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http://dx.doi.org/10.5483/BMBRep.2021.54.1.224

The role of dendritic cells in tumor microenvironments and their uses as therapeutic targets  

Kim, Chae Won (Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST))
Kim, Kyun-Do (Center for Convergent Research of Emerging Virus Infection, Korea Research Institute of Chemical Technology)
Lee, Heung Kyu (Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST))
Publication Information
BMB Reports / v.54, no.1, 2021 , pp. 31-43 More about this Journal
Abstract
Dendritic cells (DC), which consist of several different subsets, specialize in antigen presentation and are critical for mediating the innate and adaptive immune responses. DC subsets can be classified into conventional, plasmacytoid, and monocyte-derived DC in the tumor microenvironment, and each subset plays a different role. Because of the role of intratumoral DCs in initiating antitumor immune responses with tumor-derived antigen presentation to T cells, DCs have been targeted in the treatment of cancer. By regulating the functionality of DCs, several DC-based immunotherapies have been developed, including administration of tumor-derived antigens and DC vaccines. In addition, DCs participate in the mechanisms of classical cancer therapies, such as radiation therapy and chemotherapy. Thus, regulating DCs is also important in improving current cancer therapies. Here, we will discuss the role of each DC subset in antitumor immune responses, and the current status of DC-related cancer therapies.
Keywords
Cancer immunology; Cancer therapy; Dendritic cells;
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1 Diao J, Gu H, Tang M, Zhao J and Cattral MS (2018) Tumor dendritic cells (DCs) derived from precursors of conventional DCs are dispensable for intratumor CTL responses. J Immunol 201, 1306   DOI
2 Qian B-Z, Li J, Zhang H et al (2011) CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475, 222-225   DOI
3 Spary LK, Salimu J, Webber JP, Clayton A, Mason MD and Tabi Z (2014) Tumor stroma-derived factors skew monocyte to dendritic cell differentiation toward a suppressive CD14+ PD-L1+ phenotype in prostate cancer. Oncoimmunology 3, e955331   DOI
4 Laoui D, Keirsse J, Morias Y et al (2016) The tumour microenvironment harbours ontogenically distinct dendritic cell populations with opposing effects on tumour immunity. Nat Commun 7, 13720   DOI
5 Sánchez-Paulete AR, Cueto FJ, Martinez-López M et al (2016) Cancer immunotherapy with immunomodulatory anti-CD137 and anti-PD-1 monoclonal antibodies requires BATF3-dependent dendritic cells. Cancer Discov 6, 71-79   DOI
6 Spranger S, Dai D, Horton B and Gajewski TF (2017) Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy. Cancer Cell 31, 711-723.e714   DOI
7 Jongbloed SL, Kassianos AJ, McDonald KJ et al (2010) Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 207, 1247-1260   DOI
8 Broz Miranda L, Binnewies M, Boldajipour B et al (2014) Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell 26, 638-652   DOI
9 Roberts EW, Broz ML, Binnewies M et al (2016) Critical role for CD103+/CD141+ dendritic cells bearing CCR7 for tumor antigen trafficking and priming of T cell immunity in melanoma. Cancer Cell 30, 324-336   DOI
10 Wang J, Iwanowycz S, Yu F et al (2016) microRNA-155 deficiency impairs dendritic cell function in breast cancer. Oncoimmunology 5, e1232223   DOI
11 Binnewies M, Mujal AM, Pollack JL et al (2019) Unleashing type-2 dendritic cells to drive protective antitumor CD4+ T cell immunity. Cell 177, 556-571.e516   DOI
