Home Life Sciences Employing RNA viruses to fight cancer: novel insights into oncolytic virotherapy
Article
Licensed
Unlicensed Requires Authentication

Employing RNA viruses to fight cancer: novel insights into oncolytic virotherapy

  • Dörthe Masemann , Yvonne Boergeling and Stephan Ludwig EMAIL logo
Published/Copyright: April 25, 2017

Abstract

Within recent decades, viruses that specifically target tumor cells have emerged as novel therapeutic agents against cancer. These viruses do not only act via their cell-lytic properties, but also harbor immunostimulatory features to re-direct the tumor microenvironment and stimulate tumor-directed immune responses. Furthermore, oncolytic viruses are considered to be superior to classical cancer therapies due to higher selectivity towards tumor cell destruction and, consequently, less collateral damage of non-transformed healthy tissue. In particular, the field of oncolytic RNA viruses is rapidly developing since these agents possess alternative tumor-targeting strategies compared to established oncolytic DNA viruses. Thus, oncolytic RNA viruses have broadened the field of virotherapy facilitating new strategies to fight cancer. In addition to several naturally occurring oncolytic viruses, genetically modified RNA viruses that are armed to express foreign factors such as immunostimulatory molecules have been successfully tested in early clinical trials showing promising efficacy. This review aims to provide an overview of the most promising RNA viruses in clinical development, to summarize the current knowledge of clinical trials using these viral agents, and to discuss the main issues as well as future perspectives of clinical approaches using oncolytic RNA viruses.

Acknowledgments

The author’s work relevant to this article has been supported by the Deutsche Forschungsgemeinschaft [DFG graduate school GRK1409, Collaborative Research Center (SFB1009B02)], Interdisciplinary Center of Clinical Research (IZKF) of the Medical Faculty, University of Münster (Lud2/008/17), and the Deutsche Krebshilfe gGmbH (grant 70112333). Moreover, this work was kindly backed by the COST Action BM1404 Mye-EUNITER (www.mye-euniter.eu). COST is supported by the EU Framework Program Horizon 2020.

References

Abril, E., Real, L.M., Serrano, A., Jimenez, P., Garcia, A., Canton, J., Trigo, I., Garrido, F., and Ruiz-Cabello, F. (1998). Unresponsiveness to interferon associated with STAT1 protein deficiency in a gastric adenocarcinoma cell line. Cancer Immunol. Immunother. 47, 113–120.10.1007/s002620050511Search in Google Scholar

An, Y., Liu, T., He, J., Wu, H., Chen, R., Liu, Y., Wu, Y., Bai, Y., Guo, X., Zheng, Q., et al. (2016). Recombinant Newcastle disease virus expressing P53 demonstrates promising antitumor efficiency in hepatoma model. J. Biomed. Sci. 23, 55.10.1186/s12929-016-0273-0Search in Google Scholar

Anderson, B.D., Nakamura, T., Russell, S.J., and Peng, K.W. (2004). High CD46 receptor density determines preferential killing of tumor cells by oncolytic measles virus. Cancer Res. 64, 4919–4926.10.1158/0008-5472.CAN-04-0884Search in Google Scholar

Andtbacka, R.H.I., Curti, B., Hallmeyer, S., Feng, Z., Paustian, C., Bifulco, C., Fox, B., Grose, M., Davies, B., Karpathy, R., et al. (2015a). 3336 Phase II CALM extension study: enhanced immune-cell infiltration within the tumour micro-environment of patients with advanced melanoma following intralesional delivery of Coxsackievirus A21. Eur. J. Cancer 51, S677.10.1016/S0959-8049(16)31854-8Search in Google Scholar

Andtbacka, R.H.I., Curti, B.D., Kaufman, H., Daniels, G.A., Nemunaitis, J.J., Spitler, L.E., Hallmeyer, S., Lutzky, J., Schultz, S.M., Grose, M., et al. (2015b). Final data from CALM: a phase II study of Coxsackievirus A21 (CVA21) oncolytic virus immunotherapy in patients with advanced melanoma. J. Clin. Oncol. 33 (suppl; abstr 9030).10.1200/jco.2015.33.15_suppl.9030Search in Google Scholar

Atsumi, S., Matsumine, A., Toyoda, H., Niimi, R., Iino, T., and Sudo, A. (2013). Prognostic significance of CD155 mRNA expression in soft tissue sarcomas. Oncol. Lett. 5, 1771–1776.10.3892/ol.2013.1280Search in Google Scholar PubMed PubMed Central

Au, G.G., Beagley, L.G., Haley, E.S., Barry, R.D., and Shafren, D.R. (2011). Oncolysis of malignant human melanoma tumors by Coxsackieviruses A13, A15 and A18. Virol. J. 8, 22.10.1186/1743-422X-8-22Search in Google Scholar PubMed PubMed Central

Baertsch, M.A., Leber, M.F., Bossow, S., Singh, M., Engeland, C.E., Albert, J., Grossardt, C., Jager, D., von Kalle, C., and Ungerechts, G. (2014). MicroRNA-mediated multi-tissue detargeting of oncolytic measles virus. Cancer Gene Ther. 21, 373–380.10.1038/cgt.2014.40Search in Google Scholar PubMed

Bai, F.L., Yu, Y.H., Tian, H., Ren, G.P., Wang, H., Zhou, B., Han, X.H., Yu, Q.Z., and Li, D.S. (2014). Genetically engineered Newcastle disease virus expressing interleukin-2 and TNF-related apoptosis-inducing ligand for cancer therapy. Cancer. Biol. Ther. 15, 1226–1238.10.4161/cbt.29686Search in Google Scholar PubMed PubMed Central

Batliwalla, F.M., Bateman, B.A., Serrano, D., Murray, D., Macphail, S., Maino, V.C., Ansel, J.C., Gregersen, P.K., and Armstrong, C.A. (1998). A 15-year follow-up of AJCC stage III malignant melanoma patients treated postsurgically with Newcastle disease virus (NDV) oncolysate and determination of alterations in the CD8 T cell repertoire. Mol. Med. 4, 783–794.10.1007/BF03401771Search in Google Scholar

Belkowski, L.S., and Sen, G.C. (1987). Inhibition of vesicular stomatitis viral mRNA synthesis by interferons. J. Virol. 61, 653–660.10.1128/jvi.61.3.653-660.1987Search in Google Scholar

Bergelson, J.M., Cunningham, J.A., Droguett, G., Kurt-Jones, E.A., Krithivas, A., Hong, J.S., Horwitz, M.S., Crowell, R.L., and Finberg, R.W. (1997). Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320–1323.10.1126/science.275.5304.1320Search in Google Scholar

Bergmann, M., Romirer, I., Sachet, M., Fleischhacker, R., Garcia-Sastre, A., Palese, P., Wolff, K., Pehamberger, H., Jakesz, R., and Muster, T. (2001). A genetically engineered influenza A virus with ras-dependent oncolytic properties. Cancer Res. 61, 8188–8193.Search in Google Scholar

Bevelacqua, V., Bevelacqua, Y., Candido, S., Skarmoutsou, E., Amoroso, A., Guarneri, C., Strazzanti, A., Gangemi, P., Mazzarino, M.C., D’Amico, F., et al. (2012). Nectin like-5 overexpression correlates with the malignant phenotype in cutaneous melanoma. Oncotarget 3, 882–892.10.18632/oncotarget.594Search in Google Scholar

Bian, H., Fournier, P., Peeters, B., and Schirrmacher, V. (2005a). Tumor-targeted gene transfer in vivo via recombinant Newcastle disease virus modified by a bispecific fusion protein. Int. J. Oncol. 27, 377–384.10.3892/ijo.27.2.377Search in Google Scholar

Bian, H., Fournier, P., Moormann, R., Peeters, B., and Schirrmacher, V. (2005b). Selective gene transfer in vitro to tumor cells via recombinant Newcastle disease virus. Cancer Gene Ther. 12, 295–303.10.1038/sj.cgt.7700774Search in Google Scholar

