Optimizing dendritic cell-based approaches for cancer immunotherapy

Yale Journal of Biology and Medicine

Volumn 87, Issue 4, 2014, Pages 491-518

  Datta, Jashodeep ^a   Terhune, Julia H ^a,b   Lowenfeld, Lea ^a   Cintolo, Jessica A ^a   Xu, Shuwen ^a   Roses, Robert E ^a   Czerniecki, Brian J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Chemotherapy; Combination therapy; Dendritic cell; Immunotherapy; Vaccine

Indexed keywords

CANCER VACCINE; CYTOKINE; DENDRITIC CELL VACCINE; GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 2 RECEPTOR ALPHA; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR AGONIST;

ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; B CELL LYMPHOMA; BRAIN CANCER; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CELL ACTIVATION; CLINICAL EFFECTIVENESS; COLORECTAL CANCER; CROSS PRESENTATION; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DENDRITIC CELL; DRUG DESIGN; EX VIVO STUDY; HEAD AND NECK CANCER; HEMATOLOGIC MALIGNANCY; HUMAN; HUMORAL IMMUNITY; IMMUNOBIOLOGY; IMMUNOPOTENTIATION; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; KIDNEY CANCER; LUNG CANCER; LYMPHOMA; MELANOMA; MESOTHELIOMA; MOLECULARLY TARGETED THERAPY; MYELOMA; NATURAL KILLER T CELL; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PROSTATE CANCER; SARCOMA; SIGNAL TRANSDUCTION; SOLID TUMOR; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; TH2 CELL; IMMUNOLOGY; IMMUNOTHERAPY; PROCEDURES; TREATMENT OUTCOME;

CANCER VACCINES; DENDRITIC CELLS; DRUG DESIGN; HUMANS; IMMUNOTHERAPY; TREATMENT OUTCOME;

EID: 84930067333     PISSN: 00440086     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (170)

1. Palucka K, Banchereau J. Cancer im-munotherapy via dendritic cells. Nat Rev Cancer. 2012;12(4):265-77.
2. Hsu FJ, Benike C, Fagnoni F, Liles TM, Cz-erwinski D, Taidi B, et al. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat Med. 1996;2(1):52-8.
3. Schadendorf D, Ugurel S, Schuler-Thurner B, Nestle FO, Enk A, Brocker EB, 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. Ann Oncol. 2006;17(4):563-70.
4. Anguille S, Smits EL, Lion E, van Tendeloo VF, Berneman ZN. Clinical use of dendritic cells for cancer therapy. Lancet Oncol. 2014;15(7):e257-67.
5. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363(5):411-22.
6. Cintolo JA, Datta J, Mathew SJ, Czerniecki BJ. Dendritic cell-based vaccines: barriers and opportunities. Future Oncol. 2012;8(10):1273-99.
7. Inaba K, Romani N, Steinman RM. An antigen-independent contact mechanism as an early step in T cell-proliferative responses to dendritic cells. J Exp Med. 1989;170(2):527-42.
8. Mehta-Damani A, Markowicz S, Engleman EG. Generation of antigen-specific CD4+ T cell lines from naive precursors. Eur J Immunol. 1995;25(5):1206-11.
9. Mehta-Damani A, Markowicz S, Engleman EG. Generation of antigen-specific CD8+ CTLs from naive precursors. J Immunol. 1994;153(3):996-1003.
10. Zhai Y, Wang Y, Wu Z, Kupiec-Weglinski JW. Defective alloreactive CD8 T cell function and memory response in allograft recipients in the absence of CD4 help. J Immunol. 2007;179(7):4529-34.
11. Echchakir H, Bagot M, Dorothee G, Martin-valet D, Le Gouvello S, Boumsell L, et al. Cutaneous T cell lymphoma reactive CD4+ cytotoxic T lymphocyte clones display a Th1 cytokine profile and use a fas-independent pathway for specific tumor cell lysis. J Invest Dermatol. 2000;115(1):74-80.
12. Bachem A, Guttler S, Hartung E, Ebstein F, Schaefer M, Tannert A, et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as ho-mologues of mouse CD8+ dendritic cells. J Exp Med. 2010;207(6):1273-81.
13. Segura E, Durand M, Amigorena S. Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J Exp Med. 2013;210(5):1035-47.
14. Amigorena S, Savina A. Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr Opin Immunol. 2010;22(1):109-17.
15. Schiavoni G, Mattei F, Gabriele L. Type I In-terferons as Stimulators of DC-Mediated Cross-Priming: Impact on Anti-Tumor Response. Front Immunol. 2013;4:483.
