Characterization of dsRNA-induced pancreatitis model reveals the regulatory role of IFN regulatory factor 2 (Irf2) in trypsinogen5 gene transcription

Proc Natl Acad Sci U S A. 2011 Nov 15;108(46):18766-71. doi: 10.1073/pnas.1116273108. Epub 2011 Oct 31.

Abstract

Mice deficient for interferon regulatory factor (Irf)2 (Irf2(-/-) mice) exhibit immunological abnormalities and cannot survive lymphocytic choriomeningitis virus infection. The pancreas of these animals is highly inflamed, a phenotype replicated by treatment with poly(I:C), a synthetic double-stranded RNA. Trypsinogen5 mRNA was constitutively up-regulated about 1,000-fold in Irf2(-/-) mice compared with controls as assessed by quantitative RT-PCR. Further knockout of IFNα/β receptor 1(Ifnar1) abolished poly(I:C)-induced pancreatitis but had no effect on the constitutive up-regulation of trypsinogen5 gene, indicating crucial type I IFN signaling to elicit the inflammation. Analysis of Ifnar1(-/-) mice confirmed type I IFN-dependent transcriptional activation of dsRNA-sensing pattern recognition receptor genes MDA5, RIG-I, and TLR3, which induced poly(I:C)-dependent cell death in acinar cells in the absence of IRF2. We speculate that Trypsin5, the trypsinogen5 gene product, leaking from dead acinar cells triggers a chain reaction leading to lethal pancreatitis in Irf2(-/-) mice because it is resistant to a major endogenous trypsin inhibitor, Spink3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acinar Cells / metabolism
  • Animals
  • Cathepsin B / metabolism
  • Glycoproteins / metabolism
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Interferon Regulatory Factor-2 / metabolism*
  • Mice
  • Mice, Transgenic
  • Pancreatitis / genetics
  • Pancreatitis / metabolism*
  • Poly I-C / genetics
  • Prostatic Secretory Proteins / metabolism
  • RNA, Double-Stranded / metabolism*
  • Transcription, Genetic*
  • Trypsin Inhibitor, Kazal Pancreatic
  • Trypsin Inhibitors / pharmacology
  • Trypsinogen / genetics*

Substances

  • Glycoproteins
  • Interferon Regulatory Factor-2
  • Prostatic Secretory Proteins
  • RNA, Double-Stranded
  • Spink1 protein, mouse
  • Trypsin Inhibitors
  • Trypsin Inhibitor, Kazal Pancreatic
  • Trypsinogen
  • Cathepsin B
  • Poly I-C