Efficacy and safety/toxicity study of recombinant vaccinia virus JX-594 in two immunocompetent animal models of glioma

Molecular Therapy

Volumn 18, Issue 11, 2010, Pages 1927-1936

  Lun, Xueqing ^a,b   Chan, Jennifer ^a   Zhou, Hongyuan ^a,b   Sun, Beichen ^a,b   Kelly, John J P ^c   Stechishin, Owen Owen ^d   Bell, John C ^e,f   Parato, Kelley ^e   Hu, Kang ^e,f   Vaillant, Dominique ^e   Wang, Jiahu ^e   Liu, Ta Chiang ^f   Breitbach, Caroline ^f   Kirn, David ^f   Senger, Donna L ^a,b   Forsyth, Peter A ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c Division of Neurosurgery   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

^e OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^f Jennerex Biotherapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; JX 594; JX 594M; ONCOLYTIC MAMMALIAN ORTHOREOVIRUS; ONCOLYTIC MYXOMA VIRUS; ONCOLYTIC VESICULAR STOMATITIS VIRUS; ONCOLYTIC VIRUS; RAPAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER SURVIVAL; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENTIATION; DRUG SAFETY; DRUG TOLERABILITY; EX VIVO STUDY; FEMALE; GLIOMA; HUMAN; HUMAN CELL; IMMUNOCOMPETENCE; IN VITRO STUDY; INFLAMMATION; MONOTHERAPY; MOUSE; MULTIPLE DRUG DOSE; NECROSIS; NONHUMAN; ONCOLYTIC VIROTHERAPY; RAT; SINGLE DRUG DOSE;

ANIMALIA; MAMMALIAN ORTHOREOVIRUS 3; MURINAE; MUS; PRIMATES; RATTUS; RODENTIA; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 78049461363     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.183     Document Type: Article

References (48)