16. Koski GK, Cohen PA, Roses RE, Xu S, Cz-erniecki BJ. Reengineering dendritic cell-based anti-cancer vaccines. Immunol Rev. 2008;222:256-76.
17. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol. 2011;29:621-63.
18. Caminschi I, Shortman K. Boosting antibody responses by targeting antigens to dendritic cells. Trends Immunol. 2012;33(2):71-7.
19. Bergtold A, Desai DD, Gavhane A, Clynes R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity. 2005;23(5):503-14.
20. Dubois B, Caux C. Critical role of ITIM-bearing FcgammaR on DCs in the capture and presentation of native antigen to B cells. Immunity. 2005;23(5):463-4.
21. Sakai Y, Morrison BJ, Burke JD, Park JM, Terabe M, Janik JE, et al. Vaccination by genetically modified dendritic cells expressing a truncated neu oncogene prevents development of breast cancer in transgenic mice. Cancer Res. 2004;64(21):8022-8.
22. Park JM, Terabe M, Sakai Y, Munasinghe J, Forni G, Morris JC, et al. Early role of CD4+ Th1 cells and antibodies in HER-2 aden-ovirus vaccine protection against autochthonous mammary carcinomas. J Immunol. 2005;174(7):4228-36.
23. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol. 2004;5(12):1260-5.
24. Bonaccorsi I, Pezzino G, Morandi B, Fer-lazzo G. Novel perspectives on dendritic cell-based immunotherapy of cancer. Immunol Lett. 2013;155(1-2):6-10.
25. Carnaud C, Lee D, Donnars O, Park SH, Beavis A, Koezuka Y, et al. Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol. 1999;163(9):4647-50.
26. Richter J, Neparidze N, Zhang L, Nair S, Mon-esmith T, Sundaram R, et al. Clinical regressions and broad immune activation following combination therapy targeting human NKT cells in myeloma. Blood. 2013;121(3):423-30.
27. Janjic BM, Lu G, Pimenov A, Whiteside TL, Storkus WJ, Vujanovic NL. Innate direct an-ticancer effector function of human immature dendritic cells. I. Involvement of an apopto-sis-inducing pathway. J Immunol. 2002;168(4):1823-30.
28. Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macro-molecules in the major histocompatibility complex class II compartment: downregula-tion by cytokines and bacterial products. J Exp Med. 1995;182(2):389-400.
29. Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol. 1991;9:271-96.
30. Sallusto F, Schaerli P, Loetscher P, Schaniel C, Lenig D, Mackay CR, et al. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol. 1998;28(9):2760-9.
31. Zinkernagel RM. Restriction by H-2 gene complex of transfer of cell-mediated immunity to Listeria monocytogenes. Nature. 1974;251(5472):230-3.
32. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulo-cyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 1994;179(4):1109-18.
33. Linsley PS, Clark EA, Ledbetter JA. T-cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB-1. Proc Natl Acad Sci USA. 1990;87(13):5031-5.
34. Scott P. IL-12: initiation cytokine for cell-mediated immunity. Science. 1993;260(5107):496-7.
35. Ohshima Y, Tanaka Y, Tozawa H, Takahashi Y, Maliszewski C, Delespesse G. Expression and function of OX40 ligand on human dendritic cells. J Immunol. 1997;159(8):3838-48.
36. O’Doherty U, Peng M, Gezelter S, Swiggard WJ, Betjes M, Bhardwaj N, et al. Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology. 1994;82(3):487-93.
37. Olweus J, BitMansour A, Warnke R, Thompson PA, Carballido J, Picker LJ, et al. Dendritic cell ontogeny: a human dendritic cell lineage of myeloid origin. Proc Natl Acad Sci USA. 1997;94(23):12551-6.
38. Schmid MA, Kingston D, Boddupalli S, Manz MG. Instructive cytokine signals in dendritic cell lineage commitment. Immunol Rev. 2010;234(1):32-44.
39. Crozat K, Guiton R, Contreras V, Feuillet V, Dutertre CA, Ventre E, et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med. 2010;207(6):1283-92.
40. O’Keeffe M, Hochrein H, Vremec D, Camin-schi I, Miller JL, Anders EM, et al. Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med. 2002;196(10):1307-19.
41. Liu YJ. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol. 2005;23:275-306.
42. Ardavin C. Thymic dendritic cells. Immunol Today. 1997;18(7):350-61.
43. Shortman K, Caux C. Dendritic cell development: multiple pathways to nature’s adjuvants. Stem Cells. 1997;15(6):409-19.
