Dendritic cell-based vaccination in cancer: Therapeutic implications emerging from murine models

Frontiers in Immunology

Volumn 6, Issue MAY, 2015, Pages

  Mac Keon, Soledad ^a   Ruiz, María Sol ^b   Gazzaniga, Silvina ^c   Wainstok, Rosa ^a,c  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b Centro de Investigaciones Oncológicas   (Argentina)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Adjuvants; Cancer immunotherapy; Dendritic cell maturation; Dendritic cell subsets; Dendritic cell based vaccines; Dendritic cells

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; DENDRITIC CELL VACCINE; IMIQUIMOD; INDOLEAMINE 2, 3 DIOXYGENASE; INDUCIBLE T CELL COSTIMULATOR; INTERLEUKIN 2 RECEPTOR; OVALBUMIN; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; BONE MARROW DERIVED DENDRITIC CELL; CANCER MODEL; CANCER THERAPY; CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; LANGERHANS CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MONOCYTE; MOUSE; MURINE MODEL; NEOPLASM; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PLASMACYTOID DENDRITIC CELL; REVIEW; TUMOR MICROENVIRONMENT; VACCINATION;

EID: 84934288744     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00243     Document Type: Review

References (222)

1. Coulie PG, Van den Eynde BJ, van der Bruggen P, Boon T. Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat Rev Cancer (2014) 14(2):135-46. doi:10.1038/nrc3670
2. Baitsch L, Fuertes-Marraco SA, Legat A, Meyer C, Speiser DE. The three main stumbling blocks for anticancer T cells. Trends Immunol (2012) 33(7):364-72. doi:10.1016/j.it.2012.02.006
3. Crespo J, Sun H, Welling TH, Tian Z, Zou W. T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. Curr Opin Immunol (2013) 25(2):214-21. doi:10.1016/j.coi.2012.12.003
4. Coulie PG, Brichard V, Van Pel A, Wolfel T, Schneider J, Traversari C, et al. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J Exp Med (1994) 180(1):35-42. doi:10.1084/jem.180.1.35
5. Parmiani G, De Filippo A, Novellino L, Castelli C. Unique human tumor antigens: immunobiology and use in clinical trials. J Immunol (2007) 178(4):1975-9. doi:10.4049/jimmunol.178.4.1975
6. Palucka K, Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity (2013) 39(1):38-48. doi:10.1016/j.immuni.2013.07.004
7. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature (1998) 392(6673):245-52. doi:10.1038/32588
8. Mescher MF, Curtsinger JM, Agarwal P, Casey KA, Gerner M, Hammerbeck CD, et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev (2006) 211:81-92. doi:10.1111/j.0105-2896.2006.00382.x
9. Banerjee A, Gordon SM, Intlekofer AM, Paley MA, Mooney EC, Lindsten T, et al. Cutting edge: the transcription factor eomesodermin enables CD8+ T cells to compete for the memory cell niche. J Immunol (2010) 185(9):4988-92. doi:10.4049/jimmunol.1002042
10. Woo SR, Corrales L, Gajewski TF. Innate immune recognition of cancer. Annu Rev Immunol (2015) 33:445-74. doi:10.1146/annurev-immunol-032414-112043
11. 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. doi:10.1016/S1470-2045(13)70585-0
12. Butterfield LH. Dendritic cells in cancer immunotherapy clinical trials: are we making progress? Front Immunol (2013) 4:454. doi:10.3389/fimmu.2013.00454
13. Galluzzi L, Senovilla L, Vacchelli E, Eggermont A, Fridman WH, Galon J, et al. Trial watch: dendritic cell-based interventions for cancer therapy. Oncoimmunology (2012) 1(7):1111-34. doi:10.4161/onci.21494
14. Steinman RM, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med (1973) 137(5):1142-62. doi:10.1084/jem.137.5.1142
15. Gross L. Intradermal immunization of C3H mice against a sarcoma that originated in an animal of the same line. Cancer Res (1943) 3:326-33.
16. Klein G, Klein E. Immune surveillance against virus-induced tumors and nonrejectability of spontaneous tumors: contrasting consequences of host versus tumor evolution. Proc Natl Acad Sci U S A (1977) 74(5):2121-5. doi:10.1073/pnas.74.5.2121
17. Cheon DJ, Orsulic S. Mouse models of cancer. Annu Rev Pathol (2011) 6:95-119. doi:10.1146/annurev.pathol.3.121806.154244
18. Fidler IJ. Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res (1978) 38(9):2651-60.
19. Nanni P, Colombo MP, De Giovanni C, Lollini PL, Nicoletti G, Parmiani G, et al. Impaired H-2 expression in B16 melanoma variants. J Immunogenet (1983) 10(5):361-70. doi:10.1111/j.1744-313X.1983.tb00348.x
20. Overwijk WW, Restifo NP. B16 as a mouse model for human melanoma. Curr Protoc Immunol (2001) 20:20.1. doi:10.1002/0471142735.im2001s39
21. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature (2002) 417(6892):949-54. doi:10.1038/nature00766
22. Melnikova VO, Bolshakov SV, Walker C, Ananthaswamy HN. Genomic alterations in spontaneous and carcinogen-induced murine melanoma cell lines. Oncogene (2004) 23(13):2347-56. doi:10.1038/sj.onc.1207405
23. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE Jr, et al. Braf (V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet (2009) 41(5):544-52. doi:10.1038/ng.356
24. Jenkins MH, Steinberg SM, Alexander MP, Fisher JL, Ernstoff MS, Turk MJ, et al. Multiple murine BRaf (V600E) melanoma cell lines with sensitivity to PLX4032. Pigment Cell Melanoma Res (2014) 27(3):495-501. doi:10.1111/pcmr.12220
25. Rappaport A, Johnson L. Genetically engineered knock-in and conditional knock-in mouse models of cancer. Cold Spring Harb Protoc (2014) 2014(9):897-911. doi:10.1101/pdb.top069799
26. Williams SA, Anderson WC, Santaguida MT, Dylla SJ. Patient-derived xenografts, the cancer stem cell paradigm, and cancer pathobiology in the 21st century. Lab Invest (2013) 93(9):970-82. doi:10.1038/labinvest.2013.92
27. Shultz LD, Brehm MA, Garcia-Martinez JV, Greiner DL. Humanized mice for immune system investigation: progress, promise and challenges. Nat Rev Immunol (2012) 12(11):786-98. doi:10.1038/nri3311
