Efficacy and safety of a third-generation oncolytic herpes virus G47Δ in models of human esophageal carcinoma

Siegel, 2015, Cancer statistics, 2015, CA Cancer J. Clin., 65, 5, 10.3322/caac.21254 Lagergren, 2017, Oesophageal cancer, Lancet, 390, 2383, 10.1016/S0140-6736(17)31462-9 Wang, 2016, New strategies in esophageal carcinoma: translational insights from signaling pathways and immune checkpoints, Clin. Cancer Res., 22, 4283, 10.1158/1078-0432.CCR-16-0292 Abnet, 2018, Epidemiology of esophageal squamous cell carcinoma, Gastroenterology, 154, 360, 10.1053/j.gastro.2017.08.023 Ajani, 2015, Esophageal and esophagogastric junction cancers, version 1.2015, J. Natl. Compr. Canc. Netw., 13, 194, 10.6004/jnccn.2015.0028 Lordick, 2016, Oesophageal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up, Ann. Oncol., 27, v50, 10.1093/annonc/mdw329 Kitagawa, 2019, Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: part 2, Esophagus, 16, 25, 10.1007/s10388-018-0642-8 Yamasaki, 2017, Multicenter randomized phase II study of cisplatin and fluorouracil plus docetaxel (DCF) compared with cisplatin and fluorouracil plus Adriamycin (ACF) as preoperative chemotherapy for resectable esophageal squamous cell carcinoma (OGSG1003), Ann. Oncol., 28, 116, 10.1093/annonc/mdw439 Janjigian, 2018, CheckMate-032 study: efficacy and safety of nivolumab and nivolumab plus ipilimumab in patients with metastatic esophagogastric cancer, J. Clin. Oncol., 36, 2836, 10.1200/JCO.2017.76.6212 Kang, 2017, Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial, Lancet, 390, 2461, 10.1016/S0140-6736(17)31827-5 Kato, 2019, Nivolumab versus chemotherapy in patients with advanced oesophageal squamous cell carcinoma refractory or intolerant to previous chemotherapy (ATTRACTION-3): a multicentre, randomised, open-label, phase 3 trial, Lancet Oncol., 20, 1506, 10.1016/S1470-2045(19)30626-6 Schoenfeld, 2020, Acquired resistance to immune checkpoint inhibitors, Cancer Cell, 37, 443, 10.1016/j.ccell.2020.03.017 Fukuhara, 2016, Oncolytic virus therapy: a new era of cancer treatment at dawn, Cancer Sci., 107, 1373, 10.1111/cas.13027 Yokoda, 2017, Oncolytic virotherapy in upper gastrointestinal tract cancers, Oncolytic Virother., 7, 13, 10.2147/OV.S161397 Martinez-Quintanilla, 2019, Oncolytic viruses: overcoming translational challenges, J. Clin. Invest., 129, 1407, 10.1172/JCI122287 Andtbacka, 2015, Talimogene laherparepvec improves durable response rate in patients with advanced melanoma, J. Clin. Oncol., 33, 2780, 10.1200/JCO.2014.58.3377 Macedo, 2020, Clinical landscape of oncolytic virus research in 2020, J. Immunother. Cancer, 8, e001486, 10.1136/jitc-2020-001486 Terrero, 2020, Role of immunotherapy in advanced gastroesophageal cancer, Curr. Oncol. Rep., 22, 112, 10.1007/s11912-020-00975-y Fujiwara, 2019, Multidisciplinary oncolytic virotherapy for gastrointestinal cancer, Ann. Gastroenterol. Surg., 3, 396, 10.1002/ags3.12270 Zhang, 2008, Treatment of radioresistant stem-like esophageal cancer cells by an apoptotic gene-armed, telomerase-specific oncolytic adenovirus, Clin. Cancer Res., 14, 2813, 10.1158/1078-0432.CCR-07-1528 Ma, 2010, Combinatory cytotoxic effects produced by E1B-55kDa-deleted adenoviruses and chemotherapeutic agents are dependent on the agents in esophageal carcinoma, Cancer Gene Ther., 17, 803, 10.1038/cgt.2010.37 