44. Wu L, Nichogiannopoulou A, Shortman K, Georgopoulos K. Cell-autonomous defects in dendritic cell populations of Ikaros mutant mice point to a developmental relationship with the lymphoid lineage. Immunity. 1997;7(4):483-92.
45. Wu L, D’Amico A, Winkel KD, Suter M, Lo D, Shortman K. RelB is essential for the development of myeloid-related CD8alpha-dendritic cells but not of lymphoid-related CD8alpha+ dendritic cells. Immunity. 1998;9(6):839-47.
46. Guerriero A, Langmuir PB, Spain LM, Scott EW. PU.1 is required for myeloid-derived but not lymphoid-derived dendritic cells. Blood. 2000;95(3):879-85.
47. Karsunky H, Merad M, Cozzio A, Weissman IL, Manz MG. Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo. J Exp Med. 2003;198(2):305-13.
48. Shigematsu H, Reizis B, Iwasaki H, Mizuno S, Hu D, Traver D, et al. Plasmacytoid dendritic cells activate lymphoid-specific genetic programs irrespective of their cellular origin. Immunity. 2004;21(1):43-53.
49. Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002;20:197-216.
50. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Tolllike receptor 3. Nature. 2001;413(6857):732-8.
51. Roses RE, Datta J, Czerniecki BJ. Radiation as Immunomodulator: Implications for Dendritic Cell-Based Immunotherapy. Radiat Res. 2014;182(2):211-8.
52. Kawai T, Akira S. Toll-like receptor downstream signaling. Arthritis Res Ther. 2005;7(1):12-9.
53. Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, et al. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med. 2001;194(6):863-9.
54. Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. Selected Toll-like recep tor agonist combinations synergistically trig ger a T helper type 1-polarizing program in dendritic cells. Nat Immunol. 2005;6(8):769-76.
55. Xu S, Koski GK, Faries M, Bedrosian I, Mick R, Maeurer 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. 2003;171(5):2251-61.
56. Xu S, Koldovsky U, Xu M, Wang D, Fitz-patrick E, Son G, et al. High-avidity antitu-mor T-cell generation by toll receptor 8-primed, myeloid- derived dendritic cells is mediated by IL-12 production. Surgery. 2006;140(2):170-8.
57. 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 an-timelanoma CD4+ T cell responses in vitro. J Immunother. 2007;30(1):75-82.
58. Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O’Garra A, Murphy KM. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science. 1993;260(5107):547-9.
59. Nanni P, Landuzzi L, Nicoletti G, De Giovanni C, Rossi I, Croci S, et al. Immunoprevention of mammary carcinoma in HER-2/neu trans-genic mice is IFN-gamma and B cell dependent. J Immunol. 2004;173(4):2288-96.
60. Czerniecki BJ, Roses RE, Koski GK. Development of vaccines for high-risk ductal carcinoma in situ of the breast. Cancer Res. 2007;67(14):6531-4.
61. Chan SH, Perussia B, Gupta JW, Kobayashi M, Pospisil M, Young HA, et al. Induction of interferon gamma production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other in-ducers. J Exp Med. 1991;173(4):869-79.
62. Voest EE, Kenyon BM, O’Reilly MS, Truitt G, D’Amato RJ, Folkman J. Inhibition of an- giogenesis in vivo by interleukin 12. J Natl Cancer Inst. 1995;87(8):581-6.
63. Nishimura T, Iwakabe K, Sekimoto M, Ohmi Y, Yahata T, Nakui M, et al. Distinct role of antigen-specific T helper type 1 (Th1) and Th2 cells in tumor eradication in vivo. J Exp Med. 1999;190(5):617-27.
64. Aspord C, Pedroza-Gonzalez A, Gallegos M, Tindle S, Burton EC, Su D, et al. Breast cancer instructs dendritic cells to prime inter-leukin 13-secreting CD4+ T cells that facilitate tumor development. J Exp Med. 2007;204(5):1037-47.
65. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell. 2009;16(2):91-102.
66. Manel N, Unutmaz D, Littman DR. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol. 2008;9(6):641-9.
67. Volpe E, Servant N, Zollinger R, Bogiatzi SI, Hupe P, Barillot E, et al. A critical function for transforming growth factor-beta, inter-leukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat Immunol. 2008;9(6):650-7.
68. Ji Y, Zhang W. Th17 cells: positive or negative role in tumor? Cancer Immunol Im-munother. 2010;59(7):979-87.
69. Roses RE, Xu S, Xu M, Koldovsky U, Koski G, Czerniecki BJ. Differential production of IL-23 and IL-12 by myeloid-derived dendritic cells in response to TLR agonists. J Immunol. 2008;181(7):5120-7.
