Rationale for the Combination of Dendritic Cell-Based Vaccination Approaches With Chemotherapy Agents

International Review of Cell and Molecular Biology

Volumn 330, Issue , 2017, Pages 115-156

  Truxova, I ^a,b   Hensler, M ^b   Skapa, P ^a   Halaska, M J ^c   Laco, J ^d   Ryska, A ^d   Spisek, R ^a,b   Fucikova, J ^a,b  

^a UNIVERSITY HOSPITAL MOTOL   (Czech Republic)

^b Sotio   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

^d UNIVERSITY HOSPITAL HRADEC KRALOVE   (Czech Republic)

Author keywords

Chemotherapy; Damage associated molecular patterns; Dendritic cell; Immunogenic cell death; Immunotherapy

Indexed keywords

ANTINEOPLASTIC AGENT; BLEOMYCIN; BORTEZOMIB; CYCLOPHOSPHAMIDE; CYTOTOXIC AGENT; DOXORUBICIN; EPIRUBICIN; IDARUBICIN; MITOXANTRONE; OXALIPLATIN; CANCER VACCINE;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER PATIENT; CELL ACTIVATION; CELL DEATH; CELL FUNCTION; COLORECTAL CANCER; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; HUMAN; MELANOMA; MESOTHELIOMA; MULTIPLE MYELOMA; MYELOID-DERIVED SUPPRESSOR CELL; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PROSTATE CANCER; REGULATORY T LYMPHOCYTE; STOMACH CANCER; TUMOR CELL; TUMOR IMMUNOGENICITY; VACCINATION; ANIMAL; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; IMMUNOTHERAPY;

ANIMALS; ANTINEOPLASTIC AGENTS; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; DENDRITIC CELLS; HUMANS; IMMUNOTHERAPY; VACCINATION;

EID: 85007402071     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ircmb.2016.09.003     Document Type: Chapter

References (121)

1. Adams, J., The proteasome: a suitable antineoplastic target. Nat. Rev. Cancer 4 (2004), 349–360.
2. Anguille, S., Smits, E.L., Lion, E., Van Tendeloo, V.F., Berneman, Z.N., Clinical use of dendritic cells for cancer therapy. Lancet Oncol. 15 (2014), E257–E267.
3. Apetoh, L., Ghiringhelli, F., Tesniere, A., Criollo, A., Ortiz, C., Lidereau, R., Mariette, C., Chaput, N., Mira, J.P., Delaloge, S., Andre, F., Tursz, T., Kroemer, G., Zitvogel, L., The interaction between Hmgb1 and Tlr4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol. Rev. 220 (2007), 47–59.
4. Apetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., Mignot, G., Maiuri, M.C., Ullrich, E., Saulnier, P., Yang, H., Amigorena, S., Ryffel, B., Barrat, F.J., Saftig, P., Levi, F., Lidereau, R., Nogues, C., Mira, J.P., Chompret, A., Joulin, V., Clavel-Chapelon, F., Bourhis, J., Andre, F., Delaloge, S., Tursz, T., Kroemer, G., Zitvogel, L., Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13 (2007), 1050–1059.
5. Asea, A., Kraeft, S.K., Kurt-Jones, E.A., Stevenson, M.A., Chen, L.B., Finberg, R.W., Koo, G.C., Calderwood, S.K., Hsp70 stimulates cytokine production through a Cd14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6 (2000), 435–442.
6. Asea, A., Rehli, M., Kabingu, E., Boch, J.A., Bare, O., Auron, P.E., Stevenson, M.A., Calderwood, S.K., Novel signal transduction pathway utilized by extracellular Hsp70: role of toll-like receptor (Tlr) 2 and Tlr4. J. Biol. Chem. 277 (2002), 15028–15034.
7. Bezu, L., Gomes-De-Silva, L.C., Dewitte, H., Breckpot, K., Fucikova, J., Spisek, R., Galluzzi, L., Kepp, O., Kroemer, G., Combinatorial strategies for the induction of immunogenic cell death. Front. Immunol., 6, 2015, 187.
8. Boczkowski, D., Nair, S.K., Nam, J.H., Lyerly, H.K., Gilboa, E., Induction of tumor immunity and cytotoxic T lymphocyte responses using dendritic cells transfected with messenger Rna amplified from tumor cells. Cancer Res. 60 (2000), 1028–1034.
9. Brusa, D., Garetto, S., Chiorino, G., Scatolini, M., Migliore, E., Camussi, G., Matera, L., Post-apoptotic tumors are more palatable to dendritic cells and enhance their antigen cross-presentation activity. Vaccine 26 (2008), 6422–6432.
10. Bugaut, H., Bruchard, M., Berger, H., Derangere, V., Odoul, L., Euvrard, R., Ladoire, S., Chalmin, F., Vegran, F., Rebe, C., Apetoh, L., Ghiringhelli, F., Mignot, G., Bleomycin exerts ambivalent antitumor immune effect by triggering both immunogenic cell death and proliferation of regulatory T cells. Plos One, 8, 2013, E65181.
11. Calderwood, S.K., Mambula, S.S., Gray, P.J. Jr., Extracellular heat shock proteins in cell signaling and immunity. Ann. N. Y. Acad. Sci. 1113 (2007), 28–39.
