Oncolytic virus therapy for cancer: the first wave of translational clinical trials

Eager, 2011, Clinical development directions in oncolytic viral therapy, Cancer Gene Ther, 18, 305, 10.1038/cgt.2011.7 Hammill, 2010, Oncolytic virotherapy reaches adolescence, Pediatr Blood Cancer, 55, 1253, 10.1002/pbc.22724 Breitbach, 2010, Navigating the clinical development landscape for oncolytic viruses and other cancer therapeutics: no shortcuts on the road to approval, Cytokine Growth Factor Rev, 21, 85, 10.1016/j.cytogfr.2010.02.001 Vasey, 2002, Phase I trial of intraperitoneal injection of the E1B-55-kd-gene-deleted adenovirus ONYX-015 (dl1520) given on days 1 through 5 every 3 weeks in patients with recurrent/refractory epithelial ovarian cancer, J Clin Oncol, 20, 1562, 10.1200/JCO.20.6.1562 Chiocca, 2004, A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting, Mol Ther, 10, 958, 10.1016/j.ymthe.2004.07.021 Nemunaitis, 2001, Phase II trial of intratumoral administration of ONYX-015, a replication-selective adenovirus, in patients with refractory head and neck cancer, J Clin Oncol, 19, 289, 10.1200/JCO.2001.19.2.289 Khuri, 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, 10.1038/78638 Xia, 2004, [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, 23, 1666 Somia, 2000, Gene therapy: trials and tribulations, Nat Rev Genet, 1, 91, 10.1038/35038533 Douglas, 1996, Targeted gene delivery by tropism-modified adenoviral vectors, Nat Biotechnol, 14, 1574, 10.1038/nbt1196-1574 Rodriguez, 1997, Prostate attenuated replication competent adenovirus (ARCA) CN706: a selective cytotoxic for prostate-specific antigen-positive prostate cancer cells, Cancer Res, 57, 2559 Pesonen, 2012, Oncolytic immunotherapy of advanced solid tumors with a CD40L-expressing replicating adenovirus: assessment of safety and immunologic responses in patients, Cancer Res, 72, 1621, 10.1158/0008-5472.CAN-11-3001 Koski, 2010, Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF, Mol Ther, 18, 1874, 10.1038/mt.2010.161 Cerullo, 2010, Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients, Cancer Res, 70, 4297, 10.1158/0008-5472.CAN-09-3567 Hemminki, 2012, Ad3-hTERT-E1A, a fully serotype 3 oncolytic adenovirus, in patients with chemotherapy refractory cancer, Mol Ther, 20, 1821, 10.1038/mt.2012.115 Kimball, 2010, A phase I study of a tropism-modified conditionally replicative adenovirus for recurrent malignant gynecologic diseases, Clin Cancer Res, 16, 5277, 10.1158/1078-0432.CCR-10-0791 Nokisalmi, 2010, Oncolytic adenovirus ICOVIR-7 in patients with advanced and refractory solid tumors, Clin Cancer Res, 16, 3035, 10.1158/1078-0432.CCR-09-3167 Li, 2009, A phase I trial of intratumoral administration of recombinant oncolytic adenovirus overexpressing HSP70 in advanced solid tumor patients, Gene Ther, 16, 376, 10.1038/gt.2008.179 Smith, 2006, 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, 80, 1110, 10.1128/JVI.80.3.1110-1120.2006 Aghi, 2008, Oncolytic herpes virus with defective ICP6 specifically replicates in quiescent cells with homozygous genetic mutations in p16, Oncogene, 27, 4249, 10.1038/onc.2008.53 Markert, 2000, Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial, Gene Ther, 7, 867, 10.1038/sj.gt.3301205 Markert, 2009, Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM, Mol Ther, 17, 199, 10.1038/mt.2008.228 Kemeny, 2006, Phase I, open-label, dose-escalating