Black, T.L., Safer, B., Hovanessian, A., and Katze, M.G. (1989). The cellular 68,000-Mr protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: implications for translational regulation. J. Virol. 63, 2244–2251.10.1128/jvi.63.5.2244-2251.1989Search in Google Scholar

Bluming, A.Z., and Ziegler, J.L. (1971). Regression of Burkitt’s lymphoma in association with measles infection. Lancet 2, 105–106.10.1016/S0140-6736(71)92086-1Search in Google Scholar

Bodian, D. (1955). Emerging concept of poliomyelitis infection. Science 122, 105–108.10.1126/science.122.3159.105Search in Google Scholar PubMed

Boehme, K.W., Ikizler, M., Kobayashi, T., and Dermody, T.S. (2011). Reverse genetics for mammalian reovirus. Methods 55, 109–113.10.1016/j.ymeth.2011.07.002Search in Google Scholar PubMed PubMed Central

Bourgeois-Daigneault, M.C., Roy, D.G., Falls, T., Twumasi-Boateng, K., St-Germain, L.E., Marguerie, M., Garcia, V., Selman, M., Jennings, V.A., Pettigrew, J., et al. (2016). Oncolytic vesicular stomatitis virus expressing interferon-gamma has enhanced therapeutic activity. Mol. Ther. Oncolytics 3, 16001.10.1038/mto.2016.1Search in Google Scholar PubMed PubMed Central

Bradley, S., Jakes, A.D., Harrington, K., Pandha, H., Melcher, A., and Errington-Mais, F. (2014). Applications of coxsackievirus A21 in oncology. Oncolytic Virother. 3, 47–55.10.2147/OV.S56322Search in Google Scholar

Brown, M.C., Dobrikova, E.Y., Dobrikov, M.I., Walton, R.W., Gemberling, S.L., Nair, S.K., Desjardins, A., Sampson, J.H., Friedman, H.S., Friedman, A.H., et al. (2014). Oncolytic polio virotherapy of cancer. Cancer 120, 3277–3286.10.1002/cncr.28862Search in Google Scholar

Brown, M.C., Holl, E., Boczkowski, D., Walton, R., Bigner, D.D., Gromeier, M., and Nair, S.K. (2015). Oncolytic poliovirus directs tumor antigen presentation and T cell activation in vitro. J. Immunother. Cancer 3, P332–P332.10.1186/2051-1426-3-S2-P332Search in Google Scholar

Bucheit, A.D., Kumar, S., Grote, D.M., Lin, Y., von Messling, V., Cattaneo, R.B., and Fielding, A.K. (2003). An oncolytic measles virus engineered to enter cells through the CD20 antigen. Mol. Ther. 7, 62–72.10.1016/S1525-0016(02)00033-3Search in Google Scholar

Burke, M.J. (2016). Oncolytic Seneca Valley virus: past perspectives and future directions. Oncolytic Virother. 5, 81–89.10.2147/OV.S96915Search in Google Scholar

Cantin, C., Holguera, J., Ferreira, L., Villar, E., and Munoz-Barroso, I. (2007). Newcastle disease virus may enter cells by caveolae-mediated endocytosis. J. Gen. Virol. 88, 559–569.10.1099/vir.0.82150-0Search in Google Scholar

Cassel, W.A., and Garrett, R.E. (1965). Newcastle disease virus as an antineoplastic agent. Cancer 18, 863–868.10.1002/1097-0142(196507)18:7<863::AID-CNCR2820180714>3.0.CO;2-VSearch in Google Scholar

Cassel, W.A., and Murray, D.R. (1988). Treatment of stage II malignant melanoma patients with a Newcastle disease virus oncolysate. Nat. Immun. Cell Growth Regul. 7, 351–352.Search in Google Scholar

Chakrabarty, R., Tran, H., Selvaggi, G., Hagerman, A., Thompson, B., and Coffey, M. (2015). The oncolytic virus, pelareorep, as a novel anticancer agent: a review. Invest. New Drugs 33, 761–774.10.1007/s10637-015-0216-8Search in Google Scholar

Chen, S., Sun, H., Miao, K., and Deng, C.X. (2016). CRISPR-Cas9: from genome editing to cancer research. Int. J. Biol. Sci. 12, 1427–1436.10.7150/ijbs.17421Search in Google Scholar

Cheung, N.K., Walter, E.I., Smith-Mensah, W.H., Ratnoff, W.D., Tykocinski, M.L., and Medof, M.E. (1988). Decay-accelerating factor protects human tumor cells from complement-mediated cytotoxicity in vitro. J. Clin. Invest. 81, 1122–1128.10.1172/JCI113426Search in Google Scholar

Clemens, M.J. (1997). PKR – a protein kinase regulated by double-stranded RNA. Int. J. Biochem. Cell Biol. 29, 945–949.10.1016/S1357-2725(96)00169-0Search in Google Scholar

Coffey, M.C., Strong, J.E., Forsyth, P.A., and Lee, P.W. (1998). Reovirus therapy of tumors with activated Ras pathway. Science 282, 1332–1334.10.1126/science.282.5392.1332Search in Google Scholar

Cree, B.C., Bernardini, G.L., Hays, A.P., and Lowe, G. (2003). A fatal case of coxsackievirus B4 meningoencephalitis. Arch. Neurol. 60, 107–112.10.1001/archneur.60.1.107Search in Google Scholar

Cureton, D.K., Massol, R.H., Saffarian, S., Kirchhausen, T.L., and Whelan, S.P. (2009). Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 5, e1000394.10.1371/journal.ppat.1000394Search in Google Scholar

Cureton, D.K., Massol, R.H., Whelan, S.P., and Kirchhausen, T. (2010). The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLoS Pathog. 6, e1001127.10.1371/journal.ppat.1001127Search in Google Scholar

Danthi, P., Holm, G.H., Stehle, T., and Dermody, T.S. (2013). Reovirus receptors, cell entry, and proapoptotic signaling. Adv. Exp. Med. Biol. 790, 42–71.10.1007/978-1-4614-7651-1_3Search in Google Scholar

Demidenko, A.A., Blattman, J.N., Blattman, N.N., Greenberg, P.D., and Nibert, M.L. (2013). Engineering recombinant reoviruses with tandem repeats and a tetravirus 2A-like element for exogenous polypeptide expression. Proc. Natl. Acad. Sci. USA 110, E1867–76.10.1073/pnas.1220107110Search in Google Scholar

Dingli, D., Peng, K.W., Harvey, M.E., Greipp, P.R., O’Connor, M.K., Cattaneo, R., Morris, J.C., and Russell, S.J. (2004). Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter. Blood 103, 1641–1646.10.1182/blood-2003-07-2233Search in Google Scholar

Dobrikova, E.Y., Broadt, T., Poiley-Nelson, J., Yang, X., Soman, G., Giardina, S., Harris, R., and Gromeier, M. (2008). Recombinant oncolytic poliovirus eliminates glioma in vivo without genetic adaptation to a pathogenic phenotype. Mol. Ther. 16, 1865–1872.10.1038/mt.2008.184Search in Google Scholar

Doerig, R.E., Marcil, A., Chopra, A., and Richardson, C.D. (1993). The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75, 295–305.10.1016/0092-8674(93)80071-LSearch in Google Scholar

Dold, C., Rodriguez Urbiola, C., Wollmann, G., Egerer, L., Muik, A., Bellmann, L., Fiegl, H., Marth, C., Kimpel, J., and von Laer, D. (2016). Application of interferon modulators to overcome partial resistance of human ovarian cancers to VSV-GP oncolytic viral therapy. Mol. Ther. Oncolytics 3, 16021.10.1038/mto.2016.21Search in Google Scholar

Dornan, M.H., Krishnan, R., Macklin, A.M., Selman, M., El Sayes, N., Son, H.H., Davis, C., Chen, A., Keillor, K., Le, P.J., et al. (2016). First-in-class small molecule potentiators of cancer virotherapy. Sci. Rep. 6, 26786.10.1038/srep26786Search in Google Scholar