12 Ferris ST, Durai V, Wu R et al (2020) cDC1 prime and are licensed by CD4+ T cells to induce anti-tumour immunity. Nature 584, 624-629   DOI
13 Salmon H, Idoyaga J, Rahman A et al (2016) Expansion and activation of CD103+ dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity 44, 924-938   DOI
14 Novak L, Igoucheva O, Cho S and Alexeev V (2007) Characterization of the CCL21-mediated melanoma-specific immune responses and in situ melanoma eradication. Mol Cancer Ther 6, 1755   DOI
15 Bakdash G, Buschow SI, Gorris MAJ et al (2016) Expansion of a BDCA1+ CD14+ myeloid cell population in melanoma patients may attenuate the efficacy of dendritic cell vaccines. Cancer Res 76, 4332   DOI
16 Deng L, Liang H, Xu M et al (2014) STING-dependent cytosolic dna sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity 41, 843-852   DOI
17 Ghiringhelli F, Apetoh L, Tesniere A et al (2009) Activation of the NLRP3 inflammasome in dendritic cells induces IL-1β-dependent adaptive immunity against tumors. Nat Med 15, 1170-1178   DOI
18 Apetoh L, Ghiringhelli F, Tesniere A et al (2007) Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13, 1050-1059   DOI
19 Vacchelli E, Ma Y, Baracco EE et al (2015) Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1. Science 350, 972-978   DOI
20 Lecciso M, Ocadlikova D, Sangaletti S et al (2017) ATP release from chemotherapy-treated dying leukemia cells elicits an immune suppressive effect by increasing regulatory T cells and tolerogenic dendritic cells. Front Immunol 8, 1918   DOI
21 Vanpouille-Box C, Alard A, Aryankalayil MJ et al (2017) DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity. Nat Commun 8, 15618   DOI
22 Hou Y, Liang H, Rao E et al (2018) Non-canonical NF-κB antagonizes STING sensor-mediated DNA sensing in radiotherapy. Immunity 49, 490-503.e494   DOI
23 Marigo I, Zilio S, Desantis G et al (2016) T cell cancer therapy requires CD40-CD40L activation of tumor necrosis factor and inducible nitric-oxide-synthase-producing dendritic cells. Cancer Cell 30, 377-390   DOI
24 Shields JD, Kourtis IC, Tomei AA, Roberts JM and Swartz MA (2010) Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science 328, 749   DOI
25 Bottcher JP and Reis e Sousa C (2018) The role of type 1 conventional dendritic cells in cancer immunity. Trends Cancer 4, 784-792   DOI
26 Dannull J, Nair S, Su Z et al (2005) Enhancing the immunostimulatory function of dendritic cells by transfection with mRNA encoding OX40 ligand. Blood 105, 3206-3213   DOI
27 Buchan SL, Fallatah M, Thirdborough SM et al (2018) PD-1 blockade and CD27 stimulation activate distinct transcriptional programs that synergize for CD8+ T-cell-driven antitumor immunity. Clin Cancer Res 24, 2383-2394   DOI
28 Martinez-López M, Iborra S, Conde-Garrosa R and Sancho D (2015) Batf3-dependent CD103+ dendritic cells are major producers of IL-12 that drive local Th1 immunity against Leishmania major infection in mice. Eur J Immunol 45, 119-129   DOI
29 Chow MT, Ozga AJ, Servis RL et al (2019) Intratumoral activity of the CXCR3 chemokine system is required for the efficacy of anti-PD-1 therapy. Immunity 50, 1498-1512. e1495   DOI
30 Ruffell B, Chang-Strachan D, Chan V et al (2014) Macrophage IL-10 blocks CD8+ T cell-dependent responses to chemotherapy by suppressing IL-12 expression in intratumoral dendritic cells. Cancer Cell 26, 623-637   DOI
31 Enamorado M, Iborra S, Priego E et al (2017) Enhanced anti-tumour immunity requires the interplay between resident and circulating memory CD8+ T cells. Nature 8, 16073
