Recent clinical experience with oncolytic viruses

Current Pharmaceutical Biotechnology

Volumn 13, Issue 9, 2012, Pages 1834-1841

  Donnelly, O G ^a   Errington Mais, F ^a   Prestwich, R ^a   Harrington, K ^b   Pandha, H ^c   Vile, R ^d   Melcher, A A ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF SURREY   (United Kingdom)

^d MAYO CLINIC   (United States)

Author keywords

Adenovirus; Measles; Oncolytic virus; Reovirus; Vaccinia

Indexed keywords

CARBOPLATIN; CARCINOEMBRYONIC ANTIGEN; CISPLATIN; CVA 21; ETANERCEPT; FLUOROURACIL; G 207; H 101; HF 10; HSV 1020; HSV 1716; ICP 47; JX 594; JX 929; JX 963; LONTUCIREV; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; NTX 010; OBP 301; ONCOLYTIC ADENOVIRUS; ONCOLYTIC COXSACKIE VIRUS; ONCOLYTIC HERPES VIRUS; ONCOLYTIC MEASLES VIRUS; ONCOLYTIC NEWCASTLE DISEASE VIRUS; ONCOLYTIC REOVIRUS; ONCOLYTIC SENECA VALLEY VIRUS; ONCOLYTIC VACCINIA VIRUS; ONCOLYTIC VIRUS; PACLITAXEL; PV 701; REOLYSIN; TALIMOGENE LAHERPAREPVEC; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ABSENCE OF SIDE EFFECTS; ADVANCED CANCER; ARTICLE; BRAIN CANCER; BREAST CANCER; BREAST METASTASIS; CANCER IMMUNIZATION; CANCER PATIENT; COLORECTAL CANCER; DRUG DOSE ESCALATION; DRUG DOSE INCREASE; DRUG POTENCY; DRUG SAFETY; DRUG TOLERABILITY; FATIGUE; FLU LIKE SYNDROME; GLIOBLASTOMA; GLIOMA; GYNECOLOGIC CANCER; HEAD AND NECK CANCER; HERPES SIMPLEX VIRUS 1; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MELANOMA; MULTIPLE CYCLE TREATMENT; MYELOMA; NEUROENDOCRINE TUMOR; NONHUMAN; ONCOLYTIC VIROTHERAPY; OVARY CANCER; PANCREAS CANCER; PERITONEUM CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; SOLID TUMOR; UNSPECIFIED SIDE EFFECT; UTERINE TUBE TUMOR; VIRUS REPLICATION;

CLINICAL TRIALS AS TOPIC; DRUG EVALUATION, PRECLINICAL; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; VIRUS REPLICATION;

ADENOVIRIDAE; HERPES; NEWCASTLE DISEASE VIRUS; ORTHOREOVIRUS; REPLICATION COMPETENT VIRUSES;

EID: 84863543771     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112800958904     Document Type: Article

References (55)

