The emerging role of viruses in the treatment of solid tumours

Cancer Treatment Reviews

Volumn 37, Issue 8, 2011, Pages 618-632

  Bourke, M G ^a   Salwa, S ^a   Harrington, K J ^b   Kucharczyk, M J ^a   Forde, P F ^a   de Kruijf, M ^a   Soden, D ^a   Tangney, M ^a   Collins, J K ^c   O'Sullivan, G C ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Gene therapy; HSV 1716; Immunotherapy; Multimodal therapy; Oncolytic virotherapy; ONYX 015; Reovirus; Viral oncolysis; Viral vectors for gene therapy

Indexed keywords

ANTINEOPLASTIC AGENT; CARCINOEMBRYONIC ANTIGEN; CG 7870; CV 706; CYCLOPHOSPHAMIDE; CYTOCHROME P450; CYTOSINE DEAMINASE; FLUOROURACIL; FOLINIC ACID; G 207; GAMMA INTERFERON; GANCICLOVIR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HF 10; HSV 1716; INTERLEUKIN 12; INTERLEUKIN 2; JX 594; MEMBRANE COFACTOR PROTEIN; NV 1020; ONCOLYTIC PARVOVIRUS; ONYX 015; PROTEIN P53; PV 701; RIBONUCLEOTIDE REDUCTASE; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; THYMIDINE KINASE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VACCINIA ONCOLYSATE; VIROTHERAPY AGENT;

ADENOVIRUS; ANTINEOPLASTIC ACTIVITY; BLADDER CANCER; BRONCHUS CANCER; CANCER GENE THERAPY; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CELL DEATH; CHEMORADIOTHERAPY; COLORECTAL CANCER; CYTOKINE PRODUCTION; CYTOLYSIS; DENDRITIC CELL; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG POTENTIATION; DRUG SAFETY; DRUG SELECTIVITY; ESOPHAGUS CANCER; GASTROINTESTINAL TUMOR; GENE DIRECTED ENZYME PRODRUG THERAPY; GENE EXPRESSION; GLIOMA; HEAD AND NECK CARCINOMA; HEAD AND NECK TUMOR; HEPATOBILIARY SYSTEM CANCER; HERPES SIMPLEX VIRUS 1; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOSURVEILLANCE; LIVER CANCER; LIVER METASTASIS; LUNG NON SMALL CELL CANCER; MEASLES VIRUS; MELANOMA; MOUTH CANCER; MULTIMODALITY CANCER THERAPY; MULTIPLE CYCLE TREATMENT; NASOPHARYNX CARCINOMA; NEWCASTLE DISEASE PARAMYXOVIRUS; NONHUMAN; ONCOLYTIC VIROTHERAPY; OROPHARYNX CANCER; OVARY CANCER; PANCREAS CANCER; PARVOVIRUS; PERITONEUM METASTASIS; POLIOMYELITIS VIRUS; PROSTATE CANCER; REGULATORY T LYMPHOCYTE; REOVIRUS; REVIEW; SINDBIS VIRUS; SINGLE DRUG DOSE; SKIN METASTASIS; SKIN TUMOR; SOLID TUMOR; SQUAMOUS CELL CARCINOMA; TRANSGENE; TRANSITIONAL CELL CARCINOMA; TUMOR MICROENVIRONMENT; UNSPECIFIED SIDE EFFECT; UPREGULATION; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS; VIRUS INFECTION; VIRUS PARTICLE; VIRUS REPLICATION;

CLINICAL TRIALS AS TOPIC; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; VIRUSES;

EID: 80054064202     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2010.12.003     Document Type: Review

References (193)

1. Kelly E., Russell S.J. History of oncolytic viruses: genesis to genetic engineering. Mol Ther 2007, 15:651-659.
2. Karim-Kos H.E., de Vries E., Soerjomataram I., Lemmens V., Siesling S., Coebergh J.W. Recent trends of cancer in Europe: a combined approach of incidence, survival and mortality for 17 cancer sites since the 1990s. Eur J Cancer 2008, 44:1345-1389.
3. Welch H.G., Schwartz L.M., Woloshin S. Are increasing 5-year survival rates evidence of success against cancer?. JAMA 2000, 283:2975-2978.
4. Qiu D., Kurosawa M., Lin Y., Inaba Y., Matsuba T., Kikuchi S., et al. Overview of the epidemiology of pancreatic cancer focusing on the JACC Study. J Epidemiol 2005, 15(Suppl. 2):S157-S167.
5. de Vries E., Houterman S., Janssen-Heijnen M.L., Nijsten T., van de Schans S.A., Eggermont A.M., et al. Up-to-date survival estimates and historical trends of cutaneous malignant melanoma in the south-east of The Netherlands. Ann Oncol 2007, 18:1110-1116.
6. Elit L., Bondy S.J., Chen Z., Paszat L. A tale of two time periods: ovarian cancer trends in Ontario. Curr Oncol 2007, 14:57-60.
7. Glass A.G., Lacey J.V., Carreon J.D., Hoover R.N. Breast cancer incidence, 1980-2006: combined roles of menopausal hormone therapy, screening mammography, and estrogen receptor status. J Natl Cancer Inst 2007, 99:1152-1161.
8. Hakama M., Coleman M.P., Alexe D.M., Auvinen A. Cancer screening: evidence and practice in Europe 2008. Eur J Cancer 2008, 44:1404-1413.
