive T cells cocultured with supernatants from IFN-beta-1a-treated DCs exhibited decreased gene expression of the Th17 cell markers retinoic acid-related orphan nuclear hormone receptor c (RORc), IL-17A, and IL-23R. A direct IFN-beta-1a treatment of CD45RA(+) T cells cultured in Th17-polarizing conditions also down-regulated RORc, IL-17A, and IL-23R, but up-regulated IL-10 gene expression. Studies of the mechanisms involved in the Th17 cell differentiation suggest that IFN-beta-1a inhibits IL-17 and induces IL-10 secretion via activated STAT1 and STAT3, respectively. IFN-beta's suppression of Th17 cell differentiation may represent its most relevant mechanism of selective suppression of the autoimmune response in MS.

Publication types

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

MeSH terms

  • CD4-Positive T-Lymphocytes / drug effects
  • CD4-Positive T-Lymphocytes / immunology
  • Cell Differentiation / drug effects*
  • Cell Differentiation / immunology
  • Cells, Cultured
  • Dendritic Cells / drug effects*
  • Dendritic Cells / immunology
  • Down-Regulation / drug effects
  • Down-Regulation / immunology
  • Humans
  • Interferon beta-1a
  • Interferon-beta / pharmacology*
  • Interleukin-10 / agonists
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism
  • Interleukin-12 Subunit p35 / agonists
  • Interleukin-12 Subunit p35 / immunology
  • Interleukin-12 Subunit p35 / metabolism
  • Interleukin-17 / immunology*
  • Interleukin-1beta / antagonists & inhibitors
  • Interleukin-1beta / immunology
  • Interleukin-1beta / metabolism
  • Interleukin-23 Subunit p19 / antagonists & inhibitors
  • Interleukin-23 Subunit p19 / immunology
  • Interleukin-23 Subunit p19 / metabolism
  • Multiple Sclerosis / immunology*
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • Phosphorylation / drug effects
  • Phosphorylation / immunology
  • Receptors, CCR6 / antagonists & inhibitors
  • Receptors, CCR6 / immunology
  • Receptors, CCR6 / metabolism
  • Receptors, Interleukin / antagonists & inhibitors
  • Receptors, Interleukin / immunology
  • Receptors, Interleukin / metabolism
  • Receptors, Retinoic Acid / immunology
  • Receptors, Retinoic Acid / metabolism
  • Receptors, Thyroid Hormone / immunology
  • Receptors, Thyroid Hormone / metabolism
  • STAT1 Transcription Factor / drug effects
  • STAT1 Transcription Factor / immunology
  • STAT1 Transcription Factor / metabolism
  • STAT3 Transcription Factor / drug effects
  • STAT3 Transcription Factor / immunology
  • STAT3 Transcription Factor / metabolism
  • T-Lymphocytes, Helper-Inducer / drug effects*
  • T-Lymphocytes, Helper-Inducer / immunology
  • Up-Regulation / drug effects
  • Up-Regulation / immunology

Substances

  • CCR6 protein, human
  • IL23R protein, human
  • Interleukin-12 Subunit p35
  • Interleukin-17
  • Interleukin-1beta
  • Interleukin-23 Subunit p19
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • RORC protein, human
  • Receptors, CCR6
  • Receptors, Interleukin
  • Receptors, Retinoic Acid
  • Receptors, Thyroid Hormone
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Interleukin-10
  • Interferon-beta
  • Interferon beta-1a