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

Translational Research

Volumn 161, Issue 4, 2013, Pages 355-364

  Patel, Manish R ^a   Kratzke, Robert A ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AD3 HTERT E1A ONCOLYTIC ADENOVIRUS; AD5 D24 GMCSF ONCOLYTIC ADENOVIRUS; ANTINEOPLASTIC AGENT; CARBOPLATIN; CGTG 401 ONCOLYTIC ADENOVIRUS; CISPLATIN; FLUOROURACIL; G 207; GEMCITABINE; GL ONC1 ONCOLYTIC HERPES VIRUS; GLUCOCORTICOID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; H103 ONCOLYTIC ADENOVIRUS; ICOVIR 7 ONCOLYTIC ADENOVIRUS; JK 594; LONTUCIREV; MV CEA ONCOLYTIC VIRUS; MV NIS ONCOLYTIC VIRUS; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; NV 1020; ONCOLYTIC ADENOVIRUS; ONCOLYTIC VIRUS; PACLITAXEL; PEXASTIMOGENE DEVACIREPVEC; PLATINUM; REOVIRUS TYPE 3 DEARING; SORAFENIB; TACROLIMUS; TALIMOGENE LAHERPAREPVEC; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADENOVIRUS; ADVANCED CANCER; ANTIBODY RESPONSE; ANTIBODY TITER; ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CANCER CELL DESTRUCTION; CANCER COMBINATION CHEMOTHERAPY; CANCER REGRESSION; CHOLESTASIS; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; CUTANEOUS MELANOMA; DIGESTIVE SYSTEM CANCER; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG FEVER; DRUG INDUCED HEADACHE; DRUG MEGADOSE; DRUG SAFETY; ENCEPHALITIS; FLU LIKE SYNDROME; GENE CASSETTE; GENE DELETION; GENE EXPRESSION; GENETIC ENGINEERING; GLIOMA; HEAD AND NECK CANCER; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HERPES SIMPLEX VIRUS; HUMAN; HYPERBILIRUBINEMIA; IMMUNOSUPPRESSIVE TREATMENT; INJECTION SITE ERYTHEMA; LIVER CANCER; LIVER CELL CARCINOMA; LIVER METASTASIS; LIVER TUMOR; MAMMALIAN ORTHOREOVIRUS; MAXIMUM TOLERATED DOSE; MEASLES VIRUS; MELANOMA; MESOTHELIOMA; MULTIPLE CYCLE TREATMENT; MYELOMA; NASOPHARYNX CARCINOMA; NONHUMAN; ONCOLYTIC VIROTHERAPY; OVARY CANCER; OVARY CARCINOMA; OVERALL SURVIVAL; PRIORITY JOURNAL; REOVIRUS; REVIEW; SINGLE DRUG DOSE; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SOLID TUMOR; TRANSLATIONAL RESEARCH; TREATMENT RESPONSE; TUMOR IMMUNITY; TUMOR REGRESSION; UNSPECIFIED SIDE EFFECT; VACCINIA VIRUS; VIRAL GENE DELIVERY SYSTEM; VIRUS ENTRY; VIRUS GENOME; VIRUS INFECTION; VIRUS REPLICATION;

EID: 84875182214     PISSN: 19315244     EISSN: 18781810     Source Type: Journal    
DOI: 10.1016/j.trsl.2012.12.010     Document Type: Review

References (87)

1. R.M. Eager, and J. Nemunaitis Clinical development directions in oncolytic viral therapy Cancer Gene Ther 18 2011 305 317
2. A.M. Hammill, J. Conner, and T.P. Cripe Oncolytic virotherapy reaches adolescence Pediatr Blood Cancer 55 2010 1253 1263
3. C.J. Breitbach, T. Reid, J. Burke, J.C. Bell, and D.H. Kirn Navigating the clinical development landscape for oncolytic viruses and other cancer therapeutics: no shortcuts on the road to approval Cytokine Growth Factor Rev 21 2010 85 89
4. P.A. Vasey, L.N. Shulman, and S. Campos 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 2002 1562 1569
5. E.A. Chiocca, K.M. Abbed, and S. Tatter 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 2004 958 966
6. J. Nemunaitis, F. Khuri, and I. Ganly 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 2001 289 298
7. F.R. Khuri, J. Nemunaitis, and I. Ganly 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 2000 879 885
8. Z.J. Xia, J.H. Chang, and L. Zhang [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 2004 1666 1670
9. N. Somia, and I.M. Verma Gene therapy: trials and tribulations Nat Rev Genet 1 2000 91 99
10. J.T. Douglas, B.E. Rogers, and M.E. Rosenfeld Targeted gene delivery by tropism-modified adenoviral vectors Nat Biotechnol 14 1996 1574 1578
11. R. Rodriguez, E.R. Schuur, and H.Y. Lim Prostate attenuated replication competent adenovirus (ARCA) CN706: a selective cytotoxic for prostate-specific antigen-positive prostate cancer cells Cancer Res 57 1997 2559 2563
