Mutations in the glycoprotein of vesicular stomatitis virus affect cytopathogenicity: Potential for oncolytic virotherapy

Journal of Virology

Volumn 85, Issue 13, 2011, Pages 6513-6520

  Janelle, Valérie ^a,b   Brassard, Frédérick ^b   Lapierre, Pascal ^a   Lamarre, Alain ^a,b   Poliquin, Laurent ^b  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

^b UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; G PROTEIN, VESICULAR STOMATITIS VIRUS; MEMBRANE PROTEIN; ONCOLYTIC VIRUS;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL KILLING; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOPATHOGENIC EFFECT; HOST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; RNA TRANSLATION; STRAIN DIFFERENCE; TRANSCRIPTION TERMINATION; TUMOR CELL; VESICULAR STOMATITIS VIRUS; VIRUS MUTANT; VIRUS MUTATION; WILD TYPE; ANIMAL; CERCOPITHECUS; DNA SEQUENCE; FIBROBLAST; GENETICS; HUMAN; L CELL; METABOLISM; MOLECULAR GENETICS; MUTATION; PATHOGENICITY; TUMOR CELL LINE; VERO CELL; VIROLOGY;

VESICULAR STOMATITIS VIRUS;

ANIMALS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CYTOPATHOGENIC EFFECT, VIRAL; FIBROBLASTS; HUMANS; L CELLS (CELL LINE); MEMBRANE GLYCOPROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; SEQUENCE ANALYSIS, DNA; VERO CELLS; VESICULAR STOMATITIS INDIANA VIRUS; VIRAL ENVELOPE PROTEINS;

EID: 80052067233     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02484-10     Document Type: Article

References (51)

