Poly-ICLC, a multi-functional immune modulator for treating cancer

Hodi, 2018, Nivolumab plus ipilimumab or nivolumab alone versus ipilimumab alone in advanced melanoma (CheckMate 067): 4-year outcomes of a multicentre, randomised, phase 3 trial, Lancet Oncol., 19, 1480, 10.1016/S1470-2045(18)30700-9 Yang, 2016, Adoptive T-cell therapy for cancer, Adv. Immunol., 130, 279, 10.1016/bs.ai.2015.12.006 Levy, 1975, A modified polyriboinosinic-polyribocytidylic acid complex that induces interferon in primates, J. Infect. Dis., 132, 434, 10.1093/infdis/132.4.434 Levy, 1981, Interferon induction in primates by stabilized polyriiboinosinic acid-polyribocytidylic acid: effect of component size, Infect. Immun., 34, 416, 10.1128/IAI.34.2.416-421.1981 Levine, 1979, Initial clinical trial in cancer patients of polyriboinosinic-polyribocytidylic acid stabilized with poly-L-lysine, in carboxymethylcellulose [poly(ICLC)], a highly effective interferon inducer, Cancer Res., 39, 1645 Maluish, 1985, Immunomodulatory effect of Poly-ICLC in cancer patients, J. Biol. Res. Modif., 4, 656 Talmadge, 1985, Immunotherapeutic potential in murine tumor models of polyinosinic-polycytidylic acid and poly-L-lysine solubilized by carboxymethylcellulose, Cancer Res., 45, 1066 Garcia-Sastre, 2017, Ten strategies of interferon evasion by viruses, Cell Host Microbe, 22, 176, 10.1016/j.chom.2017.07.012 Caskey, 2011, Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans, J. Exp. Med., 208, 2357, 10.1084/jem.20111171 Medzhitov, 2000, Innate immunity, N. Engl. J. Med., 343, 338, 10.1056/NEJM200008033430506 Piccinini, 2010, DAMPening inflammation by modulating TLR signalling, Mediators Inflamm., 2010, 10.1155/2010/672395 Gong, 2020, DAMP-sensing receptors in sterile inflammation and inflammatory diseases, Nat. Rev. Immunol., 20, 95, 10.1038/s41577-019-0215-7 Kawai, 2007, TLR signaling, Semin. Immunol., 19, 24, 10.1016/j.smim.2006.12.004 Takeuchi, 2010, Pattern recognition receptors and inflammation, Cell, 140, 805, 10.1016/j.cell.2010.01.022 Desmet, 2012, Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination, Nat. Rev. Immunol., 12, 479, 10.1038/nri3247 Rakoff-Nahoum, 2009, Toll-like receptors and cancer, Nat. Rev. Cancer, 9, 57, 10.1038/nrc2541 Field, 1967, Inducers of interferon and host resistance. II. Multistranded synthetic polynucleotide complexes, Proc. Natl. Acad. Sci. U. S. A., 58, 1004, 10.1073/pnas.58.3.1004 Levy, 1977, Induction of interferon in vivo by polynucleotides, Tex. Rep. Biol. Med., 35, 91 Levine, 1978, Phase I-II trials of poly IC stabilized with poly-L-lysine, Cancer Treat. Rep., 62, 1907 Carter, 1972, Structural requirements of the rI n -rC n complex for induction of human interferon, J. Mol. Biol., 70, 567, 10.1016/0022-2836(72)90560-8 Avril, 2009, Not all polyriboinosinic-polyribocytidylic acids (Poly I:C) are equivalent for inducing maturation of dendritic cells: implication for alpha-type-1 polarized DCs, J. Immunother., 32, 353, 10.1097/CJI.0b013e31819d29bf Gowen, 2007, TLR3 is essential for the induction of protective immunity against Punta Toro Virus infection by the double-stranded RNA (dsRNA), poly(I:C12U), but not Poly(I:C): differential recognition of synthetic dsRNA molecules, J. Immunol., 178, 5200, 10.4049/jimmunol.178.8.5200 Sugiyama, 2008, Immunoadjuvant