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Review

Recent advances of oncolytic virus in cancer therapy

, , &
Pages 2389-2402 | Received 12 Oct 2019, Accepted 23 Jan 2020, Published online: 20 Feb 2020

References

  • Bell J, McFadden G. Viruses for tumor therapy. Cell Host Microbe. 2014;15:260–65. doi:10.1016/j.chom.2014.01.002.
  • Kelly E, Russell SJ. History of oncolytic viruses: genesis to genetic engineering. Mol Ther. 2007;15:651–59. doi:10.1038/sj.mt.6300108.
  • Kaufman HL, Ruby CE, Hughes T, Slingluff CL Jr. Current status of granulocyte-macrophage colony-stimulating factor in the immunotherapy of melanoma. J Immunother Cancer. 2014;2:11. doi:10.1186/2051-1426-2-11.
  • Farassati F, Yang AD, Lee PW. Oncogenes in Ras signalling pathway dictate host-cell permissiveness to herpes simplex virus 1. Nat Cell Biol. 2001;3:745–50. doi:10.1038/35087061.
  • Smith KD, Mezhir JJ, Bickenbach K, Veerapong J, Charron J, Posner MC, Roizman B, Weichselbaum RR. Activated MEK suppresses activation of PKR and enables efficient replication and in vivo oncolysis by Deltagamma(1)34.5 mutants of herpes simplex virus 1. J Virol. 2006;80:1110–20. doi:10.1128/JVI.80.3.1110-1120.2006.
  • Kohlhapp FJ, Kaufman HL. Molecular pathways: mechanism of action for talimogene laherparepvec, a new oncolytic virus immunotherapy. Clin Cancer Res. 2016;22:1048–54. doi:10.1158/1078-0432.CCR-15-2667.
  • Tomazin R, van Schoot NE, Goldsmith K, Jugovic P, Sempe P, Fruh K, Johnson DC. Herpes simplex virus type 2 ICP47 inhibits human TAP but not mouse TAP. J Virol. 1998;72:2560–63. doi:10.1128/JVI.72.3.2560-2563.1998.
  • 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;33:2780–88. doi:10.1200/JCO.2014.58.3377.
  • Everett AS, Pavlidakey PG, Contreras CM, De Los Santos JF, Kim JY, McKee SB, Kaufman HL, Conry RM. Chronic granulomatous dermatitis induced by talimogene laherparepvec therapy of melanoma metastases. J Cutan Pathol. 2018;45:48–53. doi:10.1111/cup.13048.
  • Esaki S, Goshima F, Kimura H, Murakami S, Nishiyama Y. Enhanced antitumoral activity of oncolytic herpes simplex virus with gemcitabine using colorectal tumor models. Int J Cancer. 2013;132:1592–601. doi:10.1002/ijc.27823.
  • Kim RD, Sarker D, Meyer T, Yau T, Macarulla T, Park JW, Choo SP, Hollebecque A, Sung MW, Lim HY, et al. First-in-human phase i study of fisogatinib (BLU-554) validates aberrant FGF19 Signaling as a driver event in hepatocellular carcinoma. Cancer Discovery. 2019;2019(9):1–12.
  • Shimoyama S, Goshima F, Teshigahara O, Kasuya H, Kodera Y, Nakao A, Nishiyama Y. Enhanced efficacy of herpes simplex virus mutant HF10 combined with paclitaxel in peritoneal cancer dissemination models. Hepatogastroenterology. 2007;54:1038–42.
  • Watanabe D, Goshima F, Mori I, Tamada Y, Matsumoto Y, Nishiyama Y. Oncolytic virotherapy for malignant melanoma with herpes simplex virus type 1 mutant HF10. J Dermatol Sci. 2008;50:185–96. doi:10.1016/j.jdermsci.2007.12.001.
  • Andtbacka RH, Ross M, Puzanov I, Milhem M, Collichio F, Delman KA, Amatruda T, Zager JS, Cranmer L, Hsueh E, et al. Patterns of clinical response with talimogene laherparepvec (T-VEC) in patients with melanoma treated in the OPTiM phase III clinical trial. Ann Surg Oncol. 2016;23:4169–77. doi:10.1245/s10434-016-5286-0.
  • Fujimoto Y, Mizuno T, Sugiura S, Goshima F, Kohno S, Nakashima T, Nishiyama Y. Intratumoral injection of herpes simplex virus HF10 in recurrent head and neck squamous cell carcinoma. Acta Otolaryngol. 2006;126:1115–17. doi:10.1080/00016480600702100.
  • Nakao A, Kasuya H, Sahin TT, Nomura N, Kanzaki A, Misawa M, Shirota T, Yamada S, Fujii T, Sugimoto H, et al. A phase I dose-escalation clinical trial of intraoperative direct intratumoral injection of HF10 oncolytic virus in non-resectable patients with advanced pancreatic cancer. Cancer Gene Ther. 2011;18:167–75. doi:10.1038/cgt.2010.65.
  • Ushijima Y, Luo C, Goshima F, Yamauchi Y, Kimura H, Nishiyama Y. Determination and analysis of the DNA sequence of highly attenuated herpes simplex virus type 1 mutant HF10, a potential oncolytic virus. Microbes Infect. 2007;9:142–49. doi:10.1016/j.micinf.2006.10.019.
  • 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.
