Poly(I:C) enhances the susceptibility of leukemic cells to NK cell cytotoxicity and phagocytosis by DC

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Lion, Eva ^a   Anguille, Sébastien ^a   Berneman, Zwi N ^a,b   Smits, Evelien L J M ^a   van Tendeloo, Viggo F I ^a,b  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b ANTWERP UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; POLYINOSINIC POLYCYTIDYLIC ACID; FLUORESCENT DYE;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CELL ACTIVATION; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DENDRITIC CELL; ELECTROPORATION; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOGENICITY; LEUKEMIA CELL; NATURAL KILLER CELL; PHAGOCYTOSIS; PURIFICATION; IMMUNOLOGY; PATHOLOGY;

DENDRITIC CELLS; ELECTROPORATION; FLUORESCENT DYES; HUMANS; KILLER CELLS, NATURAL; LEUKEMIA, MYELOID, ACUTE; PHAGOCYTOSIS; POLY I-C;

EID: 79959280119     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020952     Document Type: Article

References (103)

1. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G, (2008) Immunological aspects of cancer chemotherapy. Nat Rev Immunol 8: 59-73.
2. Degli-Esposti MA, Smyth MJ, (2005) Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol 5: 112-124.
3. Ferlazzo G, Munz C, (2009) Dendritic cell interactions with NK cells from different tissues. J Clin Immunol 29: 265-273.
4. Walzer T, Dalod M, Robbins SH, Zitvogel L, Vivier E, (2005) Natural-killer cells and dendritic cells: "l'union fait la force". Blood 106: 2252-2258.
5. Green DR, Ferguson T, Zitvogel L, Kroemer G, (2009) Immunogenic and tolerogenic cell death. Nat Rev Immunol 9: 353-363.
6. Albert ML, Sauter B, Bhardwaj N, (1998) Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392: 86-89.
7. Lin ML, Zhan Y, Villadangos JA, Lew AM, (2008) The cell biology of cross-presentation and the role of dendritic cell subsets. Immunol Cell Biol 86: 353-362.
8. Gallucci S, Matzinger P, (2001) Danger signals: SOS to the immune system. Curr Opin Immunol 13: 114-119.
9. Malmberg KJ, Bryceson YT, Carlsten M, Andersson S, Bjorklund A, et al. (2008) NK cell-mediated targeting of human cancer and possibilities for new means of immunotherapy. Cancer Immunol Immunother 57: 1541-1552.
10. Sutlu T, Alici E, (2009) Natural killer cell-based immunotherapy in cancer: current insights and future prospects. J Intern Med 266: 154-181.
11. Terme M, Ullrich E, Delahaye NF, Chaput N, Zitvogel L, (2008) Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat Immunol 9: 486-494.
12. Strowig T, Brilot F, Munz C, (2008) Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J Immunol 180: 7785-7791.
13. Garg AD, Nowis D, Golab J, Vandenabeele P, Krysko DV, et al. (2010) Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim Biophys Acta 1805: 53-71.
14. Feng H, Zeng Y, Graner MW, Katsanis E, (2002) Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 100: 4108-4115.
15. Hoffmann TK, Meidenbauer N, Dworacki G, Kanaya H, Whiteside TL, (2000) Generation of tumor-specific T-lymphocytes by cross-priming with human dendritic cells ingesting apoptotic tumor cells. Cancer Res 60: 3542-3549.
16. Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, et al. (2010) Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 207: 1247-1260.
17. Lee JJ, Foon KA, Mailliard RB, Muthuswamy R, Kalinski P, (2008) Type 1-polarized dendritic cells loaded with autologous tumor are a potent immunogen against chronic lymphocytic leukemia. J Leukoc Biol 84: 319-325.
18. Moehler MH, Zeidler M, Wilsberg V, Cornelis JJ, Woelfel T, et al. (2005) Parvovirus H-1-induced tumor cell death enhances human immune response in vitro via increased phagocytosis, maturation, and cross-presentation by dendritic cells. Hum Gene Ther 16: 996-1005.
19. Rovere P, Vallinoto C, Bondanza A, Crosti MC, Rescigno M, et al. (1998) Bystander apoptosis triggers dendritic cell maturation and antigen-presenting function. J Immunol 161: 4467-4471.
20. Schnurr M, Scholz C, Rothenfusser S, Galambos P, Dauer M, et al. (2002) Apoptotic pancreatic tumor cells are superior to cell lysates in promoting cross-priming of cytotoxic T cells and activate NK and gammadelta T cells. Cancer Res 62: 2347-2352.