Eberle, K.E., Nguyen, V.T., and Freistadt, M.S. (1995). Low levels of poliovirus replication in primary human monocytes: possible interactions with lymphocytes. Arch. Virol. 140, 2135–2150.10.1007/BF01323236Search in Google Scholar

Eggermont, A.M., Chiarion-Sileni, V., Grob, J.J., Dummer, R., Wolchok, J.D., Schmidt, H., Hamid, O., Robert, C., Ascierto, P.A., Richards, J.M., et al. (2015). Adjuvant ipilimumab versus placebo after complete resection of high-risk stage III melanoma (EORTC 18071): a randomised, double-blind, phase 3 trial. Lancet Oncol. 16, 522–530.10.1016/S1470-2045(15)70122-1Search in Google Scholar

Evans, D.J. (1999). Reverse genetics of picornaviruses. Adv. Virus Res. 53, 209–228.10.1016/S0065-3527(08)60349-8Search in Google Scholar

Ferguson, M.S., Lemoine, N.R., and Wang, Y. (2012). Systemic delivery of oncolytic viruses: hopes and hurdles. Adv. Virol. 2012, 805629.10.1155/2012/805629Search in Google Scholar PubMed PubMed Central

Fernandes, J. (2016). Oncogenes: the passport for viral oncolysis through PKR inhibition. Biomark. Cancer 8, 101–110.10.4137/BIC.S33378Search in Google Scholar PubMed PubMed Central

Fiola, C., Peeters, B., Fournier, P., Arnold, A., Bucur, M., and Schirrmacher, V. (2006). Tumor selective replication of Newcastle disease virus: association with defects of tumor cells in antiviral defence. Int. J. Cancer 119, 328–338.10.1002/ijc.21821Search in Google Scholar PubMed

Fisher, K. (2006). Striking out at disseminated metastases: the systemic delivery of oncolytic viruses. Curr. Opin. Mol. Ther. 8, 301–313.Search in Google Scholar

Fournier, J.G., Robain, O., Cerutti, I., Tardivel, I., Chany-Fournier, F., and Chany, C. (1988). Detection of vesicular stomatitis virus (VSV) RNA in the central nervous system of infected mice by in situ hybridization. Acta Neuropathol. 75, 554–556.10.1007/BF00686199Search in Google Scholar PubMed

Freeman, A.I., Zakay-Rones, Z., Gomori, J.M., Linetsky, E., Rasooly, L., Greenbaum, E., Rozenman-Yair, S., Panet, A., Libson, E., Irving, C.S., et al. (2006). Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol. Ther. 13, 221–228.10.1016/j.ymthe.2005.08.016Search in Google Scholar PubMed

Friedrich, K., Hanauer, J.R., Prufer, S., Munch, R.C., Volker, I., Filippis, C., Jost, C., Hanschmann, K.M., Cattaneo, R., Peng, K.W., et al. (2013). DARPin-targeting of measles virus: unique bispecificity, effective oncolysis, and enhanced safety. Mol. Ther. 21, 849–859.10.1038/mt.2013.16Search in Google Scholar

Galanis, E., Hartmann, L.C., Cliby, W.A., Long, H.J., Peethambaram, P.P., Barrette, B.A., Kaur, J.S., Haluska, P.J., Jr, Aderca, I., Zollman, P.J., et al. (2010). Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res. 70, 875–882.10.1158/0008-5472.CAN-09-2762Search in Google Scholar

Galanis, E., Atherton, P.J., Maurer, M.J., Knutson, K.L., Dowdy, S.C., Cliby, W.A., Haluska, P., Jr., Long, H.J., Oberg, A., Aderca, I., et al. (2015). Oncolytic measles virus expressing the sodium iodide symporter to treat drug-resistant ovarian cancer. Cancer Res. 75, 22–30.10.1158/0008-5472.CAN-14-2533Search in Google Scholar

Gebhard, J.R., Perry, C.M., Harkins, S., Lane, T., Mena, I., Asensio, V.C., Campbell, I.L., and Whitton, J.L. (1998). Coxsackievirus B3-induced myocarditis: perforin exacerbates disease, but plays no detectable role in virus clearance. Am. J. Pathol. 153, 417–428.10.1016/S0002-9440(10)65585-XSearch in Google Scholar

Ghatalia, P., Zibelman, M., Geynisman, D.M., and Plimack, E.R. (2017). Checkpoint inhibitors for the treatment of renal cell carcinoma. Curr. Treat. Options Oncol. 18, 7.10.1007/s11864-017-0458-0Search in Google Scholar PubMed

Gil, J., Alcami, J., and Esteban, M. (2000). Activation of NF-kappa B by the dsRNA-dependent protein kinase, PKR involves the IκB kinase complex. Oncogene 19, 1369–1378.10.1038/sj.onc.1203448Search in Google Scholar PubMed

Gong, J., Sachdev, E., Mita, A.C., and Mita, M.M. (2016). Clinical development of reovirus for cancer therapy: an oncolytic virus with immune-mediated antitumor activity. World J. Methodol. 6, 25–42.10.5662/wjm.v6.i1.25Search in Google Scholar PubMed PubMed Central

Gromeier, M., Alexander, L., and Wimmer, E. (1996). Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc. Natl. Acad. Sci. USA 93, 2370–2375.10.1073/pnas.93.6.2370Search in Google Scholar PubMed PubMed Central

Gromeier, M., Solecki, D., Patel, D.D., and Wimmer, E. (2000a). Expression of the human poliovirus receptor/CD155 gene during development of the central nervous system: implications for the pathogenesis of poliomyelitis. Virology 273, 248–257.10.1006/viro.2000.0418Search in Google Scholar PubMed

Gromeier, M., Lachmann, S., Rosenfeld, M.R., Gutin, P.H., and Wimmer, E. (2000b). Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc. Natl. Acad. Sci. USA 97, 6803–6808.10.1073/pnas.97.12.6803Search in Google Scholar PubMed PubMed Central

Gromeier, M., Dobrikova, E., Dobrikov, M., Brown, M., Bryant, J., Threatt, S., Boulton, S., Carter, K., Herndon, J., Desjardins, A., et al. (2014). Oncolytic poliovirus immunotherapy of glioblastoma. Neuro-oncology 16, iii41–iii41.10.1093/neuonc/nou208.69Search in Google Scholar

Grote, D., Cattaneo, R., and Fielding, A.K. (2003). Neutrophils contribute to the measles virus-induced antitumor effect: enhancement by granulocyte macrophage colony-stimulating factor expression. Cancer Res. 63, 6463–6468.Search in Google Scholar

Hales, L.M., Knowles, N.J., Reddy, P.S., Xu, L., Hay, C., and Hallenbeck, P.L. (2008). Complete genome sequence analysis of Seneca Valley virus-001, a novel oncolytic picornavirus. J. Gen. Virol. 89, 1265–1275.10.1099/vir.0.83570-0Search in Google Scholar PubMed

Hastie, E., and Grdzelishvili, V.Z. (2012). Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer. J. Gen. Virol. 93, 2529–2545.10.1099/vir.0.046672-0Search in Google Scholar PubMed PubMed Central

Hingorani, P., Zhang, W., Lin, J., Liu, L., Guha, C., and Kolb, E.A. (2011). Systemic administration of reovirus (Reolysin) inhibits growth of human sarcoma xenografts. Cancer 117, 1764–1774.10.1002/cncr.25741Search in Google Scholar PubMed

Hirasawa, K., Nishikawa, S.G., Norman, K.L., Alain, T., Kossakowska, A., and Lee, P.W. (2002). Oncolytic reovirus against ovarian and colon cancer. Cancer Res. 62, 1696–1701.Search in Google Scholar

Hirasawa, K., Nishikawa, S.G., Norman, K.L., Coffey, M.C., Thompson, B.G., Yoon, C.S., Waisman, D.M., and Lee, P.W. (2003). Systemic reovirus therapy of metastatic cancer in immune-competent mice. Cancer Res. 63, 348–353.Search in Google Scholar

Hock, K., Laengle, J., Kuznetsova, I., Egorov, A., Hegedus, B., Dome, B., Wekerle, T., Sachet, M., and Bergmann, M. (2016). Oncolytic influenza A virus expressing interleukin-15 decreases tumor growth in vivo. Surgery 161, 735–746.10.1016/j.surg.2016.08.045Search in Google Scholar PubMed

