Inhibition of alphavirus infection in cell culture and in mice with antisense morpholino oligomers

Virology

Volumn 376, Issue 2, 2008, Pages 357-370

  Paessler, Slobodan ^a,b   Rijnbrand, Rene ^a,b   Stein, David A ^b,c   Ni, Haolin ^a,b   Yun, Nadezhda E ^a,b   Dziuba, Natallia ^a,b   Borisevich, Viktoriya ^a,b   Seregin, Alexey ^a,b   Ma, Yinghong ^a,b   Blouch, Robert ^b,c   Iversen, Patrick L ^b,c   Zacks, Michele A ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c AVI BIOPHARMA INC   (United States)

Author keywords

Antisense therapy; Antiviral agents; Morpholino oligomers; Pathogenic alphaviruses; Sindbis virus; Venezuelan equine encephalitis virus

Indexed keywords

OLIGOMER; PEPTIDE CONJUGATED PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER DERIVATIVE; VIRUS RNA;

ALPHA VIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG TARGETING; GENOME; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PATHOGENICITY; PRIORITY JOURNAL; SINDBIS VIRUS; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS INFECTION; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSCRIPTION;

ADMINISTRATION, INTRANASAL; ALPHAVIRUS; ALPHAVIRUS INFECTIONS; ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CERCOPITHECUS AETHIOPS; CRICETINAE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; DRUG DESIGN; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; ENCEPHALOMYELITIS, VENEZUELAN EQUINE; INJECTIONS, SUBCUTANEOUS; MICE; MORPHOLINES; OLIGONUCLEOTIDES, ANTISENSE; SINDBIS VIRUS; VIRUS REPLICATION;

ALPHAVIRUS; ANIMALIA; MUS; SINDBIS VIRUS; VENEZUELAN EQUINE ENCEPHALITIS VIRUS;

EID: 44649132597     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.03.032     Document Type: Article

References (54)

