Biphasic function of TLR3 adjuvant on tumor and spleen dendritic cells promotes tumor T cell infiltration and regression in a vaccine therapy

OncoImmunology

Volumn 5, Issue 8, 2016, Pages

  Azuma, Masahiro ^a   Takeda, Yohei ^a   Nakajima, Hiroko ^b   Sugiyama, Haruo ^b   Ebihara, Takashi ^a,c   Oshiumi, Hiroyuki ^a,d   Matsumoto, Misako ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d KUMAMOTO UNIVERSITY   (Japan)

Author keywords

BATF3; cancer immunotherapy; CD8 + DC; IL 12p70; Poly(I:C); TICAM 1; Toll like receptor 3; WT1

Indexed keywords

CD8 ANTIGEN; CHEMOKINE RECEPTOR CXCR3; INTERLEUKIN 12; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3;

ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; MOUSE; NONHUMAN; T LYMPHOCYTE; UPREGULATION;

EID: 84980048100     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1188244     Document Type: Article

References (52)

1. M.Matsumoto, T.Seya, S.Kikkawa, S.Tsuji, K.Shida, M.Nomura, M.Kurita-Taniguchi, H.Ohigashi, H.Yokouchi, K.Takami et al. Interferon gamma-producing ability in blood lymphocytes of patients with lung cancer through activation of the innate immune system by BCG cell wall skeleton. Int Immunopharmacol 2001; 1:1559-69; PMID:11515819; http://dx.doi.org/10.1016/S1567-5769(01)00071-6
2. O.P.Joffre, E.Segura, A.Savina, S.Amigorena. Cross-presentation by dendritic cells. Nat Rev Immunol 2012; 12:557-69; PMID:22790179; http://dx.doi.org/10.1038/nri3254
3. S.R.Woo, L.Corrales, T.F.Gajewski. Innate Immune Recognition of Cancer. Annu Rev Immunol 2012; 33:445-74; http://dx.doi.org/10.1146/annurev-immunol-032414-112043
4. T.Condamine, J.Mastio, D.I.Gabrilovich. Transcriptional regulation of myeloid-derived suppressor cells. J Leukoc Biol 2015; 98:913-22; PMID:26337512; http://dx.doi.org/10.1189/jlb.4RI0515-204R
5. A.Mantovani, P.Allavena. The interaction of anticancer therapies with tumor-associated macrophages. J Exp Med 2015; 212:435-45; PMID:25753580; http://dx.doi.org/10.1084/jem.20150295
6. A.N.Desch, S.L.Gibbings, E.T.Clambey, W.J.Janssen, J.E.Slansky, R.M.Kedl, P.M.Henson, C.Jakubzick. Dendritic cell subsets require cis-activation for cytotoxic CD8 T-cell induction. Nat Commun 2014; 5:4674; PMID:25135627; http://dx.doi.org/10.1038/ncomms5674
7. N.Goutagny, Y.Estornes, U.Hasan, S.Lebecque, C.Caux. Targeting pattern recognition receptors in cancer immunotherapy. Target Oncol 2012; 7:29-54; PMID:22399234; http://dx.doi.org/10.1007/s11523-012-0213-1
8. O.Schulz, S.S.Diebold, M.Chen, T.I.Nauslund, M.A.Nolte, L.Alexopoulou, Y.T.Azuma, R.A.Flavell, P.Liljeström, C.Reis e Sousa. Toll-like receptor 3 promotes cross- priming to virus-infected cells. Nature 2005; 433:887-92; PMID:15711573; http://dx.doi.org/10.1038/nature03326
9. A.Bachem, S.Güttler, E.Hartung, F.Ebstein, M.Schaefer, A.Tannert, A.Salama, K.Movassaghi, C.Opitz, H.W.Mages et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med 2010; 207:1273-81; PMID:20479115; http://dx.doi.org/10.1084/jem.20100348
10. K.Crozat, R.Guiton, V.Contreras, V.Feuillet, C.A.Dutertre, E.Ventre, T.P.Vu Manh, T.Baranek, A.K.Storset, J.Marvel 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; 207:1283-92; PMID:20479118; http://dx.doi.org/10.1084/jem.20100223
11. S.L.Jongbloed, A.J.Kassianos, K.J.McDonald, G.J.Clark, X.Ju, C.E.Angel, C.J.Chen, P.R.Dunbar, R.B.Wadley, V.Jeet et al. Human CD141+ (BDCA-3)+ dendritic cells (DC) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010; 207:1247-60; PMID:20479116; http://dx.doi.org/10.1084/jem.20092140
