Refined methods for propagating vesicular stomatitis virus vectors that are defective for G protein expression

Journal of Virological Methods

Volumn 164, Issue 1-2, 2010, Pages 43-50

  Witko, Susan E ^a   Johnson, J Erik ^a   Kalyan, Narender K ^a   Felber, Barbara K ^b   Pavlakis, George N ^b   Sidhu, Maninder K ^a   Hendry, R Michael ^a,c   Udem, Stephen A ^a,d   Parks, Christopher L ^a,e  

^a PFIZER INC   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d Vaccine Design and Development Laboratory ^*  (United States)

^e INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

Author keywords

Electroporation; Heat shock; Negative strand RNA virus; Non propagating; Vero cells; VSV

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; PLASMID DNA; VIRUS VECTOR;

ARTICLE; BIOTECHNOLOGY; CONTROLLED STUDY; DEFECTIVE VIRUS; DNA INTEGRATION; ELECTROPORATION; GENETIC COMPLEMENTATION; GENETIC MANIPULATION; GENETIC TRANSCRIPTION; LARGE SCALE PRODUCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROCESS TECHNOLOGY; PROTEIN EXPRESSION; TRANSIENT EXPRESSION; VERO CELL; VESICULAR STOMATITIS VIRUS; VIRUS PARTICLE; VIRUS TITRATION;

ANIMALS; CERCOPITHECUS AETHIOPS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENETIC VECTORS; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VERO CELLS; VESICULOVIRUS; VIRAL ENVELOPE PROTEINS; VIRUS CULTIVATION;

RNA VIRUSES; VESICULAR STOMATITIS VIRUS;

EID: 77549084677     PISSN: 01660934     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jviromet.2009.11.023     Document Type: Article

References (82)

