Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer

Journal of General Virology

Volumn 93, Issue PART 12, 2012, Pages 2529-2545

  Hastie, Eric ^a   Grdzelishvili, Valery Z ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; BETA INTERFERON; FLUCYTOSINE; GANCICLOVIR; GLYCOPROTEIN; HYBRID PROTEIN; INTERFERON; IODINE 131; MICRORNA; OBATOCLAX; RECOMBINANT VESICULAR STOMATITIS VIRUS; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; VIROTHERAPY AGENT;

AMINO ACID SUBSTITUTION; B CELL LYMPHOMA; BLISTER; BRAIN CANCER; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER RESISTANCE; CELL CYCLE; CELL DIVISION; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; DENDRITIC CELL; ENCEPHALITIS; FEVER; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GLIOBLASTOMA; IMMUNE RESPONSE; IMMUNITY; INNATE IMMUNITY; LIVER CELL CARCINOMA; LIVER TUMOR; LIVESTOCK; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MELANOMA; MESOTHELIOMA; MONOTHERAPY; MULTIMODALITY CANCER THERAPY; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NEUROTROPISM; NONHUMAN; NOSE MUCOSA; ONCOLYTIC VIROTHERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; REPORTER GENE; REVERSE GENETICS; REVIEW; RNA VIRUS; T LYMPHOCYTE; TUMOR IMMUNITY; UTERINE CERVIX CARCINOMA; VESICULAR STOMATITIS; VESICULAR STOMATITIS VIRUS; VIRUS NUCLEOCAPSID; VIRUS RECOMBINANT; VIRUS TRANSCRIPTION;

ANIMALS; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; RECOMBINATION, GENETIC; VESICULOVIRUS;

RNA VIRUSES; VESICULAR STOMATITIS VIRUS;

EID: 84869217555     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.046672-0     Document Type: Review

References (156)

1. Alain, T., Lun, X., Martineau, Y., Sean, P., Pulendran, B., Petroulakis, E., Zemp, F. J., Lemay, C. G., Roy, D. & other authors (2010). Vesicular stomatitis virus oncolysis is potentiated by impairing mTORC1-dependent type I IFN production. Proc Natl Acad Scis U S A 107, 1576-1581.
2. Altomonte, J., Braren, R., Schulz, S., Marozin, S., Rummeny, E. J., Schmid, R. M. & Ebert, O. (2008a). Synergistic antitumor effects of transarterial viroembolization for multifocal hepatocellular carcinoma in rats. Hepatology 48, 1864-1873.
3. Altomonte, J., Wu, L., Chen, L., Meseck, M., Ebert, O., García-Sastre, A., Fallon, J. & Woo, S. L. (2008b). Exponential enhancement of oncolytic vesicular stomatitis virus potency by vector-mediated suppression of inflammatory responses in vivo. Mol Ther 16, 146-153.
4. Altomonte, J., Wu, L., Meseck, M., Chen, L., Ebert, O., Garcia-Sastre, A., Fallon, J., Mandeli, J. & Woo, S. L. (2009). Enhanced oncolytic potency of vesicular stomatitis virus through vector-mediated inhibition of NK and NKT cells. Cancer Gene Ther 16, 266-278.
5. Ausubel, L. J., Meseck, M., Derecho, I., Lopez, P., Knoblauch, C., McMahon, R., Anderson, J., Dunphy, N., Quezada, V. & other authors (2011). Current good manufacturing practice production of an oncolytic recombinant vesicular stomatitis viral vector for cancer treatment. Hum Gene Ther 22, 489-497.
6. Ayala-Breton, C., Barber, G. N., Russell, S. J. & Peng, K. W. (2012). Retargeting vesicular stomatitis virus using measles virus envelope glycoproteins. Hum Gene Ther 23, 484-491.
7. Balachandran, S. & Barber, G. N. (2004). Defective translational control facilitates vesicular stomatitis virus oncolysis. Cancer Cell 5, 51-65.
8. Balachandran, S. & Barber, G. N. (2007). PKR in innate immunity, cancer, and viral oncolysis. Methods Mol Biol 383, 277-301.
9. Ball, L. A., Pringle, C. R., Flanagan, B., Perepelitsa, V. P. & Wertz, G. W. (1999). Phenotypic consequences of rearranging the P, M, and G genes of vesicular stomatitis virus. J Virol 73, 4705-4712.
10. Barber, G. N. (2004). Vesicular stomatitis virus as an oncolytic vector. Viral Immunol 17, 516-527.
11. Barber, G. N. (2005). VSV-tumor selective replication and protein translation. Oncogene 24, 7710-7719.
12. Bergman, I., Griffin, J. A., Gao, Y. & Whitaker-Dowling, P. (2007). Treatment of implanted mammary tumors with recombinant vesicular stomatitis virus targeted to Her2/neu. Int J Cancer 121, 425-430.
13. Bi, Z., Barna, M., Komatsu, T. & Reiss, C. S. (1995). Vesicular stomatitis virus infection of the central nervous system activates both innate and acquired immunity. J Virol 69, 6466-6472.
14. Black, B. L., Rhodes, R. B., McKenzie, M. & Lyles, D. S. (1993). The role of vesicular stomatitis virus matrix protein in inhibition of hostdirected gene expression is genetically separable from its function in virus assembly. J Virol 67, 4814-4821.