Holl, E.K., Brown, M.C., Boczkowski, D., McNamara, M.A., George, D.J., Bigner, D.D., Gromeier, M., and Nair, S.K. (2016). Recombinant oncolytic poliovirus, PVSRIPO, has potent cytotoxic and innate inflammatory effects, mediating therapy in human breast and prostate cancer xenograft models. Oncotarget 7, 79828–79841.10.18632/oncotarget.12975Search in Google Scholar PubMed PubMed Central

Hotte, S.J., Lorence, R.M., Hirte, H.W., Polawski, S.R., Bamat, M.K., O’Neil, J.D., Roberts, M.S., Groene, W.S., and Major, P.P. (2007). An optimized clinical regimen for the oncolytic virus PV701. Clin. Cancer Res. 13, 977–985.10.1158/1078-0432.CCR-06-1817Search in Google Scholar PubMed

Hummeler, K., Kirk, D., and Ostapiak, M. (1954). Aseptic meningitis caused by Coxsackie virus with isolation of virus from cerebrospinal fluid. J. Am. Med. Assoc. 156, 676–679.10.1001/jama.1954.02950070004002Search in Google Scholar PubMed

Huneycutt, B.S., Bi, Z., Aoki, C.J., and Reiss, C.S. (1993). Central neuropathogenesis of vesicular stomatitis virus infection of immunodeficient mice. J. Virol. 67, 6698–6706.10.1128/jvi.67.11.6698-6706.1993Search in Google Scholar PubMed PubMed Central

Iankov, I.D., Blechacz, B., Liu, C., Schmeckpeper, J.D., Tarara, J.E., Federspiel, M.J., Caplice, N., and Russell, S.J. (2007). Infected cell carriers: a new strategy for systemic delivery of oncolytic measles viruses in cancer virotherapy. Mol. Ther. 15, 114–122.10.1038/sj.mt.6300020Search in Google Scholar PubMed

Inoue, T., Yamakawa, M., and Takahashi, T. (2002). Expression of complement regulating factors in gastric cancer cells. Mol. Pathol. 55, 193–199.10.1136/mp.55.3.193Search in Google Scholar

Irie, T., Carnero, E., Okumura, A., Garcia-Sastre, A., and Harty, R.N. (2007). Modifications of the PSAP region of the matrix protein lead to attenuation of vesicular stomatitis virus in vitro and in vivo. J. Gen. Virol. 88, 2559–2567.10.1099/vir.0.83096-0Search in Google Scholar

Israelsson, S., Jonsson, N., Gullberg, M., and Lindberg, A.M. (2011). Cytolytic replication of echoviruses in colon cancer cell lines. Virol. J. 8, 473.10.1186/1743-422X-8-473Search in Google Scholar

Janke, M., Peeters, B., de Leeuw, O., Moorman, R., Arnold, A., Fournier, P., and Schirrmacher, V. (2007). Recombinant Newcastle disease virus (NDV) with inserted gene coding for GM-CSF as a new vector for cancer immunogene therapy. Gene Ther. 14, 1639–1649.10.1038/sj.gt.3303026Search in Google Scholar

Janke, M., Peeters, B., Zhao, H., de Leeuw, O., Moorman, R., Arnold, A., Ziouta, Y., Fournier, P., and Schirrmacher, V. (2008). Activation of human T cells by a tumor vaccine infected with recombinant Newcastle disease virus producing IL-2. Int. J. Oncol. 33, 823–832.Search in Google Scholar

Jenks, N., Myers, R., Greiner, S.M., Thompson, J., Mader, E.K., Greenslade, A., Griesmann, G.E., Federspiel, M.J., Rakela, J., Borad, M.J., et al. (2010). Safety studies on intrahepatic or intratumoral injection of oncolytic vesicular stomatitis virus expressing interferon-β in rodents and nonhuman primates. Hum. Gene Ther. 21, 451–462.10.1089/hum.2009.111Search in Google Scholar

Johansson, E.S., Xing, L., Cheng, R.H., and Shafren, D.R. (2004). Enhanced cellular receptor usage by a bioselected variant of coxsackievirus a21. J. Virol. 78, 12603–12612.10.1128/JVI.78.22.12603-12612.2004Search in Google Scholar

Johnson, J.E., Nasar, F., Coleman, J.W., Price, R.E., Javadian, A., Draper, K., Lee, M., Reilly, P.A., Clarke, D.K., Hendry, R.M., et al. (2007). Neurovirulence properties of recombinant vesicular stomatitis virus vectors in non-human primates. Virology 360, 36–49.10.1016/j.virol.2006.10.026Search in Google Scholar

Johnson, D.B., Puzanov, I., and Kelley, M.C. (2015). Talimogene laherparepvec (T-VEC) for the treatment of advanced melanoma. Immunotherapy 7, 611–619.10.2217/imt.15.35Search in Google Scholar

Jurianz, K., Ziegler, S., Garcia-Schuler, H., Kraus, S., Bohana-Kashtan, O., Fishelson, Z., and Kirschfink, M. (1999). Complement resistance of tumor cells: basal and induced mechanisms. Mol. Immunol. 36, 929–939.10.1016/S0161-5890(99)00115-7Search in Google Scholar

Karcher, J., Dyckhoff, G., Beckhove, P., Reisser, C., Brysch, M., Ziouta, Y., Helmke, B.H., Weidauer, H., Schirrmacher, V., and Herold-Mende, C. (2004). Antitumor vaccination in patients with head and neck squamous cell carcinomas with autologous virus-modified tumor cells. Cancer Res. 64, 8057–8061.10.1158/0008-5472.CAN-04-1545Search in Google Scholar PubMed

Kaufman, H.L., and Bines, S.D. (2010). OPTIM trial: a Phase III trial of an oncolytic herpes virus encoding GM-CSF for unresectable stage III or IV melanoma. Future Oncol. 6, 941–949.10.2217/fon.10.66Search in Google Scholar PubMed

Kaufman, H.L., Kohlhapp, F.J., and Zloza, A. (2015). Oncolytic viruses: a new class of immunotherapy drugs. Nat. Rev. Drug Discov. 14, 642–662.10.1038/nrd4663Search in Google Scholar PubMed PubMed Central

Kazimirsky, G., Jiang, W., Slavin, S., Ziv-Av, A., and Brodie, C. (2016). Mesenchymal stem cells enhance the oncolytic effect of Newcastle disease virus in glioma cells and glioma stem cells via the secretion of TRAIL. Stem Cell. Res. Ther. 7, 149.10.1186/s13287-016-0414-0Search in Google Scholar PubMed PubMed Central

Kelly, E.J., Nace, R., Barber, G.N., and Russell, S.J. (2010). Attenuation of vesicular stomatitis virus encephalitis through microRNA targeting. J. Virol. 84, 1550–1562.10.1128/JVI.01788-09Search in Google Scholar PubMed PubMed Central

Kemball, C.C., Flynn, C.T., Hosking, M.P., Botten, J., and Whitton, J.L. (2012). Wild-type coxsackievirus infection dramatically alters the abundance, heterogeneity, and immunostimulatory capacity of conventional dendritic cells in vivo. Virology 429, 74–90.10.1016/j.virol.2012.04.005Search in Google Scholar PubMed PubMed Central

Kemp, V., Hoeben, R.C., and van den Wollenberg, D.J. (2015). Exploring reovirus plasticity for improving its use as oncolytic virus. Viruses 8, 4.10.3390/v8010004Search in Google Scholar PubMed PubMed Central

Khuri, F.R., Nemunaitis, J., Ganly, I., Arseneau, J., Tannock, I.F., Romel, L., Gore, M., Ironside, J., MacDougall, R.H., Heise, C., et al. (2000). 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. 6, 879–885.10.1038/78638Search in Google Scholar PubMed

