Deletions in the hypervariable domain of the nsP3 gene attenuate Semliki Forest virus virulence

Journal of General Virology

Volumn 87, Issue 4, 2006, Pages 937-947

  Galbraith, Sareen E ^a,b,c   Sheahan, Brian J ^b   Atkins, Gregory J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

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

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 3; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL CULTURE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE DELETION; IMMUNE RESPONSE; INFECTION RESISTANCE; INOCULATION; MOLECULAR CLONING; MOUSE; MOUSE STRAIN; MUSCLE; NONHUMAN; NOSE; PERITONEUM; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA SYNTHESIS; SEMLIKI FOREST ALPHAVIRUS; SURVIVAL; VIRUS ATTENUATION; VIRUS INFECTION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE;

ALPHAVIRUS INFECTIONS; AMINO ACID SEQUENCE; ANIMALS; BALB 3T3 CELLS; BASE SEQUENCE; CELL LINE; CRICETINAE; FEMALE; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; RNA-BINDING PROTEINS; SEMLIKI FOREST VIRUS; SEQUENCE DELETION; SPECIFIC PATHOGEN-FREE ORGANISMS; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE;

ANIMALIA; SEMLIKI FOREST VIRUS;

EID: 33645538734     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.81406-0     Document Type: Article

References (62)