15. Boudreau, J. E., Bridle, B. W., Stephenson, K. B., Jenkins, K. M., Brunelliere, J., Bramson, J. L., Lichty, B. D. & Wan, Y. (2009). Recombinant vesicular stomatitis virus transduction of dendritic cells enhances their ability to prime innate and adaptive antitumor immunity. Mol Ther 17, 1465-1472.
16. Breitbach, C. J., De Silva, N. S., Falls, T. J., Aladl, U., Evgin, L., Paterson, J., Sun, Y. Y., Roy, D. G., Rintoul, J. L. & other authors (2011). Targeting tumor vasculature with an oncolytic virus. Mol Ther 19, 886-894.
17. Bridle, B. W., Stephenson, K.B., Boudreau, J.E., Koshy, S., Kazdhan, N., Pullenayegum, E., Brunelliere, J., Bramson, J. L., Lichty, B. D. & Wan, Y. (2010). Potentiating cancer immunotherapy using an oncolytic virus. Mol Ther 18, 1430-1439.
18. Brown, C. W., Stephenson, K. B., Hanson, S., Kucharczyk, M., Duncan, R., Bell, J. C. & Lichty, B. D. (2009). The p14 FAST protein of reptilian reovirus increases vesicular stomatitis virus neuropathogenesis. J Virol 83, 552-561.
19. Cary, Z. D., Willingham, M. C. & Lyles, D. S. (2011). 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 85, 5708-5717.
20. Chakraborty, P., Seemann, J., Mishra, R. K., Wei, J. H., Weil, L., Nussenzveig, D. R., Heiber, J., Barber, G. N., Dasso, M. & Fontoura, B. M. (2009). Vesicular stomatitis virus inhibits mitotic progression and triggers cell death. EMBO Rep 10, 1154-1160.
21. Chang, G., Xu, S., Watanabe, M., Jayakar, H. R., Whitt, M. A. & Gingrich, J. R. (2010). Enhanced oncolytic activity of vesicular stomatitis virus encoding SV5-F protein against prostate cancer. J Urol 183, 1611-1618.
22. Chauhan, V. S., Furr, S. R., Sterka, D. G., Jr, Nelson, D. A., Moerdyk-Schauwecker, M., Marriott, I. & Grdzelishvili, V. Z. (2010). Vesicular stomatitis virus infects resident cells of the central nervous system and induces replication-dependent inflammatory responses. Virology 400, 187-196.
23. Chelbi-Alix, M. K., Quignon, F., Pelicano, L., Koken, M. H. & de Thé, H. (1998). Resistance to virus infection conferred by the interferoninduced promyelocytic leukemia protein. J Virol 72, 1043-1051.
24. Connor, J. H. & Lyles, D. S. (2002). Vesicular stomatitis virus infection alters the eIF4F translation initiation complex and causes dephosphorylation of the eIF4E binding protein 4E-BP1. J Virol 76, 10177-10187.
25. Coulon, P., Deutsch, V., Lafay, F., Martinet-Edelist, C., Wyers, F., Herman, R. C. & Flamand, A. (1990). Genetic evidence for multiple functions of the matrix protein of vesicular stomatitis virus. J Gen Virol 71, 991-996.
26. Cripe, T. P., Wang, P. Y., Marcato, P., Mahller, Y. Y. & Lee, P. W. (2009). Targeting cancer-initiating cells with oncolytic viruses. Mol Ther 17, 1677-1682.
27. Cureton, D. K., Massol, R. H., Whelan, S. P. & Kirchhausen, T. (2010). The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLoS Pathog 6, e1001127.
28. Dal Canto, M. C., Rabinowitz, S. G. & Johnson, T. C. (1976). Status spongiosus resulting from intracerebral infection of mice with temperature-sensitive mutants of vesicular stomatitis virus. Br J Exp Pathol 57, 321-330.
29. Dalton, K. P. & Rose, J. K. (2001). Vesicular stomatitis virus glycoprotein containing the entire green fluorescent protein on its cytoplasmic domain is incorporated efficiently into virus particles. Virology 279, 414-421.
30. Diallo, J. S., Vähä-Koskela, M., Le Boeuf, F. & Bell, J. (2012). Propagation, purification, and in vivo testing of oncolytic vesicular stomatitis virus strains. Methods Mol Biol 797, 127-140.
31. Diaz, R. M., Galivo, F., Kottke, T., Wongthida, P., Qiao, J., Thompson, J., Valdes, M., Barber, G. & Vile, R. G. (2007). Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res 67, 2840-2848.
32. Dinh, P. X., Beura, L. K., Panda, D., Das, A. & Pattnaik, A. K. (2011). Antagonistic effects of cellular poly(C) binding proteins on vesicular stomatitis virus gene expression. J Virol 85, 9459-9471.
33. Drolet, B. S., Stuart, M. A. & Derner, J. D. (2009). Infection of Melanoplus sanguinipes grasshoppers following ingestion of rangeland plant species harboring vesicular stomatitis virus. Appl Environ Microbiol 75, 3029-3033.
34. Ebert, O., Shinozaki, K., Kournioti, C., Park, M. S., García-Sastre, A. & Woo, S. L. (2004). Syncytia induction enhances the oncolytic potential of vesicular stomatitis virus in virotherapy for cancer. Cancer Res 64, 3265-3270.