12. Cao, J.X., Zhang, X.Y., Liu, J.L., Li, D., Li, J.L., Liu, Y.S., Wang, M., Xu, B.L., Wang, H.B., Wang, Z.X., Clinical efficacy of tumor antigen-pulsed Dc treatment for high-grade glioma patients: evidence from a meta-analysis. Plos One, 9, 2014, E107173.
13. Carreno, B.M., Magrini, V., Becker-Hapak, M., Kaabinejadian, S., Hundal, J., Petti, A.A., Ly, A., Lie, W.R., Hildebrand, W.H., Mardis, E.R., Linette, G.P., Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 348 (2015), 803–808.
14. Casares, N., Pequignot, M.O., Tesniere, A., Ghiringhelli, F., Roux, S., Chaput, N., Schmitt, E., Hamai, A., Hervas-Stubbs, S., Obeid, M., Coutant, F., Metivier, D., Pichard, E., Aucouturier, P., Pierron, G., Garrido, C., Zitvogel, L., Kroemer, G., Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J. Exp. Med. 202 (2005), 1691–1701.
15. Chang, C.L., Hsu, Y.T., Wu, C.C., Yang, Y.C., Wang, C., Wu, T.C., Hung, C.F., Immune mechanism of the antitumor effects generated by bortezomib. J. Immunol. 189 (2012), 3209–3220.
16. Chen, G., Ward, M.F., Sama, A.E., Wang, H., Extracellular Hmgb1 as a proinflammatory cytokine. J. Interferon Cytokine Res. 24 (2004), 329–333.
17. Chen, D., Frezza, M., Schmitt, S., Kanwar, J., Dou, Q.P., Bortezomib as the first proteasome inhibitor anticancer drug: current status and future perspectives. Curr. Cancer Drug Targets 11 (2011), 239–253.
18. Chiappori, A.A., Soliman, H., Janssen, W.E., Antonia, S.J., Gabrilovich, D.I., Ingn-225: a dendritic cell-based P53 vaccine (Ad.P53-Dc) in small cell lung cancer: observed association between immune response and enhanced chemotherapy effect. Expert Opin. Biol. Ther. 10 (2010), 983–991.
19. Chu, C.S., Boyer, J., Schullery, D.S., Gimotty, P.A., Gamerman, V., Bender, J., Levine, B.L., Coukos, G., Rubin, S.C., Morgan, M.A., Vonderheide, R.H., June, C.H., Phase I/II randomized trial of dendritic cell vaccination with or without cyclophosphamide for consolidation therapy of advanced ovarian cancer in first or second remission. Cancer Immunol. Immunother. 61 (2012), 629–641.
20. Cirone, M., Di Renzo, L., Lotti, L.V., Conte, V., Trivedi, P., Santarelli, R., Gonnella, R., Frati, L., Faggioni, A., Primary effusion lymphoma cell death induced by bortezomib and Ag 490 activates dendritic cells through Cd91. Plos One, 7, 2012, E31732.
21. Curti, A., Ferri, E., Pandolfi, S., Isidori, A., Lemoli, R.M., Dendritic cell differentiation. J. Immunol., 172, 2004, 3 Author Reply 3–4.
22. Czerniecki, B.J., Koski, G.K., Koldovsky, U., Xu, S., Cohen, P.A., Mick, R., Nisenbaum, H., Pasha, T., Xu, M., Fox, K.R., Weinstein, S., Orel, S.G., Vonderheide, R., Coukos, G., Demichele, A., Araujo, L., Spitz, F.R., Rosen, M., Levine, B.L., June, C., Zhang, P.J., Targeting Her-2/Neu in early breast cancer development using dendritic cells with staged interleukin-12 burst secretion. Cancer Res. 67 (2007), 1842–1852.
23. Daurkin, I., Eruslanov, E., Vieweg, J., Kusmartsev, S., Generation of antigen-presenting cells from tumor-infiltrated Cd11b myeloid cells with Dna demethylating agent 5-Aza-2′-deoxycytidine. Cancer Immunol. Immunother. 59 (2010), 697–706.
24. De Visser, K.E., Eichten, A., Coussens, L.M., Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 6 (2006), 24–37.
25. Delamarre, L., Holcombe, H., Mellman, I., Presentation of exogenous antigens on major histocompatibility complex (Mhc) class I and Mhc class II molecules is differentially regulated during dendritic cell maturation. J. Exp. Med. 198 (2003), 111–122.
26. Demaria, S., Santori, F.R., Ng, B., Liebes, L., Formenti, S.C., Vukmanovic, S., Select forms of tumor cell apoptosis induce dendritic cell maturation. J. Leukoc. Biol. 77 (2005), 361–368.
27. Di Francesco, A.M., Ruggiero, A., Riccardi, R., Cellular and molecular aspects of drugs of the future: oxaliplatin. Cell. Mol. Life Sci. 59 (2002), 1914–1927.
28. Doody, A.D., Kovalchin, J.T., Mihalyo, M.A., Hagymasi, A.T., Drake, C.G., Adler, A.J., Glycoprotein 96 can chaperone both Mhc class I- and class II-restricted epitopes for in vivo presentation, but selectively primes Cd8 + T cell effector function. J. Immunol. 172 (2004), 6087–6092.
29. Draube, A., Klein-Gonzalez, N., Mattheus, S., Brillant, C., Hellmich, M., Engert, A., Von Bergwelt-Baildon, M., Dendritic cell based tumor vaccination in prostate and renal cell cancer: a systematic review and meta-analysis. Plos One, 6, 2011, E18801.