1. Ahola, T., Lampio, A., Auvinen, P. & Kääriäinen, L. (1999). Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity. EMBO J 18, 3164-3172.
2. Ahola, T., Kujala, P., Tuittila, M., Blom, T., Laakkonen, P., Hinkkanen, A. & Auvinen, P. (2000). Effects of palmitoylation of replicase protein nsP1 on alphavirus infection. J Virol 74, 6725-6733.
3. Atkins, G. J., Sheahan, B. J. & Liljeström, P. (1999). The molecular pathogenesis of Semliki Forest virus: a model virus made useful? J Gen Virol 80, 2287-2297.
4. Balluz, I. M., Glasgow, G. M., Killen, H. M., Mabruk, M. J., Sheehan, B. J. & Atkins, G. J. (1993). Virulent and avirulent strains of Semliki Forest virus show similar cell tropism for the murine central nervous system but differ in the severity and rate of induction of cytolytic damage. Neuropathol Appl Neurobiol 19, 233-239.
5. De, I., Fata-Hartley, C, Sawicki, S. G. & Sawicki, D. L. (2003). Functional analysis of nsP3 phosphoprotein mutants of Sindbis virus. J Virol 77, 13106-13116.
6. de Groot, R. J., Hardy, W. R., Shirako, Y. & Strauss, J. H. (1990). Cleavage-site preferences of Sindbis virus polyproteins containing the non-structural proteinase. Evidence for temporal regulation of polyprotein processing in vivo. EMBO J 9, 2631-2638.
7. Fata, C. L., Sawicki, S. G. & Sawicki, D. L (2002a). Modification of Asn374 of nsP1 suppresses a Sindbis virus nsP4 minus-strand polymerase mutant. J Virol 76, 8641-8649.
8. Fata, C. L., Sawicki, S. G. & Sawicki, D. L. (2002b). Alphavirus minus-strand RNA synthesis: identification of a role for Arg183 of the nsP4 polymerase. J Virol 76, 8632-8640.
9. Fazakerley, J. K. (2002). Pathogenesis of Semliki Forest virus encephalitis. J Neurovirol 8, 66-74.
10. Fazakerley, J. K. (2004). Semliki Forest virus infection of laboratory mice: a model to study the pathogenesis of viral encephalitis. Arch Virol Suppl 18, 179-190.
11. Fazakerley, J. K., Boyd, A., Mikkola, M. L. & Kääriäinen, L. (2002). A single amino acid change in the nuclear localization sequence of the nsP2 protein affects the neurovirulence of Semliki Forest virus. J Virol 76, 392-396.
12. Glasgow, G. M., Sheahan, B. J., Atkins, G. J., Wahlberg, J. M., Salminen, A. & Liljeström, P. (1991). Two mutations in the envelope glycoprotein E2 of Semliki Forest virus affecting the maturation and entry patterns of the virus alter pathogenicity for mice. Virology 185, 741-748.
13. Glasgow, G. M., Killen, H. M., Liljeström, P., Sheahan, B. J. & Atkins, G. J. (1994). A single amino acid change in the E2 spike protein of a virulent strain of Semliki Forest virus attenuates pathogenicity. J Gen Virol 75, 663-668.
14. Hahn, Y. S., Strauss, E. G. & Strauss, J. H. (1989). Mapping of RNA- temperature-sensitive mutants of Sindbis virus: assignment of complementation groups A, B, and G to nonstructural proteins. J Virol 63, 3142-3150.
15. Kääriäinen, L & Söderlund, H. (1978). Structure and replication of alphaviruses. Curr Top Microbiol Immunol 82, 15-69.
16. Kääriäinen, L. & Ahola, T. (2002). Functions of alphavirus non-structural proteins in RNA replication. Prog Nucleic Acid Res Mol Biol 71, 187-222.
17. Kim, K. H., Rumenapf, T., Strauss, E. G. & Strauss, J. H. (2004). Regulation of Semliki Forest virus RNA replication: a model for the control of alphavirus pathogenesis in invertebrate hosts. Virology 323, 153-163.
18. Koonin, E. V. & Dolja, V. V. (1993). Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28, 375-430.
19. Kujala, P., Ikaheimonen, A., Ehsani, N., Vihinen, H., Auvinen, P. & Kääriäinen, L. (2001). Biogenesis of the Semliki Forest virus RNA replication complex. J Virol 75, 3873-3884.
20. Laakkonen, P., Ahola, T. & Kääriäinen, L. (1996). The effects of palmitoylation on membrane association of Semliki forest virus RNA capping enzyme. J Biol Chem 271, 28567-28571.
21. Lampio, A., Kilpelainen, I., Pesonen, S., Karhi, K., Auvinen, P., Somerharju, P. & Kääriäinen, L. (2000). Membrane binding mechanism of an RNA virus-capping enzyme. J Biol Chem 275, 37853-37859.
