A Chemically Defined TLR3 Agonist with Anticancer Activity

References

• Whitmore MM, DeVeer MJ, Edling A, Oates RK, Simons B, Lindner D, Williams BR. Synergistic activation of innate immunity by double-stranded RNA and CpG DNA promotes enhanced antitumor activity. Cancer Res. 2004;64(16):5850–11. doi:10.1158/0008-5472.CAN-04-0063.
   PubMed Web of Science ®Google Scholar
• Salem ML, Kadima AN, Cole DJ, Gillanders WE. Defining the antigen-specific T-cell response to vaccination and poly(I: c)/TLR3 signaling: evidence of enhanced primary and memory CD8 T-cell responses and antitumor immunity. J Immunother. 2005;28(3):220–228. doi:10.1097/01.cji.0000156828.75196.0d.
   PubMed Web of Science ®Google Scholar
• Tormo D, Ferrer A, Bosch P, Gaffal E, Basner-Tschakarjan E, Wenzel J, Tuting T. Therapeutic efficacy of antigen-specific vaccination and toll-like receptor stimulation against established transplanted and autochthonous melanoma in mice. Cancer Res. 2006;66(10):5427–5435. doi:10.1158/0008-5472.CAN-06-0399.
   PubMed Web of Science ®Google Scholar
• Muthuswamy R, Wang L, Pitteroff J, Gingrich JR, Kalinski P. Combination of IFNα and poly-I: c reprograms bladder cancer microenvironment for enhanced CTL attraction. J ImmunoTher Cancer. 2015;3(1):6. doi:10.1186/s40425-015-0050-8.
   PubMedGoogle Scholar
• Ayari C, Besancon M, Bergeron A, LaRue H, Bussieres V, Fradet Y. Poly(i: c) potentiates bacillus calmette-guerin immunotherapy for bladder cancer. Cancer Immunol Immunother. 2016;65(2):223–234. doi:10.1007/s00262-015-1789-y.
   PubMed Web of Science ®Google Scholar
• De Waele J, Marcq E, Van Audenaerde JR, Van Loenhout J, Deben C, Zwaenepoel K, Van de Kelft E, Van der Planken D, Menovsky T, Van den Bergh JM, et al. Poly(i: c) primes primary human glioblastoma cells for an immune response invigorated by PD-L1 blockade. Oncoimmunology. 2018;7(3):e1407899. doi:10.1080/2162402X.2017.1407899.
   PubMed Web of Science ®Google Scholar
• Aznar MA, Planelles L, Perez-Olivares M, Molina C, Garasa S, Etxeberria I, Perez G, Rodriguez I, Bolanos E, Lopez-Casas P, et al. Immunotherapeutic effects of intratumoral nanoplexed poly I: c. J ImmunoTher Cancer. 2019;7(1):116. doi:10.1186/s40425-019-0568-2.
   PubMed Web of Science ®Google Scholar
• Le Naour J, Liu P, Zhao L, Adjemian S, Sztupinszki Z, Taieb J, Mulot C, Silvin A, Dutertre CA, Ginhoux F, et al. A TLR3 ligand reestablishes chemotherapeutic responses in the context of FPR1 deficiency. Cancer Discov. 2020;11(2):408–423. doi:10.1158/2159-8290.CD-20-0465.
   PubMed Web of Science ®Google Scholar
• Alvarez M, Molina C, De Andrea CE, Fernandez-Sendin M, Villalba M, Gonzalez-Gomariz J, Ochoa MC, Teijeira A, Glez-Vaz J, Aranda F, et al. Intratumoral co-injection of the poly I: c-derivative BO-112 and a STING agonist synergize to achieve local and distant anti-tumor efficacy. J ImmunoTher Cancer. 2021;9(11):e002953. doi:10.1136/jitc-2021-002953.
   PubMed Web of Science ®Google Scholar
• Jiang Q, Wei H, Tian Z. Poly I: c enhances cycloheximide-induced apoptosis of tumor cells through TLR3 pathway. Bmc Cancer. 2008;8:12. doi:10.1186/1471-2407-8-12.
   PubMed Web of Science ®Google Scholar
• Boullart AC, Aarntzen EH, Verdijk P, Jacobs JF, Schuurhuis DH, Benitez-Ribas D, Schreibelt G, van de Rakt MW, Scharenborg NM, de Boer A, et al. Maturation of monocyte-derived dendritic cells with toll-like receptor 3 and 7/8 ligands combined with prostaglandin E2 results in high interleukin-12 production and cell migration. Cancer Immunol Immunother. 2008;57(11):1589–1597. doi:10.1007/s00262-008-0489-2.
   PubMed Web of Science ®Google Scholar
• Girart MV, Fuertes MB, Domaica CI, Rossi LE, Zwirner NW. Engagement of TLR3, TLR7, and NKG2D regulate IFN-gamma secretion but not NKG2D-mediated cytotoxicity by human NK cells stimulated with suboptimal doses of IL-12. J Immunol. 2007;179(6):3472–3479. doi:10.4049/jimmunol.179.6.3472.
