Neuroattenuation of vesicular stomatitis virus through picornaviral internal ribosome entry sites

Journal of Virology

Volumn 87, Issue 6, 2013, Pages 3217-3228

  Ammayappan, Arun ^a   Nace, Rebecca ^a   Peng, Kah Whye ^a   Russell, Stephen J ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; FOOT AND MOUTH DISEASE VIRUS; GENE ACTIVITY; GENE FUNCTION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN RHINOVIRUS; HUMAN RHINOVIRUS TYPE 2; IN VITRO STUDY; IN VIVO STUDY; INTERNAL RIBOSOME ENTRY SITE; M GENE; MOUSE; NEUROTOXICITY; NONHUMAN; PICORNAVIRUS; PRIORITY JOURNAL; VESICULAR STOMATITIS; VESICULAR STOMATITIS VIRUS; VIRUS ATTENUATION; VIRUS GENE; VIRUS TRANSCRIPTION; VIRUS VIRULENCE;

ANIMALS; CELL LINE; FOOT-AND-MOUTH DISEASE VIRUS; GENE EXPRESSION REGULATION, VIRAL; HUMANS; ONCOLYTIC VIRUSES; PROTEIN BIOSYNTHESIS; RECOMBINATION, GENETIC; RHINOVIRUS; VESICULOVIRUS; VIRAL MATRIX PROTEINS;

EID: 84874707250     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02984-12     Document Type: Article

References (57)