30. Dumitriu, I.E., Bianchi, M.E., Bacci, M., Manfredi, A.A., Rovere-Querini, P., The secretion of Hmgb1 is required for the migration of maturing dendritic cells. J. Leukoc. Biol. 81 (2007), 84–91.
31. Dunn, G.P., Old, L.J., Schreiber, R.D., The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21 (2004), 137–148.
32. Ellebaek, E., Engell-Noerregaard, L., Iversen, T.Z., Froesig, T.M., Munir, S., Hadrup, S.R., Andersen, M.H., Svane, I.M., Metastatic melanoma patients treated with dendritic cell vaccination, interleukin-2 and metronomic cyclophosphamide: results from a phase II trial. Cancer Immunol. Immunother. 61 (2012), 1791–1804.
33. Elliott, M.R., Chekeni, F.B., Trampont, P.C., Lazarowski, E.R., Kadl, A., Walk, S.F., Park, D., Woodson, R.I., Ostankovich, M., Sharma, P., Lysiak, J.J., Harden, T.K., Leitinger, N., Ravichandran, K.S., Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461 (2009), 282–286.
34. Finn, O.J., Immuno-oncology: understanding the function and dysfunction of the immune system in cancer. Ann. Oncol. 23:Suppl. 8 (2012), Viii6–Viii9.
35. Fucikova, J., Kralikova, P., Fialova, A., Brtnicky, T., Rob, L., Bartunkova, J., Spisek, R., Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res. 71 (2011), 4821–4833.
36. Fucikova, J., Moserova, I., Truxova, I., Hermanova, I., Vancurova, I., Partlova, S., Fialova, A., Sojka, L., Cartron, P.F., Houska, M., Rob, L., Bartunkova, J., Spisek, R., High hydrostatic pressure induces immunogenic cell death in human tumor cells. Int. J. Cancer 135 (2014), 1165–1177.
37. Fucikova, J., Moserova, I., Urbanova, L., Bezu, L., Kepp, O., Cremer, I., Salek, C., Strnad, P., Kroemer, G., Galluzzi, L., Spisek, R., Prognostic and predictive value of damps and damp-associated processes in cancer. Front. Immunol., 6, 2015, 402.
38. Fucikova, J., Becht, E., Iribarren, K., Goc, J., Remark, R., Damotte, D., Alifano, M., Devi, P., Biton, J., Germain, C., Lupo, A., Fridman, W.H., Dieu-Nosjean, M.C., Kroemer, G., Sautes-Fridman, C., Cremer, I., Calreticulin expression in human non-small cell lung cancers correlates with increased accumulation of antitumor immune cells and favorable prognosis. Cancer Res. 76:7 (2016), 1746–1756.
39. Gabrilovich, D.I., Nagaraj, S., Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9 (2009), 162–174.
40. Galluzzi, L., Senovilla, L., Zitvogel, L., Kroemer, G., The secret ally: immunostimulation by anticancer drugs. Nat. Rev. Drug Discov. 11 (2012), 215–233.
41. Galluzzi, L., Kepp, O., Kroemer, G., Immunogenic cell death in radiation therapy. Oncoimmunology, 2, 2013, E26536.
42. Galluzzi, L., Vacchelli, E., Bravo-San Pedro, J.M., Buque, A., Senovilla, L., Baracco, E.E., Bloy, N., Castoldi, F., Abastado, J.P., Agostinis, P., Apte, R.N., Aranda, F., Ayyoub, M., Beckhove, P., Blay, J.Y., Bracci, L., Caignard, A., Castelli, C., Cavallo, F., Celis, E., Cerundolo, V., Clayton, A., Colombo, M.P., Coussens, L., Dhodapkar, M.V., Eggermont, A.M., Fearon, D.T., Fridman, W.H., Fucikova, J., Gabrilovich, D.I., Galon, J., Garg, A., Ghiringhelli, F., Giaccone, G., Gilboa, E., Gnjatic, S., Hoos, A., Hosmalin, A., Jager, D., Kalinski, P., Karre, K., Kepp, O., Kiessling, R., Kirkwood, J.M., Klein, E., Knuth, A., Lewis, C.E., Liblau, R., Lotze, M.T., Lugli, E., Mach, J.P., Mattei, F., Mavilio, D., Melero, I., Melief, C.J., Mittendorf, E.A., Moretta, L., Odunsi, A., Okada, H., Palucka, A.K., Peter, M.E., Pienta, K.J., Porgador, A., Prendergast, G.C., Rabinovich, G.A., Restifo, N.P., Rizvi, N., Sautes-Fridman, C., Schreiber, H., Seliger, B., Shiku, H., Silva-Santos, B., Smyth, M.J., Speiser, D.E., Spisek, R., Srivastava, P.K., Talmadge, J.E., Tartour, E., Van Der Burg, S.H., Van Den Eynde, B.J., Vile, R., Wagner, H., Weber, J.S., Whiteside, T.L., Wolchok, J.D., Zitvogel, L., Zou, W., Kroemer, G., Classification of current anticancer immunotherapies. Oncotarget 5 (2014), 12472–12508.
