Dendritic cell-based cancer vaccination: quo vadis?

References

• Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu. Rev. Immunol.22, 329–360 (2004).
   PubMed Web of Science ®Google Scholar
• Dhodapkar MV, Krasovsky J, Osman K, Geller MD. Vigorous premalignancy-specific effector T cell response in the bone marrow of patients with monoclonal gammopathy. J. Exp. Med.198(11), 1753–1757 (2003).
   PubMed Web of Science ®Google Scholar
• Galon J, Costes A, Sanchez-Cabo F et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science313(5795), 1960–1964 (2006).
   PubMed Web of Science ®Google Scholar
• Schuler G, Schuler-Thurner B, Steinman RM. The use of dendritic cells in cancer immunotherapy. Curr. Opin. Immunol.15(2), 138–147 (2003).
   PubMed Web of Science ®Google Scholar
• Cerundolo V, Hermans IF, Salio M. Dendritic cells: a journey from laboratory to clinic. Nat. Immunol.5(1), 7–10 (2004).
   PubMed Web of Science ®Google Scholar
• Pulendran B, Banchereau J, Burkeholder S et al. Flt3-ligand and granulocyte colony-stimulating factor mobilize distinct human dendritic cell subsets in vivo. J. Immunol.165(1), 566–572 (2000).
   PubMed Web of Science ®Google Scholar
• Caux C, Dezutter-Dambuyant C, Schmitt D, Banchereau J. GM-CSF and TNF-α cooperate in the generation of dendritic Langerhans cells. Nature360(6401), 258–261 (1992).
   PubMed Web of Science ®Google Scholar
• Feuerstein B, Berger TG, Maczek C et al. A method for the production of cryopreserved aliquots of antigen-preloaded, mature dendritic cells ready for clinical use. J. Immunol. Methods245(1–2), 15–29 (2000).
   PubMed Web of Science ®Google Scholar
• Tuyaerts S, Aerts JL, Corthals J et al. Current approaches in dendritic cell generation and future implications for cancer immunotherapy. Cancer Immunol. Immunother.56(10), 1513–1537 (2007).
   PubMed Web of Science ®Google Scholar
• de Vries IJ, Lesterhuis WJ, Scharenborg NM et al. Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients. Clin. Cancer Res.9(14), 5091–5100 (2003).
   PubMed Web of Science ®Google Scholar
• Jonuleit H, Kuhn U, Muller G et al. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur. J. Immunol.27(12), 3135–3142 (1997).
   PubMed Web of Science ®Google Scholar
• Czerniecki BJ, Carter C, Rivoltini L et al. Calcium ionophore-treated peripheral blood monocytes and dendritic cells rapidly display characteristics of activated dendritic cells. J. Immunol.159(8), 3823–3837 (1997).
   PubMedGoogle Scholar
• Koski GK, Schwartz GN, Weng DE et al. Calcium mobilization in human myeloid cells results in acquisition of individual dendritic cell-like characteristics through discrete signaling pathways. J. Immunol.163(1), 82–92 (1999).
   Google Scholar
• Bedrosian I, Mick R, Xu S et al. Intranodal administration of peptide-pulsed mature dendritic cell vaccines results in superior CD8+ T-cell function in melanoma patients. J. Clin. Oncol.21(20), 3826–3835 (2003).
   PubMed Web of Science ®Google Scholar
• Dauer M, Obermaier B, Herten J et al. Mature dendritic cells derived from human monocytes within 48 hours: a novel strategy for dendritic cell differentiation from blood precursors. J. Immunol.170(8), 4069–4076 (2003).
   PubMed Web of Science ®Google Scholar
• Santini SM, Lapenta C, Logozzi M et al. Type I interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J. Exp. Med.191(10), 1777–1788 (2000).
   PubMed Web of Science ®Google Scholar
• Dauer M, Schad K, Herten J et al.FastDC derived from human monocytes within 48 h effectively prime tumor antigen-specific cytotoxic T cells. J. Immunol. Methods302(1–2), 145–155 (2005).
   Google Scholar
• Dauer M, Schad K, Junkmann J et al. IFN-α promotes definitive maturation of dendritic cells generated by short-term culture of monocytes with GM-CSF and IL-4. J. Leukoc. Biol.80(2), 278–286 (2006).