1. Alajez NM, Mocanu JD, Shi W, Chia MC, Breitbach CJ, Hui AB, Knowles S, Bell JC, Busson P, Takada K, Lo KW, O'Sullivan B, Gullane P, Liu FF. 2008. Efficacy of systemically administered mutant vesicular stomatitis virus (VSVDelta51) combined with radiation for nasopharyngeal carcinoma. Clin. Cancer Res. 14:4891-4897.
2. Naik S, Nace R, Federspiel MJ, Barber GN, Peng KW, Russell SJ. 2012. Curative one-shot systemic virotherapy in murine myeloma. Leukemia 26:1870-1878.
3. Shinozaki K, Ebert O, Woo SL. 2005. Treatment of multi-focal colorectal carcinoma metastatic to the liver of immune-competent and syngeneic rats by hepatic artery infusion of oncolytic vesicular stomatitis virus. Int. J. Cancer 114:659-664.
4. Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N, Bell JC. 2000. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6:821-825.
5. Willmon CL, Saloura V, Fridlender ZG, Wongthida P, Diaz RM, Thompson J, Kottke T, Federspiel M, Barber G, Albelda SM, Vile RG. 2009. Expression of IFN-beta enhances both efficacy and safety of oncolytic vesicular stomatitis virus for therapy of mesothelioma. Cancer Res. 69:7713-7720.
6. Letchworth GJ, Rodriguez LL, Del cbarrera J. 1999. Vesicular stomatitis. Vet. J. 157:239-260.
7. Newcomb WW, Tobin GJ, McGowan JJ, Brown JC. 1982. In vitro reassembly of vesicular stomatitis virus skeletons. J. Virol. 41:1055-1062.
8. Jayakar HR, Murti KG, Whitt MA. 2000. Mutations in the PPPY motif of vesicular stomatitis virus matrix protein reduce virus budding by inhibiting a late step in virion release. J. Virol. 74:9818-9827.
9. Petersen JM, Her LS, Varvel V, Lund E, Dahlberg JE. 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.
10. Stojdl DF, Lichty BD, tenOever BR, Paterson JM, Power AT, Knowles S, Marius R, Reynard J, Poliquin L, Atkins H, Brown EG, Durbin RK, Durbin JE, Hiscott J, Bell JC. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
11. Barber GN. 2004. Vesicular stomatitis virus as an oncolytic vector. Viral Immunol. 17:516-527.
12. Rabinowitz SG, Huprikar J, Dal Canto MC. 1981. Comparative neurovirulence of selected vesicular stomatitis virus temperature-sensitive mutants of complementation groups II and III. Infect. Immun. 33:120-125.
13. Reiss CS, Plakhov IV, 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.
14. 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.
15. Obuchi M, Fernandez M, Barber GN. 2003. Development of recombinant vesicular stomatitis viruses that exploit defects in host defense to augment specific oncolytic activity. J. Virol. 77:8843-8856.
16. Kelly EJ, Nace R, Barber GN, Russell SJ. 2010. Attenuation of vesicular stomatitis virus encephalitis through microRNA targeting. J. Virol. 84: 1550-1562.
17. 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. 90:959-970.
18. Ayala-Breton C, Barber GN, Russell SJ, Peng KW. 2012. Retargeting vesicular stomatitis virus using measles virus envelope glycoproteins. Hum. Gene Ther. 23:484-491.
19. Muik A, Kneiske I, Werbizki M, Wilflingseder D, Giroglou T, Ebert O, Kraft A, Dietrich U, Zimmer G, Momma S, von Laer D. 2011. Pseudotyping vesicular stomatitis virus with lymphocytic choriomeningitis virus glycoproteins enhances infectivity for glioma cells and minimizes neurotropism. J. Virol. 85:5679-5684.
20. Jang SK, Davies MV, Kaufman RJ, Wimmer E. 1989. Initiation of protein synthesis by internal entry of ribosomes into the 5= nontranslated region of encephalomyocarditis virusRNAin vivo. J. Virol. 63:1651-1660.
21. Kozak M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
22. Kuhn R, Luz N, Beck E. 1990. Functional analysis of the internal translation initiation site of foot-and-mouth disease virus. J. Virol. 64:4625-4631.
23. Pelletier J, Sonenberg N. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:320-325.
24. Belsham GJ, Sonenberg N. 2000. Picornavirus RNA translation: roles for cellular proteins. Trends Microbiol. 8:330-335.
25. Lopez-Lastra M, Rivas A, Barria MI. 2005. Protein synthesis in eukaryotes: the growing biological relevance of cap-independent translation initiation. Biol. Res. 38:121-146.
26. Pyronnet S, Pradayrol L, Sonenberg N. 2000. A cell cycle-dependent internal ribosome entry site. Mol. Cell 5:607-616.
27. Merrill MK, Dobrikova EY, Gromeier M. 2006. Cell-type-specific repression of internal ribosome entry site activity by double-stranded RNAbinding protein 76. J. Virol. 80:3147-3156.
28. Gromeier M, Alexander L, Wimmer E. 1996. Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc. Natl. Acad. Sci. U. S. A. 93:2370-2375.
29. Campbell SA, Mulvey M, Mohr I, Gromeier M. 2007. Attenuation of herpes simplex virus neurovirulence with picornavirus cis-acting genetic elements. J. Virol. 81:791-799.
30. Marschalek A, Finke S, Schwemmle M, Mayer D, Heimrich B, Stitz L, Conzelmann KK. 2009. Attenuation of rabies virus replication and virulence by picornavirus internal ribosome entry site elements. J. Virol. 83: 1911-1919.
31. Lawson ND, Stillman EA, Whitt MA, Rose JK. 1995. Recombinant vesicular stomatitis viruses from DNA. Proc. Natl. Acad. Sci. U. S. A. 92:4477-4481.
32. Finney, DJ. 1964. Statistical methods in biological assay, 2nd ed. Hafner, New York, NY.
33. Storey DG, Kang CY. 1985. Vesicular stomatitis virus-infected cells fuse when the intracellular pool of functional M protein is reduced in the presence of G protein. J. Virol. 53:374-383.
