Tumor-targeting oncolytic virus elicits potent immunotherapeutic vaccine responses to tumor antigens

References

• Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell. 2017;168:707–18. doi:10.1016/j.cell.2017.01.017.
   PubMed Web of Science ®Google Scholar
• Khalil DN, Smith EL, Brentjens RJ, Wolchok JD. The future of cancer treatment: immunomodulation, cars and combination immunotherapy. Nat Rev Clin Oncol. 2016;13:273–290. doi:10.1038/nrclinonc.2016.25.
   PubMed Web of Science ®Google Scholar
• Lichty BD, Breitbach CJ, Stojdl DF, Bell JC. Going viral with cancer immunotherapy. Nat Rev Cancer. 2014;14:559–567. doi:10.1038/nrc3770.
   PubMed Web of Science ®Google Scholar
• Russell SJ, Peng KW, Bell JC. Oncolytic virotherapy. Nat Biotechnol. 2012;30:658–670. doi:10.1038/nbt.2287.
   PubMed Web of Science ®Google Scholar
• Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, Delman KA, Spitler LE, Puzanov I, Agarwala SS, et al. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol. 2015;33:2780–2788. doi:10.1200/JCO.2014.58.3377.
   PubMed Web of Science ®Google Scholar
• Ribas A, Dummer R, Puzanov I, VanderWalde A, Andtbacka RHI, Michielin O, Olszanski AJ, Malvehy J, Cebon J, Fernandez E, et al. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell. 2017;170:1109–1119 e1110. doi:10.1016/j.cell.2017.08.027.
   PubMed Web of Science ®Google Scholar
• Russell SJ, Barber GN. Oncolytic viruses as antigen-agnostic cancer vaccines. Cancer Cell. 2018;33:599–605. doi:10.1016/j.ccell.2018.03.011.
   PubMed Web of Science ®Google Scholar
• Fountzilas C, Patel S, Mahalingam D. Oncolytic virotherapy, updates and future directions. Oncotarget. 2017;8:102617–102639. doi:10.18632/oncotarget.18309.
   PubMedGoogle Scholar
• Ferguson MS, Lemoine NR, Wang Y. Systemic delivery of oncolytic viruses: hopes and hurdles. Adv Virol. 2012;2012:805629. doi:10.1155/2012/805629.
   PubMedGoogle Scholar
• Lawler SE, Speranza MC, Cho CF, Chiocca EA. Oncolytic viruses in cancer treatment: a review. JAMA Oncol. 2017;3:841–849. doi:10.1001/jamaoncol.2016.2064.
   PubMed Web of Science ®Google Scholar
• Kepp O, Senovilla L, Vitale I, Vacchelli E, Adjemian S, Agostinis P, Apetoh L, Aranda F, Barnaba V, Bloy N, et al. Consensus guidelines for the detection of immunogenic cell death. Oncoimmunology. 2014;3:e955691. doi:10.4161/21624011.2014.955691.
   PubMed Web of Science ®Google Scholar
• Bartlett DL, Liu Z, Sathaiah M, Ravindranathan R, Guo Z, He Y, Guo ZS. Oncolytic viruses as therapeutic cancer vaccines. Mol Cancer. 2013;12:103. doi:10.1186/1476-4598-12-103.
   PubMed Web of Science ®Google Scholar
• Yin J, Markert JM, Leavenworth JW. Modulation of the intratumoral immune landscape by oncolytic herpes simplex virus virotherapy. Front Oncol. 2017;7:136. doi:10.3389/fonc.2017.00136.
   PubMed Web of Science ®Google Scholar
• Robert C. Checkpoint blockade plus oncolytic virus: a hot therapeutic cancer strategy. Trends Mol Med. 2017;23:983–985. doi:10.1016/j.molmed.2017.09.008.
   PubMed Web of Science ®Google Scholar
• Varghese S, Rabkin SD. Oncolytic herpes simplex virus vectors for cancer virotherapy. Cancer Gene Ther. 2002;9:967–978. doi:10.1038/sj.cgt.7700537.
   PubMed Web of Science ®Google Scholar
• Walsh D, Mohr I. Phosphorylation of eIF4E by Mnk-1 enhances HSV-1 translation and replication in quiescent cells. Genes Dev. 2004;18:660–672. doi:10.1101/gad.1185304.
   PubMed Web of Science ®Google Scholar
• Liu BL, Robinson M, Han ZQ, Branston RH, English C, Reay P, McGrath Y, Thomas SK, Thornton M, Bullock P, et al. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene Ther. 2003;10:292–303. doi:10.1038/sj.gt.3301885.
