Peroxynitrite-dependent killing of cancer cells and presentation of released tumor antigens by activated dendritic cells

Journal of Immunology

Volumn 184, Issue 4, 2010, Pages 1876-1884

  Fraszczak, Jennifer ^a   Trad, Malika ^a   Janikashvili, Nona ^c   Cathelin, Dominique ^a   Lakomy, Daniela ^a   Granci, Virginie ^a   Morizot, Alexandre ^a   Audia, Sylvain ^a,b   Micheau, Olivier ^a   Lagrost, Laurent ^a   Katsanis, Emmanuel ^c   Solary, Eric ^a   Larmonier, Nicolas ^c   Bonnotte, Bernard ^a,b  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b HÔPITAL DU BOCAGE   (France)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; PEROXYNITRITE; TUMOR ANTIGEN; PEROXYNITROUS ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; CANCER CELL; CANCER CELL CULTURE; CELL KILLING; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IMMUNOTHERAPY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSGENIC MOUSE; TUMOR IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL DEATH; COCULTURE; EXPERIMENTAL MELANOMA; EXPERIMENTAL NEOPLASM; HELA CELL; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CELL DEATH; CELL LINE, TUMOR; COCULTURE TECHNIQUES; DENDRITIC CELLS; HELA CELLS; HUMANS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; PEROXYNITROUS ACID;

EID: 77949896128     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900831     Document Type: Article

References (48)

1. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
2. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767-811.
3. Dubsky, P., H. Ueno, B. Piqueras, J. Connolly, J. Banchereau, and A. K. Palucka. 2005. Human dendritic cell subsets for vaccination. J. Clin. Immunol. 25: 551-572.
4. Chan, C. W., E. Crafton, H. N. Fan, J. Flook, K. Yoshimura, M. Skarica, D. Brockstedt, T. W. Dubensky, M. F. Stins, L. L. Lanier, et al. 2006. Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat. Med. 12: 207-213.
5. Chaperot, L., A. Blum, O. Manches, G. Lui, J. Angel, J. P. Molens, and J. Plumas. 2006. Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J. Immunol. 176: 248-255.
6. Chapoval, A. I., K. Tamada, and L. Chen. 2000. In vitro growth inhibition of a broad spectrum of tumor cell lines by activated human dendritic cells. Blood 95: 2346-2351.
7. Chaudhry, U. I., T. P. Kingham, G. Plitas, S. C. Katz, J. R. Raab, and R. P. DeMatteo. 2006. Combined stimulation with interleukin-18 and CpG induces murine natural killer dendritic cells to produce IFN-γ and inhibit tumor growth. Cancer Res. 66: 10497-10504.
8. Fanger, N. A., C. R. Maliszewski, K. Schooley, and T. S. Griffith. 1999. Human dendritic cells mediate cellular apoptosis via tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J. Exp. Med. 190: 1155-1164.
9. Hill, K. S., F. Errington, L. P. Steele, A. Merrick, R. Morgan, P. J. Selby, N. T. Georgopoulos, D. M. O'Donnell, and A. A. Melcher. 2008. OK432-activated human dendritic cells kill tumor cells via CD40/CD40 ligand interactions. J. Immunol. 181: 3108-3115.
10. Janjic, B. M., G. Lu, A. Pimenov, T. L. Whiteside, W. J. Storkus, and N. L. Vujanovic. 2002. Innate direct anticancer effector function of human immature dendritic cells. I. Involvement of an apoptosis-inducing pathway. J. Immunol. 168: 1823-1830.
11. Josien, R., M. Heslan, J. P. Soulillou, and M. C. Cuturi. 1997. Rat spleen dendritic cells express natural killer cell receptor protein 1 (NKR-P1) and have cytotoxic activity to select targets via a Ca2+-dependent mechanism. J. Exp. Med. 186: 467-472.
12. Liu, S., Y. Yu, M. Zhang, W. Wang, and X. Cao. 2001. The involvement of TNF-α-related apoptosis-inducing ligand in the enhanced cytotoxicity of IFN-β-stimulated human dendritic cells to tumor cells. J. Immunol. 166: 5407-5415. (Pubitemid 32374160)
13. 2, Fas ligand, and TNF-related apoptosis-inducing ligand. J. Immunol. 168: 1831-1839.
14. Manna, P. P., and T. Mohanakumar. 2002. Human dendritic cell mediated cytotoxicity against breast carcinoma cells in vitro. J. Leukoc. Biol. 72: 312-320.
15. Nicolas, A., D. Cathelin, N. Larmonier, J. Fraszczak, P. E. Puig, A. Bouchot, A. Bateman, E. Solary, and B. Bonnotte. 2007. Dendritic cells trigger tumor cell death by a nitric oxide-dependent mechanism. J. Immunol. 179: 812-818.
16. Nouri-Shirazi, M., J. Banchereau, D. Bell, S. Burkeholder, E. T. Kraus, J. Davoust, and K. A. Palucka. 2000. Dendritic cells capture killed tumor cells and present their antigens to elicit tumor-specific immune responses. J. Immunol. 165: 3797-3803.
17. Roux, S., L. Apetoh, F. Chalmin, S. Ladoire, G. Mignot, P. E. Puig, G. Lauvau, L. Zitvogel, F. Martin, B. Chauffert, et al. 2008. CD4+CD25+ Tregs control the TRAIL-dependent cytotoxicity of tumor-infiltrating DCs in rodent models of colon cancer. J. Clin. Invest. 118: 3751-3761.
18. Schmitz, M., S. Zhao, Y. Deuse, K. Schäkel, R. Wehner, H. Wöhner, K. Hölig, F. Wienforth, A. Kiessling, M. Bornhäuser, et al. 2005. Tumoricidal potential of native blood dendritic cells: direct tumor cell killing and activation of NK cell-mediated cytotoxicity. J. Immunol. 174: 4127-4134.
19. Shi, J., K. Ikeda, N. Fujii, E. Kondo, K. Shinagawa, F. Ishimaru, K. Kaneda, M. Tanimoto, X. Li, and Q. Pu. 2005. Activated human umbilical cord blood dendritic cells kill tumor cells without damaging normal hematological progenitor cells. Cancer Sci. 96: 127-133.
20. Shimamura, H., R. Cumberland, K. Hiroishi, S. C. Watkins, M. T. Lotze, and J. Baar. 2002. Murine dendritic cell-induced tumor apoptosis is partially mediated by nitric oxide. J. Immunother. 25: 226-234.
21. Stary, G., C. Bangert, M. Tauber, R. Strohal, T. Kopp, and G. Stingl. 2007. Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J. Exp. Med. 204: 1441-1451.
22. Süss, G., and K. Shortman. 1996. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand-induced apoptosis. J. Exp. Med. 183: 1789-1796.
23. Trinité, B., C. Chauvin, H. Pêche, C. Voisine, M. Heslan, and R. Josien. 2005. Immature CD4- CD103+ rat dendritic cells induce rapid caspase-independent apoptosis-like cell death in various tumor and nontumor cells and phagocytose their victims. J. Immunol. 175: 2408-2417.
