Cytokine-mediated induction of anti-apoptotic genes that are linked to nuclear factor kappa-B (NF-kappaB) signalling in human islets and in a mouse beta cell line

Diabetologia. 2009 Jun;52(6):1092-101. doi: 10.1007/s00125-009-1331-x. Epub 2009 Apr 3.

Abstract

Aims/hypothesis: The destruction of pancreatic beta cells leading to type 1 diabetes in humans is thought to occur mainly through apoptosis and necrosis induced by activated macrophages and T cells, and in which secreted cytokines play a significant role. The transcription factor nuclear factor kappa-B (NF-kappaB) plays an important role in mediating the apoptotic action of cytokines in beta cells. We therefore sought to determine the changes in expression of genes modulated by NF-kappaB in human islets exposed to a combination of IL1beta, TNF-alpha and IFN-gamma.

Methods: Microarray and gene set enrichment analysis were performed to investigate the global response of gene expression and pathways modulated in cultured human islets exposed to cytokines. Validation of a panel of NF-kappaB-regulated genes was performed by quantitative RT-PCR. The mechanism of induction of BIRC3 by cytokines was examined by transient transfection of BIRC3 promoter constructs linked to a luciferase gene in MIN6 cells, a mouse beta cell line.

Results: Enrichment of several metabolic and signalling pathways was observed in cytokine-treated human islets. In addition to the upregulation of known pro-apoptotic genes, a number of anti-apoptotic genes including BIRC3, BCL2A1, TNFAIP3, CFLAR and TRAF1 were induced by cytokines through NF-kappaB. Significant synergy between the cytokines was observed in NF-kappaB-mediated induction of the promoter of BIRC3 in MIN6 cells.

Conclusions/interpretation: These findings suggest that, via NF-kappaB activation, cytokines induce a concurrent anti-apoptotic pathway that may be critical for preserving islet integrity and viability during the progression of insulitis in type 1 diabetes.

Publication types

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

MeSH terms

  • Animals
  • Baculoviral IAP Repeat-Containing 3 Protein
  • CASP8 and FADD-Like Apoptosis Regulating Protein / genetics
  • Cell Line
  • Cells, Cultured
  • Cytokines / pharmacology*
  • DNA-Binding Proteins / genetics
  • Humans
  • Inhibitor of Apoptosis Proteins / genetics
  • Insulin-Secreting Cells / drug effects*
  • Insulin-Secreting Cells / metabolism*
  • Interferon-gamma / pharmacology
  • Interleukin-1beta / pharmacology
  • Islets of Langerhans / drug effects*
  • Islets of Langerhans / metabolism*
  • Mice
  • Minor Histocompatibility Antigens
  • NF-kappa B / metabolism*
  • Oligonucleotide Array Sequence Analysis
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / drug effects
  • TNF Receptor-Associated Factor 1 / genetics
  • Tumor Necrosis Factor-alpha / pharmacology
  • Ubiquitin-Protein Ligases

Substances

  • BCL2-related protein A1
  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • CFLAR protein, human
  • Cytokines
  • DNA-Binding Proteins
  • Inhibitor of Apoptosis Proteins
  • Interleukin-1beta
  • Minor Histocompatibility Antigens
  • NF-kappa B
  • Proto-Oncogene Proteins c-bcl-2
  • TNF Receptor-Associated Factor 1
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • BIRC3 protein, human
  • Baculoviral IAP Repeat-Containing 3 Protein
  • Birc3 protein, mouse
  • Ubiquitin-Protein Ligases