Clinical use of dendritic cells for cancer therapy

Steinman, 1973, Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution, J Exp Med, 137, 1142, 10.1084/jem.137.5.1142 Palucka, 2012, Cancer immunotherapy via dendritic cells, Nat Rev Cancer, 12, 265, 10.1038/nrc3258 Kirkwood, 2012, Immunotherapy of cancer in 2012, CA Cancer J Clin, 62, 309, 10.3322/caac.20132 Tacken, 2007, Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting, Nat Rev Immunol, 7, 790, 10.1038/nri2173 Schadendorf, 2006, 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, Ann Oncol, 17, 563, 10.1093/annonc/mdj138 Draube, 2011, Dendritic cell based tumor vaccination in prostate and renal cell cancer: a systematic review and meta-analysis, PLoS One, 6, e18801, 10.1371/journal.pone.0018801 Amos, 2011, Autoimmunity associated with immunotherapy of cancer, Blood, 118, 499, 10.1182/blood-2011-01-325266 Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N Engl J Med, 363, 711, 10.1056/NEJMoa1003466 Leonhartsberger, 2012, Quality of life during dendritic cell vaccination against metastatic renal cell carcinoma, Cancer Immunol Immunother, 61, 1407, 10.1007/s00262-012-1207-7 Widén, 2008, Overcoming immunosuppressive mechanisms, Ann Oncol, 19, vii Lion, 2012, NK cells: key to success of DC-based cancer vaccines?, Oncologist, 17, 1256, 10.1634/theoncologist.2011-0122 Boudreau, 2009, Recombinant vesicular stomatitis virus transduction of dendritic cells enhances their ability to prime innate and adaptive antitumor immunity, Mol Ther, 17, 1465, 10.1038/mt.2009.95 Rosenberg, 2004, Cancer immunotherapy: moving beyond current vaccines, Nat Med, 10, 909, 10.1038/nm1100 Huber, 2012, Interdisciplinary critique of sipuleucel-T as immunotherapy in castration-resistant prostate cancer, J Natl Cancer Inst, 104, 273, 10.1093/jnci/djr514 Robert, 2011, Ipilimumab plus dacarbazine for previously untreated metastatic melanoma, N Engl J Med, 364, 2517, 10.1056/NEJMoa1104621 Weber, 2008, Overcoming immunologic tolerance to melanoma: targeting CTLA-4 with ipilimumab (MDX-010), Oncologist, 13, 16, 10.1634/theoncologist.13-S4-16 Tay, 2006, Management of hormone refractory prostate cancer, 341 Coppin, 2005, Immunotherapy for advanced renal cell cancer, Cochrane Database Syst Rev, 1 Madan, 2010, Therapeutic cancer vaccines in prostate cancer: the paradox of improved survival without changes in time to progression, Oncologist, 15, 969, 10.1634/theoncologist.2010-0129 Saad, 2012, Overall survival: patient outcome, therapeutic objective, clinical trial end point, or public health measure?, J Clin Oncol, 30, 1750, 10.1200/JCO.2011.38.6359 Thurner, 1999, Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma, J Exp Med, 190, 1669, 10.1084/jem.190.11.1669 Slingluff, 2003, Clinical and immunologic results of a randomized phase II trial of vaccination using four melanoma peptides either administered in granulocyte-macrophage colony-stimulating factor in adjuvant or pulsed on dendritic cells, J Clin Oncol, 21, 4016, 10.1200/JCO.2003.10.005 Dillman, 2004, Phase I/II trial of melanoma patient-specific vaccine of proliferating autologous tumor cells, dendritic cells, and GM-CSF: planned interim analysis, Cancer Biother Radiopharm, 19, 658, 10.1089/1084978042484759 Dillman, 2009, Phase II trial of dendritic cells loaded with antigens from self-renewing, proliferating autologous tumor cells as patient-specific antitumor vaccines in patients with metastatic melanoma: final report, Cancer Biother Radiopharm, 24, 311, 10.1089/cbr.2008.0599 Dillman, 2012, Tumor stem cell antigens as consolidative active specific immunotherapy: a randomized phase II trial of dendritic cells versus tumor cells in patients with metastatic melanoma, J Immunother, 35, 641, 10.1097/CJI.0b013e31826f79c8 Trefzer, 2004, Vaccination with hybrids of tumor and dendritic cells induces tumor-specific T-cell and clinical responses in melanoma stage