Virally infected and matured human dendritic cells activate natural killer cells via cooperative activity of plasma membrane-bound TNF and IL-15

Blood

Volumn 116, Issue 4, 2010, Pages 575-583

  Vujanovic, Lazar ^a,b   Szymkowski, David E ^c   Alber, Sean ^b   Watkins, Simon C ^b   Vujanovic, Nikola L ^a,b   Butterfield, Lisa H ^a,b  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c Xencor Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 15; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ADENOVIRUS; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ACTIVATION; CELL FUNCTION; CELL KILLING; CELL MATURATION; CELL MEMBRANE; CELL PROLIFERATION; CELL SURFACE; DENDRITIC CELL; FEMALE; HUMAN; HUMAN CELL; INNATE IMMUNITY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT; ADENOVIRUS INFECTION; ANIMAL; CELL COMMUNICATION; CELL CULTURE; CELL DIFFERENTIATION; CELL STRAIN K 562; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; PROTEIN BINDING; VIROLOGY;

ADENOVIRIDAE INFECTIONS; ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MEMBRANE; CELLS, CULTURED; DENDRITIC CELLS; FEMALE; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-15; K562 CELLS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; PROTEIN BINDING; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77956020302     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-08-240325     Document Type: Article

References (50)

1. Hart DN. Dendritic cells: unique leukocyte populations which control the primary immune response. Blood. 1997;90(9):3245-3287.
2. Fernandez NC, Lozier A, Flament C, et al. Dendritic cells directly trigger NK cell functions: crosstalk relevant in innate anti-tumor immune responses in vivo. Nature Med. 1999;5(4):405-411. (Pubitemid 29180578)
3. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med. 2002;195(3):327-333.
4. Andoniou CE, Coudert JD, Degli-Esposti MA. Killers and beyond: NK-cell-mediated control of immune responses. Eur J Immunol. 2008;38(11):2938-2942.
5. Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med. 2002;195(3):335-341. (Pubitemid 34461491)
6. Ferlazzo G, Tsang ML, Morretta L, Melioli G, Steinman RM, Munz C. Human dendritic cells activate resting natural killer (NK) cells and are recognized via NKp30 receptor by activated NK cells. J Exp Med. 2002;195(3):343-351.
7. Zamai L, Ponti C, Mirandola P, et al. NK cells and cancer. J Immunol. 2007;178(7):4011-4016.
8. Ferlazzo G, Semino C, Melioli G. HLA class I molecule expression is up-regulated during maturation of dendritic cells, protecting them from natural killer cell-mediated lysis. Immunol Lett. 2001;76(1):37-41. (Pubitemid 32166909)
9. - NK cells: a regulatory role of monocytes and IL-10. J Immunol. 2000;165(1):139-147.
10. Xu J, Chakrabarti AK, Tan JL, Ge L, Gambotto A, Vujanovic NL. Essential role of the TNF-TNFR2 cognate interaction in mouse dendritic cell-natural killer cell crosstalk. Blood. 2007;109(8):3333-3341.
11. Mortier E, Woo T, Advincula R, Gozalo S, Ma A. IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J Exp Med. 2008;205(5):1213-1225. (Pubitemid 351679694)
12. Dubois S, Mariner J, Waldmann TA, Tagaya Y. IL-15Ralpha recycles and presents IL-15 in trans to neighboring cells. Immunity. 2002;17(5):537-547.
13. Borg C, Jalil A, Laderach D, 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):3267-3275.
14. Granucci F, Zanoni I, Pavelka N, et al. A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J Exp Med. 2004;200(3):287-295. (Pubitemid 39031248)
15. Ferlazzo G, Pack M, Thomas D, et al. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Acad Sci U S A. 2004;101(47):16606-16611.
16. Andrews MD, Scalzo AA, Yokoyama WM, Smyth MJ, Degli-Esposti MA. Functional interactions between dendritic cells and NK cells during viral infection. Nature Immunol. 2003;4(2):175-181.
17. Jinushi M, Takehara T, Kanto T, et al. Critical role of MHC class I-related chain A and B expression on IFN-alpha stimulated dendritic cells in NK cell activation: impairment in chronic hepatitis C virus infection. J Immunol. 2003;170(3):1249-1256. (Pubitemid 36139490)
18. Spaggiari GM, Carosio R, Pende D, et al. NK cell-mediated lysis of autologous antigen presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30a and NKp46. Eur J Immunol. 2001;31(6):1656-1665.
19. Hayakawa Y, Screpanti V, Yagita H, et al. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol. 2004;172(1):123-129. (Pubitemid 38020463)
20. Arthur JF, Butterfield LH, Roth MD, et al. A comparison of gene transfer methods in human dendritic cells. Cancer Gene Ther. 1997;4(1):17-25.
21. Butterfield LH, Comin-Anduix B, Vujanovic L, et al. Adenovirus MART-1-engineered autologous dendritic cell vaccine for metastatic melanoma. J Immunother. 2008;31(3):294-309.