  • Avitabile E, Lombardi G, Gianni T, Capri M, Campadelli-Fiume G. Coexpression of UL20p and gK inhibits cell-cell fusion mediated by herpes simplex virus glycoproteins gD, gH-gL, and wild-type gB or an endocytosis-defective gB mutant and downmodulates their cell surface expression. J Virol. 2004;78:8015–25. doi:10.1128/JVI.78.15.8015-8025.2004.
  • Avitabile E, Lombardi G, Campadelli-Fiume G. Herpes simplex virus glycoprotein K, but not its syncytial allele, inhibits cell-cell fusion mediated by the four fusogenic glycoproteins, gD, gB, gH, and gL. J Virol. 2003;77:6836–44. doi:10.1128/JVI.77.12.6836-6844.2003.
  • Perng GC, Dunkel EC, Geary PA, Slanina SM, Ghiasi H, Kaiwar R, Nesburn AB, Wechsler SL. The latency-associated transcript gene of herpes simplex virus type 1 (HSV-1) is required for efficient in vivo spontaneous reactivation of HSV-1 from latency. J Virol. 1994;68:8045–55. doi:10.1128/JVI.68.12.8045-8055.1994.
  • Streby KA, Geller JI, Currier MA, Warren PS, Racadio JM, Towbin AJ, Vaughan MR, Triplet M, Ott-Napier K, Dishman DJ, et al. Intratumoral injection of HSV1716, an oncolytic herpes virus, is safe and shows evidence of immune response and viral replication in young cancer patients. Clin Cancer Res. 2017;23:3566–74. doi:10.1158/1078-0432.CCR-16-2900.
  • Kim R, Sarker D, Macarulla T, Yau T, Choo SP, Meyer T, et al. 365OPhase 1 safety and clinical activity of BLU-554 in advanced hepatocellular carcinoma (HCC). Ann Oncol. 2017;28. doi:10.1093/annonc/mdx075.
  • Aghi MK, Chiocca EA. Phase ib trial of oncolytic herpes virus G207 shows safety of multiple injections and documents viral replication. Mol Ther. 2009;17:8–9. doi:10.1038/mt.2008.275.
  • Markert JM, Medlock MD, Rabkin SD, Gillespie GY, Todo T, Hunter WD, Palmer CA, Feigenbaum F, Tornatore C, Tufaro F, et al. Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther. 2000;7:867–74. doi:10.1038/sj.gt.3301205.
  • Markert JM, Liechty PG, Wang W, Gaston S, Braz E, Karrasch M, Nabors LB, Markiewicz M, Lakeman AD, Palmer CA, et al. Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol Ther. 2009;17:199–207. doi:10.1038/mt.2008.228.
  • Patel DM, Foreman PM, Nabors LB, Riley KO, Gillespie GY, Markert JM. Design of a phase I clinical trial to evaluate M032, a genetically engineered HSV-1 expressing IL-12, in patients with recurrent/progressive glioblastoma multiforme, anaplastic astrocytoma, or gliosarcoma. Hum Gene Ther Clin Dev. 2016;27:69–78. doi:10.1089/humc.2016.031.
  • Zeng W, Hu P, Wu J, Wang J, Li J, Lei L, LIU R. The oncolytic herpes simplex virus vector G47 effectively targets breast cancer stem cells. Oncol Rep. 2013;29:1108–14. doi:10.3892/or.2012.2211.
  • Fukuhara H, Martuza RL, Rabkin SD, Ito Y, Todo T. Oncolytic herpes simplex virus vector g47delta in combination with androgen ablation for the treatment of human prostate adenocarcinoma. Clin Cancer Res. 2005;11:7886–90. doi:10.1158/1078-0432.CCR-05-1090.
  • Cerullo V, Koski A, Vaha-Koskela M, Hemminki A. Chapter eight–Oncolytic adenoviruses for cancer immunotherapy: data from mice, hamsters, and humans. Adv Cancer Res. 2012;115:265–318.
  • Liang M. Clinical development of oncolytic viruses in China. Curr Pharm Biotechnol. 2012;13:1852–57. doi:10.2174/138920112800958760.
  • Raty JK, Pikkarainen JT, Wirth T, Yla-Herttuala S. Gene therapy: the first approved gene-based medicines, molecular mechanisms and clinical indications. Curr Mol Pharmacol. 2008;1:13–23. doi:10.2174/1874467210801010013.
  • Xia ZJ, Chang JH, Zhang L, Jiang WQ, Guan ZZ, Liu JW, Zhang Y, Hu XH, Wu GH, Wang HQ. Phase III randomized clinical trial of intratumoral injection of E1B gene-deleted adenovirus (H101) combined with cisplatin-based chemotherapy in treating squamous cell cancer of head and neck or esophagus. Ai Zheng. 2004;23:1666–70.
  • Liang M. Oncorine, the world first oncolytic virus medicine and its update in China. Curr Cancer Drug Targets. 2018;18:171–76. doi:10.2174/1568009618666171129221503.
  • Rudin CM, Cohen EE, Papadimitrakopoulou VA, Silverman S Jr., Recant W, El-Naggar AK, Stenson K, Lippman SM, Hong WK, Vokes EE, et al. An attenuated adenovirus, ONYX-015, as mouthwash therapy for premalignant oral dysplasia. J Clin Oncol. 2003;21:4546–52. doi:10.1200/JCO.2003.03.544.
  • Hecht JR, Bedford R, Abbruzzese JL, Lahoti S, Reid TR, Soetikno RM, Kirn DH, Freeman SM. A phase I/II trial of intratumoral endoscopic ultrasound injection of ONYX-015 with intravenous gemcitabine in unresectable pancreatic carcinoma. Clin Cancer Res. 2003;9:555–61.