12. S. Pesonen, I. Diaconu, and L. Kangasniemi Oncolytic immunotherapy of advanced solid tumors with a CD40L-expressing replicating adenovirus: assessment of safety and immunologic responses in patients Cancer Res 72 2012 1621 1631
13. A. Koski, L. Kangasniemi, and S. Escutenaire Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF Mol Ther 18 2010 1874 1884
14. V. Cerullo, S. Pesonen, and I. Diaconu Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients Cancer Res 70 2010 4297 4309
15. O. Hemminki, I. Diaconu, and V. Cerullo Ad3-hTERT-E1A, a fully serotype 3 oncolytic adenovirus, in patients with chemotherapy refractory cancer Mol Ther 20 2012 1821 1830
16. K.J. Kimball, M.A. Preuss, and M.N. Barnes A phase I study of a tropism-modified conditionally replicative adenovirus for recurrent malignant gynecologic diseases Clin Cancer Res 16 2010 5277 5287
17. P. Nokisalmi, S. Pesonen, and S. Escutenaire Oncolytic adenovirus ICOVIR-7 in patients with advanced and refractory solid tumors Clin Cancer Res 16 2010 3035 3043
18. J.L. Li, H.L. Liu, and X.R. Zhang A phase I trial of intratumoral administration of recombinant oncolytic adenovirus overexpressing HSP70 in advanced solid tumor patients Gene Ther 16 2009 376 382
19. K.D. Smith, J.J. Mezhir, and K. Bickenbach 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 2006 1110 1120
20. M. Aghi, T. Visted, R.A. Depinho, and E.A. Chiocca Oncolytic herpes virus with defective ICP6 specifically replicates in quiescent cells with homozygous genetic mutations in p16 Oncogene 27 2008 4249 4254
21. J.M. Markert, M.D. Medlock, and S.D. Rabkin Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial Gene Ther 7 2000 867 874
22. J.M. Markert, P.G. Liechty, and W. Wang Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM Mol Ther 17 2009 199 207
23. N. Kemeny, K. Brown, and A. Covey 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 2006 1214 1224
24. S.K. Geevarghese, D.A. Geller, and H.A. de Haan 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 2010 1119 1128
25. J.C. Hu, R.S. Coffin, and C.J. Davis A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor Clin Cancer Res 12 2006 6737 6747
26. H.L. Kaufman, D.W. Kim, and G. DeRaffele 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 2010 718 730
27. N.N. Senzer, H.L. Kaufman, and T. Amatruda 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 2009 5763 5771
28. H.L. Kaufman, and S.D. Bines OPTIM trial: a phase III trial of an oncolytic herpes virus encoding GM-CSF for unresectable stage III or IV melanoma Future Oncol 6 2010 941 949
29. K.J. Harrington, M. Hingorani, and M.A. Tanay 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 2010 4005 4015
30. T.H. Hwang, A. Moon, and J. Burke A mechanistic proof-of-concept clinical trial with JX-594, a targeted multi-mechanistic oncolytic poxvirus, in patients with metastatic melanoma Mol Ther 19 2011 1913 1922
31. C.J. Breitbach, J. Burke, and D. Jonker Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans Nature 477 2011 99 102
32. B.H. Park, T. Hwang, and T.C. Liu Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial Lancet Oncol 9 2008 533 542
33. T.C. Liu, T. Hwang, B.H. Park, J. Bell, and D.H. Kirn The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma Mol Ther 16 2008 1637 1642
34. J. Heo, C.J. Breitbach, and A. Moon 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 2011 1170 1179
35. D.G. Morris, X. Feng, and L.M. Difrancesco 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 2012 [Epub ahead of print]
36. L. Vidal, H.S. Pandha, and T.A. Yap A phase I study of intravenous oncolytic reovirus type 3 Dearing in patients with advanced cancer Clin Cancer Res 14 2008 7127 7137
37. E.M. Karapanagiotou, V. Roulstone, and K. Twigger Phase I/II trial of carboplatin and paclitaxel chemotherapy in combination with intravenous oncolytic reovirus in patients with advanced malignancies Clin Cancer Res 18 2012 2080 2089
38. M.P. Lolkema, H.T. Arkenau, and K. Harrington A phase I study of the combination of intravenous reovirus type 3 Dearing and gemcitabine in patients with advanced cancer Clin Cancer Res 17 2011 581 588
