Intratumoral delivery of TriMix mRNA results in T-cell activation by cross-presenting dendritic cells

Cancer Immunology Research

Volumn 4, Issue 2, 2016, Pages 146-156

  Van Lint, Sandra ^a   Renmans, Dries ^a   Broos, Katrijn ^a   Goethals, Lode ^a   Maenhout, Sarah ^a   Benteyn, Daphne ^a   Goyvaerts, Cleo ^a   Du Four, Stephanie ^a   Van Der Jeught, Kevin ^a   Bialkowski, Lukasz ^a   Flamand, Veronique ^b   Heirman, Carlo ^a   Thielemans, Kris ^a   Breckpot, Karine ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CD70 ANTIGEN; MESSENGER RNA; TOLL LIKE RECEPTOR 4; TUMOR ANTIGEN; BIOLOGICAL MARKER; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLUMINESCENCE; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; DENDRITIC CELL; DRUG DELIVERY SYSTEM; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; T LYMPHOCYTE ACTIVATION; TUMOR CELL INOCULATION; TUMOR GROWTH; ANIMAL; CROSS PRESENTATION; CYTOTOXICITY; DISEASE MODEL; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MORTALITY; NEOPLASM; PATHOLOGY; PHENOTYPE; T LYMPHOCYTE; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD70; BIOMARKERS; CD40 LIGAND; CELL LINE, TUMOR; CROSS-PRIMING; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; LYMPHOCYTE ACTIVATION; MICE; NEOPLASMS; PHENOTYPE; RNA, MESSENGER; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 4;

EID: 84962019868     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0163     Document Type: Article

References (42)