21. Spisek R, Charalambous A, Mazumder A, Vesole DH, Jagannath S, et al. (2007) Bortezomib enhances dendritic cell (DC)-mediated induction of immunity to human myeloma via exposure of cell surface heat shock protein 90 on dying tumor cells: therapeutic implications. Blood 109: 4839-4845.
22. Spisek R, Chevallier P, Morineau N, Milpied N, Avet-Loiseau H, et al. (2002) Induction of leukemia-specific cytotoxic response by cross-presentation of late-apoptotic leukemic blasts by autologous dendritic cells of nonleukemic origin. Cancer Res 62: 2861-2868.
23. Strome SE, Voss S, Wilcox R, Wakefield TL, Tamada K, et al. (2002) Strategies for antigen loading of dendritic cells to enhance the antitumor immune response. Cancer Res 62: 1884-1889.
24. von Euw EM, Barrio MM, Furman D, Bianchini M, Levy EM, et al. (2007) Monocyte-derived dendritic cells loaded with a mixture of apoptotic/necrotic melanoma cells efficiently cross-present gp100 and MART-1 antigens to specific CD8(+) T lymphocytes. J Transl Med 5: 19.
25. Fry TJ, Shand JL, Milliron M, Tasian SK, Mackall CL, (2009) Antigen loading of DCs with irradiated apoptotic tumor cells induces improved anti-tumor immunity compared to other approaches. Cancer Immunol Immunother 58: 1257-1264.
26. Henry F, Boisteau O, Bretaudeau L, Lieubeau B, Meflah K, et al. (1999) Antigen-presenting cells that phagocytose apoptotic tumor-derived cells are potent tumor vaccines. Cancer Res 59: 3329-3332.
27. Ronchetti A, Rovere P, Iezzi G, Galati G, Heltai S, et al. (1999) Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines. J Immunol 163: 130-136.
28. Hallett WH, Ames E, Motarjemi M, Barao I, Shanker A, et al. (2008) Sensitization of tumor cells to NK cell-mediated killing by proteasome inhibition. J Immunol 180: 163-170.
29. Lanier LL, (2005) Missing self, NK cells, and The White Album. J Immunol 174: 6565.
30. Kim MJ, Kim HB, Bae JH, Lee JW, Park SJ, et al. (2009) Sensitization of human K562 leukemic cells to TRAIL-induced apoptosis by inhibiting the DNA-PKcs/Akt-mediated cell survival pathway. Biochem Pharmacol 78: 573-582.
31. Lundqvist A, Abrams SI, Schrump DS, Alvarez G, Suffredini D, et al. (2006) Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: a novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Res 66: 7317-7325.
32. Rohner A, Langenkamp U, Siegler U, Kalberer CP, Wodnar-Filipowicz A, (2007) Differentiation-promoting drugs up-regulate NKG2D ligand expression and enhance the susceptibility of acute myeloid leukemia cells to natural killer cell-mediated lysis. Leuk Res 31: 1393-1402.
33. Szczepanski MJ, Szajnik M, Welsh A, Foon KA, Whiteside TL, et al. (2010) Interleukin-15 enhances natural killer cell cytotoxicity in patients with acute myeloid leukemia by upregulating the activating NK cell receptors. Cancer Immunol Immunother 59: 73-79.
34. Koh CY, Blazar BR, George T, Welniak LA, Capitini CM, et al. (2001) Augmentation of antitumor effects by NK cell inhibitory receptor blockade in vitro and in vivo. Blood 97: 3132-3137.
35. Sheridan C, (2006) First-in-class cancer therapeutic to stimulate natural killer cells. Nat Biotechnol 24: 597.
36. Triulzi C, Vertuani S, Curcio C, Antognoli A, Seibt J, et al. (2010) Antibody-dependent natural killer cell-mediated cytotoxicity engendered by a kinase-inactive human HER2 adenovirus-based vaccination mediates resistance to breast tumors. Cancer Res 70: 7431-7441.
37. Wu L, Parton A, Lu L, Adams M, Schafer P, et al. (2011) Lenalidomide enhances antibody-dependent cellular cytotoxicity of solid tumor cells in vitro: influence of host immune and tumor markers. Cancer Immunol Immunother.
38. Smits EL, Berneman ZN, Van Tendeloo VF, (2009) Immunotherapy of acute myeloid leukemia: current approaches. Oncologist 14: 240-252.