study of a genetically engineered herpes simplex virus, NV1020, in subjects with metastatic colorectal carcinoma to the liver, Hum Gene Ther, 17, 1214, 10.1089/hum.2006.17.1214 Geevarghese, 2010, Phase I/II study of oncolytic herpes simplex virus NV1020 in patients with extensively pretreated refractory colorectal cancer metastatic to the liver, Hum Gene Ther, 21, 1119, 10.1089/hum.2010.020 Hu, 2006, A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor, Clin Cancer Res, 12, 6737, 10.1158/1078-0432.CCR-06-0759 Kaufman, 2010, Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage IIIc and IV melanoma, Ann Surg Oncol, 17, 718, 10.1245/s10434-009-0809-6 Senzer, 2009, Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpes virus in patients with unresectable metastatic melanoma, J Clin Oncol, 27, 5763, 10.1200/JCO.2009.24.3675 Kaufman, 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, 10.2217/fon.10.66 Harrington, 2010, Phase I/II study of oncolytic HSV GM-CSF in combination with radiotherapy and cisplatin in untreated stage III/IV squamous cell cancer of the head and neck, Clin Cancer Res, 16, 4005, 10.1158/1078-0432.CCR-10-0196 Hwang, 2011, A mechanistic proof-of-concept clinical trial with JX-594, a targeted multi-mechanistic oncolytic poxvirus, in patients with metastatic melanoma, Mol Ther, 19, 1913, 10.1038/mt.2011.132 Breitbach, 2011, Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans, Nature, 477, 99, 10.1038/nature10358 Park, 2008, Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial, Lancet Oncol, 9, 533, 10.1016/S1470-2045(08)70107-4 Liu, 2008, The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma, Mol Ther, 16, 1637, 10.1038/mt.2008.143 Heo, 2011, Sequential therapy with JX-594, a targeted oncolytic poxvirus, followed by sorafenib in hepatocellular carcinoma: preclinical and clinical demonstration of combination efficacy, Mol Ther, 19, 1170, 10.1038/mt.2011.39 Morris, 2012, 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, 10.1007/s10637-012-9865-z Vidal, 2008, A phase I study of intravenous oncolytic reovirus type 3 Dearing in patients with advanced cancer, Clin Cancer Res, 14, 7127, 10.1158/1078-0432.CCR-08-0524 Karapanagiotou, 2012, Phase I/II trial of carboplatin and paclitaxel chemotherapy in combination with intravenous oncolytic reovirus in patients with advanced malignancies, Clin Cancer Res, 18, 2080, 10.1158/1078-0432.CCR-11-2181 Lolkema, 2011, A phase I study of the combination of intravenous reovirus type 3 Dearing and gemcitabine in patients with advanced cancer, Clin Cancer Res, 17, 581, 10.1158/1078-0432.CCR-10-2159 Comins, 2010, REO-10: a phase I study of intravenous reovirus and docetaxel in patients with advanced cancer, Clin Cancer Res, 16, 5564, 10.1158/1078-0432.CCR-10-1233 Taqi, 1981, Regression of Hodgkin's disease after measles, Lancet, 1, 1112, 10.1016/S0140-6736(81)92286-8 Gross, 1971, Measles and leukemia, Lancet, 1, 397, 10.1016/S0140-6736(71)92232-X Pasquinucci, 1971, Possible effect of measles on leukemia, Lancet, 1, 136, 10.1016/S0140-6736(71)90869-5 Zygiert, 1971, Hodgkin’s disease: remissions after measles, Lancet, 1, 593, 10.1016/S0140-6736(71)91186-X Griffin, 2001, Measles virus, 1401 Noyce, 2012, Nectin 4 is the epithelial cell receptor for measles virus, Trends Microbiol, 20, 429, 10.1016/j.tim.2012.05.006 Muhlebach, 2011, Adherens junction protein nectin-4 is the epithelial