39. C. Comins, J. Spicer, and A. Protheroe REO-10: a phase I study of intravenous reovirus and docetaxel in patients with advanced cancer Clin Cancer Res 16 2010 5564 5572
40. A.M. Taqi, M.B. Abdurrahman, A.M. Yakubu, and A.F. Fleming Regression of Hodgkin's disease after measles Lancet 1 1981 1112
41. S. Gross Measles and leukemia Lancet 1 1971 397 398
42. G. Pasquinucci Possible effect of measles on leukemia Lancet 1 1971 136
43. Z. Zygiert Hodgkin's disease: remissions after measles Lancet 1 1971 593
44. D. Griffin, and W. Bellini Measles virus D. Knipe, P. Howley, Fields virology 2001 Lippencott Williams & Wilkins Philadelphia 1401 1441
45. R.S. Noyce, and C.D. Richardson Nectin 4 is the epithelial cell receptor for measles virus Trends Microbiol 20 2012 429 439
46. M.D. Muhlebach, M. Mateo, and P.L. Sinn Adherens junction protein nectin-4 is the epithelial receptor for measles virus Nature 480 2011 530 533
47. S. Fabre-Lafay, F. Monville, and S. Garrido-Urbani Nectin-4 is a new histological and serological tumor associated marker for breast cancer BMC Cancer 7 2007 73
48. A. Takano, N. Ishikawa, and R. Nishino Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer Cancer Res 69 2009 6694 6703
49. M.S. Derycke, S.E. Pambuccian, and C.B. Gilks Nectin 4 overexpression in ovarian cancer tissues and serum: potential role as a serum biomarker Am J Clin Pathol 134 2010 835 845
50. D. Dingli, K.W. Peng, and M.E. Harvey Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter Blood 103 2004 1641 1646
51. D. Grote, S.J. Russell, and T.I. Cornu Live attenuated measles virus induces regression of human lymphoma xenografts in immunodeficient mice Blood 97 2001 3746 3754
52. K. Hasegawa, L. Pham, and M.K. O'Connor Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter Clin Cancer Res 12 2006 1868 1875
53. H. Li, K.W. Peng, D. Dingli, R.A. Kratzke, and S.J. Russell Oncolytic measles viruses encoding interferon beta and the thyroidal sodium iodide symporter gene for mesothelioma virotherapy Cancer Gene Ther 17 2010 550 558
54. C.J. McDonald, C. Erlichman, and J.N. Ingle A measles virus vaccine strain derivative as a novel oncolytic agent against breast cancer Breast Cancer ResTreat 99 2006 177 184
55. P. Msaouel, I.D. Iankov, and C. Allen Engineered measles virus as a novel oncolytic therapy against prostate cancer Prostate 69 2009 82 91
56. K.W. Peng, C.J. TenEyck, and E. Galanis Intraperitoneal therapy of ovarian cancer using an engineered measles virus Cancer Res 62 2002 4656 4662
57. L.K. Phuong, C. Allen, and K.W. Peng 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 2003 2462 2469
58. E. Galanis, L.C. Hartmann, and W.A. Cliby Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer Cancer Res 70 2010 875 882
59. M. Markman, K. Webster, and K. Zanotti Phase 2 trial of carboplatin plus tamoxifen in platinum-resistant ovarian cancer and primary carcinoma of the peritoneum Gynecol Oncol 94 2004 404 408
60. M. Markman, K. Webster, and K. Zanotti 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 2004 699 701
61. A. Gauvrit, S. Brandler, and C. Sapede-Peroz Measles virus induces oncolysis of mesothelioma cells and allows dendritic cells to cross-prime tumor-specific CD8 response Cancer Research 68 2008 4882 4892
62. O.G. Donnelly, F. Errington-Mais, and L. Steele Measles virus causes immunogenic cell death in human melanoma Gene Ther 20 2013 7 15
63. R.M. Myers, S.M. Greiner, and M.E. Harvey Preclinical pharmacology and toxicology of intravenous MV-NIS, an oncolytic measles virus administered with or without cyclophosphamide Clin Pharmacol Ther 82 2007 700 710
64. K.W. Peng, R. Myers, and A. Greenslade Using clinically approved cyclophosphamide regimens to control the humoral immune response to oncolytic viruses Gene Ther 2012 [Epub ahead of print]
65. J. Qiao, H. Wang, and T. Kottke Cyclophosphamide facilitates antitumor efficacy against subcutaneous tumors following intravenous delivery of reovirus Clin Cancer Res 14 2008 259 269