9. Voltz E., Gronemeyer H. A new era of cancer therapy: cancer cell targeted therapies are coming of age. Int J Biochem Cell Biol 2008, 40:1-8.
10. Giaccone G. Clinical impact of novel treatment strategies. Oncogene 2002, 21:6970-6981.
11. Dock G. The influence of complicating diseases upon leukemia. Am J Med Sci 1904, 127:563-592.
12. DePace N.G. Sulla scomparsa di un enorme cancro vegetante del callo dell'utero senza cura chirurgica. Ginecologica 1912, 9:82.
13. Coley W.B. The treatment of malignant tumors by repeated inoculations of erysipelas: with a report of ten original cases. Am J Med Sci 1893, 105:487-511.
14. Moore A.E. The destructive effects of the virus of Russian Far East encephalitis on the transplantable mouse sarcoma 180. Cancer 1949, 2:525-534.
15. Moore A. Inhibition of growth of five transplantable mouse tumours by the virus of Russian far east encephalitis. Cancer 1951, 4:375-382.
16. Russell S.J., Peng K.W. Viruses as anticancer drugs. Trends Pharmacol Sci 2007, 28:326-333.
17. Vaha-Koskela M.J., Heikkila J.E., Hinkkanen A.E. Oncolytic viruses in cancer therapy. Cancer Lett 2007, 254:178-216.
18. Garber K. China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst 2006, 98:298-300.
19. Gomez-Navarro J., Curiel D.T. Conditionally replicative adenoviral vectors for cancer gene therapy. Lancet Oncol 2000, 1:148-158.
20. Abril E., Mendez R.E., Garcia A., Serrano A., Cabrera T., Garrido F., et al. Characterization of a gastric tumor cell line defective in MHC class I inducibility by both alpha- and gamma-interferon. Tissue Antigens 1996, 47:391-398.
21. Wong L.H., Krauer K.G., Hatzinisiriou I., Estcourt M.J., Hersey P., Tam N.D., et al. Interferon-resistant human melanoma cells are deficient in ISGF3 components, STAT1, STAT2, and p48-ISGF3gamma. J Biol Chem 1997, 272:28779-28785.
22. Huang P.I., Chang J.F., Kirn D.H., Liu T.C. Targeted genetic and viral therapy for advanced head and neck cancers. Drug Discov Today 2009, 14:570-578.
23. Seth P. Vector-mediated cancer gene therapy: an overview. Cancer Biol Ther 2005, 4:512-517.
24. Liu T.C., Kirn D. Systemic efficacy with oncolytic virus therapeutics: clinical proof-of-concept and future directions. Cancer Res 2007, 67:429-432.
25. Pandha H., Melcher A., Harrington K., Vile R. Oncolytic viruses: time to compare, contrast, and combine? 5th international meeting on replicating oncolytic virus therapeutics. Banff, Alberta, Canada, 18-22 March 2009. Mol Ther 2009, 17:934-935.
26. Aghi M., Martuza R.L. Oncolytic viral therapies - the clinical experience. Oncogene 2005, 24:7802-7816.
27. Alvarez R.D., Gomez-Navarro J., Wang M., Barnes M.N., Strong T.V., Arani R.B., et al. Adenoviral-mediated suicide gene therapy for ovarian cancer. Mol Ther 2000, 2:524-530.
28. Vile R., Ando D., Kirn D. The oncolytic virotherapy treatment platform for cancer: unique biological and biosafety points to consider. Cancer Gene Ther 2002, 9:1062-1067.
29. Hawkins L.K., Lemoine N.R., Kirn D. Oncolytic biotherapy: a novel therapeutic plafform. Lancet Oncol 2002, 3:17-26.
30. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003, 63:5821-5828.
31. Jordan C.T., Guzman M.L., Noble M. Cancer stem cells. N Engl J Med 2006, 355:1253-1261.
32. Kim C.F., Jackson E.L., Woolfenden A.E., Lawrence S., Babar I., Vogel S., et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005, 121:823-835.
33. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988.
34. Jones R.J., Matsui W.H., Smith B.D. Cancer stem cells: are we missing the target?. J Natl Cancer Inst 2004, 96:583-585.
35. Huff C.A., Matsui W.H., Douglas Smith B., Jones R.J. Strategies to eliminate cancer stem cells: clinical implications. Eur J Cancer 2006, 42:1293-1297.
36. Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5:275-284.
37. Short J.J., Curiel D.T. Oncolytic adenoviruses targeted to cancer stem cells. Mol Cancer Ther 2009, 8:2096-2102.
38. Cripe T.P., Wang P.Y., Marcato P., Mahller Y.Y., Lee P.W. Targeting cancer-initiating cells with oncolytic viruses. Mol Ther 2009, 17:1677-1682.
39. Marcato P., Dean C.A., Giacomantonio C.A., Lee P.W. Oncolytic reovirus effectively targets breast cancer stem cells. Mol Ther 2009, 17:972-979.
40. Mahller Y.Y., Williams J.P., Baird W.H., Mitton B., Grossheim J., Saeki Y., et al. PLoS One 2009, 4:e4235.
41. Whiteside T.L. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008, 27:5904-5912.
42. Finn O.J. Cancer immunology. N Engl J Med 2008, 358:2704-2715.
43. Grigorieva I., Thomas X., Epstein J. The bone marrow stromal environment is a major factor in myeloma cell resistance to dexamethasone. Exp Hematol 1998, 26:597-603.