28. Sugamura K, Asao H, Kondo M, Tanaka N, Ishii N, Ohbo K, et al. The interleukin-2 receptor gamma chain: its role in the multiple cytokine receptor complexes and T cell development in XSCID. Annu Rev Immunol (1996) 14:179-205. doi:10.1146/annurev.immunol.14.1.179
29. Cao X, Shores EW, Hu-Li J, Anver MR, Kelsall BL, Russell SM, et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity (1995) 2(3):223-38. doi:10.1016/1074-7613(95)90047-0
30. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol (2005) 174(10):6477-89. doi:10.4049/jimmunol.174.10.6477
31. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol (2007) 7(2):118-30. doi:10.1038/nri2017
32. Spranger S, Frankenberger B, Schendel DJ. NOD/scid IL-2Rg (null) mice: a preclinical model system to evaluate human dendritic cell-based vaccine strategies in vivo. J Transl Med (2012) 10:30. doi:10.1186/1479-5876-10-30
33. Harui A, Kiertscher SM, Roth MD. Reconstitution of huPBL-NSG mice with donor-matched dendritic cells enables antigen-specific T-cell activation. J Neuroimmune Pharmacol (2011) 6(1):148-57. doi:10.1007/s11481-010-9223-x
34. Rongvaux A, Willinger T, Martinek J, Strowig T, Gearty SV, Teichmann LL, et al. Development and function of human innate immune cells in a humanized mouse model. Nat Biotechnol (2014) 32(4):364-72. doi:10.1038/nbt.2858
35. Drake AC, Chen Q, Chen J. Engineering humanized mice for improved hematopoietic reconstitution. Cell Mol Immunol (2012) 9(3):215-24. doi:10.1038/cmi.2012.6
36. Morse MA, Zhou LJ, Tedder TF, Lyerly HK, Smith C. Generation of dendritic cells in vitro from peripheral blood mononuclear cells with granulocyte-macrophage-colony-stimulating factor, interleukin-4, and tumor necrosis factor-alpha for use in cancer immunotherapy. Ann Surg (1997) 226(1):6-16. doi:10.1097/00000658-199707000-00002
37. Mitchell D, Yong M, Schroder W, Black M, Tirrell M, Olive C. Dual stimulation of MyD88-dependent toll-like receptors induces synergistically enhanced production of inflammatory cytokines in murine bone marrow-derived dendritic cells. J Infect Dis (2010) 202(2):318-29. doi:10.1086/653499
38. Mac Keon S, Gazzaniga S, Mallerman J, Bravo AI, Mordoh J, Wainstok R. Vaccination with dendritic cells charged with apoptotic/necrotic B16 melanoma induces the formation of subcutaneous lymphoid tissue. Vaccine (2010) 28(51):8162-8. doi:10.1016/j.vaccine.2010.09.095
39. Ruiz MS, Mac Keon S, Campisano S, Bravo AI, Gazzaniga S, Wainstok R. CD207 (+) cells recruitment to the vaccination site and draining lymph nodes after the administration of DC-Apo/Nec vaccine in mice. Vaccine (2014) 32(11):1229-32. doi:10.1016/j.vaccine.2014.01.025
40. Suzuki H, Wang B, Shivji GM, Toto P, Amerio P, Tomai MA, et al. Imiquimod, a topical immune response modifier, induces migration of Langerhans cells. J Invest Dermatol (2000) 114(1):135-41. doi:10.1046/j.1523-1747.2000.00833.x
41. Nair S, McLaughlin C, Weizer A, Su Z, Boczkowski D, Dannull J, et al. Injection of immature dendritic cells into adjuvant-treated skin obviates the need for ex vivo maturation. J Immunol (2003) 171(11):6275-82. doi:10.4049/jimmunol.171.11.6275
42. Wei H, Wang S, Zhang D, Hou S, Qian W, Li B, et al. Targeted delivery of tumor antigens to activated dendritic cells via CD11c molecules induces potent antitumor immunity in mice. Clin Cancer Res (2009) 15(14):4612-21. doi:10.1158/1078-0432.CCR-08-3321
43. Wang B, Zaidi N, He LZ, Zhang L, Kuroiwa JM, Keler T, et al. Targeting of the non-mutated tumor antigen HER2/neu to mature dendritic cells induces an integrated immune response that protects against breast cancer in mice. Breast Cancer Res (2012) 14(2):R39. doi:10.1186/bcr3135
44. Matheoud D, Perie L, Hoeffel G, Vimeux L, Parent I, Maranon C, et al. Cross-presentation by dendritic cells from live cells induces protective immune responses in vivo. Blood (2010) 115(22):4412-20. doi:10.1182/blood-2009-11-255935
45. Matheoud D, Baey C, Vimeux L, Tempez A, Valente M, Louche P, et al. Dendritic cells crosspresent antigens from live B16 cells more efficiently than from apoptotic cells and protect from melanoma in a therapeutic model. PLoS One (2011) 6(4):e19104. doi:10.1371/journal.pone.0019104
46. Ma F, Zhang J, Zhang C. The TLR7 agonists imiquimod and gardiquimod improve DC-based immunotherapy for melanoma in mice. Cell Mol Immunol (2010) 7(5):381-8. doi:10.1038/cmi.2010.30
47. Flacher V, Tripp CH, Mairhofer DG, Steinman RM, Stoitzner P, Idoyaga J, et al. Murine Langerin+ dermal dendritic cells prime CD8+ T cells while Langerhans cells induce cross-tolerance. EMBO Mol Med (2014) 6(9):1191-204. doi:10.15252/emmm.201303283
48. Keller AM, Xiao Y, Peperzak V, Naik SH, Borst J. Costimulatory ligand CD70 allows induction of CD8+ T-cell immunity by immature dendritic cells in a vaccination setting. Blood (2009) 113(21):5167-75. doi:10.1182/blood-2008-03-148007
49. Sanchez PJ, McWilliams JA, Haluszczak C, Yagita H, Kedl RM. Combined TLR/CD40 stimulation mediates potent cellular immunity by regulating dendritic cell expression of CD70 in vivo. J Immunol (2007) 178(3):1564-72. doi:10.4049/jimmunol.178.3.1564
50. McWilliams JA, Sanchez PJ, Haluszczak C, Gapin L, Kedl RM. Multiple innate signaling pathways cooperate with CD40 to induce potent, CD70-dependent cellular immunity. Vaccine (2010) 28(6):1468-76. doi:10.1016/j.vaccine.2009.11.071
51. Eberting CL, Shrayer DP, Butmarc J, Falanga V. Histologic progression of B16 F10 metastatic melanoma in C57BL/6 mice over a six week time period: distant metastases before local growth. J Dermatol (2004) 31(4):299-304. doi:10.1111/j.1346-8138.2004.tb00676.x
52. Bobek V, Kolostova K, Pinterova D, Kacprzak G, Adamiak J, Kolodziej J, et al. A clinically relevant, syngeneic model of spontaneous, highly metastatic B16 mouse melanoma. Anticancer Res (2010) 30(12):4799-803.