35. Edge, R. E., Falls, T. J., Brown, C. W., Lichty, B. D., Atkins, H. & Bell, J. C. (2008). A let-7 microRNA-sensitive vesicular stomatitis virus demonstrates tumor-specific replication. Mol Ther 16, 1437-1443.
36. Egan, M. A., Chong, S. Y., Rose, N. F., Megati, S., Lopez, K. J., Schadeck, E. B., Johnson, J. E., Masood, A., Piacente, P. & other authors (2004). Immunogenicity of attenuated vesicular stomatitis virus vectors expressing HIV type 1 Env and SIV Gag proteins: comparison of intranasal and intramuscular vaccination routes. AIDS Res Hum Retroviruses 20, 989-1004.
37. Faria, P. A., Chakraborty, P., Levay, A., Barber, G. N., Ezelle, H. J., Enninga, J., Arana, C., van Deursen, J. & Fontoura, B. M. (2005). VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol Cell 17, 93-102.
38. Fernandez, M., Porosnicu, M., Markovic, D. & Barber, G. N. (2002). Genetically engineered vesicular stomatitis virus in gene therapy: application for treatment of malignant disease. J Virol 76, 895-904.
39. Finke, S. & Conzelmann, K. K. (2005). Recombinant rhabdoviruses: vectors for vaccine development and gene therapy. Curr Top Microbiol Immunol 292, 165-200.
40. Flanagan, E. B., Zamparo, J. M., Ball, L. A., Rodriguez, L. L. & Wertz, G. W. (2001). Rearrangement of the genes of vesicular stomatitis virus eliminates clinical disease in the natural host: new strategy for vaccine development. J Virol 75, 6107-6114.
41. Frei, K., Malipiero, U. V., Leist, T. P., Zinkernagel, R. M., Schwab, M. E. & Fontana, A. (1989). On the cellular source and function of interleukin 6 produced in the central nervous system in viral diseases. Eur J Immunol 19, 689-694.
42. Friedman, G. K., Cassady, K. A., Beierle, E. A., Markert, J. M. & Gillespie, G. Y. (2012). Targeting pediatric cancer stem cells with oncolytic virotherapy. Pediatr Res 71, 500-510.
43. Furr, S. R., Chauhan, V. S., Sterka, D., Jr, Grdzelishvili, V. Z. & Marriott, I. (2008). Characterization of retinoic acid-inducible gene-I expression in primary murine glia following exposure to vesicular stomatitis virus. J Neurovirol 14, 503-513.
44. Furr, S. R., Moerdyk-Schauwecker, M., Grdzelishvili, V. Z. & Marriott, I. (2010). RIG-I mediates nonsegmented negative-sense RNA virusinduced inflammatory immune responses of primary human astrocytes. Glia 58, 1620-1629.
45. Gaddy, D. F. & Lyles, D. S. (2005). Vesicular stomatitis viruses expressing wild-type or mutant M proteins activate apoptosis through distinct pathways. J Virol 79, 4170-4179.
46. Gaddy, D. F. & Lyles, D. S. (2007). Oncolytic vesicular stomatitis virus induces apoptosis via signaling through PKR, Fas, and Daxx. J Virol 81, 2792-2804.
47. Galivo, F., Diaz, R. M., Thanarajasingam, U., Jevremovic, D., Wongthida, P., Thompson, J., Kottke, T., Barber, G. N., Melcher, A. & Vile, R. G. (2010). Interference of CD40L-mediated tumor immunotherapy by oncolytic vesicular stomatitis virus. Hum Gene Ther 21, 439-450.
48. Gao, Y., Whitaker-Dowling, P., Watkins, S. C., Griffin, J. A. & Bergman, I. (2006). Rapid adaptation of a recombinant vesicular stomatitis virus to a targeted cell line. J Virol 80, 8603-8612.
49. Garber, K. (2006). China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst 98, 298-300.
50. Ge, P., Tsao, J., Schein, S., Green, T. J., Luo, M. & Zhou, Z. H. (2010). Cryo-EM model of the bullet-shaped vesicular stomatitis virus. Science 327, 689-693.
51. Georgel, P., Jiang, Z., Kunz, S., Janssen, E., Mols, J., Hoebe, K., Bahram, S., Oldstone, M. B. & Beutler, B. (2007). Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway. Virology 362, 304-313.
52. + regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 56, 641-648.
53. Goel, A., Carlson, S. K., Classic, K. L., Greiner, S., Naik, S., Power, A. T., Bell, J. C. & Russell, S. J. (2007). Radioiodide imaging and radiovirotherapy of multiple myeloma using VSV(D51)-NIS, an attenuated vesicular stomatitis virus encoding the sodium iodide symporter gene. Blood 110, 2342-2350.
54. Hamacher, R., Schmid, R. M., Saur, D. & Schneider, G. (2008). Apoptotic pathways in pancreatic ductal adenocarcinoma. Mol Cancer 7, 64.
55. Hammill, A. M., Conner, J. & Cripe, T. P. (2010). Oncolytic virotherapy reaches adolescence. Pediatr Blood Cancer 55, 1253-1263.
56. Hanahan, D. & Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
57. Hansen, D. E., Thurmond, M. C. & Thorburn, M. (1985). Factors associated with the spread of clinical vesicular stomatitis in California dairy cattle. Am J Vet Res 46, 789-795.