24. Vanderheyde, N., E. Aksoy, Z. Amraoui, P. Vandenabeele, M. Goldman, and F. Willems. 2001. Tumoricidal activity of monocyte-derived dendritic cells: evidence for a caspase-8-dependent, Fas-associated death domain-independent mechanism. J. Immunol. 167: 3565-3569.
25. Vidalain, P. O., O. Azocar, H. Yagita, C. Rabourdin-Combe, and C. Servet-Delprat. 2001. Cytotoxic activity of human dendritic cells is differentially regulated by double-stranded RNA and CD40 ligand. J. Immunol. 167: 3765-3772.
26. Yang, R., D. Xu, A. Zhang, and A. Gruber. 2001. Immature dendritic cells kill ovarian carcinoma cells by a FAS/FASL pathway, enabling them to sensitize tumor-specific CTLs. Int. J. Cancer 94: 407-413.
27. Larmonier, N., J. Fraszczak, D. Lakomy, B. Bonnotte, and E. Katsanis. 2009. Killer dendritic cells and their potential for cancer immunotherapy. Cancer Immunol. Immunother. 59: 1-11.
28. Martin, F., A. Caignard, J. F. Jeannin, A. Leclerc, and M. Martin. 1983. Selection by trypsin of two sublines of rat colon cancer cells forming progressive or regressive tumors. Int. J. Cancer 32: 623-627. (Pubitemid 14247908)
29. Micheau, O., S. Lens, O. Gaide, K. Alevizopoulos, and J. Tschopp. 2001. NF-kappaB signals induce the expression of c-FLIP. Mol. Cell. Biol. 21: 5299-5305.
30. Bonnotte, B., N. Favre, S. Reveneau, O. Micheau, N. Droin, C. Garrido, A. Fontana, B. Chauffert, E. Solary, and F. Martin. 1998. Cancer cell sensitization to fas-mediated apoptosis by sodium butyrate. Cell Death Differ. 5: 480-487.
31. Green, L. C., D. A. Wagner, J. Glogowski, P. L. Skipper, J. S. Wishnok, and S. R. Tannenbaum. 1982. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126: 131-138.
32. Larmonier, N., D. Mérino, A. Nicolas, D. Cathelin, A. Besson, A. Bateman, E. Solary, F. Martin, E. Katsanis, and B. Bonnotte. 2006. Apoptotic, necrotic, or fused tumor cells: an equivalent source of antigen for dendritic cell loading. Apoptosis 11: 1513-1524.
33. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176: 1693-1702.
34. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rössner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92.
35. Vremec, D., J. Pooley, H. Hochrein, L. Wu, and K. Shortman. 2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164: 2978-2986. (Pubitemid 30148956)
36. Anjuère, F., P. Martín, I. Ferrero, M. L. Fraga, G. M. del Hoyo, N. Wright, and C. Ardavín. 1999. Definition of dendritic cell subpopulations present in the spleen, Peyer's patches, lymph nodes, and skin of the mouse. Blood 93: 590-598.
37. Horuzsko, A., F. Lenfant, D. H. Munn, and A. L. Mellor. 2001. Maturation of antigen-presenting cells is compromised in HLA-G transgenic mice. Int. Immunol. 13: 385-394.
38. Taieb, J., N. Chaput, C. Ménard, L. Apetoh, E. Ullrich, M. Bonmort, M. Péquignot, N. Casares, M. Terme, C. Flament, et al. 2006. A novel dendritic cell subset involved in tumor immunosurveillance. Nat. Med. 12: 214-219.
39. Virág, L., E. Szabó , P. Gergely, and C. Szabó. 2003. Peroxynitrite-induced cytotoxicity: mechanism and opportunities for intervention. Toxicol. Lett. 140-141: 113-124.
40. Trujillo, M., G. Ferrer-Sueta, and R. Radi. 2008. Peroxynitrite detoxification and its biologic implications. Antioxid. Redox Signal. 10: 1607-1620.
41. Babior, B. M. 2000. The NADPH oxidase of endothelial cells. IUBMB Life 50: 267-269.
42. Nagaraj, S., K. Gupta, V. Pisarev, L. Kinarsky, S. Sherman, L. Kang, D. L. Herber, J. Schneck, and D. I. Gabrilovich. 2007. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 13: 828-835.
43. Sanderson, S., and N. Shastri. 1994. LacZ inducible, antigen/MHC-specific T cell hybrids. Int. Immunol. 6: 369-376.
44. Dearman, R. J., M. Cumberbatch, G. Maxwell, D. A. Basketter, and I. Kimber. 2009. Toll-like receptor ligand activation of murine bone marrow-derived dendritic cells. Immunology 126: 475-484.
45. Dowling, D., C. M. Hamilton, and S. M. O'Neill. 2008. A comparative analysis of cytokine responses, cell surface marker expression and MAPKs in DCs matured with LPS compared with a panel of TLR ligands. Cytokine 41: 254-262.
46. Wink, D. A., K. M. Miranda, and M. G. Espey. 2001. Cytotoxicity related to oxidative and nitrosative stress by nitric oxide. Exp. Biol. Med. (Maywood) 226: 621-623.
47. Muijsers, R. B., E. van Den Worm, G. Folkerts, C. J. Beukelman, A. S. Koster, D. S. Postma, and F. P. Nijkamp. 2000. Apocynin inhibits peroxynitrite formation by murine macrophages. Br. J. Pharmacol. 130: 932-936.
48. Liu, Q., C. Zhang, A. Sun, Y. Zheng, L. Wang, and X. Cao. 2009. Tumor-educated CD1 1bhighIalow regulatory dendritic cells suppress T cell response through arginase I. J. Immunol. 182: 6207-6216.