39. Barrett AJ, Le Blanc K, (2010) Immunotherapy prospects for acute myeloid leukaemia. Clin Exp Immunol 161: 223-232.
40. Costello RT, Sivori S, Marcenaro E, Lafage-Pochitaloff M, Mozziconacci MJ, et al. (2002) Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood 99: 3661-3667.
41. Fauriat C, Just-Landi S, Mallet F, Arnoulet C, Sainty D, et al. (2007) Deficient expression of NCR in NK cells from acute myeloid leukemia: Evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood 109: 323-330.
42. Fauriat C, Moretta A, Olive D, Costello RT, (2005) Defective killing of dendritic cells by autologous natural killer cells from acute myeloid leukemia patients. Blood 106: 2186-2188.
43. Costello RT, Fauriat C, Sivori S, Marcenaro E, Olive D, (2004) NK cells: innate immunity against hematological malignancies? Trends Immunol 25: 328-333.
44. Verheyden S, Demanet C, (2008) NK cell receptors and their ligands in leukemia. Leukemia 22: 249-257.
45. Nowbakht P, Ionescu MC, Rohner A, Kalberer CP, Rossy E, et al. (2005) Ligands for natural killer cell-activating receptors are expressed upon the maturation of normal myelomonocytic cells but at low levels in acute myeloid leukemias. Blood 105: 3615-3622.
46. Salih HR, Antropius H, Gieseke F, Lutz SZ, Kanz L, et al. (2003) Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 102: 1389-1396.
47. McCartney S, Vermi W, Gilfillan S, Cella M, Murphy TL, et al. (2009) Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J Exp Med 206: 2967-2976.
48. Akira S, Takeda K, (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
49. Smits EL, Cools N, Lion E, Van Camp K, Ponsaerts P, et al. (2010) The Toll-like receptor 7/8 agonist resiquimod greatly increases the immunostimulatory capacity of human acute myeloid leukemia cells. Cancer Immunol Immunother 59: 35-46.
50. Matsumoto M, Seya T, (2008) TLR3: interferon induction by double-stranded RNA including poly(I:C). Adv Drug Deliv Rev 60: 805-812.
51. Salaun B, Coste I, Rissoan MC, Lebecque SJ, Renno T, (2006) TLR3 can directly trigger apoptosis in human cancer cells. J Immunol 176: 4894-4901.
52. Salem ML, El-Naggar SA, Kadima A, Gillanders WE, Cole DJ, (2006) The adjuvant effects of the toll-like receptor 3 ligand polyinosinic-cytidylic acid poly (I:C) on antigen-specific CD8+ T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu. Vaccine 24: 5119-5132.
53. Smits EL, Ponsaerts P, Van de Velde AL, Van Driessche A, Cools N, et al. (2007) Proinflammatory response of human leukemic cells to dsRNA transfection linked to activation of dendritic cells. Leukemia 21: 1691-1699.
54. Girart MV, Fuertes MB, Domaica CI, Rossi LE, Zwirner NW, (2007) 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 179: 3472-3479.
55. Akazawa T, Ebihara T, Okuno M, Okuda Y, Shingai M, et al. (2007) Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells. Proc Natl Acad Sci U S A 104: 252-257.
56. Lauzon NM, Mian F, MacKenzie R, Ashkar AA, (2006) The direct effects of Toll-like receptor ligands on human NK cell cytokine production and cytotoxicity. Cell Immunol 241: 102-112.
57. Perrot I, Deauvieau F, Massacrier C, Hughes N, Garrone P, et al. (2010) 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 185: 2080-2088.
58. Pisegna S, Pirozzi G, Piccoli M, Frati L, Santoni A, et al. (2004) p38 MAPK activation controls the TLR3-mediated up-regulation of cytotoxicity and cytokine production in human NK cells. Blood 104: 4157-4164.
59. Schmidt KN, Leung B, Kwong M, Zarember KA, Satyal S, et al. (2004) APC-independent activation of NK cells by the Toll-like receptor 3 agonist double-stranded RNA. J Immunol 172: 138-143.
60. Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, et al. (2004) 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 101: 10116-10121.
61. Adams M, Navabi H, Jasani B, Man S, Fiander A, et al. (2003) Dendritic cell (DC) based therapy for cervical cancer: use of DC pulsed with tumour lysate and matured with a novel synthetic clinically non-toxic double stranded RNA analogue poly [I]:poly [C(12)U] (Ampligen R). Vaccine 21: 787-790.