58. Harashima, A., Guettouche, T. & Barber, G. N. (2010). Phosphorylation of the NFAR proteins by the dsRNA-dependent protein kinase PKR constitutes a novel mechanism of translational regulation and cellular defense. Genes Dev 24, 2640-2653.
59. Heiber, J. F. & Barber, G. N. (2011). Vesicular stomatitis virus expressing tumor suppressor p53 is a highly attenuated, potent oncolytic agent. J Virol 85, 10440-10450.
60. Heinrich, B. S., Cureton, D. K., Rahmeh, A. A. & Whelan, S. P. (2010). Protein expression redirects vesicular stomatitis virus RNA synthesis to cytoplasmic inclusions. PLoS Pathog 6, e1000958.
61. Hoffmann, M., Wu, Y. J., Gerber, M., Berger-Rentsch, M., Heimrich, B., Schwemmle, M. & Zimmer, G. (2010). Fusion-active glycoprotein G mediates the cytotoxicity of vesicular stomatitis virus M mutants lacking host shut-off activity. J Gen Virol 91, 2782-2793.
62. Hornung, V., Ellegast, J., Kim, S., Brzózka, K., Jung, A., Kato, H., Poeck, H., Akira, S., Conzelmann, K. K. & other authors (2006). 59-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997.
63. Huneycutt, B. S., Bi, Z., Aoki, C. J. & Reiss, C. S. (1993). Central neuropathogenesis of vesicular stomatitis virus infection of immunodeficient mice. J Virol 67, 6698-6706.
64. Ikeda, K., Wakimoto, H., Ichikawa, T., Jhung, S., Hochberg, F. H., Louis, D. N. & Chiocca, E. A. (2000). Complement depletion facilitates the infection of multiple brain tumors by an intravascular, replication-conditional herpes simplex virus mutant. J Virol 74, 4765-4775.
65. Irie, T., Carnero, E., Okumura, A., García-Sastre, A. & Harty, R. N. (2007). Modifications of the PSAP region of the matrix protein lead to attenuation of vesicular stomatitis virus in vitro and in vivo. J Gen Virol 88, 2559-2567.
66. Janelle, V., Brassard, F., Lapierre, P., Lamarre, A. & Poliquin, L. (2011). Mutations in the glycoprotein of vesicular stomatitis virus affect cytopathogenicity: potential for oncolytic virotherapy. J Virol 85, 6513-6520.
67. Jenks, N., Myers, R., Greiner, S. M., Thompson, J., Mader, E. K., Greenslade, A., Griesmann, G. E., Federspiel, M. J., Rakela, J. & other authors (2010). Safety studies on intrahepatic or intratumoral injection of oncolytic vesicular stomatitis virus expressing interferonb in rodents and nonhuman primates. Hum Gene Ther 21, 451-462.
68. Jensen, H., Andresen, L., Nielsen, J., Christensen, J. P. & Skov, S. (2011). Vesicular stomatitis virus infection promotes immune evasion by preventing NKG2D-ligand surface expression. PLoS ONE 6, e23023.
69. Johnson, J. E., Nasar, F., Coleman, J. W., Price, R. E., Javadian, A., Draper, K., Lee, M., Reilly, P. A., Clarke, D. K. & other authors (2007). Neurovirulence properties of recombinant vesicular stomatitis virus vectors in non-human primates. Virology 360, 36-49.
70. Kelly, E. & Russell, S. J. (2007). History of oncolytic viruses: genesis to genetic engineering. Mol Ther 15, 651-659.
71. Kelly, E. J., Nace, R., Barber, G. N. & Russell, S. J. (2010). Attenuation of vesicular stomatitis virus encephalitis through microRNA targeting. J Virol 84, 1550-1562.
72. Kopecky, S. A., Willingham, M. C. & Lyles, D. S. (2001). Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J Virol 75, 12169-12181.
73. Kottke, T., Diaz, R. M., Kaluza, K., Pulido, J., Galivo, F., Wongthida, P., Thompson, J., Willmon, C., Barber, G. N. & other authors (2008a). Use of biological therapy to enhance both virotherapy and adoptive T-cell therapy for cancer. Mol Ther 16, 1910-1918.
74. Kottke, T., Galivo, F., Wongthida, P., Diaz, R. M., Thompson, J., Jevremovic, D., Barber, G. N., Hall, G., Chester, J. & other authors (2008b). Treg depletion-enhanced IL-2 treatment facilitates therapy of established tumors using systemically delivered oncolytic virus. Mol Ther 16, 1217-1226.
75. Kottke, T., Hall, G., Pulido, J., Diaz, R. M., Thompson, J., Chong, H., Selby, P., Coffey, M., Pandha, H. & other authors (2010). Antiangiogenic cancer therapy combined with oncolytic virotherapy leads to regression of established tumors in mice. J Clin Invest 120, 1551-1560.
76. Krishnamoorthy, J., Mounir, Z., Raven, J. F. & Koromilas, A. E. (2008). The eIF2a kinases inhibit vesicular stomatitis virus replication independently of eIF2alpha phosphorylation. Cell Cycle 7, 2346-2351.
77. Labib, M., Zamay, A. S., Muharemagic, D., Chechik, A., Bell, J. C. & Berezovski, M. V. (2012). Electrochemical sensing of aptamerfacilitated virus immunoshielding. Anal Chem 84, 1677-1686.