43. Gardai, S.J., Mcphillips, K.A., Frasch, S.C., Janssen, W.J., Starefeldt, A., Murphy-Ullrich, J.E., Bratton, D.L., Oldenborg, P.A., Michalak, M., Henson, P.M., Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of Lrp on the phagocyte. Cell 123 (2005), 321–334.
44. Garg, A.D., Nowis, D., Golab, J., Vandenabeele, P., Krysko, D.V., Agostinis, P., Immunogenic cell death, damps and anticancer therapeutics: an emerging amalgamation. Biochim. Biophys. Acta 1805 (2010), 53–71.
45. Garg, A.D., Krysko, D.V., Vandenabeele, P., Agostinis, P., Hypericin-based photodynamic therapy induces surface exposure of damage-associated molecular patterns like Hsp70 and calreticulin. Cancer Immunol. Immunother. 61 (2012), 215–221.
46. Garg, A.D., Krysko, D.V., Verfaillie, T., Kaczmarek, A., Ferreira, G.B., Marysael, T., Rubio, N., Firczuk, M., Mathieu, C., Roebroek, A.J., Annaert, W., Golab, J., De Witte, P., Vandenabeele, P., Agostinis, P., A novel pathway combining calreticulin exposure and Atp secretion in immunogenic cancer cell death. EMBO J. 31 (2012), 1062–1079.
47. Garg, A.D., Galluzzi, L., Apetoh, L., Baert, T., Birge, R.B., Bravo-San Pedro, J.M., Breckpot, K., Brough, D., Chaurio, R., Cirone, M., Coosemans, A., Coulie, P.G., De Ruysscher, D., Dini, L., De Witte, P., Dudek-Peric, A.M., Faggioni, A., Fucikova, J., Gaipl, U.S., Golab, J., Gougeon, M.L., Hamblin, M.R., Hemminki, A., Herrmann, M., Hodge, J.W., Kepp, O., Kroemer, G., Krysko, D.V., Land, W.G., Madeo, F., Manfredi, A.A., Mattarollo, S.R., Maueroder, C., Merendino, N., Multhoff, G., Pabst, T., Ricci, J.E., Riganti, C., Romano, E., Rufo, N., Smyth, M.J., Sonnemann, J., Spisek, R., Stagg, J., Vacchelli, E., Vandenabeele, P., Vandenberk, L., Van Den Eynde, B.J., Van Gool, S., Velotti, F., Zitvogel, L., Agostinis, P., Molecular and translational classifications of damps in immunogenic cell death. Front. Immunol., 6, 2015, 588.
48. Gebremeskel, S., Johnston, B., Concepts and mechanisms underlying chemotherapy induced immunogenic cell death: impact on clinical studies and considerations for combined therapies. Oncotarget 6 (2015), 41600–41619.
49. Ghiringhelli, F., Menard, C., Puig, P.E., Ladoire, S., Roux, S., Martin, F., Solary, E., Le Cesne, A., Zitvogel, L., Chauffert, B., Metronomic cyclophosphamide regimen selectively depletes Cd4+Cd25 + regulatory T cells and restores T and Nk effector functions in end stage cancer patients. Cancer Immunol. Immunother. 56 (2007), 641–648.
50. Ghiringhelli, F., Apetoh, L., Tesniere, A., Aymeric, L., Ma, Y., Ortiz, C., Vermaelen, K., Panaretakis, T., Mignot, G., Ullrich, E., Perfettini, J.L., Schlemmer, F., Tasdemir, E., Uhl, M., Genin, P., Civas, A., Ryffel, B., Kanellopoulos, J., Tschopp, J., Andre, F., Lidereau, R., Mclaughlin, N.M., Haynes, N.M., Smyth, M.J., Kroemer, G., Zitvogel, L., Activation of the Nlrp3 inflammasome in dendritic cells induces Il-1beta-dependent adaptive immunity against tumors. Nat. Med. 15 (2009), 1170–1178.
51. Hegmans, J.P., Veltman, J.D., Lambers, M.E., De Vries, I.J., Figdor, C.G., Hendriks, R.W., Hoogsteden, H.C., Lambrecht, B.N., Aerts, J.G., Consolidative dendritic cell-based immunotherapy elicits cytotoxicity against malignant mesothelioma. Am. J. Respir. Crit. Care Med. 181 (2010), 1383–1390.
52. Hsu, F.J., Benike, C., Fagnoni, F., Liles, T.M., Czerwinski, D., Taidi, B., Engleman, E.G., Levy, R., Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat. Med. 2 (1996), 52–58.
53. Hu, D.E., Moore, A.M., Thomsen, L.L., Brindle, K.M., Uric acid promotes tumor immune rejection. Cancer Res. 64 (2004), 5059–5062.
54. Jackaman, C., Majewski, D., Fox, S.A., Nowak, A.K., Nelson, D.J., Chemotherapy broadens the range of tumor antigens seen by cytotoxic Cd8(+) T cells in vivo. Cancer Immunol. Immunother. 61 (2012), 2343–2356.
55. Kaneno, R., Shurin, G.V., Tourkova, I.L., Shurin, M.R., Chemomodulation of human dendritic cell function by antineoplastic agents in low noncytotoxic concentrations. J. Transl. Med., 7, 2009, 58.
56. Klechevsky, E., Flamar, A.L., Cao, Y., Blanck, J.P., Liu, M., O'bar, A., Agouna-Deciat, O., Klucar, P., Thompson-Snipes, L., Zurawski, S., Reiter, Y., Palucka, A.K., Zurawski, G., Banchereau, J., Cross-priming Cd8 + T cells by targeting antigens to human dendritic cells through DCIR. Blood 116 (2010), 1685–1697.
