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Published in: BMC Immunology 1/2018

Open Access 01-12-2018 | Research article

Pathogen recognition by NK cells amplifies the pro-inflammatory cytokine production of monocyte-derived DC via IFN-γ

Authors: Tammy Oth, Thomas H. P. M. Habets, Wilfred T. V. Germeraad, Marijke I. Zonneveld, Gerard M. J. Bos, Joris Vanderlocht

Published in: BMC Immunology | Issue 1/2018

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Abstract

Background

Besides their prominent role in the elimination of infected or malignantly transformed cells, natural killer (NK) cells serve as modulators of adaptive immune responses. Enhancing bidirectional crosstalk between NK cells and dendritic cells (DC) is considered a promising tool to potentiate cancer vaccines. We investigated to what extent direct sensing of viral and bacterial motifs by NK cells contributes to the response of inflammatory DC against the same pathogenic stimulus.

Results

We demonstrated that sensing of bacterial and viral PAMPs by NK cells contributes to DC cytokine production via NK cell-derived soluble factors. This enhancement of DC cytokine production was dependent on the pattern recognition receptor (PRR) agonist but also on the cytokine environment in which NK cells recognized the pathogen, indicating the importance of accessory cell activation for this mechanism. We showed in blocking experiments that NK cell-mediated amplification of DC cytokine secretion is dependent on NK cell-derived IFN-γ irrespective of the PRR that is sensed by the NK cell.

Conclusions

These findings illustrate the importance of bidirectional interaction between different PRR-expressing immune cells, which can have implications on the selection of adjuvants for vaccination strategies.
Appendix
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Literature
1.
go back to reference Oldham RK, Herberman RB. Evaluation of cell-mediated cytotoxic reactivity against tumor associated antigens with 125I-iododeoxyuridine labeled target cells. J Immunol. 1973;111(6):862–71.PubMed Oldham RK, Herberman RB. Evaluation of cell-mediated cytotoxic reactivity against tumor associated antigens with 125I-iododeoxyuridine labeled target cells. J Immunol. 1973;111(6):862–71.PubMed
2.
go back to reference Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331(6013):44–9.CrossRefPubMedPubMedCentral Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331(6013):44–9.CrossRefPubMedPubMedCentral
3.
go back to reference Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–10.CrossRefPubMed Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–10.CrossRefPubMed
5.
go back to reference Agaugue S, Marcenaro E, Ferranti B, Moretta L, Moretta A. Human natural killer cells exposed to IL-2, IL-12, IL-18, or IL-4 differently modulate priming of naive T cells by monocyte-derived dendritic cells. Blood. 2008;112(5):1776–83.CrossRefPubMed Agaugue S, Marcenaro E, Ferranti B, Moretta L, Moretta A. Human natural killer cells exposed to IL-2, IL-12, IL-18, or IL-4 differently modulate priming of naive T cells by monocyte-derived dendritic cells. Blood. 2008;112(5):1776–83.CrossRefPubMed
6.
go back to reference Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol. 1999;17:189–220.CrossRefPubMed Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol. 1999;17:189–220.CrossRefPubMed
7.
go back to reference Welsh RM, Brubaker JO, Vargas-Cortes M, O'Donnell CL. Natural killer (NK) cell response to virus infections in mice with severe combined immunodeficiency. The stimulation of NK cells and the NK cell-dependent control of virus infections occur independently of T and B cell function. J Exp Med. 1991;173(5):1053–63.CrossRefPubMed Welsh RM, Brubaker JO, Vargas-Cortes M, O'Donnell CL. Natural killer (NK) cell response to virus infections in mice with severe combined immunodeficiency. The stimulation of NK cells and the NK cell-dependent control of virus infections occur independently of T and B cell function. J Exp Med. 1991;173(5):1053–63.CrossRefPubMed
8.
go back to reference Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med. 1989;320(26):1731–5.CrossRefPubMed Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med. 1989;320(26):1731–5.CrossRefPubMed
9.