1. Kelly, E.; Russell, S. J. History of oncolytic viruses: genesis to genetic engineering. Mol. Ther., 2007, 15, 651-659.
2. Liu, T.; Galanis, E.; Kirn, D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat. Clin. Prac. Oncol., 2007, 4, 101-117.
3. Guse, K.; Hemminki, A. Cancer gene therapy with oncolytic adenoviruses. J. BUON, 2009, 14 (Suppl 1), S7-15.
4. Kawashima, T.; Kagawa, S.; Kobayashi, N.; Shirakiya, Y.; Umeoka, T.; Teraishi, F.; Taki, M.; Kyo, S.; Tanaka, N.; Fujiwara, T. Telomerase-specific replication-selective virotherapy for human cancer. Clin. Cancer Res., 2004, 10, 285-292.
5. Garber, K. China approves world's first oncolytic virus therapy for cancer treatment. J. Natl. Cancer Inst., 2006, 98, 298-300.
6. Xia, Z.; Chang, J.; Zhang, L.; Jiang, W.; Guan, Z.; Liu, J.; Zhang, Y.; Hu, X.; Wu, G.; Wang, H.; Chen, Z.; Chen, J.; Zhou, Q.; Lu, J.; Fan, Q.; Huang, J.; Zheng, X. Phase III randomized clinical trial of intratumoral injection of E1B gene-deleted adenovirus (H101) combined with cisplatin-based chemotherapy in treating squamous cell cancer of head and neck or esophagus. Ai Zheng, 2004, 23, 1666-1670.
7. Nemunaitis, J.; Senzer, N.; Sarmiento, S.; Zhang, Y.; Arzaga, R.; Sands, B.; Maples, P.; Tong, A. W. A phase I trial of intravenous infusion of ONYX-015 and enbrel in solid tumor patients. Cancer Gene Ther., 2007, 14, 885-893.
8. Pesonen, S.; Nokisalmi, P.; Escutenaire, S.; Sarkioja, M.; Raki, M.; Cerullo, V.; Kangasniemi, L.; Laasonen, L.; Ribacka, C.; Guse, K.; Haavisto, E.; Oksanen, M.; Rajecki, M.; Helminen, A.; Ristimaki, A.; Karioja-Kallio, A.; Karli, E.; Kantola, T.; Bauerschmitz, G.; Kanerva, A.; Joensuu, T.; Hemminki, A. Prolonged systemic circulation of chimeric oncolytic adenovirus Ad5/3-Cox2L-D24 in patients with metastatic and refractory solid tumors. Gene Ther., 2010, 17(7), 892-904
9. Chang, J.; Zhao, X.; Wu, X.; Guo, Y.; Guo, H.; Cao, J.; Guo, Y.; Lou, D.; Yu, D.; Li, J. A Phase I study of KH901, a conditionally replicating granulocyte-macrophage colony-stimulating factor: armed oncolytic adenovirus for the treatment of head and neck cancers. Cancer Biol. Ther., 2009, 8, 676-682.
10. Cerullo, V.; Pesonen, S.; Diaconu, I.; Escutenaire, S.; Raki, M.; Sarkioja, M.; Ahtiainen, L.; Karli, E.; Holm, S.; Arstila, P.; Kangasniemi, L.; Guse, K.; Nokisalmi, P.; Haavisto, E.; Karioja-Kallio, A.; Ugolini, M.; Oksanen, M.; Joensuu, T.; Laasonen, L.; Kanerva, A.; Hemminki, A. Safety and efficacy of oncolytic adenovirus expressing granulocyte macrophage colony-stimulating factor (GM-CSF) in advanced metastatic cancer patients. Mol. Ther., 2009, 17, S107.
11. Nemunaitis, J.; Tong, A. W.; Nemunaitis, M.; Senzer, N.; Phadke, A. P.; Bedell, C.; Adams, N.; Zhang, Y.; Maples, P. B.; Chen, S.; Pappen, B.; Burke, J.; Ichimaru, D.; Urata, Y.; Fujiwara, T. A phase i study of telomerase-specific replication competent oncolytic adenovirus (telomelysin) for various solid tumors. Mol. Ther., 2009, 18, 429-434.
12. Harrington, K. J.; Vile, R. G.; Melcher, A.; Chester, J.; Pandha, H. S. Clinical trials with oncolytic reovirus: Moving beyond phase I into combinations with standard therapeutics. Cytokine Growth Factor Rev., 2010, 21(2-3),91-98.
13. Vidal, L.; Pandha, H. S.; Yap, T. A.; White, C. L.; Twigger, K.; Vile, R. G.; Melcher, A.; Coffey, M.; Harrington, K. J.; DeBono, J. S. A phase i study of intravenous oncolytic reovirus type 3 dearing in patients with advanced cancer. Clin. Cancer Res., 2008, 14, 7127-7137.