1. Ahmed, M., and D. S. Lyles. 1998. Effect of vesicular stomatitis virus matrix protein on transcription directed by host RNA polymerases I, II, and III. J. Virol. 72:8413-8419.
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., et al. 2009. Vesicular stomatitis virus M protein mutant stimulates maturation of Toll-like receptor 7 (TLR7)-positive dendritic cells through TLR-dependent and -independent mechanisms. J. Virol. 83:2962- 2975.
4. Balachandran, S., and G. N. Barber. 2004. Defective translational control facilitates vesicular stomatitis virus oncolysis. Cancer Cell 5:51-65.
5. Balachandran, S., and G. N. Barber. 2000. Vesicular stomatitis virus (VSV) therapy of tumors. IUBMB Life 50:135-138.
6. 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 gene expression is genetically separable from its function in virus assembly. J. Virol. 67:4814-4821.
7. Bordoli, L., et al. 2009. Protein structure homology modeling using SWISSMODEL workspace. Nat. Protoc. 4:1-13.
8. Braxton, C. L., S. H. Puckett, S. B. Mizel, and D. S. Lyles. 2010. Protection against lethal vaccinia virus challenge by using an attenuated matrix protein mutant vesicular stomatitis virus vaccine vector expressing poxvirus antigens. J. Virol. 84:3552-3561.
9. Cobleigh, M. A., L. Buonocore, S. L. Uprichard, J. K. Rose, and M. D. Robek. 2010. A vesicular stomatitis virus-based hepatitis B virus vaccine vector provides protection against challenge in a single dose. J. Virol. 84: 7513-7522.
10. Connor, J. H., and D. S. Lyles. 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.
11. Desforges, M., et al. 2001. Different host-cell shutoff strategies related to the matrix protein lead to persistance of vesicular stomatitis virus mutants on fibroblast cells. Virus Res. 76:87-102.
12. Desforges, M., et al. 2002. Matrix protein mutations contribute to inefficient induction of apoptosis leading to persistent infection of human neural cells by vesicular stomatitis virus. Virology 295:63-73.
13. Ferran, M., and J. Lucas-Lenard. 1997. The vesicular stomatitis virus matrix protein inhibits transcription from the human beta interferon promoter. J. Virol. 71:371-377.
14. Flood, E. A., M. O. McKenzie, and D. S. Lyles. 2000. Role of M protein aggregation in defective assembly of temperature-sensitive M protein mutants of vesicular stomatitis virus. Virology 278:520-533.
15. Francoeur, M. A., L. Poliquin, and C. P. Stanners. 1987. The isolation of interferon-inducing mutants of vesicular stomatitis virus with altered viral P function for the inhibition of total protein synthesis. Virology 160:236-245.
16. Garcia-Sastre, A., and C. A. Biron. 2006. Type 1 Interferons and the virushost relationship: a lesson in detente. Science 312:879-882.
17. Ge, P., et al. 2010. Cryo-EM model of the bullet-shaped vesicular stomatitis virus. Science 327:689-693.
18. Geisbert, T. W., D. G. Bausch, and H. Feldmann. 2010. Prospects for immunisation against Marburg and Ebola viruses. Rev. Med. Virol. 20:344-357.
19. Georgel, P., et al. 2007. Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway. Virology 362:304- 313.
20. Glodowski, D. R., J. M. Petersen, and J. E. Dahlberg. 2002. Complex nuclear localization signals in the matrix protein of vesicular stomatitis virus. J. Biol. Chem. 277:46864-46870.
21. Grupe, A., et al. 2001. In silico mapping of complex disease-related traits in mice. Science 292:1915-1918.
22. Hoffmann, M., et al. 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.
23. 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.
24. 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.
25. 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.
26. Krissinel, E., and K. Henrick. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D 60:2256-2268.
27. Larkin, M. A., et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
28. Le Blanc, I., et al. 2005. Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7:653-664.
29. Letchworth, G. J., L. L. Rodriguez, and J. Del Cbarrera. 1999. Vesicular stomatitis. Vet. J. 157:239-260.
30. Lichty, B. D., A. T. Power, D. F. Stojdl, and J. C. Bell. 2004. Vesicular stomatitis virus: re-inventing the bullet. Trends Mol. Med. 10:211-217.
31. Lyles, D. S., L. Puddington, and B. J. J. McCreedy. 1988. Vesicular stomatitis virus M protein in the nuclei of infected cells. J. Virol. 62:4387-4392.
32. McCreedy, B. J. J., and D. S. Lyles. 1989. Distribution of M protein and nucleocapsid protein of vesicular stomatitis virus in infected cell plasma membranes. Virus Res. 14:189-205.
33. Mire, C. E., D. Dube, S. E. Delos, J. M. White, and M. A. Whitt. 2009. Glycoprotein-dependent acidification of vesicular stomatitis virus enhances release of matrix protein. J. Virol. 83:12139-12150.
34. Petersen, J. M., L. S. Her, V. Varvel, E. Lund, and J. E. Dahlberg. 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.
35. Roche, S., S. Bressanelli, F. A. Rey, and Y. Gaudin. 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187-191.
36. Roche, S., F. A. Rey, Y. Gaudin, and S. Bressanelli. 2007. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315:843-848.
37. Rose, J. K., and M. A. Whitt. 2001. Rhabdoviridae: the viruses and their replication. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
38. Schincariol, A. L., and A. F. Howatson. 1970. Replication of vesicular stomatitis virus. I. Viral specific RNA and nucleoprotein in infected L cells. Virology 42:732-743.
39. Schuler, L., X. Daura, and W. van Gunsteren. 2001. An improved GROMOS96 force field for aliphatic hydrocarbons in the condensed phase. J. Comput. Chem. 22:1205-1218.
40. Schwartz, J. A., et al. 2010. Potent vesicular stomatitis virus-based avian influenza vaccines provide long-term sterilizing immunity against heterologous challenge. J. Virol. 84:4611-4618.
41. Stark, G. R., I. M. Kerr, and B. R. Williams. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67:227-264.
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. Sun, X., V. K. Yau, B. J. Briggs, and G. R. Whittaker. 2005. Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338:53-60.
45. Swinteck, B. D., and D. S. Lyles. 2008. Plasma membrane microdomains containing vesicular stomatitis virus M protein are separate from microdomains containing G protein and nucleocapsids. J. Virol. 82:5536- 5547.
46. Vandepol, S. B., L. Lefrançois, and J. J. Holland. 1986. Sequences of the major antibody binding epitopes of the Indiana serotype of vesicular stomatitis virus. Virol. J. 148:312-325.
47. Wagner, E. K., and M. J. Hewlett. 2004. Basic virology, 2nd ed. Blackwell Science, Ames, IA.
48. Whitt, M. A. 2010. Generation of VSV pseudotypes using recombinant G-VSV for studies on virus entry, identification of entry inhibitors, and immune responses to vaccines. J. Virol. Methods 169:365-374.
49. 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.
50. Wongthida, P., et al. 2011. VSV oncolytic virotherapy in the B16 model depends upon intact MyD88 signaling. Mol. Ther. 19:150-158.
51. Ye, Z., et al. 1994. Membrane-binding domains and cytopathogenesis of the matrix protein of vesicular stomatitis virus. J. Virol. 68:7386-7396