Attenuated expression of A20 markedly increases the efficacy of double-stranded RNA-activated dendritic cells as an anti-cancer vaccine

J Immunol. 2009 Jan 15;182(2):860-70. doi: 10.4049/jimmunol.182.2.860.

Abstract

A20 is a zinc finger protein with ubiquitin-modifying activity. A20 has been described as negatively regulating signaling induced by the TNF receptor and TLR family in a number of cell types, including mouse bone marrow-derived dendritic cells (DCs). However, the expression and effect of A20 in activated human monocyte-derived DCs have not been previously evaluated. We report that DCs activated with the TLR3 ligand poly(I:C) up-regulate A20. Down-regulating A20 demonstrated its role in the functional activation of DCs. A20 down-regulated DCs showed higher activation of the transcription factors NF-kappaB and activator protein-1, which resulted in increased and sustained production of IL-6, IL-10, and IL-12p70. We additionally silenced the immunosuppressive cytokine IL-10 and demonstrated that IL-10 inhibits T cell proliferation. We further demonstrated that A20 down-regulated DCs skew naive CD4+ T cells toward IFN-gamma producing Th1 cells, a process which is dependent on IL-12p70 and which is unaffected by IL-10. Furthermore, A20 and/or IL-10 down-regulated DCs had an enhanced capacity to prime Melan-A/MART-1 specific CD8+ T cells. Finally, we demonstrated that potent T cell stimulatory DCs are generated by the simultaneous delivery of poly(I:C12U), A20, or A20/IL-10 small interfering RNA and Ag-encoding mRNA, introducing a one step approach to improve DC-based vaccines. Together these findings demonstrate that A20 negatively regulates NF-kappaB and activator protein-1 in DCs and that down-regulation of A20 results in DCs with enhanced T cell stimulatory capacity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / biosynthesis
  • Adjuvants, Immunologic / genetics*
  • Adjuvants, Immunologic / physiology
  • CD4-Positive T-Lymphocytes / immunology
  • Cancer Vaccines / genetics*
  • Cancer Vaccines / immunology*
  • Cells, Cultured
  • Coculture Techniques
  • DNA-Binding Proteins
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Dendritic Cells / transplantation*
  • Down-Regulation / genetics
  • Down-Regulation / immunology*
  • Humans
  • Interleukin-10 / biosynthesis
  • Interleukin-12 / biosynthesis
  • Interleukin-6 / biosynthesis
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / genetics*
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Monocytes / immunology
  • Monocytes / metabolism
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / biosynthesis
  • Nuclear Proteins / antagonists & inhibitors
  • Nuclear Proteins / biosynthesis
  • Nuclear Proteins / genetics*
  • RNA Interference / immunology
  • RNA, Double-Stranded / physiology*
  • RNA, Small Interfering / physiology
  • Transcription Factor AP-1 / antagonists & inhibitors
  • Transcription Factor AP-1 / biosynthesis
  • Tumor Necrosis Factor alpha-Induced Protein 3
  • Up-Regulation / genetics
  • Up-Regulation / immunology*

Substances

  • Adjuvants, Immunologic
  • Cancer Vaccines
  • DNA-Binding Proteins
  • Interleukin-6
  • Intracellular Signaling Peptides and Proteins
  • NF-kappa B
  • Nuclear Proteins
  • RNA, Double-Stranded
  • RNA, Small Interfering
  • Transcription Factor AP-1
  • Interleukin-10
  • Interleukin-12
  • TNFAIP3 protein, human
  • Tumor Necrosis Factor alpha-Induced Protein 3