70. Paustian C, Taylor P, Johnson T, Xu M, Ramirez N, Rosenthal KS, et al. Extracellular ATP and Toll-like receptor 2 agonists trigger in human monocytes an activation program that favors T helper 17. PloS One. 2013;8(1):e54804.
71. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6(11):1133-41.
72. Pene J, Chevalier S, Preisser L, Venereau E, Guilleux MH, Ghannam S, et al. Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes. J Immunol. 2008;180(11):7423-30.
73. Wang L, Yi T, Kortylewski M, Pardoll DM, Zeng D, Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med. 2009;206(7):1457-64.
74. Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, Kaiser A, et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood. 2008;112(2):362-73.
75. Wei S, Zhao E, Kryczek I, Zou W. Th17 cells have stem cell-like features and promote long-term immunity. Oncoimmunology. 2012;1(4):516-9.
76. Apostolopoulos V, Thalhammer T, Tzakos AG, Stojanovska L. Targeting antigens to dendritic cell receptors for vaccine development. J Drug Deliv. 2013;2013:869718.
77. Caminschi I, Maraskovsky E, Heath WR. Targeting Dendritic Cells in vivo for Cancer Therapy. Front Immunol. 2012;3:13.
78. Mahnke K, Qian Y, Fondel S, Brueck J, Becker C, Enk AH. Targeting of antigens to activated dendritic cells in vivo cures metastatic melanoma in mice. Cancer Res. 2005;65(15):7007-12.
79. Charalambous A, Oks M, Nchinda G, Ya-mazaki S, Steinman RM. Dendritic cell targeting of survivin protein in a xenogeneic form elicits strong CD4+ T cell immunity to mouse survivin. J Immunol. 2006;177(12):8410-21.
80. Flynn BJ, Kastenmuller K, Wille-Reece U, Tomaras GD, Alam M, Lindsay RW, et al. Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York vaccinia virus induces robust T-cell immunity in nonhuman primates. Proc Natl Acad Sci USA. 2011;108(17):7131-6.
81. Stern JN, Keskin DB, Kato Z, Waldner H, Schallenberg S, Anderson A, et al. Promoting tolerance to proteolipid protein-induced experimental autoimmune encephalomyelitis through targeting dendritic cells. Proc Natl Acad Sci USA. 2010;107(40):17280-5.
82. Sheng KC, Pouniotis DS, Wright MD, Tang CK, Lazoura E, Pietersz GA, et al. Mannan derivatives induce phenotypic and functional maturation of mouse dendritic cells. Immunology. 2006;118(3):372-83.
83. Tsuji T, Matsuzaki J, Kelly MP, Ramakrishna V, Vitale L, He LZ, et al. Antibody-targeted NY-ESO-1 to mannose receptor or DEC-205 in vitro elicits dual human CD8+ and CD4+ T cell responses with broad antigen specificity. J Immunol. 2011;186(2):1218-27.
84. Morse MA, Bradley DA, Keler T, Laliberte RJ, Green JA, Davis TA, et al. CDX-1307: a novel vaccine under study as treatment for muscle-invasive bladder cancer. Expert Rev Vaccines. 2011;10(6):733-42.
85. Dhodapkar M V, Sznol M, Zhao B, Wang D, Car-vajal RD, Keohan ML, et al. Induction of antigen-specific immunity with a vaccine targeting NY-ESO-1 to the dendritic cell receptor DEC-205. Sci Transl Med. 2014;6(232):232-51.
86. Engering A, Geijtenbeek TB, van Vliet SJ, Wijers M, van Liempt E, Demaurex N, et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol. 2002;168(5):2118-26.
87. Kretz-Rommel A, Qin F, Dakappagari N, Torensma R, Faas S, Wu D, et al. In vivo targeting of antigens to human dendritic cells through DC-SIGN elicits stimulatory immune responses and inhibits tumor growth in grafted mouse models. J Immunother. 2007;30(7):715-26.
88. Meyer-Wentrup F, Cambi A, Joosten B, Looman MW, de Vries IJ, Figdor CG, et al. DCIR is endocytosed into human dendritic cells and inhibits TLR8-mediated cytokine production. J Leukoc Biol. 2009;85(3):518-25.
89. Klechevsky E, Flamar AL, Cao Y, Blanck JP, Liu M, O’Bar A, et al. Cross-priming CD8+ T cells by targeting antigens to human dendritic cells through DCIR. Blood. 2010;116(10):1685-97.