12. L.F.Poulin, M.Salio, E.Griessinger, F.Anjos-Afonso, L.Craciun, J.L.Chen, A.M.Keller, O.Joffre, S.Zelenay, E.Nye et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 2010; 207:1261-71; PMID:20479117; http://dx.doi.org/10.1084/jem.20092618
13. T.Seya, H.Shime, Y.Takeda, M.Tatematsu, K.Takashima, M.Matsumoto. Adjuvant for vaccine immunotherapy of cancer - focusing on Toll-like receptor 2 and 3 agonists for safely enhancing antitumor immunity. Cancer Sci 2015; 106:1659-68; PMID:26395101; http://dx.doi.org/10.1111/cas.12824
14. T.Seya, M.Azuma, M.Matsumoto. Targeting TLR3 with no RIG-I/MDA5 activation is effective in immunotherapy for cancer. Expert Opin Ther Targets 2013; 17:533-44; PMID:23414438; http://dx.doi.org/10.1517/14728222.2013.765407
15. E.Vacchelli, A.Eggermont, C.Sautès-Fridman, J.Galon, L.Zitvogel, G.Kroemer, L.Galluzzi. Trial Watch:Toll-like receptor agonists for cancer therapy. Oncoimmunology 2013; 2:e25238; PMID:24083080; http://dx.doi.org/10.4161/onci.25238
16. M.Matsumoto, T.Seya. TLR3:interferon induction by double-stranded RNA including Poly(I:C). Adv Drug Deliv Rev 2008; 60:805-12; PMID:18262679; http://dx.doi.org/10.1016/j.addr.2007.11.005
17. L.Galluzzi, E.Vacchelli, A.Eggermont, W.H.Fridman, J.Galon, C.Sautès-Fridman, E.Tartour, L.Zitvogel, G.Kroemer. Trial Watch:Experimental Toll-like receptor agonists for cancer therapy. Oncoimmunology 2012; 1:699-716; PMID:22934262; http://dx.doi.org/10.4161/onci.20696
18. P.Sabbatini, T.Tsuji, L.Ferran, E.Ritter, C.Sedrak, K.Tuballes, A.A.Jungbluth, G.Ritter, C.Aghajanian, K.Bell-McGuinn et al. Phase I trial of overlapping long peptides from a tumor self-antigen and poly-ICLC shows rapid induction of integrated immune response in ovarian cancer patients. Clin Cancer Res 2012; 18:6497-508; PMID:23032745; http://dx.doi.org/10.1158/1078-0432.CCR-12-2189
19. H.Kato, O.Takeuchi, S.Sato, M.Yoneyama, M.Yamamoto, K.Matsui, S.Uematsu, A.Jung, T.Kawai, K.J.Ishii et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441:101-5; PMID:16625202; http://dx.doi.org/10.1038/nature04734
20. M.Matsumoto, M.Tatematsu, F.Nishikawa, M.Azuma, H.Shime, T.Seya. Defined TLR3-specific adjuvant that induces NK and cytotoxic T cell activation without significant cytokine production in vivo. Nat Commun 2015; 6:6280; PMID:25692975; http://dx.doi.org/10.1038/ncomms7280
21. M.Y.Gerner, L.M.Heltemes-Harris, B.T.Fife, M.F.Mescher. Cutting edge:IL-12 and type I IFN differentially program CD8 T cells for programmed death 1 re-expression levels and tumor control. J Immunol 2013; 191:1011-5; PMID:23804712; http://dx.doi.org/10.4049/jimmunol.1300652
22. L.Zitvogel, G.Kroemer. CD103+ dendritic cells producing interleukin-12 in anticancer immunosurveillance. Cancer Cell 2014; 26:591-3; PMID:25517740; http://dx.doi.org/10.1016/j.ccell.2014.10.008
23. D.M.Pardoll. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-64; PMID:22437870; http://dx.doi.org/10.1038/nrc3239
24. T.Yokosuka, M.Takamatsu, W.Kobayashi-Imanishi, A.Hashimoto-Tane, M.Azuma, T.Saito. Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 2012; 209:1201-17; PMID:22641383; http://dx.doi.org/10.1084/jem.20112741
25. H.Shime, M.Matsumoto, H.Oshiumi, S.Tanaka, A.Nakane, Y.Iwakura, H.Tahara, N.Inoue, T.Seya. Toll-like receptor 3 signaling converts tumor-supporting myeloid cells to tumoricidal effectors. Proc Natl Acad Sci U S A 2012; 109:2066-71; PMID:22308357; http://dx.doi.org/10.1073/pnas.1113099109
