Oncolytic vesicular stomatitis virus induces apoptosis in U87 glioblastoma cells by a type II death receptor mechanism and induces cell death and tumor clearance in vivo

Journal of Virology

Volumn 85, Issue 12, 2011, Pages 5708-5717

  Cary, Zachary D ^a   Willingham, Mark C ^a   Lyles, Douglas S ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DEATH RECEPTOR; DEATH RECEPTOR 2; FAS ANTIBODY; FAS ANTIGEN; ONCOLYTIC VESICULAR STOMATITIS VIRUS; ONCOLYTIC VIRUS; PROTEIN BCL XL; UNCLASSIFIED DRUG; VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL STRAIN U87; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA VIRUS INFECTION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; VESICULAR STOMATITIS VIRUS;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; FEMALE; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; MITOCHONDRIA; MUTATION; ONCOLYTIC VIROTHERAPY; RECEPTORS, DEATH DOMAIN; TREATMENT OUTCOME; VESICULAR STOMATITIS INDIANA VIRUS; VIRAL MATRIX PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MURINAE; VESICULAR STOMATITIS VIRUS;

EID: 79958166679     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02393-10     Document Type: Article

References (56)

1. Ahmed, M., S. D. Cramer, and D. S. Lyles. 2004. Sensitivity of prostate tumors to wild type and M protein mutant vesicular stomatitis viruses. Virology 330:34-49.
2. Ahmed, M., et al. 2003. Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J. Virol. 77:4646- 4657.
3. Ahmed, M., S. Puckett, and D. S. Lyles. 2010. Susceptibility of breast cancer cells to an oncolytic matrix (M) protein mutant of vesicular stomatitis virus. Cancer Gene Ther. 17:883-892.
4. Balachandran, S., and G. N. Barber. 2000. Vesicular stomatitis virus (VSV) therapy of tumors. IUBMB Life 50:135-138.
5. Balachandran, S., M. Porosnicu, and G. N. Barber. 2001. Oncolytic activity of vesicular stomatitis virus is effective against tumors exhibiting aberrant p53, Ras, or myc function and involves the induction of apoptosis. J. Virol. 75:3474-3479.
6. Balachandran, S., et al. 2000. Alpha/beta interferons potentiate virus-induced apoptosis through activation of the FADD/caspase-8 death signaling pathway. J. Virol. 74:1513-1523.
7. Bell, J. C., K. A. Garson, B. D. Lichty, and D. F. Stojdl. 2002. Oncolytic viruses: programmable tumour hunters. Curr. Gene Ther. 2:243-254.
8. Bianchi, M. E., and A. A. Manfredi. 2007. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol. Rev. 220:35-46.
9. Black, B. L., and D. S. Lyles. 1992. Vesicular stomatitis-virus matrix protein inhibits host cell-directed transcription of target genes in vivo. J. Virol. 66:4058-4064.
10. Black, B. L., R. B. Rhodes, M. McKenzie, and D. S. Lyles. 1993. The role of vesicular stomatitis-virus matrix protein in inhibition of host-directed geneexpression is genetically separable from its function in virus assembly. J. Virol. 67:4814-4821.
11. Cattaneo, R., T. Miest, E. V. Shashkova, and M. A. Barry. 2008. Reprogrammed viruses as cancer therapeutics: targeted, armed and shielded. Nat. Rev. Microbiol. 6:529-540.
12. Ebert, O., et al. 2004. Syncytia induction enhances the oncolytic potential of vesicular stomatitis virus in virotherapy for cancer. Cancer Res. 64:3265- 3270.
13. Ferran, M. C., and J. M. LucasLenard. 1997. The vesicular stomatitis virus matrix protein inhibits transcription from the human beta interferon promoter. J. Virol. 71:371-377.
14. Freeman, A. I., et al. 2006. Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol. Ther. 13:221-228.
15. Furnari, F. B., et al. 2007. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 21:2683-2710.
16. Gaddy, D. F., and D. S. Lyles. 2007. Oncolytic vesicular stomatitis virus induces apoptosis via signaling through PKR, Fas, and Daxx. J. Virol. 81: 2792-2804.
17. Gaddy, D. F., and D. S. Lyles. 2005. Vesicular stomatitis viruses expressing wild-type or mutant M proteins activate apoptosis through distinct pathways. J. Virol. 79:4170-4179.
18. He, S., et al. 2009. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137:1100-1111.
19. Hoffmann, D., and O. Wildner. 2007. Comparison of herpes simplex virusand conditionally replicative adenovirus-based vectors for glioblastoma treatment. Cancer Gene Ther. 14:627-639.
20. Jost, P. J., et al. 2009. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 460:1035-1039.
21. Kazama, H., et al. 2008. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 29:21-32.
22. Kopecky, S. A., and D. S. Lyles. 2003. The cell-rounding activity of the vesicular stomatitis virus matrix protein is due to the induction of cell death. J. Virol. 77:5524-5528.
23. Kopecky, S. A., and D. S. Lyles. 2003. Contrasting effects of matrix protein on apoptosis in HeLa and BHK cells infected with vesicular stomatitis virus are due to inhibition of host gene expression. J. Virol. 77:4658-4669.
24. Kopecky, S. A., M. C. Willingham, and D. S. Lyles. 2001. Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J. Virol. 75:12169-12181.
