Inflammation conditions mature dendritic cells to retain the capacity to present new antigens but with altered cytokine secretion function

J Immunol. 2014 Oct 15;193(8):3851-9. doi: 10.4049/jimmunol.1303215. Epub 2014 Sep 8.

Abstract

Dendritic cells (DCs) are directly activated by pathogen-associated molecular patterns (PAMPs) and undergo maturation. Mature DCs express high levels of MHC class II molecules ("signal 1"), upregulate T cell costimulatory receptors ("signal 2"), and secrete "signal 3" cytokines (e.g., IL-12). Mature DCs efficiently present Ags linked to the activating PAMP and prime naive T cells. However, mature DCs downregulate MHC II synthesis, which prevents them from presenting newly encountered Ags. DCs can also be indirectly activated by inflammatory mediators released during infection (e.g., IFN). Indirectly activated DCs mature but do not present pathogen Ags (as they have not encountered the pathogen) and do not provide signal 3. Therefore, although they are probably generated in large numbers upon infection or vaccination, indirectly activated DCs are considered to play little or no role in T cell immunity. In this article, we show that indirectly activated DCs retain their capacity to present Ags encountered after maturation in vivo. They can also respond to PAMPs, but the previous encounter of inflammatory signals alters their cytokine (signal 3) secretion pattern. This implies that the immune response elicited by a PAMP is more complex than predicted by the examination of the immunogenic features of directly activated DCs, and that underlying inflammatory processes can skew the immune response against pathogens. Our observations have important implications for the design of vaccines and for the understanding of the interactions between simultaneous infections, or of infection in the context of ongoing sterile inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigen Presentation / immunology*
  • CD8 Antigens / biosynthesis
  • Cell Differentiation / immunology
  • Cytokines / immunology*
  • Dendritic Cells / immunology*
  • Histocompatibility Antigens Class II / biosynthesis
  • Inflammation / immunology*
  • Inflammation Mediators / immunology
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred CBA
  • Mice, Knockout
  • Ovalbumin / immunology
  • T-Lymphocytes / immunology
  • Toll-Like Receptor 9 / genetics
  • Toll-Like Receptor 9 / immunology
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Ubiquitin-Protein Ligases / biosynthesis

Substances

  • CD8 Antigens
  • Cytokines
  • Histocompatibility Antigens Class II
  • Inflammation Mediators
  • Tlr9 protein, mouse
  • Toll-Like Receptor 9
  • Tumor Necrosis Factor-alpha
  • Ovalbumin
  • MARCH1 protein, mouse
  • Ubiquitin-Protein Ligases