   PubMed Web of Science ®Google Scholar
• MacLean AR, ul-Fareed M, Robertson L, Harland J, Brown SM. Herpes simplex virus type 1 deletion variants 1714 and 1716 pinpoint neurovirulence-related sequences in glasgow strain 17+ between immediate early gene 1 and the ‘a’ sequence. J Gen Virol. 1991;72(Pt 3):631–639. doi:10.1099/0022-1317-72-3-631.
   PubMed Web of Science ®Google Scholar
• Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello G, Wright W, Weinrich S, Shay J, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994;266:2011–2015. doi:10.1126/science.7605428.
   PubMed Web of Science ®Google Scholar
• Wirth T, Zender L, Schulte B, Mundt B, Plentz R, Rudolph KL, Manns M, Kubicka S, Kühnel F, et al. A telomerase-dependent conditionally replicating adenovirus for selective treatment of cancer. Cancer Res. 2003;63:3181–3188.
   PubMed Web of Science ®Google Scholar
• Huang TG, Savontaus MJ, Shinozaki K, Sauter BV, Woo SL. Telomerase-dependent oncolytic adenovirus for cancer treatment. Gene Ther. 2003;10:1241–1247. doi:10.1038/sj.gt.3301987.
   PubMed Web of Science ®Google Scholar
• Kawashima T, Kagawa S, Kobayashi N, Shirakiya Y, Umeoka T, Teraishi F, Taki M, Kyo S, Tanaka N, Fujiwara T, et al. Telomerase-specific replication-selective virotherapy for human cancer. Clin Cancer Res. 2004;10:285–292. doi:10.1158/1078-0432.CCR-1075-3.
   PubMed Web of Science ®Google Scholar
• Huang Q, Zhang X, Wang H, Yan B, Kirkpatrick J, Dewhrist MW, Li CY. A novel conditionally replicative adenovirus vector targeting telomerase-positive tumor cells. Clin Cancer Res. 2004;10:1439–1445. doi:10.1158/1078-0432.CCR-03-0122.
   PubMed Web of Science ®Google Scholar
• Li WC, Ralphs KL, Tosh D. Isolation and culture of adult mouse hepatocytes. Methods Mol Biol. 2010;633:185–196.
   PubMedGoogle Scholar
• Zhao W, Wang L, Han H, Jin K, Lin N, Guo T, Chen Y, Cheng H, Lu F, Fang W, et al. 1B50-1, a mAb raised against recurrent tumor cells, targets liver tumor-initiating cells by binding to the calcium channel alpha2delta1 subunit. Cancer Cell. 2013;23:541–556. doi:10.1016/j.ccr.2013.02.025.
   PubMed Web of Science ®Google Scholar
• Lin C, Li H, Hao M, Xiong D, Luo Y, Huang C, Yuan Q, Zhang J, Xia N, et al. Increasing the efficiency of CRISPR/Cas9-mediated precise genome editing of HSV-1 virus in human cells. Sci Rep. 2016;6:34531. doi:10.1038/srep34531.
   PubMed Web of Science ®Google Scholar
• Takakura M, Kyo S, Kanaya T, Hirano H, Takeda J, Yutsudo M, Inoue M. Cloning of human telomerase catalytic subunit (hTERT) gene promoter and identification of proximal core promoter sequences essential for transcriptional activation in immortalized and cancer cells. Cancer Res. 1999;59:551–557.
   PubMed Web of Science ®Google Scholar
• Maclean AR. Preparation of HSV-DNA and production of infectious virus. Methods Mol Med. 1998;10:19–25. doi:10.1385/0-89603-347-3:19.
   PubMedGoogle Scholar
• Lynas C, Hill TJ, Maitland NJ, Love S. Latent infection with the MS strain of herpes simplex virus type 2 in the mouse following intracerebral inoculation. J Neurol Sci. 1993;120:107–114. doi:10.1016/0022-510X(93)90033-U.
   PubMed Web of Science ®Google Scholar
• Huang CH, Yuan Q, Chen PJ, Zhang YL, Chen CR, Zheng QB, Yeh S-H, Yu H, Xue Y, Chen Y-X, et al. Influence of mutations in hepatitis B virus surface protein on viral antigenicity and phenotype in occult HBV strains from blood donors. J Hepatol. 2012;57:720–729. doi:10.1016/j.jhep.2012.05.009.
   PubMed Web of Science ®Google Scholar
• Hummel JL, Safroneeva E, Mossman KL. The role of ICP0-Null HSV-1 and interferon signaling defects in the effective treatment of breast adenocarcinoma. Mol Ther. 2005;12:1101–1110. doi:10.1016/j.ymthe.2005.07.533.