   Google Scholar
• Jarnjak-Jankovic S, Hammerstad H, Saeboe-Larssen S, Kvalheim G, Gaudernack G. A full scale comparative study of methods for generation of functional dendritic cells for use as cancer vaccines. BMC Cancer7, 119 (2007).
   PubMed Web of Science ®Google Scholar
• Xu S, Koski GK, Faries M et al. Rapid high efficiency sensitization of CD8+ T cells to tumor antigens by dendritic cells leads to enhanced functional avidity and direct tumor recognition through an IL-12-dependent mechanism. J. Immunol.171(5), 2251–2261 (2003).
   PubMed Web of Science ®Google Scholar
• Smith CM, Wilson NS, Waithman J et al. Cognate CD4+ T cell licensing of dendritic cells in CD8+ T cell immunity. Nat. Immunol.5(11), 1143–1148 (2004).
   PubMed Web of Science ®Google Scholar
• Kalinski P, Vieira PL, Schuitemaker JH, de Jong EC, Kapsenberg ML. Prostaglandin E2 is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood97(11), 3466–3469 (2001).
   PubMed Web of Science ®Google Scholar
• Schadendorf D, Ugurel S, Schuler-Thurner B et al. Dacarbazine (DTIC) versus vaccination with autologous peptide-pulsed dendritic cells (DC) in first-line treatment of patients with metastatic melanoma: a randomized Phase III trial of the DC study group of the DeCOG. Annu. Oncol.17(4), 563–570 (2006).
   PubMed Web of Science ®Google Scholar
• Mailliard RB, Wankowicz-Kalinska A, Cai Q et al. α-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res.64(17), 5934–5937 (2004).
   PubMed Web of Science ®Google Scholar
• Wesa A, Kalinski P, Kirkwood JM, Tatsumi T, Storkus WJ. Polarized type-1 dendritic cells (DC1) producing high levels of IL-12 family members rescue patient Th1-type antimelanoma CD4+ T cell responses in vitro. J. Immunother.30(1), 75–82 (2007).
   PubMed Web of Science ®Google Scholar
• Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol.6(8), 769–776 (2005).
   PubMed Web of Science ®Google Scholar
• Bonehill A, Tuyaerts S, Van Nuffel AM et al. Enhancing the T-cell stimulatory capacity of human dendritic cells by co-electroporation with CD40L, CD70 and constitutively active TLR4 encoding mRNA. Mol. Ther.16(6), 1170–1180 (2008).
   PubMed Web of Science ®Google Scholar
• Czerniecki BJ, Koski GK, Koldovsky U et al. Targeting HER-2/neu in early breast cancer development using dendritic cells with staged interleukin-12 burst secretion. Cancer Res.67(4), 1842–1852 (2007).
   PubMed Web of Science ®Google Scholar
• Peng JC, Hyde C, Pai S et al. Monocyte-derived DC primed with TLR agonists secrete IL-12p70 in a CD40-dependent manner under hyperthermic conditions. J. Immunother.29(6), 606–615 (2006).
   PubMed Web of Science ®Google Scholar
• Luft T, Jefford M, Luetjens P et al. Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E2 regulates the migratory capacity of specific DC subsets. Blood100(4), 1362–1372 (2002).
   PubMed Web of Science ®Google Scholar
• Haenssle H, Buhl T, Knudsen S et al. CD40 ligation during dendritic cell maturation reduces cell death and prevents interleukin-10-induced regression to macrophage-like monocytes. Exp. Dermatol.17(3), 177–187 (2008).
   Google Scholar
• Schnurr M, Toy T, Shin A et al. Extracellular nucleotide signaling by P2 receptors inhibits IL-12 and enhances IL-23 expression in human dendritic cells: a novel role for the cAMP pathway. Blood105(4), 1582–1589 (2005).
   PubMed Web of Science ®Google Scholar
• Braun D, Longman RS, Albert ML. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood106(7), 2375–2381 (2005).
   PubMed Web of Science ®Google Scholar
• Banerjee DK, Dhodapkar MV, Matayeva E, Steinman RM, Dhodapkar KM. Expansion of FOXP3 high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood108(8), 2655–2661 (2006).