go back to reference Orange JS. Human natural killer cell deficiencies and susceptibility to infection. Microbes Infection / Institut Pasteur. 2002;4(15):1545–58.CrossRef Orange JS. Human natural killer cell deficiencies and susceptibility to infection. Microbes Infection / Institut Pasteur. 2002;4(15):1545–58.CrossRef
10.
go back to reference Orange JS. Human natural killer cell deficiencies. Curr Opin Allergy Clin Immunol. 2006;6(6):399–409.CrossRefPubMed Orange JS. Human natural killer cell deficiencies. Curr Opin Allergy Clin Immunol. 2006;6(6):399–409.CrossRefPubMed
11.
go back to reference Orange JS, Ballas ZK. Natural killer cells in human health and disease. Clin Immunol. 2006;118(1):1–10.CrossRefPubMed Orange JS, Ballas ZK. Natural killer cells in human health and disease. Clin Immunol. 2006;118(1):1–10.CrossRefPubMed
12.
go back to reference Byrne P, McGuirk P, Todryk S, Mills KH. Depletion of NK cells results in disseminating lethal infection with Bordetella pertussis associated with a reduction of antigen-specific Th1 and enhancement of Th2, but not Tr1 cells. Eur J Immunol. 2004;34(9):2579–88.CrossRefPubMed Byrne P, McGuirk P, Todryk S, Mills KH. Depletion of NK cells results in disseminating lethal infection with Bordetella pertussis associated with a reduction of antigen-specific Th1 and enhancement of Th2, but not Tr1 cells. Eur J Immunol. 2004;34(9):2579–88.CrossRefPubMed
13.
go back to reference Sporri R, Joller N, Albers U, Hilbi H, Oxenius A. MyD88-dependent IFN-gamma production by NK cells is key for control of legionella pneumophila infection. J Immunol. 2006;176(10):6162–71.CrossRefPubMed Sporri R, Joller N, Albers U, Hilbi H, Oxenius A. MyD88-dependent IFN-gamma production by NK cells is key for control of legionella pneumophila infection. J Immunol. 2006;176(10):6162–71.CrossRefPubMed
14.
go back to reference Small CL, McCormick S, Gill N, Kugathasan K, Santosuosso M, Donaldson N, Heinrichs DE, Ashkar A, Xing Z. NK cells play a critical protective role in host defense against acute extracellular Staphylococcus Aureus bacterial infection in the lung. J Immunol. 2008;180(8):5558–68.CrossRefPubMed Small CL, McCormick S, Gill N, Kugathasan K, Santosuosso M, Donaldson N, Heinrichs DE, Ashkar A, Xing Z. NK cells play a critical protective role in host defense against acute extracellular Staphylococcus Aureus bacterial infection in the lung. J Immunol. 2008;180(8):5558–68.CrossRefPubMed
15.
go back to reference Trinchieri G, Sher A. Cooperation of toll-like receptor signals in innate immune defence. Nat Rev Immunol. 2007;7(3):179–90.CrossRefPubMed Trinchieri G, Sher A. Cooperation of toll-like receptor signals in innate immune defence. Nat Rev Immunol. 2007;7(3):179–90.CrossRefPubMed
17.
go back to reference Lee HK, Iwasaki A. Innate control of adaptive immunity: dendritic cells and beyond. Semin Immunol. 2007;19(1):48–55.CrossRefPubMed Lee HK, Iwasaki A. Innate control of adaptive immunity: dendritic cells and beyond. Semin Immunol. 2007;19(1):48–55.CrossRefPubMed
18.
go back to reference Borg C, Jalil A, Laderach D, Maruyama K, Wakasugi H, Charrier S, Ryffel B, Cambi A, Figdor C, Vainchenker W, et al. NK cell activation by dendritic cells (DCs) requires the formation of a synapse leading to IL-12 polarization in DCs. Blood. 2004;104(10):3267–75.CrossRefPubMed Borg C, Jalil A, Laderach D, Maruyama K, Wakasugi H, Charrier S, Ryffel B, Cambi A, Figdor C, Vainchenker W, et al. NK cell activation by dendritic cells (DCs) requires the formation of a synapse leading to IL-12 polarization in DCs. Blood. 2004;104(10):3267–75.CrossRefPubMed
19.