   PubMed Web of Science ®Google Scholar
• Holay N, Kim Y, Lee P, Gujar S. Sharpening the edge for precision cancer immunotherapy: targeting tumor antigens through oncolytic vaccines. Front Immunol. 2017;8:800. doi:10.3389/fimmu.2017.00800.
   PubMed Web of Science ®Google Scholar
• Romero D. Immunotherapy: oncolytic viruses prime antitumour immunity. Nat Rev Clin Oncol. 2018;15:135. doi:10.1038/nrclinonc.2018.15.
   PubMed Web of Science ®Google Scholar
• Samson A, Scott KJ, Taggart D, West EJ, Wilson E, Nuovo GJ, Thomson S, Corns R, Mathew RK, Fuller MJ, et al. Intravenous delivery of oncolytic reovirus to brain tumor patients immunologically primes for subsequent checkpoint blockade. Sci Transl Med. 2018;10:eaam7577. doi:10.1126/scitranslmed.aam7577.
   PubMed Web of Science ®Google Scholar
• Desjardins A, Gromeier M, Herndon JE 2nd, Beaubier N, Bolognesi DP, Friedman AH, Friedman HS, McSherry F, Muscat AM, Nair S, et al. Recurrent Glioblastoma treated with recombinant poliovirus. N Engl J Med. 2018;379:150–161. doi:10.1056/NEJMoa1716435.
   PubMed Web of Science ®Google Scholar
• Russell SJ, Peng KW. Oncolytic virotherapy: a contest between apples and oranges. Mol Ther. 2017;25:1107–1116. doi:10.1016/j.ymthe.2017.03.026.
   PubMed Web of Science ®Google Scholar
• Le Boeuf F, Batenchuk C, Vaha-Koskela M, Breton S, Roy D, Lemay C, Cox J, Abdelbary H, Falls T, Waghray G, et al. Model-based rational design of an oncolytic virus with improved therapeutic potential. Nat Commun. 2013;4:1974. doi:10.1038/ncomms2974.
   PubMed Web of Science ®Google Scholar
• Kyo S, Inoue M. Complex regulatory mechanisms of telomerase activity in normal and cancer cells: how can we apply them for cancer therapy? Oncogene. 2002;21:688–697. doi:10.1038/sj.onc.1205163.
   PubMed Web of Science ®Google Scholar
• Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA. Highly recurrent TERT promoter mutations in human melanoma. Science. 2013;339:957–959. doi:10.1126/science.1229259.
   PubMed Web of Science ®Google Scholar
• Zhang W, Ge K, Zhao Q, Zhuang X, Deng Z, Liu L, Li J, Zhang Y, Dong Y, Zhang Y, et al. A novel oHSV-1 targeting telomerase reverse transcriptase-positive cancer cells via tumor-specific promoters regulating the expression of ICP4. Oncotarget. 2015;6:20345–20355. doi:10.18632/oncotarget.3884.
   PubMedGoogle Scholar
• Sundaresan P, Hunter WD, Martuza RL, Rabkin SD. Attenuated, replication-competent herpes simplex virus type 1 mutant G207: safety evaluation in mice. J Virol. 2000;74:3832–3841. doi:10.1128/JVI.74.8.3832-3841.2000.
   PubMed Web of Science ®Google Scholar
• Kowalsky SJ, Liu Z, Feist M, Berkey SE, Ma C, Ravindranathan R, Dai E, Roy EJ, Guo ZS, Bartlett DL, et al. Superagonist IL-15-armed oncolytic virus elicits potent antitumor immunity and therapy that are enhanced with PD-1 blockade. Mol Ther. 2018;26:2476–2486. doi:10.1016/j.ymthe.2018.07.013.
   PubMed Web of Science ®Google Scholar
• Zamarin D, Ricca JM, Sadekova S, Oseledchyk A, Yu Y, Blumenschein WM, Wong J, Gigoux M, Merghoub T, Wolchok JD, et al. PD-L1 in tumor microenvironment mediates resistance to oncolytic immunotherapy. J Clin Invest. 2018;128:1413–1428. doi:10.1172/JCI98047.
   PubMed Web of Science ®Google Scholar
• Zamarin D, Holmgaard RB, Subudhi SK, Park JS, Mansour M, Palese P, Merghoub T, Wolchok JD, Allison JP, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med. 2014;6:226ra232. doi:10.1126/scitranslmed.3008095.
   Web of Science ®Google Scholar
• Freedman JD, Duffy MR, Lei-Rossmann J, Muntzer A, Scott EM, Hagel J, Campo L, Bryant RJ, Verrill C, Lambert A, et al. An oncolytic virus expressing a T-cell engager simultaneously targets cancer and immunosuppressive stromal cells. Cancer Res. 2018;78:6852–6865. doi:10.1158/0008-5472.CAN-18-1750.