III and IV patients, Int J Cancer, 110, 730, 10.1002/ijc.20191 Vilella, 2004, Pilot study of treatment of biochemotherapy-refractory stage IV melanoma patients with autologous dendritic cells pulsed with a heterologous melanoma cell line lysate, Cancer Immunol Immunother, 53, 651, 10.1007/s00262-003-0495-3 Kyte, 2006, Phase I/II trial of melanoma therapy with dendritic cells transfected with autologous tumor-mRNA, Cancer Gene Ther, 13, 905, 10.1038/sj.cgt.7700961 Nakai, 2006, Vaccination of Japanese patients with advanced melanoma with peptide, tumor lysate or both peptide and tumor lysate-pulsed mature, monocyte-derived dendritic cells, J Dermatol, 33, 462, 10.1111/j.1346-8138.2006.00110.x Nakai, 2008, Evaluation of survival in Japanese stage IV melanoma patients treated with melanoma antigen-pulsed mature monocyte-derived dendritic cells, J Dermatol, 35, 801, 10.1111/j.1346-8138.2008.00575.x Hersey, 2008, Phase I/II study of treatment with matured dendritic cells with or without low dose IL-2 in patients with disseminated melanoma, Cancer Immunol Immunother, 57, 1039, 10.1007/s00262-007-0435-8 Ellebaek, 2012, Metastatic melanoma patients treated with dendritic cell vaccination, Interleukin-2 and metronomic cyclophosphamide: results from a phase II trial, Cancer Immunol Immunother, 61, 1791, 10.1007/s00262-012-1242-4 Oshita, 2012, Dendritic cell-based vaccination in metastatic melanoma patients: phase II clinical trial, Oncol Rep, 28, 1131, 10.3892/or.2012.1956 Aarntzen, 2013, Targeting CD4(+) T-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination, Cancer Res, 73, 19, 10.1158/0008-5472.CAN-12-1127 Tel, 2013, Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients, Cancer Res, 73, 1063, 10.1158/0008-5472.CAN-12-2583 Murphy, 1996, Phase I clinical trial: T-cell therapy for prostate cancer using autologous dendritic cells pulsed with HLA-A0201-specific peptides from prostate-specific membrane antigen, Prostate, 29, 371, 10.1002/(SICI)1097-0045(199612)29:6<371::AID-PROS5>3.0.CO;2-B Tjoa, 1997, Follow-up evaluation of prostate cancer patients infused with autologous dendritic cells pulsed with PSMA peptides, Prostate, 32, 272, 10.1002/(SICI)1097-0045(19970901)32:4<272::AID-PROS7>3.0.CO;2-L Tjoa, 1998, Evaluation of phase I/II clinical trials in prostate cancer with dendritic cells and PSMA peptides, Prostate, 36, 39, 10.1002/(SICI)1097-0045(19980615)36:1<39::AID-PROS6>3.0.CO;2-6 Small, 2006, Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer, J Clin Oncol, 24, 3089, 10.1200/JCO.2005.04.5252 Higano, 2009, Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer, Cancer, 115, 3670, 10.1002/cncr.24429 Hildenbrand, 2007, Immunotherapy of patients with hormone-refractory prostate carcinoma pre-treated with interferon-gamma and vaccinated with autologous PSA-peptide loaded dendritic cells—a pilot study, Prostate, 67, 500, 10.1002/pros.20539 Kantoff, 2010, Sipuleucel-T immunotherapy for castration-resistant prostate cancer, N Engl J Med, 363, 411, 10.1056/NEJMoa1001294 Yu, 2004, Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma, Cancer Res, 64, 4973, 10.1158/0008-5472.CAN-03-3505 Niu, 2004, Experimental and clinical research of dendritic cell and syngeneic immunotherapy of brain glioma, Chinese-German J Clin Oncol, 3, 147, 10.1007/s10330-003-0189-5 Liau, 2005, Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment, Clin Cancer Res, 11, 5515, 10.1158/1078-0432.CCR-05-0464 Yamanaka, 2005, Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: results of a clinical phase I/II trial, Clin Cancer Res, 11, 4160, 10.1158/1078-0432.CCR-05-0120 De Vleeschouwer, 2008, Postoperative adjuvant dendritic cell-based immunotherapy in patients with relapsed glioblastoma multiforme, Clin Cancer Res, 14, 3098, 10.1158/1078-0432.CCR-07-4875 Sampson, 2009, An epidermal growth factor receptor variant III-targeted vaccine is safe and immunogenic in patients