Source: http://www.asmscience.org/content/book/10.1128/9781555815561.ch22
Timestamp: 2019-04-21 08:42:13+00:00

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Diagrammatic representation of alphavirus replication in permissive cells. The replication cycle is depicted as a series of temporally regulated steps: ( 1 ) translation and processing of nonstructural polyprotein; ( 2 ) synthesis of complementary, negative-sense RNA; ( 3 ) synthesis of progeny genomes; ( 4 ) synthesis of subgenomic RNAs; ( 5 ) translation and processing of structural polyprotein C/PE2/6KE1; ( 6 ) packaging of progeny genomes into nucleocapsids; and ( 7 ) envelopment of progeny virions at the plasma membrane.
Induction of IFN-α/β as measured by a biological assay of supernatants collected from virus-infected (multiplicity of infection = 3) MEF cultures at different times postinfection. nc SINV is the Sindbis virus strain TR339 with the noncytopathic nsP2 726 G mutation ( 30 ). wt SINV is the TR339 strain of Sindbis virus. SeV is a Sendai virus stock acquired from the American Type Culture Collection. Asterisks indicate times at which samples were not taken due to complete cytopathic effect. hpi, hours postinfection.
Production of IFN-α/β measured by biological assay of serum after infection of CD-1 mice with similar doses (pfu or IU) of SINV (TR339 strain), EEEV, or VEEV virus or replicon particles. In EEEV-infected mice, IFN levels were below the limit of detection (*). hpi, hours postinfection.
Relative sensitivity of the replication of SINV (TR339 strain), VEEV, or EEEV to IFN-α/β priming of Swiss 3T3 murine fibroblasts. Cells were treated with the indicated IFN concentration for 12 h prior to infection (multiplicity of infection = 3), and CPE was measured at 24 h postinfection.
Diagrammatic representation of the PKR-mediated and PKR/RNase L/Mx-independent antiviral effects in SINV-infected primary DCs and mice in vivo. Constitutively expressed PKR significantly suppresses early virus replication; however, secreted IFN-α/β acts via an alternative pathway in the presence or absence of PKR, RNase L, and Mx to protect cells and clear virus infection. In the absence of the IFN-α/β-induced alternative pathway, virus replication continues unabated, resulting in cell death.
1. Aguilar, P. V.,, S. Paessler,, A. S. Carrara,, S. Baron,, J. Poast,, E. Wang,, A. C. Moncayo,, M. Anishchenko,, D. Watts,, R. B. Tesh, and, S. C. Weaver. 2005. Variation in interferon sensitivity and induction among strains of eastern equine encephalitis virus. J. Virol. 79: 11300– 11310.
2. Aguilar, P. V.,, S. C. Weaver, and, C. F. Basler. 2007. Capsid protein of eastern equine encephalitis virus inhibits host cell gene expression. J. Virol. 81: 3866– 3876.
3. Aguilar, P. V.,, L. W. Leung,, E. Wang,, S. C. Weaver, and, C. F. Basler. 2008. A five amino acid deletion of the Eastern equine encephalitis virus capsid protein attenuates replication in mammalian but not mosquito cells. J. Virol. Epub ahead of print.
4. Ahola, T.,, A. Lampio,, P. Auvinen, and, L. Kaariainen. 1999. Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity. EMBO J. 18: 3164– 3172.
5. Al Khatib, K.,, B. R. Williams,, R. H. Silverman,, W. Halford, and, D. J. Carr. 2003. The murine double-stranded RNA-dependent protein kinase PKR and the murine 2′,5′-oligoadenylate synthetase-dependent RNase L are required for IFN-beta-mediated resistance against herpes simplex virus type 1 in primary trigeminal ganglion culture. Virology 313: 126– 135.
6. Aronson, J. F.,, F. B. Grieder,, N. L. Davis,, P. C. Charles,, T. Knott,, K. Brown, and, R. E. Johnston. 2000. A single-site mutant and revertants arising in vivo define early steps in the pathogenesis of Venezuelan equine encephalitis virus. Virology 270: 111– 123.
