Toll-like receptor 3 signaling induces chronic pancreatitis through the Fas/Fas ligand-mediated cytotoxicity

Tohoku J Exp Med. 2009 Mar;217(3):175-84. doi: 10.1620/tjem.217.175.

Abstract

Innate immunity plays important roles in host defense against pathogens, but may also contribute to the development of autoimmune diseases under certain conditions. Toll-like receptors (TLRs) recognize various pathogens and induce innate immunity. We herein present a mouse model for chronic pancreatitis, which was induced by TLR3 signaling that generated the Fas/Fas ligand (FasL)-mediated cytotoxicity. An analogue of viral double-stranded RNA, polyinosinic:polycytidylic acid (poly I:C), which is recognized by TLR3, was injected into autoimmune-prone strains: MRL/Mp mice (MRL/+), MRL/Mp mice with a deficit of Fas (MRL/lpr) and MRL/Mp mice with a deficit of functional FasL (MRL/gld). The pancreatitis in MRL/+ mice was initiated by the destruction of pancreatic ductules, and its severity was significantly higher than that in MRL/lpr mice or MRL/gld mice. Using a pancreatic duct epithelial cell line MRL/S-1 newly established from the MRL/gld mouse that lacks FasL, we showed that treatment with poly I:C significantly induced the expression of Fas on the cultured cells. MRL/S-1 cells were destructed when co-cultured with splenocytes bearing intact FasL prepared from MRL/+ or MRL/lpr mice, but the magnitude of cytotoxicity was smaller with splenocytes of MRL/gld mice. Likewise, synthetic FasL protein showed cytotoxicity on MRL/S-1 cells. Furthermore, MRL/S-1 cells expressed higher levels of chemokines after the treatment with poly I:C, suggesting that the poly I:C-mediated induction of chemokines may be responsible for recruitment of lymphoid cells to the pancreatic periductular regions. These findings indicate that TLR3 signaling generates the Fas/FasL-mediated cytotoxicity, thereby leading to the development of chronic pancreatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Chemokines / metabolism
  • Cytotoxicity Tests, Immunologic
  • Cytotoxicity, Immunologic / immunology*
  • Epithelial Cells
  • Fas Ligand Protein / metabolism*
  • Gene Expression Regulation / drug effects
  • Immunity, Innate*
  • Immunohistochemistry
  • Mice
  • Mice, Mutant Strains
  • Microarray Analysis
  • Pancreatitis, Chronic / etiology*
  • Pancreatitis, Chronic / immunology
  • Poly I-C / metabolism
  • Poly I-C / pharmacology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / immunology*
  • Toll-Like Receptor 3 / metabolism*

Substances

  • Chemokines
  • Fas Ligand Protein
  • TLR3 protein, human
  • Toll-Like Receptor 3
  • Poly I-C