14. Forsyth, P.; Roldan, G.; George, D.; Wallace, C.; Palmer, C. A.; Morris, D.; Cairncross, G.; Matthews, M. V.; Markert, J.; Gillespie, Y.; Coffey, M.; Thompson, B.; Hamilton, M. A Phase i trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol. Ther., 2008, 16, 627-632.
15. Bell, J. Oncolytic VIruses: An approved product on the horizon? Mol. Ther., 2010, 18, 233-234.
16. Nakamura, T.; Russell, J. S. Oncolytic measles viruses for cancer therapy. Expert Opin. Biol. Ther., 2005, 4(10), 1685-1692.
17. Allen, C.; Paraskevakou, G.; Liu, C.; Iankov, I. D.; Msaouel, P.; Zollman, P.; Myers, R.; Peng, K. W.; Russell, S. J.; Galanis, E. Oncolytic measles virus strains in the treatment of gliomas. Expert. Opin. Biol. Ther., 2008, 8, 213-220.
18. Msaouel, P.; Iankov, I. D.; Allen, C.; Morris, J. C.; Messling, V. V.; Cattaneo, R.; Koutsilieris, M.; Russell, S. J.; Galanis, E. Engineered measles virus as a novel oncolytic therapy against prostate cancer. Prostate, 2009, 69, 82-91.
19. Gauvrit, A.; Brandler, S.; Sapede-Peroz, C.; Boisgerault, N.; Tangy, F.; Grégoire, M. Measles virus induces oncolysis of mesothelioma cells and allows dendritic cells to cross-prime tumorspecific CD8 response. Cancer Res., 2008, 68, 4882-4892.
20. Hasegawa, K.; Pham, L.; O'Connor, M. K.; Federspiel, M. J.; Russell, S. J.; Peng, K. Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter. Clin. Cancer Res., 2006, 12, 1868-1875.
21. Heinzerling, L.; Kunzi, V.; Oberholzer, P. A.; Kundig, T.; Naim, H.; Dummer, R. Oncolytic measles virus in cutaneous T-cell lymphomas mounts antitumor immune responses in vivo and targets interferon- resistant tumor cells. Blood, 2005, 106, 2287-2294.
22. Galanis, E.; Hartmann, L. C.; Cliby, W. A.; Long, H. J.; Peethambaram, P. P.; Barrette, B. A.; Kaur, J. S.; Haluska, P. J.; Aderca, I.; Zollman, P. J.; Sloan, J. A.; Keeney, G.; Atherton, P. J.; Podratz, K. C.; Dowdy, S. C.; Stanhope, C. R.; Wilson, T. O.; Federspiel, M. J.; Peng, K.; Russell, S. J. 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.
23. Nakao, A.; Takeda, S.; Shimoyama, S.; Kasuya, H.; Kimata, H.; Teshigahara, O.; Sawaki, M.; Kikumori, T.; Kodera, Y.; Nagasaka, T.; Goshima, F.; Nishiyama, Y.; Imai, T. Clinical experiment of mutant herpes simplex virus HF10 therapy for cancer. Curr. Cancer Drug Targets, 2007, 7, 169-174.
24. Fujimoto, Y.; Mizuno, T.; Sugiura, S.; Goshima, F.; Kohno, S.; Nakashima, T.; Nishiyama, Y. Intratumoral injection of herpes simplex virus HF10 in recurrent head and neck squamous cell carcinoma. Acta Oto-Laryngologica, 2006, 126, 1115.
25. Markert, J. M.; Medlock, M. D.; Rabkin, S. D.; Gillespie, G. Y.; Todo, T.; Hunter, W. D.; Palmer, C. A.; Feigenbaum, F.; Tornatore, C.; Tufaro, F.; Martuza, R. L. Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene. Ther., 2000, 7, 867-874.
26. MacKie, R. M.; Stewart, B.; Brown, S. M. Intralesional injection of herpes simplex virus 1716 in metastatic melanoma. Lancet, 2001, 357, 525-526.
27. Rampling, R.; Cruickshank, G.; Papanastassiou, V.; Nicoll, J.; Hadley, D.; Brennan, D.; Petty, R.; MacLean, A.; Harland, J.; McKie, E.; Mabbs, R.; Brown, M. Toxicity evaluation of replication- competent herpes simplex virus (ICP 34.5 null mutant 1716) in patients with recurrent malignant glioma. Gene. Ther., 2000, 7, 859-866.
28. Papanastassiou, V.; Rampling, R.; Fraser, M.; Petty, R.; Hadley, D.; Nicoll, J.; Harland, J.; Mabbs, R.; Brown, M. The potential for efficacy of the modified (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Ther., 2002, 9, 398-406.