57. Kovarova, L., Buchler, T., Pour, L., Zahradova, L., Ocadlikova, D., Svobodnik, A., Penka, M., Vorlicek, J., Hajek, R., Dendritic cell counts and their subsets during treatment of multiple myeloma. Neoplasma 54 (2007), 297–303.
58. Krishnadas, D.K., Shusterman, S., Bai, F., Diller, L., Sullivan, J.E., Cheerva, A.C., George, R.E., Lucas, K.G., A phase I trial combining decitabine/dendritic cell vaccine targeting mage-A1, mage-A3 and Ny-Eso-1 for children with relapsed or therapy-refractory neuroblastoma and sarcoma. Cancer Immunol. Immunother. 64 (2015), 1251–1260.
59. Kroemer, G., Galluzzi, L., Kepp, O., Zitvogel, L., Immunogenic cell death in cancer therapy. Annu. Rev. Immunol. 31 (2013), 51–72.
60. Krysko, D.V., Garg, A.D., Kaczmarek, A., Krysko, O., Agostinis, P., Vandenabeele, P., Immunogenic cell death and damps in cancer therapy. Nat. Rev. Cancer 12 (2012), 860–875.
61. Krysko, O., Love Aaes, T., Bachert, C., Vandenabeele, P., Krysko, D.V., Many faces of damps in cancer therapy. Cell Death Dis., 4, 2013, E631.
62. Lennon-Dumenil, A.M., Bakker, A.H., Wolf-Bryant, P., Ploegh, H.L., Lagaudriere-Gesbert, C., A closer look at proteolysis and MHC-class-II-restricted antigen presentation. Curr. Opin. Immunol. 14 (2002), 15–21.
63. Lesterhuis, W.J., De Vries, I.J., Aarntzen, E.A., De Boer, A., Scharenborg, N.M., Van De Rakt, M., Van Spronsen, D.J., Preijers, F.W., Figdor, C.G., Adema, G.J., Punt, C.J., A pilot study on the immunogenicity of dendritic cell vaccination during adjuvant oxaliplatin/capecitabine chemotherapy in colon cancer patients. Br. J. Cancer 103 (2010), 1415–1421.
64. Lesterhuis, W.J., Punt, C.J., Hato, S.V., Eleveld-Trancikova, D., Jansen, B.J., Nierkens, S., Schreibelt, G., De Boer, A., Van Herpen, C.M., Kaanders, J.H., Van Krieken, J.H., Adema, G.J., Figdor, C.G., De Vries, I.J., Platinum-based drugs disrupt Stat6-mediated suppression of immune responses against cancer in humans and mice. J. Clin. Invest. 121 (2011), 3100–3108.
65. Linnemann, C., Van Buuren, M.M., Bies, L., Verdegaal, E.M., Schotte, R., Calis, J.J., Behjati, S., Velds, A., Hilkmann, H., Atmioui, D.E., Visser, M., Stratton, M.R., Haanen, J.B., Spits, H., Van Der Burg, S.H., Schumacher, T.N., High-throughput epitope discovery reveals frequent recognition of Neo-antigens by Cd4 + T cells in human melanoma. Nat. Med. 21 (2015), 81–85.
66. Liu, W.M., Fowler, D.W., Smith, P., Dalgleish, A.G., Pre-treatment with chemotherapy can enhance the antigenicity and immunogenicity of tumours by promoting adaptive immune responses. Br. J. Cancer 102 (2010), 115–123.
67. Liu, W.M., Scott, K.A., Thompson, M., Dalgleish, A.G., Dendritic cell phenotype can be improved by certain chemotherapies and is associated with alterations to P21(Waf1/Cip1.). Cancer Immunol. Immunother. 62 (2013), 1553–1561.
68. Ma, Y., Adjemian, S., Mattarollo, S.R., Yamazaki, T., Aymeric, L., Yang, H., Portela Catani, J.P., Hannani, D., Duret, H., Steegh, K., Martins, I., Schlemmer, F., Michaud, M., Kepp, O., Sukkurwala, A.Q., Menger, L., Vacchelli, E., Droin, N., Galluzzi, L., Krzysiek, R., Gordon, S., Taylor, P.R., Van Endert, P., Solary, E., Smyth, M.J., Zitvogel, L., Kroemer, G., Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 38 (2013), 729–741.
69. Ma, Y., Mattarollo, S.R., Adjemian, S., Yang, H., Aymeric, L., Hannani, D., Portela Catani, J.P., Duret, H., Teng, M.W., Kepp, O., Wang, Y., Sistigu, A., Schultze, J.L., Stoll, G., Galluzzi, L., Zitvogel, L., Smyth, M.J., Kroemer, G., Ccl2/Ccr2-dependent recruitment of functional antigen-presenting cells into tumors upon chemotherapy. Cancer Res. 74 (2014), 436–445.
70. Martinon, F., Petrilli, V., Mayor, A., Tardivel, A., Tschopp, J., Gout-associated uric acid crystals activate the Nalp3 inflammasome. Nature 440 (2006), 237–241.