  • Fueyo J, Alemany R, Gomez-Manzano C, Fuller GN, Khan A, Conrad CA, Liu T-J, Jiang H, Lemoine MG, Suzuki K, et al. Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. J Natl Cancer Inst. 2003;95:652–60. doi:10.1093/jnci/95.9.652.
  • Lang FF, Conrad C, Gomez-Manzano C, Yung WKA, Sawaya R, Weinberg JS, Prabhu SS, Rao G, Fuller GN, Aldape KD, et al. Phase I study of DNX-2401 (Delta-24-RGD) oncolytic adenovirus: replication and immunotherapeutic effects in recurrent malignant glioma. J Clin Oncol. 2018;36:1419–27. doi:10.1200/JCO.2017.75.8219.
  • Eissa IR, Bustos-Villalobos I, Ichinose T, Matsumura S, Naoe Y, Miyajima N, Morimoto D, Mukoyama N, Zhiwen W, Tanaka M, et al. The current status and future prospects of oncolytic viruses in clinical trials against melanoma, glioma, pancreatic, and breast cancers. Cancers (Basel). 2018;10:356–78. doi:10.3390/cancers10100356.
  • Ranki T, Pesonen S, Hemminki A, Partanen K, Kairemo K, Alanko T, Lundin J, Linder N, Turkki R, Ristimäki A, et al. Phase I study with ONCOS-102 for the treatment of solid tumors - an evaluation of clinical response and exploratory analyses of immune markers. J Immunother Cancer. 2016;4:17. doi:10.1186/s40425-016-0121-5.
  • Vera B, Martinez-Velez N, Xipell E, Acanda de la Rocha A, Patino-Garcia A, Saez-Castresana J, Gonzalez-Huarriz M, Cascallo M, Alemany R, Alonso MM, et al. Characterization of the antiglioma effect of the oncolytic adenovirus VCN-01. PLoS One. 2016;11:e0147211. doi:10.1371/journal.pone.0147211.
  • Pascual-Pasto G, Bazan-Peregrino M, Olaciregui NG, Restrepo-Perdomo CA, Mato-Berciano A, Ottaviani D, Weber K, Correa G, Paco S, Vila-Ubach M, et al. Therapeutic targeting of the RB1 pathway in retinoblastoma with the oncolytic adenovirus VCN-01. Sci Transl Med. 2019;11:eaat9321. doi:10.1126/scitranslmed.aat9321.
  • Nokisalmi P, Pesonen S, Escutenaire S, Sarkioja M, Raki M, Cerullo V, Laasonen L, Alemany R, Rojas J, Cascallo M, et al. Oncolytic adenovirus ICOVIR-7 in patients with advanced and refractory solid tumors. Clin Cancer Res. 2010;16:3035–43. doi:10.1158/1078-0432.CCR-09-3167.
  • Garcia M, Moreno R, Gil-Martin M, Cascallo M, de Olza MO, Cuadra C, Piulats JM, Navarro V, Domenech M, Alemany R, et al. A phase 1 trial of oncolytic adenovirus ICOVIR-5 administered intravenously to cutaneous and uveal melanoma patients. Hum Gene Ther. 2019;30:352–64. doi:10.1089/hum.2018.107.
  • ONCORINE. Recombinant human adenovirus type 5 Injection. [accessed 2019 September]. http://www.sunwaybio.com.cn/en/product.html
  • Khuri FR, Nemunaitis J, Ganly I, Arseneau J, Tannock IF, Romel L, Gore M, Ironside J, MacDougall RH, Heise C, et al. a controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer. Nat Med. 2000;6:879–85. doi:10.1038/78638.
  • Parato KA, Senger D, Forsyth PA, Bell JC. Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer. 2005;5:965–76. doi:10.1038/nrc1750.
  • Smith E, Breznik J, Lichty BD. Strategies to enhance viral penetration of solid tumors. Hum Gene Ther. 2011;22:1053–60. doi:10.1089/hum.2010.227.
  • Strauss R, Lieber A. Anatomical and physical barriers to tumor targeting with oncolytic adenoviruses in vivo. Curr Opin Mol Ther. 2009;11:513–22.
  • Jacobetz MA, Chan DS, Neesse A, Bapiro TE, Cook N, Frese KK, Feig C, Nakagawa T, Caldwell ME, Zecchini HI, et al. Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer. Gut. 2013;62:112–20. doi:10.1136/gutjnl-2012-302529.
  • Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell. 2012;21:418–29. doi:10.1016/j.ccr.2012.01.007.
  • Thompson CB, Shepard HM, O’Connor PM, Kadhim S, Jiang P, Osgood RJ, Bookbinder LH, Li X, Sugarman BJ, Connor RJ, et al. Enzymatic depletion of tumor hyaluronan induces antitumor responses in preclinical animal models. Mol Cancer Ther. 2010;9:3052–64. doi:10.1158/1535-7163.MCT-10-0470.
  • Eriksson E, Milenova I, Wenthe J, Stahle M, Leja-Jarblad J, Ullenhag G, Dimberg A, Moreno R, Alemany R, Loskog A, et al. Shaping the tumor stroma and sparking immune activation by CD40 and 4-1BB signaling induced by an armed oncolytic virus. Clin Cancer Res. 2017;23:5846–57. doi:10.1158/1078-0432.CCR-17-0285.