53. Xia S, Wei J, Wang J, Sun H, Zheng W, Li Y, et al. A requirement of dendritic cell-derived interleukin-27 for the tumor infiltration of regulatory T cells. J Leukoc Biol (2014) 95(5):733-42. doi:10.1189/jlb.0713371
54. Richmond A, Su Y. Mouse xenograft models vs GEM models for human cancer therapeutics. Dis Model Mech (2008) 1(2-3):78-82. doi:10.1242/dmm.000976
55. Oflazoglu E, Elliott M, Takita H, Ferrone S, Henderson RA, Repasky EA. Adoptively transferred human lung tumor specific cytotoxic T cells can control autologous tumor growth and shape tumor phenotype in a SCID mouse xenograft model. J Transl Med (2007) 5:29. doi:10.1186/1479-5876-5-29
56. Hylander BL, Punt N, Tang H, Hillman J, Vaughan M, Bshara W, et al. Origin of the vasculature supporting growth of primary patient tumor xenografts. J Transl Med (2013) 11:110. doi:10.1186/1479-5876-11-110
57. Eirew P, Steif A, Khattra J, Ha G, Yap D, Farahani H, et al. Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution. Nature (2014) 518:422-6. doi:10.1038/nature13952
58. Pino S, Brehm MA, Covassin-Barberis L, King M, Gott B, Chase TH, et al. Development of novel major histocompatibility complex class I and class II-deficient NOD-SCID IL2R gamma chain knockout mice for modeling human xenogeneic graft-versus-host disease. Methods Mol Biol (2010) 602:105-17. doi:10.1007/978-1-60761-058-8_7
59. Mishra S, Lavelle BJ, Desrosiers J, Ardito MT, Terry F, Martin WD, et al. Dendritic cell-mediated, DNA-based vaccination against hepatitis C induces the multi-epitope-specific response of humanized, HLA transgenic mice. PLoS One (2014) 9(8):e104606. doi:10.1371/journal.pone.0104606
60. Meixlsperger S, Leung CS, Ramer PC, Pack M, Vanoaica LD, Breton G, et al. CD141+ dendritic cells produce prominent amounts of IFN-alpha after dsRNA recognition and can be targeted via DEC-205 in humanized mice. Blood (2013) 121(25):5034-44. doi:10.1182/blood-2012-12-473413
61. Malissen B, Tamoutounour S, Henri S. The origins and functions of dendritic cells and macrophages in the skin. Nat Rev Immunol (2014) 14(6):417-28. doi:10.1038/nri3683
62. Merad M, Sathe P, Helft J, Miller J, Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol (2013) 31:563-604. doi:10.1146/annurev-immunol-020711-074950
63. Miller JC, Brown BD, Shay T, Gautier EL, Jojic V, Cohain A, et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol (2012) 13(9):888-99. doi:10.1038/ni.2370
64. Belz GT, Nutt SL. Transcriptional programming of the dendritic cell network. Nat Rev Immunol (2012) 12(2):101-13. doi:10.1038/nri3149
65. Stoecklinger A, Eticha TD, Mesdaghi M, Kissenpfennig A, Malissen B, Thalhamer J, et al. Langerin+ dermal dendritic cells are critical for CD8+ T cell activation and IgH gamma-1 class switching in response to gene gun vaccines. J Immunol (2011) 186(3):1377-83. doi:10.4049/jimmunol.1002557
66. 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. doi:10.1126/science.1136080
67. Xu Y, Zhan Y, Lew AM, Naik SH, Kershaw MH. Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J Immunol (2007) 179(11):7577-84. doi:10.4049/jimmunol.179.11.7577
68. Naik SH, Proietto AI, Wilson NS, Dakic A, Schnorrer P, Fuchsberger M, et al. Cutting edge: generation of splenic CD8+ and CD8-dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J Immunol (2005) 174(11):6592-7. doi:10.4049/jimmunol.174.11.6592
69. Dalod M, Chelbi R, Malissen B, Lawrence T. Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J (2014) 33(10):1104-16. doi:10.1002/embj.201488027
70. Schlitzer A, McGovern N, Teo P, Zelante T, Atarashi K, Low D, et al. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity (2013) 38(5):970-83. doi:10.1016/j.immuni.2013.04.011
71. Shortman K, Heath WR. The CD8+ dendritic cell subset. Immunol Rev (2010) 234(1):18-31. doi:10.1111/j.0105-2896.2009.00870.x
72. Ginhoux F, Liu K, Helft J, Bogunovic M, Greter M, Hashimoto D, et al. The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med (2009) 206(13):3115-30. doi:10.1084/jem.20091756
73. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol (2004) 5(10):987-95. doi:10.1038/ni1112
74. Mitsui H, Watanabe T, Saeki H, Mori K, Fujita H, Tada Y, et al. Differential expression and function of toll-like receptors in Langerhans cells: comparison with splenic dendritic cells. J Invest Dermatol (2004) 122(1):95-102. doi:10.1046/j.0022-202X.2003.22116.x
75. Sancho D, Mourao-Sa D, Joffre OP, Schulz O, Rogers NC, Pennington DJ, et al. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J Clin Invest (2008) 118(6):2098-110. doi:10.1172/JCI34584
76. Liu K, Victora GD, Schwickert TA, Guermonprez P, Meredith MM, Yao K, et al. In vivo analysis of dendritic cell development and homeostasis. Science (2009) 324(5925):392-7. doi:10.1126/science.1170540
77. Heng TS, Painter MW. The immunological genome project: networks of gene expression in immune cells. Nat Immunol (2008) 9(10):1091-4. doi:10.1038/ni1008-1091
78. Drobits B, Holcmann M, Amberg N, Swiecki M, Grundtner R, Hammer M, et al. Imiquimod clears tumors in mice independent of adaptive immunity by converting pDCs into tumor-killing effector cells. J Clin Invest (2012) 122(2):575-85. doi:10.1172/JCI61034
79. Mouries J, Moron G, Schlecht G, Escriou N, Dadaglio G, Leclerc C. Plasmacytoid dendritic cells efficiently cross-prime naive T cells in vivo after TLR activation. Blood (2008) 112(9):3713-22. doi:10.1182/blood-2008-03-146290
80. Guery L, Dubrot J, Lippens C, Brighouse D, Malinge P, Irla M, et al. Ag-presenting CpG-activated pDCs prime Th17 cells that induce tumor regression. Cancer Res (2014) 74(22):6430-40. doi:10.1158/0008-5472.CAN-14-1149
81. Liu C, Lou Y, Lizee G, Qin H, Liu S, Rabinovich B, et al. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J Clin Invest (2008) 118(3):1165-75. doi:10.1172/JCI33583
82. Treilleux I, Blay JY, Bendriss-Vermare N, Ray-Coquard I, Bachelot T, Guastalla JP, et al. Dendritic cell infiltration and prognosis of early stage breast cancer. Clin Cancer Res (2004) 10(22):7466-74. doi:10.1158/1078-0432.CCR-04-0684