62. Benwell RK, Hruska JE, Fritsche KL, Lee DR, (2010) Double stranded RNA- relative to other TLR ligand-activated dendritic cells induce extremely polarized human Th1 responses. Cell Immunol 264: 119-126.
63. Boullart AC, Aarntzen EH, Verdijk P, Jacobs JF, Schuurhuis DH, et al. (2008) Maturation of monocyte-derived dendritic cells with Toll-like receptor 3 and 7/8 ligands combined with prostaglandin E2 results in high interleukin-12 production and cell migration. Cancer Immunol Immunother 57: 1589-1597.
64. Lore K, Betts MR, Brenchley JM, Kuruppu J, Khojasteh S, et al. (2003) Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J Immunol 171: 4320-4328.
65. Strowig T, Brilot F, Arrey F, Bougras G, Thomas D, et al. (2008) Tonsilar NK cells restrict B cell transformation by the Epstein-Barr virus via IFN-gamma. PLoS Pathog 4: e27.
66. Verdijk RM, Mutis T, Esendam B, Kamp J, Melief CJ, et al. (1999) Polyriboinosinic polyribocytidylic acid (poly(I:C)) induces stable maturation of functionally active human dendritic cells. J Immunol 163: 57-61.
67. Moretta A, Marcenaro E, Parolini S, Ferlazzo G, Moretta L, (2008) NK cells at the interface between innate and adaptive immunity. Cell Death Differ 15: 226-233.
68. Zanoni I, Granucci F, Foti M, Ricciardi-Castagnoli P, (2007) Self-tolerance, dendritic cell (DC)-mediated activation and tissue distribution of natural killer (NK) cells. Immunol Lett 110: 6-17.
69. Datta SK, Redecke V, Prilliman KR, Takabayashi K, Corr M, et al. (2003) A subset of Toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells. J Immunol 170: 4102-4110.
70. Durand V, Wong SY, Tough DF, Le Bon A, (2004) Shaping of adaptive immune responses to soluble proteins by TLR agonists: a role for IFN-alpha/beta. Immunol Cell Biol 82: 596-602.
71. Fujimoto C, Nakagawa Y, Ohara K, Takahashi H, (2004) Polyriboinosinic polyribocytidylic acid [poly(I:C)]/TLR3 signaling allows class I processing of exogenous protein and induction of HIV-specific CD8+ cytotoxic T lymphocytes. Int Immunol 16: 55-63.
72. Cui Z, Le UM, Qiu F, Shaker DS, (2007) Learning from viruses: the necrotic bodies of tumor cells with intracellular synthetic dsRNA induced strong anti-tumor immune responses. Pharm Res 24: 1645-1652.
73. Cui Z, Qiu F, (2006) Synthetic double-stranded RNA poly(I:C) as a potent peptide vaccine adjuvant: therapeutic activity against human cervical cancer in a rodent model. Cancer Immunol Immunother 55: 1267-1279.
74. Salio M, Cerundolo V, (2005) Viral immunity: cross-priming with the help of TLR3. Curr Biol 15: R336-339.
75. Schulz O, Diebold SS, Chen M, Naslund TI, Nolte MA, et al. (2005) Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 433: 887-892.
76. Frleta D, Yu CI, Klechevsky E, Flamar AL, Zurawski G, et al. (2009) Influenza virus and poly(I:C) inhibit MHC class I-restricted presentation of cell-associated antigens derived from infected dead cells captured by human dendritic cells. J Immunol 182: 2766-2776.
77. McBride S, Hoebe K, Georgel P, Janssen E, (2006) Cell-associated double-stranded RNA enhances antitumor activity through the production of type I IFN. J Immunol 177: 6122-6128.
78. Lion E, Smits EL, Berneman ZN, Van Tendeloo VF, (2009) Acute myeloid leukemic cell lines loaded with synthetic dsRNA trigger IFN-gamma secretion by human NK cells. Leuk Res 33: 539-546.
79. Smyth MJ, Cretney E, Kershaw MH, Hayakawa Y, (2004) Cytokines in cancer immunity and immunotherapy. Immunol Rev 202: 275-293.
80. Pfeffer LM, Dinarello CA, Herberman RB, Williams BR, Borden EC, et al. (1998) Biological properties of recombinant alpha-interferons: 40th anniversary of the discovery of interferons. Cancer Res 58: 2489-2499.