   PubMed Web of Science ®Google Scholar
• Shime H, Matsumoto M, Oshiumi H, Tanaka S, Nakane A, Iwakura Y, Tahara H, Inoue N, Seya T. Toll-like receptor 3 signaling converts tumor-supporting myeloid cells to tumoricidal effectors. Proc Natl Acad Sci U S A. 2012;109(6):2066–2071. doi:10.1073/pnas.1113099109.
   PubMed Web of Science ®Google Scholar
• Forghani P, Waller EK. Poly (I: c) modulates the immunosuppressive activity of myeloid-derived suppressor cells in a murine model of breast cancer. Breast Cancer Res Treat. 2015;153(1):21–30. doi:10.1007/s10549-015-3508-y.
   PubMed Web of Science ®Google Scholar
• Chin AI, Miyahira AK, Covarrubias A, Teague J, Guo B, Dempsey PW, Cheng G. Toll-like receptor 3-mediated suppression of TRAMP prostate cancer shows the critical role of type I interferons in tumor immune surveillance. Cancer Res. 2010;70(7):2595–2603. doi:10.1158/0008-5472.CAN-09-1162.
   PubMed Web of Science ®Google Scholar
• Galli R, Starace D, Busa R, Angelini DF, Paone A, De Cesaris P, Filippini A, Sette C, Battistini L, Ziparo E, et al. TLR stimulation of prostate tumor cells induces chemokine-mediated recruitment of specific immune cell types. J Immunol. 2010;184(12):6658–6669. doi:10.4049/jimmunol.0902401.
   PubMed Web of Science ®Google Scholar
• Sistigu A, Yamazaki T, Vacchelli E, Chaba K, Enot DP, Adam J, Vitale I, Goubar A, Baracco EE, Remedios C, et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med. 2014;20(11):1301–1309. doi:10.1038/nm.3708.
   PubMed Web of Science ®Google Scholar
• Vacchelli E, Sistigu A, Yamazaki T, Vitale I, Zitvogel L, Kroemer G. Autocrine signaling of type 1 interferons in successful anticancer chemotherapy. Oncoimmunol. 2015;4:e988042.
   PubMed Web of Science ®Google Scholar
• Fan L, Zhou P, Chen AX, Liu GY, Yu KD, Shao ZM. Toll-like receptor 3 -926T>A increased the risk of breast cancer through decreased transcriptional activity. Oncoimmunol. 2019;8(12):e1673126. doi:10.1080/2162402X.2019.1673126.
   PubMed Web of Science ®Google Scholar
• Castro FA, Forsti A, Buch S, Kalthoff H, Krauss C, Bauer M, Egberts J, Schniewind B, Broering DC, Schreiber S, et al. TLR-3 polymorphism is an independent prognostic marker for stage II colorectal cancer. Eur J Cancer. 2011;47(8):1203–1210. doi:10.1016/j.ejca.2010.12.011.
   PubMed Web of Science ®Google Scholar
• Huang Z, He A, Wang J, Lu H, Xu X, Zhang R, Liao W, Feng Q, Wu L. Toll-like receptor 3 is a potential prognosis marker and associated with immune infiltration in stomach adenocarcinoma. Cancer Biomark. 2022;34(1):77–93. doi:10.3233/CBM-210354.
   PubMed Web of Science ®Google Scholar
• Mosaad YM, Metwally SS, Farag RE, Lotfy ZF, AbdelTwab HE. Association between toll-like receptor 3 (TLR3) rs3775290, TLR7 rs179008, TLR9 rs352140 and chronic HCV. Immunol Invest. 2019;48(3):321–332. doi:10.1080/08820139.2018.1527851.
   PubMed Web of Science ®Google Scholar
• Sghaier I, Zidi S, Mouelhi L, Ghazoueni E, Brochot E, Almawi WY, Loueslati BY. TLR3 and TLR4 SNP variants in the liver disease resulting from hepatitis B virus and hepatitis C virus infection. Br J Biomed Sci. 2019;76(1):35–41. doi:10.1080/09674845.2018.1547179.
   PubMed Web of Science ®Google Scholar
• Melssen MM, Petroni GR, Chianese-Bullock KA, Wages NA, Grosh WW, Varhegyi N, Smolkin ME, Smith KT, Galeassi NV, Deacon DH, et al. A multipeptide vaccine plus toll-like receptor agonists LPS or polyICLC in combination with incomplete freund’s adjuvant in melanoma patients. J ImmunoTher Cancer. 2019;7(1):163. doi:10.1186/s40425-019-0625-x.
   PubMed Web of Science ®Google Scholar
• Pavlick A, Blazquez AB, Meseck M, Lattanzi M, Ott PA, Marron TU, Holman RM, Mandeli J, Salazar AM, McClain CB, et al. Combined vaccination with NY-ESO-1 protein, poly-ICLC, and montanide improves humoral and cellular immune responses in patients with high-risk melanoma. Cancer Immunol Res. 2020;8(1):70–80. doi:10.1158/2326-6066.CIR-19-0545.