26. Y.Iwai, M.Ishida, Y.Tanaka, T.Okazaki, T.Honjo, N.Minato. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci U S A 2002; 99:12293-7; PMID:12218188; http://dx.doi.org/10.1073/pnas.192461099
27. A.O.Kamphorst, R.Ahmed. Manipulating the PD-1 pathway to improve immunity. Curr Opin of Immunol 2013; 25:381-8; http://dx.doi.org/10.1016/j.coi.2013.03.003
28. M.Azuma, T.Ebihara, H.Oshiumi, M.Matsumoto, T.Seya. Cross-priming for antitumor CTL induced by soluble Ag + polyI:C depends on the TICAM-1 pathway in mouse CD11c(+)/CD8α(+) dendritic cells. Oncoimmunology 2012; 1:581-92; PMID:22934250; http://dx.doi.org/10.4161/onci.19893
29. B.T.Edelson, W.KCW, R.Juang, M.Kohyama, L.A.Benoit, P.A.Klekotka, C.Moon, J.C.Albring, W.Ise, D.G.Michael et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med 2010; 207:823-36; PMID:20351058; http://dx.doi.org/10.1084/jem.20091627
30. B.T.Edelson, T.R.Bradstreet, W.KCW, K.Hildner, J.W.Herzog, J.Sim, J.H.Russell, T.L.Murphy, E.R.Unanue, K.M.Murphy. Batf3-dependent CD11b(low/-) peripheral dendritic cells are GM-CSF-independent and are not required for Th cell priming after subcutaneous immunization. PLoS One 2011; 6:e25660; PMID:22065991; http://dx.doi.org/10.1371/journal.pone.0025660
31. K.Hildner, B.T.Edelson, W.E.Purtha, M.S.Diamond, H.Matsushita, M.Kohyama, B.Calderon, B.U.Schraml, E.R.Unanue, M.S.Diamond et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 2008; 322:1097-100; PMID:19008445; http://dx.doi.org/10.1126/science.1164206
32. T.L.Murphy, R.Tussiwand, K.M.Murphy. Specificity through cooperation:BATF-IRF interactions control immune-regulatory networks. Nat Rev Immunol 2013; 13:499-509; PMID:23787991; http://dx.doi.org/10.1038/nri3470
33. A.Mildner, S.Jung. Development and function of dendritic cell subsets. Immunity 2014; 40:642-56; PMID:24837101; http://dx.doi.org/10.1016/j.immuni.2014.04.016
34. H.Nakajima, Y.Oka, A.Tsuboi, N.Tatsumi, Y.Yamamoto, F.Fujiki, Z.Li, A.Murao, S.Morimoto, N.Hosen et al. Enhanced tumor immunity of WT1 peptide vaccination by interferon-β administration. Vaccine 2012; 30:722-9; PMID:22133512; http://dx.doi.org/10.1016/j.vaccine.2011.11.074
35. J.Zou, T.Kawai, T.Tsuchida, T.Kozaki, H.Tanaka, K.S.Shin, H.Kumar, S.Akira. Poly IC triggers a cathepsin D- and IPS-1-dependent pathway to enhance cytokine production and mediate dendritic cell necroptosis. Immunity 2013; 38:717-28; PMID:23601685; http://dx.doi.org/10.1016/j.immuni.2012.12.007
36. M.Sasai, M.Shingai, K.Funami, M.Yoneyama, T.Fujita, M.Matsumoto, T.Seya. NAK-associated protein 1 participates in both the TLR3 and the cytoplasmic pathways in type I IFN induction. J Immunol 2006; 177:8676-83; PMID:17142768; http://dx.doi.org/10.4049/jimmunol.177.12.8676
37. M.P.Colombo, G.Trinchieri. Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev 2002; 13:155-68; PMID:11900991; http://dx.doi.org/10.1016/S1359-6101(01)00032-6
38. T.Sugiyama, K.Hoshino, M.Saito, T.Yano, I.Sasaki, C.Yamazaki, S.Akira, T.Kaisho. Immunoadjuvant effects of polyadenylic:polyuridylic acids through TLR3 and TLR7. Int Immunol 2008; 20:1-9; PMID:17981792; http://dx.doi.org/10.1093/intimm/dxm112
39. P.C.Tumeh, C.L.Harview, J.H.Yearley, I.P.Shintaku, E.M.Taylor, L.Robert, B.1.Chmielowski, M.Spasic, G.Henry, V.Ciobanu et al. PD-1 blockage induces responses by inhibiting adaptive immune resistance. Nature 2014; 515:568-73; PMID:25428505; http://dx.doi.org/10.1038/nature13954