71. Martins, I., Kepp, O., Schlemmer, F., Adjemian, S., Tailler, M., Shen, S., Michaud, M., Menger, L., Gdoura, A., Tajeddine, N., Tesniere, A., Zitvogel, L., Kroemer, G., Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress. Oncogene 30 (2011), 1147–1158.
72. Martins, I., Wang, Y., Michaud, M., Ma, Y., Sukkurwala, A.Q., Shen, S., Kepp, O., Metivier, D., Galluzzi, L., Perfettini, J.L., Zitvogel, L., Kroemer, G., Molecular mechanisms of Atp secretion during immunogenic cell death. Cell Death Differ. 21 (2014), 79–91.
73. Matzinger, P., Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12 (1994), 991–1045.
74. Mikyskova, R., Stepanek, I., Indrova, M., Bieblova, J., Simova, J., Truxova, I., Moserova, I., Fucikova, J., Bartunkova, J., Spisek, R., Reinis, M., Dendritic cells pulsed with tumor cells killed by high hydrostatic pressure induce strong immune responses and display therapeutic effects both in murine Tc-1 and tramp-C2 tumors when combined with docetaxel chemotherapy. Int. J. Oncol. 48 (2016), 953–964.
75. Murshid, A., Gong, J., Calderwood, S.K., Hsp90-peptide complexes stimulate antigen presentation through the class II pathway after binding scavenger receptor srec-I. Immunobiology 219 (2014), 924–931.
76. Nakahara, T., Uchi, H., Lesokhin, A.M., Avogadri, F., Rizzuto, G.A., Hirschhorn-Cymerman, D., Panageas, K.S., Merghoub, T., Wolchok, J.D., Houghton, A.N., Cyclophosphamide enhances immunity by modulating the balance of dendritic cell subsets in lymphoid organs. Blood 115 (2010), 4384–4392.
77. Nakai, N., Hartmann, G., Kishimoto, S., Katoh, N., Dendritic cell vaccination in human melanoma: relationships between clinical effects and vaccine parameters. Pigment Cell Melanoma Res. 23 (2010), 607–619.
78. Nestle, F.O., Alijagic, S., Gilliet, M., Sun, Y., Grabbe, S., Dummer, R., Burg, G., Schadendorf, D., Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 4 (1998), 328–332.
79. Niiya, M., Niiya, K., Kiguchi, T., Shibakura, M., Asaumi, N., Shinagawa, K., Ishimaru, F., Kiura, K., Ikeda, K., Ueoka, H., Tanimoto, M., Induction of Tnf-alpha, Upa, Il-8 and Mcp-1 by doxorubicin in human lung carcinoma cells. Cancer Chemother. Pharmacol. 52 (2003), 391–398.
80. Nowak, A.K., Lake, R.A., Marzo, A.L., Scott, B., Heath, W.R., Collins, E.J., Frelinger, J.A., Robinson, B.W., Induction of tumor cell apoptosis in vivo increases tumor antigen cross-presentation, cross-priming rather than cross-tolerizing host tumor-specific Cd8 T cells. J. Immunol. 170 (2003), 4905–4913.
81. Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G.M., Apetoh, L., Perfettini, J.L., Castedo, M., Mignot, G., Panaretakis, T., Casares, N., Metivier, D., Larochette, N., Van Endert, P., Ciccosanti, F., Piacentini, M., Zitvogel, L., Kroemer, G., Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13 (2007), 54–61.
82. Palucka, K., Banchereau, J., Cancer immunotherapy via dendritic cells. Nat. Rev. Cancer 12 (2012), 265–277.
83. Papewalis, C., Jacobs, B., Wuttke, M., Ullrich, E., Baehring, T., Fenk, R., Willenberg, H.S., Schinner, S., Cohnen, M., Seissler, J., Zacharowski, K., Scherbaum, W.A., Schott, M., Ifn-alpha skews monocytes into Cd56+-expressing dendritic cells with potent functional activities in vitro and in vivo. J. Immunol. 180 (2008), 1462–1470.
84. Pawaria, S., Binder, R.J., Cd91-dependent programming of T-helper cell responses following heat shock protein immunization. Nat. Commun., 2, 2011, 521.
85. Podrazil, M., Horvath, R., Becht, E., Rozkova, D., Bilkova, P., Sochorova, K., Hromadkova, H., Kayserova, J., Vavrova, K., Lastovicka, J., Vrabcova, P., Kubackova, K., Gasova, Z., Jarolim, L., Babjuk, M., Spisek, R., Bartunkova, J., Fucikova, J., Phase I/II clinical trial of dendritic-cell based immunotherapy (dcvac/Pca) combined with chemotherapy in patients with metastatic, castration-resistant prostate cancer. Oncotarget 6 (2015), 18192–18205.
86. Pol, J., Vacchelli, E., Aranda, F., Castoldi, F., Eggermont, A., Cremer, I., Sautes-Fridman, C., Fucikova, J., Galon, J., Spisek, R., Tartour, E., Zitvogel, L., Kroemer, G., Galluzzi, L., Trial watch: immunogenic cell death inducers for anticancer chemotherapy. Oncoimmunology, 4, 2015, E1008866.
87. Rabbani, A., Finn, R.M., Ausio, J., The anthracycline antibiotics: antitumor drugs that alter chromatin structure. Bioessays 27 (2005), 50–56.