32 Mittal D, Vijayan D, Putz EM et al (2017) Interleukin-12 from CD103+ Batf3-dependent dendritic cells required for NK-cell suppression of metastasis. Cancer Immnol 5, 1098   DOI
33 Oba T, Hoki T, Yamauchi T et al (2020) A critical role of CD40 and CD70 signaling in conventional type 1 dendritic cells in expansion and antitumor efficacy of adoptively transferred tumor-specific T cells. J Immunol 205, 1867-1877   DOI
34 Kalbasi A and Ribas A (2020) Tumour-intrinsic resistance to immune checkpoint blockade. Nat Rev Immunol 20, 25-39   DOI
35 Mayoux M, Roller A, Pulko V et al (2020) Dendritic cells dictate responses to PD-L1 blockade cancer immunotherapy. Sci Transl Med 12, eaav7431   DOI
36 Schetters STT, Rodriguez E, Kruijssen LJW et al (2020) Monocyte-derived APCs are central to the response of PD1 checkpoint blockade and provide a therapeutic target for combination therapy. J Immunother Cancer 8, e000588   DOI
37 Morrison AH, Diamond MS, Hay CA, Byrne KT and Vonderheide RH (2020) Sufficiency of CD40 activation and immune checkpoint blockade for T cell priming and tumor immunity. Proc Natl Acad Sci U S A 117, 8022   DOI
38 Wang H, Hu S, Chen X et al (2017) cGAS is essential for the antitumor effect of immune checkpoint blockade. Proc Natl Acad Sci U S A 114, 1637   DOI
39 Garris CS, Arlauckas SP, Kohler RH et al (2018) Successful anti-PD-1 cancer immunotherapy requires T cell- dendritic cell crosstalk involving the cytokines IFN-γ and IL-12. Immunity 49, 1148-1161.e1147   DOI
40 Cauwels A, Van Lint S, Paul F et al (2018) Delivering type I interferon to dendritic cells empowers tumor eradication and immune combination treatments. Cancer Res 78, 463   DOI
41 Alloatti A, Rookhuizen DC, Joannas L et al (2017) Critical role for Sec22b-dependent antigen cross-presentation in antitumor immunity. J Exp Med 214, 2231-2241   DOI
42 Nemunaitis J (2005) Vaccines in cancer: GVAXⓇ, a GM-CSF gene vaccine. Expert Rev Vaccines 4, 259-274   DOI
43 Bottcher JP, Bonavita E, Chakravarty P et al (2018) NK cells stimulate recruitment of cDC1 into the tumor microenvironment promoting cancer immune control. Cell 172, 1022-1037.e1014   DOI
44 Barry KC, Hsu J, Broz ML et al (2018) A natural killer-dendritic cell axis defines checkpoint therapy-responsive tumor microenvironments. Nat Med 24, 1178-1191   DOI
45 Maier B, Leader AM, Chen ST et al (2020) A conserved dendritic-cell regulatory program limits antitumour immunity. Nature 580, 257-262   DOI
46 Zong J, Keskinov AA, Shurin GV and Shurin MR (2016) Tumor-derived factors modulating dendritic cell function. Cancer Immnol Immunother 65, 821-833   DOI
47 Gottfried E, Kunz-Schughart LA, Ebner S et al (2006) Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood 107, 2013-2021   DOI
48 Villadangos JA and Young L (2008) Antigen-presentation properties of plasmacytoid dendritic cells. Immunity 29, 352-361   DOI
49 Xu MM, Pu Y, Han D et al (2017) Dendritic cells but not macrophages sense tumor mitochondrial DNA for crosspriming through signal regulatory protein α signaling. Immunity 47, 363-373.e365   DOI
50 Villablanca EJ, Raccosta L, Zhou D et al (2010) Tumormediated liver X receptor-α activation inhibits CC chemokine receptor-7 expression on dendritic cells and dampens antitumor responses. Nat Med 16, 98-105   DOI
51 Zitvogel L, Galluzzi L, Kepp O, Smyth MJ and Kroemer G (2015) Type I interferons in anticancer immunity. Nat Rev Immunol 15, 405-414   DOI