34. Takehara M. 1975. Polykaryocytosis induced by vesicular stomatitis virus infection in BHK-21 cells. Arch. Virol. 49:297-306.
35. Ahmed M, Cramer SD, Lyles DS. 2004. Sensitivity of prostate tumors to wild type and M protein mutant vesicular stomatitis viruses. Virology 330:34-49.
36. Pilipenko EV, Pestova TV, Kolupaeva VG, Khitrina EV, Poperechnaya AN, Agol VI, Hellen CU. 2000. A cell cycle-dependent protein serves as a template-specific translation initiation factor. Genes Dev. 14:2028-2045.
37. Faul EJ, Lyles DS, Schnell MJ. 2009. Interferon response and viral evasion by members of the family rhabdoviridae. Viruses 1:832-851.
38. Albertini AA, Baquero E, Ferlin A, Gaudin Y. 2012. Molecular and cellular aspects of rhabdovirus entry. Viruses 4:117-139.
39. Fearns R, Collins PL. 1999. Role of the M2-1 transcription antitermination protein of respiratory syncytial virus in sequential transcription. J. Virol. 73:5852-5864.
40. Iverson LE, Rose JK. 1981. Localized attenuation and discontinuous synthesis during vesicular stomatitis virus transcription. Cell 23:477-484.
41. Duntsch CD, Zhou Q, Jayakar HR, Weimar JD, Robertson JH, Pfeffer LM, Wang L, Xiang Z, Whitt MA. 2004. Recombinant vesicular stomatitis virus vectors as oncolytic agents in the treatment of high-grade gliomas in an organotypic brain tissue slice-glioma coculture model. J. Neurosurg. 100:1049-1059.
42. Goel A, Carlson SK, Classic KL, Greiner S, Naik S, Power AT, Bell JC, Russell SJ. 2007. Radioiodide imaging and radiovirotherapy of multiple myeloma using VSV(Delta51)-NIS, an attenuated vesicular stomatitis virus encoding the sodium iodide symporter gene. Blood 110:2342-2350.
43. Hadaschik BA, Zhang K, So AI, Fazli L, Jia W, Bell JC, Gleave ME, Rennie PS. 2008. Oncolytic vesicular stomatitis viruses are potent agents for intravesical treatment of high-risk bladder cancer. Cancer Res. 68: 4506-4510.
44. Lichty BD, Stojdl DF, Taylor RA, Miller L, Frenkel I, Atkins H, Bell JC. 2004. Vesicular stomatitis virus: a potential therapeutic virus for the treatment of hematologic malignancy. Hum. Gene Ther. 15:821-831.
45. Ebert O, Harbaran S, Shinozaki K, Woo SL. 2005. Systemic therapy of experimental breast cancer metastases by mutant vesicular stomatitis virus in immune-competent mice. Cancer Gene Ther. 12:350-358.
46. Wu L, Huang TG, Meseck M, Altomonte J, Ebert O, Shinozaki K, Garcia-Sastre A, Fallon J, Mandeli J, Woo SL. 2008. rVSV(M Delta 51)-M3 is an effective and safe oncolytic virus for cancer therapy. Hum. Gene Ther. 19:635-647.
47. Paglino JC, van den Pol AN. 2011. Vesicular stomatitis virus has extensive oncolytic activity against human sarcomas: rare resistance is overcome by blocking interferon pathways. J. Virol. 85:9346-9358.
48. Alain T, Lun X, Martineau Y, Sean P, Pulendran B, Petroulakis E, Zemp FJ, Lemay CG, Roy D, Bell JC, Thomas G, Kozma SC, Forsyth PA, Costa-Mattioli M, Sonenberg N. 2010. Vesicular stomatitis virus oncolysis is potentiated by impairing mTORC1-dependent type I IFN production. Proc. Natl. Acad. Sci. U. S. A. 107:1576-1581.
49. Diallo JS, Le Boeuf F, Lai F, Cox J, Vaha-Koskela M, Abdelbary H, MacTavish H, Waite K, Falls T, Wang J, Brown R, Blanchard JE, Brown ED, Kirn DH, Hiscott J, Atkins H, Lichty BD, Bell JC. 2010. A highthroughput pharmacoviral approach identifies novel oncolytic virus sensitizers. Mol. Ther. 18:1123-1129.
50. Cawood R, Chen HH, Carroll F, Bazan-Peregrino M, van Rooijen N, Seymour LW. 2009. Use of tissue-specific microRNA to control pathology of wild-type adenovirus without attenuation of its ability to kill cancer cells. PLoS Pathog. 5:e1000440. doi:10.1371/journal.ppat.1000440.
51. Edge RE, Falls TJ, Brown CW, Lichty BD, Atkins H, Bell JC. 2008. A let-7 MicroRNA-sensitive vesicular stomatitis virus demonstrates tumorspecific replication. Mol. Ther. 16:1437-1443.
52. Kelly EJ, Hadac EM, Greiner S, Russell SJ. 2008. Engineering microRNA responsiveness to decrease virus pathogenicity. Nat. Med. 14:1278-1283.
53. Ylosmaki E, Hakkarainen T, Hemminki A, Visakorpi T, Andino R, Saksela K. 2008. Generation of a conditionally replicating adenovirus based on targeted destruction of E1A mRNA by a cell type-specific MicroRNA. J. Virol. 82:11009-11015.
54. Kubo T, Shimose S, Matsuo T, Fujimori J, Sakaguchi T, Yamaki M, Shinozaki K, Woo SL, Ochi M. 2011. Oncolytic vesicular stomatitis virus administered by isolated limb perfusion suppresses osteosarcoma growth. J. Orthop. Res. 29:795-800.
55. Cesaire R, Oliere S, Sharif-Askari E, Loignon M, Lezin A, Olindo S, Panelatti G, Kazanji M, Aloyz R, Panasci L, Bell JC, Hiscott J. 2006. Oncolytic activity of vesicular stomatitis virus in primary adult T-cell leukemia. Oncogene 25:349-358.
56. Murphy AM, Besmer DM, Moerdyk-Schauwecker M, Moestl N, Ornelles DA, Mukherjee P, Grdzelishvili VZ. 2012. Vesicular stomatitis virus as an oncolytic agent against pancreatic ductal adenocarcinoma. J. Virol. 86:3073-3087.
57. Ausubel LJ, Meseck M, Derecho I, Lopez P, Knoblauch C, McMahon R, Anderson J, Dunphy N, Quezada V, Khan R, Huang P, Dang W, Luo M, Hsu D, Woo SL, Couture L. 2011. Current good manufacturing practice production of an oncolytic recombinant vesicular stomatitis viral vector for cancer treatment. Hum. Gene Ther. 22:489-497.