   PubMed Web of Science ®Google Scholar
• Slingluff CL Jr., Petroni GR, Chianese-Bullock KA, Wages NA, Olson WC, Smith KT, Haden K, Dengel LT, Dickinson A, Reed C, et al. Trial to evaluate the immunogenicity and safety of a melanoma helper peptide vaccine plus incomplete freund’s adjuvant, cyclophosphamide, and polyICLC (Mel63). J ImmunoTher Cancer. 2021;9(1):e000934. doi:10.1136/jitc-2020-000934.
   PubMed Web of Science ®Google Scholar
• Kyi C, Roudko V, Sabado R, Saenger Y, Loging W, Mandeli J, Thin TH, Lehrer D, Donovan M, Posner M, et al. Therapeutic immune modulation against solid cancers with intratumoral poly-ICLC: a pilot trial. Clin Cancer Res. 2018;24(20):4937–4948. doi:10.1158/1078-0432.CCR-17-1866.
   PubMed Web of Science ®Google Scholar
• Hammerich L, Marron TU, Upadhyay R, Svensson-Arvelund J, Dhainaut M, Hussein S, Zhan Y, Ostrowski D, Yellin M, Marsh H, et al. Systemic clinical tumor regressions and potentiation of PD1 blockade with in situ vaccination. Nat Med. 2019;25(5):814–824. doi:10.1038/s41591-019-0410-x.
   PubMed Web of Science ®Google Scholar
• Marquez-Rodas I, Longo F, Rodriguez-Ruiz ME, Calles A, Ponce S, Jove M, Rubio-Viqueira B, Perez-Gracia JL, Gomez-Rueda A, Lopez-Tarruella S, et al. Intratumoral nanoplexed poly I: c BO-112 in combination with systemic anti-PD-1 for patients with anti-PD-1-refractory tumors. Sci Transl Med. 2020;12(565). doi:10.1126/scitranslmed.abb0391.
   PubMed Web of Science ®Google Scholar
• Le Naour J, Galluzzi L, Zitvogel L, Kroemer G, Vacchelli E. Trial watch: tLR3 agonists in cancer therapy. Oncoimmunol. 2020;9(1):1771143. doi:10.1080/2162402X.2020.1771143.
   PubMed Web of Science ®Google Scholar
• Le Naour J, Kroemer G. Trial watch: toll-like receptor ligands in cancer therapy. Oncoimmunol. 2023;12(1):2180237. doi:10.1080/2162402X.2023.2180237.
   PubMed Web of Science ®Google Scholar
• Thierry S, Maadadi S, Berton A, Dimier L, Perret C, Vey N, Ourfali S, Saccas M, Caron S, Boucard-Jourdin M, et al. TL-532, a novel specific toll-like receptor 3 agonist rationally designed for targeting cancers: discovery process and biological characterization. Microbial Cell. 2023;10(6):117–132. in press. doi:10.15698/mic2023.06.797.
   PubMed Web of Science ®Google Scholar
• Zhao L, Liu P, Xie W, Zhang S, Thieme S, Zitvogel L, Kroemer G, Kepp O. A genotype-phenotype screening system using conditionally immortalized immature dendritic cells. STAR Protoc. 2021;2(3):100732. doi:10.1016/j.xpro.2021.100732.
   PubMedGoogle Scholar
• Vacchelli E, Ma Y, Baracco EE, Sistigu A, Enot DP, Pietrocola F, Yang H, Adjemian S, Chaba K, Semeraro M, et al. Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1. Science. 2015;350(6263):972–978. doi:10.1126/science.aad0779.
   PubMed Web of Science ®Google Scholar
• Salaun B, Zitvogel L, Asselin-Paturel C, Morel Y, Chemin K, Dubois C, Massacrier C, Conforti R, Chenard MP, Sabourin JC, et al. TLR3 as a biomarker for the therapeutic efficacy of double-stranded RNA in breast cancer. Cancer Res. 2011;71(5):1607–1614. doi:10.1158/0008-5472.CAN-10-3490.
   PubMed Web of Science ®Google Scholar
• Migeotte I, Communi D, Parmentier M. Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev. 2006;17(6):501–519. doi:10.1016/j.cytogfr.2006.09.009.
   PubMed Web of Science ®Google Scholar
• Biselli E, Agliari E, Barra A, Bertani FR, Gerardino A, De Ninno A, Mencattini A, Di Giuseppe D, Mattei F, Schiavoni G, et al. Organs on chip approach: a tool to evaluate cancer -immune cells interactions. Sci Rep. 2017;7(1):12737. doi:10.1038/s41598-017-13070-3.
   PubMed Web of Science ®Google Scholar
• Enot DP, Vacchelli E, Jacquelot N, Zitvogel L, Kroemer G. TumGrowth: an open-access web tool for the statistical analysis of tumor growth curves. Oncoimmunol. 2018;7(9):e1462431. doi:10.1080/2162402X.2018.1462431.
   PubMed Web of Science ®Google Scholar