52 Fuertes MB, Kacha AK, Kline J et al (2011) Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8+ dendritic cells. J Exp Med 208, 2005-2016   DOI
53 Diamond MS, Kinder M, Matsushita H et al (2011) Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 208, 1989-2003   DOI
54 Yan W-L, Shen K-Y, Tien C-Y, Chen Y-A and Liu S-J (2017) Recent progress in GM-CSF-based cancer immunotherapy. Immunotherapy 9, 347-360   DOI
55 Bommareddy PK, Patel A, Hossain S and Kaufman HL (2017) Talimogene laherparepvec (T-VEC) and other oncolytic viruses for the treatment of melanoma. Am J Clin Dermatol 18, 1-15   DOI
56 Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS and Kim-Schulze S (2010) Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding gm-csf in patients with stage IIIc and IV melanoma. Ann Surg Oncol 17, 718-730   DOI
57 Aznar MA, Planelles L, Perez-Olivares M et al (2019) Immunotherapeutic effects of intratumoral nanoplexed poly I:C. J Immunother Cancer 7, 116   DOI
58 Robinson RA, DeVita VT, Levy HB, Baron S, Hubbard SP and Levine AS (1976) A phase I-II trial of multipledose polyriboinosinic-polyribocytidylic acid in patients with leukemia or solid tumors. J Natl Cancer Inst 57, 599-602   DOI
59 Kyi C, Roudko V, Sabado R et al (2018) Therapeutic immune modulation against solid cancers with intratumoral poly-ICLC: a pilot trial. Clin Cancer Res 24, 4937-4948   DOI
60 Navabi H, Jasani B, Reece A et al (2009) A clinical grade poly I:C-analogue (AmpligenⓇ) promotes optimal DC maturation and Th1-type T cell responses of healthy donors and cancer patients in vitro. Vaccine 27, 107-115   DOI
61 Corrales L, Glickman Laura H, McWhirter Sarah M et al (2015) Direct activation of sting in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep 11, 1018-1030   DOI
62 Finn OJ (2017) Human tumor antigens yesterday, today, and tomorrow. Cancer Immunol Res 5, 347   DOI
63 Harari A, Graciotti M, Bassani-Sternberg M and Kandalaft LE (2020) Antitumour dendritic cell vaccination in a priming and boosting approach. Nat Rev Drug Discov 19, 635-652   DOI
64 Ott PA, Hu Z, Keskin DB et al (2017) An immunogenic personal neoantigen vaccine for patients with melanoma. Nature 547, 217-221   DOI
65 Gleisner MA, Pereda C, Tittarelli A et al (2020) A heatshocked melanoma cell lysate vaccine enhances tumor infiltration by prototypic effector T cells inhibiting tumor growth. J Immunother Cancer 8, e000999   DOI
66 Callmann CE, Cole LE, Kusmierz CD, Huang Z, Horiuchi D and Mirkin CA (2020) Tumor cell lysate-loaded immunostimulatory spherical nucleic acids as therapeutics for triple-negative breast cancer. Proc Natl Acad Sci U S A 117, 17543   DOI
67 Yarchoan M, Johnson BA, Lutz ER, Laheru DA and Jaffee EM (2017) Targeting neoantigens to augment antitumour immunity. Nat Rev Cancer 17, 209-222   DOI
68 Rizvi NA, Hellmann MD, Snyder A et al (2015) Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348, 124-128   DOI
69 Balachandran VP, Luksza M, Zhao JN et al (2017) Identification of unique neoantigen qualities in long-term survivors of pancreatic cancer. Nature 551, 512-516   DOI
70 Keskin DB, Anandappa AJ, Sun J et al (2019) Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial. Nature 565, 234-239   DOI
71 Kim JH, Lee Y, Bae Y-S et al (2007) Phase I/II study of immunotherapy using autologous tumor lysate-pulsed dendritic cells in patients with metastatic renal cell carcinoma. Clin Immunol 125, 257-267   DOI
72 Powell A, Creaney J, Broomfield S, Van Bruggen I and Robinson B (2006) Recombinant GM-CSF plus autologous tumor cells as a vaccine for patients with mesothelioma. Lung Cancer 52, 189-197   DOI