22. Vujanovic L, Whiteside TL, Potter DM, Chu J, Ferrone S, Butterfield LH. Regulation of antigen presentation machinery in human dendritic cells by recombinant adenovirus. Cancer Immunol Immunother. 2009;58(1):121-133.
23. Evdokimova VN, Liu Y, Potter DM, Butterfield LH. AFP-specific CD4+ helper T-cell responses in healthy donors and HCC patients. J Immunother. 2007;30(4):425-437. (Pubitemid 46684432)
24. Butterfield LH, Jilani SM, Chakraborty NG, et al. Generation of melanoma-specific cytotoxic T lymphocytes by dendritic cells transduced with a MART-1 adenovirus. J Immunol. 1998;161(10):5607-5613.
25. Wargo JA, Schumacher LY, Comin-Anduix B, et al. Natural killer cells play a critical role in the immune response following immunization with melanoma-antigen-engineered dendritic cells. Cancer Gene Ther. 2005;12(6):516-527.
26. Steed PM, Tansey MG, Zalevsky J, et al. Inactivation of TNF signaling by rationally designed dominant-negative TNF variants. Science. 2003;301(5641):1895-1898.
27. Zalevsky J, Secher T, Ezhevsky SA, et al. Dominant-negative inhibitors of soluble TNF attenuate experimental arthritis without suppressing innate immunity to infection. J Immunol. 2007;179(3):1872-1883.
28. McCoy MK, Martinez TN, Ruhn KA, et al. Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J Neurosci. 2006;26(37):9365-9375.
29. Vujanovic L, Mandic M, Olson WC, Kirkwood JM, Storkus WJ. A mycoplasma peptide elicits heteroclitic CD4+ T cell responses against tumor antigen MAGE-A6. Clin Cancer Res. 2007;13(22):6796-6806. (Pubitemid 350206818)
30. Kim GG, Donnenberg VS, Donnenberg AD, Gooding W, Whiteside TL. A novel multiparametric flow cytometry-based cytotoxicity assay simultaneously immunophenotypes effector cells: comparisons to a 4 h 51Cr-release assay. J Immunol Methods. 2007;325(1):51-66.
31. Pross HF, Baines MG, Rubin P, Shragge P, Patterson MS. Spontaneous lymphocyte-mediated cytotoxicity against tumor target cells: XI. The quantitation of natural killer cell activity. J Clin Immunol. 1981;1(1):51-63.
32. Schumacher L, Ribas A, Dissette VB, et al. Human dendritic cell maturation by adenovirus transduction enhances tumor antigen-specific T-cell responses. J Immunother. 2004;27(3):191-200. (Pubitemid 39118083)
33. Vitolo D, Vujanovic NL, Rabinowich H, Schlesinger M, Herberman RB, Whiteside TL. Rapid IL-2-induced adherence of human natural killer cells. J Immunol. 1993;151(4):1926-1937.
34. + NK helper cells. J Exp Med. 2005;202(7):941-953.
35. Lu G, Janjic BM, Janjic J, Whiteside TL, Storkus WJ, Vujanovic NL. Innate direct anticancer effector function of human immature dendritic cells: II. Role of TNF, LT-alpha1beta2, Fas ligand and TRAIL. J Immunol. 2002;168(4):1831-1839.
36. Masson AT, McVicar DW, Smith CA, Toung HA, War CF, Ortaldo JR. Regulation of NK cells through the 80-kDa TNFR (CD120b). J Leukoc Biol. 1995;58(2):249-255.
37. Mailliard RB, Wankowicz-Kalinska A, Cai Q, et al. Alpha-type 1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res. 2004;64(17):5934-5937.
38. Mailliard RB, Son YI, Redlinger R, et al. 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):2366-2373.
39. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245-252.
40. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003;3(12):984-993.
41. Robertson MJ, Ritz J. Biology and clinical relevance of human NK cells. Blood. 1990;76(12):2421-2438.
42. Lanier LL, Phillips JH. Natural killer cells. Curr Opin Immunol. 1992;4(1):38-42.
43. Cella M, Engering A, Pinet V, Pieters J, Lanzavecchia A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature. 1997;388(6644):782-787. (Pubitemid 27375158)
44. Jewett A, Bonavida B. Pivotal role of endogenous TNF-alpha in the IL-2-driven activation and proliferation of the functionally immature NK free subset. Cell Immunol. 1993;151(2):257-269.
45. Philpott NJ, Nociari M, Elkon KB, Falck-Pedersen E. Adenovirus-induced maturation of dendritic cells through a PI3 kinase-mediated TNF-alpha induction pathway. Proc Natl Acad Sci U S A. 2004;101(16):6200-6205.
46. Huntington ND, Legrand N, Alves NL, et al. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J Exp Med. 2009;206(1):25-34.
47. Ullrich E, Bonmort M, Mignot G, et al. Transpresentation of IL-15 dictates IFN-producing killer dendritic cells effector functions. J Immunol. 2008;180(12):7887-7897.
48. Kashii Y, Giorda R, Herberman RB, Whiteside TL, Vujanovic NL. Constitutive expression and role of the tumor necrosis factor family ligands in apoptotic killing by human natural killer cells. J Immunol. 1999;163(10):5358- 5366.
49. Brilot F, Strowig T, Roberts S, Arrey F, Münz C. NK cell survival mediated through the regulatory synapse with human DCs requires IL-15Ralpha. J Clin Invest. 2007;117(11):3316-3329. (Pubitemid 350096988)
50. Cheng C, Gall JG, Kong WP, et al. Mechanism of ad5 vaccine immunity and toxicity: fiber shaft targeting of dendritic cells. PLoS Pathog. 2007;3(2):e25.