go back to reference Fernandez NC, Flament C, Crepineau F, Angevin E, Vivier E, Zitvogel L. Dendritic cells (DC) promote natural killer (NK) cell functions: dynamics of the human DC/NK cell cross talk. Eur Cytokine Netw. 2002;13(1):17–27.PubMed Fernandez NC, Flament C, Crepineau F, Angevin E, Vivier E, Zitvogel L. Dendritic cells (DC) promote natural killer (NK) cell functions: dynamics of the human DC/NK cell cross talk. Eur Cytokine Netw. 2002;13(1):17–27.PubMed
20.
go back to reference Van Elssen CH, Vanderlocht J, Frings PW, Senden-Gijsbers BL, Schnijderberg MC, van Gelder M, Meek B, Libon C, Ferlazzo G, Germeraad WT, et al. Klebsiella Pneumoniae-triggered DC recruit human NK cells in a CCR5-dependent manner leading to increased CCL19-responsiveness and activation of NK cells. Eur J Immunol. 2010;40(11):3138–49.CrossRefPubMed Van Elssen CH, Vanderlocht J, Frings PW, Senden-Gijsbers BL, Schnijderberg MC, van Gelder M, Meek B, Libon C, Ferlazzo G, Germeraad WT, et al. Klebsiella Pneumoniae-triggered DC recruit human NK cells in a CCR5-dependent manner leading to increased CCL19-responsiveness and activation of NK cells. Eur J Immunol. 2010;40(11):3138–49.CrossRefPubMed
21.
go back to reference Mailliard RB, Alber SM, Shen H, Watkins SC, Kirkwood JM, Herberman RB, Kalinski P. IL-18-induced CD83+CCR7+ NK helper cells. J Exp Med. 2005;202(7):941–53.CrossRefPubMedPubMedCentral Mailliard RB, Alber SM, Shen H, Watkins SC, Kirkwood JM, Herberman RB, Kalinski P. IL-18-induced CD83+CCR7+ NK helper cells. J Exp Med. 2005;202(7):941–53.CrossRefPubMedPubMedCentral
22.
go back to reference Hart OM, Athie-Morales V, O'Connor GM, Gardiner CM. TLR7/8-mediated activation of human NK cells results in accessory cell-dependent IFN-gamma production. J Immunol. 2005;175(3):1636–42.CrossRefPubMed Hart OM, Athie-Morales V, O'Connor GM, Gardiner CM. TLR7/8-mediated activation of human NK cells results in accessory cell-dependent IFN-gamma production. J Immunol. 2005;175(3):1636–42.CrossRefPubMed
23.
go back to reference Marcenaro E, Ferranti B, Falco M, Moretta L, Moretta A. Human NK cells directly recognize Mycobacterium Bovis via TLR2 and acquire the ability to kill monocyte-derived DC. Int Immunol. 2008;20(9):1155–67.CrossRefPubMed Marcenaro E, Ferranti B, Falco M, Moretta L, Moretta A. Human NK cells directly recognize Mycobacterium Bovis via TLR2 and acquire the ability to kill monocyte-derived DC. Int Immunol. 2008;20(9):1155–67.CrossRefPubMed
24.
go back to reference Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, Giese T, Endres S, Hartmann G. 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;168(9):4531–7.CrossRefPubMed Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, Giese T, Endres S, Hartmann G. 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;168(9):4531–7.CrossRefPubMed
25.
go back to reference Gorski KS, Waller EL, Bjornton-Severson J, Hanten JA, Riter CL, Kieper WC, Gorden KB, Miller JS, Vasilakos JP, Tomai MA, et al. Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int Immunol. 2006;18(7):1115–26.CrossRefPubMed Gorski KS, Waller EL, Bjornton-Severson J, Hanten JA, Riter CL, Kieper WC, Gorden KB, Miller JS, Vasilakos JP, Tomai MA, et al. Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int Immunol. 2006;18(7):1115–26.CrossRefPubMed
26.
