Peripheral and islet interleukin-17 pathway activation characterizes human autoimmune diabetes and promotes cytokine-mediated β-cell death

Diabetes. 2011 Aug;60(8):2112-9. doi: 10.2337/db10-1643. Epub 2011 Jun 9.

Abstract

Objective: CD4 T-cells secreting interleukin (IL)-17 are implicated in several human autoimmune diseases, but their role in type 1 diabetes has not been defined. To address the relevance of such cells, we examined IL-17 secretion in response to β-cell autoantigens, IL-17A gene expression in islets, and the potential functional consequences of IL-17 release for β-cells.

Research design and methods: Peripheral blood CD4 T-cell responses to β-cell autoantigens (proinsulin, insulinoma-associated protein, and GAD65 peptides) were measured by IL-17 enzyme-linked immunospot assay in patients with new-onset type 1 diabetes (n = 50). mRNA expression of IL-17A and IFNG pathway genes was studied by qRT-PCR using islets obtained from subjects who died 5 days and 10 years after diagnosis of disease, respectively, and from matched control subjects. IL-17 effects on the function of human islets, rat β-cells, and the rat insulinoma cell line INS-1E were examined.

Results: A total of 27 patients (54%) showed IL-17 reactivity to one or more β-cell peptides versus 3 of 30 (10%) control subjects (P = 0.0001). In a single case examined close to diagnosis, islet expression of IL17A, RORC, and IL22 was detected. It is noteworthy that we show that IL-17 mediates significant and reproducible enhancement of IL-1β/interferon (IFN)-γ-induced and tumor necrosis factor (TNF)-α/IFN-γ-induced apoptosis in human islets, rat β-cells, and INS-1E cells, in association with significant upregulation of β-cell IL17RA expression via activation of the transcription factors STAT1 and nuclear factor (NF)-κB.

Conclusions: Circulating IL-17(+) β-cell-specific autoreactive CD4 T-cells are a feature of type 1 diabetes diagnosis. We disclose a novel pathway to β-cell death involving IL-17 and STAT1 and NF-κB, rendering this cytokine a novel disease biomarker and potential therapeutic target.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Apoptosis / drug effects
  • CD4-Positive T-Lymphocytes / immunology*
  • Cell Line, Tumor
  • Cytokines / physiology
  • Diabetes Mellitus, Type 1 / immunology*
  • Female
  • Humans
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / pathology*
  • Insulinoma / metabolism
  • Interleukin-17 / biosynthesis
  • Interleukin-17 / physiology*
  • Interleukin-22
  • Interleukins / biosynthesis
  • Male
  • NF-kappa B / physiology
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / biosynthesis
  • Pancreatic Neoplasms / metabolism
  • Rats
  • Rats, Wistar
  • STAT1 Transcription Factor / physiology
  • Tumor Necrosis Factor-alpha / physiology

Substances

  • Cytokines
  • IL17A protein, human
  • Interleukin-17
  • Interleukins
  • NF-kappa B
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • RORC protein, human
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Tumor Necrosis Factor-alpha