Effective innate and adaptive antimelanoma immunity through localized TLR7/8 activation

Journal of Immunology

Volumn 193, Issue 9, 2014, Pages 4722-4731

  Singh, Manisha ^a   Khong, Hiep ^a,b   Dai, Zhimin ^a   Huang, Xue Fei ^a   Wargo, Jennifer A ^a   Cooper, Zachary A ^a   Vasilakos, John P ^c   Hwu, Patrick ^a,b   Overwijk, Willem W ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c 3M COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3M 052; ANTIBODY; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GAMMA INTERFERON; INTERFERON; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PERFORIN; PROGRAMMED DEATH 1 LIGAND 1 ANTIBODY; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMIDAZOLE DERIVATIVE; MONOCLONAL ANTIBODY; RESIQUIMOD;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; B LYMPHOCYTE; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG POTENTIATION; INNATE IMMUNITY; MACROPHAGE; MELANOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PLASMACYTOID DENDRITIC CELL; TUMOR IMMUNITY; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOTOXICITY; DRUG EFFECTS; EXPERIMENTAL MELANOMA; IMMUNOLOGY; INTRALESIONAL DRUG ADMINISTRATION; LEUKOCYTE; METABOLISM; PATHOLOGY; PHENOTYPE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL LINE; TUMOR VOLUME;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, MONOCLONAL; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHEMOKINE CCL2; CTLA-4 ANTIGEN; CYTOTOXICITY, IMMUNOLOGIC; IMIDAZOLES; IMMUNITY, INNATE; INJECTIONS, INTRALESIONAL; LEUKOCYTES; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; NITRIC OXIDE; PHENOTYPE; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8; TUMOR BURDEN;

EID: 84908147322     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401160     Document Type: Article

References (52)