83. Sisirak V, Faget J, Gobert M, Goutagny N, Vey N, Treilleux I, et al. Impaired IFN-alpha production by plasmacytoid dendritic cells favors regulatory T-cell expansion that may contribute to breast cancer progression. Cancer Res (2012) 72(20):5188-97. doi:10.1158/0008-5472.CAN-11-3468
84. Wei S, Kryczek I, Zou L, Daniel B, Cheng P, Mottram P, et al. Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res (2005) 65(12):5020-6. doi:10.1158/0008-5472.CAN-04-4043
85. Watkins SK, Zhu Z, Riboldi E, Shafer-Weaver KA, Stagliano KE, Sklavos MM, et al. FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer. J Clin Invest (2011) 121(4):1361-72. doi:10.1172/JCI44325
86. Conrad C, Gregorio J, Wang YH, Ito T, Meller S, Hanabuchi S, et al. Plasmacytoid dendritic cells promote immunosuppression in ovarian cancer via ICOS costimulation of Foxp3 (+) T-regulatory cells. Cancer Res (2012) 72(20):5240-9. doi:10.1158/0008-5472.CAN-12-2271
87. Sorrentino R, Morello S, Luciano A, Crother TR, Maiolino P, Bonavita E, et al. Plasmacytoid dendritic cells alter the antitumor activity of CpG-oligodeoxynucleotides in a mouse model of lung carcinoma. J Immunol (2010) 185(8):4641-50. doi:10.4049/jimmunol.1000881
88. Le Mercier I, Poujol D, Sanlaville A, Sisirak V, Gobert M, Durand I, et al. Tumor promotion by intratumoral plasmacytoid dendritic cells is reversed by TLR7 ligand treatment. Cancer Res (2013) 73(15):4629-40. doi:10.1158/0008-5472.CAN-12-3058
89. Blasius AL, Giurisato E, Cella M, Schreiber RD, Shaw AS, Colonna M. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J Immunol (2006) 177(5):3260-5. doi:10.4049/jimmunol.177.5.3260
90. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest (2007) 117(9):2570-82. doi:10.1172/JCI31911
91. Johnson BA III, Kahler DJ, Baban B, Chandler PR, Kang B, Shimoda M, et al. B-lymphoid cells with attributes of dendritic cells regulate T cells via indoleamine 2,3-dioxygenase. Proc Natl Acad Sci U S A (2010) 107(23):10644-8. doi:10.1073/pnas.0914347107
92. Vinay DS, Kim CH, Chang KH, Kwon BS. PDCA expression by B lymphocytes reveals important functional attributes. J Immunol (2010) 184(2):807-15. doi:10.4049/jimmunol.0902528
93. Faget J, Bendriss-Vermare N, Gobert M, Durand I, Olive D, Biota C, et al. ICOS-ligand expression on plasmacytoid dendritic cells supports breast cancer progression by promoting the accumulation of immunosuppressive CD4+ T cells. Cancer Res (2012) 72(23):6130-41. doi:10.1158/0008-5472.CAN-12-2409
94. Borkowski TA, Letterio JJ, Farr AG, Udey MC. A role for endogenous transforming growth factor beta 1 in Langerhans cell biology: the skin of transforming growth factor beta 1 null mice is devoid of epidermal Langerhans cells. J Exp Med (1996) 184(6):2417-22. doi:10.1084/jem.184.6.2417
95. Nagao K, Ginhoux F, Leitner WW, Motegi S, Bennett CL, Clausen BE, et al. Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci U S A (2009) 106(9):3312-7. doi:10.1073/pnas.0807126106
96. Poulin LF, Henri S, de Bovis B, Devilard E, Kissenpfennig A, Malissen B. The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med (2007) 204(13):3119-31. doi:10.1084/jem.20071724
97. Ginhoux F, Collin MP, Bogunovic M, Abel M, Leboeuf M, Helft J, et al. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med (2007) 204(13):3133-46. doi:10.1084/jem.20071733
98. Douillard P, Stoitzner P, Tripp CH, Clair-Moninot V, Ait-Yahia S, McLellan AD, et al. Mouse lymphoid tissue contains distinct subsets of langerin/CD207 dendritic cells, only one of which represents epidermal-derived Langerhans cells. J Invest Dermatol (2005) 125(5):983-94. doi:10.1111/j.0022-202X.2005.23951.x
99. Flacher V, Douillard P, Ait-Yahia S, Stoitzner P, Clair-Moninot V, Romani N, et al. Expression of langerin/CD207 reveals dendritic cell heterogeneity between inbred mouse strains. Immunology (2008) 123(3):339-47. doi:10.1111/j.1365-2567.2007.02785.x
100. Henri S, Poulin LF, Tamoutounour S, Ardouin L, Guilliams M, de Bovis B, et al. CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med (2010) 207(1):189-206. doi:10.1084/jem.20091964
101. Idoyaga J, Cheong C, Suda K, Suda N, Kim JY, Lee H, et al. Cutting edge: langerin/CD207 receptor on dendritic cells mediates efficient antigen presentation on MHC I and II products in vivo. J Immunol (2008) 180(6):3647-50. doi:10.4049/jimmunol.180.6.3647
102. Stoitzner P, Green LK, Jung JY, Price KM, Tripp CH, Malissen B, et al. Tumor immunotherapy by epicutaneous immunization requires Langerhans cells. J Immunol (2008) 180(3):1991-8. doi:10.4049/jimmunol.180.3.1991
103. Flacher V, Tripp CH, Stoitzner P, Haid B, Ebner S, Del Frari B, et al. Epidermal Langerhans cells rapidly capture and present antigens from C-type lectin-targeting antibodies deposited in the dermis. J Invest Dermatol (2010) 130(3):755-62. doi:10.1038/jid.2009.343
104. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science (2008) 322(5904):1097-100. doi:10.1126/science.1164206
105. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM, Murphy KM, et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8{alpha}+ dendritic cells. J Exp Med (2011) 208(10):2005-16. doi:10.1084/jem.20101159
106. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med (2011) 208(10):1989-2003. doi:10.1084/jem.20101158
107. Azadmehr A, Pourfathollah AA, Amirghofran Z, Hassan ZM, Moazzeni SM. Enhancement of Th1 immune response by CD8alpha (+) dendritic cells loaded with heat shock proteins enriched tumor extract in tumor-bearing mice. Cell Immunol (2009) 260(1):28-32. doi:10.1016/j.cellimm.2009.07.003
108. Farrand KJ, Dickgreber N, Stoitzner P, Ronchese F, Petersen TR, Hermans IF. Langerin+ CD8alpha+ dendritic cells are critical for cross-priming and IL-12 production in response to systemic antigens. J Immunol (2009) 183(12):7732-42. doi:10.4049/jimmunol.0902707
109. Macho-Fernandez E, Cruz LJ, Ghinnagow R, Fontaine J, Bialecki E, Frisch B, et al. Targeted delivery of alpha-galactosylceramide to CD8alpha+ dendritic cells optimizes type I NKT cell-based antitumor responses. J Immunol (2014) 193(2):961-9. doi:10.4049/jimmunol.1303029