1. Abes S., Moulton H.M., Clair P., Prevot P., Youngblood D.S., Wu R.P., Iversen P.L., and Lebleu B. Vectorization of morpholino oligomers by the (R-Ahx-R)(4) peptide allows efficient splicing correction in the absence of endosomolytic agents. J. Control. Release 116 3 (2006) 304-313
2. Anishchenko M., Bowen R.A., Paessler S., Austgen L., Greene I.P., and Weaver S.C. Venezuelan encephalitis emergence mediated by a phylogenetically predicted viral mutation. Proc. Natl. Acad. Sci. U. S. A. 103 13 (2006) 4994-4999
3. Berge T.O., Banks I.S., and Tigertt W.D. Attenuation of Venezuelan equine encephalomyelitis virus by in vitro cultivation in guinea pig heart cells. Am. J. Hyg. 73 (1961) 209-218
4. Burrer R., Neuman B.W., Ting J.P., Stein D.A., Moulton H.M., Iversen P.L., Kuhn P., and Buchmeier M.J. Antiviral effects of antisense morpholino oligomers in murine Coronavirus infection models. J. Virol. 81 11 (2007) 5637-5648
5. Caplen N.J., Zheng Z., Falgout B., and Morgan R.A. Inhibition of viral gene expression and replication in mosquito cells by dsRNA-triggered RNA interference. Mol. Ther. 6 2 (2002) 243-251
6. De Clercq E. Antivirals and antiviral strategies. Nat. Rev. Microbiol. 2 9 (2004) 704-720
7. Deas T.S., Binduga-Gajewska I., Tilgner M., Ren P., Stein D.A., Moulton H.M., Iversen P.L., Kauffman E.B., Kramer L.D., and Shi P.Y. Inhibition of flavivirus infections by antisense oligomers specifically suppressing viral translation and RNA replication. J. Virol. 79 8 (2005) 4599-4609
8. Deas T.S., Bennett C.J., Jones S.A., Tilgner M., Ren P., Behr M.J., Stein D.A., Iversen P.L., Kramer L.D., Bernard K.A., and Shi P.Y. In vitro resistance selection and in vivo efficacy of morpholino oligomers against West Nile virus. Antimicrob. Agents Chemother. 51 7 (2007) 2470-2482
9. Enterlein S., Warfield K.L., Swenson D.L., Stein D.A., Smith J.L., Gamble C.S., Kroeker A.D., Iversen P.L., Bavari S., and Muhlberger E. VP35 knockdown inhibits Ebola virus amplification and protects against lethal infection in mice. Antimicrob. Agents Chemother. 50 3 (2006) 984-993
10. Frolov I., Hardy R., and Rice C.M. Cis-acting RNA elements at the 5′ end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis. Rna 7 11 (2001) 1638-1651
11. Ge Q., Pastey M., Kobasa D., Puthavathana P., Lupfer C., Bestwick R.K., Iversen P.L., Chen J., and Stein D.A. Inhibition of multiple subtypes of influenza a virus in cell cultures with morpholino oligomers. Antimicrob. Agents Chemother. 50 11 (2006) 3724-3733
12. Gorchakov R., Hardy R., Rice C.M., and Frolov I. Selection of functional 5′ cis-acting elements promoting efficient sindbis virus genome replication. J. Virol. 78 1 (2004) 61-75
13. Griffin D.E. Alphaviruses. In: Knipe D.M., and Howley P.M. (Eds). Fields' Virology. Fifth Edition 2 (2007), Lippincott, Williams and Wilkins, Philadelphia 917-962
14. Hawley R.J., and Eitzen Jr. E.M. Biological weapons-a primer for microbiologists. Annu. Rev. Microbiol. 55 (2001) 235-253
15. Heasman J. Morpholino oligos: making sense of antisense?. Dev. Biol. 243 2 (2002) 209-214
16. Holden K.L., Stein D.A., Pierson T.C., Ahmed A.A., Clyde K., Iversen P.L., and Harris E. Inhibition of dengue virus translation and RNA synthesis by a morpholino oligomer targeted to the top of the terminal 3′ stem-loop structure. Virology 344 2 (2006) 439-452
17. Keene K.M., Foy B.D., Sanchez-Vargas I., Beaty B.J., Blair C.D., and Olson K.E. RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A. 101 49 (2004) 17240-17245
18. Kinney R.M., Johnson B.J., Welch J.B., Tsuchiya K.R., and Trent D.W. The full-length nucleotide sequences of the virulent Trinidad donkey strain of Venezuelan equine encephalitis virus and its attenuated vaccine derivative, strain TC-83. Virology 170 1 (1989) 19-30
19. Kinney R.M., Huang C.Y., Rose B.C., Kroeker A.D., Dreher T.W., Iversen P.L., and Stein D.A. Inhibition of dengue virus serotypes 1 to 4 in vero cell cultures with morpholino oligomers. J. Virol. 79 8 (2005) 5116-5128
20. Kurreck J. Antisense technologies. Improvement through novel chemical modifications. Eur. J. Biochem. 270 8 (2003) 1628-1644
21. Lemm J.A., Rumenapf T., Strauss E.G., Strauss J.H., and Rice C.M. Polypeptide requirements for assembly of functional Sindbis virus replication complexes: a model for the temporal regulation of minus- and plus-strand RNA synthesis. EMBO J. 13 12 (1994) 2925-2934
22. Levis R., Schlesinger S., and Huang H.V. Promoter for Sindbis virus RNA-dependent subgenomic RNA transcription. J. Virol. 64 4 (1990) 1726-1733
23. Liljestrom P., and Garoff H. A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology (N.Y.) 9 12 (1991) 1356-1361
24. Masiero M., Nardo G., Indraccolo S., and Favaro E. RNA interference: implications for cancer treatment. Mol. Aspects Med. 28 1 (2007) 143-166
25. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 1-2 (1983) 55-63
26. Moulton H.M., Hase M.C., Smith K.M., and Iversen P.L. HIV Tat peptide enhances cellular delivery of antisense morpholino oligomers. Antisense Nucleic Acid Drug Dev. 13 1 (2003) 31-43
27. Moulton H.M., Nelson M.H., Hatlevig S.A., Reddy M.T., and Iversen P.L. Cellular uptake of antisense morpholino oligomers conjugated to arginine-rich peptides. Bioconjug. Chem. 15 2 (2004) 290-299
28. Nasevicius A., and Ekker S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26 2 (2000) 216-220
29. Nelson M.H., Stein D.A., Kroeker A.D., Hatlevig S.A., Iversen P.L., and Moulton H.M. Arginine-rich peptide conjugation to morpholino oligomers: effects on antisense activity and specificity. Bioconjug. Chem. 16 4 (2005) 959-966