1. In: Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Siedman J.G., Smith J.A., and Struhl K. (Eds). Current Protocols in Molecular Biology (1987), Greene Publishing Associates and Wiley Interscience, New York
2. Barnes L.M., and Dickson A.J. Mammalian cell factories for efficient and stable protein expression. Curr. Opin. Biotechnol. 17 (2006) 381-386
3. Blanchard E., Brand D., and Roingeard P. Endogenous virus and hepatitis C virus-like particle budding in BHK-21 cells. J. Virol. 77 (2003) 3888-3889 (Author reply 3889)
4. Boshart M., Weber F., Jahn G., Dorsch-Hasler K., Fleckenstein B., and Schaffner W. A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41 (1985) 521-530
5. Bukreyev A., Skiadopoulos M.H., Murphy B.R., and Collins P.L. Nonsegmented negative-strand viruses as vaccine vectors. J. Virol. 80 (2006) 10293-10306
6. Chan S.Y. Characterization of recombinant BHK-21 endogenous particles: R-type particles. Biologicals 22 (1994) 121-125
7. Clarke D.K., Cooper D., Egan M.A., Hendry R.M., Parks C.L., and Udem S.A. Recombinant vesicular stomatitis virus as an HIV-1 vaccine vector. Springer Semin. Immunopathol. 28 (2006) 239-253
8. Compans R.W., Holmes K.V., Dales S., and Choppin P.W. An electron microscopic study of moderate and virulent virus-cell interactions of the parainfluenza virus SV5. Virology 30 (1966) 411-426
9. Cooper, D., Witko, S.E., Calderon, P.C., Wright, K.J., Johnson, J.E., Guo, M., Kotash, C.S., Nowak, R.M., Natuk, R.J., Hendry, R.M., Udem, S.A., Parks, C.L., in preparation. Evaluation neurovirulence, immunogenicity, and in vitro packaging of two types of propagation-defective vesicular stomatitis virus vaccine vectors.
10. Corbel S.Y., and Rossi F.M. Latest developments and in vivo use of the Tet system: ex vivo and in vivo delivery of tetracycline-regulated genes. Curr. Opin. Biotechnol. 13 (2002) 448-452
11. Cronin J., Zhang X.Y., and Reiser J. Altering the tropism of lentiviral vectors through pseudotyping. Curr. Gene Ther. 5 (2005) 387-398
12. Daddario-DiCaprio K.M., Geisbert T.W., Geisbert J.B., Stroher U., Hensley L.E., Grolla A., Fritz E.A., Feldmann F., Feldmann H., and Jones S.M. Cross-protection against Marburg virus strains by using a live, attenuated recombinant vaccine. J. Virol. 80 (2006) 9659-9666
13. Daddario-DiCaprio K.M., Geisbert T.W., Stroher U., Geisbert J.B., Grolla A., Fritz E.A., Fernando L., Kagan E., Jahrling P.B., Hensley L.E., Jones S.M., and Feldmann H. Postexposure protection against Marburg haemorrhagic fever with recombinant vesicular stomatitis virus vectors in non-human primates: an efficacy assessment. Lancet 367 (2006) 1399-1404
14. DuBridge R.B., Tang P., Hsia H.C., Leong P.M., Miller J.H., and Calos M.P. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7 (1987) 379-387
15. Egan M.A., Chong S.Y., Megati S., Montefiori D.C., Rose N.F., Boyer J.D., Sidhu M.K., Quiroz J., Rosati M., Schadeck E.B., Pavlakis G.N., Weiner D.B., Rose J.K., Israel Z.R., Udem S.A., and Eldridge J.H. Priming with plasmid DNAs expressing interleukin-12 and simian immunodeficiency virus gag enhances the immunogenicity and efficacy of an experimental AIDS vaccine based on recombinant vesicular stomatitis virus. AIDS Res. Hum. Retroviruses 21 (2005) 629-643
16. Egan M.A., Chong S.Y., Rose N.F., Megati S., Lopez K.J., Schadeck E.B., Johnson J.E., Masood A., Piacente P., Druilhet R.E., Barras P.W., Hasselschwert D.L., Reilly P., Mishkin E.M., Montefiori D.C., Lewis M.G., Clarke D.K., Hendry R.M., Marx P.A., Eldridge J.H., Udem S.A., Israel Z.R., and Rose J.K. 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 (2004) 989-1004
17. Emiliusen L., Gough M., Bateman A., Ahmed A., Voellmy R., Chester J., Diaz R.M., Harrington K., and Vile R. A transcriptional feedback loop for tissue-specific expression of highly cytotoxic genes which incorporates an immunostimulatory component. Gene Ther. 8 (2001) 987-998
18. Feldmann H., Jones S.M., Daddario-DiCaprio K.M., Geisbert J.B., Stroher U., Grolla A., Bray M., Fritz E.A., Fernando L., Feldmann F., Hensley L.E., and Geisbert T.W. Effective post-exposure treatment of Ebola infection. PLoS Pathog. 3 (2007) e2