110. Arora P, Baena A, Yu KO, Saini NK, Kharkwal SS, Goldberg MF, et al. A single subset of dendritic cells controls the cytokine bias of natural killer T cell responses to diverse glycolipid antigens. Immunity (2014) 40(1):105-16. doi:10.1016/j.immuni.2013.12.004
111. Salio M, Silk JD, Cerundolo V. Recent advances in processing and presentation of CD1 bound lipid antigens. Curr Opin Immunol (2010) 22(1):81-8. doi:10.1016/j.coi.2009.12.008
112. Poulin LF, Reyal Y, Uronen-Hansson H, Schraml BU, Sancho D, Murphy KM, et al. DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood (2012) 119(25):6052-62. doi:10.1182/blood-2012-01-406967
113. Cerovic V, Houston SA, Scott CL, Aumeunier A, Yrlid U, Mowat AM, et al. Intestinal CD103 (-) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol (2013) 6(1):104-13. doi:10.1038/mi.2012.53
114. Desch AN, Randolph GJ, Murphy K, Gautier EL, Kedl RM, Lahoud MH, et al. CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J Exp Med (2011) 208(9):1789-97. doi:10.1084/jem.20110538
115. Decrausaz L, Domingos-Pereira S, Duc M, Bobst M, Romero P, Schiller JT, et al. Parenteral is more efficient than mucosal immunization to induce regression of human papillomavirus-associated genital tumors. Int J Cancer (2011) 129(3):762-72. doi:10.1002/ijc.25973
116. Sandoval F, Terme M, Nizard M, Badoual C, Bureau MF, Freyburger L, et al. Mucosal imprinting of vaccine-induced CD8 (+) T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med (2013) 5(172):172ra20. doi:10.1126/scitranslmed.3004888
117. Kim-Schulze S, Kim HS, Wainstein A, Kim DW, Yang WC, Moroziewicz D, et al. Intrarectal vaccination with recombinant vaccinia virus expressing carcinoembronic antigen induces mucosal and systemic immunity and prevents progression of colorectal cancer. J Immunol (2008) 181(11):8112-9. doi:10.4049/jimmunol.181.11.8112
118. Broz ML, Binnewies M, Boldajipour B, Nelson AE, Pollack JL, Erle DJ, et al. Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell (2014) 26(5):638-52. doi:10.1016/j.ccell.2014.09.007
119. Woo SR, Fuertes MB, Corrales L, Spranger S, Furdyna MJ, Leung MY, et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity (2014) 41(5):830-42. doi:10.1016/j.immuni.2014.10.017
120. Schulz O, Jaensson E, Persson EK, Liu X, Worbs T, Agace WW, et al. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med (2009) 206(13):3101-14. doi:10.1084/jem.20091925
121. Lewis KL, Caton ML, Bogunovic M, Greter M, Grajkowska LT, Ng D, et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity (2011) 35(5):780-91. doi:10.1016/j.immuni.2011.08.013
122. Guermonprez P, Khelef N, Blouin E, Rieu P, Ricciardi-Castagnoli P, Guiso N, et al. The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha (M)beta (2) integrin (CD11b/CD18). J Exp Med (2001) 193(9):1035-44. doi:10.1084/jem.193.9.1035
123. Dadaglio G, Fayolle C, Zhang X, Ryffel B, Oberkampf M, Felix T, et al. Antigen targeting to CD11b+ dendritic cells in association with TLR4/TRIF signaling promotes strong CD8+ T cell responses. J Immunol (2014) 193(4):1787-98. doi:10.4049/jimmunol.1302974
124. Segura E, Amigorena S. Inflammatory dendritic cells in mice and humans. Trends Immunol (2013) 34(9):440-5. doi:10.1016/j.it.2013.06.001
125. Dominguez PM, Ardavin C. Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol Rev (2010) 234(1):90-104. doi:10.1111/j.0105-2896.2009.00876.x
126. Nagai Y, Garrett KP, Ohta S, Bahrun U, Kouro T, Akira S, et al. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity (2006) 24(6):801-12. doi:10.1016/j.immuni.2006.04.008
127. Segura E, Amigorena S. Identification of human inflammatory dendritic cells. Oncoimmunology (2013) 2(5):e23851. doi:10.4161/onci.23851
128. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity (2013) 38(4):729-41. doi:10.1016/j.immuni.2013.03.003
129. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med (1992) 176(6):1693-702. doi:10.1084/jem.176.6.1693
130. Labeur MS, Roters B, Pers B, Mehling A, Luger TA, Schwarz T, et al. Generation of tumor immunity by bone marrow-derived dendritic cells correlates with dendritic cell maturation stage. J Immunol (1999) 162(1):168-75.
131. Goldszmid RS, Idoyaga J, Bravo AI, Steinman R, Mordoh J, Wainstok R. Dendritic cells charged with apoptotic tumor cells induce long-lived protective CD4+ and CD8+ T cell immunity against B16 melanoma. J Immunol (2003) 171(11):5940-7. doi:10.4049/jimmunol.171.11.5940
132. Campisano S, Mac Keon S, Gazzaniga S, Ruiz MS, Traian MD, Mordoh J, et al. Anti-melanoma vaccinal capacity of CD11c-positive and-negative cell populations present in GM-CSF cultures derived from murine bone marrow precursors. Vaccine (2013) 31(2):354-61. doi:10.1016/j.vaccine.2012.10.114
133. Brasel K, De Smedt T, Smith JL, Maliszewski CR. Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood (2000) 96(9):3029-39.
134. Chen W, Antonenko S, Sederstrom JM, Liang X, Chan AS, Kanzler H, et al. Thrombopoietin cooperates with FLT3-ligand in the generation of plasmacytoid dendritic cell precursors from human hematopoietic progenitors. Blood (2004) 103(7):2547-53. doi:10.1182/blood-2003-09-3058
135. Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen JL, et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med (2010) 207(6):1261-71. doi:10.1084/jem.20092618
136. Balan S, Ollion V, Colletti N, Chelbi R, Montanana-Sanchis F, Liu H, et al. Human XCR1+ dendritic cells derived in vitro from CD34+ progenitors closely resemble blood dendritic cells, including their adjuvant responsiveness, contrary to monocyte-derived dendritic cells. J Immunol (2014) 193(4):1622-35. doi:10.4049/jimmunol.1401243
137. Lee J, Breton G, Oliveira TY, Zhou YJ, Aljoufi A, Puhr S, et al. Restricted dendritic cell and monocyte progenitors in human cord blood and bone marrow. J Exp Med (2015) 212(3):385-99. doi:10.1084/jem.20141442
138. Petersen TR, Sika-Paotonu D, Knight DA, Simkins HM, Hermans IF. Exploiting the role of endogenous lymphoid-resident dendritic cells in the priming of NKT cells and CD8+ T cells to dendritic cell-based vaccines. PLoS One (2011) 6(3):e17657. doi:10.1371/journal.pone.0017657
