Microbial lipopeptides induce the production of IL-17 in Th cells

J Immunol. 2000 Dec 1;165(11):6107-15. doi: 10.4049/jimmunol.165.11.6107.

Abstract

Naive Th cells can be directed in vitro to develop into Th1 or Th2 cells by IL-12 or IL-4, respectively. In vivo, chronic immune reactions lead to polarized Th cytokine patterns. We found earlier that Borrelia burgdorferi, the spirochaete that causes Lyme disease, induces Th1 development in alpha beta TCR-transgenic Th cells. Here, we used TCR-transgenic Th cells and oligonucleotide arrays to analyze the differences between Th1 cells induced by IL-12 vs those induced by B. burgdorferi. Transgenic Th cells primed with peptide in the presence of B. burgdorferi expressed several mRNAs, including the mRNA encoding IL-17, at significantly higher levels than Th cells primed with peptide and IL-12. Cytometric single-cell analysis of Th cell cytokine production revealed that IL-17 cannot be categorized as either Th1 or Th2 cytokine. Instead, almost all IL-17-producing Th cells simultaneously produced TNF-alpha and most IL-17(+) Th cells also produced GM-CSF. This pattern was also observed in humans. Th cells from synovial fluid of patients with Lyme arthritis coexpressed IL-17 and TNF-alpha upon polyclonal stimulation. The induction of IL-17 production in Th cells is not restricted to B. burgdorferi. Priming of TCR-transgenic Th cells in the presence of mycobacterial lysates also induced IL-17/TNF-alpha coproduction. The physiological stimulus for IL-17 production was hitherto unknown. We show here for the first time that microbial stimuli induce the expression of IL-17 together with TNF-alpha in both murine and human T cells. Chronic IL-17 expression induced by microbes could be an important mediator of infection-induced immunopathology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthritis, Reactive / immunology
  • Bacterial Proteins / chemical synthesis
  • Bacterial Proteins / immunology*
  • Borrelia burgdorferi Group / immunology*
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / microbiology
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Cells, Cultured
  • Chemokines / biosynthesis
  • Chemokines / genetics
  • Cytokines / biosynthesis
  • Cytokines / genetics
  • Granulocyte-Macrophage Colony-Stimulating Factor / biosynthesis
  • Humans
  • Immunophenotyping
  • Interleukin-12 / physiology
  • Interleukin-17 / biosynthesis*
  • Interleukin-18 / physiology
  • Interleukin-6 / physiology
  • Lipoproteins / chemical synthesis
  • Lipoproteins / immunology*
  • Lyme Disease / immunology
  • Lymphocyte Activation / genetics
  • Mice
  • Mice, Inbred BALB C
  • Mice, Transgenic
  • Peptides / chemical synthesis
  • Peptides / immunology*
  • RNA, Messenger / biosynthesis
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • Synovial Fluid / cytology
  • Synovial Fluid / immunology
  • Synovial Fluid / metabolism
  • Synovial Fluid / microbiology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • T-Lymphocyte Subsets / microbiology
  • T-Lymphocytes, Helper-Inducer / cytology
  • T-Lymphocytes, Helper-Inducer / immunology*
  • T-Lymphocytes, Helper-Inducer / metabolism*
  • T-Lymphocytes, Helper-Inducer / microbiology
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Th2 Cells / immunology
  • Th2 Cells / metabolism
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Up-Regulation / genetics
  • Up-Regulation / immunology

Substances

  • Bacterial Proteins
  • Chemokines
  • Cytokines
  • Interleukin-17
  • Interleukin-18
  • Interleukin-6
  • Lipoproteins
  • Peptides
  • RNA, Messenger
  • Receptors, Antigen, T-Cell, alpha-beta
  • Tumor Necrosis Factor-alpha
  • Interleukin-12
  • Granulocyte-Macrophage Colony-Stimulating Factor