73 Tsuji T, Matsuzaki J, Kelly MP et al (2011) 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 186, 1218   DOI
74 Carreno BM, Magrini V, Becker-Hapak M et al (2015) A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 348, 803   DOI
75 Anguille S, Smits EL, Lion E, van Tendeloo VF and Berneman ZN (2014) Clinical use of dendritic cells for cancer therapy. Lancet Oncol 15, e257-e267   DOI
76 Draube A, Klein-González N, Mattheus S et al (2011) Dendritic cell based tumor vaccination in prostate and renal cell cancer: a systematic review and meta-analysis. PLoS One 6, e18801   DOI
77 Kantoff PW, Higano CS, Shore ND et al (2010) Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363, 411-422   DOI
78 Mastelic-Gavillet B, Balint K, Boudousquie C, Gannon PO and Kandalaft LE (2019) Personalized dendritic cell vaccines-recent breakthroughs and encouraging clinical results. Front Immunol 10, 766   DOI
79 van Willigen WW, Bloemendal M, Gerritsen WR, Schreibelt G, de Vries IJM and Bol KF (2018) Dendritic cell cancer therapy: vaccinating the right patient at the right time. Front Immunol 9, 2265   DOI
80 Perez CR and De Palma M (2019) Engineering dendritic cell vaccines to improve cancer immunotherapy. Nat Commun 10, 5408   DOI
81 Okada N, Mori N, Koretomo R et al (2005) Augmentation of the migratory ability of DC-based vaccine into regional lymph nodes by efficient CCR7 gene transduction. Gene Ther 12, 129-139   DOI
82 Birkholz K, Schwenkert M, Kellner C et al (2010) Targeting of DEC-205 on human dendritic cells results in efficient MHC class II-restricted antigen presentation. Blood 116, 2277-2285   DOI
83 Yang X, Lian K, Meng T et al (2018) Immune adjuvant targeting micelles allow efficient dendritic cell migration to lymph nodes for enhanced cellular immunity. ACS Appl Mater Interfaces 10, 33532-33544   DOI
84 Labidi-Galy SI, Treilleux I, Goddard-Leon S et al (2012) Plasmacytoid dendritic cells infiltrating ovarian cancer are associated with poor prognosis. OncoImmunology 1, 380-382   DOI
85 Aspord C, Leccia M-T, Charles J and Plumas J (2013) Plasmacytoid dendritic cells support melanoma progression by promoting Th2 and regulatory immunity through OX40L and ICOSL. Cancer Immunol Res 1, 402   DOI
86 Conrad C, Gregorio J, Wang Y-H et al (2012) Plasmacytoid dendritic cells promote immunosuppression in ovarian cancer via icos costimulation of Foxp3+ T-regulatory cells. Cancer Res 72, 5240   DOI
87 Faget J, Bendriss-Vermare N, Gobert M et al (2012) ICOS-ligand expression on plasmacytoid dendritic cells supports breast cancer progression by promoting the accumulation of immunosuppressive CD4+ T cells. Cancer Res 72, 6130   DOI
88 Pedroza-Gonzalez A, Zhou G, Vargas-Mendez E et al (2015) Tumor-infiltrating plasmacytoid dendritic cells promote immunosuppression by Tr1 cells in human liver tumors. Oncoimmunology 4, e1008355-e1008355
89 Wei S, Kryczek I, Zou L et al (2005) Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res 65, 5020   DOI
90 Treilleux I, Blay J-Y, Bendriss-Vermare N et al (2004) Dendritic cell infiltration and prognosis of early stage breast cancer. Clin Cancer Res 10, 7466   DOI
91 Sisirak V, Vey N, Goutagny N et al (2013) Breast cancer-derived transforming growth factor-β and tumor necrosis factor-α compromise interferon-α production by tumor-associated plasmacytoid dendritic cells. Int J Cancer 133, 771-778   DOI