1. Hoffmann, J., and S. Akira. 2013. Innate immunity. Curr. Opin. Immunol. 25: 1-3.
2. Lou, Y., C. Liu, G. Lizée, W. Peng, C. Xu, Y. Ye, B. A. Rabinovich, Y. Hailemichael, A. Gelbard, D. Zhou, et al. 2011. Antitumor activity mediated by CpG: the route of administration is critical. J. Immunother. 34: 279-288.
3. Brody, J. D., W. Z. Ai, D. K. Czerwinski, J. A. Torchia, M. Levy, R. H. Advani, Y. H. Kim, R. T. Hoppe, S. J. Knox, L. K. Shin, et al. 2010. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study. J. Clin. Oncol. 28: 4324-4332.
4. Woodmansee, C., J. Pillow, and R. B. Skinner, Jr. 2006. The role of topical immune response modifiers in skin cancer. Drugs 66: 1657-1664.
5. Alessi, S. S., J. A. Sanches, W. R. Oliveira, M. C. Messina, E. R. Pimentel, and C. Festa Neto. 2009. Treatment of cutaneous tumors with topical 5% imiquimod cream. Clinics (Sao Paulo) 64: 961-966.
6. Garland, S. M., J. W. Sellors, A. Wikstrom, C. S. Petersen, C. Aranda, S. Aractingi, and R. D. Maw, Imiquimod Study Group. 2001. Imiquimod 5% cream is a safe and effective self-applied treatment for anogenital warts - results of an open-label, multicentre phase IIIB trial. Int. J. STD AIDS 12: 722-729.
7. Ooi, T., R. S. Barnetson, L. Zhuang, S. McKane, J. H. Lee, H. B. Slade, and G. M. Halliday. 2006. Imiquimod-induced regression of actinic keratosis is associated with infiltration by T lymphocytes and dendritic cells: a randomized controlled trial. Br. J. Dermatol. 154: 72-78.
8. Drobits, B., M. Holcmann, N. Amberg, M. Swiecki, R. Grundtner, M. Hammer, M. Colonna, and M. Sibilia. 2012. Imiquimod clears tumors in mice independent of adaptive immunity by converting pDCs into tumor-killing effector cells. J. Clin. Invest. 122: 575-585.
9. Aranda, F., D. Llopiz, N. Díaz-Valdés, J. I. Riezu-Boj, J. Bezunartea, M. Ruiz, M. Martínez, M. Durantez, C. Mansilla, J. Prieto, et al. 2011. Adjuvant combination and antigen targeting as a strategy to induce polyfunctional and high-avidity T-cell responses against poorly immunogenic tumors. Cancer Res. 71: 3214-3224.
10. Stockfleth, E., U. Trefzer, C. Garcia-Bartels, T. Wegner, T. Schmook, and W. Sterry. 2003. The use of Toll-like receptor-7 agonist in the treatment of basal cell carcinoma: an overview. Br. J. Dermatol. 149(Suppl. 66): 53-56.
11. Mantovani, A., S. Sozzani, M. Locati, P. Allavena, and A. Sica. 2002. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23: 549-555.
12. Biswas, S. K., and A. Mantovani. 2010. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11: 889-896.
13. Nesbit, M., H. Schaider, T. H. Miller, and M. Herlyn. 2001. Low-level monocyte chemoattractant protein-1 stimulation of monocytes leads to tumor formation in nontumorigenic melanoma cells. J. Immunol. 166: 6483-6490.
14. Tang, X., C. Mo, Y. Wang, D. Wei, and H. Xiao. 2013. Anti-tumour strategies aiming to target tumour-associated macrophages. Immunology 138: 93-104.
15. Herwig, M. C., C. Bergstrom, J. R. Wells, T. Höller, and H. E. Grossniklaus. 2013. M2/M1 ratio of tumor associated macrophages and PPAR-γ expression in uveal melanomas with class 1 and class 2 molecular profiles. Exp. Eye Res. 107: 52-58.
16. Heusinkveld, M., and S. H. van der Burg. 2011. Identification and manipulation of tumor associated macrophages in human cancers. J. Transl. Med. 9: 216.
17. Comito, G., E. Giannoni, C. P. Segura, P. Barcellos-de-Souza, M. R. Raspollini, G. Baroni, M. Lanciotti, S. Serni, and P. Chiarugi. 2014. Cancer-associated fibroblasts and M2-polarized macrophages synergize during prostate carcinoma progression. Oncogene 33: 2423-2431.
18. Smirnov, D., J. J. Schmidt, J. T. Capecchi, and P. D. Wightman. 2011. Vaccine adjuvant activity of 3M-052: an imidazoquinoline designed for local activity without systemic cytokine induction. Vaccine 29: 5434-5442.
19. Müller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
20. V600E cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 41: 544-552.
21. Applequist, S. E., R. P. Wallin, and H. G. Ljunggren. 2002. Variable expression of Toll-like receptor in murine innate and adaptive immune cell lines. Int. Immunol. 14: 1065-1074.
22. Hemmi, H., T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, and S. Akira. 2002. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3: 196-200.
23. Shirota, Y., H. Shirota, and D. M. Klinman. 2012. Intratumoral injection of CpG oligonucleotides induces the differentiation and reduces the immunosuppressive activity of myeloid-derived suppressor cells. J. Immunol. 188: 1592-1599.
24. Liu, C., Y. Lou, G. Lizée, H. Qin, S. Liu, B. Rabinovich, G. J. Kim, Y. H. Wang, Y. Ye, A. G. Sikora, et al. 2008. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J. Clin. Invest. 118: 1165-1175.
25. Ma, J., L. Liu, G. Che, N. Yu, F. Dai, and Z. You. 2010. The M1 form of tumor-associated macrophages in non-small cell lung cancer is positively associated with survival time. BMC Cancer 10: 112.