go back to reference Chalifour A, Jeannin P, Gauchat JF, Blaecke A, Malissard M, N'Guyen T, Thieblemont N, Delneste Y. Direct bacterial protein PAMP recognition by human NK cells involves TLRs and triggers alpha-defensin production. Blood. 2004;104(6):1778–83.CrossRefPubMed Chalifour A, Jeannin P, Gauchat JF, Blaecke A, Malissard M, N'Guyen T, Thieblemont N, Delneste Y. Direct bacterial protein PAMP recognition by human NK cells involves TLRs and triggers alpha-defensin production. Blood. 2004;104(6):1778–83.CrossRefPubMed
27.
go back to reference Athie-Morales V, O'Connor GM, Gardiner CM. Activation of human NK cells by the bacterial pathogen-associated molecular pattern muramyl dipeptide. J Immunol. 2008;180(6):4082–9.CrossRefPubMed Athie-Morales V, O'Connor GM, Gardiner CM. Activation of human NK cells by the bacterial pathogen-associated molecular pattern muramyl dipeptide. J Immunol. 2008;180(6):4082–9.CrossRefPubMed
28.
go back to reference Perrot I, Deauvieau F, Massacrier C, Hughes N, Garrone P, Durand I, Demaria O, Viaud N, Gauthier L, Blery M, et al. TLR3 and rig-like receptor on myeloid dendritic cells and rig-like receptor on human NK cells are both mandatory for production of IFN-gamma in response to double-stranded RNA. J Immunol. 2010;185(4):2080–8.CrossRefPubMedPubMedCentral Perrot I, Deauvieau F, Massacrier C, Hughes N, Garrone P, Durand I, Demaria O, Viaud N, Gauthier L, Blery M, et al. TLR3 and rig-like receptor on myeloid dendritic cells and rig-like receptor on human NK cells are both mandatory for production of IFN-gamma in response to double-stranded RNA. J Immunol. 2010;185(4):2080–8.CrossRefPubMedPubMedCentral
29.
go back to reference Duluc D, Tan F, Scotet M, Blanchard S, Fremaux I, Garo E, Horvat B, Eid P, Delneste Y, Jeannin P. PolyI:C plus IL-2 or IL-12 induce IFN-gamma production by human NK cells via autocrine IFN-beta. Eur J Immunol. 2009;39(10):2877–84.CrossRefPubMed Duluc D, Tan F, Scotet M, Blanchard S, Fremaux I, Garo E, Horvat B, Eid P, Delneste Y, Jeannin P. PolyI:C plus IL-2 or IL-12 induce IFN-gamma production by human NK cells via autocrine IFN-beta. Eur J Immunol. 2009;39(10):2877–84.CrossRefPubMed
30.
go back to reference Girart MV, Fuertes MB, Domaica CI, Rossi LE, Zwirner NW. Engagement of TLR3, TLR7, and NKG2D regulate IFN-gamma secretion but not NKG2D-mediated cytotoxicity by human NK cells stimulated with suboptimal doses of IL-12. J Immunol. 2007;179(6):3472–9.CrossRefPubMed Girart MV, Fuertes MB, Domaica CI, Rossi LE, Zwirner NW. Engagement of TLR3, TLR7, and NKG2D regulate IFN-gamma secretion but not NKG2D-mediated cytotoxicity by human NK cells stimulated with suboptimal doses of IL-12. J Immunol. 2007;179(6):3472–9.CrossRefPubMed
31.
go back to reference Sivori S, Carlomagno S, Moretta L, Moretta A. Comparison of different CpG oligodeoxynucleotide classes for their capability to stimulate human NK cells. Eur J Immunol. 2006;36(4):961–7.CrossRefPubMed Sivori S, Carlomagno S, Moretta L, Moretta A. Comparison of different CpG oligodeoxynucleotide classes for their capability to stimulate human NK cells. Eur J Immunol. 2006;36(4):961–7.CrossRefPubMed
32.
go back to reference Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, Moretta L, Moretta A. CpG and double-stranded RNA trigger human NK cells by toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci U S A. 2004;101(27):10116–21.CrossRefPubMedPubMedCentral Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, Moretta L, Moretta A. CpG and double-stranded RNA trigger human NK cells by toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci U S A. 2004;101(27):10116–21.CrossRefPubMedPubMedCentral
33.
