Fast dendritic cells stimulated with alternative maturation mixtures induce polyfunctional and long-lasting activation of innate and adaptive effector cells with tumor-killing capabilities

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3328-3337

  Massa, Chiara ^a   Seliger, Barbara ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CL 097; GAMMA INTERFERON; IMIDAZOQUINOLINE DERIVATIVE; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; LIGAND; PHOSPHORYL LIPID A; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 4 LIGAND; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL INTERACTION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DENDRITIC CELL; EFFECTOR CELL; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; INTERMETHOD COMPARISON; KILLER CELL; NORMAL HUMAN; PRIORITY JOURNAL;

ADAPTIVE IMMUNITY; ANTIGENS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84875448312     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202024     Document Type: Article

References (43)

1. Draube, A., N. Klein-González, S. Mattheus, C. Brillant, M. Hellmich, A. Engert, and M. von Bergwelt-Baildon. 2011. Dendritic cell based tumor vaccination in prostate and renal cell cancer: a systematic review and metaanalysis. PLoS One 6: e18801.
2. Nakai, N., G. Hartmann, S. Kishimoto, and N. Katoh. 2010. Dendritic cell vaccination in human melanoma: relationships between clinical effects and vaccine parameters. Pigment Cell Melanoma Res. 23: 607-619.
3. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179: 1109-1118.
4. Jonuleit, H., U. Kühn, G. Müller, K. Steinbrink, L. Paragnik, E. Schmitt, J. Knop, and A. H. Enk. 1997. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serumfree conditions. Eur. J. Immunol. 27: 3135-3142.
5. Curtsinger, J. M., C. S. Schmidt, A. Mondino, D. C. Lins, R. M. Kedl, M. K. Jenkins, and M. F. Mescher. 1999. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J. Immunol. 162: 3256-3262.
6. Schmidt, C. S., and M. F. Mescher. 1999. Adjuvant effect of IL-12: conversion of peptide antigen administration from tolerizing to immunizing for CD8+ T cells in vivo. J. Immunol. 163: 2561-2567.
7. Anguille, S., E. L. J. M. Smits, N. Cools, H. Goossens, Z. N. Berneman, and V. F. I. Van Tendeloo. 2009. Short-term cultured, interleukin-15 differentiated dendritic cells have potent immunostimulatory properties. J. Transl. Med. 7: 109.
8. Dauer, M., B. Obermaier, J. Herten, C. Haerle, K. Pohl, S. Rothenfusser, M. Schnurr, S. Endres, and A. Eigler. 2003. Mature dendritic cells derived from human monocytes within 48 hours: a novel strategy for dendritic cell differentiation from blood precursors. J. Immunol. 170: 4069-4076.
9. Boullart, A. C. I., E. H. J. G. Aarntzen, P. Verdijk, J. F. M. Jacobs, D. H. Schuurhuis, D. Benitez-Ribas, G. Schreibelt, M. W. M. M. van de Rakt, N. M. Scharenborg, A. de Boer, 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.
10. Mailliard, R. B., A. Wankowicz-Kalinska, Q. Cai, A. Wesa, C. M. Hilkens, M. L. Kapsenberg, J. M. Kirkwood, W. J. Storkus, and P. Kalinski. 2004. Alphatype-1 polarized dendritic cells: a novel immunization tool with optimized CTLinducing activity. Cancer Res. 64: 5934-5937.
11. Ten Brinke, A., M. L. Karsten, M. C. Dieker, J. J. Zwaginga, and S. M. van Ham. 2007. The clinical grade maturation cocktail monophosphoryl lipid A plus IFNgamma generates monocyte-derived dendritic cells with the capacity to migrate and induce Th1 polarization. Vaccine 25: 7145-7152.