29. Harrow, S.; Papanastassiou, V.; Harland, J.; Mabbs, R.; Petty, R.; Fraser, M.; Hadley, D.; Patterson, J.; Brown, S. M.; Rampling, R. 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.
30. Markert, J. M.; Liechty, P. G.; Wang, W.; Gaston, S.; Braz, E.; Karrasch, M.; Nabors, L. B.; Markiewicz, M.; Lakeman, A. D.; Palmer, C. A.; Parker, J. N.; Whitley, R. J.; Gillespie, G. Y. Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol. Ther., 2008, 17, 199-207.
31. Karrasch, M.; Gillespie, G. Y.; Braz, E.; Liechty, P. G.; Nabors, L. B.; Lakeman, A. D.; Palmer, C. A.; Parker, J. N.; Whitley, R. J.; Markert, J. M. Treatment of recurrent malignant glioma with G207, a genetically engineered herpes simplex virus-1, followed by irradiation: Phase I study results. - ASCO. J. Clin. Oncol., 2009, 27, Suppl; abstr 2042.
32. Fong, Y.; Kim, T.; Bhargava, A.; Schwartz, L.; Brown, K.; Brody, L.; Covey, A.; Karrasch, M.; Getrajdman, G.; Mescheder, A.; Jarnagin, W.; Kemeny, N. A herpes oncolytic virus can be delivered via the vasculature to produce biologic changes in human colorectal cancer. Mol. Ther., 2008, 17, 389-394.
33. Mace, A. T. M.; Ganly, I.; Soutar, D. S.; Brown, S. M. Potential for efficacy of the oncolytic Herpes simplex virus 1716 in patients with oral squamous cell carcinoma. Head Neck, 2008, 30, 1045-1051.
34. Senzer, N. N.; Kaufman, H. L.; Amatruda, T.; Nemunaitis, M.; Reid, T.; Daniels, G.; Gonzalez, R.; Glaspy, J.; Whitman, E.; Harrington, K.; Goldsweig, H.; Marshall, T.; Love, C.; Coffin, R.; Nemunaitis, J. J. 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., 2009, 27, 5763-5771.
35. Kaufman, H. L.; Kim, D. W.; DeRaffele, G.; Mitcham, J.; Coffin, R. S.; Kim-Schulze, S. 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., 2010, 17, 718-730.
36. 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.; Roberts, M. S.; Rabin, H.; Bamat, M. K.; Lorence, R. M. Phase I trial of intravenous administration of PV701, an oncolytic virus, in patients with advanced solid cancers. J. Clin. Oncol., 2002, 20, 2251-2266.
37. Laurie, S. A.; Bell, J. C.; Atkins, H. L.; Roach, J.; Bamat, M. K.; O'Neil, J. D.; Roberts, M. S.; Groene, W. S.; Lorence, R. M. A phase 1 clinical study of intravenous administration of pv701, an oncolytic virus, using two-step desensitization. Clin. Cancer Res., 2006, 12, 2555-2562.
38. 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.; Major, P. P. An optimized clinical regimen for the oncolytic virus PV701. Clin. Cancer Res., 2007, 13, 977-985.
39. Elkord, E.; Dangoor, A.; Drury, N. L.; Harrop, R.; Burt, D. J.; Drijfhout, J. W.; Hamer, C.; Andrews, D.; Naylor, S.; Sherlock, D.; Hawkins, R. E.; Stern, P. L. An MVA-based vaccine targeting the oncofetal antigen 5T4 in patients undergoing surgical resection of colorectal cancer liver metastases. J. Immunother., 2008, 31, 820-829.
40. Elkord, E.; Dangoor, A.; Burt, D. J.; Southgate, T. D.; Daayana, S.; Harrop, R.; Drijfhout, J. W.; Sherlock, D.; Hawkins, R. E.; Stern, P. L. Immune evasion mechanisms in colorectal cancer liver metastasis patients vaccinated with TroVax (MVA-5T4). Cancer Immunol. Immunother., 2009, 58, 1657-1667.
41. Amato, R. J.; Shingler, W.; Naylor, S.; Jac, J.; Willis, J.; Saxena, S.; Hernandez-McClain, J.; Harrop, R. Vaccination of renal cell cancer patients with modified vaccinia ankara delivering tumor antigen 5T4 (TroVax) administered with interleukin 2: A phase II trial. Clin. Cancer Res., 2008, 14, 7504-7510.