   PubMed Web of Science ®Google Scholar
• Wobser M, Voigt H, Houben R et al. Dendritic cell based antitumor vaccination: impact of functional indoleamine 2,3-dioxygenase expression. Cancer Immunol. Immunother.56(7), 1017–1024 (2007).
   PubMed Web of Science ®Google Scholar
• Krause P, Singer E, Darley PI et al. Prostaglandin E2 is a key factor for monocyte-derived dendritic cell maturation: enhanced T cell stimulatory capacity despite IDO. J. Leukoc. Biol.82(5), 1106–1114 (2007).
   Google Scholar
• von Bergwelt-Baildon MS, Popov A, Saric T et al. CD25 and indoleamine 2,3-dioxygenase are up-regulated by prostaglandin E2 and expressed by tumor-associated dendritic cells in vivo: additional mechanisms of T-cell inhibition. Blood108(1), 228–237 (2006).
   PubMed Web of Science ®Google Scholar
• Terness P, Chuang JJ, Bauer T, Jiga L, Opelz G. Regulation of human auto- and alloreactive T cells by indoleamine 2,3-dioxygenase (IDO)-producing dendritic cells: too much ado about IDO? Blood105(6), 2480–2486 (2005).
   PubMed Web of Science ®Google Scholar
• Zobywalski A, Javorovic M, Frankenberger B et al. Generation of clinical grade dendritic cells with capacity to produce biologically active IL-12p70. J. Transl. Med.5, 18 (2007).
   PubMed Web of Science ®Google Scholar
• Boullart AC, Aarntzen EH, Verdijk P et al. 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. DOI: 10.1007/s00262-008-0489-2 (2008) (Epub ahead of print).
   Google Scholar
• Dauer M, Lam V, Arnold H et al. Combined use of Toll-like receptor agonists and prostaglandin E2 in the FastDC model: rapid generation of human monocyte-derived dendritic cells capable of migration and IL-12p70 production. J. Immunol. Methods337(2) 97–105 (2008).
   PubMed Web of Science ®Google Scholar
• Furset G, Floisand Y, Sioud M. Impaired expression of indoleamine 2,3-dioxygenase in monocyte-derived dendritic cells in response to Toll-like receptor-7/8 ligands. Immunology123(2), 263–271 (2008).
   PubMed Web of Science ®Google Scholar
• Schnurr M, Chen Q, Shin A et al. Tumor antigen processing and presentation depend critically on dendritic cell type and the mode of antigen delivery. Blood105(6), 2465–2472 (2005).
   PubMed Web of Science ®Google Scholar
• Schnurr M, Galambos P, Scholz C et al. Tumor cell lysate-pulsed human dendritic cells induce a T-cell response against pancreatic carcinoma cells: an in vitro model for the assessment of tumor vaccines. Cancer Res.61(17), 6445–6450 (2001).
   PubMed Web of Science ®Google Scholar
• Shimizu K, Kuriyama H, Kjaergaard J et al. Comparative analysis of antigen loading strategies of dendritic cells for tumor immunotherapy. J. Immunother.27(4), 265–272 (2004).
   PubMed Web of Science ®Google Scholar
• Parkhurst MR, DePan C, Riley JP, Rosenberg SA, Shu S. Hybrids of dendritic cells and tumor cells generated by electrofusion simultaneously present immunodominant epitopes from multiple human tumor-associated antigens in the context of MHC class I and class II molecules. J. Immunol.170(10), 5317–5325 (2003).
   PubMed Web of Science ®Google Scholar
• Nair SK, Heiser A, Boczkowski D et al. Induction of cytotoxic T cell responses and tumor immunity against unrelated tumors using telomerase reverse transcriptase RNA transfected dendritic cells. Nat. Med.6(9), 1011–1017 (2000).
   PubMed Web of Science ®Google Scholar
• Dullaers M, Breckpot K, Van Meirvenne S et al. Side-by-side comparison of lentivirally transduced and mRNA-electroporated dendritic cells: implications for cancer immunotherapy protocols. Mol. Ther.10(4), 768–779 (2004).