44. Huszthy P.C., Immervoll H., Wang J., Goplen D., Miletic H., Eide G.E., et al. Cellular effects of oncolytic viral therapy on the glioblastoma microenvironment. Gene Ther 2010, 17:202-216.
45. De Silva N., Atkins H., Kirn D.H., Bell J.C., Breitbach C.J. Double trouble for tumours: exploiting the tumour microenvironment to enhance anticancer effect of oncolytic viruses. Cytokine Growth Factor Rev 2010, 21:135-141.
46. Ottolino-Perry K., Diallo J.S., Lichty B.D., Bell J.C., McCart J.A. Intelligent design: combination therapy with oncolytic viruses. Mol Ther 2010, 18:251-263.
47. Kumar S., Gao L., Yeagy B., Reid T. Virus combinations and chemotherapy for the treatment of human cancers. Curr Opin Mol Ther 2008, 10:371-379.
48. Ring C.J. Cytolytic viruses as potential anti-cancer agents. J Gen Virol 2002, 83:491-502.
49. Stojdl D.F., Lichty B., Knowles S., Marius R., Atkins H., Sonenberg N., et al. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat Med 2000, 6:821-825.
50. Sinkovics J.G., Horvath J.C. Newcastle disease virus (NDV): brief history of its oncolytic strains. J Clin Virol 2000, 16:1-15.
51. Strong J.E., Coffey M.C., Tang D., Sabinin P., Lee P.W. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J 1998, 17:3351-3362.
52. Evgin L., Vaha-Koskela M., Rintoul J., Falls T., Le Boeuf F., Barrett J.W., et al. Potent oncolytic activity of raccoonpox virus in the absence of natural pathogenicity. Mol Ther 2010, 18:896-902.
53. Woo Y., Kelly K.J., Stanford M.M., Galanis C., Chun Y.S., Fong Y., et al. Myxoma virus is oncolytic for human pancreatic adenocarcinoma cells. Ann Surg Oncol 2008, 15:2329-2335.
54. Wang G., Barrett J.W., Stanford M., Werden S.J., Johnston J.B., Gao X., et al. Infection of human cancer cells with myxoma virus requires Akt activation via interaction with a viral ankyrin-repeat host range factor. Proc Natl Acad Sci USA 2006, 103:4640-4645.
55. Rommelaere J., Cornelis J.J. Antineoplastic activity of parvoviruses. J Virol Meth. 1991, 33:233-251.
56. Wang K.S., Kuhn R.J., Strauss E.G., Ou S., Strauss J.H. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol 1992, 66:4992-5001.
57. van den Brule F.A., Castronovo V., Menard S., Giavazzi R., Marzola M., Belotti D., et al. Expression of the 67 kD laminin receptor in human ovarian carcinomas as defined by a monoclonal antibody, MLuC5. Eur J Cancer 1996, 32A:1598-1602.
58. Kolodkin-Gal D., Zamir G., Edden Y., Pikarsky E., Pikarsky A., Haim H., et al. Herpes simplex virus type 1 preferentially targets human colon carcinoma: role of extracellular matrix. J Virol 2008, 82:999-1010.
59. Merrill M.K., Bernhardt G., Sampson J.H., Wikstrand C.J., Bigner D.D., Gromeier M. Poliovirus receptor CD155-targeted oncolysis of glioma. Neuro Oncol 2004, 6:208-217.
60. Asaoka K., Tada M., Sawamura Y., Ikeda J., Abe H. Dependence of efficient adenoviral gene delivery in malignant glioma cells on the expression levels of the Coxsackievirus and adenovirus receptor. J Neurosurg 2000, 92:1002-1008.
61. Bucheit A.D., Kumar S., Grote D.M., Lin Y., von Messling V., Cattaneo R.B., et al. An oncolytic measles virus engineered to enter cells through the CD20 antigen. Mol Ther 2003, 7:62-72.
62. Fielding A.K. Measles as a potential oncolytic virus. Rev Med Virol 2005, 15:135-142.
63. Sellers W.R., Kaelin W.G. Role of the retinoblastoma protein in the pathogenesis of human cancer. J Clin Oncol 1997, 15:3301-3312.
64. Levine A.J. P53, the cellular gatekeeper for growth and division. Cell 1997, 88:323-331.
65. Soria C., Estermann F.E., Espantman K.C., O'Shea C.C. Heterochromatin silencing of p53 target genes by a small viral protein. Nature 2010, 466:1076-1081.
66. Mineta T., Rabkin S.D., Yazaki T., Hunter W.D., Martuza R.L. Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas. Nat Med 1995, 1:938-943.
67. Randazzo B.P., Kucharczuk J.C., Litzky L.A., Kaiser L.R., Brown S.M., MacLean A., et al. Herpes simplex 1716 - an ICP 34.5 mutant - is severely replication restricted in human skin xenografts in vivo. Virology 1996, 223:392-395.
68. Nemunaitis J., Meyers T., Senzer N., Cunningham C., West H., Vallieres E., et al. Phase I Trial of sequential administration of recombinant DNA and adenovirus expressing L523S protein in early stage non-small-cell lung cancer. Mol Ther 2006, 13:1185-1191.
69. Alcami A., Symons J.A., Smith G.L. The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J Virol 2000, 74:11230-11239.