22. LaStarza, M. W., Lemm, J. A. & Rice, C. M. (1994a). Genetic analysis of the nsP3 region of Sindbis virus: evidence for roles in minus-strand and subgenomic RNA synthesis. J Virol 68, 5781-5791.
23. LaStarza, M. W., Grakoui, A. & Rice, C. M. (1994b). Deletion and duplication mutations in the C-terminal nonconserved region of Sindbis virus nsP3: effects on phosphorylation and on virus replication in vertebrate and invertebrate cells. Virology 202, 224-232.
24. Lemm, J. A. & Rice, C. M. (1993). Roles of nonstructural polyproteins and cleavage products in regulating Sindbis virus RNA replication and transcription. J Virol 67, 1916-1926.
25. Lemm, J. A., Rumenapf, T., Strauss, E. G., Strauss, J. H. & Rice, C. M. (1994). 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, 2925-2934.
26. Lemm, J. A., Bergqvist, A., Read, C. M. & Rice, C. M. (1998). Template-dependent initiation of Sindbis virus RNA replication in vitro. J Virol 72, 6546-6553.
27. Li, G. P., La Starza, M. W., Hardy, W. R., Strauss, J. H. & Rice, C. M. (1990). Phosphorylation of Sindbis virus nsP3 in vivo and in vitro. Virology 179, 416-427.
28. Liljeström, P., Lusa, S., Huylebroeck, D. & Garoff, H. (1991). In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release. J Virol 65, 4107-4113.
29. Meissner, J. D., Huang, C. Y., Pfeffer, M. & Kinney, R. M. (1999). Sequencing of prototype viruses in the Venezuelan equine encephalitis antigenic complex. Virus Res 64, 43-59.
30. Merits, A., Vasiljeva, L., Ahola, T., Kääriäinen, L. & Auvinen, P. (2001). Proteolytic processing of Semliki Forest virus-specific non-structural polyprotein by nsP2 protease. J Gen Virol 82, 765-773.
31. Oberste, M. S., Parker, M. D. & Smith, J. F. (1996). Complete sequence of Venezuelan equine encephalitis virus subtype IE reveals conserved and hypervariable domains within the C terminus of nsP3. Virology 219, 314-320.
32. Pathak, S. & Webb, H. E. (1974). Possible mechanisms for the transport of Semliki forest virus into and within mouse brain. An electron-microscopic study. J Neurol Sci 23, 175-184.
33. Pehrson, J. R. L. & Fuji, R. N. (1998). Evolutionary conservation of histone macroH2A subtypes and domains. Nucleic Acids Res 26, 2837-2842.
34. Peränen, J. (1991). Localization and phosphorylation of Semliki Forest virus non-structural protein nsP3 expressed in COS cells from a cloned cDNA. J Gen Virol 72, 195-199.
35. Peränen, J. & Kääriäinen, L. (1991). Biogenesis of type I cytopathic vacuoles in Semliki Forest virus-infected BHK cells. J Virol 65, 1623-1627.
36. Peränen, J., Takkinen, K., Kalkkinen, N. & Kääriäinen, L. (1988). Semliki Forest virus-specific non-structural protein nsp3 is a phosphoprotein. J Gen Virol 69, 2165-2178.
37. Peränen, J., Laakkonen, P., Hyvönen, M. & Kääriäinen, L. (1995). The alphavirus replicase protein nsp1 is membrane-associated and has affinity to endocytic organelles. Virology 208, 610-620.
38. Rikkonen, M. (1996). Functional significance of the nuclear-targeting and NTP-binding motifs of Semliki Forest virus nonstructural protein nsP2. Virology 218, 352-361.
39. Saleh, S. M., Poidinger, M., Mackenzie, J. S., Broom, A. K., Lindsay, M. D. & Hall, R. A. (2003). Complete genomic sequence of the Australian south-west genotype of Sindbis virus: comparisons with other Sindbis strains and identification of a unique deletion in the 3′-untranslated region. Virus Genes 26, 317-327.
40. Salonen, A., Vasiljeva, L., Merits, A., Magden, J., Jokitalo, E & Kääriäinen, L. (2003). Properly folded nonstructural polyprotein directs the Semliki Forest virus replication complex to the endosomal compartment. J Virol 77, 1691-1702.
41. Sammin, D. J., Butler, D., Atkins, G. J. & Sheahan, B. J. (1999). Cell death mechanisms in the olfactory bulb of rats infected intranasally with Semliki Forest virus. Neuropathol Appl Neurobiol 25, 236-243.
42. Santagati, M. G., Määttä, J. A., Itäranta, P. V., Salmi, A. A. & Hinkkanen, A. E. (1995). The Semliki Forest virus E2 gene as a virulence determinant. J Gen Virol 76, 47-52.