90. Platt CD, Ma JK, Chalouni C, Ebersold M, Bou-Reslan H, Carano RA, et al. Mature dendritic cells use endocytic receptors to capture and present antigens. Proc Natl Acad Sci USA. 2010;107(9):4287-92.
91. Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C, Yamazaki S, et al. Differential antigen processing by dendritic cell subsets in vivo. Science. 2007;315(5808):107-11.
92. Li D, Romain G, Flamar AL, Duluc D, Dul-laers M, Li XH, et al. Targeting self- and foreign antigens to dendritic cells via DC-ASGPR generates IL-10-producing suppressive CD4+ T cells. J Exp Med. 2012;209(1):109-21.
93. Joffre OP, Sancho D, Zelenay S, Keller AM, Reis e Sousa C. Efficient and versatile manipulation of the peripheral CD4+ T-cell compartment by antigen targeting to DNGR-1/CLEC9A. Eur J Immunol. 2010;40(5):1255-65.
94. Young JW, Steinman RM. Accessory cell requirements for the mixed-leukocyte reaction and polyclonal mitogens, as studied with a new technique for enriching blood dendritic cells. Cell Immunol. 1988;111(1):167-82.
95. Markowicz S, Engleman EG. Granulocyte-macrophage colony-stimulating factor promotes differentiation and survival of human peripheral blood dendritic cells in vitro. J Clin Invest. 1990;85(3):955-61.
96. Draube A, Klein-Gonzalez N, Mattheus S, Brillant C, Hellmich M, Engert A, et al. Dendritic cell based tumor vaccination in prostate and renal cell cancer: a systematic review and meta-analysis. PloS One. 2011;6(4):e18801.
97. de Vries IJ, Lesterhuis WJ, Scharenborg NM, Engelen L P, Ruiter DJ, Gerritsen MJ, et al. Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients. Clin Cancer Res. 2003;9(14):5091-100.
98. Yamanaka R, Homma J, Yajima N, Tsuchiya N, Sano M, Kobayashi T, et al. Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: results of a clinical phase I/II trial. Clin Cancer Res. 2005;11(11):4160-7.
99. Strioga MM, Felzmann T, Powell DJ Jr., Ostapenko V, Dobrovolskiene NT, Ma-tuskova M, et al. Therapeutic dendritic cell-based cancer vaccines: the state of the art. Crit Rev Immunol. 2013;33(6):489-547.
100. Czerniecki BJ, Koski GK, Koldovsky U, Xu S, Cohen PA, Mick R, et al. Targeting HER-2/neu in early breast cancer development using dendritic cells with staged interleukin-12 burst secretion. Cancer Res. 2007;67(4):1842-52.
101. Carreno BM, Becker-Hapak M, Huang A, Chan M, Alyasiry A, Lie WR, et al. IL-12p70-producing patient DC vaccine elicits Tc1-polarized immunity. J Clin Invest. 2013;123(8):3383-94.
102. Okada H, Kalinski P, Ueda R, Hoji A, Ko-hanbash G, Donegan TE, et al. Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol. 2011;29(3):330-6.
103. Mailliard RB, Wankowicz-Kalinska A, Cai Q, Wesa A, Hilkens CM, Kapsenberg ML, et al. alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res. 2004;64(17):5934-7.
104. Zobywalski A, Javorovic M, Frankenberger B, Pohla H, Kremmer E, Bigalke I, et al. Generation of clinical grade dendritic cells with capacity to produce biologically active IL-12p70. J Transl Med. 2007;5:18.
105. Koski GK, Koldovsky U, Xu S, Mick R, Sharma A, Fitzpatrick E, et al. A novel dendritic cell-based immunization approach for the induction of durable Th1-polarized anti-HER-2/neu responses in women with early breast cancer. J Immunother. 2012;35(1):54-65.
106. Dohnal AM, Graffi S, Witt V, Eichstill C, Wagner D, Ul-Haq S, et al. Comparative evaluation of techniques for the manufacturing of dendritic cell-based cancer vaccines. J Cell Mol Med. 2009;13(1):125-35.
107. Vopenkova K, Mollova K, Buresova I, Michalek J. Complex evaluation of human monocyte-de-rived dendritic cells for cancer immunotherapy. J Cell Mol Med. 2012;16(11):2827-37.
108. Evel-Kabler K, Chen SY. Dendritic cell-based tumor vaccines and antigen presentation attenuators. Mol Ther. 2006;13(5):850-8.
109. Mathis D, Benoist C. Back to central tolerance. Immunity. 2004;20(5):509-16.
110. Sioud M, Sorensen D. Generation of an effective anti-tumor immunity after immunization with xenogeneic antigens. Eur J Immunol. 2003;33(1):38-45.