   PubMed Web of Science ®Google Scholar
• Li X, Wang P, Li H, Du X, Liu M, Huang Q, Wang Y, Wang S. The efficacy of oncolytic adenovirus is mediated by T-cell responses against virus and tumor in syrian hamster model. Clin Cancer Res. 2017;23:239–249. doi:10.1158/1078-0432.CCR-16-0477.
   PubMed Web of Science ®Google Scholar
• Zamarin D, Holmgaard RB, Ricca J, Plitt T, Palese P, Sharma P, Merghoub T, Wolchok JD, Allison JP. Intratumoral modulation of the inducible co-stimulator ICOS by recombinant oncolytic virus promotes systemic anti-tumour immunity. Nat Commun. 2017;8:14340. doi:10.1038/ncomms14340.
   PubMed Web of Science ®Google Scholar
• Marelli G, Howells A, Lemoine NR, Wang Y. Oncolytic viral therapy and the immune system: a double-edged sword against cancer. Front Immunol. 2018;9:866. doi:10.3389/fimmu.2018.00866.
   PubMed Web of Science ®Google Scholar
• Errington F, Steele L, Prestwich R, Harrington KJ, Pandha HS, Vidal L, de Bono J, Selby P, Coffey M, Vile R, et al. Reovirus activates human dendritic cells to promote innate antitumor immunity. J Immunol. 2008;180:6018–6026. doi:10.4049/jimmunol.180.9.6018.
   PubMed Web of Science ®Google Scholar
• Bhat R, Rommelaere J. Emerging role of natural killer cells in oncolytic virotherapy. Immunotargets Ther. 2015;4:65–77. doi:10.2147/ITT.S55549.
   PubMed Web of Science ®Google Scholar
• Alvarez-Breckenridge CA, Yu J, Price R, Wojton J, Pradarelli J, Mao H, Wei M, Wang Y, He S, Hardcastle J, et al. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat Med. 2012;18:1827–1834. doi:10.1038/nm.3013.
   PubMed Web of Science ®Google Scholar
• Altomonte J, Wu L, Chen L, Meseck M, Ebert O, Garcia-Sastre A, Fallon J, Woo SL. Exponential enhancement of oncolytic vesicular stomatitis virus potency by vector-mediated suppression of inflammatory responses in vivo. Mol Ther. 2008;16:146–153. doi:10.1038/sj.mt.6300343.
   PubMed Web of Science ®Google Scholar
• Miller CG, Fraser NW. Requirement of an integrated immune response for successful neuroattenuated HSV-1 therapy in an intracranial metastatic melanoma model. Mol Ther. 2003;7:741–747. doi:10.1016/S1525-0016(03)00120-5.
   PubMed Web of Science ®Google Scholar
• Bhat R, Dempe S, Dinsart C, Rommelaere J. Enhancement of NK cell antitumor responses using an oncolytic parvovirus. Int J Cancer. 2011;128:908–919. doi:10.1002/ijc.25415.
   PubMed Web of Science ®Google Scholar
• Moynihan KD, Opel CF, Szeto GL, Tzeng A, Zhu EF, Engreitz JM, Williams RT, Rakhra K, Zhang MH, Rothschilds AM, et al. Eradication of large established tumors in mice by combination immunotherapy that engages innate and adaptive immune responses. Nat Med. 2016;22:1402–1410. doi:10.1038/nm.4200.
   PubMed Web of Science ®Google Scholar
• Kim MK, Breitbach CJ, Moon A, Heo J, Lee YK, Cho M, Lee JW, Kim S-G, Kang DH, Bell JC, et al. Oncolytic and immunotherapeutic vaccinia induces antibody-mediated complement-dependent cancer cell lysis in humans. Sci Transl Med. 2013;5:185ra163. doi:10.1126/scitranslmed.3005361.
   Web of Science ®Google Scholar
• Sharma P, Allison JP. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell. 2015;161:205–214. doi:10.1016/j.cell.2015.03.030.
   PubMed Web of Science ®Google Scholar
• Yarchoan M, Johnson BA 3rd, Lutz ER, Laheru DA, Jaffee EM. Targeting neoantigens to augment antitumour immunity. Nat Rev Cancer. 2017;17:209–222. doi:10.1038/nrc.2016.154.
   PubMed Web of Science ®Google Scholar
• van der Burg SH, Arens R, Ossendorp F, van Hall T, Melief CJ. Vaccines for established cancer: overcoming the challenges posed by immune evasion. Nat Rev Cancer. 2016;16:219–233. doi:10.1038/nrc.2016.16.
   PubMed Web of Science ®Google Scholar