78. Lawson, N. D., Stillman, E. A., Whitt, M. A. & Rose, J. K. (1995). Recombinant vesicular stomatitis viruses from DNA. Proc Natl Acad Sci U S A 92, 4477-4481.
79. Le Boeuf, F., Diallo, J. S., McCart, J. A., Thorne, S., Falls, T., Stanford, M., Kanji, F., Auer, R., Brown, C. W. & other authors (2010). Synergistic interaction between oncolytic viruses augments tumor killing. Mol Ther 18, 888-895.
80. Le Boeuf, F., Niknejad, N., Wang, J., Auer, R., Weberpals, J. I., Bell, J. C. & Dimitroulakos, J. (2012). Sensitivity of cervical carcinoma cells to vesicular stomatitis virus-induced oncolysis: potential role of human papilloma virus infection. Int J Cancer 131, E204-E215.
81. Leveille, S., Goulet, M. L., Lichty, B. D. & Hiscott, J. (2011a). Vesicular stomatitis virus oncolytic treatment interferes with tumor-associated dendritic cell functions and abrogates tumor antigen presentation. J Virol 85, 12160-12169.
82. Leveille, S., Samuel, S., Goulet, M. L. & Hiscott, J. (2011b). Enhancing VSV oncolytic activity with an improved cytosine deaminase suicide gene strategy. Cancer Gene Ther 18, 435-443.
83. Li, Q. & Tainsky, M. A. (2011). Epigenetic silencing of IRF7 and/or IRF5 in lung cancer cells leads to increased sensitivity to oncolytic viruses. PLoS ONE 6, e28683.
84. Lichty, B. D., Power, A. T., Stojdl, D. F. & Bell, J. C. (2004). Vesicular stomatitis virus: re-inventing the bullet. Trends Mol Med 10, 210-216.
85. Linge, C., Gewert, D., Rossmann, C., Bishop, J. A. & Crowe, J. S. (1995). Interferon system defects in human malignant melanoma. Cancer Res 55, 4099-4104.
86. Lyles, D. S. & Rupprecht, C. E. (2007). Rhabdoviridae. In Fields Virology, 5th edn, pp. 1363-1408. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
87. Marozin, S., Altomonte, J., Stadler, F., Thasler, W. E., Schmid, R. M. & Ebert, O. (2008). Inhibition of the IFN-b response in hepatocellular carcinoma by alternative spliced isoform of IFN regulatory factor-3. Mol Ther 16, 1789-1797.
88. Marozin, S., De Toni, E. N., Rizzani, A., Altomonte, J., Junger, A., Schneider, G., Thasler, W. E., Kato, N., Schmid, R. M. & Ebert, O. (2010). Cell cycle progression or translation control is not essential for vesicular stomatitis virus oncolysis of hepatocellular carcinoma. PLoS ONE 5, e10988.
89. Martinez, I., Rodriguez, L. L., Jimenez, C., Pauszek, S. J. & Wertz, G. W. (2003). Vesicular stomatitis virus glycoprotein is a determinant of pathogenesis in swine, a natural host. J Virol 77, 8039-8047.
90. Matin, S. F., Rackley, R. R., Sadhukhan, P. C., Kim, M. S., Novick, A. C. & Bandyopadhyay, S. K. (2001). Impaired a-interferon signaling in transitional cell carcinoma: lack of p48 expression in 5637 cells. Cancer Res 61, 2261-2266.
91. Melcher, A., Parato, K., Rooney, C. M. & Bell, J. C. (2011). Thunder and lightning: immunotherapy and oncolytic viruses collide. Mol Ther 19, 1008-1016.
92. Miller, J., Bidula, S. M., Jensen, T. M. & Reiss, C. S. (2009). Cytokinemodified VSV is attenuated for neural pathology, but is both highly immunogenic and oncolytic. Int J Infereron Cytokine Mediator Res 1, 15-32.
93. Miller, J. M., Bidula, S. M., Jensen, T. M. & Reiss, C. S. (2010). Vesicular stomatitis virus modified with single chain IL-23 exhibits oncolytic activity against tumor cells in vitro and in vivo. Int J Infereron Cytokine Mediator Res 2010, 63-72.
94. Mire, C. E. & Whitt, M. A. (2011). The protease-sensitive loop of the vesicular stomatitis virus matrix protein is involved in virus assembly and protein translation. Virology 416, 16-25.
95. Moerdyk-Schauwecker, M., Destephanis, D., Hastie, E. & Grdzelishvili, V. Z. (2011). Detecting protein-protein interactions in vesicular stomatitis virus using a cytoplasmic yeast two hybrid system. J Virol Methods 173, 203-212.
96. Moussavi, M., Fazli, L., Tearle, H., Guo, Y., Cox, M., Bell, J., Ong, C., Jia, W. & Rennie, P. S. (2010). Oncolysis of prostate cancers induced by vesicular stomatitis virus in PTEN knockout mice. Cancer Res 70, 1367-1376.
97. Muik, A., Kneiske, I., Werbizki, M., Wilflingseder, D., Giroglou, T., Ebert, O., Kraft, A., Dietrich, U., Zimmer, G. & other authors (2011). Pseudotyping vesicular stomatitis virus with lymphocytic choriomeningitis virus glycoproteins enhances infectivity for glioma cells and minimizes neurotropism. J Virol 85, 5679-5684.