effects of polyadenylic:polyuridylic acids through TLR3 and TLR7, Int. Immunol., 20, 1, 10.1093/intimm/dxm112 Thompson, 1996, Results of a double-blind placebo-controlled study of the double-stranded RNA drug polyI:polyC12U in the treatment of HIV infection, Eur. J. Clin. Microbiol. Infect. Dis., 15, 580, 10.1007/BF01709367 Armstrong, 1992, A phase I study of ampligen in human immunodeficiency virus-infected subjects, J. Infect. Dis., 166, 717, 10.1093/infdis/166.4.717 Trumpfheller, 2008, The microbial mimic poly IC induces durable and protective CD4+ T cell immunity together with a dendritic cell targeted vaccine, Proc. Natl. Acad. Sci. U. S. A., 105, 2574, 10.1073/pnas.0711976105 Alexopoulou, 2001, Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3, Nature, 413, 732, 10.1038/35099560 Gitlin, 2006, Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus, Proc. Natl. Acad. Sci. U. S. A., 103, 8459, 10.1073/pnas.0603082103 McCartney, 2009, Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells, J. Exp. Med., 206, 2967, 10.1084/jem.20091181 Kato, 2006, Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses, Nature, 441, 101, 10.1038/nature04734 Kato, 2008, Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5, J. Exp. Med., 205, 1601, 10.1084/jem.20080091 Sultan, 2018, Role of MDA5 and interferon-I in dendritic cells for T cell expansion by anti-tumor peptide vaccines in mice, Cancer Immunol. Immunother., 67, 1091, 10.1007/s00262-018-2164-6 Loo, 2011, Immune signaling by RIG-I-like receptors, Immunity, 34, 680, 10.1016/j.immuni.2011.05.003 Matsumoto, 2008, TLR3: interferon induction by double-stranded RNA including poly(I:C), Adv. Drug Deliv. Rev., 60, 805, 10.1016/j.addr.2007.11.005 Ishii, 2008, Host innate immune receptors and beyond: making sense of microbial infections, Cell Host Microbe, 3, 352, 10.1016/j.chom.2008.05.003 Zou, 2013, Poly IC triggers a cathepsin D- and IPS-1-dependent pathway to enhance cytokine production and mediate dendritic cell necroptosis, Immunity, 38, 717, 10.1016/j.immuni.2012.12.007 Cheng, 2007, Double-stranded DNA and double-stranded RNA induce a common antiviral signaling pathway in human cells, Proc. Natl. Acad. Sci. U. S. A., 104, 9035, 10.1073/pnas.0703285104 Rajan, 2010, Activation of the NLRP3 inflammasome by intracellular poly I:C, FEBS Lett., 584, 4627, 10.1016/j.febslet.2010.10.036 Palchetti, 2015, Transfected poly(I:C) activates different dsRNA receptors, leading to apoptosis or immunoadjuvant response in androgen-independent prostate cancer cells, J. Biol. Chem., 290, 5470, 10.1074/jbc.M114.601625 Schwarzenberger, 2001, Poly-L-lysine-based molecular conjugate vectors: a high efficiency gene transfer system for human progenitor and leukemia cells, Am. J. Med. Sci., 321, 129, 10.1097/00000441-200102000-00004 Zhang, 2010, Poly(L-lysine) nanostructured particles for gene delivery and hormone stimulation, Biomaterials, 31, 1699, 10.1016/j.biomaterials.2009.11.032 Sonawane, 2003, Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes, J. Biol. Chem., 278, 44826, 10.1074/jbc.M308643200 Wagner, 1992, Coupling of adenovirus to transferrin-polylysine/DNA complexes greatly enhances receptor-mediated gene delivery and expression of transfected genes, Proc. Natl. Acad. Sci. U. S. A., 89, 6099, 10.1073/pnas.89.13.6099 