70. Le Boeuf F., Diallo J.S., McCart J.A., Thorne S., Falls T., Stanford M., et al. Synergistic interaction between oncolytic viruses augments tumor killing. Mol Ther 2010, 18:888-895.
71. Springfeld C., von Messling V., Frenzke M., Ungerechts G., Buchholz C.J., Cattaneo R. Oncolytic efficacy and enhanced safety of measles virus activated by tumor-secreted matrix metalloproteinases. Cancer Res 2006, 66:7694-7700.
72. DeWeese T.L., van der Poel H., Li S., Mikhak B., Drew R., Goemann M., et al. A phase I trial of CV706, a replication-competent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res 2001, 61:7464-7472.
73. Kasuya H., Takeda S., Nomoto S., Nakao A. The potential of oncolytic virus therapy for pancreatic cancer. Cancer Gene Ther 2005, 12:725-736.
74. Kurihara T., Brough D.E., Kovesdi I., Kufe D.W. Selectivity of a replication-competent adenovirus for human breast carcinoma cells expressing the MUC1 antigen. J Clin Invest 2000, 106:763-771.
75. Hallenbeck P.L., Chang Y.N., Hay C., Golightly D., Stewart D., Lin J., et al. A novel tumor-specific replication-restricted adenoviral vector for gene therapy of hepatocellular carcinoma. Hum Gene Ther 1999, 10:1721-1733.
76. Peng K.W., Russell S.J. Viral vector targeting. Curr Opin Biotechnol 1999, 10:454-457.
77. Galanis E., Vile R., Russell S.J. Delivery systems intended for in vivo gene therapy of cancer: targeting and replication competent viral vectors. Crit Rev Oncol Hematol 2001, 38:177-192.
78. Kirn D. Oncolytic virotherapy for cancer with the adenovirus dl1520 (Onyx-015): results of phase I and II trials. Expert Opin Biol Ther 2001, 1:525-538.
79. Thirukkumaran C.M., Nodwell M.J., Hirasawa K., Shi Z.Q., Diaz R., Luider J., et al. Oncolytic viral therapy for prostate cancer: efficacy of reovirus as a biological therapeutic. Cancer Res 2010, 70:2435-2444.
80. Forsyth P., Roldan G., George D., Wallace C., Palmer C.A., Morris D., et al. A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther 2008, 16:627-632.
81. Park B.H., Hwang T., Liu T.C., Sze D.Y., Kim J.S., Kwon H.C., et al. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol 2008, 9:533-542.
82. Fujimoto Y., Mizuno T., Sugiura S., Goshima F., Kohno S., Nakashima T., et al. Intratumoral injection of herpes simplex virus HF10 in recurrent head and neck squamous cell carcinoma. Acta Otolaryngol 2006, 126:1115-1117.
83. Kimata H., Imai T., Kikumori T., Teshigahara O., Nagasaka T., Goshima F., et al. Pilot study of oncolytic viral therapy using mutant herpes simplex virus (HF10) against recurrent metastatic breast cancer. Ann Surg Oncol 2006, 13:1078-1084.
84. Coukos G., Makrigiannakis A., Montas S., Kaiser L.R., Toyozumi T., Benjamin I., et al. Multi-attenuated herpes simplex virus-1 mutant G207 exerts cytotoxicity against epithelial ovarian cancer but not normal mesothelium and is suitable for intraperitoneal oncolytic therapy. Cancer Gene Ther 2000, 7:275-283.
85. Peng K.W., TenEyck C.J., Galanis E., Kalli K.R., Hartmann L.C., Russell S.J. Intraperitoneal therapy of ovarian cancer using an engineered measles virus. Cancer Res 2002, 62:4656-4662.
86. Coukos G., Courreges M.C., Benencia F. Intraperitoneal oncolytic and tumor vaccination therapy with replication-competent recombinant virus: the herpes paradigm. Curr Gene Ther 2003, 3:113-125.
87. Galanis E., Hartmann L.C., Cliby W.A., Long H.J., Peethambaram P.P., Barrette B.A., et al. Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res 2010, 70:875-882.
88. Vasey P.A., Shulman L.N., Campos S., Davis J., Gore M., Johnston S., et al. 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 2002, 20:1562-1569.
89. Gomella L.G., Mastrangelo M.J., McCue P.A., Maguire H.J., Mulholland S.G., Lattime E.C. Phase i study of intravesical vaccinia virus as a vector for gene therapy of bladder cancer. J Urol 2001, 166:1291-1295.
90. Buller R.E., Runnebaum I.B., Karlan B.Y., Horowitz J.A., Shahin M., Buekers T., et al. A phase I/II trial of rAd/p53 (SCH 58500) gene replacement in recurrent ovarian cancer. Cancer Gene Ther 2002, 9:553-566.
91. Wolf J.K., Bodurka D.C., Gano J.B., Deavers M., Ramondetta L., Ramirez P.T., et al. A phase I study of Adp53 (INGN 201; ADVEXIN) for patients with platinum- and paclitaxel-resistant epithelial ovarian cancer. Gynecol Oncol 2004, 94:442-448.
92. Parato K.A., Senger D., Forsyth P.A., Bell J.C. Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer 2005, 5:965-976.
93. Pecora A.L., Rizvi N., Cohen G.I., Meropol N.J., Sterman D., Marshall J.L., et al. Phase I trial of intravenous administration of PV701, an oncolytic virus, in patients with advanced solid cancers. J Clin Oncol 2002, 20:2251-2266.