Kim, M., Williamson, C.T., Prudhomme, J., Bebb, D.G., Riabowol, K., Lee, P.W., Lees-Miller, S.P., Mori, Y., Rahman, M.M., McFadden, G., et al. (2010). The viral tropism of two distinct oncolytic viruses, reovirus and myxoma virus, is modulated by cellular tumor suppressor gene status. Oncogene 29, 3990–3996.10.1038/onc.2010.137Search in Google Scholar PubMed PubMed Central

Krishnamurthy, S., Takimoto, T., Scroggs, R.A., and Portner, A. (2006). Differentially regulated interferon response determines the outcome of Newcastle disease virus infection in normal and tumor cell lines. J. Virol. 80, 5145–5155.10.1128/JVI.02618-05Search in Google Scholar PubMed PubMed Central

Langland, J.O., Pettiford, S., Jiang, B., and Jacobs, B.L. (1994). Products of the porcine group C rotavirus NSP3 gene bind specifically to double-stranded RNA and inhibit activation of the interferon-induced protein kinase PKR. J. Virol. 68, 3821–3829.10.1128/jvi.68.6.3821-3829.1994Search in Google Scholar

Laurie, S.A., Bell, J.C., Atkins, H.L., Roach, J., Bamat, M.K., O’Neil, J.D., Roberts, M.S., Groene, W.S., and Lorence, R.M. (2006). A phase 1 clinical study of intravenous administration of PV701, an oncolytic virus, using two-step desensitization. Clin. Cancer Res. 12, 2555–2562.10.1158/1078-0432.CCR-05-2038Search in Google Scholar PubMed

LeBlanc, A.K., Naik, S., Galyon, G.D., Jenks, N., Steele, M., Peng, K.W., Federspiel, M.J., Donnell, R., and Russell, S.J. (2013). Safety studies on intravenous administration of oncolytic recombinant vesicular stomatitis virus in purpose-bred beagle dogs. Hum. Gene Ther. Clin. Dev. 24, 174–181.10.1089/humc.2013.165Search in Google Scholar PubMed PubMed Central

Li, L., Spendlove, I., Morgan, J., and Durrant, L.G. (2001). CD55 is over-expressed in the tumour environment. Br. J. Cancer 84, 80–86.10.1054/bjoc.2000.1570Search in Google Scholar PubMed PubMed Central

Liang, M. (2012). Clinical development of oncolytic viruses in China. Curr. Pharm. Biotechnol. 13, 1852–1857.10.2174/138920112800958760Search in Google Scholar PubMed

Lichty, B.D., Breitbach, C.J., Stojdl, D.F., and Bell, J.C. (2014). Going viral with cancer immunotherapy. Nat. Rev. Cancer. 14, 559–567.10.1038/nrc3770Search in Google Scholar PubMed

Liu, Z., Zhao, X., Mao, H., Baxter, P.A., Huang, Y., Yu, L., Wadhwa, L., Su, J.M., Adesina, A., Perlaky, L., et al. (2013). Intravenous injection of oncolytic picornavirus SVV-001 prolongs animal survival in a panel of primary tumor-based orthotopic xenograft mouse models of pediatric glioma. Neuro Oncol. 15, 1173–1185.10.1093/neuonc/not065Search in Google Scholar PubMed PubMed Central

Lorence, R.M., Katubig, B.B., Reichard, K.W., Reyes, H.M., Phuangsab, A., Sassetti, M.D., Walter, R.J., and Peeples, M.E. (1994a). Complete regression of human fibrosarcoma xenografts after local Newcastle disease virus therapy. Cancer Res. 54, 6017–6021.Search in Google Scholar

Lorence, R.M., Reichard, K.W., Katubig, B.B., Reyes, H.M., Phuangsab, A., Mitchell, B.R., Cascino, C.J., Walter, R.J., and Peeples, M.E. (1994b). Complete regression of human neuroblastoma xenografts in athymic mice after local Newcastle disease virus therapy. J. Natl. Cancer Inst. 86, 1228–1233.10.1093/jnci/86.16.1228Search in Google Scholar PubMed

Lu, Y., Wambach, M., Katze, M.G., and Krug, R.M. (1995). Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 214, 222–228.10.1006/viro.1995.9937Search in Google Scholar PubMed

Lu, W., Zheng, S., Li, X.F., Huang, J.J., Zheng, X., and Li, Z. (2004). Intra-tumor injection of H101, a recombinant adenovirus, in combination with chemotherapy in patients with advanced cancers: a pilot phase II clinical trial. World J. Gastroenterol. 10, 3634–3638.10.3748/wjg.v10.i24.3634Search in Google Scholar PubMed PubMed Central

Luig, C., Kother, K., Dudek, S.E., Gaestel, M., Hiscott, J., Wixler, V., and Ludwig, S. (2010). MAP kinase-activated protein kinases 2 and 3 are required for influenza A virus propagation and act via inhibition of PKR. FASEB J. 24, 4068–4077.10.1096/fj.10-158766Search in Google Scholar PubMed

Mader, E.K., Maeyama, Y., Lin, Y., Butler, G.W., Russell, H.M., Galanis, E., Russell, S.J., Dietz, A.B., and Peng, K.W. (2009). Mesenchymal stem cell carriers protect oncolytic measles viruses from antibody neutralization in an orthotopic ovarian cancer therapy model. Clin. Cancer Res. 15, 7246–7255.10.1158/1078-0432.CCR-09-1292Search in Google Scholar

Mansour, M., Palese, P., and Zamarin, D. (2011). Oncolytic specificity of Newcastle disease virus is mediated by selectivity for apoptosis-resistant cells. J. Virol. 85, 6015–6023.10.1128/JVI.01537-10Search in Google Scholar

Mao, Q., Wang, Y., Yao, X., Bian, L., Wu, X., Xu, M., and Liang, Z. (2014). Coxsackievirus A16: epidemiology, diagnosis, and vaccine. Hum. Vaccin Immunother. 10, 360–367.10.4161/hv.27087Search in Google Scholar

Marcato, P., Dean, C.A., Giacomantonio, C.A., and Lee, P.W. (2009). Oncolytic reovirus effectively targets breast cancer stem cells. Mol. Ther. 17, 972–979.10.1038/mt.2009.58Search in Google Scholar

Mardis, E.R., and Wilson, R.K. (2009). Cancer genome sequencing: a review. Hum. Mol. Genet. 18, R163–8.10.1093/hmg/ddp396Search in Google Scholar

Marier, R., Rodriguez, W., Chloupek, R.J., Brandt, C.D., Kim, H.W., Baltimore, R.S., Parker, C.L., and Artenstein, M.S. (1975). Coxsackievirus B5 infection and aseptic meningitis in neonates and children. Am. J. Dis. Child. 129, 321–325.10.1001/archpedi.1975.02120400031007Search in Google Scholar

Marozin, S., Altomonte, J., Stadler, F., Thasler, W.E., Schmid, R.M., and Ebert, O. (2008). Inhibition of the IFN-β response in hepatocellular carcinoma by alternative spliced isoform of IFN regulatory factor-3. Mol. Ther. 16, 1789–1797.10.1038/mt.2008.201Search in Google Scholar

Masson, D., Jarry, A., Baury, B., Blanchardie, P., Laboisse, C., Lustenberger, P., and Denis, M.G. (2001). Overexpression of the CD155 gene in human colorectal carcinoma. Gut 49, 236–240.10.1136/gut.49.2.236Search in Google Scholar

Mendelsohn, C.L., Wimmer, E., and Racaniello, V.R. (1989). Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56, 855–865.10.1016/0092-8674(89)90690-9Search in Google Scholar

Miles, L.A., Poirier, J.T., and Rudin, C.M. (2016). Identification of the anthrax toxin receptor (ANTXR1) as the high affinity cellular receptor for Seneca Valley virus (SVV) [abstract]. Cancer Res. 76, Abstract nr 4356.10.1158/1538-7445.AM2016-4356Search in Google Scholar

Miller, J.P., Geng, Y., Ng, H.L., Yang, O.O., and Krogstad, P. (2009). Packaging limits and stability of HIV-1 sequences in a coxsackievirus B vector. Vaccine 27, 3992–4000.10.1016/j.vaccine.2009.04.035Search in Google Scholar PubMed PubMed Central