receptor for measles virus, Nature, 480, 530, 10.1038/nature10639 Fabre-Lafay, 2007, Nectin-4 is a new histological and serological tumor associated marker for breast cancer, BMC Cancer, 7, 73, 10.1186/1471-2407-7-73 Takano, 2009, Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer, Cancer Res, 69, 6694, 10.1158/0008-5472.CAN-09-0016 Derycke, 2010, Nectin 4 overexpression in ovarian cancer tissues and serum: potential role as a serum biomarker, Am J Clin Pathol, 134, 835, 10.1309/AJCPGXK0FR4MHIHB Dingli, 2004, Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter, Blood, 103, 1641, 10.1182/blood-2003-07-2233 Grote, 2001, Live attenuated measles virus induces regression of human lymphoma xenografts in immunodeficient mice, Blood, 97, 3746, 10.1182/blood.V97.12.3746 Hasegawa, 2006, Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter, Clin Cancer Res, 12, 1868, 10.1158/1078-0432.CCR-05-1803 Li, 2010, Oncolytic measles viruses encoding interferon beta and the thyroidal sodium iodide symporter gene for mesothelioma virotherapy, Cancer Gene Ther, 17, 550, 10.1038/cgt.2010.10 McDonald, 2006, A measles virus vaccine strain derivative as a novel oncolytic agent against breast cancer, Breast Cancer ResTreat, 99, 177, 10.1007/s10549-006-9200-5 Msaouel, 2009, Engineered measles virus as a novel oncolytic therapy against prostate cancer, Prostate, 69, 82, 10.1002/pros.20857 Peng, 2002, Intraperitoneal therapy of ovarian cancer using an engineered measles virus, Cancer Res, 62, 4656 Phuong, 2003, Use of a vaccine strain of measles virus genetically engineered to produce carcinoembryonic antigen as a novel therapeutic agent against glioblastoma multiform, Cancer Res, 63, 2462 Galanis, 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, 10.1158/0008-5472.CAN-09-2762 Markman, 2004, Phase 2 trial of carboplatin plus tamoxifen in platinum-resistant ovarian cancer and primary carcinoma of the peritoneum, Gynecol Oncol, 94, 404, 10.1016/j.ygyno.2004.05.004 Markman, 2004, Survival following the documentation of platinum and taxane resistance in ovarian cancer: a single institution experience involving multiple phase 2 clinical trials, Gynecol Oncol, 93, 699, 10.1016/j.ygyno.2004.03.023 Gauvrit, 2008, Measles virus induces oncolysis of mesothelioma cells and allows dendritic cells to cross-prime tumor-specific CD8 response, Cancer Research, 68, 4882, 10.1158/0008-5472.CAN-07-6265 Donnelly, 2013, Measles virus causes immunogenic cell death in human melanoma, Gene Ther, 20, 7, 10.1038/gt.2011.205 Myers, 2007, Preclinical pharmacology and toxicology of intravenous MV-NIS, an oncolytic measles virus administered with or without cyclophosphamide, Clin Pharmacol Ther, 82, 700, 10.1038/sj.clpt.6100409 Peng, 2012, Using clinically approved cyclophosphamide regimens to control the humoral immune response to oncolytic viruses, Gene Ther Qiao, 2008, Cyclophosphamide facilitates antitumor efficacy against subcutaneous tumors following intravenous delivery of reovirus, Clin Cancer Res, 14, 259, 10.1158/1078-0432.CCR-07-1510 Lun, 2009, Efficacy of systemically administered oncolytic vaccinia virotherapy for malignant gliomas is enhanced by combination therapy with rapamycin or cyclophosphamide, Clin Cancer Res, 15, 2777, 10.1158/1078-0432.CCR-08-2342 Cerullo, 2011, Immunological effects of low-dose cyclophosphamide in cancer patients treated with oncolytic adenovirus, Mol