1. Pinzon-Charry A, Maxwell T, Lopez JA. Dendritic cell dysfunction in cancer: a mechanism for immunosuppression. Immunol Cell Biol 2005;83:451-61.
2. Tran Janco JM, Lamichhane P, Karyampudi L, Knutson KL. Tumorinfiltrating dendritic cells in cancer pathogenesis. J Immunol 2015;194:2985-91.
3. Van der Jeught K, Bialkowski L, Daszkiewicz L, Broos K, Goyvaerts C, Renmans D, et al. Targeting the tumor microenvironment to enhance antitumor immune responses. Oncotarget 2015;6:1359-81.
4. Singh M, Overwijk WW. Intratumoral immunotherapy for melanoma. Cancer Immunol Immunother 2015;64:911-21.
5. Marabelle A, Kohrt H, Caux C, Levy R. Intratumoral immunization: a new paradigm for cancer therapy. Clin Cancer Res 2014;20:1747-56.
6. Huang B, Zhao J, Li H, He KL, Chen Y, Chen SH, et al. Toll-like receptors on tumor cells facilitate evasion of immune surveillance. Cancer Res 2005;65:5009-14.
7. Chiodoni C, Lezzi M, Guiducci C, Sangaletti S, Alessandrini I, Ratti C, et al. Triggering CD40 on endothelial cells contributes to tumor growth. J Exp Med 2006;203:2441-50.
8. Furumoto K, Soares L, Engleman EG, Merad M. Induction of potent antitumor immunity by in situ targeting of intratumoral DCs. J Clin Invest 2004;113:774-83.
9. 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;322:1097-100.
10. Kreutz M, Tacken PJ, Figdor CG. Targeting dendritic cells-why bother? Blood 2013;121:2836-44.
11. Kreutz M, Giquel B, Hu Q, Abuknesha R, Uematsu S, Akira S, et al. Antibody-antigen-adjuvant conjugates enable co-delivery of antigen and adjuvant to dendritic cells in cis but only have partial targeting specificity. PLoS One 2011;7:e40208.
12. Tacken PJ, Zeelenberg IS, Cruz LJ, van Hout-Kuijer MA, van de Glind G, Fokkink RG, et al. Targeted delivery of TLR ligands to human and mouse dendritic cells strongly enhances adjuvanticity. Blood 2011;118:6836-44.
13. Tacken PJ, Figdor CG. Targeted antigen delivery and activation of dendritic cells in vivo: steps towards cost effective vaccines. Semin Immunol 2011;23:12-20.
14. Goyvaerts C, Broos K, Escors D, Heirman C, Raes G, De Baetselier P, et al. The transduction pattern of IL-12-encoding lentiviral vectors shapes the immunological outcome. Eur J Immunol 2015;45:3351-61.
15. Goyvaerts C, Breckpot K. Pros and cons of antigen-presenting cell targeted tumor vaccines. J Immunol Res 2015;2015:785634.
16. Goyvaerts C, De Groeve K, Van Lint S, Heirman C, Van Ginderachter JA, De Baetselier P, et al. Immunogenicity of targeted lentivectors. Oncotarget 2014;5:704-15.
17. Bonehill A, Tuyaerts S, Van Nuffel AM, Heirman C, Bos TJ, Fostier K, et al. Enhancing the T-cell stimulatory capacity of human dendritic cells by coelectroporation with CD40L, CD70 and constitutively active TLR4 encoding mRNA. Mol Ther 2008;16:1170-80.
18. Bonehill A, Van Nuffel AM, Corthals J, Tuyaerts S, Heirman C, François V, et al. Single-step antigen loading and activation of dendritic cells by mRNA electroporation for the purpose of therapeutic vaccination in melanoma patients. Clin Cancer Res 2009;15:3366-75.
19. Van Lint S, Goyvaerts C, Maenhout S, Goethals L, Disy A, Benteyn D, et al. Preclinical evaluation of TriMix and antigen mRNA-based antitumor therapy. Cancer Res 2012;72:1661-71.
20. Pen JJ, De Keersmaecker B, Maenhout SK, Van Nuffel AM, Heirman C, Corthals J, et al. Modulation of regulatory T cell function by monocytederived dendritic cells matured through electroporation with mRNA encoding CD40 ligand, constitutively active TLR4, and CD70. J Immunol 2013;191:1976-83.
21. Breckpot K, Dullaers M, Bonehill A, van Meirvenne S, Heirman C, de Greef C, et al. Lentivirally transduced dendritic cells as a tool for cancer immunotherapy. J Gene Med 2003;5:654-67.
22. Bonehill A, Heirman C, Tuyaerts S, Michiels A, Breckpot K, Brasseur F, et al. Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules. J Immunol 2004;172:6649-57.
23. Van der Jeught K, Tjok Joe P, Bialkowski L, Heirman C, Daszkiewicz L, Liechtenstein T, et al. Intratumoral administration of mRNA encoding a fusokine consisting of IFN-beta and the ectodomain of the TGF-beta receptor II potentiates antitumor immunity. Oncotarget 2014;5:10100-13.
24. Keyaerts M, Verschueren J, Bos TJ, Tchouate-Gainkam LO, Peleman C, Breckpot K, et al. Dynamic bioluminescence imaging for quantitative tumour burden assessment using IV or IP administration of D: -luciferin: effect on intensity, time kinetics and repeatability of photon emission. Eur J Nucl Med Mol Imaging 2008;35:999-1007.
25. Dullaers M, Breckpot K, Van Meirvenne S, Bonehill A, Tuyaerts S, Michiels A, et al. Side-by-side comparison of lentivirally transduced and mRNA-electroporated dendritic cells: implications for cancer immunotherapy protocols. Mol Ther 2004;10:768-79.
26. Breckpot K, Escors D, Arce F, Lopes L, Karwacz K, Van Lint S, et al. HIV-1 lentiviral vector immunogenicity ismediated by Toll-like receptor3 (TLR3) and TLR7. J Virol 2010;84:5627-36.
27. Zhi L, Kim P, Thompson BD, Pitsillides C, Bankovich AJ, Yun SH, et al. FTY720 blocks egress of T cells in part by abrogation of their adhesion on the lymph node sinus. J Immunol 2011;187:2244-51.
28. Hargadon KM. Tumor-altered dendritic cell function: implications for antitumor immunity. Front Immunol 2013;4:192.
29. 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;26:638-52.
30. Marzo AL, Lake RA, Lo D, Sherman L, McWilliam A, Nelson D, et al. Tumor antigens are constitutively presented in the draining lymph nodes. J Immunol 1999;162:5838-45.
31. Bai XF, Gao JX, Liu J, Wen J, Zheng P, Liu Y. On the site and mode of antigen presentation for the initiationof clonal expansion of CD8 T cells specific for a natural tumor antigen. Cancer Res 2001;61:6860-7.
32. Hargadon KM, Brinkman CC, Sheasley-O'neill S L, Nichols LA, Bullock TN, Engelhard VH. Incomplete differentiation of antigenspecific CD8 T cells in tumor-draining lymph nodes. J Immunol 2006;177:6081-90.
33. 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;14:135-46.
34. Boisguerin V, Castle JC, Loewer M, Diekmann J, Mueller F, Britten CM, et al. Translation of genomics-guided RNA-based personalised cancer vaccines: towards the bedside. Br J Cancer 2014;111:1469-75.
35. Kreiter S, Castle JC, Tureci O, Sahin U. Targeting the tumor mutanome for personalized vaccination therapy. Oncoimmunology 2012;1:768-9.
36. Castle JC, Kreiter S, Diekmann J, Löwer M, van de Roemer N, de Graaf J, et al. Exploiting the mutanome for tumor vaccination. Cancer Res 2012;72:1081-91.
37. Baars PA, Sierro S, Arens R, Tesselaar K, Hooibrink B, Klenerman P, et al. Properties of murine (CD8+) CD27-T cells. Eur J Immunol 2005;35:3131-41.
38. Diken M, Kreiter S, Selmi A, Britten CM, Huber C, Türeci Ö, et al. Selective uptake of naked vaccine RNA by dendritic cells is driven by macropinocytosis and abrogated upon DC maturation. Gene Ther 2011;18:702-8.
39. Sahin U, Kariko K, Tureci O. mRNA-based therapeutics-developing a new class of drugs. Nat Rev Drug Discov 2014;13:759-80.
40. Anderson BR, Muramatsu H, Jha BK, Silverman RH, Weissman D, Kariko K. Nucleoside modifications in RNA limit activation of 2' -5'-oligoadenylate synthetase and increase resistance to cleavage by RNase L. Nucleic Acids Res 2011;39:9329-38.
41. Anderson BR, Muramatsu H, Nallagatla SR, Bevilacqua PC, Sansing LH, Weissman D, et al. Incorporation of pseudouridine into mRNA enhances translation by diminishing PKR activation. Nucleic Acids Res 2010;38:5884-92.
42. Kariko K, Muramatsu H, Welsh FA, Ludwig J, Kato H, Akira S, et al. Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Mol Ther 2008;16:1833-40.