94. Laurie S.A., Bell J.C., Atkins H.L., Roach J., Bamat M.K., O'Neil J.D., et al. A phase 1 clinical study of intravenous administration of PV701, an oncolytic virus, using two-step desensitization. Clin Cancer Res 2006, 12:2555-2562.
95. Hotte S.J., Lorence R.M., Hirte H.W., Polawski S.R., Bamat M.K., O'Neil J.D., et al. An optimized clinical regimen for the oncolytic virus PV701. Clin Cancer Res 2007, 13:977-985.
96. Fong Y., Kim T., Bhargava A., Schwartz L., Brown K., Brody L., et al. A herpes oncolytic virus can be delivered via the vasculature to produce biologic changes in human colorectal cancer. Mol Ther 2009, 17:389-394.
97. Kemeny N., Brown K., Covey A., Kim T., Bhargava A., Brody L., et al. 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 2006, 17:1214-1224.
98. Reid T.R., Freeman S., Post L., McCormick F., Sze D.Y. Effects of Onyx-015 among metastatic colorectal cancer patients that have failed prior treatment with 5-FU/leucovorin. Cancer Gene Ther 2005, 12:673-681.
99. Nemunaitis J., Cunningham C., Buchanan A., Blackburn A., Edelman G., Maples P., et al. Intravenous infusion of a replication-selective adenovirus (ONYX-015) in cancer patients: safety, feasibility and biological activity. Gene Ther 2001, 8:746-759.
100. Small E.J., Carducci M.A., Burke J.M., Rodriguez R., Fong L., van Ummersen L., et al. A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol Ther 2006, 14:107-117.
101. Vidal L., Pandha H.S., Yap T.A., White C.L., Twigger K., Vile R.G., et al. A phase I study of intravenous oncolytic reovirus type 3 Dearing in patients with advanced cancer. Clin Cancer Res 2008, 14:7127-7137.
102. Dunn G.P., Old L.J., Schreiber R.D. The three Es of cancer immunoediting. Annu Rev Immunol 2004, 22:329-360.
103. Balkwill F., Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 2001, 357:539-545.
104. Paus R., Nickoloff B.J., Ito T. A 'hairy' privilege. Trends Immunol 2005, 26:32-40.
105. Gajewski T.F., Meng Y., Blank C., Brown I., Kacha A., Kline J., et al. Immune resistance orchestrated by the tumor microenvironment. Immunol Rev 2006, 213:131-145.
106. O'Connell J., Bennett M.W., O'Sullivan G.C., Collins J.K., Shanahan F. The Fas counterattack: cancer as a site of immune privilege. Immunol Today 1999, 20:46-52.
107. Shanahan F., O'Connell J., O'Sullivan G.C. Confirmation of the Fas counterattack in host-tumor relations. Gastroenterology 1997, 113:1804-1806.
108. O'Sullivan G.C., Corbett A.R., Shanahan F., Collins J.K. Regional immunosuppression in esophageal squamous cancer: evidence from functional studies with matched lymph nodes. J Immunol 1996, 157:4717-4720.
109. O'Mahony A.M., O'Sullivan G.C., O'Connell J., Cotter T.G., Collins J.K. An immune suppressive factor derived from esophageal squamous carcinoma induces apoptosis in normal and transformed cells of lymphoid lineage. J Immunol 1993, 151:4847-4856.
110. Simpson E. A historical perspective on immunological privilege. Immunol Rev 2006, 213:12-22.
111. Streilein J.W. Immune privilege as the result of local tissue barriers and immunosuppressive microenvironments. Curr Opin Immunol 1993, 5:428-432.
112. Iweala O.I., Nagler C.R. Immune privilege in the gut: the establishment and maintenance of non-responsiveness to dietary antigens and commensal flora. Immunol Rev 2006, 213:82-100.
113. Mellor A.L., Munn D.H. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 2004, 4:762-774.
114. Mellor A.L., Munn D.H. Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat Rev Immunol 2008, 8:74-80.
115. Probst H.C., Lagnel J., Kollias G., van den Broek M. Inducible transgenic mice reveal resting dendritic cells as potent inducers of CD8+ T cell tolerance. Immunity 2003, 18:713-720.
116. Ferguson T.A., Griffith T.S. A vision of cell death: Fas ligand and immune privilege 10 years later. Immunol Rev 2006, 213:228-238.
117. Munn D.H., Sharma M.D., Hou D., Baban B., Lee J.R., Antonia S.J., et al. Expression of indoleamine 2, 3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J Clin Invest 2004, 114:280-290.
118. Waldmann H., Graca L., Cobbold S., Adams E., Tone M., Tone Y. Regulatory T cells and organ transplantation. Semin Immunol 2004, 16:119-126.
119. Uyttenhove C., Pilotte L., Theate I., Stroobant V., Colau D., Parmentier N., et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2, 3-dioxygenase. Nat Med 2003, 9:1269-1274.
120. Dercamp C., Chemin K., Caux C., Trinchieri G., Vicari A.P. Distinct and overlapping roles of interleukin-10 and CD25+ regulatory T cells in the inhibition of antitumor CD8 T-cell responses. Cancer Res 2005, 65:8479-8486.