go back to reference Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA, Storkus WJ, Kalinski P. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol. 2003;171(5):2366–73.CrossRefPubMed Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA, Storkus WJ, Kalinski P. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol. 2003;171(5):2366–73.CrossRefPubMed
34.
go back to reference Wong JL, Berk E, Edwards RP, Kalinski P. IL-18-primed helper NK cells collaborate with dendritic cells to promote recruitment of effector CD8+ T cells to the tumor microenvironment. Cancer Res. 2013;73(15):4653–62.CrossRefPubMedPubMedCentral Wong JL, Berk E, Edwards RP, Kalinski P. IL-18-primed helper NK cells collaborate with dendritic cells to promote recruitment of effector CD8+ T cells to the tumor microenvironment. Cancer Res. 2013;73(15):4653–62.CrossRefPubMedPubMedCentral
35.
36.
go back to reference Wong JL, Mailliard RB, Moschos SJ, Edington H, Lotze MT, Kirkwood JM, Kalinski P. Helper activity of natural killer cells during the dendritic cell-mediated induction of melanoma-specific cytotoxic T cells. J Immunother. 2011;34(3):270–8.CrossRefPubMedPubMedCentral Wong JL, Mailliard RB, Moschos SJ, Edington H, Lotze MT, Kirkwood JM, Kalinski P. Helper activity of natural killer cells during the dendritic cell-mediated induction of melanoma-specific cytotoxic T cells. J Immunother. 2011;34(3):270–8.CrossRefPubMedPubMedCentral
37.
go back to reference Oth T, Schnijderberg MC, Senden-Gijsbers BL, Germeraad WT, Bos GM, Vanderlocht J. Monitoring the initiation and kinetics of human dendritic cell-induced polarization of autologous naive CD4+ T cells. PLoS One. 2014;9(8):e103725.CrossRefPubMedPubMedCentral Oth T, Schnijderberg MC, Senden-Gijsbers BL, Germeraad WT, Bos GM, Vanderlocht J. Monitoring the initiation and kinetics of human dendritic cell-induced polarization of autologous naive CD4+ T cells. PLoS One. 2014;9(8):e103725.CrossRefPubMedPubMedCentral
38.
go back to reference De Maria A, Bozzano F, Cantoni C, Moretta L. Revisiting human natural killer cell subset function revealed cytolytic CD56(dim)CD16+ NK cells as rapid producers of abundant IFN-gamma on activation. Proc Natl Acad Sci U S A. 2011;108(2):728–32.CrossRefPubMed De Maria A, Bozzano F, Cantoni C, Moretta L. Revisiting human natural killer cell subset function revealed cytolytic CD56(dim)CD16+ NK cells as rapid producers of abundant IFN-gamma on activation. Proc Natl Acad Sci U S A. 2011;108(2):728–32.CrossRefPubMed
39.
go back to reference Nieto M, Navarro F, Perez-Villar JJ, del Pozo MA, Gonzalez-Amaro R, Mellado M, Frade JM, Martinez AC, Lopez-Botet M, Sanchez-Madrid F. Roles of chemokines and receptor polarization in NK-target cell interactions. J Immunol. 1998;161(7):3330–9.PubMed Nieto M, Navarro F, Perez-Villar JJ, del Pozo MA, Gonzalez-Amaro R, Mellado M, Frade JM, Martinez AC, Lopez-Botet M, Sanchez-Madrid F. Roles of chemokines and receptor polarization in NK-target cell interactions. J Immunol. 1998;161(7):3330–9.PubMed
40.
go back to reference Oliva A, Kinter AL, Vaccarezza M, Rubbert A, Catanzaro A, Moir S, Monaco J, Ehler L, Mizell S, Jackson R, et al. Natural killer cells from human immunodeficiency virus (HIV)-infected individuals are an important source of CC-chemokines and suppress HIV-1 entry and replication in vitro. J Clin Invest. 1998;102(1):223–31.CrossRefPubMedPubMedCentral Oliva A, Kinter AL, Vaccarezza M, Rubbert A, Catanzaro A, Moir S, Monaco J, Ehler L, Mizell S, Jackson R, et al. Natural killer cells from human immunodeficiency virus (HIV)-infected individuals are an important source of CC-chemokines and suppress HIV-1 entry and replication in vitro. J Clin Invest. 1998;102(1):223–31.CrossRefPubMedPubMedCentral
41.