Ther, 19, 1737, 10.1038/mt.2011.113 Guo, 2010, The combination of immunosuppression and carrier cells significantly enhances the efficacy of oncolytic poxvirus in the pre-immunized host, Gene Ther, 17, 1465, 10.1038/gt.2010.104 Mingozzi, 2012, Prevalence and pharmacological modulation of humoral immunity to AAV vectors in gene transfer to synovial tissue, Gene Ther, 10.1038/gt.2012.55 Mingozzi, 2012, Pharmacological modulation of humoral immunity in a nonhuman primate model of AAV gene transfer for hemophilia B, Mol Ther, 20, 1410, 10.1038/mt.2012.84 Power, 2007, Carrier cell-based delivery of an oncolytic virus circumvents antiviral immunity, Mol Ther, 15, 123, 10.1038/sj.mt.6300039 Munguia, 2008, Cell carriers to deliver oncolytic viruses to sites of myeloma tumor growth, Gene Ther, 15, 797, 10.1038/gt.2008.45 Coukos, 1999, Use of carrier cells to deliver a replication-selective herpes simplex virus-1 mutant for the intraperitoneal therapy of epithelial ovarian cancer, Clin Cancer Res, 5, 1523 Ilett, 2009, Dendritic cells and T cells deliver oncolytic reovirus for tumour killing despite pre-existing anti-viral immunity, Gene Ther, 16, 689, 10.1038/gt.2009.29 Thorne, 2010, Targeting localized immune suppression within the tumor through repeat cycles of immune cell-oncolytic virus combination therapy, Mol Ther, 18, 1698, 10.1038/mt.2010.140 Mader, 2009, Mesenchymal stem cell carriers protect oncolytic measles viruses from antibody neutralization in an orthotopic ovarian cancer therapy model, Clin Cancer Res, 15, 7246, 10.1158/1078-0432.CCR-09-1292 Wei, 2007, Targeted release of oncolytic measles virus by blood outgrowth endothelial cells in situ inhibits orthotopic gliomas, Gene Ther, 14, 1573, 10.1038/sj.gt.3303027 Kottke, 2008, Use of biological therapy to enhance both virotherapy and adoptive T-cell therapy for cancer, Mol Ther, 16, 1910, 10.1038/mt.2008.212 Dudek, 2010, Endothelial lineage cell as a vehicle for systemic delivery of cancer gene therapy, Transl Res, 156, 136, 10.1016/j.trsl.2010.07.003 Bodempudi, 2010, Blood outgrowth endothelial cell-based systemic delivery of antiangiogenic gene therapy for solid tumors, Cancer Gene Ther, 17, 855, 10.1038/cgt.2010.42 Ahmed, 2010, Bone marrow mesenchymal stem cells loaded with an oncolytic adenovirus suppress the anti-adenoviral immune response in the cotton rat model, Mol Ther, 18, 1846, 10.1038/mt.2010.131 Garcia-Castro, 2010, Treatment of metastatic neuroblastoma with systemic oncolytic virotherapy delivered by autologous mesenchymal stem cells: an exploratory study, Cancer Gene Ther, 17, 476, 10.1038/cgt.2010.4 Yong, 2009, Human bone marrow-derived mesenchymal stem cells for intravascular delivery of oncolytic adenovirus Delta24-RGD to human gliomas, Cancer Res, 69, 8932, 10.1158/0008-5472.CAN-08-3873 Diaz, 2007, Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus, Cancer Res, 67, 2840, 10.1158/0008-5472.CAN-06-3974 Willmon, 2009, Expression of IFN-beta enhances both efficacy and safety of oncolytic vesicular stomatitis virus for therapy of mesothelioma, Cancer Res, 69, 7713, 10.1158/0008-5472.CAN-09-1013 Li, 2010, Oncolytic measles viruses encoding interferon beta and the thyroidal sodium iodide symporter gene for mesothelioma virotherapy, Cancer Gene Ther, 17, 550, 10.1038/cgt.2010.10 Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N Engl J Med, 363, 711, 10.1056/NEJMoa1003466