19. Finke S., and Conzelmann K.K. Recombinant rhabdoviruses: vectors for vaccine development and gene therapy. Curr. Top. Microbiol. Immunol. 292 (2005) 165-200
20. Fratantoni J.C., Dzekunov S., Singh V., and Liu L.N. A non-viral gene delivery system designed for clinical use. Cytotherapy 5 (2003) 208-210
21. GlaxoSmithKline. Rotarix (Rotavirus Vaccine, Live, Oral) Oral Suspension (2008), FDA. http://www.fda.gov/Cber/products/rotarix.htm
22. Gossen M., and Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 5547-5551
23. Graf M., Bojak A., Deml L., Bieler K., Wolf H., and Wagner R. Concerted action of multiple cis-acting sequences is required for Rev dependence of late human immunodeficiency virus type 1 gene expression. J. Virol. 74 (2000) 10822-10826
24. Grigera P.R., Marzocca M.P., Capozzo A.V., Buonocore L., Donis R.O., and Rose J.K. Presence of bovine viral diarrhea virus (BVDV) E2 glycoprotein in VSV recombinant particles and induction of neutralizing BVDV antibodies in mice. Virus Res. 69 (2000) 3-15
25. Jalah R., Rosati M., Kulkarni V., Patel V., Bergamaschi C., Valentin A., Zhang G.M., Sidhu M.K., Eldridge J.H., Weiner D.B., Pavlakis G.N., and Felber B.K. Efficient systemic expression of bioactive IL-15 in mice upon delivery of optimized DNA expression plasmids. DNA Cell Biol. 26 (2007) 827-840
26. Jayakar H.R., Jeetendra E., and Whitt M.A. Rhabdovirus assembly and budding. Virus Res. 106 (2004) 117-132
27. Jeetendra E., Ghosh K., Odell D., Li J., Ghosh H.P., and Whitt M.A. The membrane-proximal region of vesicular stomatitis virus glycoprotein G ectodomain is critical for fusion and virus infectivity. J. Virol. 77 (2003) 12807-12818
28. Jeetendra E., Robison C.S., Albritton L.M., and Whitt M.A. The membrane-proximal domain of vesicular stomatitis virus G protein functions as a membrane fusion potentiator and can induce hemifusion. J. Virol. 76 (2002) 12300-12311
29. Jones S.M., Feldmann H., Stroher U., Geisbert J.B., Fernando L., Grolla A., Klenk H.D., Sullivan N.J., Volchkov V.E., Fritz E.A., Daddario K.M., Hensley L.E., Jahrling P.B., and Geisbert T.W. Live attenuated recombinant vaccine protects nonhuman primates against Ebola and Marburg viruses. Nat. Med. 11 (2005) 786-790
30. Kahn J.S., Roberts A., Weibel C., Buonocore L., and Rose J.K. Replication-competent or attenuated, nonpropagating vesicular stomatitis viruses expressing respiratory syncytial virus (RSV) antigens protect mice against RSV challenge. J. Virol. 75 (2001) 11079-11087
31. Kapadia S.U., Simon I.D., and Rose J.K. SARS vaccine based on a replication-defective recombinant vesicular stomatitis virus is more potent than one based on a replication-competent vector. Virology 376 (2008) 165-172
32. Kaur J., Tang R.S., Spaete R.R., and Schickli J.H. Optimization of plasmid-only rescue of highly attenuated and temperature-sensitive respiratory syncytial virus (RSV) vaccine candidates for human trials. J. Virol. Methods (2008)
33. Klas S.D., Lavine C.L., Whitt M.A., and Miller M.A. IL-12-assisted immunization against Listeria monocytogenes using replication-restricted VSV-based vectors. Vaccine 24 (2006) 1451-1461
34. Klas S.D., Robison C.S., Whitt M.A., and Miller M.A. Adjuvanticity of an IL-12 fusion protein expressed by recombinant deltaG-vesicular stomatitis virus. Cell Immunol. 218 (2002) 59-73
35. Kochetov A.V., Ischenko I.V., Vorobiev D.G., Kel A.E., Babenko V.N., Kisselev L.L., and Kolchanov N.A. Eukaryotic mRNAs encoding abundant and scarce proteins are statistically dissimilar in many structural features. FEBS Lett. 440 (1998) 351-355
36. Kozak M. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266 (1991) 19867-19870
37. Kroeger P.E., and Morimoto R.I. Selection of new HSF1 and HSF2 DNA-binding sites reveals difference in trimer cooperativity. Mol. Cell. Biol. 14 (1994) 7592-7603
38. Kudla G., Lipinski L., Caffin F., Helwak A., and Zylicz M. High guanine and cytosine content increases mRNA levels in mammalian cells. PLoS Biol. 4 (2006) e180