1. Martuza, RL, Malick, A, Markert, JM, Ruffner, KL and Coen, DM (1991). Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science 252: 854-856.
2. Fueyo, J, Gomez-Manzano, C, Alemany, R, Lee, PS, McDonnell, TJ, Mitlianga, P et al. (2000). A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene 19: 2-12.
3. Wilcox, ME, Yang, W, Senger, D, Rewcastle, NB, Morris, DG, Brasher, PM et al. (2001). Reovirus as an oncolytic agent against experimental human malignant gliomas. J Natl Cancer Inst 93: 903-912.
4. Gromeier, M, Lachmann, S, Rosenfeld, MR, Gutin, PH and Wimmer, E (2000). Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc Natl Acad Sci USA 97: 6803-6808.
5. Lun, X, Yang, W, Alain, T, Shi, ZQ, Muzik, H, Barrett, JW et al. (2005). Myxoma virus is a novel oncolytic virus with signifcant antitumor activity against experimental human gliomas. Cancer Res 65: 9982-9990.
6. Lun, X, Senger, DL, Alain, T, Oprea, A, Parato, K, Stojdl, D et al. (2006). Effects of intravenously administered recombinant vesicular stomatitis virus (VSV(ΔM51)) on multifocal and invasive gliomas. J Natl Cancer Inst 98: 1546-1557.
7. Markert, JM, Medlock, MD, Rabkin, SD, Gillespie, GY, Todo, T, Hunter, WD et al. (2000). Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther 7: 867-874.
8. Chiocca, EA, Abbed, KM, Tatter, S, Louis, DN, Hochberg, FH, Barker, F et al. (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: 958-966.
9. Freeman, AI, Zakay-Rones, Z, Gomori, JM, Linetsky, E, Rasooly, L, Greenbaum, E et al. (2006). Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol Ther 13: 221-228.
10. Forsyth, P, Roldán, G, George, D, Wallace, C, Palmer, CA, Morris, D et al. (2008). A phase I trial of intratumoral administration of reovirus in patients with histologically confrmed recurrent malignant gliomas. Mol Ther 16: 627-632.
11. Harrow, S, Papanastassiou, V, Harland, J, Mabbs, R, Petty, R, Fraser, M et al. (2004). HSV1716 injection into the brain adjacent to tumour following surgical resection of high-grade glioma: safety data and long-term survival. Gene Ther 11: 1648-1658.
12. Papanastassiou, V, Rampling, R, Fraser, M, Petty, R, Hadley, D, Nicoll, J et al. (2002). The potential for effcacy of the modifed (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Ther 9: 398-406.
13. Aghi, MK and Chiocca, EA (2009). Phase ib trial of oncolytic herpes virus G207 shows safety of multiple injections and documents viral replication. Mol Ther 17: 8-9.
14. Markert, JM, Liechty, PG, Wang, W, Gaston, S, Braz, E, Karrasch, M et al. (2009). Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol Ther 17: 199-207.
15. Hodge, JW, Schlom, J, Donohue, SJ, Tomaszewski, JE, Wheeler, CW, Levine, BS et al. (1995). A recombinant vaccinia virus expressing human prostate-specifc antigen (PSA): safety and immunogenicity in a non-human primate. Int J Cancer 63: 231-237.
16. Fulginiti, VA, Papier, A, Lane, JM, Neff, JM and Henderson, DA (2003). Smallpox vaccination: a review, part I. Background, vaccination technique, normal vaccination and revaccination, and expected normal reactions. Clin Infect Dis 37: 241-250.
17. Madan, RA, Arlen, PM and Gulley, JL (2007). PANVAC-VF: poxviral-based vaccine therapy targeting CEA and MUC1 in carcinoma. Expert Opin Biol Ther 7: 543-554.
18. Park, BH, Hwang, T, Liu, TC, Sze, DY, Kim, JS, Kwon, HC et al. (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: 533-542.
19. Timiryasova, TM, Li, J, Chen, B, Chong, D, Langridge, WH, Gridley, DS et al. (1999). Antitumor effect of vaccinia virus in glioma model. Oncol Res 11: 133-144.
20. Lun, XQ, Jang, JH, Tang, N, Deng, H, Head, R, Bell, JC et al. (2009). Effcacy of systemically administered oncolytic vaccinia virotherapy for malignant gliomas is enhanced by combination therapy with rapamycin or cyclophosphamide. Clin Cancer Res 15: 2777-2788.
21. McCart, JA, Puhlmann, M, Lee, J, Hu, Y, Libutti, SK, Alexander, HR et al. (2000). Complex interactions between the replicating oncolytic effect and the enzyme/ prodrug effect of vaccinia-mediated tumor regression. Gene Ther 7: 1217-1223.
22. Kim, JH, Oh, JY, Park, BH, Lee, DE, Kim, JS, Park, HE et al. (2006). Systemic armed oncolytic and immunologic therapy for cancer with JX-594, a targeted poxvirus expressing GM-CSF. Mol Ther 14: 361-370.
23. Zhang, Q, Yu, YA, Wang, E, Chen, N, Danner, RL, Munson, PJ et al. (2007). Eradication of solid human breast tumors in nude mice with an intravenously injected light-emitting oncolytic vaccinia virus. Cancer Res 67: 10038-10046.
24. Hung, CF, Tsai, YC, He, L, Coukos, G, Fodor, I, Qin, L et al. (2007). Vaccinia virus preferentially infects and controls human and murine ovarian tumors in mice. Gene Ther 14: 20-29.
25. Deng, H, Tang, N, Stief, AE, Mehta, N, Baig, E, Head, R et al. (2008). Oncolytic virotherapy for multiple myeloma using a tumour-specifc double-deleted vaccinia virus. Leukemia 22: 2261-2264.
