IL-1beta, IFN-gamma and TNF-alpha increase vulnerability of pancreatic beta cells to autoimmune destruction

J Autoimmun. 2003 Jun;20(4):303-12. doi: 10.1016/s0896-8411(03)00039-8.

Abstract

In the pathogenesis of type-1 diabetes insulin-producing beta-cells are destroyed by cellular autoimmune processes. The locality of beta-cell destruction is the inflamed pancreatic islet. During insulitis cytokines released from islet-infiltrating mononuclear cells affect beta-cells at several levels. We investigated whether cytokine-induced beta-cell destruction is associated with changes in the expression of the surface receptors intercellular adhesion molecule (ICAM)-1 and Fas. Islets from diabetes-prone and congenic diabetes-resistant BB rats were exposed to interleukin (IL)-1beta alone or in combination with interferon (IFN)-gamma plus tumour necrosis factor (TNF)-alpha. Cytokines decreased islet insulin content, suppressed glucose stimulated insulin secretion and generated enhanced amounts of nitric oxide and DNA-strand breaks. While no membrane alterations of IL-1beta treated islets cells were detectable, the cytokine combination caused damage of cell membranes. Independent of diabetes susceptibility IL-1beta treated islet beta-cells expressed a significantly increased amount of ICAM-1 on their surfaces which was not further increased by IFN-gamma+TNF-alpha. However, IL-1beta induced Fas expression was significantly enhanced only on beta-cells from diabetes-prone BB rats. From these results we suggest that IL-1beta mediates the major stimulus for ICAM-1 induction which is possibly a necessary but not sufficient step in the process of beta-cell destruction. Obviously, the additional enhancement of Fas expression on the surface of beta-cells is important for destruction. The combined action of all three cytokines induced the expression of Fas on the beta-cell surface independent of diabetes susceptibility, indicating that such a strong stimulus in vitro may induce processes different from the precise mechanisms of beta-cell destruction in vivo.

MeSH terms

  • Animals
  • Animals, Congenic
  • Autoimmunity / drug effects*
  • DNA Damage
  • Diabetes Mellitus, Type 1 / etiology
  • Diabetes Mellitus, Type 1 / immunology
  • In Vitro Techniques
  • Insulin / metabolism
  • Insulin Secretion
  • Intercellular Adhesion Molecule-1 / metabolism
  • Interferon-gamma / pharmacology*
  • Interleukin-1 / pharmacology*
  • Islets of Langerhans / drug effects*
  • Islets of Langerhans / immunology*
  • Nitrites / metabolism
  • Rats
  • Rats, Inbred BB
  • Recombinant Proteins / pharmacology
  • Tumor Necrosis Factor-alpha / pharmacology*
  • fas Receptor / metabolism

Substances

  • Insulin
  • Interleukin-1
  • Nitrites
  • Recombinant Proteins
  • Tumor Necrosis Factor-alpha
  • fas Receptor
  • Intercellular Adhesion Molecule-1
  • Interferon-gamma