66. X.Q. Lun, J.H. Jang, and N. Tang Efficacy of systemically administered oncolytic vaccinia virotherapy for malignant gliomas is enhanced by combination therapy with rapamycin or cyclophosphamide Clin Cancer Res 15 2009 2777 2788
67. V. Cerullo, I. Diaconu, and L. Kangasniemi Immunological effects of low-dose cyclophosphamide in cancer patients treated with oncolytic adenovirus Mol Ther 19 2011 1737 1746
68. Z.S. Guo, V. Parimi, and M.E. O'Malley The combination of immunosuppression and carrier cells significantly enhances the efficacy of oncolytic poxvirus in the pre-immunized host Gene Ther 17 2010 1465 1475
69. F. Mingozzi, Y. Chen, and S.C. Edmonson Prevalence and pharmacological modulation of humoral immunity to AAV vectors in gene transfer to synovial tissue Gene Ther 2012
70. F. Mingozzi, Y. Chen, and S.L. Murphy Pharmacological modulation of humoral immunity in a nonhuman primate model of AAV gene transfer for hemophilia B Mol Ther 20 2012 1410 1416
71. A.T. Power, J. Wang, and T.J. Falls Carrier cell-based delivery of an oncolytic virus circumvents antiviral immunity Mol Ther 15 2007 123 130
72. A. Munguia, T. Ota, T. Miest, and S.J. Russell Cell carriers to deliver oncolytic viruses to sites of myeloma tumor growth Gene Ther 15 2008 797 806
73. G. Coukos, A. Makrigiannakis, and E.H. Kang 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 1999 1523 1537
74. E.J. Ilett, R.J. Prestwich, and T. Kottke Dendritic cells and T cells deliver oncolytic reovirus for tumour killing despite pre-existing anti-viral immunity Gene Ther 16 2009 689 699
75. S.H. Thorne, W. Liang, and P. Sampath Targeting localized immune suppression within the tumor through repeat cycles of immune cell-oncolytic virus combination therapy Mol Ther 18 2010 1698 1705
76. E.K. Mader, Y. Maeyama, and Y. Lin Mesenchymal stem cell carriers protect oncolytic measles viruses from antibody neutralization in an orthotopic ovarian cancer therapy model Clin Cancer Res 15 2009 7246 7255
77. J. Wei, J. Wahl, and T. Nakamura Targeted release of oncolytic measles virus by blood outgrowth endothelial cells in situ inhibits orthotopic gliomas Gene Ther 14 2007 1573 1586
78. T. Kottke, R.M. Diaz, and K. Kaluza Use of biological therapy to enhance both virotherapy and adoptive T-cell therapy for cancer Mol Ther 16 2008 1910 1918
79. A.Z. Dudek Endothelial lineage cell as a vehicle for systemic delivery of cancer gene therapy Transl Res 156 2010 136 146
80. V. Bodempudi, J.R. Ohlfest, and K. Terai Blood outgrowth endothelial cell-based systemic delivery of antiangiogenic gene therapy for solid tumors Cancer Gene Ther 17 2010 855 863
81. A.U. Ahmed, C.E. Rolle, and M.A. Tyler Bone marrow mesenchymal stem cells loaded with an oncolytic adenovirus suppress the anti-adenoviral immune response in the cotton rat model Mol Ther 18 2010 1846 1856
82. J. Garcia-Castro, R. Alemany, and M. Cascallo Treatment of metastatic neuroblastoma with systemic oncolytic virotherapy delivered by autologous mesenchymal stem cells: an exploratory study Cancer Gene Ther 17 2010 476 483
83. R.L. Yong, N. Shinojima, and J. Fueyo Human bone marrow-derived mesenchymal stem cells for intravascular delivery of oncolytic adenovirus Delta24-RGD to human gliomas Cancer Res 69 2009 8932 8940
84. R.M. Diaz, F. Galivo, and T. Kottke Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus Cancer Res 67 2007 2840 2848
85. C.L. Willmon, V. Saloura, and Z.G. Fridlender Expression of IFN-beta enhances both efficacy and safety of oncolytic vesicular stomatitis virus for therapy of mesothelioma Cancer Res 69 2009 7713 7720
86. H. Li, K.W. Peng, D. Dingli, R.A. Kratzke, and S.J. Russell Oncolytic measles viruses encoding interferon beta and the thyroidal sodium iodide symporter gene for mesothelioma virotherapy Cancer Gene Ther 17 2010 550 558
87. F.S. Hodi, S.J. O'Day, and D.F. McDermott Improved survival with ipilimumab in patients with metastatic melanoma N Engl J Med 363 2010 711 723