26. McCart, JA, Ward, JM, Lee, J, Hu, Y, Alexander, HR, Libutti, SK et al. (2001). Systemic cancer therapy with a tumor-selective vaccinia virus mutant lacking thymidine kinase and vaccinia growth factor genes. Cancer Res 61: 8751-8757.
27. Naik, AM, Chalikonda, S, McCart, JA, Xu, H, Guo, ZS, Langham, G et al. (2006). Intravenous and isolated limb perfusion delivery of wild type and a tumor-selective replicating mutant vaccinia virus in nonhuman primates. Hum Gene Ther 17: 31-45.
28. Liu, TC, Hwang, T, Park, BH, Bell, J and Kirn, DH (2008). The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma. Mol Ther 16: 1637-1642.
29. Park, BH, Hwang, T, Liu, TC, Sze, DY, Kim, JS, Kwon, HC et al. (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: 533-542.
30. Yang, WQ, Lun, X, Palmer, CA, Wilcox, ME, Muzik, H, Shi, ZQ et al. (2004). Effcacy and safety evaluation of human reovirus type 3 in immunocompetent animals: racine and nonhuman primates. Clin Cancer Res 10: 8561-8576.
31. Lun, X, Alain, T, Zemp, FJ, Zhou, H, Rahman, MM, Hamilton, MG et al. (2010). Myxoma virus virotherapy for glioma in immunocompetent animal models: optimizing administration routes and synergy with rapamycin. Cancer Res 70: 598-608.
32. Alain, T, Lun, XQ, Martineau, Y, Sean, P, Pulendran, B, Petroulakis, E et al. (2010). Vesicular stomatitis virus oncolysis is potentiated by impairing mTORC1-dependent type I IFN production. Proc Natl Acad Sci USA 107: 1576-1581.
33. Gilbertson, RJ and Rich, JN (2007). Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 7: 733-736.
34. Bao, S, Wu, Q, McLendon, RE, Hao, Y, Shi, Q, Hjelmeland, AB et al. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
35. Jiang, H, Gomez-Manzano, C, Aoki, H, Alonso, MM, Kondo, S, McCormick, F et al. (2007). Examination of the therapeutic potential of Δ-24-RGD in brain tumor stem cells: role of autophagic cell death. J Natl Cancer Inst 99: 1410-1414.
36. Wakimoto, H, Kesari, S, Farrell, CJ, Curry, WT Jr, Zaupa, C, Aghi, M et al. (2009). Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 69: 3472-3481.
37. Currier, MA, Gillespie, RA, Sawtell, NM, Mahller, YY, Stroup, G, Collins, MH et al. (2008). Effcacy and safety of the oncolytic herpes simplex virus rRp450 alone and combined with cyclophosphamide. Mol Ther 16: 879-885.
38. Smith, JG, Raper, SE, Wheeldon, EB, Hackney, D, Judy, K, Wilson, JM et al. (1997). Intracranial administration of adenovirus expressing HSV-TK in combination with ganciclovir produces a dose-dependent, self-limiting infammatory response. Hum Gene Ther 8: 943-954.
39. Cello, J, Toyoda, H, Dejesus, N, Dobrikova, EY, Gromeier, M and Wimmer, E (2008). Growth phenotypes and biosafety profles in poliovirus-receptor transgenic mice of recombinant oncolytic polio/human rhinoviruses. J Med Virol 80: 352-359.
40. Todo, T, Feigenbaum, F, Rabkin, SD, Lakeman, F, Newsome, JT, Johnson, PA et al. (2000). Viral shedding and biodistribution of G207, a multimutated, conditionally replicating herpes simplex virus type 1, after intracerebral inoculation in aotus. Mol Ther 2: 588-595.
41. Myers, R, Harvey, M, Kaufmann, TJ, Greiner, SM, Krempski, JW, Raffel, C et al. (2008). Toxicology study of repeat intracerebral administration of a measles virus derivative producing carcinoembryonic antigen in rhesus macaques in support of a phase I/II clinical trial for patients with recurrent gliomas. Hum Gene Ther 19: 690-698.
42. Naganuma, H, Sasaki, A, Satoh, E, Nagasaka, M, Isoe, S, Nakano, S et al. (1997). Long-term survival in a young patient with anaplastic glioma. Brain Tumor Pathol 14: 71-74.
43. Abou-Ghazal, M, Yang, DS, Qiao, W, Reina-Ortiz, C, Wei, J, Kong, LY et al. (2008). The incidence, correlation with tumor-infltrating infammation, and prognosis of phosphorylated STAT3 expression in human gliomas. Clin Cancer Res 14: 8228-8235.
44. Blumenthal, DT, Raizer, JJ, Rosenblum, MK, Bilsky, MH, Hariharan, S and Abrey, LE (1999). Primary intracranial neoplasms in patients with HIV. Neurology 52: 1648-1651.
45. Moriyama, EH, Bisland, SK, Lilge, L and Wilson, BC (2004). Bioluminescence imaging of the response of rat gliosarcoma to ALA-PpIX-mediated photodynamic therapy. Photochem Photobiol 80: 242-249.
46. Szentirmai, O, Baker, CH, Lin, N, Szucs, S, Takahashi, M, Kiryu, S et al. (2006). Noninvasive bioluminescence imaging of luciferase expressing intracranial U87 xenografts: correlation with magnetic resonance imaging determined tumor volume and longitudinal use in assessing tumor growth and antiangiogenic treatment effect. Neurosurgery 58: 365-372; discussion 365.
47. Kelly, JJ, Stechishin, O, Chojnacki, A, Lun, X, Sun, B, Senger, DL et al. (2009). Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells 27: 1722-1733.
48. Wang, L, Rahn, JJ, Lun, X, Sun, B, Kelly, JJ, Weiss, S et al. (2008). Gamma-secretase represents a therapeutic target for the treatment of invasive glioma mediated by the p75 neurotrophin receptor. PLoS Biol 6: e289.