Ma, 2017, Histone deacetylase inhibitor trichostatin A enhances the antitumor effect of the oncolytic adenovirus H101 on esophageal squamous cell carcinoma in vitro and in vivo, Oncol. Lett., 13, 4868, 10.3892/ol.2017.6069 Nemunaitis, 2010, A phase I study of telomerase-specific replication competent oncolytic adenovirus (telomelysin) for various solid tumors, Mol. Ther., 18, 429, 10.1038/mt.2009.262 Khan, 2019, Phase II study of a telomerase-specific oncolytic adenovirus (OBP-301, Telomelysin) in combination with pembrolizumab in gastric and gastroesophageal junction adenocarcinoma, J. Clin. Oncol., 37, TPS4145, 10.1200/JCO.2019.37.15_suppl.TPS4145 Todo, 2001, Oncolytic herpes simplex virus vector with enhanced MHC class I presentation and tumor cell killing, Proc. Natl. Acad. Sci. U S A, 98, 6396, 10.1073/pnas.101136398 Mineta, 1995, Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas, Nat. Med., 1, 938, 10.1038/nm0995-938 Fukuhara, 2005, Oncolytic herpes simplex virus vector g47delta in combination with androgen ablation for the treatment of human prostate adenocarcinoma, Clin. Cancer Res., 11, 7886, 10.1158/1078-0432.CCR-05-1090 Todo, 2001, In situ expression of soluble B7-1 in the context of oncolytic herpes simplex virus induces potent antitumor immunity, Cancer Res., 61, 153 Fukuhara, 2005, Triple gene-deleted oncolytic herpes simplex virus vector double-armed with interleukin 18 and soluble B7-1 constructed by bacterial artificial chromosome-mediated system, Cancer Res., 65, 10663, 10.1158/0008-5472.CAN-05-2534 Ino, 2006, Triple combination of oncolytic herpes simplex virus-1 vectors armed with interleukin-12, interleukin-18, or soluble B7-1 results in enhanced antitumor efficacy, Clin. Cancer Res., 12, 643, 10.1158/1078-0432.CCR-05-1494 Tsuji, 2013, An armed oncolytic herpes simplex virus expressing thrombospondin-1 has an enhanced in vivo antitumor effect against human gastric cancer, Int. J. Cancer, 132, 485, 10.1002/ijc.27681 Saha, 2017, Macrophage polarization contributes to glioblastoma eradication by combination immunovirotherapy and immune checkpoint blockade, Cancer Cell, 32, 253, 10.1016/j.ccell.2017.07.006 Nakatake, 2018, Third-generation oncolytic herpes simplex virus inhibits the growth of liver tumors in mice, Cancer Sci., 109, 600, 10.1111/cas.13492 Yamada, 2020, Neoadjuvant use of oncolytic herpes virus G47Δ enhances the antitumor efficacy of radiofrequency ablation, Mol. Ther. Oncolytics, 18, 535, 10.1016/j.omto.2020.08.010 Sugawara, 2020, Efficacy of a third-generation oncolytic herpes virus G47Δ in advanced stage models of human gastric cancer, Mol. Ther. Oncolytics, 17, 205, 10.1016/j.omto.2020.03.022 Ishino, 2021, Oncolytic virus therapy with HSV-1 for hematological malignancies, Mol. Ther., 29, 762, 10.1016/j.ymthe.2020.09.041 Oku, 2021, Oncolytic herpes simplex virus type 1 (HSV-1) in combination with lenalidomide for plasma cell neoplasms, Br. J. Haematol., 192, 343, 10.1111/bjh.17173 Taguchi, 2019, Oncolytic virus therapy in Japan: progress in clinical trials and future perspectives, Jpn. J. Clin. Oncol., 49, 201, 10.1093/jjco/hyy170 Tung, 2018, Preclinical study of novel curcumin analogue SSC-5 using orthotopic tumor xenograft model for esophageal squamous cell carcinoma, Cancer Res. Treat., 50, 1362, 10.4143/crt.2017.353 Bibby, 2004, Orthotopic