92 Zilionis R, Engblom C, Pfirschke C et al (2019) Single-cell transcriptomics of human and mouse lung cancers reveals conserved myeloid populations across individuals and species. Immunity 50, 1317-1334.e1310   DOI
93 Mittal D, Gubin MM, Schreiber RD and Smyth MJ (2014) New insights into cancer immunoediting and its three component phases--elimination, equilibrium and escape. Curr Opin Immunol 27, 16-25   DOI
94 Chen Daniel S and Mellman I (2013) Oncology meets immunology: the cancer-immunity cycle. Immunity 39, 1-10   DOI
95 Hildner K, Edelson BT, Purtha WE et al (2008) Batf3 deficiency reveals a critical role for CD8α dendritic cells in cytotoxic T cell immunity. Science 322, 1097-1100   DOI
96 Gaudino SJ and Kumar P (2019) Cross-talk between antigen presenting cells and T cells impacts intestinal homeostasis, bacterial infections, and tumorigenesis. Front Immunol 10, 360   DOI
97 Wculek SK, Cueto FJ, Mujal AM, Melero I, Krummel MF and Sancho D (2020) Dendritic cells in cancer immunology and immunotherapy. Nat Rev Immunol 20, 7-24   DOI
98 Gardner A, de Mingo Pulido A and Ruffell B (2020) Dendritic cells and their role in immunotherapy. Front Immunol 11, 924-924   DOI
99 Terra M, Oberkampf M, Fayolle C et al (2018) Tumorderived TGFβ alters the ability of plasmacytoid dendritic cells to respond to innate immune signaling. Cancer Res 78, 3014   DOI
100 Bruchhage K-L, Heinrichs S, Wollenberg B and Pries R (2018) IL-10 in the microenvironment of HNSCC inhibits the CpG ODN induced IFN-α secretion of pDCs. Oncol Lett 15, 3985-3990
101 Bi E, Li R, Bover LC et al (2018) E-cadherin expression on multiple myeloma cells activates tumor-promoting properties in plasmacytoid DCs. J Clin Investig 128, 4821-4831   DOI
102 Nakano H, Lin KL, Yanagita M et al (2009) Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat Immunol 10, 394-402   DOI
103 Sharma MD, Rodriguez PC, Koehn BH et al (2018) Activation of p53 in immature myeloid precursor cells controls differentiation into Ly6c+ CD103+ monocytic antigen-presenting cells in tumors. Immunity 48, 91-106.e106   DOI
104 Lee JM, Lee M-H, Garon E et al (2017) Phase I trial of intratumoral injection of CCL21 gene-modified dendritic cells in lung cancer elicits tumor- specific immune responses and CD8+ T-cell infiltration. Clin Cancer Res 23, 4556-4568   DOI
105 Lind EF, Millar DG, Dissanayake D et al (2015) miR-155 upregulation in dendritic cells is sufficient to break tolerance in vivo by negatively regulating SHIP1. J Immunol 195, 4632   DOI
106 Wilgenhof S, Corthals J, Heirman C et al (2016) Phase II study of autologous monocyte-derived mrna electroporated dendritic cells (TriMixDC-MEL) plus ipilimumab in patients with pretreated advanced melanoma. J Clin Oncol 34, 1330-1338   DOI
107 Yang S-C, Hillinger S, Riedl K et al (2004) Intratumoral administration of dendritic cells overexpressing CCL21 generates systemic antitumor responses and confers tumor immunity. Clin Cancer Res 10, 2891   DOI
108 Wculek SK, Amores-Iniesta J, Conde-Garrosa R, Khouili SC, Melero I and Sancho D (2019) Effective cancer immunotherapy by natural mouse conventional type-1 dendritic cells bearing dead tumor antigen. J Immunother Cancer 7, 100   DOI
109 Kadam P and Sharma S (2020) PD-1 immune checkpoint blockade promotes therapeutic cancer vaccine to eradicate lung cancer. Vaccines 8, 317   DOI
110 Teng C-F, Wang T, Wu T-H et al (2020) Combination therapy with dendritic cell vaccine and programmed death ligand 1 immune checkpoint inhibitor for hepatocellular carcinoma in an orthotopic mouse model. Ther Adv Med Oncol 12, 1758835920922034