98. Muik, A., Dold, C., Geiß, Y., Volk, A., Werbizki, M., Dietrich, U. & von Laer, D. (2012). Semireplication-competent vesicular stomatitis virus as a novel platform for oncolytic virotherapy. J Mol Med (Berl) 90, 959-970.
99. Murphy, A. M., Besmer, D. M., Moerdyk-Schauwecker, M., Moestl, N., Ornelles, D. A., Mukherjee, P. & Grdzelishvili, V. Z. (2012). Vesicular stomatitis virus as an oncolytic agent against pancreatic ductal adenocarcinoma. J Virol 86, 3073-3087.
100. Naik, S. & Russell, S. J. (2009). Engineering oncolytic viruses to exploit tumor specific defects in innate immune signaling pathways. Expert Opin Biol Ther 9, 1163-1176.
101. Naik, S., Nace, R., Federspiel, M. J., Barber, G. N., Peng, K. W. & Russell, S. J. (2012). Curative one-shot systemic virotherapy in murine myeloma. Leukemia 26, 1870-1878.
102. Nakashima, H., Kaur, B. & Chiocca, E. A. (2010). Directing systemic oncolytic viral delivery to tumors via carrier cells. Cytokine Growth Factor Rev 21, 119-126.
103. Nguyên, T. L., Abdelbary, H., Arguello, M., Breitbach, C., Leveille, S., Diallo, J. S., Yasmeen, A., Bismar, T. A., Kirn, D. & other authors (2008). Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proc Natl Acad Sci U S A 105, 14981-14986.
104. Noser, J. A., Mael, A. A., Sakuma, R., Ohmine, S., Marcato, P., Lee, P. W. & Ikeda, Y. (2007). The RAS/Raf1/MEK/ERK signaling pathway facilitates VSV-mediated oncolysis: implication for the defective interferon response in cancer cells. Mol Ther 15, 1531-1536.
105. Obuchi, M., Fernandez, M. & Barber, G. N. (2003). Development of recombinant vesicular stomatitis viruses that exploit defects in host defense to augment specific oncolytic activity. J Virol 77, 8843-8856.
106. Oliere, S., Arguello, M., Mesplede, T., Tumilasci, V., Nakhaei, P., Stojdl, D., Sonenberg, N., Bell, J. & Hiscott, J. (2008). Vesicular stomatitis virus oncolysis of T lymphocytes requires cell cycle entry and translation initiation. J Virol 82, 5735-5749.
107. Ozduman, K., Wollmann, G., Ahmadi, S. A. & van den Pol, A. N. (2009). Peripheral immunization blocks lethal actions of vesicular stomatitis virus within the brain. J Virol 83, 11540-11549.
108. Pearson, A. S., Koch, P. E., Atkinson, N., Xiong, M., Finberg, R. W., Roth, J. A. & Fang, B. (1999). Factors limiting adenovirus-mediated gene transfer into human lung and pancreatic cancer cell lines. Clin Cancer Res 5, 4208-4213.
109. Peng, K. W., Myers, R., Greenslade, A., Mader, E., Greiner, S., Federspiel, M. J., Dispenzieri, A. & Russell, S. J. (2012). Using clinically approved cyclophosphamide regimens to control the humoral immune response to oncolytic viruses. Gene Ther (in press). doi:10.1038/gt.2012.31
110. Petersen, J. M., Her, L. S., Varvel, V., Lund, E. & Dahlberg, J. E. (2000). The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol Cell Biol 20, 8590-8601.
111. Pfeffer, L. M., Wang, C., Constantinescu, S. N., Croze, E., Blatt, L. M., Albino, A. P. & Nanus, D. M. (1996). Human renal cancers resistant to IFN's antiproliferative action exhibit sensitivity to IFN's geneinducing and antiviral actions. J Urol 156, 1867-1871.
112. Plakhov, I. V., Arlund, E. E., Aoki, C. & Reiss, C. S. (1995). The earliest events in vesicular stomatitis virus infection of the murine olfactory neuroepithelium and entry of the central nervous system. Virology 209, 257-262.
113. Porosnicu, M., Mian, A. & Barber, G. N. (2003). The oncolytic effect of recombinant vesicular stomatitis virus is enhanced by expression of the fusion cytosine deaminase/uracil phosphoribosyltransferase suicide gene. Cancer Res 63, 8366-8376.
114. Power, A. T. & Bell, J. C. (2007). Cell-based delivery of oncolytic viruses: a new strategic alliance for a biological strike against cancer. Mol Ther 15, 660-665.
115. Power, A. T. & Bell, J. C. (2008). Taming the Trojan horse: optimizing dynamic carrier cell/oncolytic virus systems for cancer biotherapy. Gene Ther 15, 772-779.
116. Pulido, J., Kottke, T., Thompson, J., Galivo, F., Wongthida, P., Diaz, R. M., Rommelfanger, D., Ilett, E., Pease, L. & other authors (2012). Using virally expressed melanoma cDNA libraries to identify tumorassociated antigens that cure melanoma. Nat Biotechnol 30, 337-343.
117. Qiao, J., Wang, H., Kottke, T., Diaz, R. M., Willmon, C., Hudacek, A., Thompson, J., Parato, K., Bell, J. & other authors (2008a). Loading of oncolytic vesicular stomatitis virus onto antigen-specific T cells enhances the efficacy of adoptive T-cell therapy of tumors. Gene Ther 15, 604-616.