   PubMed Web of Science ®Google Scholar
• Bonehill A, Heirman C, Thielemans K. Genetic approaches for the induction of a CD4+ T cell response in cancer immunotherapy. J. Gene Med.7(6), 686–695 (2005).
   PubMed Web of Science ®Google Scholar
• Bonehill A, Heirman C, Tuyaerts S et al. Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules. J. Immunol.172(11), 6649–6657 (2004).
   PubMed Web of Science ®Google Scholar
• Kang TH, Lee JH, Bae HC et al. Enhancement of dendritic cell-based vaccine potency by targeting antigen to endosomal/lysosomal compartments. Immunol. Lett.106(2), 126–134 (2006).
   PubMed Web of Science ®Google Scholar
• Romero P, Cerottini JC, Speiser DE. Monitoring tumor antigen specific T-cell responses in cancer patients and Phase I clinical trials of peptide-based vaccination. Cancer Immunol. Immunother.53(3), 249–255 (2004).
   PubMed Web of Science ®Google Scholar
• Britten CM, Janetzki S, van der Burg SH, Gouttefangeas C, Hoos A. Toward the harmonization of immune monitoring in clinical trials: quo vadis? Cancer Immunol. Immunother.57(3), 285–288 (2008).
   PubMedGoogle Scholar
• Keilholz U, Martus P, Scheibenbogen C. Immune monitoring of T-cell responses in cancer vaccine development. Clin. Cancer Res.12(7 Pt 2), 2346s–2352s (2006).
   PubMed Web of Science ®Google Scholar
• Michalek J, Kocak I, Fait V, Zaloudik J, Hajek R. Detection and long-term in vivo monitoring of individual tumor-specific T cell clones in patients with metastatic melanoma. J. Immunol.178(11), 6789–6795 (2007).
   Google Scholar
• van der Burg SH, Menon AG, Redeker A et al. Magnitude and polarization of P53-specific T-helper immunity in connection to leukocyte infiltration of colorectal tumors. Int. J. Cancer107(3), 425–433 (2003).
   PubMedGoogle Scholar
• van der Burg SH. Therapeutic vaccines in cancer: moving from immunomonitoring to immunoguiding. Expert Rev. Vaccines7(1), 1–5 (2008).
   PubMed Web of Science ®Google Scholar
• Zhang Y, Renkvist N, Sun Z et al. A polyclonal anti-vaccine CD4 T cell response detected with HLA-DP4 multimers in a melanoma patient vaccinated with MAGE-3.DP4-peptide-pulsed dendritic cells. Eur. J. Immunol.35(4), 1066–1075 (2005).
   Google Scholar
• Zhang Y, Sun Z, Nicolay H et al. Monitoring of anti-vaccine CD4 T cell frequencies in melanoma patients vaccinated with a MAGE-3 protein. J. Immunol.174(4), 2404–2411 (2005).
   Google Scholar
• Boon T, Coulie PG, Van den Eynde BJ, van der Bruggen P. Human T cell responses against melanoma. Annu. Rev. Immunol.24, 175–208 (2006).
   PubMed Web of Science ®Google Scholar
• Slingluff CL Jr, Engelhard VH, Ferrone S. Peptide and dendritic cell vaccines. Clin Cancer Res12(7 Pt 2), 2342s–2345s (2006).
   Web of Science ®Google Scholar
• Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol.25, 267–296 (2007).
   PubMed Web of Science ®Google Scholar
• Katz JB, Muller AJ, Prendergast GC. Indoleamine 2,3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol. Rev.222, 206–221 (2008).
   PubMed Web of Science ®Google Scholar
• Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol.6(4), 295–307 (2006).
   PubMed Web of Science ®Google Scholar
• Gabrilovich DI, Corak J, Ciernik IF, Kavanaugh D, Carbone DP. Decreased antigen presentation by dendritic cells in patients with breast cancer. Clin. Cancer Res.3(3), 483–490 (1997).
   PubMed Web of Science ®Google Scholar
• Kusmartsev S, Gabrilovich DI. Inhibition of myeloid cell differentiation in cancer: the role of reactive oxygen species. J. Leukoc. Biol.74(2), 186–196 (2003).