with glioblastoma multiforme, Mol Cancer Ther, 8, 2773, 10.1158/1535-7163.MCT-09-0124 Ardon, 2010, Integration of autologous dendritic cell-based immunotherapy in the primary treatment for patients with newly diagnosed glioblastoma multiforme: a pilot study, J Neurooncol, 99, 261, 10.1007/s11060-010-0131-y Chang, 2011, A phase I/II clinical trial investigating the adverse and therapeutic effects of a postoperative autologous dendritic cell tumor vaccine in patients with malignant glioma, J Clin Neurosci, 18, 1048, 10.1016/j.jocn.2010.11.034 Fadul, 2011, Immune response in patients with newly diagnosed glioblastoma multiforme treated with intranodal autologous tumor lysate-dendritic cell vaccination after radiation chemotherapy, J Immunother, 34, 382, 10.1097/CJI.0b013e318215e300 Prins, 2011, Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy, Clin Cancer Res, 17, 1603, 10.1158/1078-0432.CCR-10-2563 Ardon, 2012, Integration of autologous dendritic cell-based immunotherapy in the standard of care treatment for patients with newly diagnosed glioblastoma: results of the HGG-2006 phase I/II trial, Cancer Immunol Immunother, 61, 2033, 10.1007/s00262-012-1261-1 Cho, 2012, Adjuvant immunotherapy with whole-cell lysate dendritic cells vaccine for glioblastoma multiforme: a phase II clinical trial, World Neurosurg, 77, 736, 10.1016/j.wneu.2011.08.020 Jie, 2012, Clinical application of a dendritic cell vaccine raised against heat-shocked glioblastoma, Cell Biochem Biophys, 62, 91, 10.1007/s12013-011-9265-6 Valle, 2012, Dendritic cell vaccination in glioblastoma after fluorescence-guided resection, World J Clin Oncol, 3, 142, 10.5306/wjco.v3.i11.142 Vik-Mo, 2013, Therapeutic vaccination against autologous cancer stem cells with mRNA-transfected dendritic cells in patients with glioblastoma, Cancer Immunol Immunother, 62, 1499, 10.1007/s00262-013-1453-3 Su, 2003, Immunological and clinical responses in metastatic renal cancer patients vaccinated with tumor RNA-transfected dendritic cells, Cancer Res, 63, 2127 Kim, 2007, Phase I/II study of immunotherapy using autologous tumor lysate-pulsed dendritic cells in patients with metastatic renal cell carcinoma, Clin Immunol, 125, 257, 10.1016/j.clim.2007.07.014 Berntsen, 2008, Therapeutic dendritic cell vaccination of patients with metastatic renal cell carcinoma: a clinical phase 1/2 trial, J Immunother, 31, 771, 10.1097/CJI.0b013e3181833818 Schwaab, 2009, Clinical and immunologic effects of intranodal autologous tumor lysate-dendritic cell vaccine with Aldesleukin (interleukin 2) and IFN-alpha2a therapy in metastatic renal cell carcinoma patients, Clin Cancer Res, 15, 4986, 10.1158/1078-0432.CCR-08-3240 Amin, 2013, Prolonged survival with personalized immunotherapy (AGS-003) in combination with sunitinib in unfavorable risk metastatic RCC (mRCC), Proc Am Soc Clin Oncol, 31 Sheikh, 2013, Sipuleucel-T immune parameters correlate with survival: an analysis of the randomized phase 3 clinical trials in men with castration-resistant prostate cancer, Cancer Immunol Immunother, 62, 137, 10.1007/s00262-012-1317-2 Johnson, 2003, End points and United States Food and Drug Administration approval of oncology drugs, J Clin Oncol, 21, 1404, 10.1200/JCO.2003.08.072 Sharma, 2011, Novel cancer immunotherapy agents with survival benefit: recent successes and next steps, Nat Rev Cancer, 11, 805, 10.1038/nrc3153 Escudier, 2007, Sorafenib in advanced clear-cell renal-cell carcinoma, N Engl J Med, 356, 125, 10.1056/NEJMoa060655 Escudier, 2009, Sorafenib for treatment of renal cell carcinoma: final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial, J Clin Oncol, 27, 3312, 10.1200/JCO.2008.19.5511 Wolchok, 2009, Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria, Clin Cancer Res, 15, 7412, 10.1158/1078-0432.CCR-09-1624 Hoos, 2012, Evolution of end points for cancer immunotherapy trials, Ann Oncol, 23, viii, 