Higher activation of TLR9 in plasmacytoid dendritic cells by microbial DNA compared with self-DNA based on CpG-specific recognition of phosphodiester DNA

J Leukoc Biol. 2009 Sep;86(3):663-70. doi: 10.1189/jlb.0509314. Epub 2009 Jul 20.

Abstract

TLR9 detects DNA in endolysosomal compartments of human B cells and PDC. Recently, the concept of the CpG motif specificity of TLR9-mediated detection, specifically of natural phosphodiester DNA, has been challenged. Unlike in human B cells, CpG specificity of natural phosphodiester DNA recognition in human PDC has not been analyzed in the literature. Here, we found that the induction of IFN-alpha and TNF-alpha in human PDC by phosphodiester ODNs containing one or two CG dinucleotides was reduced to a lower level when the CG dinucleotides were methylated and was abolished if the CGs were switched to GCs. Consistent with a high frequency of unmethylated CG dinucleotides, bacterial DNA induced high levels of IFN-alpha in PDC; IFN-alpha was reduced but not abolished upon methylation of bacterial DNA. Mammalian DNA containing low numbers of CG dinucleotides, which are frequently methylated, induced IFN-alpha in PDC consistently but on a much lower level than bacterial DNA. For activation of PDC, phosphodiester ODNs and genomic DNA strictly required complexation with cationic molecules such as the keratinocyte-derived antimicrobial peptide LL37 or a scrambled derivative. In conclusion, we demonstrate that self-DNA complexed to cationic molecules activate PDC and thus, indeed, may function as DAMPs; nevertheless, the preference of PDC for CpG containing DNA provides the basis for the discrimination of microbial from self-DNA even if DNA is presented in the condensed form of a complex.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antimicrobial Cationic Peptides / immunology*
  • Cathelicidins
  • Cell Line
  • Cells, Cultured
  • CpG Islands / genetics
  • CpG Islands / immunology
  • DNA / genetics
  • DNA / immunology
  • DNA Methylation
  • DNA, Bacterial / genetics
  • DNA, Bacterial / immunology*
  • DNA, Bacterial / isolation & purification
  • Dendritic Cells / immunology*
  • Dinucleoside Phosphates / immunology*
  • Humans
  • Kidney / cytology
  • Leukocytes, Mononuclear / immunology
  • Lymphocyte Activation / immunology
  • Phosphorothioate Oligonucleotides / immunology*
  • Toll-Like Receptor 9 / immunology*

Substances

  • Antimicrobial Cationic Peptides
  • Cathelicidins
  • DNA, Bacterial
  • Dinucleoside Phosphates
  • Phosphorothioate Oligonucleotides
  • Toll-Like Receptor 9
  • cytidylyl-3'-5'-guanosine
  • DNA