Miyamoto, S., Inoue, H., Nakamura, T., Yamada, M., Sakamoto, C., Urata, Y., Okazaki, T., Marumoto, T., Takahashi, A., Takayama, K., et al. (2012). Coxsackievirus B3 is an oncolytic virus with immunostimulatory properties that is active against lung adenocarcinoma. Cancer Res. 72, 2609–2621.10.1158/0008-5472.CAN-11-3185Search in Google Scholar

Moreau, B., Bastedo, C., Michel, R.P., and Ghali, P. (2011). Hepatitis and encephalitis due to Coxsackie virus A9 in an adult. Case Reports Gastroenterol. 5, 617–622.10.1159/000333135Search in Google Scholar

Morton, C.L., Houghton, P.J., Kolb, E.A., Gorlick, R., Reynolds, C.P., Kang, M.H., Maris, J.M., Keir, S.T., Wu, J., and Smith, M.A. (2010). Initial testing of the replication competent Seneca Valley virus (NTX-010) by the pediatric preclinical testing program. Pediatr. Blood Cancer. 55, 295–303.10.1002/pbc.22535Search in Google Scholar

Muehlebach, M.D., Mateo, M., Sinn, P.L., Prufer, S., Uhlig, K.M., Leonard, V.H., Navaratnarajah, C.K., Frenzke, M., Wong, X.X., Sawatsky, B., et al. (2011). Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 480, 530–533.10.1038/nature10639Search in Google Scholar

Muik, A., Kneiske, I., Werbizki, M., Wilflingseder, D., Giroglou, T., Ebert, O., Kraft, A., Dietrich, U., Zimmer, G., Momma, S., et al. (2011). Pseudotyping vesicular stomatitis virus with lymphocytic choriomeningitis virus glycoproteins enhances infectivity for glioma cells and minimizes neurotropism. J. Virol. 85, 5679–5684.10.1128/JVI.02511-10Search in Google Scholar

Muik, A., Stubbert, L.J., Jahedi, R.Z., Geibeta, Y., Kimpel, J., Dold, C., Tober, R., Volk, A., Klein, S., Dietrich, U., et al. (2014). Re-engineering vesicular stomatitis virus to abrogate neurotoxicity, circumvent humoral immunity, and enhance oncolytic potency. Cancer Res. 74, 3567–3578.10.1158/0008-5472.CAN-13-3306Search in Google Scholar

Mundschau, L.J., and Faller, D.V. (1992). Oncogenic ras induces an inhibitor of double-stranded RNA-dependent eukaryotic initiation factor 2 α-kinase activation. J. Biol. Chem. 267, 23092–23098.10.1016/S0021-9258(18)50061-2Search in Google Scholar

Nakai, R., Maniwa, Y., Tanaka, Y., Nishio, W., Yoshimura, M., Okita, Y., Ohbayashi, C., Satoh, N., Ogita, H., Takai, Y., et al. (2010). Overexpression of Necl-5 correlates with unfavorable prognosis in patients with lung adenocarcinoma. Cancer. Sci. 101, 1326–1330.10.1111/j.1349-7006.2010.01530.xSearch in Google Scholar PubMed

Nakamura, T., Peng, K.W., Harvey, M., Greiner, S., Lorimer, I.A., James, C.D., and Russell, S.J. (2005). Rescue and propagation of fully retargeted oncolytic measles viruses. Nat. Biotechnol. 23, 209–214.10.1038/nbt1060Search in Google Scholar PubMed

Nakaya, T., Cros, J., Park, M.S., Nakaya, Y., Zheng, H., Sagrera, A., Villar, E., Garcia-Sastre, A., and Palese, P. (2001). Recombinant Newcastle disease virus as a vaccine vector. J. Virol. 75, 11868–11873.10.1128/JVI.75.23.11868-11873.2001Search in Google Scholar PubMed PubMed Central

Niu, Z., Bai, F., Sun, T., Tian, H., Yu, D., Yin, J., Li, S., Li, T., Cao, H., Yu, Q., et al. (2015). Recombinant Newcastle disease virus expressing IL15 demonstrates promising antitumor efficiency in melanoma model. Technol. Cancer. Res. Treat. 14, 607–615.10.7785/tcrt.2012.500414Search in Google Scholar

Norman, K.L., and Lee, P.W. (2000). Reovirus as a novel oncolytic agent. J. Clin. Invest. 105, 1035–1038.10.1172/JCI9871Search in Google Scholar

Noyce, R.S., Bondre, D.G., Ha, M.N., Lin, L.T., Sisson, G., Tsao, M.S., and Richardson, C.D. (2011). Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 7, e1002240.10.1371/journal.ppat.1002240Search in Google Scholar

Obuchi, M., Fernandez, M., and Barber, G.N. (2003). Development of recombinant vesicular stomatitis viruses that exploit defects in host defense to augment specific oncolytic activity. J. Virol. 77, 8843–8856.10.1128/JVI.77.16.8843-8856.2003Search in Google Scholar

Parker Kerrigan, B.C., Shimizu, Y., Andreeff, M., and Lang, F.F. (2017). Mesenchymal stromal cells for the delivery of oncolytic viruses in gliomas. Cytotherapy 19, 445–457.10.1016/j.jcyt.2017.02.002Search in Google Scholar

Patel, M.R., Jacobson, B.A., Ji, Y., Drees, J., Tang, S., Xiong, K., Wang, H., Prigge, J.E., Dash, A.S., Kratzke, A.K., et al. (2015). Vesicular stomatitis virus expressing interferon-beta is oncolytic and promotes antitumor immune responses in a syngeneic murine model of non-small cell lung cancer. Oncotarget 6, 33165–33177.10.18632/oncotarget.5320Search in Google Scholar

Pecora, A.L., Rizvi, N., Cohen, G.I., Meropol, N.J., Sterman, D., Marshall, J.L., Goldberg, S., Gross, P., O’Neil, J.D., Groene, W.S., et al. (2002). Phase I trial of intravenous administration of PV701, an oncolytic virus, in patients with advanced solid cancers. J. Clin. Oncol. 20, 2251–2266.10.1200/JCO.2002.08.042Search in Google Scholar

Peng, K.W., Facteau, S., Wegman, T., O’Kane, D., and Russell, S.J. (2002). Non-invasive in vivo monitoring of trackable viruses expressing soluble marker peptides. Nat. Med. 8, 527–531.10.1038/nm0502-527Search in Google Scholar

Phuangsab, A., Lorence, R.M., Reichard, K.W., Peeples, M.E., and Walter, R.J. (2001). Newcastle disease virus therapy of human tumor xenografts: antitumor effects of local or systemic administration. Cancer Lett. 172, 27–36.10.1016/S0304-3835(01)00617-6Search in Google Scholar

Pizzuto, M.S., Silic-Benussi, M., Ciminale, V., Elderfield, R.A., Capua, I., and Barclay, W.S. (2016). An engineered avian-origin influenza A virus for pancreatic ductal adenocarcinoma virotherapy. J. Gen. Virol. 97, 2166–2179.10.1099/jgv.0.000549Search in Google Scholar PubMed

Platt, R.J., Chen, S., Zhou, Y., Yim, M.J., Swiech, L., Kempton, H.R., Dahlman, J.E., Parnas, O., Eisenhaure, T.M., Jovanovic, M., et al. (2014). CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159, 440–455.10.1016/j.cell.2014.09.014Search in Google Scholar PubMed PubMed Central

Poirier, J.T., Dobromilskaya, I., Moriarty, W.F., Peacock, C.D., Hann, C.L., and Rudin, C.M. (2013). Selective tropism of Seneca Valley virus for variant subtype small cell lung cancer. J. Natl. Cancer Inst. 105, 1059–1065.10.1093/jnci/djt130Search in Google Scholar PubMed PubMed Central