10.1093/annonc/mds263 Beer, 2011, Randomized trial of autologous cellular immunotherapy with sipuleucel-T in androgen-dependent prostate cancer, Clin Cancer Res, 17, 4558, 10.1158/1078-0432.CCR-10-3223 Di Lorenzo, 2011, Immunotherapy for the treatment of prostate cancer, Nat Rev Clin Oncol, 8, 551, 10.1038/nrclinonc.2011.72 Stein, 2011, Tumor regression and growth rates determined in five intramural NCI prostate cancer trials: the growth rate constant as an indicator of therapeutic efficacy, Clin Cancer Res, 17, 907, 10.1158/1078-0432.CCR-10-1762 de Vries, 2003, Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients, Clin Cancer Res, 9, 5091 Okada, 2011, J Clin Oncol, 29, 330, 10.1200/JCO.2010.30.7744 Carreno, 2013, IL-12p70-producing patient DC vaccine elicits Tc1-polarized immunity, J Clin Invest, 123, 3383, 10.1172/JCI68395 Ueno, 2010, Harnessing human dendritic cell subsets for medicine, Immunol Rev, 234, 199, 10.1111/j.0105-2896.2009.00884.x Romano, 2011, Peptide-loaded Langerhans cells, despite increased IL15 secretion and T-cell activation in vitro, elicit antitumor T-cell responses comparable to peptide-loaded monocyte-derived dendritic cells in vivo, Clin Cancer Res, 17, 1984, 10.1158/1078-0432.CCR-10-3421 Anguille, 2013, Interleukin-15 dendritic cells as vaccine candidates for cancer immunotherapy, Hum Vaccin Immunother, 9, 1956, 10.4161/hv.25373 Boullart, 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, 10.1007/s00262-008-0489-2 Fujita, 2009, Effective immunotherapy against murine gliomas using type 1 polarizing dendritic cells–significant roles of CXCL10, Cancer Res, 69, 1587, 10.1158/0008-5472.CAN-08-2915 Pierret, 2009, Correlation between prior therapeutic dendritic cell vaccination and the outcome of patients with metastatic melanoma treated with ipilimumab, Proc Am Soc Clin Oncol, 27 Ribas, 2009, Dendritic cell vaccination combined with CTLA4 blockade in patients with metastatic melanoma, Clin Cancer Res, 15, 6267, 10.1158/1078-0432.CCR-09-1254 Hamid, 2013, Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma, N Engl J Med, 369, 134, 10.1056/NEJMoa1305133 Wolchok, 2013, Nivolumab plus ipilimumab in advanced melanoma, N Engl J Med, 369, 122, 10.1056/NEJMoa1302369 Smits, 2008, The use of TLR7 and TLR8 ligands for the enhancement of cancer immunotherapy, Oncologist, 13, 859, 10.1634/theoncologist.2008-0097 Whiteside, 2010, Inhibiting the inhibitors: evaluating agents targeting cancer immunosuppression, Expert Opin Biol Ther, 10, 1019, 10.1517/14712598.2010.482207 Shimizu, 1999, Systemic administration of interleukin 2 enhances the therapeutic efficacy of dendritic cell-based tumor vaccines, Proc Natl Acad Sci USA, 96, 2268, 10.1073/pnas.96.5.2268 Escobar, 2005, Dendritic cell immunizations alone or combined with low doses of interleukin-2 induce specific immune responses in melanoma patients, Clin Exp Immunol, 142, 555, 10.1111/j.1365-2249.2005.02948.x Redman, 2008, Phase Ib trial assessing autologous, tumor-pulsed dendritic cells as a vaccine administered with or without IL-2 in patients with metastatic melanoma, J Immunother, 31, 591, 10.1097/CJI.0b013e31817fd90b Mirza, 2006, All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients, Cancer Res, 66, 9299, 10.1158/0008-5472.CAN-06-1690 Zitvogel, 2008, The anticancer immune response: indispensable for therapeutic success?, J Clin Invest, 118, 1991, 10.1172/JCI35180 Ridolfi, 2013, Low-dose temozolomide before dendritic-cell vaccination reduces (specifically) CD4+CD25++Foxp3+ regulatory T-cells in advanced melanoma patients, J Transl Med, 11, 135, 10.1186/1479-5876-11-135 Chen, 2013, Chemoimmunotherapy: reengineering tumor immunity, Cancer Immunol Immunother, 62, 203, 10.1007/s00262-012-1388-0 Wang, 2005, Interleukin-7-dependent expansion and persistence of melanoma-specific T cells in lymphodepleted mice lead to tumor regression and editing, Cancer Res, 65, 10569, 