139. Allan RS, Waithman J, Bedoui S, Jones CM, Villadangos JA, Zhan Y, et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity (2006) 25(1):153-62. doi:10.1016/j.immuni.2006.04.017
140. Kleindienst P, Brocker T. Endogenous dendritic cells are required for amplification of T cell responses induced by dendritic cell vaccines in vivo. J Immunol (2003) 170(6):2817-23. doi:10.4049/jimmunol.170.6.2817
141. Yewdall AW, Drutman SB, Jinwala F, Bahjat KS, Bhardwaj N. CD8+ T cell priming by dendritic cell vaccines requires antigen transfer to endogenous antigen presenting cells. PLoS One (2010) 5(6):e11144. doi:10.1371/journal.pone.0011144
142. Ali OA, Emerich D, Dranoff G, Mooney DJ. In situ regulation of DC subsets and T cells mediates tumor regression in mice. Sci Transl Med (2009) 1(8):8ra19. doi:10.1126/scitranslmed.3000359
143. Lou Y, Liu C, Kim GJ, Liu YJ, Hwu P, Wang G. Plasmacytoid dendritic cells synergize with myeloid dendritic cells in the induction of antigen-specific antitumor immune responses. J Immunol (2007) 178(3):1534-41. doi:10.4049/jimmunol.178.3.1534
144. Dolan BP, Gibbs KD Jr, Ostrand-Rosenberg S. Dendritic cells cross-dressed with peptide MHC class I complexes prime CD8+ T cells. J Immunol (2006) 177(9):6018-24. doi:10.4049/jimmunol.177.9.6018
145. Dolan BP, Gibbs KD Jr, Ostrand-Rosenberg S. Tumor-specific CD4+ T cells are activated by "cross-dressed" dendritic cells presenting peptide-MHC class II complexes acquired from cell-based cancer vaccines. J Immunol (2006) 176(3):1447-55. doi:10.4049/jimmunol.176.3.1447
146. Li L, Kim S, Herndon JM, Goedegebuure P, Belt BA, Satpathy AT, et al. Cross-dressed CD8alpha+/CD103+ dendritic cells prime CD8+ T cells following vaccination. Proc Natl Acad Sci U S A (2012) 109(31):12716-21. doi:10.1073/pnas.1203468109
147. Groettrup M, Kirk CJ, Basler M. Proteasomes in immune cells: more than peptide producers? Nat Rev Immunol (2010) 10(1):73-8. doi:10.1038/nri2687
148. Guillaume B, Stroobant V, Bousquet-Dubouch MP, Colau D, Chapiro J, Parmentier N, et al. Analysis of the processing of seven human tumor antigens by intermediate proteasomes. J Immunol (2012) 189(7):3538-47. doi:10.4049/jimmunol.1103213
149. Macagno A, Gilliet M, Sallusto F, Lanzavecchia A, Nestle FO, Groettrup M. Dendritic cells up-regulate immunoproteasomes and the proteasome regulator PA28 during maturation. Eur J Immunol (1999) 29(12):4037-42. doi:10.1002/(SICI)1521-4141(199912)29:12 <4037::AID-IMMU4037> 3.0.CO;2-T
150. Dannull J, Haley NR, Archer G, Nair S, Boczkowski D, Harper M, et al. Melanoma immunotherapy using mature DCs expressing the constitutive proteasome. J Clin Invest (2013) 123(7):3135-45. doi:10.1172/JCI67544
151. Butterfield LH, Palucka AK, Britten CM, Dhodapkar MV, Hakansson L, Janetzki S, et al. Recommendations from the iSBTc-SITC/FDA/NCI workshop on immunotherapy biomarkers. Clin Cancer Res (2011) 17(10):3064-76. doi:10.1158/1078-0432.CCR-10-2234
152. Castle JC, Kreiter S, Diekmann J, Lower M, van de Roemer N, de Graaf J, et al. Exploiting the mutanome for tumor vaccination. Cancer Res (2012) 72(5):1081-91. doi:10.1158/0008-5472.CAN-11-3722
153. Casey DG, Lysaght J, James T, Bateman A, Melcher AA, Todryk SM. Heat shock protein derived from a non-autologous tumour can be used as an anti-tumour vaccine. Immunology (2003) 110(1):105-11. doi:10.1046/j.1365-2567.2003.01726.x
154. Li B, Simmons A, Du T, Lin C, Moskalenko M, Gonzalez-Edick M, et al. Allogeneic GM-CSF-secreting tumor cell immunotherapies generate potent anti-tumor responses comparable to autologous tumor cell immunotherapies. Clin Immunol (2009) 133(2):184-97. doi:10.1016/j.clim.2009.07.008
155. Ning N, Pan Q, Zheng F, Teitz-Tennenbaum S, Egenti M, Yet J, et al. Cancer stem cell vaccination confers significant antitumor immunity. Cancer Res (2012) 72(7):1853-64. doi:10.1158/0008-5472.CAN-11-1400
156. Teitz-Tennenbaum S, Wicha MS, Chang AE, Li Q. Targeting cancer stem cells via dendritic-cell vaccination. Oncoimmunology (2012) 1(8):1401-3. doi:10.4161/onci.21026
157. Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med (2000) 191(3):423-34. doi:10.1084/jem.191.3.423
158. Fry TJ, Shand JL, Milliron M, Tasian SK, Mackall CL. Antigen loading of DCs with irradiated apoptotic tumor cells induces improved anti-tumor immunity compared to other approaches. Cancer Immunol Immunother (2009) 58(8):1257-64. doi:10.1007/s00262-008-0638-7
159. Deng L, Liang H, Xu M, Yang X, Burnette B, Arina A, et al. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity (2014) 41(5):843-52. doi:10.1016/j.immuni.2014.10.019
160. Schnurr M, Scholz C, Rothenfusser S, Galambos P, Dauer M, Robe J, et al. Apoptotic pancreatic tumor cells are superior to cell lysates in promoting cross-priming of cytotoxic T cells and activate NK and gammadelta T cells. Cancer Res (2002) 62(8):2347-52.
161. Inzkirweli N, Guckel B, Sohn C, Wallwiener D, Bastert G, Lindner M. Antigen loading of dendritic cells with apoptotic tumor cell-preparations is superior to that using necrotic cells or tumor lysates. Anticancer Res (2007) 27(4B):2121-9.
162. Yoon TJ, Kim JY, Kim H, Hong C, Lee H, Lee CK, et al. Anti-tumor immunostimulatory effect of heat-killed tumor cells. Exp Mol Med (2008) 40(1):130-44. doi:10.3858/emm.2008.40.1.130
163. Kawahara M, Takaku H. Intradermal immunization with combined baculovirus and tumor cell lysate induces effective antitumor immunity in mice. Int J Oncol (2013) 43(6):2023-30. doi:10.3892/ijo.2013.2125
164. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol (2013) 31:51-72. doi:10.1146/annurev-immunol-032712-100008
165. Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer (2012) 12(12):860-75. doi:10.1038/nrc3380
166. Todryk S, Melcher AA, Hardwick N, Linardakis E, Bateman A, Colombo MP, et al. Heat shock protein 70 induced during tumor cell killing induces Th1 cytokines and targets immature dendritic cell precursors to enhance antigen uptake. J Immunol (1999) 163(3):1398-408.