Pol, J.G., Zhang, L., Bridle, B.W., Stephenson, K.B., Resseguier, J., Hanson, S., Chen, L., Kazdhan, N., Bramson, J.L., Stojdl, D.F., et al. (2014). Maraba virus as a potent oncolytic vaccine vector. Mol. Ther. 22, 420–429.10.1038/mt.2013.249Search in Google Scholar PubMed PubMed Central

Pol, J., Buque, A., Aranda, F., Bloy, N., Cremer, I., Eggermont, A., Erbs, P., Fucikova, J., Galon, J., Limacher, J.M., et al. (2015). Trial Watch – Oncolytic viruses and cancer therapy. Oncoimmunology 5, e1117740.10.1080/2162402X.2015.1117740Search in Google Scholar PubMed PubMed Central

Rajani, K., Parrish, C., Kottke, T., Thompson, J., Zaidi, S., Ilett, L., Shim, K.G., Diaz, R.M., Pandha, H., Harrington, K., et al. (2016). Combination therapy with reovirus and anti-PD-1 blockade controls tumor growth through innate and adaptive immune responses. Mol. Ther. 24, 166–174.10.1038/mt.2015.156Search in Google Scholar PubMed PubMed Central

Ramirez, M., Garcia-Castro, J., Melen, G.J., Gonzalez-Murillo, A., and Franco-Luzon, L. (2015). Patient-derived mesenchymal stem cells as delivery vehicles for oncolytic virotherapy: novel state-of-the-art technology. Oncolytic Virother 4, 149–155.10.2147/OV.S66010Search in Google Scholar PubMed PubMed Central

Reddy, P.S., Burroughs, K.D., Hales, L.M., Ganesh, S., Jones, B.H., Idamakanti, N., Hay, C., Li, S.S., Skele, K.L., Vasko, A.J., et al. (2007). Seneca Valley virus, a systemically deliverable oncolytic picornavirus, and the treatment of neuroendocrine cancers. J. Natl. Cancer Inst. 99, 1623–1633.10.1093/jnci/djm198Search in Google Scholar PubMed PubMed Central

Remon, J., Pardo, N., Martinez-Marti, A., Cedres, S., Navarro, A., Martinez de Castro, A.M., and Felip, E. (2017). Immune-checkpoint inhibition in first-line treatment of advanced non-small cell lung cancer patients: current status and future approaches. Lung Cancer 106, 70–75.10.1016/j.lungcan.2017.02.002Search in Google Scholar PubMed

Roner, M.R., and Joklik, W.K. (2001). Reovirus reverse genetics: incorporation of the CAT gene into the reovirus genome. Proc. Natl. Acad. Sci. USA 98, 8036–8041.10.1073/pnas.131203198Search in Google Scholar PubMed PubMed Central

Rose, N.F., Roberts, A., Buonocore, L., and Rose, J.K. (2000). Glycoprotein exchange vectors based on vesicular stomatitis virus allow effective boosting and generation of neutralizing antibodies to a primary isolate of human immunodeficiency virus type 1. J. Virol. 74, 10903–10910.10.1128/JVI.74.23.10903-10910.2000Search in Google Scholar

Rudin, C.M., Poirier, J.T., Senzer, N.N., Stephenson, J., Jr, Loesch, D., Burroughs, K.D., Reddy, P.S., Hann, C.L., and Hallenbeck, P.L. (2011). Phase I clinical study of Seneca Valley virus (SVV-001), a replication-competent picornavirus, in advanced solid tumors with neuroendocrine features. Clin. Cancer Res. 17, 888–895.10.1158/1078-0432.CCR-10-1706Search in Google Scholar

Ruiz, A.J., and Russell, S.J. (2015). MicroRNAs and oncolytic viruses. Curr. Opin. Virol. 13, 40–48.10.1016/j.coviro.2015.03.007Search in Google Scholar

Russell, S.J. (2002). RNA viruses as virotherapy agents. Cancer Gene Ther. 9, 961–966.10.1038/sj.cgt.7700535Search in Google Scholar

Russell, S.J., Federspiel, M.J., Peng, K.W., Tong, C., Dingli, D., Morice, W.G., Lowe, V., O’Connor, M.K., Kyle, R.A., Leung, N., et al. (2014). Remission of disseminated cancer after systemic oncolytic virotherapy. Mayo Clin. Proc. 89, 926–933.10.1016/j.mayocp.2014.04.003Search in Google Scholar

San Roman, K., Villar, E., and Munoz-Barroso, I. (1999). Acidic pH enhancement of the fusion of Newcastle disease virus with cultured cells. Virology 260, 329–341.10.1006/viro.1999.9841Search in Google Scholar

Sanchez-Felipe, L., Villar, E., and Munoz-Barroso, I. (2014). Entry of Newcastle Disease Virus into the host cell: role of acidic pH and endocytosis. Biochim. Biophys. Acta 1838, 300–309.10.1016/j.bbamem.2013.08.008Search in Google Scholar

Schmitt, B. (2002). Vesicular stomatitis. Vet. Clin. North Am. Food Anim. Pract. 18, 453–9, vii–viii.10.1016/S0749-0720(02)00031-2Search in Google Scholar

Senzer, N.N., Kaufman, H.L., Amatruda, T., Nemunaitis, M., Reid, T., Daniels, G., Gonzalez, R., Glaspy, J., Whitman, E., Harrington, K., et al. (2009). Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J. Clin. Oncol. 27, 5763–5771.10.1200/JCO.2009.24.3675Search in Google Scholar PubMed

Shafren, D.R., Dorahy, D.J., Ingham, R.A., Burns, G.F., and Barry, R.D. (1997). Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. J. Virol. 71, 4736–4743.10.1128/jvi.71.6.4736-4743.1997Search in Google Scholar

Shafren, D.R., Sylvester, D., Johansson, E.S., Campbell, I.G., and Barry, R.D. (2005). Oncolysis of human ovarian cancers by echovirus type 1. Int. J. Cancer 115, 320–328.10.1002/ijc.20866Search in Google Scholar PubMed

Shmulevitz, M., Gujar, S.A., Ahn, D.G., Mohamed, A., and Lee, P.W. (2012). Reovirus variants with mutations in genome segments S1 and L2 exhibit enhanced virion infectivity and superior oncolysis. J. Virol. 86, 7403–7413.10.1128/JVI.00304-12Search in Google Scholar

Singh, P.K., Doley, J., Kumar, G.R., Sahoo, A.P., and Tiwari, A.K. (2012). Oncolytic viruses & their specific targeting to tumour cells. Indian J. Med. Res. 136, 571–584.Search in Google Scholar

Sloan, K.E., Eustace, B.K., Stewart, J.K., Zehetmeier, C., Torella, C., Simeone, M., Roy, J.E., Unger, C., Louis, D.N., Ilag, L.L., et al. (2004). CD155/PVR plays a key role in cell motility during tumor cell invasion and migration. BMC Cancer 4, 73.10.1186/1471-2407-4-73Search in Google Scholar

Staeheli, P., and Pavlovic, J. (1991). Inhibition of vesicular stomatitis virus mRNA synthesis by human MxA protein. J. Virol. 65, 4498–4501.10.1128/jvi.65.8.4498-4501.1991Search in Google Scholar

Steiner, H.H., Bonsanto, M.M., Beckhove, P., Brysch, M., Geletneky, K., Ahmadi, R., Schuele-Freyer, R., Kremer, P., Ranaie, G., Matejic, D., et al. (2004). Antitumor vaccination of patients with glioblastoma multiforme: a pilot study to assess feasibility, safety, and clinical benefit. J. Clin. Oncol. 22, 4272–4281.10.1200/JCO.2004.09.038Search in Google Scholar

Stobart, C.C., and Moore, M.L. (2014). RNA virus reverse genetics and vaccine design. Viruses 6, 2531–2550.10.3390/v6072531Search in Google Scholar

Stojdl, D.F., Lichty, B., Knowles, S., Marius, R., Atkins, H., Sonenberg, N., and Bell, J.C. (2000). Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6, 821–825.10.1038/77558Search in Google Scholar