  • Dong W, van Ginkel JW, Au KY, Alemany R, Meulenberg JJ, van Beusechem VW. ORCA-010, a novel potency-enhanced oncolytic adenovirus, exerts strong antitumor activity in preclinical models. Hum Gene Ther. 2014;25:897–904. doi:10.1089/hum.2013.229.
  • Gros A, Martinez-Quintanilla J, Puig C, Guedan S, Mollevi DG, Alemany R, Cascallo M. Bioselection of a gain of function mutation that enhances adenovirus 5 release and improves its antitumoral potency. Cancer Res. 2008;68:8928–37. doi:10.1158/0008-5472.CAN-08-1145.
  • Ramesh N, Ge Y, Ennist DL, Zhu M, Mina M, Ganesh S, Reddy PS, Yu DC. CG0070, a conditionally replicating granulocyte macrophage colony-stimulating factor–armed oncolytic adenovirus for the treatment of bladder cancer. Clin Cancer Res. 2006;12:305–13. doi:10.1158/1078-0432.CCR-05-1059.
  • Packiam VT, Lamm DL, Barocas DA, Trainer A, Fand B, Davis RL 3rd, Clark W, Kroeger M, Dumbadze I, Chamie K, et al. An open label, single-arm, phase II multicenter study of the safety and efficacy of CG0070 oncolytic vector regimen in patients with BCG-unresponsive non-muscle-invasive bladder cancer: interim results. Urol Oncol. 2018;36:440–47. doi:10.1016/j.urolonc.2017.07.005.
  • Cheng T, Song Y, Zhang Y, Zhang C, Yin J, Chi Y, Zhou D. A novel oncolytic adenovirus based on simian adenovirus serotype 24. Oncotarget. 2017;8:26871–85. doi:10.18632/oncotarget.15845.
  • Xing M, Wang X, Chi Y, Zhou D. Gene therapy for colorectal cancer using adenovirus-mediated full-length antibody, cetuximab. Oncotarget. 2016;7:28262–72. doi:10.18632/oncotarget.v7i19.
  • Abbink P, Lemckert AA, Ewald BA, Lynch DM, Denholtz M, Smits S, Holterman L, Damen I, Vogels R, Thorner AR, et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol. 2007;81:4654–63. doi:10.1128/JVI.02696-06.
  • Waddington SN, McVey JH, Bhella D, Parker AL, Barker K, Atoda H, Pink R, Buckley SMK, Greig JA, Denby L, et al. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell. 2008;132:397–409. doi:10.1016/j.cell.2008.01.016.
  • Uchino J, Curiel DT, Ugai H, Glorioso JC. Species D human adenovirus type 9 exhibits better virus-spread ability for antitumor efficacy among alternative serotypes. PLoS One. 2014;9:e87342. doi:10.1371/journal.pone.0087342.
  • Kaufmann JK, Nettelbeck DM. Virus chimeras for gene therapy, vaccination, and oncolysis: adenoviruses and beyond. Trends Mol Med. 2012;18:365–76. doi:10.1016/j.molmed.2012.04.008.
  • Schoggins JW, Nociari M, Philpott N, Falck-Pedersen E. Influence of fiber detargeting on adenovirus-mediated innate and adaptive immune activation. J Virol. 2005;79:11627–37. doi:10.1128/JVI.79.18.11627-11637.2005.
  • Parker AL, Waddington SN, Buckley SM, Custers J, Havenga MJ, van Rooijen N, Goudsmit J, McVey JH, Nicklin SA, Baker AH, et al. Effect of neutralizing sera on factor x-mediated adenovirus serotype 5 gene transfer. J Virol. 2009;83:479–83. doi:10.1128/JVI.01878-08.
  • Rogee S, Grellier E, Bernard C, Jouy N, Loyens A, Beauvillain JC, Fender P, Corjon S, Hong SS, Boulanger P, et al. Influence of chimeric human-bovine fibers on adenoviral uptake by liver cells and the antiviral immune response. Gene Ther. 2010;17:880–91. doi:10.1038/gt.2010.37.
  • Coughlan L, Alba R, Parker AL, Bradshaw AC, McNeish IA, Nicklin SA, Baker AH. Tropism-modification strategies for targeted gene delivery using adenoviral vectors. Viruses. 2010;2:2290–355. doi:10.3390/v2102290.
  • Majhen D, Calderon H, Chandra N, Fajardo CA, Rajan A, Alemany R, Custers J. Adenovirus-based vaccines for fighting infectious diseases and cancer: progress in the field. Hum Gene Ther. 2014;25:301–17. doi:10.1089/hum.2013.235.
  • Magnusson MK, Hong SS, Boulanger P, Lindholm L. Genetic retargeting of adenovirus: novel strategy employing “deknobbing” of the fiber. J Virol. 2001;75:7280–89. doi:10.1128/JVI.75.16.7280-7289.2001.
  • O’Riordan CR, Lachapelle A, Delgado C, Parkes V, Wadsworth SC, Smith AE, Francis GE. PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody in vitro and in vivo. Hum Gene Ther. 1999;10:1349–58. doi:10.1089/10430349950018021.
  • Lee YS, Kim SW. Bioreducible polymers for therapeutic gene delivery. J Control Release. 2014;190:424–39. doi:10.1016/j.jconrel.2014.04.012.
  • Douglas JT, Miller CR, Kim M, Dmitriev I, Mikheeva G, Krasnykh V, Curiel DT. A system for the propagation of adenoviral vectors with genetically modified receptor specificities. Nat Biotechnol. 1999;17:470–75. doi:10.1038/8647.