   PubMed Web of Science ®Google Scholar
• Paranjpe MS, Boone CW, Takeichi N. Discussion paper: specific paralysis of the antitumor cellular immune response produced by growing tumors studied with a radioisotope footpad assay. Ann. NY Acad. Sci.276, 254–259 (1976).
   Google Scholar
• Jarnicki AG, Lysaght J, Todryk S, Mills KH. Suppression of antitumor immunity by IL-10 and TGF-β-producing T cells infiltrating the growing tumor: influence of tumor environment on the induction of CD4+ and CD8+ regulatory T cells. J. Immunol.177(2), 896–904 (2006).
   PubMed Web of Science ®Google Scholar
• Negin B, Panka D, Wang W et al. Effect of melanoma on immune function in the regional lymph node basin. Clin. Cancer Res.14(3), 654–659 (2008).
   Google Scholar
• Tuettenberg A, Becker C, Huter E et al. Induction of strong and persistent MelanA/MART-1-specific immune responses by adjuvant dendritic cell-based vaccination of stage II melanoma patients. Int. J. Cancer118(10), 2617–2627 (2006).
   PubMed Web of Science ®Google Scholar
• O’Rourke MG, Johnson M, Lanagan C et al. Durable complete clinical responses in a Phase I/II trial using an autologous melanoma cell/dendritic cell vaccine. Cancer Immunol. Immunother.52(6), 387–395 (2003).
   PubMed Web of Science ®Google Scholar
• Broomfield S, Currie A, van der Most RG et al. Partial, but not complete, tumor-debulking surgery promotes protective antitumor memory when combined with chemotherapy and adjuvant immunotherapy. Cancer Res.65(17), 7580–7584 (2005).
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol.8(1), 59–73 (2008).
   PubMed Web of Science ®Google Scholar
• Menard C, Martin F, Apetoh L, Bouyer F, Ghiringhelli F. Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity. Cancer Immunol. Immunother. [Epub ahead of print] DOI: 10.1007/s00262-008-0505-6 (2008).
   Google Scholar
• Gulley JL, Madan RA, Arlen PM. Enhancing efficacy of therapeutic vaccinations by combination with other modalities. Vaccine25(Suppl. 2), B89–B96 (2007).
   PubMed Web of Science ®Google Scholar
• Correale P, Aquino A, Giuliani A et al. Treatment of colon and breast carcinoma cells with 5-fluorouracil enhances expression of carcinoembryonic antigen and susceptibility to HLA-A*02.01 restricted, CEA-peptide-specific cytotoxic T cells in vitro. Int. J. Cancer104(4), 437–445 (2003).
   PubMed Web of Science ®Google Scholar
• Lacour S, Hammann A, Wotawa A et al. Anticancer agents sensitize tumor cells to tumor necrosis factor-related apoptosis-inducing ligand-mediated caspase-8 activation and apoptosis. Cancer Res.61(4), 1645–1651 (2001).
   PubMed Web of Science ®Google Scholar
• Tong Y, Song W, Crystal RG. Combined intratumoral injection of bone marrow-derived dendritic cells and systemic chemotherapy to treat pre-existing murine tumors. Cancer Res.61(20), 7530–7535 (2001).
   PubMed Web of Science ®Google Scholar
• Martin F, Caignard A, Olsson O, Jeannin JF, Leclerc A. Tumoricidal effect of macrophages exposed to adriamycin in vivo or in vitro. Cancer Res.42(9), 3851–3857 (1982).
   PubMed Web of Science ®Google Scholar
• Shindo H, Ogura T, Masuno T, Hayashi S, Kishimoto S. Induction of activated macrophages by intraperitoneal injection of mitomycin C in mice. Cancer Immunol. Immunother.20(2), 145–150 (1985).
   Google Scholar
• Carson WE 3rd, Shapiro CL, Crespin TR, Thornton LM, Andersen BL. Cellular immunity in breast cancer patients completing taxane treatment. Clin. Cancer Res.10(10), 3401–3409 (2004).
   PubMed Web of Science ®Google Scholar
• Yu B, Kusmartsev S, Cheng F et al. Effective combination of chemotherapy and dendritic cell administration for the treatment of advanced-stage experimental breast cancer. Clin. Cancer Res.9(1), 285–294 (2003).
   PubMed Web of Science ®Google Scholar
• Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature436(7054), 1186–1190 (2005).