40. R.S.Herbst, J.C.Soria, M.Kowanetz, G.D.Fine, O.Hamid, M.S.Gordon, J.A.Sosman, D.F.McDermott, J.D.Powderly, S.N.Gettinger et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014; 515:563-7; PMID:25428504; http://dx.doi.org/10.1038/nature14011
41. M.L.Broz, M.Binnewies, B.Boldajipour, A.E.Nelson, J.L.Pollack, D.J.Erle, A.Barczak, M.D.Rosenblum, A.Daud, D.L.Barber et al. Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity. Cancer Cell 2014; 26:638-52; PMID:25446897; http://dx.doi.org/10.1016/j.ccell.2014.09.007
42. P.D.Krueger, T.S.Kim, S.J.Sung, T.J.Braciale, Y.S.Hahn. Liver-resident CD103+ dendritic cells prime antiviral CD8+ T cells in situ. J Immunol 2015; 194:3213-22; PMID:25712214; http://dx.doi.org/10.4049/jimmunol.1402622
43. K.Asano, A.Nabeyama, Y.Miyake, C.H.Qiu, A.Kurita, M.Tomura, O.Kanagawa, S.Fujii, M.Tanaka. CD169-positive macrophages dominate antitumor immunity by crosspresenting dead cell-associated antigens. Immunity 2011; 34:85-95; PMID:21194983; http://dx.doi.org/10.1016/j.immuni.2010.12.011
44. T.Miyake, Y.Kumagai, H.Kato, Z.Guo, K.Matsushita, T.Saitoh, T.Kawagoe, H.Kumar, M.H.Jang, T.Kawai et al. Poly I:C-induced activation of NK cells by CD8 α+ dendritic cells via the IPS-1 and TRIF-dependent pathways. J Immunol 2009; 183:2522-8; PMID:19635904; http://dx.doi.org/10.4049/jimmunol.0901500
45. Y.Zhang, G.Chen, Z.Liu, S.Tian, J.Zhang, C.D.Carey, K.M.Murphy, W.J.Storkus, L.D.FaloJr, Z.You. Genetic vaccines to potentiate the effective CD103+ dendritic cell-mediated cross-priming of antitumor immunity. J Immunol 2015; 194:5937-47; PMID:25972487; http://dx.doi.org/10.4049/jimmunol.1500089
46. A.Pantel, A.Teixeira, E.Haddad, E.G.Wood, R.M.Steinman, M.P.Longhi. Direct type I IFN but not MDA5/TLR3 activation of dendritic cells is required for maturation and metabolic shift to glycolysis after poly IC stimulation. PLoS Biol 2014; 12:e1001759; PMID:24409099; http://dx.doi.org/10.1371/journal.pbio.1001759
47. T.N.Schumacher, R.D.Schreiber. Neoantigens in cancer immunotherapy. Science 2015; 348:69-74; PMID:25838375; http://dx.doi.org/10.1126/science.aaa4971
48. C.J.Melief. Cancer immunotherapy by dendritic cells. Immunity 2008; 29:372-83; PMID:18799145; http://dx.doi.org/10.1016/j.immuni.2008.08.004
49. O.A.Ali, C.Verbeke, C.Johnson, R.W.Sands, S.A.Lewin, D.White, E.Doherty, G.Dranoff, D.J.Mooney. Identification of immune factors regulating antitumor immunity using polymeric vaccines with multiple adjuvants. Cancer Res 2014; 74:1670-81; PMID:24480625; http://dx.doi.org/10.1158/0008-5472.CAN-13-0777
50. B.McNally, M.Willette, F.Ye, S.Partida-Sanchez, E.Flaño. Intranasal administration of dsRNA analog poly(I:C) induces interferon-α receptor-dependent accumulation of antigen experienced T cells in the airways. PLoS One 2012; 7:e51351; PMID:23236482; http://dx.doi.org/10.1371/journal.pone.0051351
51. T.Ebihara, M.Azuma, H.Oshiumi, J.Kasamatsu, K.Iwabuchi, K.Matsumoto, H.Saito, T.Taniguchi, M.Matsumoto, T.Seya. Identification of a polyI:C-inducible membrane protein, that participates in dendritic cell-mediated natural killer cell activation. J Exp Med 2010; 207:2675-87; PMID:21059856; http://dx.doi.org/10.1084/jem.20091573
52. T.Akazawa, T.Ebihara, M.Okuno, Y.Okuda, M.Shingai, K.Tsujimura, T.Takahashi, M.Ikawa, M.Okabe, N.Inoue et al. Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells. Proc Natl Acad Sci U S A 2007; 104:252-7; PMID:17190817; http://dx.doi.org/10.1073/pnas.0605978104