88. Schiavoni, G., Sistigu, A., Valentini, M., Mattei, F., Sestili, P., Spadaro, F., Sanchez, M., Lorenzi, S., D'urso, M.T., Belardelli, F., Gabriele, L., Proietti, E., Bracci, L., Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res. 71 (2011), 768–778.
89. Schumacher, L.Y., Vo, D.D., Garban, H.J., Comin-Anduix, B., Owens, S.K., Dissette, V.B., Glaspy, J.A., Mcbride, W.H., Bonavida, B., Economou, J.S., Ribas, A., Immunosensitization of tumor cells to dendritic cell-activated immune responses with the proteasome inhibitor bortezomib (Ps-341, velcade). J. Immunol. 176 (2006), 4757–4765.
90. Senovilla, L., Vacchelli, E., Galon, J., Adjemian, S., Eggermont, A., Fridman, W.H., Sautes-Fridman, C., Ma, Y., Tartour, E., Zitvogel, L., Kroemer, G., Galluzzi, L., Trial watch: prognostic and predictive value of the immune infiltrate in cancer. Oncoimmunology 1 (2012), 1323–1343.
91. Shurin, G.V., Tourkova, I.L., Kaneno, R., Shurin, M.R., Chemotherapeutic agents in noncytotoxic concentrations increase antigen presentation by dendritic cells Via an Il-12-dependent mechanism. J. Immunol. 183 (2009), 137–144.
92. Singh-Jasuja, H., Toes, R.E., Spee, P., Munz, C., Hilf, N., Schoenberger, S.P., Ricciardi-Castagnoli, P., Neefjes, J., Rammensee, H.G., Arnold-Schild, D., Schild, H., Cross-presentation of glycoprotein 96-associated antigens on major histocompatibility complex class I molecules requires receptor-mediated endocytosis. J. Exp. Med. 191 (2000), 1965–1974.
93. Sistigu, A., Viaud, S., Chaput, N., Bracci, L., Proietti, E., Zitvogel, L., Immunomodulatory effects of cyclophosphamide and implementations for vaccine design. Semin. Immunopathol. 33 (2011), 369–383.
94. Sistigu, A., Yamazaki, T., Vacchelli, E., Chaba, K., Enot, D.P., Adam, J., Vitale, I., Goubar, A., Baracco, E.E., Remedios, C., Fend, L., Hannani, D., Aymeric, L., Ma, Y., Niso-Santano, M., Kepp, O., Schultze, J.L., Tuting, T., Belardelli, F., Bracci, L., La Sorsa, V., Ziccheddu, G., Sestili, P., Urbani, F., Delorenzi, M., Lacroix-Triki, M., Quidville, V., Conforti, R., Spano, J.P., Pusztai, L., Poirier-Colame, V., Delaloge, S., Penault-Llorca, F., Ladoire, S., Arnould, L., Cyrta, J., Dessoliers, M.C., Eggermont, A., Bianchi, M.E., Pittet, M., Engblom, C., Pfirschke, C., Preville, X., Uze, G., Schreiber, R.D., Chow, M.T., Smyth, M.J., Proietti, E., Andre, F., Kroemer, G., Zitvogel, L., Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat. Med. 20 (2014), 1301–1309.
95. Soeda, A., Morita-Hoshi, Y., Makiyama, H., Morizane, C., Ueno, H., Ikeda, M., Okusaka, T., Yamagata, S., Takahashi, N., Hyodo, I., Takaue, Y., Heike, Y., Regular dose of gemcitabine induces an increase in Cd14 + monocytes and Cd11c + dendritic cells in patients with advanced pancreatic cancer. Jpn. J. Clin. Oncol. 39 (2009), 797–806.
96. Spisek, R., Charalambous, A., Mazumder, A., Vesole, D.H., Jagannath, S., Dhodapkar, M.V., 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 (2007), 4839–4845.
97. Steinman, R.M., Turley, S., Mellman, I., Inaba, K., The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191 (2000), 411–416.
98. Stockwin, L.H., Mcgonagle, D., Martin, I.G., Blair, G.E., Dendritic cells: immunological sentinels with a central role in health and disease. Immunol. Cell Biol. 78 (2000), 91–102.
99. Stojanovska, V., Sakkal, S., Nurgali, K., Platinum-based chemotherapy: gastrointestinal immunomodulation and enteric nervous system toxicity. Am. J. Physiol. Gastrointest. Liver Physiol. 308 (2015), G223–G232.
100. Svane, I.M., Pedersen, A.E., Johansen, J.S., Johnsen, H.E., Nielsen, D., Kamby, C., Ottesen, S., Balslev, E., Gaarsdal, E., Nikolajsen, K., Claesson, M.H., Vaccination with P53 peptide-pulsed dendritic cells is associated with disease stabilization in patients with P53 expressing advanced breast cancer; monitoring of serum Ykl-40 and Il-6 as response biomarkers. Cancer Immunol. Immunother. 56 (2007), 1485–1499.
101. Tanaka, H., Matsushima, H., Mizumoto, N., Takashima, A., Classification of chemotherapeutic agents based on their differential in vitro effects on dendritic cells. Cancer Res. 69 (2009), 6978–6986.
102. Tanaka, H., Matsushima, H., Nishibu, A., Clausen, B.E., Takashima, A., Dual therapeutic efficacy of vinblastine as a unique chemotherapeutic agent capable of inducing dendritic cell maturation. Cancer Res. 69 (2009), 6987–6994.