39. Lawson N.D., Stillman E.A., Whitt M.A., and Rose J.K. Recombinant vesicular stomatitis viruses from DNA. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 4477-4481
40. Majid A.M., Ezelle H., Shah S., and Barber G.N. Evaluating replication-defective vesicular stomatitis virus as a vaccine vehicle. J. Virol. 80 (2006) 6993-7008
41. Maldarelli F., Martin M.A., and Strebel K. Identification of posttranscriptionally active inhibitory sequences in human immunodeficiency virus type 1 RNA: novel level of gene regulation. J. Virol. 65 (1991) 5732-5743
42. Meier J.L., and Stinski M.F. Regulation of human cytomegalovirus immediate-early gene expression. Intervirology 39 (1996) 331-342
43. Merck. RotaTeq (Rotavirus Vaccine, Live, Oral, Petavalent) (2006), FDA. http://www.fda.gov/cber/products/rotateq.htm
44. Nasioulas G., Zolotukhin A.S., Tabernero C., Solomin L., Cunningham C.P., Pavlakis G.N., and Felber B.K. Elements distinct from human immunodeficiency virus type 1 splice sites are responsible for the Rev dependence of env mRNA. J. Virol. 68 (1994) 2986-2993
45. Olsen H.S., Cochrane A.W., and Rosen C. Interaction of cellular factors with intragenic cis-acting repressive sequences within the HIV genome. Virology 191 (1992) 709-715
46. Oomens A.G., Megaw A.G., and Wertz G.W. Infectivity of a human respiratory syncytial virus lacking the SH, G, and F proteins is efficiently mediated by the vesicular stomatitis virus G protein. J. Virol. 77 (2003) 3785-3798
47. Publicover J., Ramsburg E., and Rose J.K. A single-cycle vaccine vector based on vesicular stomatitis virus can induce immune responses comparable to those generated by a replication-competent vector. J. Virol. 79 (2005) 13231-13238
48. Reese M.G., Eeckman F.H., Kulp D., and Haussler D. Improved splice site detection in Genie. J. Comput. Biol. 4 (1997) 311-323
49. Roberts A., Buonocore L., Price R., Forman J., and Rose J.K. Attenuated vesicular stomatitis viruses as vaccine vectors. J. Virol. 73 (1999) 3723-3732
50. Roberts A., Kretzschmar E., Perkins A.S., Forman J., Price R., Buonocore L., Kawaoka Y., and Rose J.K. Vaccination with a recombinant vesicular stomatitis virus expressing an influenza virus hemagglutinin provides complete protection from influenza virus challenge. J. Virol. 72 (1998) 4704-4711
51. Robison C.S., and Whitt M.A. The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. J. Virol. 74 (2000) 2239-2246
52. Rome C., Couillaud F., and Moonen C.T. Spatial and temporal control of expression of therapeutic genes using heat shock protein promoters. Methods 35 (2005) 188-198
53. Rose J.K., and Whitt M.A. Rhabdoviradae: the viruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology vol. 1 (2001), Lippincott Williams and Wilkins, Philadelphia 1221-1244
54. Rose N.F., Marx P.A., Luckay A., Nixon D.F., Moretto W.J., Donahoe S.M., Montefiori D., Roberts A., Buonocore L., and Rose J.K. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106 (2001) 539-549
55. Rose N.F., Roberts A., Buonocore L., and Rose J.K. Glycoprotein exchange vectors based on vesicular stomatitis virus allow effective boosting and generation of neutralizing antibodies to a primary isolate of human immunodeficiency virus type 1. J. Virol. 74 (2000) 10903-10910
56. Schlereth B., Rose J.K., Buonocore L., ter Meulen V., and Niewiesk S. Successful vaccine-induced seroconversion by single-dose immunization in the presence of measles virus-specific maternal antibodies. J. Virol. 74 (2000) 4652-4657
57. Schneider R., Campbell M., Nasioulas G., Felber B.K., and Pavlakis G.N. Inactivation of the human immunodeficiency virus type 1 inhibitory elements allows Rev-independent expression of Gag and Gag/protease and particle formation. J. Virol. 71 (1997) 4892-4903
58. Schnell M.J., Johnson J.E., Buonocore L., and Rose J.K. Construction of a novel virus that targets HIV-1-infected cells and controls HIV-1 infection. Cell 90 (1997) 849-857
59. Schnell M.J., Mebatsion T., and Conzelmann K.K. Infectious rabies viruses from cloned cDNA. EMBO J. 13 (1994) 4195-4203