   PubMed Web of Science ®Google Scholar
• Suzuki E, Kapoor V, Jassar AS, Kaiser LR, Albelda SM. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res.11(18), 6713–6721 (2005).
   PubMed Web of Science ®Google Scholar
• Nowak AK, Robinson BW, Lake RA. Gemcitabine exerts a selective effect on the humoral immune response: implications for combination chemo–immunotherapy. Cancer Res.62(8), 2353–2358 (2002).
   PubMed Web of Science ®Google Scholar
• Nowak AK, Lake RA, Marzo AL et al. 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(10), 4905–4913 (2003).
   PubMed Web of Science ®Google Scholar
• Nowak AK, Robinson BW, Lake RA. Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res.63(15), 4490–4496 (2003).
   PubMed Web of Science ®Google Scholar
• Obeid M, Tesniere A, Ghiringhelli F et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med.13(1), 54–61 (2007).
   PubMed Web of Science ®Google Scholar
• Apetoh L, Ghiringhelli F, Tesniere A et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med.13(9), 1050–1059 (2007).
   PubMed Web of Science ®Google Scholar
• Apetoh L, Ghiringhelli F, Tesniere A et al. The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol. Rev.220, 47–59 (2007).
   PubMed Web of Science ®Google Scholar
• Antonia SJ, Mirza N, Fricke I et al. Combination of p53 cancer vaccine with chemotherapy in patients with extensive stage small cell lung cancer. Clin. Cancer Res.12(3 Pt 1), 878–887 (2006).
   PubMed Web of Science ®Google Scholar
• Gribben JG, Ryan DP, Boyajian R et al. Unexpected association between induction of immunity to the universal tumor antigen CYP1B1 and response to next therapy. Clin. Cancer Res.11(12), 4430–4436 (2005).
   PubMed Web of Science ®Google Scholar
• Correale P, Del Vecchio MT, La Placa M et al. Chemotherapeutic drugs may be used to enhance the killing efficacy of human tumor antigen peptide-specific CTLs. J. Immunother.31(2), 132–147 (2008).
   PubMed Web of Science ®Google Scholar
• Bauer C, Bauernfeind F, Sterzik A et al. Dendritic cell-based vaccination combined with gemcitabine increases survival in a murine pancreatic carcinoma model. Gut56(9), 1275–1282 (2007).
   PubMed Web of Science ®Google Scholar
• Curiel TJ, Coukos G, Zou L et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med.10(9), 942–949 (2004).
   PubMed Web of Science ®Google Scholar
• Attia P, Maker AV, Haworth LR, Rogers-Freezer L, Rosenberg SA. Inability of a fusion protein of IL-2 and diphtheria toxin (denileukin diftitox, DAB389IL-2, ONTAK) to eliminate regulatory T lymphocytes in patients with melanoma. J. Immunother.28(6), 582–592 (2005).
   PubMed Web of Science ®Google Scholar
• Ghiringhelli F, Menard C, Puig PE et al. 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(5), 641–648 (2007).
   PubMed Web of Science ®Google Scholar
• Holtl L, Ramoner R, Zelle-Rieser C et al. Allogeneic dendritic cell vaccination against metastatic renal cell carcinoma with or without cyclophosphamide. Cancer Immunol. Immunother.54(7), 663–670 (2005).
   PubMed Web of Science ®Google Scholar
• Maker AV, Phan GQ, Attia P et al. Tumor regression and autoimmunity in patients treated with cytotoxic T lymphocyte-associated antigen 4 blockade and interleukin 2: a Phase I/II study. Ann. Surg. Oncol.12(12), 1005–1016 (2005).
   PubMed Web of Science ®Google Scholar
• Munoz R, Shaked Y, Bertolini F et al. Anti-angiogenic treatment of breast cancer using metronomic low-dose chemotherapy. Breast14(6), 466–479 (2005).
   PubMed Web of Science ®Google Scholar
• Correale P, Cusi MG, Tsang KY et al. Chemo–immunotherapy of metastatic colorectal carcinoma with gemcitabine plus FOLFOX 4 followed by subcutaneous granulocyte macrophage colony-stimulating factor and interleukin-2 induces strong immunologic and antitumor activity in metastatic colon cancer patients. J. Clin. Oncol.23(35), 8950–8958 (2005).