models of cancer for preclinical drug evaluation: advantages and disadvantages, Eur. J. Cancer, 40, 852, 10.1016/j.ejca.2003.11.021 Kuroda, 2014, Establishment of a non-invasive semi-quantitative bioluminescent imaging method for monitoring of an orthotopic esophageal cancer mouse model, PLoS One, 9, e114562, 10.1371/journal.pone.0114562 Kastrukoff, 2012, The effect of mouse strain on herpes simplex virus type 1 (HSV-1) infection of the central nervous system (CNS), Herpesviridae, 3, 4, 10.1186/2042-4280-3-4 Irie, 1989, Spread of herpes simplex virus type-1 (Miyama +GC strain) to the central nervous system after intraperitoneal inoculation: the role of the myenteric plexus of the gut, Arch. Virol., 105, 247, 10.1007/BF01311361 Ilson, 2018, Management of patients with adenocarcinoma or squamous cancer of the esophagus, Gastroenterology, 154, 437, 10.1053/j.gastro.2017.09.048 Zhang, 2016, Real-time GFP intravital imaging of the differences in cellular and angiogenic behavior of subcutaneous and orthotopic nude-mouse models of human PC-3 prostate cancer, J. Cell. Biochem., 117, 2546, 10.1002/jcb.25547 Yanagihara, 2006, A photon counting technique for quantitatively evaluating progression of peritoneal tumor dissemination, Cancer Res., 66, 7532, 10.1158/0008-5472.CAN-05-3259 Chahlavi, 1999, Effect of prior exposure to herpes simplex virus 1 on viral vector-mediated tumor therapy in immunocompetent mice, Gene Ther., 6, 1751, 10.1038/sj.gt.3301003 Connolly, 2021, The structural basis of herpesvirus entry, Nat. Rev. Microbiol., 19, 110, 10.1038/s41579-020-00448-w Todo, 2000, Viral shedding and biodistribution of G207, a multimutated, conditionally replicating herpes simplex virus type 1, after intracerebral inoculation in Aotus, Mol. Ther., 2, 588, 10.1006/mthe.2000.0200 Hunter, 1999, Attenuated, replication-competent herpes simplex virus type 1 mutant G207: safety evaluation of intracerebral injection in nonhuman primates, J. Virol., 73, 6319, 10.1128/JVI.73.8.6319-6326.1999 Sundaresan, 2000, Attenuated, replication-competent herpes simplex virus type 1 mutant G207: safety evaluation in mice, J. Virol., 74, 3832, 10.1128/JVI.74.8.3832-3841.2000 Tai, 2013, Preventing postoperative metastatic disease by inhibiting surgery-induced dysfunction in natural killer cells, Cancer Res., 73, 97, 10.1158/0008-5472.CAN-12-1993 Bourgeois-Daigneault, 2018, Neoadjuvant oncolytic virotherapy before surgery sensitizes triple-negative breast cancer to immune checkpoint therapy, Sci. Transl. Med., 10, eaao1641, 10.1126/scitranslmed.aao1641 Ahmed, 2020, A new oncolytic Vaccinia virus augments antitumor immune responses to prevent tumor recurrence and metastasis after surgery, J. Immunother. Cancer, 8, e000415, 10.1136/jitc-2019-000415 Sugawara, 2021, Oncolytic herpes virus G47Δ works synergistically with CTLA-4 inhibition through dynamic intratumoral immune modulation, Mol. Ther. Oncolytics, 22, 129, 10.1016/j.omto.2021.05.004 Todo, 1999, Systemic antitumor immunity in experimental brain tumor therapy using a multimutated, replication-competent herpes simplex virus, Hum. Gene Ther., 10, 2741, 10.1089/10430349950016483 Toyoshima, 2009, Generation of a syngeneic mouse model to study the intraperitoneal dissemination of ovarian cancer with in vivo luciferase imaging, Luminescence, 24, 324, 10.1002/bio.1112