81. Le Bon A, Tough DF, (2008) Type I interferon as a stimulus for cross-priming. Cytokine Growth Factor Rev 19: 33-40.
82. Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, et al. (1999) Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 5: 405-411.
83. Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, et al. (2003) Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 171: 2366-2373.
84. Romagnani C, Della Chiesa M, Kohler S, Moewes B, Radbruch A, et al. (2005) Activation of human NK cells by plasmacytoid dendritic cells and its modulation by CD4+ T helper cells and CD4+ CD25hi T regulatory cells. Eur J Immunol 35: 2452-2458.
85. Fernandez NC, Flament C, Crepineau F, Angevin E, Vivier E, et al. (2002) Dendritic cells (DC) promote natural killer (NK) cell functions: dynamics of the human DC/NK cell cross talk. Eur Cytokine Netw 13: 17-27.
86. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, et al. (2002) Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 195: 327-333.
87. Gerosa F, Gobbi A, Zorzi P, Burg S, Briere F, et al. (2005) The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J Immunol 174: 727-734.
88. Wehner R, Lobel B, Bornhauser M, Schakel K, Cartellieri M, et al. (2009) Reciprocal activating interaction between 6-sulfo LacNAc+ dendritic cells and NK cells. Int J Cancer 124: 358-366.
89. Prestwich RJ, Errington F, Steele LP, Ilett EJ, Morgan RS, et al. (2009) Reciprocal human dendritic cell-natural killer cell interactions induce antitumor activity following tumor cell infection by oncolytic reovirus. J Immunol 183: 4312-4321.
90. Vujanovic L, Szymkowski DE, Alber S, Watkins SC, Vujanovic NL, et al. (2010) Virally infected and matured human dendritic cells activate natural killer cells via cooperative activity of plasma membrane-bound TNF and IL-15. Blood 116: 575-583.
91. Yu Y, Hagihara M, Ando K, Gansuvd B, Matsuzawa H, et al. (2001) Enhancement of human cord blood CD34+ cell-derived NK cell cytotoxicity by dendritic cells. J Immunol 166: 1590-1600.
92. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, et al. (2002) Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med 195: 343-351.
93. Munz C, Dao T, Ferlazzo G, de Cos MA, Goodman K, et al. (2005) Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells. Blood 105: 266-273.
94. Ferlazzo G, Morandi B, D'Agostino A, Meazza R, Melioli G, et al. (2003) 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 33: 306-313.
95. Piccioli D, Sbrana S, Melandri E, Valiante NM, (2002) Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med 195: 335-341.
96. Carbone E, Terrazzano G, Ruggiero G, Zanzi D, Ottaiano A, et al. (1999) Recognition of autologous dendritic cells by human NK cells. Eur J Immunol 29: 4022-4029.
97. Marcenaro E, Della Chiesa M, Bellora F, Parolini S, Millo R, et al. (2005) IL-12 or IL-4 prime human NK cells to mediate functionally divergent interactions with dendritic cells or tumors. J Immunol 174: 3992-3998.
98. Pietra G, Romagnani C, Mazzarino P, Millo E, Moretta L, et al. (2003) Comparative analysis of NK- or NK-CTL-mediated lysis of immature or mature autologous dendritic cells. Eur J Immunol 33: 3427-3432.
99. Wilson JL, Heffler LC, Charo J, Scheynius A, Bejarano MT, et al. (1999) Targeting of human dendritic cells by autologous NK cells. J Immunol 163: 6365-6370.
100. Bontkes HJ, Kramer D, Ruizendaal JJ, Meijer CJ, Hooijberg E, (2008) Tumor associated antigen and interleukin-12 mRNA transfected dendritic cells enhance effector function of natural killer cells and antigen specific T-cells. Clin Immunol 127: 375-384.
101. Ferlazzo G, Pack M, Thomas D, Paludan C, Schmid D, et al. (2004) Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci U S A 101: 16606-16611.
102. Zanoni I, Foti M, Ricciardi-Castagnoli P, Granucci F, (2005) TLR-dependent activation stimuli associated with Th1 responses confer NK cell stimulatory capacity to mouse dendritic cells. J Immunol 175: 286-292.
103. Kamath AT, Sheasby CE, Tough DF, (2005) Dendritic cells and NK cells stimulate bystander T cell activation in response to TLR agonists through secretion of IFN-alpha beta and IFN-gamma. J Immunol 174: 767-776.