   PubMed Web of Science ®Google Scholar
• Bronte V, Serafini P, Mazzoni A, Segal DM, Zanovello P. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol.24(6), 302–306 (2003).
   PubMed Web of Science ®Google Scholar
• Villadangos JA, Schnorrer P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol.7(7), 543–555 (2007).
   PubMed Web of Science ®Google Scholar
• McGreal EP, Miller JL, Gordon S. Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr. Opin. Immunol.17(1), 18–24 (2005).
   PubMed Web of Science ®Google Scholar
• He LZ, Crocker A, Lee J et al. Antigenic targeting of the human mannose receptor induces tumor immunity. J. Immunol.178(10), 6259–6267 (2007).
   PubMed Web of Science ®Google Scholar
• Hawiger D, Inaba K, Dorsett Y et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med.194(6), 769–779 (2001).
   PubMed Web of Science ®Google Scholar
• Bonifaz LC, Bonnyay DP, Charalambous A et al.In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J. Exp. Med.199(6), 815–824 (2004).
   PubMed Web of Science ®Google Scholar
• Tacken PJ, de Vries IJ, Gijzen K et al. Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood106(4), 1278–1285 (2005).
   PubMed Web of Science ®Google Scholar
• Lin ML, Zhan Y, Villadangos JA, Lew AM. The cell biology of cross-presentation and the role of dendritic cell subsets. Immunol. Cell Biol.86(4), 353–362 (2008).
   PubMed Web of Science ®Google Scholar
• Tacken PJ, de Vries IJ, Torensma R, Figdor CG. Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting. Nat. Rev. Immunol.7(10), 790–802 (2007).
   PubMed Web of Science ®Google Scholar
• Morein B, Sundquist B, Hoglund S, Dalsgaard K, Osterhaus A. Iscom, a novel structure for antigenic presentation of membrane proteins from enveloped viruses. Nature308(5958), 457–460 (1984).
   PubMed Web of Science ®Google Scholar
• Drane D, Gittleson C, Boyle J, Maraskovsky E. ISCOMATRIX adjuvant for prophylactic and therapeutic vaccines. Expert Rev. Vaccines6(5), 761–772 (2007).
   PubMed Web of Science ®Google Scholar
• Maraskovsky E, Sjolander S, Drane DP et al. NY-ESO-1 protein formulated in ISCOMATRIX adjuvant is a potent anticancer vaccine inducing both humoral and CD8+ T-cell-mediated immunity and protection against NY-ESO-1+ tumors. Clin. Cancer Res.10(8), 2879–2890 (2004).
   PubMed Web of Science ®Google Scholar
• Davis ID, Chen W, Jackson H et al. Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4+ and CD8+ T cell responses in humans. Proc. Natl Acad. Sci. USA101(29), 10697–10702 (2004).
   PubMed Web of Science ®Google Scholar
• Krieg AM. Development of TLR9 agonists for cancer therapy. J. Clin. Invest.117(5), 1184–1194 (2007).
   PubMed Web of Science ®Google Scholar
• Kornbluth RS, Stone GW. Immunostimulatory combinations: designing the next generation of vaccine adjuvants. J. Leukoc. Biol.80(5), 1084–1102 (2006).
   PubMedGoogle Scholar
• Wilson NS, Behrens GM, Lundie RJ et al. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol.7(2), 165–172 (2006).
   PubMed Web of Science ®Google Scholar
• Heit A, Schmitz F, O’Keeffe M et al. Protective CD8 T cell immunity triggered by CpG-protein conjugates competes with the efficacy of live vaccines. J. Immunol.174(7), 4373–4380 (2005).
   PubMed Web of Science ®Google Scholar
• Blander JM, Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature440(7085), 808–812 (2006).
   PubMed Web of Science ®Google Scholar
• Hsu FJ, Benike C, Fagnoni F et al. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat. Med.2(1), 52–58 (1996).
   PubMed Web of Science ®Google Scholar
• Gilboa E. DC-based cancer vaccines. J. Clin. Invest.117(5), 1195–1203 (2007).
   PubMed Web of Science ®Google Scholar