103. Tesniere, A., Panaretakis, T., Kepp, O., Apetoh, L., Ghiringhelli, F., Zitvogel, L., Kroemer, G., Molecular characteristics of immunogenic cancer cell death. Cell Death Differ. 15 (2008), 3–12.
104. Tesniere, A., Schlemmer, F., Boige, V., Kepp, O., Martins, I., Ghiringhelli, F., Aymeric, L., Michaud, M., Apetoh, L., Barault, L., Mendiboure, J., Pignon, J.P., Jooste, V., Van Endert, P., Ducreux, M., Zitvogel, L., Piard, F., Kroemer, G., Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 29 (2010), 482–491.
105. Udono, H., Srivastava, P.K., Comparison of tumor-specific immunogenicities of stress-induced proteins Gp96, Hsp90, and Hsp70. J. Immunol. 152 (1994), 5398–5403.
106. Vacchelli, E., Eggermont, A., Sautes-Fridman, C., Galon, J., Zitvogel, L., Kroemer, G., Galluzzi, L., Trial watch: oncolytic viruses for cancer therapy. Oncoimmunology, 2, 2013, E24612.
107. Vacchelli, E., Vitale, I., Eggermont, A., Fridman, W.H., Fucikova, J., Cremer, I., Galon, J., Tartour, E., Zitvogel, L., Kroemer, G., Galluzzi, L., Trial watch: dendritic cell-based interventions for cancer therapy. Oncoimmunology, 2, 2013, E25771.
108. Vacchelli, E., Ma, Y., Baracco, E.E., Sistigu, A., Enot, D.P., Pietrocola, F., Yang, H., Adjemian, S., Chaba, K., Semeraro, M., Signore, M., De Ninno, A., Lucarini, V., Peschiaroli, F., Businaro, L., Gerardino, A., Manic, G., Ulas, T., Gunther, P., Schultze, J.L., Kepp, O., Stoll, G., Lefebvre, C., Mulot, C., Castoldi, F., Rusakiewicz, S., Ladoire, S., Apetoh, L., Bravo-San Pedro, J.M., Lucattelli, M., Delarasse, C., Boige, V., Ducreux, M., Delaloge, S., Borg, C., Andre, F., Schiavoni, G., Vitale, I., Laurent-Puig, P., Mattei, F., Zitvogel, L., Kroemer, G., Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1. Science 350 (2015), 972–978.
109. Van Eden, W., Spiering, R., Broere, F., Van Der Zee, R., A case of mistaken identity: HSPs are no DAMPs but dampers. Cell Stress Chaperones 17 (2012), 281–292.
110. Vandenabeele, P., Galluzzi, L., Vanden Berghe, T., Kroemer, G., Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11 (2010), 700–714.
111. Viaud, S., Thery, C., Ploix, S., Tursz, T., Lapierre, V., Lantz, O., Zitvogel, L., Chaput, N., Dendritic cell-derived exosomes for cancer immunotherapy: what's next?. Cancer Res. 70 (2010), 1281–1285.
112. Vincent, J., Mignot, G., Chalmin, F., Ladoire, S., Bruchard, M., Chevriaux, A., Martin, F., Apetoh, L., Rebe, C., Ghiringhelli, F., 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 70 (2010), 3052–3061.
113. Wang, Y., Ma, X., Su, C., Peng, B., Du, J., Jia, H., Luo, M., Fang, C., Wei, Y., Uric acid enhances the antitumor immunity of dendritic cell-based vaccine. Sci. Rep., 5, 2015, 16427.
114. Yi, Q., Szmania, S., Freeman, J., Qian, J., Rosen, N.A., Viswamitra, S., Cottler-Fox, M., Barlogie, B., Tricot, G., Van Rhee, F., Optimizing dendritic cell-based immunotherapy in multiple myeloma: intranodal injections of idiotype-pulsed Cd40 ligand-matured vaccines led to induction of type-1 and cytotoxic T-cell immune responses in patients. Br. J. Haematol. 150 (2010), 554–564.
115. Zhang, Z., Yu, X., Wang, Z., Wu, P., Huang, J., Anthracyclines potentiate anti-tumor immunity: a new opportunity for chemoimmunotherapy. Cancer Lett. 369 (2015), 331–335.
116. Zhao, M., Li, H., Li, L., Zhang, Y., Effects of a gemcitabine plus platinum regimen combined with a dendritic cell-cytokine induced killer immunotherapy on recurrence and survival rate of non-small cell lung cancer patients. Exp. Ther. Med. 7 (2014), 1403–1407.
117. Ziccheddu, G., Proietti, E., Moschella, F., The janus face of cyclophosphamide: a sterile inflammatory response that potentiates cancer immunotherapy. Oncoimmunology, 2, 2013, E25789.
118. Zitvogel, L., Apetoh, L., Ghiringhelli, F., Kroemer, G., Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 8 (2008), 59–73.
119. Zitvogel, L., Kepp, O., Kroemer, G., Decoding cell death signals in inflammation and immunity. Cell 140 (2010), 798–804.
120. Zitvogel, L., Galluzzi, L., Smyth, M.J., Kroemer, G., Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 39 (2013), 74–88.
121. Zitvogel, L., Galluzzi, L., Kepp, O., Smyth, M.J., Kroemer, G., Type I interferons in anticancer immunity. Nat. Rev. Immunol. 15 (2015), 405–414.