CD8+ T cell responses following replication-defective adenovirus serotype 5 immunization are dependent on CD11c+ dendritic cells but show redundancy in their requirement of TLR and nucleotide-binding oligomerization domain-like receptor signaling

J Immunol. 2010 Aug 1;185(3):1513-21. doi: 10.4049/jimmunol.1000338. Epub 2010 Jul 7.

Abstract

Replication-defective adenovirus serotype 5 (rAd5) is the most potent recombinant vector for eliciting CD8 T cell responses in humans. In this study, the innate mechanisms that influence T cell responses following rAd5 immunization were assessed in mice. Using rAd5 expressing enhanced GFP (eGFP-rAd5), we show that rAd5 transfects CD11c(+) dendritic cells (DCs) in draining lymph nodes in vivo following s.c. or i.m. immunization. Among distinct DC subsets, eGFP expression was highest in CD11c(+)CD8(-)B220(-) with a lower frequency detected in CD11c(+)CD8(+)B220(-) and CD11c(+)B220(+) plasmacytoid DCs. CD11c(+) DCs but not CD11c(-) cells from mice immunized with rAd5 encoding the SIINFEKL peptide induced proliferation of naive OT-I CD8 T cells. Furthermore, CD11c(+)CD8(+)B220(-) was the most potent DC subset for eliciting naive OT-I CD8 T cell proliferation. Of note, mice with pre-existing immunity to rAd5 had a substantial decrease in eGFP expression in DCs, which was associated with approximately 2-fold decrease in Th1 and complete inhibition of CD8 responses. Thus, pre-existing rAd5 immunity has a greater influence on CD8 compared with CD4 T cell responses. In terms of how innate cytokines and signaling pathways influenced T cell immunity following rAd5 immunization, we show that the magnitude and quality of CD8 T cell responses are partially dependent on MyD88 but independent of IL-12, type I IFN, apoptosis-associated speck-like protein, nucleotide-binding oligomerization domain-like receptor protein 3, and IL-1. Taken together, these data demonstrate a critical role for CD11c(+) DCs for CD8 responses but striking redundancy for innate cytokines and signaling by TLR and nucleotide-binding oligomerization domain-like receptor pathways.

MeSH terms

  • Adenoviruses, Human / genetics
  • Adenoviruses, Human / immunology*
  • Animals
  • Antigen Presentation / immunology
  • CD11c Antigen / biosynthesis*
  • CD11c Antigen / genetics
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / virology
  • Defective Viruses / immunology*
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Dendritic Cells / virology
  • Immunity, Innate
  • Immunophenotyping
  • Interferon Type I / physiology
  • Interleukin-12 / physiology
  • Intracellular Signaling Peptides and Proteins / physiology*
  • Lymph Nodes / immunology
  • Lymph Nodes / pathology
  • Lymph Nodes / virology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Oligodeoxyribonucleotides / metabolism*
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Toll-Like Receptors / genetics
  • Toll-Like Receptors / physiology*
  • Viral Vaccines / administration & dosage
  • Viral Vaccines / genetics
  • Viral Vaccines / immunology
  • Virion / immunology
  • Virion / pathogenicity

Substances

  • CD11c Antigen
  • Interferon Type I
  • Intracellular Signaling Peptides and Proteins
  • NLRC5 protein, mouse
  • Oligodeoxyribonucleotides
  • Toll-Like Receptors
  • Viral Vaccines
  • Interleukin-12