167. Calderwood SK, Theriault JR, Gong J. How is the immune response affected by hyperthermia and heat shock proteins? Int J Hyperthermia (2005) 21(8):713-6. doi:10.1080/02656730500340794
168. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med (2000) 6(4):435-42. doi:10.1038/74697
169. Wang XY, Yi H, Yu X, Zuo D, Subjeck JR. Enhancing antigen cross-presentation and T-cell priming by complexing protein antigen to recombinant large heat-shock protein. Methods Mol Biol (2011) 787:277-87. doi:10.1007/978-1-61779-295-3_21
170. Jiang J, Xie D, Zhang W, Xiao G, Wen J. Fusion of Hsp70 to Mage-a1 enhances the potency of vaccine-specific immune responses. J Transl Med (2013) 11:300. doi:10.1186/1479-5876-11-300
171. McNulty S, Colaco CA, Blandford LE, Bailey CR, Baschieri S, Todryk S. Heat-shock proteins as dendritic cell-targeting vaccines-getting warmer. Immunology (2013) 139(4):407-15. doi:10.1111/imm.12104
172. Enomoto Y, Bharti A, Khaleque AA, Song B, Liu C, Apostolopoulos V, et al. Enhanced immunogenicity of heat shock protein 70 peptide complexes from dendritic cell-tumor fusion cells. J Immunol (2006) 177(9):5946-55. doi:10.4049/jimmunol.177.9.5946
173. Harshyne LA, Watkins SC, Gambotto A, Barratt-Boyes SM. Dendritic cells acquire antigens from live cells for cross-presentation to CTL. J Immunol (2001) 166(6):3717-23. doi:10.4049/jimmunol.166.6.3717
174. Toes RE, Blom RJ, van der Voort E, Offringa R, Melief CJ, Kast WM. Protective antitumor immunity induced by immunization with completely allogeneic tumor cells. Cancer Res (1996) 56(16):3782-7.
175. Yasuda T, Kamigaki T, Kawasaki K, Nakamura T, Yamamoto M, Kanemitsu K, et al. Superior anti-tumor protection and therapeutic efficacy of vaccination with allogeneic and semiallogeneic dendritic cell/tumor cell fusion hybrids for murine colon adenocarcinoma. Cancer Immunol Immunother (2007) 56(7):1025-36. doi:10.1007/s00262-006-0252-5
176. Merrick A, Diaz RM, O'Donnell D, Selby P, Vile R, Melcher A. Autologous versus allogeneic peptide-pulsed dendritic cells for anti-tumour vaccination: expression of allogeneic MHC supports activation of antigen specific T cells, but impairs early naive cytotoxic priming and anti-tumour therapy. Cancer Immunol Immunother (2008) 57(6):897-906. doi:10.1007/s00262-007-0426-9
177. Suzuki T, Fukuhara T, Tanaka M, Nakamura A, Akiyama K, Sakakibara T, et al. Vaccination of dendritic cells loaded with interleukin-12-secreting cancer cells augments in vivo antitumor immunity: characteristics of syngeneic and allogeneic antigen-presenting cell cancer hybrid cells. Clin Cancer Res (2005) 11(1):58-66.
178. Herzog GI, Solgi G, Wiegmann DS, Nienhaus C, Schrezenmeier H, Yildiz T, et al. Quality of tumor lysates used for pulsing dendritic cells is influenced by the method used to harvest adherent tumor cells. BMC Res Notes (2011) 4:153. doi:10.1186/1756-0500-4-153
179. Olin MR, Andersen BM, Zellmer DM, Grogan PT, Popescu FE, Xiong Z, et al. Superior efficacy of tumor cell vaccines grown in physiologic oxygen. Clin Cancer Res (2010) 16(19):4800-8. doi:10.1158/1078-0432.CCR-10-1572
180. Koido S, Homma S, Okamoto M, Namiki Y, Takakura K, Uchiyama K, et al. Strategies to improve the immunogenicity of anticancer vaccines based on dendritic cell/malignant cell fusions. Oncoimmunology (2013) 2(9):e25994. doi:10.4161/onci.25994
181. Tanaka Y, Koido S, Ohana M, Liu C, Gong J. Induction of impaired antitumor immunity by fusion of MHC class II-deficient dendritic cells with tumor cells. J Immunol (2005) 174(3):1274-80. doi:10.4049/jimmunol.174.3.1274
182. Ishida A, Tanaka H, Hiura T, Miura S, Watanabe S, Matsuyama K, et al. Generation of anti-tumour effector T cells from naive T cells by stimulation with dendritic/tumour fusion cells. Scand J Immunol (2007) 66(5):546-54. doi:10.1111/j.1365-3083.2007.02012.x
183. Tamai H, Watanabe S, Zheng R, Deguchi K, Cohen PA, Koski GK, et al. Effective treatment of spontaneous metastases derived from a poorly immunogenic murine mammary carcinoma by combined dendritic-tumor hybrid vaccination and adoptive transfer of sensitized T cells. Clin Immunol (2008) 127(1):66-77. doi:10.1016/j.clim.2007.12.001
184. Guo GH, Chen SZ, Yu J, Zhang J, Luo LL, Xie LH, et al. In vivo anti-tumor effect of hybrid vaccine of dendritic cells and esophageal carcinoma cells on esophageal carcinoma cell line 109 in mice with severe combined immune deficiency. World J Gastroenterol (2008) 14(8):1167-74. doi:10.3748/wjg.14.1167
185. Yamamoto M, Kamigaki T, Yamashita K, Hori Y, Hasegawa H, Kuroda D, et al. Enhancement of anti-tumor immunity by high levels of Th1 and Th17 with a combination of dendritic cell fusion hybrids and regulatory T cell depletion in pancreatic cancer. Oncol Rep (2009) 22(2):337-43. doi:10.3892/or_00000442
186. Tan C, Dannull J, Nair SK, Ding E, Tyler DS, Pruitt SK, et al. Local secretion of IL-12 augments the therapeutic impact of dendritic cell-tumor cell fusion vaccination. J Surg Res (2013) 185(2):904-11. doi:10.1016/j.jss.2013.06.045
187. Chen X, Liu Z, Huang Y, Li R, Zhang H, Dong S, et al. Superior anti-tumor protection and therapeutic efficacy of vaccination with dendritic cell/tumor cell fusion hybrids for murine Lewis lung carcinoma. Autoimmunity (2014) 47(1):46-56. doi:10.3109/08916934.2013.850080
188. Tanaka Y, Koido S, Chen D, Gendler SJ, Kufe D, Gong J. Vaccination with allogeneic dendritic cells fused to carcinoma cells induces antitumor immunity in MUC1 transgenic mice. Clin Immunol (2001) 101(2):192-200. doi:10.1006/clim.2001.5112
189. Chen D, Xia J, Tanaka Y, Chen H, Koido S, Wernet O, et al. Immunotherapy of spontaneous mammary carcinoma with fusions of dendritic cells and mucin 1-positive carcinoma cells. Immunology (2003) 109(2):300-7. doi:10.1046/j.1365-2567.2003.01656.x
190. Koido S, Hara E, Homma S, Torii A, Mitsunaga M, Yanagisawa S, et al. Streptococcal preparation OK-432 promotes fusion efficiency and enhances induction of antigen-specific CTL by fusions of dendritic cells and colorectal cancer cells. J Immunol (2007) 178(1):613-22. doi:10.4049/jimmunol.178.1.613
191. Caminschi I, Shortman K. Boosting antibody responses by targeting antigens to dendritic cells. Trends Immunol (2012) 33(2):71-7. doi:10.1016/j.it.2011.10.007