  • Rancourt C, Robertson MW 3rd, Wang M, Goldman CK, Kelly JF, Alvarez RD, Siegal GP, Curiel DT. Endothelial cell vehicles for delivery of cytotoxic genes as a gene therapy approach for carcinoma of the ovary. Clin Cancer Res. 1998;4:265–70.
  • Dmitriev I, Kashentseva E, Rogers BE, Krasnykh V, Curiel DT. Ectodomain of coxsackievirus and adenovirus receptor genetically fused to epidermal growth factor mediates adenovirus targeting to epidermal growth factor receptor-positive cells. J Virol. 2000;74:6875–84. doi:10.1128/JVI.74.15.6875-6884.2000.
  • van Beusechem VW, Mastenbroek DC, van den Doel PB, Lamfers ML, Grill J, Wurdinger T, Haisma HJ, Pinedo HM, Gerritsen WR. Conditionally replicative adenovirus expressing a targeting adapter molecule exhibits enhanced oncolytic potency on CAR-deficient tumors. Gene Ther. 2003;10:1982–91. doi:10.1038/sj.gt.3302103.
  • Bhattacharjee S, Yadava PK. Measles virus: background and oncolytic virotherapy. Biochem Biophys Rep. 2018;13:58–62. doi:10.1016/j.bbrep.2017.12.004.
  • Enders JF, Peebles TC. Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proc Soc Exp Biol Med. 1954;86:277–86. doi:10.3181/00379727-86-21073.
  • Enders JF, Katz SL, Milovanovic MV, Holloway A. Studies on an attenuated measles-virus vaccine. I. Development and preparations of the vaccine: technics for assay of effects of vaccination. N Engl J Med. 1960;263:153–59. doi:10.1056/NEJM196007282630401.
  • Hashiguchi T, Kajikawa M, Maita N, Takeda M, Kuroki K, Sasaki K, Kohda D, Yanagi Y, Maenaka K. Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc Natl Acad Sci USA. 2007;104:19535–40. doi:10.1073/pnas.0707830104.
  • Russell SJ, Federspiel MJ, Peng KW, Tong C, Dingli D, Morice WG, Lowe V, O’Connor MK, Kyle RA, Leung N, et al. Remission of disseminated cancer after systemic oncolytic virotherapy. Mayo Clin Proc. 2014;89:926–33. doi:10.1016/j.mayocp.2014.04.003.
  • Mader EK, Maeyama Y, Lin Y, Butler GW, Russell HM, Galanis E, Russell SJ, Dietz AB, Peng K-W. Mesenchymal stem cell carriers protect oncolytic measles viruses from antibody neutralization in an orthotopic ovarian cancer therapy model. Clin Cancer Res. 2009;15:7246–55. doi:10.1158/1078-0432.CCR-09-1292.
  • Miest TS, Yaiw KC, Frenzke M, Lampe J, Hudacek AW, Springfeld C, von Messling V, Ungerechts G, Cattaneo R. Envelope-chimeric entry-targeted measles virus escapes neutralization and achieves oncolysis. Mol Ther. 2011;19:1813–20. doi:10.1038/mt.2011.92.
  • Thirukkumaran C, Shi ZQ, Thirukkumaran P, Luider J, Kopciuk K, Spurrell J, Elzinga K, Morris D. PUMA and NF-kB are cell signaling predictors of reovirus oncolysis of breast cancer. PLoS One. 2017;12:e0168233. doi:10.1371/journal.pone.0168233.
  • Samson A, Bentham MJ, Scott K, Nuovo G, Bloy A, Appleton E, Adair RA, Dave R, Peckham-Cooper A, Toogood G, et al. Oncolytic reovirus as a combined antiviral and anti-tumour agent for the treatment of liver cancer. Gut. 2018;67:562–73. doi:10.1136/gutjnl-2016-312009.
  • Morris DG, Feng X, DiFrancesco LM, Fonseca K, Forsyth PA, Paterson AH, Coffey MC, Thompson B. REO-001: A phase I trial of percutaneous intralesional administration of reovirus type 3 dearing (Reolysin(R)) in patients with advanced solid tumors. Invest New Drugs. 2013;31:696–706. doi:10.1007/s10637-012-9865-z.
  • Lolkema MP, Arkenau HT, Harrington K, Roxburgh P, Morrison R, Roulstone V, Twigger K, Coffey M, Mettinger K, Gill G, et al. A phase I study of the combination of intravenous reovirus type 3 Dearing and gemcitabine in patients with advanced cancer. Clin Cancer Res. 2011;17:581–88. doi:10.1158/1078-0432.CCR-10-2159.
  • Forsyth P, Roldan G, George D, Wallace C, Palmer CA, Morris D, Cairncross G, Matthews MV, Markert J, Gillespie Y, et al. A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther. 2008;16:627–32. doi:10.1038/sj.mt.6300403.
  • Harrington KJ, Karapanagiotou EM, Roulstone V, Twigger KR, White CL, Vidal L, Beirne D, Prestwich R, Newbold K, Ahmed M, et al. Two-stage phase I dose-escalation study of intratumoral reovirus type 3 dearing and palliative radiotherapy in patients with advanced cancers. Clin Cancer Res. 2010;16:3067–77.
  • Vidal L, Pandha HS, Yap TA, White CL, Twigger K, Vile RG, Melcher A, Coffey M, Harrington KJ, DeBono JS, et al. A phase I study of intravenous oncolytic reovirus type 3 Dearing in patients with advanced cancer. Clin Cancer Res. 2008;14:7127–37. doi:10.1158/1078-0432.CCR-08-0524.