121. Miyara M., Sakaguchi S. Natural regulatory T cells: mechanisms of suppression. Trends Mol Med 2007, 13:108-116.
122. Bennett M.W., O'Connell J., O'Sullivan G.C., Roche D., Brady C., Kelly J., et al. Expression of Fas ligand by human gastric adenocarcinomas: a potential mechanism of immune escape in stomach cancer. Gut 1999, 44:156-162.
123. O'Connell J., Bennett M.W., O'Sullivan G.C., Collins J.K., Shanahan F. The Fas counterattack: a molecular mechanism of tumor immune privilege. Mol Med 1997, 3:294-300.
124. O'Connell J., O'Sullivan G.C., Collins J.K., Shanahan F. The Fas counterattack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand. J Exp Med 1996, 184:1075-1082.
125. Bernt K.M., Ni S., Gaggar A., Li Z.Y., Shayakhmetov D.M., Lieber A. The effect of sequestration by nontarget tissues on anti-tumor efficacy of systemically applied, conditionally replicating adenovirus vectors. Mol Ther 2003, 8:746-755.
126. Green N.K., Herbert C.W., Hale S.J., Hale A.B., Mautner V., Harkins R., et al. Extended plasma circulation time and decreased toxicity of polymer-coated adenovirus. Gene Ther 2004, 11:1256-1263.
127. Stevenson M., Hale A.B., Hale S.J., Green N.K., Black G., Fisher K.D., et al. Incorporation of a laminin-derived peptide (SIKVAV) on polymer-modified adenovirus permits tumor-specific targeting via alpha6-integrins. Cancer Gene Ther 2007, 14:335-345.
128. Bangari D.S., Mittal S.K. Current strategies and future directions for eluding adenoviral vector immunity. Curr Gene Ther 2006, 6:215-226.
129. Novella I.S., Gilbertson D.L., Borrego B., Domingo E., Holland J.J. Adaptability costs in immune escape variants of vesicular stomatitis virus. Virus Res 2005, 107:27-34.
130. Willmon C., Harrington K., Kottke T., Prestwich R., Melcher A., Vile R. Cell carriers for oncolytic viruses: Fed Ex for cancer therapy. Mol Ther 2009, 17:1667-1676.
131. Monsky W.L., Fukumura D., Gohongi T., Ancukiewcz M., Weich H.A., Torchilin V.P., et al. Augmentation of transvascular transport of macromolecules and nanoparticles in tumors using vascular endothelial growth factor. Cancer Res 1999, 59:4129-4135.
132. Liu Y., Deisseroth A. Tumor vascular targeting therapy with viral vectors. Blood 2006, 107:3027-3033.
133. Hallak L.K., Merchan J.R., Storgard C.M., Loftus J.C., Russell S.J. Targeted measles virus vector displaying echistatin infects endothelial cells via alpha(v)beta3 and leads to tumor regression. Cancer Res 2005, 65:5292-5300.
134. McCormick F. Future prospects for oncolytic therapy. Oncogene 2005, 24:7817-7819.
135. Wein L.M., Wu J.T., Kirn D.H. Validation and analysis of a mathematical model of a replication-competent oncolytic virus for cancer treatment: implications for virus design and delivery. Cancer Res 2003, 63:1317-1324.
136. Fulci G., Breymann L., Gianni D., Kurozomi K., Rhee S.S., Yu J., et al. Cyclophosphamide enhances glioma virotherapy by inhibiting innate immune responses. Proc Natl Acad Sci USA 2006, 103:12873-12878.
137. Kottke T., Thompson J., Diaz R.M., Pulido J., Willmon C., Coffey M., et al. Improved systemic delivery of oncolytic reovirus to established tumors using preconditioning with cyclophosphamide-mediated Treg modulation and interleukin-2. Clin Cancer Res 2009, 15:561-569.
138. Ikeda K., Ichikawa T., Wakimoto H., Silver J.S., Deisboeck T.S., Finkelstein D., et al. Oncolytic virus therapy of multiple tumors in the brain requires suppression of innate and elicited antiviral responses. Nat Med 1999, 5:881-887.
139. Wojton J., Kaur B. Impact of tumor microenvironment on oncolytic viral therapy. Cytokine Growth Factor Rev 2010, 21:127-134.
140. Kim J.H., Lee Y.S., Kim H., Huang J.H., Yoon A.R., Yun C.O. Relaxin expression from tumor-targeting adenoviruses and its intratumoral spread, apoptosis induction, and efficacy. J Natl Cancer Inst 2006, 98:1482-1493.
141. Crittenden M.R., Thanarajasingam U., Vile R.G., Gough M.J. Intratumoral immunotherapy: using the tumour against itself. Immunology 2005, 114:11-22.
142. Sinkovics J.G. Viral oncolysates as human tumor vaccines. Int Rev Immunol 1991, 7:259-287.
143. Mocellin S., Wang E., Marincola F.M. Cytokines and immune response in the tumor microenvironment. J Immunother (1991) 2001, 24:392-407.
144. Cassel W.A., Murray D.R., Torbin A.H., Olkowski Z.L., Moore M.E. Viral oncolysate in the management of malignant melanoma. I. Preparation of the oncolysate and measurement of immunologic responses. Cancer 1977, 40:672-679.
145. Murray D.R., Cassel W.A., Torbin A.H., Olkowski Z.L., Moore M.E. Viral oncolysate in the management of malignant melanoma. II. Clinical studies. Cancer 1977, 40:680-686.