30. Neuman B.W., Stein D.A., Kroeker A.D., Churchill M.J., Kim A.M., Kuhn P., Dawson P., Moulton H.M., Bestwick R.K., Iversen P.L., and Buchmeier M.J. Inhibition, escape, and attenuated growth of severe acute respiratory syndrome Coronavirus treated with antisense morpholino oligomers. J. Virol. 79 15 (2005) 9665-9676
31. Ni H., Yun N.E., Zacks M.A., Weaver S.C., Tesh R.B., da Rosa A.P., Powers A.M., Frolov I., and Paessler S. Recombinant alphaviruses are safe and useful serological diagnostic tools. Am. J. Trop. Med. Hyg. 76 4 (2007) 774-781
32. Niesters H.G., and Strauss J.H. Defined mutations in the 5′ nontranslated sequence of Sindbis virus RNA. J. Virol. 64 9 (1990) 4162-4168
33. O'Brien L. Inhibition of multiple strains of Venezuelan equine encephalitis virus by a pool of four short interfering RNAs. Antivir. Res. (2006) 1-10
34. Oberste M.S., Parker M.D., and Smith J.F. Complete sequence of Venezuelan equine encephalitis virus subtype IE reveals conserved and hypervariable domains within the C terminus of nsP3. Virology 219 1 (1996) 314-320
35. Paessler S., Fayzulin R.Z., Anishchenko M., Greene I.P., Weaver S.C., and Frolov I. Recombinant sindbis/venezuelan equine encephalitis virus is highly attenuated and immunogenic. J. Virol. 77 17 (2003) 9278-9286
36. Paessler S., Ni H., Petrakova O., Fayzulin R.Z., Yun N., Anishchenko M., Weaver S.C., and Frolov I. Replication and clearance of Venezuelan equine encephalitis virus from the brains of animals vaccinated with chimeric SIN/VEE viruses. J. Virol. 80 6 (2006) 2784-2796
37. Rice C.M., Levis R., Strauss J.H., and Huang H.V. Production of infectious RNA transcripts from Sindbis virus cDNA clones: mapping of lethal mutations, rescue of a temperature-sensitive marker, and in vitro mutagenesis to generate defined mutants. J. Virol. 61 12 (1987) 3809-3819
38. Rico-Hesse R., Weaver S.C., de Siger J., Medina G., and Salas R.A. Emergence of a new epidemic/epizootic Venezuelan equine encephalitis virus in South America. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 5278-5281
39. Roehrig J.T., and Bolin R.A. Monoclonal antibodies capable of distinguishing epizootic from enzootic varieties of Subtype I Venezuelan equine encephalitis viruses in a rapid indirect immunofluorescence assay. J. Clin. Microbiol. 35 7 (1997) 1887-1890
40. Scherer W.F., Dickerman R.W., and Ordonez J.V. Discovery and geographic distribution of Venezuelan encephalitis virus in Guatemala, Honduras, and British Honduras during 1965-68, and its possible movement to Central America and Mexico. Am. J. Trop. Med. Hyg. 19 4 (1970) 703-711
41. Schubert S., and Kurreck J. Oligonucleotide-based antiviral strategies. Handb. Exp. Pharmacol. 173 (2006) 261-287
42. Sidwell R.W., and Smee D.F. Viruses of the Bunya- and Togaviridae families: potential as bioterrorism agents and means of control. Antiviral. Res. 57 1-2 (2003) 101-111
43. Stein D., Foster E., Huang S.B., Weller D., and Summerton J. A specificity comparison of four antisense types: morpholino, 2′-O-methyl RNA, DNA, and phosphorothioate DNA. Antisense Nucleic Acid Drug Dev. 7 3 (1997) 151-157
44. Strauss J.H., and Strauss E.G. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58 3 (1994) 491-562
45. Summerton J., and Weller D. Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7 3 (1997) 187-195
46. Tsiang M., Weiss B.G., and Schlesinger S. Effects of 5′-terminal modifications on the biological activity of defective interfering RNAs of Sindbis virus. J. Virol. 62 1 (1988) 47-53
47. Vagnozzi A., Stein D.A., Iversen P.L., and Rieder E. Inhibition of foot-and-mouth disease virus infections in cell cultures with antisense morpholino oligomers. J. Virol. 81 21 (2007) 11669-11680
48. van den Born E., Stein D.A., Iversen P.L., and Snijder E.J. Antiviral activity of morpholino oligomers designed to block various aspects of Equine Arteritis virus amplification in cell culture. J. Gen. Virol. 86 Pt 11 (2005) 3081-3090
49. Vasiljeva L., Merits A., Auvinen P., and Kaariainen L. Identification of a novel function of the alphavirus capping apparatus. RNA 5′-triphosphatase activity of Nsp2. J. Biol. Chem. 275 23 (2000) 17281-17287
50. Wang E., Barrera R., Boshell J., Ferro C., Freier J.E., Navarro J.C., Salas R., Vasquez C., and Weaver S.C. Genetic and phenotypic changes accompanying the emergence of epizootic subtype IC Venezuelan equine encephalitis viruses from an enzootic subtype ID progenitor. J. Virol. 73 5 (1999) 4266-4271
51. Weaver S.C., Ferro C., Barrera R., Boshell J., and Navarro J.C. Venezuelan equine encephalitis*. Annu. Rev. Entomol. 49 (2004) 141-174
52. Youngblood D.S., Hatlevig S.A., Hassinger J.N., Iversen P.L., and Moulton H.M. Stability of cell-penetrating peptide-morpholino oligomer conjugates in human serum and in cells. Bioconjug. Chem. 18 1 (2007) 50-60
53. Yuan J., Stein D.A., Lim T., Qiu D., Coughlin S., Liu Z., Wang Y., Blouch R., Moulton H.M., Iversen P.L., and Yang D. Inhibition of coxsackievirus B3 in cell cultures and in mice by peptide-conjugated morpholino oligomers targeting the internal ribosome entry site. J. Virol. 80 23 (2006) 11510-11519
54. Zhang Y.J., Stein D.A., Fan S.M., Wang K.Y., Kroeker A.D., Meng X.J., Iversen P.L., and Matson D.O. Suppression of porcine reproductive and respiratory syndrome virus replication by morpholino antisense oligomers. Vet. Microbiol. 117 2-4 (2006) 117-129