  • Chakrabarty R, Tran H, Selvaggi G, Hagerman A, Thompson B, Coffey M. The oncolytic virus, pelareorep, as a novel anticancer agent: a review. Invest New Drugs. 2015;33:761–74. doi:10.1007/s10637-015-0216-8.
  • ORYX announces positive phase I/IIa data for oncolytic virus parvoryx demonstrating safety, anti-tumor effects, partial responses and prolonged overall survival in metastatic, inoperable pancreatic cancer. [accessed 2019 September]. https://www.biospace.com/article/oryx-announces-positive-phase-i-iia-data-for-oncolytic-virus-parvoryx-demonstrating-safety-anti-tumor-effects-partial-responses-and-prolonged-overall-survival-in-metastatic-inoperable-pancreatic-cancer/
  • Adams WR, Prince AF. Cellular changes associated with infection of the Ehrlich ascites tumor with Newcastle disease virus. Ann N Y Acad Sci. 1959;81:89–100. doi:10.1111/j.1749-6632.1959.tb49298.x.
  • Mason EJ, Kaufman N. The toxic properties of massive inoculums of Newcastle disease virus and influenza virus (PR8) for cell strains derived from normal and neoplastic tissue. Am J Pathol. 1960;37:231–43.
  • Eaton MD, Levinthal JD, Scala AR. Contribution of antiviral immunity to oncolysis by Newcastle disease virus in a murine lymphoma. J Natl Cancer Inst. 1967;39:1089–97.
  • Eaton SA MD. Further observations on the inhibitory effect of myxoviruses on a transplantable murine leukemia. Proc Soc Exp Biol Med. 1969;132(1):20–26. doi:10.3181/00379727-132-34138.
  • Vigil A, Park MS, Martinez O, Chua MA, Xiao S, Cros JF, Martínez-Sobrido L, Woo SLC, García-Sastre A. Use of reverse genetics to enhance the oncolytic properties of Newcastle disease virus. Cancer Res. 2007;67:8285–92. doi:10.1158/0008-5472.CAN-07-1025.
  • Zamarin D, Martinez-Sobrido L, Kelly K, Mansour M, Sheng G, Vigil A, García-Sastre A, Palese P, Fong Y. Enhancement of oncolytic properties of recombinant newcastle disease virus through antagonism of cellular innate immune responses. Mol Ther. 2009;17:697–706. doi:10.1038/mt.2008.286.
  • Ahlert T, Schirrmacher V. Isolation of a human melanoma adapted Newcastle disease virus mutant with highly selective replication patterns. Cancer Res. 1990;50:5962–68.
  • Li P, Chen CH, Li S, Givi B, Yu Z, Zamarin D, Palese P, Fong Y, Wong RJ. Therapeutic effects of a fusogenic newcastle disease virus in treating head and neck cancer. Head Neck. 2011;33:1394–99. doi:10.1002/hed.v33.10.
  • Silberhumer GR, Brader P, Wong J, Serganova IS, Gonen M, Gonzalez SJ, Blasberg R, Zamarin D, Fong Y. Genetically engineered oncolytic Newcastle disease virus effectively induces sustained remission of malignant pleural mesothelioma. Mol Cancer Ther. 2010;9:2761–69. doi:10.1158/1535-7163.MCT-10-0090.
  • Song KY, Wong J, Gonzalez L, Sheng G, Zamarin D, Fong Y. Antitumor efficacy of viral therapy using genetically engineered Newcastle disease virus [NDV(F3aa)-GFP] for peritoneally disseminated gastric cancer. J Mol Med (Berl). 2010;88:589–96. doi:10.1007/s00109-010-0605-6.
  • Fabian Z, Torocsik B, Kiss K, Csatary LK, Bodey B, Tigyi J, Csatary C, Szeberényi J. Induction of apoptosis by a Newcastle disease virus vaccine (MTH-68/H) in PC12 rat phaeochromocytoma cells. Anticancer Res. 2001;21:125–35.
  • Szeberenyi J, Fabian Z, Torocsik B, Kiss K, Csatary LK. Newcastle disease virus-induced apoptosis in PC12 pheochromocytoma cells. Am J Ther. 2003;10:282–88. doi:10.1097/00045391-200307000-00008.
  • Lorence RMRP, Rood PA. Newcastle disease virus as an antineoplastic agent: induction of tumor necrosisfactor-a and augmentation of its cytotoxicity. J Natl Cancer Inst. 1988;80(16):1305–12. doi:10.1093/jnci/80.16.1305.
  • Zorn U, Dallmann I, Grosse J, Kirchner H, Poliwoda H, Atzpodien J. Induction of cytokines and cytotoxicity against tumor cells by Newcastle disease virus. Cancer Biother. 1994;9:225–35. doi:10.1089/cbr.1994.9.225.
  • Termeer CC, Schirrmacher V, Brocker EB, Becker JC. Newcastle disease virus infection induces B7-1/B7-2-independent T-cell costimulatory activity in human melanoma cells. Cancer Gene Ther. 2000;7:316–23. doi:10.1038/sj.cgt.7700109.
  • Lorence RM, Katubig BB, Reichard KW, Reyes HM, Phuangsab A, Sassetti MD, Walter RJ, Peeples ME. Complete regression of human fibrosarcoma xenografts after local Newcastle disease virus therapy. Cancer Res. 1994;54:6017–21.