go back to reference Schreibelt G, Tel J, Sliepen KH, Benitez-Ribas D, Figdor CG, Adema GJ, de Vries IJ. Toll-like receptor expression and function in human dendritic cell subsets: implications for dendritic cell-based anti-cancer immunotherapy. Cancer Immunol Immunother. 2010;59(10):1573–82.CrossRefPubMed Schreibelt G, Tel J, Sliepen KH, Benitez-Ribas D, Figdor CG, Adema GJ, de Vries IJ. Toll-like receptor expression and function in human dendritic cell subsets: implications for dendritic cell-based anti-cancer immunotherapy. Cancer Immunol Immunother. 2010;59(10):1573–82.CrossRefPubMed
42.
go back to reference van Montfoort N, van der Aa E, Woltman AM. Understanding MHC class I presentation of viral antigens by human dendritic cells as a basis for rational design of therapeutic vaccines. Front Immunol. 2014;5:182.CrossRefPubMedPubMedCentral van Montfoort N, van der Aa E, Woltman AM. Understanding MHC class I presentation of viral antigens by human dendritic cells as a basis for rational design of therapeutic vaccines. Front Immunol. 2014;5:182.CrossRefPubMedPubMedCentral
43.
go back to reference Galluzzi L, Vacchelli E, Eggermont A, Fridman WH, Galon J, Sautes-Fridman C, Tartour E, Zitvogel L, Kroemer G. Trial watch: experimental toll-like receptor agonists for cancer therapy. Oncoimmunology. 2012;1(5):699–716.CrossRefPubMedPubMedCentral Galluzzi L, Vacchelli E, Eggermont A, Fridman WH, Galon J, Sautes-Fridman C, Tartour E, Zitvogel L, Kroemer G. Trial watch: experimental toll-like receptor agonists for cancer therapy. Oncoimmunology. 2012;1(5):699–716.CrossRefPubMedPubMedCentral
44.
go back to reference Kokkinopoulos I, Jordan WJ, Ritter MA. Toll-like receptor mRNA expression patterns in human dendritic cells and monocytes. Mol Immunol. 2005;42(8):957–68.CrossRefPubMed Kokkinopoulos I, Jordan WJ, Ritter MA. Toll-like receptor mRNA expression patterns in human dendritic cells and monocytes. Mol Immunol. 2005;42(8):957–68.CrossRefPubMed
45.
go back to reference Marcenaro E, Della Chiesa M, Bellora F, Parolini S, Millo R, Moretta L, Moretta A. IL-12 or IL-4 prime human NK cells to mediate functionally divergent interactions with dendritic cells or tumors. J Immunol. 2005;174(7):3992–8.CrossRefPubMed Marcenaro E, Della Chiesa M, Bellora F, Parolini S, Millo R, Moretta L, Moretta A. IL-12 or IL-4 prime human NK cells to mediate functionally divergent interactions with dendritic cells or tumors. J Immunol. 2005;174(7):3992–8.CrossRefPubMed
46.
go back to reference Leong JW, Chase JM, Romee R, Schneider SE, Sullivan RP, Cooper MA, Fehniger TA. Preactivation with IL-12, IL-15, and IL-18 induces CD25 and a functional high-affinity IL-2 receptor on human cytokine-induced memory-like natural killer cells. Biol Blood Marrow Transplant. 2014;20(4):463–73.CrossRefPubMedPubMedCentral Leong JW, Chase JM, Romee R, Schneider SE, Sullivan RP, Cooper MA, Fehniger TA. Preactivation with IL-12, IL-15, and IL-18 induces CD25 and a functional high-affinity IL-2 receptor on human cytokine-induced memory-like natural killer cells. Biol Blood Marrow Transplant. 2014;20(4):463–73.CrossRefPubMedPubMedCentral
47.