192. Hartung E, Becker M, Bachem A, Reeg N, Jakel A, Hutloff A, et al. Induction of potent CD8 T cell cytotoxicity by specific targeting of antigen to cross-presenting dendritic cells in vivo via murine or human XCR1. J Immunol (2015) 194(3):1069-79. doi:10.4049/jimmunol.1401903
193. Dhodapkar MV, Sznol M, Zhao B, Wang D, Carvajal 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):232ra51. doi:10.1126/scitranslmed.3008068
194. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell (2001) 106(3):255-8. doi:10.1016/S0092-8674(01)00449-4
195. Van Brussel I, Berneman ZN, Cools N. Optimizing dendritic cell-based immunotherapy: tackling the complexity of different arms of the immune system. Mediators Inflamm (2012) 2012:690643. doi:10.1155/2012/690643
196. Taraban VY, Rowley TF, Al-Shamkhani A. Cutting edge: a critical role for CD70 in CD8 T cell priming by CD40-licensed APCs. J Immunol (2004) 173(11):6542-6. doi:10.4049/jimmunol.173.11.6542
197. Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J, et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity (2004) 21(2):279-88. doi:10.1016/j.immuni.2004.06.014
198. 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. doi:10.1002/eji.1830271209
199. 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. doi:10.1186/1479-5876-5-18
200. Curtsinger JM, Johnson CM, Mescher MF. CD8 T cell clonal expansion and development of effector function require prolonged exposure to antigen, costimulation, and signal 3 cytokine. J Immunol (2003) 171(10):5165-71. doi:10.4049/jimmunol.171.10.5165
201. Agarwal P, Raghavan A, Nandiwada SL, Curtsinger JM, Bohjanen PR, Mueller DL, et al. Gene regulation and chromatin remodeling by IL-12 and type I IFN in programming for CD8 T cell effector function and memory. J Immunol (2009) 183(3):1695-704. doi:10.4049/jimmunol.0900592
202. Zapala L, Wolny R, Wachowska M, Jakobisiak M, Lasek W. Synergistic antitumor effect of JAWSII dendritic cells and interleukin 12 in a melanoma mouse model. Oncol Rep (2013) 29(3):1208-14. doi:10.3892/or.2012.2193
203. Leonard JP, Sherman ML, Fisher GL, Buchanan LJ, Larsen G, Atkins MB, et al. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-gamma production. Blood (1997) 90(7):2541-8.
204. 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. doi:10.1172/JCI68395
205. Peterson AC, Harlin H, Gajewski TF. Immunization with Melan-A peptide-pulsed peripheral blood mononuclear cells plus recombinant human interleukin-12 induces clinical activity and T-cell responses in advanced melanoma. J Clin Oncol (2003) 21(12):2342-8. doi:10.1200/JCO.2003.12.144
206. Hamid O, Solomon JC, Scotland R, Garcia M, Sian S, Ye W, et al. Alum with interleukin-12 augments immunity to a melanoma peptide vaccine: correlation with time to relapse in patients with resected high-risk disease. Clin Cancer Res (2007) 13(1):215-22. doi:10.1158/1078-0432.CCR-06-1450
207. Inaba K, Steinman RM, Pack MW, Aya H, Inaba M, Sudo T, et al. Identification of proliferating dendritic cell precursors in mouse blood. J Exp Med (1992) 175(5):1157-67. doi:10.1084/jem.175.5.1157
208. Dranoff G. GM-CSF-secreting melanoma vaccines. Oncogene (2003) 22(20):3188-92. doi:10.1038/sj.onc.1206459
209. Ojima T, Iwahashi M, Nakamura M, Matsuda K, Naka T, Nakamori M, et al. The boosting effect of co-transduction with cytokine genes on cancer vaccine therapy using genetically modified dendritic cells expressing tumor-associated antigen. Int J Oncol (2006) 28(4):947-53. doi:10.3892/ijo.28.4.947
210. Narusawa M, Inoue H, Sakamoto C, Matsumura Y, Takahashi A, Inoue T, et al. TLR7 ligand augments GM-CSF-initiated antitumor immunity through activation of plasmacytoid dendritic cells. Cancer Immunol Res (2014) 2(6):568-80. doi:10.1158/2326-6066.CIR-13-0143
211. Mach N, Gillessen S, Wilson SB, Sheehan C, Mihm M, Dranoff G. Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res (2000) 60(12):3239-46.
212. Kawai T, Akira S. Signaling to NF-kappaB by toll-like receptors. Trends Mol Med (2007) 13(11):460-9. doi:10.1016/j.molmed.2007.09.002
213. Prchal M, Pilz A, Simma O, Lingnau K, von Gabain A, Strobl B, et al. Type I interferons as mediators of immune adjuvants for T-and B cell-dependent acquired immunity. Vaccine (2009) 27(Suppl 6):G17-20. doi:10.1016/j.vaccine.2009.10.016
214. Datta SK, Redecke V, Prilliman KR, Takabayashi K, Corr M, Tallant T, et al. A subset of toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells. J Immunol (2003) 170(8):4102-10. doi:10.4049/jimmunol.170.8.4102
215. Warger T, Osterloh P, Rechtsteiner G, Fassbender M, Heib V, Schmid B, et al. Synergistic activation of dendritic cells by combined toll-like receptor ligation induces superior CTL responses in vivo. Blood (2006) 108(2):544-50. doi:10.1182/blood-2005-10-4015
216. Sidky YA, Borden EC, Weeks CE, Reiter MJ, Hatcher JF, Bryan GT. Inhibition of murine tumor growth by an interferon-inducing imidazoquinolinamine. Cancer Res (1992) 52(13):3528-33.
217. Lee JR, Shin JH, Park JH, Song SU, Choi GS. Combined treatment with intratumoral injection of dendritic cells and topical application of imiquimod for murine melanoma. Clin Exp Dermatol (2007) 32(5):541-9. doi:10.1111/j.1365-2230.2007.02453.x
218. Wilgenhof S, Van Nuffel AM, Corthals J, Heirman C, Tuyaerts S, Benteyn D, et al. Therapeutic vaccination with an autologous mRNA electroporated dendritic cell vaccine in patients with advanced melanoma. J Immunother (2011) 34(5):448-56. doi:10.1097/CJI.0b013e31821dcb31
219. Fujii S, Liu K, Smith C, Bonito AJ, Steinman RM. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J Exp Med (2004) 199(12):1607-18. doi:10.1084/jem.20040317
220. Taraban VY, Martin S, Attfield KE, Glennie MJ, Elliott T, Elewaut D, et al. Invariant NKT cells promote CD8+ cytotoxic T cell responses by inducing CD70 expression on dendritic cells. J Immunol (2008) 180(7):4615-20. doi:10.4049/jimmunol.180.7.4615
221. Dang Y, Wagner WM, Gad E, Rastetter L, Berger CM, Holt GE, et al. Dendritic cell-activating vaccine adjuvants differ in the ability to elicit antitumor immunity due to an adjuvant-specific induction of immunosuppressive cells. Clin Cancer Res (2012) 18(11):3122-31. doi:10.1158/1078-0432.CCR-12-0113
222. Prins RM, Soto H, Konkankit V, Odesa SK, Eskin A, Yong WH, et al. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res (2011) 17(6):1603-15. doi:10.1158/1078-0432.CCR-10-2563