111. Palucka K, Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity. 2013;39(1):38-48.
112. Jonuleit H, Kuhn U, Muller G, Steinbrink K, Paragnik L, Schmitt E, et al. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol. 1997;27(12):3135-42.
113. Bedrosian I, Mick R, Xu S, Nisenbaum H, Faries M, Zhang P, et al. Intranodal administration of peptide-pulsed mature dendritic cell vaccines results in superior CD8+ T-cell function in melanoma patients. J Clin Oncol. 2003;21(20):3826-35.
114. Sharma A, Koldovsky U, Xu S, Mick R, Roses R, Fitzpatrick E, et al. HER-2 pulsed dendritic cell vaccine can eliminate HER-2 expression and impact ductal carcinoma in situ. Cancer. 2012;118(17):4354-62.
115. Van Tendeloo VF, Van de Velde A, Van Driessche A, Cools N, Anguille S, Ladell K, et al. Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci USA. 2010;107(31):13824-9.
116. Small EJ, Schellhammer PF, Higano CS, Redfern CH, Nemunaitis JJ, Valone FH, et al. Placebo-controlled phase III trial of im-munologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer. J Clin Oncol. 2006;24(19):3089-94.
117. Leonhartsberger N, Ramoner R, Falkensam-mer C, Rahm A, Gander H, Holtl L, et al. Quality of life during dendritic cell vaccination against metastatic renal cell carcinoma. Cancer Immunol Immunother. 2012;61(9):1407-13.
118. Huber ML, Haynes L, Parker C, Iversen P. Interdisciplinary critique of sipuleucel-T as im-munotherapy in castration-resistant prostate cancer. J Natl Cancer Inst. 2012;104(4):273-9.
119. Hoos A, Eggermont AM, Janetzki S, Hodi FS, Ibrahim R, Anderson A, et al. Improved endpoints for cancer immunotherapy trials. J Natl Cancer Inst. 2010;102(18):1388-97.
120. Weber J. Ipilimumab: controversies in its development, utility and autoimmune adverse events. Cancer Immunol Immunother. 2009;58(5):823-30.
121. Wolchok JD, Hoos A, O’Day S, Weber JS, Hamid O, Lebbe C, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15(23):7412-20.
122. Tel J, Aarntzen EH, Baba T, Schreibelt G, Schulte BM, Benitez-Ribas D, et al. Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients. Cancer Res. 2013;73(3):1063-75.
123. Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, Angel CE, et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med. 2010;207(6):1247-60.
124. Anguille S, Lion E, Van den Bergh J, Van Acker HH, Willemen Y, Smits EL, et al. In-terleukin-15 dendritic cells as vaccine candidates for cancer immunotherapy. Hum Vaccin Immunother. 2013;9(9):1956-61.
125. Dubsky P, Saito H, Leogier M, Dantin C, Connolly JE, Banchereau J, et al. IL-15-in-duced human DC efficiently prime melanoma-specific naive CD8+ T cells to differentiate into CTL. Eur J Immunol. 2007;37(6):1678-90.
126. Van Nuffel AM, Benteyn D, Wilgenhof S, Corthals J, Heirman C, Neyns B, et al. Intravenous and intradermal TriMix-dendritic cell therapy results in a broad T-cell response and durable tumor response in a chemorefractory stage IV-M1c melanoma patient. Cancer Immunol Immunother. 2012;61(7):1033-43.
127. Lee MK, Xu S, Fitzpatrick EH, Sharma A, Graves HL, Czerniecki BJ. Inhibition of CD4+CD25+ regulatory T cell function and conversion into Th1-like effectors by a Tolllike receptor-activated dendritic cell vaccine. PloS One. 2013;8(11):e74698.
128. Nair S, Boczkowski D, Fassnacht M, Piset-sky D, Gilboa E. Vaccination against the forkhead family transcription factor Foxp3 enhances tumor immunity. Cancer Res. 2007;67(1):371-80.
129. Jacobs JF, Punt CJ, Lesterhuis WJ, Sutmuller RP, Brouwer HM, Scharenborg NM, et al. Dendritic cell vaccination in combination with anti-CD25 monoclonal antibody treatment: a phase I/II study in metastatic melanoma patients. Clin Cancer Res. 2010;16(20):5067-78.
130. Dannull J, Su Z, Rizzieri D, Yang BK, Cole-man D, Yancey D, et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest. 2005;115(12):3623-33.
131. Morse MA, Hobeika AC, Osada T, Serra D, Niedzwiecki D, Lyerly HK, et al. Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines. Blood. 2008;112(3):610-8.