146. Sinkovics J.G., Horvath J.C. Vaccination against human cancers (review). Int J Oncol 2000, 16:81-96.
147. Sinkovics J.G., Horvath J.C. Evidence accumulating in support of cancer vaccines combined with chemotherapy: a pragmatic review of past and present efforts. Int J Oncol 2006, 29:765-777.
148. Batliwalla F.M., Bateman B.A., Serrano D., Murray D., Macphail S., Maino V.C., et al. 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 1998, 4:783-794.
149. Wallack M.K., Bash J.A., Leftheriotis E., Seigler H., Bland K., Wanebo H., et al. Positive relationship of clinical and serologic responses to vaccinia melanoma oncolysate. Arch Surg 1987, 122:1460-1463.
150. Whelan M.C., Casey G., Macconmara M., Lederer J.A., Soden D., Collins J.K., et al. Effective immunotherapy of weakly immunogenic solid tumours using a combined immunogene therapy and regulatory T-cell inactivation. Cancer Gene Ther 2010, 17:501-511.
151. Prestwich R., Vile R., Melcher A. Cancer immunotherapy. N Engl J Med 2008, 359:1072. [author reply 1073].
152. Prestwich R.J., Harrington K.J., Vile R.G., Melcher A.A. Immunotherapeutic potential of oncolytic virotherapy. Lancet Oncol 2008, 9:610-612.
153. Collins C.G., Tangney M., Larkin J.O., Casey G., Whelan M.C., Cashman J., et al. Local gene therapy of solid tumors with GM-CSF and B7-1 eradicates both treated and distal tumors. Cancer Gene Ther 2006, 13:1061-1071.
154. Cashman J.P., Larkin J.O., Casey G., Whelan M.C., Collins C., Aarons S., et al. Immune gene therapy as a neoadjuvant to surgical excision to control metastatic cancers. Cancer Lett 2008, 262:94-102.
155. Mastrangelo M.J., Lattime E.C. Virotherapy clinical trials for regional disease: in situ immune modulation using recombinant poxvirus vectors. Cancer Gene Ther 2002, 9:1013-1021.
156. Robinson B.W., Mukherjee S.A., Davidson A., Morey S., Musk A.W., Ramshaw I., et al. Cytokine gene therapy or infusion as treatment for solid human cancer. J Immunother 1998, 21:211-217.
157. Hu J.C., Coffin R.S., Davis C.J., Graham N.J., Groves N., Guest P.J., et al. A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin Cancer Res 2006, 12:6737-6747.
158. Mastrangelo M.J., Maguire H.C., Eisenlohr L.C., Laughlin C.E., Monken C.E., McCue P.A., et al. Intratumoral recombinant GM-CSF-encoding virus as gene therapy in patients with cutaneous melanoma. Cancer Gene Ther 1999, 6:409-422.
159. Harrington K.J., Hingorani M., Tanay M.A., Hickey J., Bhide S.A., Clarke P.M., et al. 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 2010, 16:4005-4015.
160. Comins C., Heinemann L., Harrington K., Melcher A., De Bono J., Pandha H. Reovirus: viral therapy for cancer 'as nature intended'. Clin Oncol (R Coll Radiol) 2008, 20:548-554.
161. Coffey M.C., Strong J.E., Forsyth P.A., Lee P.W. Reovirus therapy of tumors with activated Ras pathway. Science 1998, 282:1332-1334.
162. Norman K.L., Lee P.W. Not all viruses are bad guys: the case for reovirus in cancer therapy. Drug Discov Today 2005, 10:847-855.
163. Ganly I., Kirn D., Eckhardt G., Rodriguez G.I., Soutar D.S., Otto R., et al. A phase I study of Onyx-015, an E1B attenuated adenovirus, administered intratumorally to patients with recurrent head and neck cancer. Clin Cancer Res 2000, 6:798-806.
164. Nemunaitis J., Ganly I., Khuri F., Arseneau J., Kuhn J., McCarty T., et al. Selective replication and oncolysis in p53 mutant tumors with ONYX-015, an E1B-55kD gene-deleted adenovirus, in patients with advanced head and neck cancer: a phase II trial. Cancer Res 2000, 60:6359-6366.
165. Mulvihill S., Warren R., Venook A., Adler A., Randlev B., Heise C., et al. Safety and feasibility of injection with an E1B-55 kDa gene-deleted, replication-selective adenovirus (ONYX-015) into primary carcinomas of the pancreas: a phase I trial. Gene Ther 2001, 8:308-315.
166. Makower D., Rozenblit A., Kaufman H., Edelman M., Lane M.E., Zwiebel J., et al. Phase II clinical trial of intralesional administration of the oncolytic adenovirus ONYX-015 in patients with hepatobiliary tumors with correlative p53 studies. Clin Cancer Res 2003, 9:693-702.
167. Rudin C.M., Cohen E.E., Papadimitrakopoulou V.A., Silverman S., Recant W., El-Naggar A.K., et al. An attenuated adenovirus, ONYX-015, as mouthwash therapy for premalignant oral dysplasia. J Clin Oncol 2003, 21:4546-4552.
168. Harrow S., Papanastassiou V., Harland J., Mabbs R., Petty R., Fraser M., et al. HSV1716 injection into the brain adjacent to tumour following surgical resection of high-grade glioma: safety data and long-term survival. Gene Ther 2004, 11:1648-1658.