10.1158/0008-5472.CAN-05-2117 Kandalaft, 2013, Autologous lysate-pulsed dendritic cell vaccination followed by adoptive transfer of vaccine-primed ex vivo co-stimulated T cells in recurrent ovarian cancer, OncoImmunology, 2, e22664, 10.4161/onci.22664 Schlom, 2012, Therapeutic cancer vaccines: current status and moving forward, J Natl Cancer Inst, 104, 599, 10.1093/jnci/djs033 Jacobs, 2012, Regulatory T cells in melanoma: the final hurdle towards effective immunotherapy?, Lancet Oncol, 13, e32, 10.1016/S1470-2045(11)70155-3 Jacobs, 2010, Dendritic cell vaccination in combination with anti-CD25 monoclonal antibody treatment: a phase I/II study in metastatic melanoma patients, Clin Cancer Res, 16, 5067, 10.1158/1078-0432.CCR-10-1757 Dannull, 2005, Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells, J Clin Invest, 115, 3623, 10.1172/JCI25947 Morse, 2008, Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines, Blood, 112, 610, 10.1182/blood-2008-01-135319 Baur, 2013, Denileukin diftitox (ONTAK) induces a tolerogenic phenotype in dendritic cells and stimulates survival of resting Treg, Blood, 122, 2185, 10.1182/blood-2012-09-456988 Yamada, 2012, Differential effects of denileukin diftitox IL-2 immunotoxin on NK and regulatory T cells in nonhuman primates, J Immunol, 188, 6063, 10.4049/jimmunol.1200656 Radojcic, 2010, Cyclophosphamide resets dendritic cell homeostasis and enhances antitumor immunity through effects that extend beyond regulatory T cell elimination, Cancer Immunol Immunother, 59, 137, 10.1007/s00262-009-0734-3 Heine, 2011, Immunomodulatory effects of anti-angiogenic drugs, Leukemia, 25, 899, 10.1038/leu.2011.24 Sakamaki, 2014, Lenalidomide enhances the protective effect of a therapeutic vaccine and reverses immune suppression in mice bearing established lymphomas, Leukemia, 28, 329, 10.1038/leu.2013.177 Najjar, 2013, Clinical perspectives on targeting of myeloid derived suppressor cells in the treatment of cancer, Front Oncol, 3, 49, 10.3389/fonc.2013.00049 Poschke, 2012, Myeloid-derived suppressor cells impair the quality of dendritic cell vaccines, Cancer Immunol Immunother, 61, 827, 10.1007/s00262-011-1143-y Fujita, 2011, COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells, Cancer Res, 71, 2664, 10.1158/0008-5472.CAN-10-3055 Schilling, 2013, Vemurafenib reverses immunosuppression by myeloid derived suppressor cells, Int J Cancer, 133, 1653, 10.1002/ijc.28168 Knight, 2013, Host immunity contributes to the anti-melanoma activity of BRAF inhibitors, J Clin Invest, 123, 1371, 10.1172/JCI66236 Ott, 2013, Inhibition of both BRAF and MEK in BRAF(V600E) mutant melanoma restores compromised dendritic cell (DC) function while having differential direct effects on DC properties, Cancer Immunol Immunother, 62, 811, 10.1007/s00262-012-1389-z Gulley, 2011, Impact of tumour volume on the potential efficacy of therapeutic vaccines, Curr Oncol, 18, e150, 10.3747/co.v18i3.783 Van Tendeloo, 2010, Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination, Proc Natl Acad Sci USA, 107, 13824, 10.1073/pnas.1008051107 Anguille, 2012, Dendritic cell vaccination in acute myeloid leukemia, Cytotherapy, 14, 647, 10.3109/14653249.2012.693744 Gabrilovich, 2007, Combination of chemotherapy and immunotherapy for cancer: a paradigm revisited, Lancet Oncol, 8, 2, 10.1016/S1470-2045(06)70985-8 Wheeler, 2004, Clinical responsiveness of glioblastoma multiforme to chemotherapy after vaccination, Clin Cancer Res, 10, 5316, 10.1158/1078-0432.CCR-04-0497 Bracci, 2014, Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer, Cell Death Differ, 21, 15, 10.1038/cdd.2013.67 Aragon-Ching, 2007, Impact of androgen-deprivation therapy on the immune system: implications for combination therapy of prostate cancer, Front Biosci, 12, 4957, 10.2741/2441 Kalbasi, 2013, Radiation and immunotherapy: a synergistic combination, J Clin Invest, 123, 2756, 10.1172/JCI69219