132. Baur AS, Lutz MB, Schierer S, Beltrame L, Theiner G, Zinser E, et al. Denileukin diftitox (ONTAK) induces a tolerogenic phenotype in dendritic cells and stimulates survival of resting Treg. Blood. 2013;122(13):2185-94.
133. Yamada Y, Aoyama A, Tocco G, Boskovic S, Nadazdin O, Alessandrini A, et al. Differential effects of denileukin diftitox IL-2 immunotoxin on NK and regulatory T cells in nonhuman primates. J Immunol. 2012;188(12):6063-70.
134. Valzasina B, Guiducci C, Dislich H, Killeen N, Weinberg AD, Colombo MP. Triggering of OX40 (CD134) on CD4(+)CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR. Blood. 2005;105(7):2845-51.
135. Ko HJ, Kim YJ, Kim YS, Chang WS, Ko SY, Chang SY, et al. A combination of chemoim-munotherapies can efficiently break self-tolerance and induce antitumor immunity in a tolerogenic murine tumor model. Cancer Res. 2007;67(15):7477-86.
136. Casares N, Rudilla F, Arribillaga L, Llopiz D, Riezu-Boj JI, Lozano T, et al. A peptide inhibitor of FOXP3 impairs regulatory T cell activity and improves vaccine efficacy in mice. J Immunol. 2010;185(9):5150-9.
137. Pere H, Montier Y, Bayry J, Quintin-Colonna F, Merillon N, Dransart E, et al. A CCR4 antagonist combined with vaccines induces antigen-specific CD8+ T cells and tumor immunity against self antigens. Blood. 2011;118(18):4853-62.
138. Poschke I, Mao Y, Adamson L, Salazar-On-fray F, Masucci G, Kiessling R. Myeloid-de-rived suppressor cells impair the quality of dendritic cell vaccines. Cancer Immunol Im-munother. 2012;61(6):827-38.
139. Najjar YG, Finke JH. Clinical perspectives on targeting of myeloid derived suppressor cells in the treatment of cancer. Front Oncol. 2013;3:49.
140. Fujita M, Kohanbash G, Fellows-Mayle W, Hamilton RL, Komohara Y, Decker SA, et al. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 2011;71(7):2664-74.
141. Kirkwood JM, Butterfield LH, Tarhini AA, Zarour H, Kalinski P, Ferrone S. Im-munotherapy of cancer in 2012. CA Cancer J Clin. 2012;62(5):309-35.
142. Maker AV, Attia P, Rosenberg SA. Analysis of the cellular mechanism of antitumor responses and autoimmunity in patients treated with CTLA-4 blockade. J Immunol. 2005;175(11):7746-54.
143. Ribas A, Comin-Anduix B, Chmielowski B, Jalil J, de la Rocha P, McCannel TA, et al. Dendritic cell vaccination combined with CTLA4 blockade in patients with metastatic melanoma. Clin Cancer Res. 2009;15(19):6267-76.
144. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. 2013;369(2):134-44.
145. Rosenblatt J, Glotzbecker B, Mills H, Vasir B, Tzachanis D, Levine JD, et al. PD-1 blockade by CT-011, anti-PD-1 antibody, enhances ex vivo T-cell responses to autologous dendritic cell/myeloma fusion vaccine. J Im-munother. 2011;34(5):409-18.
146. Shimizu K, Fields RC, Giedlin M, Mule JJ. Systemic administration of interleukin 2 enhances the therapeutic efficacy of dendritic cell-based tumor vaccines. Proc Natl Acad Sci USA. 1999;96(5):2268-73.
147. Escobar A, Lopez M, Serrano A, Ramirez M, Perez C, Aguirre A, et al. Dendritic cell immunizations alone or combined with low doses of interleukin-2 induce specific immune responses in melanoma patients. Clin Exp Immunol. 2005;142(3):555-68.
148. Redman BG, Chang AE, Whitfield J, Esper P, Jiang G, Braun T, et al. 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. 2008;31(6):591-8.
149. Miller RL, Gerster JF, Owens ML, Slade HB, Tomai MA. Imiquimod applied topically: a novel immune response modifier and new class of drug. Int J Immunopharmacol. 1999;21(1):1-14.
150. Hofmann MA, Kors C, Audring H, Walden P, Sterry W, Trefzer U. Phase 1 evaluation of intralesionally injected TLR9-agonist PF-3512676 in patients with basal cell carcinoma or metastatic melanoma. J Immunother. 2008;31(5):520-7.
