Home LiteratureArticle Details
PMID: 15218108 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells.

Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, Moretta L, Moretta A

Abstract

Toll-like receptors (TLRs) are pattern-recognition receptors responsible for triggering cells of innate immunity. In this study we investigated the expression and function of TLRs 3 and 9 in human natural killer (NK) cells. In the presence of IL-12, freshly isolated NK cells responded to double-stranded RNA or unmethylated CpG DNA and expressed CD69 and CD25 activation markers. Because both markers were expressed by virtually all NK cells, this would suggest that most of them can be triggered by TLRs. Remarkably, NK cell stimulation also resulted in the induction of their functional program as revealed by IFN-gamma and tumor necrosis factor-alpha release and by up-regulation of cytolytic activity against tumor cells. IL-8 could efficiently substitute IL-12 in supporting NK cell responses to TLR-mediated stimulation. Importantly, freshly isolated NK cells acquired the ability to lyse immature dendritic cells after stimulation with double-stranded RNA and IL-12. However, responses to these stimuli were not restricted to fresh NK cells, because significant responses were also detected in polyclonal NK cells cultured in the presence of exogenous IL-2 for several weeks. The analysis of NK cell clones revealed some degree of heterogeneity in the ability to respond to TLR stimulation also among NK clones derived from a single donor. These data suggest that stimuli acting on TLR not only activate immature dendritic cells to release IL-12 but also render NK cells capable of receiving triggering signals from pathogen-associated molecules, thus exerting a regulatory control on the early steps of innate immune responses against infectious agents.

MeSH Terms
Cells, Cultured Cytokines/biosynthesis Cytotoxicity, Immunologic/drug effects Dendritic Cells/immunology Humans Interleukin-2/pharmacology Killer Cells, Natural/immunology Membrane Glycoproteins/physiology Oligodeoxyribonucleotides/pharmacology Poly I-C/pharmacology RNA, Double-Stranded/pharmacology Receptors, Cell Surface/physiology Toll-Like Receptors
Chemicals
CPG-oligonucleotide Cytokines Interleukin-2 Membrane Glycoproteins Oligodeoxyribonucleotides RNA, Double-Stranded Receptors, Cell Surface Toll-Like Receptors Poly I-C
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Sivori Simona
Dipartimento di Medicina Sperimentale, Università di Genova, Via Leon Battista Alberti 2, 16132 Genoa, Italy.
Falco Michela
Della Chiesa Mariella
Carlomagno Simona
Vitale Massimo
Moretta Lorenzo
Moretta Alessandro
References (34)
34 references, click to expand
  1. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition.
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9237-42 PMID: 11470918
  2. Toll-like receptors: critical proteins linking innate and acquired immunity.
    Nat Immunol. 2001 Aug;2(8):675-80 PMID: 11477402
  3. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens.
    J Exp Med. 2001 Sep 17;194(6):863-9 PMID: 11561001
  4. Cutting edge: Role of Toll-like receptor 9 in CpG DNA-induced activation of human cells.
    J Immunol. 2001 Oct 1;167(7):3555-8 PMID: 11564765
  5. Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12.
    Eur J Immunol. 2001 Oct;31(10):3026-37 PMID: 11592079
  6. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3.
    Nature. 2001 Oct 18;413(6857):732-8 PMID: 11607032
  7. Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells.
    Eur J Immunol. 2001 Nov;31(11):3388-93 PMID: 11745357
  8. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway.
    Nat Immunol. 2002 Feb;3(2):196-200 PMID: 11812998
  9. Reciprocal activating interaction between natural killer cells and dendritic cells.
    J Exp Med. 2002 Feb 4;195(3):327-33 PMID: 11828007
  10. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells.
    J Exp Med. 2002 Feb 4;195(3):335-41 PMID: 11828008
  11. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells.
    J Exp Med. 2002 Feb 4;195(3):343-51 PMID: 11828009
  12. CpG motifs in bacterial DNA and their immune effects.
    Annu Rev Immunol. 2002;20:709-60 PMID: 11861616
  13. Stimulation of toll-like receptor 4 expression in human mononuclear phagocytes by interferon-gamma: a molecular basis for priming and synergism with bacterial lipopolysaccharide.
    Blood. 2002 May 1;99(9):3427-31 PMID: 11964313
  14. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides.
    J Immunol. 2002 May 1;168(9):4531-7 PMID: 11970999
  15. Natural killer cells and dendritic cells: rendezvous in abused tissues.
    Nat Rev Immunol. 2002 Dec;2(12):957-64 PMID: 12461568
  16. Mammalian Toll-like receptors.
    Curr Opin Immunol. 2003 Feb;15(1):5-11 PMID: 12495726
  17. The interaction between NK cells and dendritic cells in bacterial infections results in rapid induction of NK cell activation and in the lysis of uninfected dendritic cells.
    Eur J Immunol. 2003 Feb;33(2):306-13 PMID: 12548561
  18. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells.
    J Immunol. 2003 May 1;170(9):4465-74 PMID: 12707322
  19. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors.
    Eur J Immunol. 2003 Jun;33(6):1657-66 PMID: 12778484
  20. The toll-like receptor repertoire of human B lymphocytes: inducible and selective expression of TLR9 and TLR10 in normal and transformed cells.
    Blood. 2003 Aug 1;102(3):956-63 PMID: 12689944
  21. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic.
    J Immunol. 2004 Feb 1;172(3):1455-62 PMID: 14734722
  22. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene.
    Science. 1998 Dec 11;282(5396):2085-8 PMID: 9851930
  23. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells.
    Eur J Immunol. 1999 May;29(5):1656-66 PMID: 10359120
  24. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens.
    Nature. 1999 Oct 21;401(6755):811-5 PMID: 10548109
  25. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells.
    J Exp Med. 1999 Nov 15;190(10):1505-16 PMID: 10562324
  26. Delineation of a CpG phosphorothioate oligodeoxynucleotide for activating primate immune responses in vitro and in vivo.
    J Immunol. 2000 Feb 1;164(3):1617-24 PMID: 10640783
  27. Toll-like receptors: a growing family of immune receptors that are differentially expressed and regulated by different leukocytes.
    J Leukoc Biol. 2000 Apr;67(4):450-6 PMID: 10770275
  28. Innate immunity.
    N Engl J Med. 2000 Aug 3;343(5):338-44 PMID: 10922424
  29. Toll-like receptors in the induction of the innate immune response.
    Nature. 2000 Aug 17;406(6797):782-7 PMID: 10963608
  30. A Toll-like receptor recognizes bacterial DNA.
    Nature. 2000 Dec 7;408(6813):740-5 PMID: 11130078
  31. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5.
    Nature. 2001 Apr 26;410(6832):1099-103 PMID: 11323673
  32. Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire.
    J Immunol. 2001 Jun 1;166(11):6477-82 PMID: 11359797
  33. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite.
    J Immunol. 2001 Jul 1;167(1):416-23 PMID: 11418678
  34. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity.
    Cell. 2001 Aug 10;106(3):259-62 PMID: 11509173
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2004-07-06
Epub
2004-00-24
Pages
10116-21
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC454174
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com