Stojdl, D.F., Lichty, B.D., tenOever, B.R., Paterson, J.M., Power, A.T., Knowles, S., Marius, R., Reynard, J., Poliquin, L., Atkins, H., et al. (2003). VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer. Cell. 4, 263–275.10.1016/S1535-6108(03)00241-1Search in Google Scholar

Taqi, A.M., Abdurrahman, M.B., Yakubu, A.M., and Fleming, A.F. (1981). Regression of Hodgkin’s disease after measles. Lancet 1, 1112.10.1016/S0140-6736(81)92286-8Search in Google Scholar

Tatsuo, H., Ono, N., Tanaka, K., and Yanagi, Y. (2000). SLAM (CDw150) is a cellular receptor for measles virus. Nature 406, 893–897.10.1038/35022579Search in Google Scholar PubMed

Termeer, C.C., Schirrmacher, V., Brocker, E.B., and Becker, J.C. (2000). Newcastle disease virus infection induces B7-1/B7-2-independent T-cell costimulatory activity in human melanoma cells. Cancer Gene Ther. 7, 316–323.10.1038/sj.cgt.7700109Search in Google Scholar PubMed

Tong, A.W., Senzer, N., Cerullo, V., Templeton, N.S., Hemminki, A., and Nemunaitis, J. (2012). Oncolytic viruses for induction of anti-tumor immunity. Curr. Pharm. Biotechnol. 13, 1750–1760.10.2174/138920112800958913Search in Google Scholar PubMed

Toyoda, H., Yin, J., Mueller, S., Wimmer, E., and Cello, J. (2007). Oncolytic treatment and cure of neuroblastoma by a novel attenuated poliovirus in a novel poliovirus-susceptible animal model. Cancer Res. 67, 2857–2864.10.1158/0008-5472.CAN-06-3713Search in Google Scholar PubMed

van den Wollenberg, D.J., van den Hengel, S.K., Dautzenberg, I.J., Cramer, S.J., Kranenburg, O., and Hoeben, R.C. (2008). A strategy for genetic modification of the spike-encoding segment of human reovirus T3D for reovirus targeting. Gene Ther. 15, 1567–1578.10.1038/gt.2008.118Search in Google Scholar PubMed

van den Wollenberg, D.J., Dautzenberg, I.J., Ros, W., Lipinska, A.D., van den Hengel, S.K., and Hoeben, R.C. (2015). Replicating reoviruses with a transgene replacing the codons for the head domain of the viral spike. Gene Ther. 22, 267–279.10.1038/gt.2014.126Search in Google Scholar PubMed

Venkataraman, S., Reddy, S.P., Loo, J., Idamakanti, N., Hallenbeck, P.L., and Reddy, V.S. (2008). Structure of Seneca Valley virus-001: an oncolytic picornavirus representing a new genus. Structure 16, 1555–1561.10.1016/j.str.2008.07.013Search in Google Scholar PubMed PubMed Central

Vigil, A., Park, M.S., Martinez, O., Chua, M.A., Xiao, S., Cros, J.F., Martinez-Sobrido, L., Woo, S.L., and Garcia-Sastre, A. (2007). Use of reverse genetics to enhance the oncolytic properties of Newcastle disease virus. Cancer Res. 67, 8285–8292.10.1158/0008-5472.CAN-07-1025Search in Google Scholar PubMed

Voutsadakis, I.A. (2016). Immune blockade inhibition in breast cancer. Anticancer Res. 36, 5607–5622.10.21873/anticanres.11145Search in Google Scholar PubMed

Wadhwa, L., Hurwitz, M.Y., Chevez-Barrios, P., and Hurwitz, R.L. (2007). Treatment of invasive retinoblastoma in a murine model using an oncolytic picornavirus. Cancer Res. 67, 10653–10656.10.1158/0008-5472.CAN-07-2352Search in Google Scholar PubMed

Wahid, R., Cannon, M.J., and Chow, M. (2005). Dendritic cells and macrophages are productively infected by poliovirus. J. Virol. 79, 401–409.10.1128/JVI.79.1.401-409.2005Search in Google Scholar PubMed PubMed Central

Wilcox, M.E., Yang, W., Senger, D., Rewcastle, N.B., Morris, D.G., Brasher, P.M., Shi, Z.Q., Johnston, R.N., Nishikawa, S., Lee, P.W., et al. (2001). Reovirus as an oncolytic agent against experimental human malignant gliomas. J. Natl. Cancer Inst. 93, 903–912.10.1093/jnci/93.12.903Search in Google Scholar PubMed

Wild, T.F., Malvoisin, E., and Buckland, R. (1991). Measles virus: both the haemagglutinin and fusion glycoproteins are required for fusion. J. Gen. Virol. 72(Pt 2), 439–442.10.1099/0022-1317-72-2-439Search in Google Scholar PubMed

Wollmann, G., Rogulin, V., Simon, I., Rose, J.K., and van den Pol, A.N. (2010). Some attenuated variants of vesicular stomatitis virus show enhanced oncolytic activity against human glioblastoma cells relative to normal brain cells. J. Virol. 84, 1563–1573.10.1128/JVI.02040-09Search in Google Scholar PubMed PubMed Central

Wollmann, G., Davis, J.N., Bosenberg, M.W., and van den Pol, A.N. (2013). Vesicular stomatitis virus variants selectively infect and kill human melanomas but not normal melanocytes. J. Virol. 87, 6644–6659.10.1128/JVI.03311-12Search in Google Scholar PubMed PubMed Central

Wong, L.H., Krauer, K.G., Hatzinisiriou, I., Estcourt, M.J., Hersey, P., Tam, N.D., Edmondson, S., Devenish, R.J., and Ralph, S.J. (1997). Interferon-resistant human melanoma cells are deficient in ISGF3 components, STAT1, STAT2, and p48-ISGF3gamma. J. Biol. Chem. 272, 28779–28785.10.1074/jbc.272.45.28779Search in Google Scholar PubMed

Wongthida, P., Diaz, R.M., Pulido, C., Rommelfanger, D., Galivo, F., Kaluza, K., Kottke, T., Thompson, J., Melcher, A., and Vile, R. (2011). Activating systemic T-cell immunity against self tumor antigens to support oncolytic virotherapy with vesicular stomatitis virus. Hum. Gene Ther. 22, 1343–1353.10.1089/hum.2010.216Search in Google Scholar PubMed PubMed Central

Xue, W., Chen, S., Yin, H., Tammela, T., Papagiannakopoulos, T., Joshi, N.S., Cai, W., Yang, G., Bronson, R., Crowley, D.G., et al. (2014). CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514, 380–384.10.1038/nature13589Search in Google Scholar PubMed PubMed Central

Yang, H., Wang, H., Shivalila, C.S., Cheng, A.W., Shi, L., and Jaenisch, R. (2013). One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370–1379.10.1016/j.cell.2013.08.022Search in Google Scholar PubMed PubMed Central

Yu, L., Baxter, P.A., Zhao, X., Liu, Z., Wadhwa, L., Zhang, Y., Su, J.M., Tan, X., Yang, J., Adesina, A., et al. (2011). A single intravenous injection of oncolytic picornavirus SVV-001 eliminates medulloblastomas in primary tumor-based orthotopic xenograft mouse models. Neuro Oncol. 13, 14–27.10.1093/neuonc/noq148Search in Google Scholar PubMed PubMed Central

Zamarin, D., and Palese, P. (2012). Oncolytic Newcastle disease virus for cancer therapy: old challenges and new directions. Future Microbiol. 7, 347–367.10.2217/fmb.12.4Search in Google Scholar PubMed PubMed Central

Zamarin, D., Holmgaard, R.B., Subudhi, S.K., Park, J.S., Mansour, M., Palese, P., Merghoub, T., Wolchok, J.D., and Allison, J.P. (2014). Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci. Transl. Med. 6, 226ra32.10.1126/scitranslmed.3008095Search in Google Scholar PubMed PubMed Central

Received: 2017-1-13
Accepted: 2017-4-8
Published Online: 2017-4-25
Published in Print: 2017-7-26

©2017 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 23.1.2026 from https://www.degruyterbrill.com/document/doi/10.1515/hsz-2017-0103/html
Scroll to top button