42. Hawkins, R. E.; Macdermott, C.; Shablak, A.; Hamer, C.; Thistlethwaite, F.; Drury, N. L.; Chikoti, P.; Shingler, W.; Naylor, S.; Harrop, R. Vaccination of patients with metastatic renal cancer with modified vaccinia Ankara encoding the tumor antigen 5T4 (TroVax) given alongside interferon-alpha. J. Immunother., 2009, 32, 424-429.
43. Kaufman, H. L.; Taback, B.; Sherman, W.; Kim, D. W.; Shingler, W. H.; Moroziewicz, D.; DeRaffele, G.; Mitcham, J.; Carroll, M. W.; Harrop, R.; Naylor, S.; Kim-Schulze, S. Phase II trial of modified vaccinia ankara (MVA) virus expressing 5T4 and high dose interleukin- 2 (IL-2) in patients with metastatic renal cell carcinoma. J. Transl. Med., 7, 2-2.
44. Amato, R. J.; Shingler, W.; Goonewardena, M.; de Belin, J.; Naylor, S.; Jac, J.; Willis, J.; Saxena, S.; Hernandez-McClain, J.; Harrop, R. Vaccination of renal cell cancer patients with modified vaccinia Ankara delivering the tumor antigen 5T4 (TroVax) alone or administered in combination with interferon-alpha (IFN-alpha): a phase 2 trial. J. Immunother., 2009, 32, 765-772.
45. Harrop, R.; Drury, N.; Shingler, W.; Chikoti, P.; Redchenko, I.; Carroll, M. W.; Kingsman, S. M.; Naylor, S.; Melcher, A.; Nicholls, J.; Wassan, H.; Habib, N.; Anthoney, A. Vaccination of colorectal cancer patients with modified vaccinia ankara encoding the tumor antigen 5T4 (TroVax) given alongside chemotherapy induces potent immune responses. Clin. Cancer Res., 2007, 13, 4487-4494.
46. Merrick, A. E.; Ilett, E. J.; Melcher, A. A. JX-594, a targeted oncolytic poxvirus for the treatment of cancer. Curr. Opin. Investig. Drugs, 2009, 10, 1372-1382.
47. Mastrangelo, M. J.; Maguire, H. C.; Eisenlohr, L. C.; Laughlin, C. E.; Monken, C. E.; McCue, P. A.; Kovatich, A. J.; Lattime, E. C. Intratumoral recombinant GM-CSF-encoding virus as gene therapy in patients with cutaneous melanoma. Cancer Gene Ther., 1999, 6, 409-422.
48. Park, B.; Hwang, T.; Liu, T.; Sze, D. Y.; Kim, J.; Kwon, H.; Oh, S. Y.; Han, S.; Yoon, J.; Hong, S. 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.
49. Alemany, R. A smart move against cancer for vaccinia virus. Lancet Oncol., 2008, 9, 507-508.
50. White, C. L.; Twigger, K. R.; Vidal, L.; De Bono, J. S.; Coffey, M.; Heinemann, L.; Morgan, R.; Merrick, A.; Errington, F.; Vile, R. G.; Melcher, A. A.; Pandha, H. S.; Harrington, K. J. Characterization of the adaptive and innate immune response to intravenous oncolytic reovirus (Dearing type 3) during a phase I clinical trial. Gene Ther., 2008, 15, 911-920.
51. Qiao, J.; Kottke, T.; Willmon, C.; Galivo, F.; Wongthida, P.; Diaz, R. M.; Thompson, J.; Ryno, P.; Barber, G.; Chester, J.; Selby, P.; Harrington, K.; Melcher, A.; Vile, R. G. Purging metastases in lymphoid organs using a combination of antigen-nonspecific adoptive T cell therapy, oncolytic virotherapy and immunotherapy. Nat. Med., 2008, 14, 37-44.
52. 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.
53. Power, A. T.; Bell, J. C. Taming the trojan horse: Optimizing dynamic carrier cell/oncolytic virus systems for cancer biotherapy. Gene Ther., 2008, 15, 772-779.
54. Thorne, S. H.; Contag, C. H. Integrating the biological characteristics of oncolytic viruses and immune cells can optimize therapeutic benefits of cell-based delivery. Gene Ther., 2008, 15, 753-758.
55. Wahl, R. L.; Jacene, H.; Kasamon, Y.; Lodge, M. A. From RECIST to PERCIST: Evolving considerations for PET response criteria in solid tumors. J. Nucl. Med., 2009, 50, 122S-150S.