151. Muthuswamy R, Berk E, Junecko BF, Zeh HJ, Zureikat AH, Normolle D, et al. NF-kap-paB hyperactivation in tumor tissues allows tumor-selective reprogramming of the chemokine microenvironment to enhance the recruitment of cytolytic T effector cells. Cancer Res. 2012;72(15):3735-43.
152. Weir GM, Liwski RS, Mansour M. Immune modulation by chemotherapy or im-munotherapy to enhance cancer vaccines. Cancers (Basel). 2011;3(3):3114-42.
153. Wheeler CJ, Black KL, Liu G, Mazer M, Zhang XX, Pepkowitz S, et al. Vaccination elicits correlated immune and clinical responses in glioblastoma multiforme patients. Cancer Res. 2008;68(14):5955-64.
154. Zitvogel L, Apetoh L, Ghiringhelli F, Andre F, Tesniere A, Kroemer G. The anticancer immune response: indispensable for therapeutic success? J Clin Invest. 2008;118(6):1991-2001.
155. Ridolfi L, Petrini M, Granato AM, Gentilcore G, Simeone E, Ascierto PA, et al. Low-dose temozolomide before dendritic-cell vaccination reduces (specifically) CD4+CD25++Foxp3+ regulatory T-cells in advanced melanoma patients. J Transl Med. 2013;11:135.
156. Nowak AK, Lake RA, Marzo AL, Scott B, Heath WR, Collins EJ, 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. 2003;170(10):4905-13.
157. Le HK, Graham L, Cha E, Morales JK, Man-jili MH, Bear HD. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int Immunophar-macol. 2009;9(7-8):900-9.
158. von Mehren M, Arlen P, Tsang KY, Rogatko A, Meropol N, Cooper HS, et al. Pilot study of a dual gene recombinant avipox vaccine containing both carcinoembryonic antigen (CEA) and B7.1 transgenes in patients with recurrent CEA-expressing adenocarcinomas. Clin Cancer Res. 2000;6(6):2219-28.
159. Palermo B, Del Bello D, Sottini A, Serana F, Ghidini C, Gualtieri N, et al. Dacarbazine treatment before peptide vaccination enlarges T-cell repertoire diversity of melan-a-spe-cific, tumor-reactive CTL in melanoma patients. Cancer Res. 2010;70(18):7084-92.
160. Antonia SJ, Mirza N, Fricke I, Chiappori A, Thompson P, Williams N, et al. Combination of p53 cancer vaccine with chemotherapy in patients with extensive stage small cell lung cancer. Clin Cancer Res. 2006;12(3 Pt 1):878-87.
161. Lesterhuis WJ, de Vries IJ, Aarntzen EA, de Boer A, Scharenborg NM, van de Rakt M, et al. A pilot study on the immunogenicity of dendritic cell vaccination during adjuvant oxali-platin/capecitabine chemotherapy in colon cancer patients. Br J Cancer. 2010;103(9):1415-21.
162. Hauser SH, Calorini L, Wazer DE, Gattoni-Celli S. Radiation-enhanced expression of major histocompatibility complex class I antigen H-2Db in B16 melanoma cells. Cancer Res. 1993;53(8):1952-5.
163. Hareyama M, Imai K, Kubo K, Takahashi H, Koshiba H, Hinoda Y, et al. Effect of radiation on the expression of carcinoembryonic antigen of human gastric adenocarcinoma cells. Cancer. 1991;67(9):2269-74.
164. Dunn PL, North RJ. Selective radiation resistance of immunologically induced T cells as the basis for irradiation-induced T-cell-me-diated regression of immunogenic tumor. J Leukoc Biol. 1991;49(4):388-96.
165. Zhang B, Bowerman NA, Salama JK, Schmidt H, Spiotto MT, Schietinger A, et al. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med. 2007;204(1):49-55.
166. Heine A, Held SA, Bringmann A, Holderried TA, Brossart P. Immunomodulatory effects of anti-an-giogenic drugs. Leukemia. 2011;25(6):899-905.
167. Ko JS, Zea AH, Rini BI, Ireland JL, Elson P, Cohen P, et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res. 2009;15(6):2148-57.
168. Ozao-Choy J, Ma G, Kao J, Wang GX, Meseck M, Sung M, et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 2009;69(6):2514-22.
169. Knight DA, Ngiow SF, Li M, Parmenter T, Mok S, Cass A, et al. Host immunity contributes to the anti-melanoma activity of BRAF inhibitors. J Clin Invest. 2013;123(3):1371-81.
170. Ott PA, Henry T, Baranda SJ, Frleta D, Manches O, Bogunovic D, et al. 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. 2013;62(4):811-22.