43. Santagati, M. G., Määttä, J. A., Röyttä, M., Salmi, A. A. & Hinkkanen, A. E. (1998). The significance of the 3′-nontranslated region and E2 amino acid mutations in the virulence of Semliki Forest virus in mice. Virology 243, 66-77.
44. Shirako, Y. & Strauss, J. H. (1994). Regulation of Sindbis virus RNA replication: uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand RNA synthesis. J Virol 68, 1874-1885.
45. Shirako, Y., Strauss, E. G. & Strauss, J. H. (2000). Suppressor mutations that allow sindbis virus RNA polymerase to function with nonaromatic amino acids at the N-terminus: evidence for interaction between nsP1 and nsP4 in minus-strand RNA synthesis. Virology 276, 148-160.
46. Smyth, J. W., Fleeton, M. N., Sheahan, B. J. & Atkins, G. J. (2005). Treatment of rapidly growing K-BALB and CT26 mouse tumours using Semliki Forest virus and its derived vector. Gene Ther 12, 147-159.
47. Soilu-Hänninen, M., Erälinna, J. P., Hukkanen, V., Röyttä, M., Salmi, A. A. & Salonen, R. (1994). Semliki Forest virus infects mouse brain endothelial cells and causes blood-brain barrier damage. J Virol 68, 6291-6298.
48. Strauss, J. H. & Strauss, E. G. (1994). The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58, 491-562.
49. Strauss, E. G., Levinson, R., Rice, C. M., Dalrymple, J. & Strauss, J. H. (1988). Nonstructural proteins nsP3 and nsP4 of Ross River and O'Nyong-nyong viruses: sequence and comparison with those of other alphaviruses. Virology 164, 265-274.
50. Suopanki, J., Sawicki, D. L., Sawicki, S. G. & Kääriäinen, L. (1998). Regulation of alphavirus 26S mRNA transcription by replicase component nsP2. J Gen Virol 79, 309-319.
51. Tarbatt, C. J., Glasgow, G. M., Mooney, D. A., Sheehan, B. J. & Atkins, G. J. (1997). Sequence analysis of the avirulent, demyelinating A7 strain of Semliki Forest virus. J Gen Virol 78, 1551-1557.
52. Tuittila, M. & Hinkkanen, A. E. (2003). Amino acid mutations in the replicase protein nsP3 of Semliki Forest virus cumulatively affect neurovirulence. J Gen Virol 84, 1525-1533.
53. Tuittila, M. T., Santagati, M. G., Röyttä, M., Määttä, J. A. & Hinkkanen, A. E. (2000). Replicase complex genes of Semliki Forest virus confer lethal neurovirulence. J Virol 74, 4579-4589.
54. Vasiljeva, L., Merits, A., Auvinen, P. & Kääriäinen, L. (2000). Identification of a novel function of the Alphavirus capping apparatus. RNA 5′-triphosphatase activity of Nsp2. J Biol Chem 275, 17281-17287.
55. Vasiljeva, L., Valmu, L., Kääriäinen, L. & Merits, A. (2001). Site-specific protease activity of the carboxyl-terminal domain of Semliki Forest virus replicase protein nsP2. J Biol Chem 276, 30786-30793.
56. Vasiljeva, L., Merits, A., Golubtsov, A., Sizemskaja, V., Kääriäinen, L. & Ahola, T. (2003). Regulation of the sequential processing of Semliki Forest virus replicase polyprotein. J Biol Chem 278, 41636-41645.
57. Vihinen, H. & Saarinen, J. (2000). Phosphorylation site analysis of Semliki Forest virus nonstructural protein 3. J Biol Chem 275, 27775-27783.
58. Vihinen, H., Ahola, T., Tuittila, M., Merits, A. & Kääriäinen, L. (2001). Elimination of phosphorylation sites of Semliki Forest virus replicase protein nsP3. J Biol Chem 276, 5745-5752.
59. Wang, Y. F., Sawicki, S. G. & Sawicki, D. L. (1991). Sindbis virus nsP1 functions in negative-strand RNA synthesis. J Virol 65, 985-988.
60. Wang, Y. F., Sawicki, S. G. & Sawicki, D. L (1994). Alphavirus nsP3 functions to form replication complexes transcribing negative-strand RNA. J Virol 68, 6466-6475.
61. Wang, H. L., O'Rear, J. & Stollar, V. (1996). Mutagenesis of the Sindbis virus nsP1 protein: effects on methyltransferase activity and viral infectivity. Virology 217, 527-531.
62. Weston, J., Villoing, S., Bremont, M. & 8 other authors (2002). Comparison of two aquatic alphaviruses, salmon pancreas disease virus and sleeping disease virus, by using genome sequence analysis, monoclonal reactivity, and cross-infection. J Virol 76, 6155-6163.