26. Ezekowitz, R. A., and S. Gordon. 1984. Alterations of surface properties by macrophage activation: expression of receptors for Fc and mannose-terminal glycoproteins and differentiation antigens. Contemp. Top. Immunobiol. 13: 33-56.
27. high monocytes. Cancer Res. 70: 5728-5739.
28. Rahat, M. A., and B. Hemmerlein. 2013. Macrophage-tumor cell interactions regulate the function of nitric oxide. Front. Physiol. 4: 144.
29. Perez-Gracia, J. L., S. Labiano, M. E. Rodriguez-Ruiz, M. F. Sanmamed, and I. Melero. 2014. Orchestrating immune check-point blockade for cancer im-munotherapy in combinations. Curr. Opin. Immunol. 27: 89-97.
30. Curran, M. A., W. Montalvo, H. Yagita, and J. P. Allison. 2010. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc. Natl. Acad. Sci. USA 107: 4275-4280.
31. Li, J., W. Song, D. K. Czerwinski, B. Varghese, S. Uematsu, S. Akira, A. M. Krieg, and R. Levy. 2007. Lymphoma immunotherapy with CpG oligo-deoxynucleotides requires TLR9 either in the host or in the tumor itself. J. Immunol. 179: 2493-2500.
32. + dendritic cell subset. Immunol. Rev. 234: 18-31.
33. Inglefield, J. R., C. D. Dumitru, S. S. Alkan, S. J. Gibson, K. E. Lipson, M. A. Tomai, C. J. Larson, and J. P. Vasilakos. 2008. TLR7 agonist 852A inhibition of tumor cell proliferation is dependent on plasmacytoid dendritic cells and type I IFN. J. Interferon Cytokine Res. 28: 253-263.
34. + human plasmacytoid dendritic cells kill tumor cells in vitro: mechanisms of imiquimod-and IFN-α-mediated antitumor reactivity. J. Immunol. 188: 1583-1591.
35. Prins, R. M., N. Craft, K. W. Bruhn, H. Khan-Farooqi, R. C. Koya, R. Stripecke, J. F. Miller, and L. M. Liau. 2006. The TLR-7 agonist, imiquimod, enhances dendritic cell survival and promotes tumor antigen-specific T cell priming: relation to central nervous system antitumor immunity. J. Immunol. 176: 157-164.
36. Broomfield, S. A., R. G. van der Most, A. C. Prosser, S. Mahendran, M. G. Tovey, M. J. Smyth, B. W. Robinson, and A. J. Currie. 2009. Locally administered TLR7 agonists drive systemic antitumor immune responses that are enhanced by anti-CD40 immunotherapy. J. Immunol. 182: 5217-5224.
37. Hansen, B. D., H. Schmidt, H. von der Maase, P. Sjoegren, R. Agger, and M. Hokland. 2006. Tumour-associated macrophages are related to progression in patients with metastatic melanoma following interleukin-2 based immunotherapy. Acta Oncol. 45: 400-405.
38. Byrne, S. N., M. C. Knox, and G. M. Halliday. 2008. TGFβ is responsible for skin tumour infiltration by macrophages enabling the tumours to escape immune destruction. Immunol. Cell Biol. 86: 92-97.
39. Bronkhorst, I. H., and M. J. Jager. 2012. Uveal melanoma: the inflammatory microenvironment. J. Innate Immun. 4: 454-462.
40. Kudo-Saito, C., H. Shirako, M. Ohike, N. Tsukamoto, and Y. Kawakami. 2013. CCL2 is critical for immunosuppression to promote cancer metastasis. Clin. Exp. Metastasis 30: 393-405.
41. O'Sullivan, T., R. Saddawi-Konefka, W. Vermi, C. M. Koebel, C. Arthur, J. M. White, R. Uppaluri, D. M. Andrews, S. F. Ngiow, M. W. Teng, et al. 2012. Cancer immunoediting by the innate immune system in the absence of adaptive immunity. J. Exp. Med. 209: 1869-1882.
42. Fridlender, Z. G., A. Jassar, I. Mishalian, L. C. Wang, V. Kapoor, G. Cheng, J. Sun, S. Singhal, L. Levy, and S. M. Albelda. 2013. Using macrophage activation to augment immunotherapy of established tumours. Br. J. Cancer 108: 1288-1297.
43. De Palma, M., and C. E. Lewis. 2013. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 23: 277-286.
44. Brahmer, J. R. 2012. PD-1-targeted immunotherapy: recent clinical findings. Clin. Adv. Hematol. Oncol. 10: 674-675.
45. Gazzaniga, S., A. I. Bravo, A. Guglielmotti, N. van Rooijen, F. Maschi, A. Vecchi, A. Mantovani, J. Mordoh, and R. Wainstok. 2007. Targeting tumor-associated macrophages and inhibition of MCP-1 reduce angiogenesis and tumor growth in a human melanoma xenograft. J. Invest. Dermatol. 127: 2031-2041.
46. Mizutani, K., S. Sud, N. A. McGregor, G. Martinovski, B. T. Rice, M. J. Craig, Z. S. Varsos, H. Roca, and K. J. Pienta. 2009. The chemokine CCL2 increases prostate tumor growth and bone metastasis through macrophage and osteoclast recruitment. Neoplasia 11: 1235-1242.
47. Zhu, X., M. Fujita, L. A. Snyder, and H. Okada. 2011. Systemic delivery of neutralizing antibody targeting CCL2 for glioma therapy. J. Neurooncol. 104: 83-92.
48. Qian, B. Z., J. Li, H. Zhang, T. Kitamura, J. Zhang, L. R. Campion, E. A. Kaiser, L. A. Snyder, and J. W. Pollard. 2011. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475: 222-225.
49. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227: 75-86.
50. + T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice. J. Immunol. 184: 4006-4016.
51. + T cells. Sci. Transl. Med. 5: 200ra116.
52. Holmgaard, R. B., D. Zamarin, D. H. Munn, J. D. Wolchok, and J. P. Allison. 2013. Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J. Exp. Med. 210: 1389-1402.