NOD2/CARD15 mediates induction of the antimicrobial peptide human beta-defensin-2

J Biol Chem. 2006 Jan 27;281(4):2005-11. doi: 10.1074/jbc.M511044200. Epub 2005 Nov 30.

Abstract

Production of inducible antimicrobial peptides offers a first and rapid defense response of epithelial cells against invading microbes. Human beta-defensin-2 (hBD-2) is an antimicrobial peptide induced in various epithelia upon extracellular as well as intracellular bacterial challenge. Nucleotide-binding oligomerization domain protein 2 (NOD2/CARD15) is a cytosolic protein involved in intracellular recognition of microbes by sensing peptidoglycan fragments (e.g. muramyl dipeptide). We used luciferase as a reporter gene for a 2.3-kb hBD-2 promoter to test the hypothesis that NOD2 mediates the induction of hBD-2. Activation of NOD2 in NOD2-overexpressing human embryonic kidney 293 cells through its ligand muramyl dipeptide (MDP) induced hBD-2 expression. In contrast, overexpression of NOD2 containing the 3020insC frame-shift mutation, the most frequent NOD2 variant associated with Crohn disease, resulted in defective induction of hBD-2 through MDP. Luciferase gene reporter analyses and site-directed mutagenesis experiments demonstrated that functional binding sites for NF-kappaB and AP-1 in the hBD-2 promoter are required for NOD2-mediated induction of hBD-2 through MDP. Moreover, the NF-kappaB inhibitor Helenalin as well as a super-repressor form of the NF-kappaB inhibitor IkappaB strongly inhibited NOD2-mediated hBD-2 promoter activation. Expression of NOD2 was detected in primary keratinocytes, and stimulation of these cells with MDP induced hBD-2 peptide release. In contrast, small interference RNA-mediated down-regulation of NOD2 expression in primary keratinocytes resulted in a defective induction of hBD-2 upon MDP treatment. Together, these data suggest that NOD2 serves as an intracellular pattern recognition receptor to enhance host defense by inducing the production of antimicrobial peptides such as hBD-2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Infective Agents / pharmacology*
  • Antimicrobial Cationic Peptides / chemistry
  • Antimicrobial Cationic Peptides / pharmacology
  • Binding Sites
  • Biotinylation
  • Cell Line
  • Crohn Disease / metabolism
  • DNA, Complementary / metabolism
  • Down-Regulation
  • Enzyme-Linked Immunosorbent Assay
  • Epithelial Cells / metabolism
  • Frameshift Mutation
  • Genes, Reporter
  • Humans
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Keratinocytes / metabolism
  • Ligands
  • Luciferases / metabolism
  • Mutagenesis, Site-Directed
  • Mutation
  • NF-kappa B / metabolism
  • Nod2 Signaling Adaptor Protein
  • Peptides / chemistry
  • Peptidoglycan / chemistry
  • Plasmids / metabolism
  • Promoter Regions, Genetic
  • RNA / metabolism
  • RNA, Small Interfering / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sesquiterpenes / pharmacology
  • Sesquiterpenes, Guaiane
  • Transcription Factor AP-1 / metabolism
  • Transfection
  • beta-Defensins / pharmacology*

Substances

  • Anti-Infective Agents
  • Antimicrobial Cationic Peptides
  • DEFB4A protein, human
  • DNA, Complementary
  • Intracellular Signaling Peptides and Proteins
  • Ligands
  • NF-kappa B
  • NOD2 protein, human
  • Nod2 Signaling Adaptor Protein
  • Peptides
  • Peptidoglycan
  • RNA, Small Interfering
  • Sesquiterpenes
  • Sesquiterpenes, Guaiane
  • Transcription Factor AP-1
  • beta-Defensins
  • helenalin
  • RNA
  • Luciferases