  • Zamarin D, Vigil A, Kelly K, Garcia-Sastre A, Fong Y. Genetically engineered Newcastle disease virus for malignant melanoma therapy. Gene Ther. 2009;16:796–804. doi:10.1038/gt.2009.14.
  • Altomonte J, Marozin S, Schmid RM, Ebert O. Engineered newcastle disease virus as an improved oncolytic agent against hepatocellular carcinoma. Mol Ther. 2010;18:275–84. doi:10.1038/mt.2009.231.
  • Reichard KW, Lorence RM, Katubig BB, Peeples ME, Reyes HM. Retinoic acid enhances killing of neuroblastoma cells by Newcastle disease virus. J Pediatr Surg. 1993;28:1221–25. discussion 1225–1226. doi:10.1016/S0022-3468(05)80302-1.
  • Lorence RM, Reichard KW, Katubig BB, Reyes HM, Phuangsab A, Mitchell BR, Cascino CJ, Walter RJ, Peeples ME. Complete regression of human neuroblastoma xenografts in athymic mice after local Newcastle disease virus therapy. J Natl Cancer Inst. 1994;86:1228–33. doi:10.1093/jnci/86.16.1228.
  • Tzadok-David Y, Metzkin-Eizenberg M, Zakay-Rones Z. The effect of a mesogenic and a lentogenic Newcastle disease virus strain on Burkitt lymphoma Daudi cells. J Cancer Res Clin Oncol. 1995;121:169–74. doi:10.1007/BF01198099.
  • Bar-Eli N, Giloh H, Schlesinger M, Zakay-Rones Z. Preferential cytotoxic effect of Newcastle disease virus on lymphoma cells. J Cancer Res Clin Oncol. 1996;122:409–15. doi:10.1007/BF01212880.
  • Schirrmacher V, Griesbach A, Ahlert T. Antitumor effects of Newcastle disease virus in vivo: local versus systemic effects. Int J Oncol. 2001;18:945–52. doi:10.3892/ijo.18.5.945.
  • Washburn B, Schirrmacher V. Human tumor cell infection by Newcastle disease virus leads to upregulation of HLA and cell adhesion molecules and to induction of interferons, chemokines and finally apoptosis. Int J Oncol. 2002;21:85–93. doi:10.3892/ijo.21.1.85.
  • Zulkifli MM, Ibrahim R, Ali AM, Aini I, Jaafar H, Hilda SS, Alitheen NB, Abdullah JM. Newcastle diseases virus strain V4UPM displayed oncolytic ability against experimental human malignant glioma. Neurol Res. 2009;31:3–10. doi:10.1179/174313208X325218.
  • Cassel WA, Murray DR, Torbin AH, Olkowski ZL, Moore ME. Viral oncolysate in the management of malignant melanoma. I. Preparation of the oncolysate and measurement of immunologic responses. Cancer. 1977;40:672–79.
  • Murray DR, Cassel WA, Torbin AH, Olkowski ZL, Moore ME. Viral oncolysate in the management of malignant melanoma. II. Clinical studies. Cancer. 1977;40:680–86.
  • Cassel WA, Murray DR. Treatment of stage II malignant melanoma patients with a Newcastle disease virus oncolysate. Nat Immun Cell Growth Regul. 1988;7:351–52.
  • Cassel WA, Murray DR. A ten-year follow-up on stage II malignant melanoma patients treated postsurgically with Newcastle disease virus oncolysate. Med Oncol Tumor Pharmacother. 1992;9:169–71. doi:10.1007/bf02987752.
  • Liebrich W, Schlag P, Manasterski M, Lehner B, Stohr M, Moller P, Schirrmacher V. In vitro and clinical characterisation of a Newcastle disease virus-modified autologous tumour cell vaccine for treatment of colorectal cancer patients. Eur J Cancer. 1991;27:703–10. doi:10.1016/0277-5379(91)90170-I.
  • Schlag P, Manasterski M, Gerneth T, Hohenberger P, Dueck M, Herfarth C, Liebrich W, Schirrmacher V. Active specific immunotherapy with Newcastle-disease-virus-modified autologous tumor cells following resection of liver metastases in colorectal cancer. First evaluation of clinical response of a phase II-trial. Cancer Immunol Immunother. 1992;35:325–30. doi:10.1007/BF01741145.
  • Schulze T, Kemmner W, Weitz J, Wernecke KD, Schirrmacher V, Schlag PM. Efficiency of adjuvant active specific immunization with Newcastle disease virus modified tumor cells in colorectal cancer patients following resection of liver metastases: results of a prospective randomized trial. Cancer Immunol Immunother. 2009;58:61–69. doi:10.1007/s00262-008-0526-1.
  • Ockert D, Schirrmacher V, Beck N, Stoelben E, Ahlert T, Flechtenmacher J, Hagmüller E, Buchcik R, Nagel M, Saeger HD, et al. Newcastle disease virus-infected intact autologous tumor cell vaccine for adjuvant active specific immunotherapy of resected colorectal carcinoma. Clin Cancer Res. 1996;2:21–28.
  • Liang W, Wang H, Sun TM, Yao WQ, Chen LL, Jin Y, Li CL, Meng FJ. Application of autologous tumor cell vaccine and NDV vaccine in treatment of tumors of digestive tract. World J Gastroenterol. 2003;9:495–98. doi:10.3748/wjg.v9.i3.495.