Freeman, 2013, Modeling the proton sponge hypothesis: examining proton sponge effectiveness for enhancing intracellular gene delivery through multiscale modeling, J. Biomater. Sci. Polym. Ed., 24, 398, 10.1080/09205063.2012.690282 Longhi, 2009, Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant, J. Exp. Med., 206, 1589, 10.1084/jem.20090247 Stahl-Hennig, 2009, Synthetic double-stranded RNAs are adjuvants for the induction of T helper 1 and humoral immune responses to human papillomavirus in rhesus macaques, PLoS Pathog., 5, 10.1371/journal.ppat.1000373 Cho, 2013, BiVax: a peptide/poly-IC subunit vaccine that mimics an acute infection elicits vast and effective anti-tumor CD8 T-cell responses, Cancer Immunol. Immunother., 62, 787, 10.1007/s00262-012-1382-6 Cho, 2009, Optimized peptide vaccines eliciting extensive CD8 T-cell responses with therapeutic antitumor effects, Cancer Res., 69, 9012, 10.1158/0008-5472.CAN-09-2019 Wang, 2010, Cutting edge: polyinosinic:polycytidylic acid boosts the generation of memory CD8 T cells through melanoma differentiation-associated protein 5 expressed in stromal cells, J. Immunol., 184, 2751, 10.4049/jimmunol.0903201 Salazar, 2014, Therapeutic in situ autovaccination agains solid cancer siwth intratumoral poly-ICLC: case report, hypothesis, and clinical trial, Cancer Immunol. Res., 2, 720, 10.1158/2326-6066.CIR-14-0024 Chew, 2012, TLR 3 expressing tumor parenchyma and infiltrating natural killer cells in hepatocellular carcinoma patients, J. Natl. Cancer Inst., 104, 1796, 10.1093/jnci/djs436 Ho, 2015, TLR3 agonist and Sorafenib combinatorial therapy promotes immune activation and controls hepatocellular carcinoma progression, Oncotarget, 6, 27252, 10.18632/oncotarget.4583 Houot, 2009, T-cell modulation combined with intratumoral CpG cures lymphoma in a mouse model without the need for chemotherapy, Blood, 113, 3546, 10.1182/blood-2008-07-170274 Brody, 2010, In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study, J. Clin. Oncol., 28, 4324, 10.1200/JCO.2010.28.9793 Kyi, 2018, Therapeutic immune modulation against solid cancers with intratumoral poly-ICLC: a pilot trial, Clin. Cancer Res., 24, 4937, 10.1158/1078-0432.CCR-17-1866 Nagato, 2014, Combinatorial immunotherapy of poly-IC and blockade of programmed death-ligand 1 induce effective CD8 T-cell responses against established tumors, Clin. Cancer Res., 20, 1223, 10.1158/1078-0432.CCR-13-2781 Sultan, 2020, Poly-IC enhances the effectiveness of cancer immunotherapy by promoting T cell tumor infiltration, J. Immunother. Cancer, 8, 10.1136/jitc-2020-001224 Muller, 2003, Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response, Trends Immunol., 24, 327, 10.1016/S1471-4906(03)00117-0 Johnson, 2000, A role for the cell adhesion molecule CD44 and sulfation in leukocyte-endothelial cell adhesion during an inflammatory response?, Biochem. Pharmacol., 59, 455, 10.1016/S0006-2952(99)00266-X Sørensen, 2012, The scavenger endothelial cell: a new player in homeostasis and immunity, Am. J. Physiol. Regul. Integr. Comp. Physiol., 303, R1217, 10.1152/ajpregu.00686.2011 Seternes, 2002, Scavenger endothelial cells of vertebrates: a nonperipheral leukocyte system for high-capacity elimination of waste macromolecules, Proc. Natl. Acad. Sci. U. S. A., 99, 7594, 10.1073/pnas.102173299