12. Zobywalski, A., M. Javorovic, B. Frankenberger, H. Pohla, E. Kremmer, I. Bigalke, and D. J. Schendel. 2007. Generation of clinical grade dendritic cells with capacity to produce biologically active IL-12p70. J. Transl. Med. 5: 18.
13. Moretta, A. 2002. Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat. Rev. Immunol. 2: 957-964.
14. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22: 633-640.
15. Björkström, N. K., T. Lindgren, M. Stoltz, C. Fauriat, M. Braun, M. Evander, J. Michaëlsson, K. J. Malmberg, J. Klingström, C. Ahlm, and H. G. Ljunggren. 2011. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J. Exp. Med. 208: 13-21.
16. Foley, B., S. Cooley, M. R. Verneris, M. Pitt, J. Curtsinger, X. Luo, S. Lopez-Vergès, L. L. Lanier, D. Weisdorf, and J. S. Miller. 2012. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 119: 2665-2674.
17. Sun, J. C., J. N. Beilke, and L. L. Lanier. 2009. Adaptive immune features of natural killer cells. Nature 457: 557-561.
18. Ho, W. Y., H. N. Nguyen, M. Wolfl, J. Kuball, and P. D. Greenberg. 2006. In vitro methods for generating CD8+ T-cell clones for immunotherapy from the naive repertoire. J. Immunol. Methods 310: 40-52.
19. Della Chiesa, M., M. Vitale, S. Carlomagno, G. Ferlazzo, L. Moretta, and A. Moretta. 2003. 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. 33: 1657-1666.
20. Jiang, W., N. R. Chai, D. Maric, and B. Bielekova. 2011. Unexpected role for granzyme K in CD56bright NK cell-mediated immunoregulation of multiple sclerosis. J. Immunol. 187: 781-790.
21. Cerboni, C., A. Zingoni, M. Cippitelli, M. Piccoli, L. Frati, and A. Santoni. 2007. Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK2 cell lysis. Blood 110: 606-615.
22. Soderquest, K., T. Walzer, B. Zafirova, L. S. Klavinskis, B. Polić, E. Vivier, G. M. Lord, and A. Martín-Fontecha. 2011. Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J. Immunol. 186: 3304-3308.
23. Ruggeri, L., M. Capanni, M. Casucci, I. Volpi, A. Tosti, K. Perruccio, E. Urbani, R. S. Negrin, M. F. Martelli, and A. Velardi. 1999. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 94: 333-339.
24. Igarashi, T., J. Wynberg, R. Srinivasan, B. Becknell, J. P. J. McCoy, Jr., Y. Takahashi, D. A. Suffredini, W. M. Linehan, M. A. Caligiuri, and R. W. Childs. 2004. Enhanced cytotoxicity of allogeneic NK cells with killer immunoglobulin-like receptor ligand incompatibility against melanoma and renal cell carcinoma cells. Blood 104: 170-177.
25. De Maria, A., F. Bozzano, C. Cantoni, and L. Moretta. 2011. 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. USA 108: 728-732.
26. Juelke, K., M. Killig, M. Luetke-Eversloh, E. Parente, J. Gruen, B. Morandi, G. Ferlazzo, A. Thiel, I. Schmitt-Knosalla, and C. Romagnani. 2010. CD62L expression identifies a unique subset of polyfunctional CD56dim NK cells. Blood 116: 1299-1307.
27. Sun, J. C., S. Lopez-Verges, C. C. Kim, J. L. DeRisi, and L. L. Lanier. 2011. NK cells and immune "memory." J. Immunol. 186: 1891-1897.
28. Kowalczyk, D., W. Skorupski, M. Drews, and J. Nowak. 1994. Different pattern of T cell receptor delta gene rearrangement in tumour-infiltrating lymphocytes and peripheral blood in patients with solid tumours. Cancer Immunol. Immunother. 39: 275-278.
29. Thomas, M. L., R. A. Badwe, R. K. Deshpande, U. C. Samant, and S. V. Chiplunkar. 2001. Role of adhesion molecules in recruitment of Vdelta1 T cells from the peripheral blood to the tumor tissue of esophageal cancer patients. Cancer Immunol. Immunother. 50: 218-225.