118. Qiao, J., Wang, H., Kottke, T., White, C., Twigger, K., Diaz, R. M., Thompson, J., Selby, P., de Bono, J. & other authors (2008b). Cyclophosphamide facilitates antitumor efficacy against subcutaneous tumors following intravenous delivery of reovirus. Clin Cancer Res 14, 259-269.
119. Quiroz, E., Moreno, N., Peralta, P. H. & Tesh, R. B. (1988). A human case of encephalitis associated with vesicular stomatitis virus (Indiana serotype) infection. Am J Trop Med Hyg 39, 312-314.
120. Reiss, C. S., Plakhov, I. V. & Komatsu, T. (1998). Viral replication in olfactory receptor neurons and entry into the olfactory bulb and brain. Ann N Y Acad Sci 855, 751-761.
121. Rieder, M. & Conzelmann, K. K. (2009). Rhabdovirus evasion of the interferon system. J Interferon Cytokine Res 29, 499-510.
122. Rose, N. F., Marx, P. A., Luckay, A., Nixon, D. F., Moretto, W. J., Donahoe, S. M., Montefiori, D., Roberts, A., Buonocore, L. & Rose, J. K. (2001). An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106, 539-549.
123. Saloura, V., Wang, L. C., Fridlender, Z. G., Sun, J., Cheng, G., Kapoor, V., Sterman, D. H., Harty, R. N., Okumura, A. & other authors (2010). Evaluation of an attenuated vesicular stomatitis virus vector expressing interferon-beta for use in malignant pleural mesothelioma: heterogeneity in interferon responsiveness defines potential efficacy. Hum Gene Ther 21, 51-64.
124. Samuel, S., Tumilasci, V. F., Oliere, S., Nguyên, T. L., Shamy, A., Bell, J. & Hiscott, J. (2010). VSV oncolysis in combination with the BCL-2 inhibitor obatoclax overcomes apoptosis resistance in chronic lymphocytic leukemia. Mol Ther 18, 2094-2103.
125. Sarojini, S., Theofanis, T. & Reiss, C. S. (2011). Interferon-induced tetherin restricts vesicular stomatitis virus release in neurons. DNA Cell Biol 30, 965-974.
126. Schache, P., Gürlevik, E., Strüver, N., Woller, N., Malek, N., Zender, L., Manns, M., Wirth, T., Kühnel, F. & Kubicka, S. (2009). VSV virotherapy improves chemotherapy by triggering apoptosis due to proteasomal degradation of Mcl-1. Gene Ther 16, 849-861.
127. Schellekens, H., Smiers-de Vreede, E., de Reus, A. & Dijkema, R. (1984). Antiviral activity of interferon in rats and the effect of immune suppression. J Gen Virol 65, 391-396.
128. Schnell, M. J., Buonocore, L., Kretzschmar, E., Johnson, E. & Rose, J. K. (1996). Foreign glycoproteins expressed from recombinant vesicular stomatitis viruses are incorporated efficiently into virus particles. Proc Natl Acad Sci U S A 93, 11359-11365.
129. Sharif-Askari, E., Nakhaei, P., Oliere, S., Tumilasci, V., Hernandez, E., Wilkinson, P., Lin, R., Bell, J. & Hiscott, J. (2007). Bax-dependent mitochondrial membrane permeabilization enhances IRF3-mediated innate immune response during VSV infection. Virology 365, 20-33.
130. Shi, Z., Cai, Z., Sanchez, A., Zhang, T., Wen, S., Wang, J., Yang, J., Fu, S. & Zhang, D. (2011). A novel Toll-like receptor that recognizes vesicular stomatitis virus. J Biol Chem 286, 4517-4524.
131. Shin, E. J., Wanna, G. B., Choi, B., Aguila, D., III, Ebert, O., Genden, E. M. & Woo, S. L. (2007a). Interleukin-12 expression enhances vesicular stomatitis virus oncolytic therapy in murine squamous cell carcinoma. Laryngoscope 117, 210-214.
132. Shin, E. J., Chang, J. I., Choi, B., Wanna, G., Ebert, O., Genden, E. M. & Woo, S. L. (2007b). Fusogenic vesicular stomatitis virus for the treatment of head and neck squamous carcinomas. Otolaryngol Head Neck Surg 136, 811-817.
133. Shinozaki, K., Ebert, O., Suriawinata, A., Thung, S. N. & Woo, S. L. (2005). Prophylactic alpha interferon treatment increases the therapeutic index of oncolytic vesicular stomatitis virus virotherapy for advanced hepatocellular carcinoma in immune-competent rats. J Virol 79, 13705-13713.
134. Staeheli, P. & Pavlovic, J. (1991). Inhibition of vesicular stomatitis virus mRNA synthesis by human MxA protein. J Virol 65, 4498-4501.
135. Stanifer, M. L., Cureton, D. K. & Whelan, S. P. (2011). A recombinant vesicular stomatitis virus bearing a lethal mutation in the glycoprotein gene uncovers a second site suppressor that restores fusion. J Virol 85, 8105-8115.
