Induction of inflammatory cytokines and interferon responses by double-stranded and single-stranded siRNAs is sequence-dependent and requires endosomal localization

J Mol Biol. 2005 May 20;348(5):1079-90. doi: 10.1016/j.jmb.2005.03.013. Epub 2005 Mar 22.

Abstract

The potential induction of inflammatory cytokines and interferon responses by small-interfering RNAs (siRNAs) represents a major obstacle for their use as inhibitors of gene expression. Therapeutic applications of siRNAs will require a better understanding of the mechanisms that trigger such unwanted effects, especially in freshly isolated human cells. Surprisingly, the induction of tumor necrosis factor (TNF-alpha) and interleukin-6 (IL-6) in adherent peripheral blood mononuclear cells (PBMC) was not restricted to double-stranded siRNAs, because induction was also obtained with single-stranded siRNAs (sense or antisense strands). The immunostimulatory effects were sequence-dependent, since only certain sequences are prone to induce inflammatory responses while others are not. The induction of TNF-alpha, IL-6 and interferon alpha (IFN-alpha) was chloroquine-sensitive and dependent more likely on endosomal Toll-like receptor signaling in particular TLR8. Indeed, no significant immunostimulatory effects were detected when either double or single-stranded siRNAs were delivered directly to cytoplasm via electroporation. Both RNA types activated a NF-kappaB promoter-driven luciferase gene in transiently transfected human adherent PBMC. Moreover, culture of immature dendritic cells with either double or single-stranded siRNAs stimulated interleukin-12 production and induced the expression of CD83, an activation marker. Interestingly, several double-stranded siRNAs did not induce TNF-alpha, IL-6 and IFN-alpha production, however, their single-stranded sense or antisense did. Taken together, the present data indicate for the first time that the induction of inflammatory cytokines and IFN-alpha responses by either double-stranded or single-stranded siRNAs in adherent PBMC is sequence-dependent and requires endosomal intracellular signaling. The finding that endosomal localization of self-RNAs (sense strands) can trigger Toll-like receptor signaling in adherent human PBMC is intriguing because it indicates that endosomal self-RNAs can display a molecular pattern capable for activating innate immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Cytokines / biosynthesis*
  • Cytokines / genetics
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Endosomes / chemistry
  • Endosomes / physiology*
  • Gene Expression / drug effects
  • Gene Expression / genetics
  • Humans
  • Interferon-alpha / genetics
  • Interferon-alpha / metabolism
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology
  • NF-kappa B / genetics
  • Promoter Regions, Genetic / drug effects
  • Promoter Regions, Genetic / genetics
  • RNA, Double-Stranded / analysis
  • RNA, Double-Stranded / genetics
  • RNA, Double-Stranded / pharmacology*
  • RNA, Small Interfering / analysis
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / pharmacology*
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / physiology
  • Toll-Like Receptor 8
  • Toll-Like Receptors
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Cytokines
  • Interferon-alpha
  • Interleukin-6
  • Membrane Glycoproteins
  • NF-kappa B
  • RNA, Double-Stranded
  • RNA, Small Interfering
  • Receptors, Cell Surface
  • TLR8 protein, human
  • Toll-Like Receptor 8
  • Toll-Like Receptors
  • Tumor Necrosis Factor-alpha