25. Krakstad, C., and M. Chekenya. 2010. Survival signalling and apoptosis resistance in glioblastomas: opportunities for targeted therapeutics. Mol. Cancer 9:135.
26. Kroemer, G., et al. 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16:3-11.
27. Lee, H. K., and A. Iwasaki. 2008. Autophagy and antiviral immunity. Curr. Opin. Immunol. 20:23-29.
28. Lee, H. K., J. M. Lund, B. Ramanathan, N. Mizushima, and A. Iwasaki. 2007. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315:1398-1401.
29. Lun, X., et al. 2006. Effects of intravenously administered recombinant vesicular stomatitis virus (VSVΔM51) on multifocal and invasive gliomas. J. Natl. Cancer Inst. 98:1546-1557.
30. Lun, X. Q., et al. 2009. Efficacy of systemically administered oncolytic vaccinia virotherapy for malignant gliomas is enhanced by combination therapy with rapamycin or cyclophosphamide. Clin. Cancer Res. 15:2777-2788.
31. Markert, J. 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.
32. Melcher, A., et al. 1998. Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat. Med. 4:581-587.
33. Myers, R., 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.
34. Ozduman, K., G. Wollmann, S. A. Ahmadi, and A. N. van den Pol. 2009. Peripheral immunization blocks lethal actions of vesicular stomatitis virus within the brain. J. Virol. 83:11540-11549.
35. Pearce, A. F., and D. S. Lyles. 2009. Vesicular stomatitis virus induces apoptosis primarily through Bak rather than Bax by inactivating Mcl-1 and Bcl-XL. J. Virol. 83:9102-9112.
36. Rieger, J., U. Naumann, T. Glaser, A. Ashkenazi, and M. Weller. 1998. APO2 ligand: a novel lethal weapon against malignant glioma? FEBS Lett. 427:124-128.
37. Rovere-Querini, P., et al. 2004. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 5:825-830.
38. Scaffidi, C., et al. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1675-1687.
39. Scaffidi, C., et al. 1999. Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J. Biol. Chem. 274:22532-22538.
40. Shah, A. C., et al. 2007. Enhanced antiglioma activity of chimeric HCMV/ HSV-1 oncolytic viruses. Gene Ther. 14:1045-1054.
41. Sharif-Askari, E., et al. 2007. Bax-dependent mitochondrial membrane permeabilization enhances IRF3-mediated innate immune response during VSV infection. Virology 365:20-33.
42. Stojdl, D. F., et al. 2000. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6:821-825.
43. Stojdl, D. F., et al. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263- 275.
44. Strik, H., et al. 1999. BCL-2 family protein expression in initial and recurrent glioblastomas: modulation by radiochemotherapy. J. Neurol. Neurosurg. Psychiatr. 67:763-768.
45. Studebaker, A. W., et al. 2010. Treatment of medulloblastoma with a modified measles virus. Neuro. Oncol. 12:1034-1042.
46. Tumilasci, V. F., et al. 2008. Targeting the apoptotic pathway with BCL-2 inhibitors sensitizes primary chronic lymphocytic leukemia cells to vesicular stomatitis virus-induced oncolysis. J. Virol. 82:8487-8499.
47. U. S. Department of Health and Human Services. 2008. Minutes of the Recombinant DNA Advisory Committee 12/3-4/2008. Recombinant DNA Advisory Committee, U. S. Department of Health and Human Services, Rockville, MD. http://oba.od.nih.gov/oba/RAC/meetings/dec2008/RAC_Minutes _12-08.pdf.
48. U. S. Department of Health and Human Services. 2008. Minutes of the Recombinant DNA Advisory Committee 9/9-10/08. Recombinant DNA Advisory Committee, U. S. Department of Health and Human Services, Rockville, MD. http://oba.od.nih.gov/oba/RAC/meetings/Sept2008/RAC_Minutes _09-08.pdf.
49. Wilkinson, J. C., E. Cepero, L. H. Boise, and C. S. Duckett. 2004. Upstream regulatory role for XIAP in receptor-mediated apoptosis. Mol. Cell. Biol. 24:7003-7014.
50. Wilkinson, J. C., et al. 2004. VIAF, a conserved inhibitor of apoptosis (IAP)-interacting factor that modulates caspase activation. J. Biol. Chem. 279:51091-51099.
51. Wollmann, G., M. D. Robek, and A. N. van den Pol. 2007. Variable deficiencies in the interferon response enhance susceptibility to vesicular stomatitis virus oncolytic actions in glioblastoma cells but not in normal human glial cells. J. Virol. 81:1479-1491.
52. Wollmann, G., V. Rogulin, I. Simon, J. K. Rose, and A. N. van den Pol. 2010. Some attenuated variants of vesicular stomatitis virus show enhanced oncolytic activity against human glioblastoma cells relative to normal brain cells. J. Virol. 84:1563-1573.
53. Wollmann, G., P. Tattersall, and A. N. van den Pol. 2005. Targeting human glioblastoma cells: comparison of nine viruses with oncolytic potential. J. Virol. 79:6005-6022.
54. Yin, X. M. 2000. Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways. Cell Res. 10:161-167.
55. Yin, X. M., et al. 1999. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400:886-891.
56. Zemp, F. J., J. C. Corredor, X. Lun, D. A. Muruve, and P. A. Forsyth. 2010. Oncolytic viruses as experimental treatments for malignant gliomas: using a scourge to treat a devil. Cytokine Growth Factor Rev. 21:103-117.