  • Pomer S, Schirrmacher V, Thiele R, Lohrke H, Brkovic D, Staehler G. Tumor response and 4 year survival-data of patients with advanced renal-cell carcinoma treated with autologous tumor vaccine and subcutaneous R-IL-2 and IFN-alpha(2b). Int J Oncol. 1995;6:947–54. doi:10.3892/ijo.6.5.947.
  • Elankumaran S, Chavan V, Qiao D, Shobana R, Moorkanat G, Biswas M, Samal SK. Type I interferon-sensitive recombinant newcastle disease virus for oncolytic virotherapy. J Virol. 2010;84:3835–44. doi:10.1128/JVI.01553-09.
  • Wilden H, Fournier P, Zawatzky R, Schirrmacher V. Expression of RIG-I, IRF3, IFN-beta and IRF7 determines resistance or susceptibility of cells to infection by Newcastle disease virus. Int J Oncol. 2009;34:971–82. doi:10.3892/ijo_00000223.
  • Fiola C, Peeters B, Fournier P, Arnold A, Bucur M, Schirrmacher V. Tumor selective replication of Newcastle disease virus: association with defects of tumor cells in antiviral defence. Int J Cancer. 2006;119:328–38. doi:10.1002/(ISSN)1097-0215.
  • Krishnamurthy S, Takimoto T, Scroggs RA, Portner A. Differentially regulated interferon response determines the outcome of Newcastle disease virus infection in normal and tumor cell lines. J Virol. 2006;80:5145–55. doi:10.1128/JVI.02618-05.
  • Mansour M, Palese P, Zamarin D. Oncolytic specificity of Newcastle disease virus is mediated by selectivity for apoptosis-resistant cells. J Virol. 2011;85:6015–23. doi:10.1128/JVI.01537-10.
  • Lazar I, Yaacov B, Shiloach T, Eliahoo E, Kadouri L, Lotem M, Perlman R, Zakay-Rones Z, Panet A, Ben-Yehuda D, et al. The oncolytic activity of Newcastle disease virus NDV-HUJ on chemoresistant primary melanoma cells is dependent on the proapoptotic activity of the inhibitor of apoptosis protein Livin. J Virol. 2010;84:639–46. doi:10.1128/JVI.00401-09.
  • Wu Y, Zhang X, Wang X, Wang L, Hu S, Liu X, Meng S. Apoptin enhances the oncolytic properties of Newcastle disease virus. Intervirology. 2012;55:276–86. doi:10.1159/000328325.
  • Maamary J, Array F, Gao Q, Garcia-Sastre A, Steinman RM, Palese P, Nchinda G. Newcastle disease virus expressing a dendritic cell-targeted HIV gag protein induces a potent gag-specific immune response in mice. J Virol. 2011;85:2235–46. doi:10.1128/JVI.02036-10.
  • Puhler F, Willuda J, Puhlmann J, Mumberg D, Romer-Oberdorfer A, Beier R. Generation of a recombinant oncolytic Newcastle disease virus and expression of a full IgG antibody from two transgenes. Gene Ther. 2008;15:371–83. doi:10.1038/sj.gt.3303095.
  • About CAVATAK®. [accessed 2019 September]. https://www.viralytics.com/our-pipeline/cavatak/cavataktm/
  • [accessed 2019 September].https://www.cancertherapyadvisor.com/home/cancer-topics/general-oncology/phase-3-trial-for-oncolytic-viral-therapy-pexa-vec-in-advanced-liver-cancer-terminated-early/
  • light-emitting oncolytic vaccinia virus GL-ONC1. [accessed 2019 September]. https://www.cancer.gov/publications/dictionaries/cancer-drug/def/light-emitting-oncolytic-vaccinia-virus-gl-onc1.
  • Downs-Canner S, Guo ZS, Ravindranathan R, Breitbach CJ, O’Malley ME, Jones HL, Moon A, McCart JA, Shuai Y, Zeh HJ, et al. Phase 1 study of intravenous oncolytic poxvirus (vvDD) in patients with advanced solid cancers. Mol Ther. 2016;24:1492–501. doi:10.1038/mt.2016.101.
  • Zhang H, Lin Y, Li K, Liang J, Xiao X, Cai J, Tan Y, Xing F, Mai J, Li Y, et al. Naturally existing oncolytic virus M1 is nonpathogenic for the Nonhuman primates after multiple rounds of repeated intravenous injections. Hum Gene Ther. 2016;27:700–11. doi:10.1089/hum.2016.038.
  • Lin Y, Zhang H, Liang J, Li K, Zhu W, Fu L, Wang F, Zheng X, Shi H, Wu S, et al. Identification and characterization of alphavirus M1 as a selective oncolytic virus targeting ZAP-defective human cancers. Proc Natl Acad Sci USA. 2014;111:E4504–4512. doi:10.1073/pnas.1408759111.
  • Wang Y, Huang H, Zou H, Tian X, Hu J, Qiu P, Hu H, Yan G. Liposome encapsulation of oncolytic virus M1 to reduce immunogenicity and immune clearance in vivo. Mol Pharm. 2019;16:779–85. doi:10.1021/acs.molpharmaceut.8b01046.
  • Lundstrom K. Oncolytic alphaviruses in cancer immunotherapy. Vaccines (Basel). 2017;5:9. doi:10.3390/vaccines5020009.
  • Roy DG, Bell JC. Cell carriers for oncolytic viruses: current challenges and future directions. Oncolytic Virother. 2013;2:47–56. doi:10.2147/OV.S36623.

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