60. Schwartz S., Campbell M., Nasioulas G., Harrison J., Felber B.K., and Pavlakis G.N. Mutational inactivation of an inhibitory sequence in human immunodeficiency virus type 1 results in Rev-independent gag expression. J. Virol. 66 (1992) 7176-7182
61. Schwartz S., Felber B.K., and Pavlakis G.N. Distinct RNA sequences in the gag region of human immunodeficiency virus type 1 decrease RNA stability and inhibit expression in the absence of Rev protein. J. Virol. 66 (1992) 150-159
62. Schwartz S., Felber B.K., and Pavlakis G.N. Mechanism of translation of monocistronic and multicistronic human immunodeficiency virus type 1 mRNAs. Mol. Cell. Biol. 12 (1992) 207-219
63. Shaw G., and Kamen R. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46 (1986) 659-667
64. Sheets R. History and Characterization of the Vero Cell Line (2000), FDA. http://www.fda.gov/ohrms/dockets/ac/00/backgrd/3616b1a.pdf
65. Shipman Jr. C., Vander Weide G.C., and Ma B.I. Prevalence of type R virus-like particles in clones of BHK-21 cells. Virology 38 (1969) 707-710
66. Spielhofer P., Bachi T., Fehr T., Christiansen G., Cattaneo R., Kaelin K., Billeter M.A., and Naim H.Y. Chimeric measles viruses with a foreign envelope. J. Virol. 72 (1998) 2150-2159
67. Surman S.R., Collins P.L., Murphy B.R., and Skiadopoulos M.H. An improved method for the recovery of recombinant paramyxovirus vaccine candidates suitable for use in human clinical trials. J. Virol. Methods 141 (2007) 30-33
68. Swinteck B.D., and Lyles D.S. Plasma membrane microdomains containing vesicular stomatitis virus M protein are separate from microdomains containing G protein and nucleocapsids. J. Virol. 82 (2008) 5536-5547
69. Takada A., Robison C., Goto H., Sanchez A., Murti K.G., Whitt M.A., and Kawaoka Y. A system for functional analysis of Ebola virus glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14764-14769
70. Ternette N., Stefanou D., Kuate S., Uberla K., and Grunwald T. Expression of RNA virus proteins by RNA polymerase II dependent expression plasmids is hindered at multiple steps. Virol. J. 4 (2007) 51
71. Ternette N., Tippler B., Uberla K., and Grunwald T. Immunogenicity and efficacy of codon optimized DNA vaccines encoding the F-protein of respiratory syncytial virus. Vaccine 25 (2007) 7271-7279
72. Wang G., Mulligan M.J., Baldwin D.N., and Linial M.L. Endogenous virus of BHK-21 cells complicates electron microscopy studies of foamy virus maturation. J. Virol. 73 (1999) 8917
73. Wang Y., and Morgan W.D. Cooperative interaction of human HSF1 heat shock transcription factor with promoter DNA. Nucleic Acids Res. 22 (1994) 3113-3118
74. Whelan S.P., Ball L.A., Barr J.N., and Wertz G.T. Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 8388-8392
75. Whelan S.P., Barr J.N., and Wertz G.W. Transcription and replication of nonsegmented negative-strand RNA viruses. In: Kawaoka Y. (Ed). Biology of Negative-strand RNA Viruses: The Power of Reverse Genetics (2004), Springer, New York 61-119
76. Witko S.E., Kotash C., Sidhu M.S., Udem S.A., and Parks C.L. Inhibition of measles virus minireplicon-encoded reporter gene expression by V protein. Virology 348 (2006) 107-119
77. Witko S.E., Kotash C.S., Nowak R.M., Johnson J.E., Boutilier L.A., Melville K.J., Heron S.G., Clarke D.K., Abramovitz A.S., Hendry R.M., Sidhu M.S., Udem S.A., and Parks C.L. An efficient helper-virus-free method for rescue of recombinant paramyxoviruses and rhadoviruses from a cell line suitable for vaccine development. J. Virol. Methods 135 (2006) 91-101
78. Wu C. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11 (1995) 441-469
79. Yee J.K., Friedmann T., and Burns J.C. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell. Biol. 43 Pt A (1994) 99-112
80. Zhang M.Q. Statistical features of human exons and their flanking regions. Hum. Mol. Genet. 7 (1998) 919-932
81. Zhou J., and Blissard G.W. Display of heterologous proteins on gp64null baculovirus virions and enhanced budding mediated by a vesicular stomatitis virus G-stem construct. J. Virol. 82 (2008) 1368-1377
82. Zubiaga A.M., Belasco J.G., and Greenberg M.E. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol. 15 (1995) 2219-2230