169. Markert J.M., Liechty P.G., Wang W., Gaston S., Braz E., Karrasch M., 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.
170. Lal S., Lauer U.M., Niethammer D., Beck J.F., Schlegel P.G. Suicide genes: past, present and future perspectives. Immunol Today 2000, 21:48-54.
171. Portsmouth D., Hlavaty J., Renner M. Suicide genes for cancer therapy. Mol Aspects Med 2007, 28:4-41.
172. Nasu Y., Saika T., Ebara S., Kusaka N., Kaku H., Abarzua F., et al. Suicide gene therapy with adenoviral delivery of HSV-tK gene for patients with local recurrence of prostate cancer after hormonal therapy. Mol Ther 2007, 15:834-840.
173. Braybrooke J.P., Slade A., Deplanque G., Harrop R., Madhusudan S., Forster M.D., et al. Phase I study of MetXia-P450 gene therapy and oral cyclophosphamide for patients with advanced breast cancer or melanoma. Clin Cancer Res 2005, 11:1512-1520.
174. Kan O., Kingsman S., Naylor S. Cytochrome P450-based cancer gene therapy: current status. Expert Opin Biol Ther 2002, 2:857-868.
175. Freytag S.O., Khil M., Stricker H., Peabody J., Menon M., DePeralta-Venturina M., et al. Phase I study of replication-competent adenovirus-mediated double suicide gene therapy for the treatment of locally recurrent prostate cancer. Cancer Res 2002, 62:4968-4976.
176. Altaner C. Prodrug cancer gene therapy. Cancer Lett 2008, 270:191-201.
177. McNeish I.A., Bell S.J., Lemoine N.R. Gene therapy progress and prospects: cancer gene therapy using tumour suppressor genes. Gene Ther 2004, 11:497-503.
178. Almazov V.P., Kochetkov D.V., Chumakov P.M. The use of p53 as a tool for human cancer therapy. Mol Biol (Mosk) 2007, 41:947-963.
179. Guan Y.S., Liu Y., Zou Q., He Q., La Z., Yang L., et al. Adenovirus-mediated wild-type p53 gene transfer in combination with bronchial arterial infusion for treatment of advanced non-small-cell lung cancer, one year follow-up. J Zhejiang Univ Sci B 2009, 10:331-340.
180. Shimada H., Matsubara H., Shiratori T., Shimizu T., Miyazaki S., Okazumi S., et al. Phase I/II adenoviral p53 gene therapy for chemoradiation resistant advanced esophageal squamous cell carcinoma. Cancer Sci 2006, 97:554-561.
181. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
182. Gold J.S., Dematteo R.P. Combined surgical and molecular therapy: the gastrointestinal stromal tumor model. Ann Surg 2006, 244:176-184.
183. Rajan B., Ross G., Lim C.C., Ashley S., Goode D., Traish D., et al. Survival in patients with recurrent glioma as a measure of treatment efficacy: prognostic factors following nitrosourea chemotherapy. Eur J Cancer 1994, 30A:1809-1815.
184. Chu R.L., Post D.E., Khuri F.R., Van Meir E.G. Use of replicating oncolytic adenoviruses in combination therapy for cancer. Clin Cancer Res 2004, 10:5299-5312.
185. Fujita T., Teh B.S., Timme T.L., Mai W.Y., Satoh T., Kusaka N., et al. Sustained long-term immune responses after in situ gene therapy combined with radiotherapy and hormonal therapy in prostate cancer patients. Int J Radiat Oncol Biol Phys 2006, 65:84-90.
186. Pan J.J., Zhang S.W., Chen C.B., Xiao S.W., Sun Y., Liu C.Q., et al. Effect of recombinant adenovirus-p53 combined with radiotherapy on long-term prognosis of advanced nasopharyngeal carcinoma. J Clin Oncol 2009, 27:799-804.
187. Harrington K.J., Karapanagiotou E.M., Roulstone V., Twigger K.R., White C.L., Vidal L., 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, 16:3067-3077.
188. Nguyen T.L., Abdelbary H., Arguello M., Breitbach C., Leveille S., Diallo J.S., et al. Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proc Natl Acad Sci USA 2008, 105:14981-14986.
189. Milanesi E., Costantini P., Gambalunga A., Colonna R., Petronilli V., Cabrelle A., et al. The mitochondrial effects of small organic ligands of BCL-2: sensitization of BCL-2-overexpressing cells to apoptosis by a pyrimidine-2, 4, 6-trione derivative. J Biol Chem 2006, 281:10066-10072.
190. Tumilasci V.F., Oliere S., Nguyen T.L., Shamy A., Bell J., Hiscott J. Targeting the apoptotic pathway with BCL-2 inhibitors sensitizes primary chronic lymphocytic leukemia cells to vesicular stomatitis virus-induced oncolysis. J Virol 2008, 82:8487-8499.
191. Lee S.B., Esteban M. The interferon-induced double-stranded RNA-activated human p68 protein kinase inhibits the replication of vaccinia virus. Virology 1993, 193:1037-1041.
192. Hu W., Hofstetter W., Guo W., Li H., Pataer A., Peng H.H., et al. JNK-deficiency enhanced oncolytic vaccinia virus replication and blocked activation of double-stranded RNA-dependent protein kinase. Cancer Gene Ther 2008, 15:616-624.
193. Dimmock N.J. Introduction to modern virology 2007, Blackwell. 6th ed.