136. Stephenson, K. B., Barra, N. G., Davies, E., Ashkar, A. A. & Lichty, B. D. (2012). Expressing human interleukin-15 from oncolytic vesicular stomatitis virus improves survival in a murine metastatic colon adenocarcinoma model through the enhancement of antitumor immunity. Cancer Gene Ther 19, 238-246.
137. Stojdl, D. F., Lichty, B., Knowles, S., Marius, R., Atkins, H., Sonenberg, N. & Bell, J. C. (2000). Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat Med 6, 821-825.
138. Stojdl, D. F., Lichty, B. D., tenOever, B. R., Paterson, J. M., Power, A. T., Knowles, S., Marius, R., Reynard, J., Poliquin, L. & other authors (2003). VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4, 263-275.
139. Sun, W. H., Pabon, C., Alsayed, Y., Huang, P. P., Jandeska, S., Uddin, S., Platanias, L. C. & Rosen, S. T. (1998). Interferon-a resistance in a cutaneous T-cell lymphoma cell line is associated with lack of STAT1 expression. Blood 91, 570-576.
140. Tumilasci, V. F., Oliere, S., Nguyên, T. L., Shamy, A., Bell, J. & Hiscott, J. (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.
141. van den Pol, A. N., Dalton, K. P. & Rose, J. K. (2002). Relative neurotropism of a recombinant rhabdovirus expressing a green fluorescent envelope glycoprotein. J Virol 76, 1309-1327.
142. Wang, B. X., Rahbar, R. & Fish, E. N. (2011). Interferon: current status and future prospects in cancer therapy. J Interferon Cytokine Res 31, 545-552.
143. Weidner, J. M., Jiang, D., Pan, X. B., Chang, J., Block, T. M. & Guo, J. T. (2010). Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J Virol 84, 12646-12657.
144. Whelan, S. P., Ball, L. A., Barr, J. N. & Wertz, G. T. (1995). Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. Proc Natl Acad Sci U S A 92, 8388-8392.
145. Whitlow, Z. W., Connor, J. H. & Lyles, D. S. (2006). Preferential translation of vesicular stomatitis virus mRNAs is conferred by transcription from the viral genome. J Virol 80, 11733-11742.
146. Whitlow, Z. W., Connor, J. H. & Lyles, D. S. (2008). New mRNAs are preferentially translated during vesicular stomatitis virus infection. J Virol 82, 2286-2294.
147. Willmon, C., Diaz, R. M., Wongthida, P., Galivo, F., Kottke, T., Thompson, J., Albelda, S., Harrington, K., Melcher, A. & Vile, R. (2011). Vesicular stomatitis virus-induced immune suppressor cells generate antagonism between intratumoral oncolytic virus and cyclophosphamide. Mol Ther 19, 140-149.
148. Wollmann, G., Tattersall, P. & van den Pol, A. N. (2005). Targeting human glioblastoma cells: comparison of nine viruses with oncolytic potential. J Virol 79, 6005-6022.
149. Wollmann, G., Rogulin, V., Simon, I., Rose, J. K. & van den Pol, A. N. (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.
150. Wong, L. H., Krauer, K. G., Hatzinisiriou, I., Estcourt, M. J., Hersey, P., Tam, N. D., Edmondson, S., Devenish, R. J. & Ralph, S. J. (1997). Interferon-resistant human melanoma cells are deficient in ISGF3 components, STAT1, STAT2, and p48-ISGF3c. J Biol Chem 272, 28779-28785.
151. Wongthida, P., Diaz, R. M., Galivo, F., Kottke, T., Thompson, J., Pulido, J., Pavelko, K., Pease, L., Melcher, A. & Vile, R. (2010). Type III IFN interleukin-28 mediates the antitumor efficacy of oncolytic virus VSV in immune-competent mouse models of cancer. Cancer Res 70, 4539-4549.
152. Wongthida, P., Diaz, R. M., Galivo, F., Kottke, T., Thompson, J., Melcher, A. & Vile, R. (2011a). VSV oncolytic virotherapy in the B16 model depends upon intact MyD88 signaling. Mol Ther 19, 150-158.
153. Wongthida, P., Diaz, R. M., Pulido, C., Rommelfanger, D., Galivo, F., Kaluza, K., Kottke, T., Thompson, J., Melcher, A. & Vile, R. (2011b). Activating systemic T-cell immunity against self tumor antigens to support oncolytic virotherapy with vesicular stomatitis virus. Hum Gene Ther 22, 1343-1353.
154. Wu, L., Huang, T. G., Meseck, M., Altomonte, J., Ebert, O., Shinozaki, K., García-Sastre, A., Fallon, J., Mandeli, J. & Woo, S. L. (2008). rVSV(MD51)-M3 is an effective and safe oncolytic virus for cancer therapy. Hum Gene Ther 19, 635-647.
155. Yuan, H., Puckett, S. & Lyles, D. S. (2001). Inhibition of host transcription by vesicular stomatitis virus involves a novel mechanism that is independent of phosphorylation of TATA-binding protein (TBP) or association of TBP with TBP-associated factor subunits. J Virol 75, 4453-4458.
156. Zhang, K. X., Matsui, Y., Hadaschik, B. A., Lee, C., Jia, W., Bell, J. C., Fazli, L., So, A. I. & Rennie, P. S. (2010). Down-regulation of type I interferon receptor sensitizes bladder cancer cells to vesicular stomatitis virus-induced cell death. Int J Cancer 127, 830-838.