go back to reference Ni J, Miller M, Stojanovic A, Garbi N, Cerwenka A. Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors. J Exp Med. 2012;209(13):2351–65.CrossRefPubMedPubMedCentral Ni J, Miller M, Stojanovic A, Garbi N, Cerwenka A. Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors. J Exp Med. 2012;209(13):2351–65.CrossRefPubMedPubMedCentral
48.
go back to reference Vitale M, Della Chiesa M, Carlomagno S, Pende D, Arico M, Moretta L, Moretta A. NK-dependent DC maturation is mediated by TNFalpha and IFNgamma released upon engagement of the NKp30 triggering receptor. Blood. 2005;106(2):566–71.CrossRefPubMed Vitale M, Della Chiesa M, Carlomagno S, Pende D, Arico M, Moretta L, Moretta A. NK-dependent DC maturation is mediated by TNFalpha and IFNgamma released upon engagement of the NKp30 triggering receptor. Blood. 2005;106(2):566–71.CrossRefPubMed
49.
go back to reference Ma F, Zhang J, Zhang J, Zhang C. The TLR7 agonists imiquimod and gardiquimod improve DC-based immunotherapy for melanoma in mice. Cell Mol Immunol. 2010;7(5):381–8.CrossRefPubMedPubMedCentral Ma F, Zhang J, Zhang J, Zhang C. The TLR7 agonists imiquimod and gardiquimod improve DC-based immunotherapy for melanoma in mice. Cell Mol Immunol. 2010;7(5):381–8.CrossRefPubMedPubMedCentral
50.
go back to reference Schierloh P, Yokobori N, Aleman M, Landoni V, Geffner L, Musella RM, Castagnino J, Baldini M, Abbate E, de la Barrera SS, et al. Mycobacterium tuberculosis-induced gamma interferon production by natural killer cells requires cross talk with antigen-presenting cells involving toll-like receptors 2 and 4 and the mannose receptor in tuberculous pleurisy. Infect Immun. 2007;75(11):5325–37.CrossRefPubMedPubMedCentral Schierloh P, Yokobori N, Aleman M, Landoni V, Geffner L, Musella RM, Castagnino J, Baldini M, Abbate E, de la Barrera SS, et al. Mycobacterium tuberculosis-induced gamma interferon production by natural killer cells requires cross talk with antigen-presenting cells involving toll-like receptors 2 and 4 and the mannose receptor in tuberculous pleurisy. Infect Immun. 2007;75(11):5325–37.CrossRefPubMedPubMedCentral
51.
go back to reference Muntasell A, Costa-Garcia M, Vera A, Marina-Garcia N, Kirschning CJ, Lopez-Botet M. Priming of NK cell anti-viral effector mechanisms by direct recognition of human cytomegalovirus. Front Immunol. 2013;4:40.CrossRefPubMedPubMedCentral Muntasell A, Costa-Garcia M, Vera A, Marina-Garcia N, Kirschning CJ, Lopez-Botet M. Priming of NK cell anti-viral effector mechanisms by direct recognition of human cytomegalovirus. Front Immunol. 2013;4:40.CrossRefPubMedPubMedCentral
52.
go back to reference Van Elssen CH, Oth T, Germeraad WT, Bos GM, Vanderlocht J. Natural killer cells: the secret weapon in dendritic cell vaccination strategies. Clin Cancer Res. 2014;20(5):1095–103.CrossRefPubMed Van Elssen CH, Oth T, Germeraad WT, Bos GM, Vanderlocht J. Natural killer cells: the secret weapon in dendritic cell vaccination strategies. Clin Cancer Res. 2014;20(5):1095–103.CrossRefPubMed
Metadata
Title
Pathogen recognition by NK cells amplifies the pro-inflammatory cytokine production of monocyte-derived DC via IFN-γ
Authors
Tammy Oth
Thomas H. P. M. Habets
Wilfred T. V. Germeraad
Marijke I. Zonneveld
Gerard M. J. Bos
Joris Vanderlocht
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Immunology / Issue 1/2018
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/s12865-018-0247-y

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