30. Viey, E., G. Fromont, B. Escudier, Y. Morel, S. Da Rocha, S. Chouaib, and A. Caignard. 2005. Phosphostim-activated gamma delta T cells kill autologous metastatic renal cell carcinoma. J. Immunol. 174: 1338-1347.
31. Laggner, U., P. Di Meglio, G. K. Perera, C. Hundhausen, K. E. Lacy, N. Ali, C. H. Smith, A. C. Hayday, B. J. Nickoloff, and F. O. Nestle. 2011. Identification of a novel proinflammatory human skin-homing Vγ9Vδ2 T cell subset with a potential role in psoriasis. J. Immunol. 187: 2783-2793.
32. Poggi, A., M. R. Zocchi, P. Costa, E. Ferrero, G. Borsellino, R. Placido, S. Galgani, M. Salvetti, C. Gasperini, G. Ristori, et al. 1999. IL-12-mediated NKRP1A up-regulation and consequent enhancement of endothelial transmigration of V delta 2+ TCR gamma delta+ Tlymphocytes from healthy donors and multiple sclerosis patients. J. Immunol. 162: 4349-4354.
33. Kobayashi, H., Y. Tanaka, J. Yagi, N. Minato, and K. Tanabe. 2011. Phase I/II study of adoptive transfer of γδ T cells in combination with zoledronic acid and IL-2 to patients with advanced renal cell carcinoma. Cancer Immunol. Immunother. 60: 1075-1084.
34. Sakamoto, M., J. Nakajima, T. Murakawa, T. Fukami, Y. Yoshida, T. Murayama, S. Takamoto, H. Matsushita, and K. Kakimi. 2011. Adoptive immunotherapy for advanced non-small cell lung cancer using zoledronate-expanded γδ T cells: a phase I clinical study. J. Immunother. 34: 202-211.
35. Cui, Y., L. Kang, L. Cui, and W. He. 2009. Human gammadelta T cell recognition of lipid A is predominately presented by CD1b or CD1c on dendritic cells. Biol. Direct 4: 47.
36. Conti, L., R. Casetti, M. Cardone, B. Varano, A. Martino, F. Belardelli, F. Poccia, and S. Gessani. 2005. Reciprocal activating interaction between dendritic cells and pamidronate-stimulated gammadelta T cells: role of CD86 and inflammatory cytokines. J. Immunol. 174: 252-260.
37. Gruenbacher, G., H. Gander, A. Rahm, W. Nussbaumer, N. Romani, and M. Thurnher. 2009. CD56+ human blood dendritic cells effectively promote TH1-type gammadelta T-cell responses. Blood 114: 4422-4431.
38. Kato, Y., Y. Tanaka, H. Tanaka, S. Yamashita, and N. Minato. 2003. Requirement of species-specific interactions for the activation of human gamma delta T cells by pamidronate. J. Immunol. 170: 3608-3613.
39. Alexander, A. A. Z., A. Maniar, J. S. Cummings, A. M. Hebbeler, D. H. Schulze, B. R. Gastman, C. D. Pauza, S. E. Strome, and A. I. Chapoval. 2008. Isopentenyl pyrophosphate-activated CD56+ gammadelta T lymphocytes display potent antitumor activity toward human squamous cell carcinoma. Clin. Cancer Res. 14: 4232-4240.
40. Qin, G., Y. Liu, J. Zheng, Z. Xiang, I. H. Y. Ng, J. S. Malik Peiris, Y. L. Lau, and W. Tu. 2012. Phenotypic and functional characterization of human gd T-cell subsets in response to influenza A viruses. J. Infect. Dis. 205: 1646-1653.
41. Takahara, M., M. Miyai, M. Tomiyama, M. Mutou, A. J. Nicol, and M. Nieda. 2008. Copulsing tumor antigen-pulsed dendritic cells with zoledronate efficiently enhance the expansion of tumor antigen-specific CD8+ T cells via Vgamma9gammadelta T cell activation. J. Leukoc. Biol. 83: 742-754.
42. Traxlmayr, M. W., D. Wesch, A. M. Dohnal, P. Funovics, M. B. Fischer, D. Kabelitz, and T. Felzmann. 2010. Immune suppression by gammadelta T-cells as a potential regulatory mechanism after cancer vaccination with IL-12 secreting dendritic cells. J. Immunother. 33: 40-52.
43. Casella, C. R., and T. C. Mitchell. 2008. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell. Mol. Life Sci. 65: 3231-3240.