7. Atkins, G. J., and, C. L. Lancashire. 1976. The induction of interferon by temperature-sensitive mutants of Sindbis virus: its relationship to double-stranded RNA synthesis and cytopathic effect. J. Gen. Virol. 30: 157– 165.
8. Baron, S.,, C. E. Buckler,, R. V. McCloskey, and, R. L. Kirschstein. 1966. Role of interferon during viremia. I. Production of circulating interferon. J. Immunol. 96: 12– 16.
9. Basler, C. F., and, A. Garcia-Sastre. 2002. Viruses and the type I interferon antiviral system: induction and evasion. Int. Rev. Immunol. 21: 305– 337.
10. Beard, J. R.,, M. Trent,, G. A. Sam, and, V. C. Delpech. 1997. Self-reported morbidity of Barmah Forest virus infection on the north coast of New South Wales. Med. J. Aust. 167: 525– 528.
11. Bick, M. J.,, J. W. Carroll,, G. Gao,, S. P. Goff,, C. M. Rice, and, M. R. Macdonald. 2003. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J. Virol. 77: 11555– 11562.
12. Bonnard, M.,, C. Mirtsos,, S. Suzuki,, K. Graham,, J. Huang,, M. Ng,, A. Itie,, A. Wakeham,, A. Shahinian,, W. J. Henzel,, A. J. Elia,, W. Shillinglaw,, T. W. Mak,, Z. Cao, and, W. C. Yeh. 2000. Deficiency of T2K leads to apoptotic liver degeneration and impaired NFkappaB-dependent gene transcription. EMBO J. 19: 4976– 4985.
13. Bradish, C. J.,, K. Allner, and, H. B. Maber. 1972. Infection, interaction and the expression of virulence by defined strains of Semliki forest virus. J. Gen. Virol. 16: 359– 372.
14. Brawand, P.,, D. R. Fitzpatrick,, B. W. Greenfield,, K. Brasel,, C. R. Maliszewski, and, T. De Smedt. 2002. Murine plasmacytoid pre-dendritic cells generated from Flt3 ligand-supplemented bone marrow cultures are immature APCs. J. Immunol. 169: 6711– 6719.
15. Breakwell, L.,, P. Dosenovic,, G. B. Karlsson Hedestam,, M. D’Amato,, P. Liljestrom,, J. Fazakerley, and, G. M. McInerney. 2007. Semliki Forest virus nonstructural protein 2 is involved in suppression of the type I interferon response. J. Virol. 81: 8677– 8684.
16. Byrnes, A. P.,, J. E. Durbin, and, D. E. Griffin. 2000. Control of Sindbis virus infection by antibody in interferon-deficient mice. J. Virol. 74: 3905– 3908.
17. Chantler, J.,, J. S. Wolinsky, and, A. Tingle. 2001. Rubella virus, p. 963–990. In D. M. Knipe and, P. M. Howley (ed.), Fields Virology, 4th ed. Lippincott, Williams & Wilkins, Philadelphia, PA.
18. Charles, P. C.,, J. Trgovcich,, N. L. Davis, and, R. E. Johnston. 2001. Immunopathogenesis and immune modulation of Venezuelan equine encephalitis virus-induced disease in the mouse. Virology 284: 190– 202.
19. Charles, P. C.,, E. Walters,, F. Margolis, and, R. E. Johnston. 1995. Mechanism of neuroinvasion of Venezuelan equine encephalitis virus in the mouse. Virology 208: 662– 671.
20. Choi, H. K.,, L. Tong,, W. Minor,, P. Dumas,, U. Boege,, M. G. Rossmann, and, G. Wengler. 1991. Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354: 37– 43.
21. Couderc, T.,, F. Chretien,, C. Shilte,, O. Disson,, M. Brigitte,, F. Guivel-Benhassine,, Y. Touret,, G. Barau,, N. Cayet,, I. Schuffenecker,, P. Despres,, F. Arenzana-Seisedos,, A. Michault,, M. L. Albert, and, M. Lecuit. 2008. A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS. Pathog. 4: e29.
22. Davis, N. L.,, F. B. Grieder,, J. F. Smith,, G. F. Greenwald,, M. L. Valenski,, D. C. Sellon,, P. C. Charles, and, R. E. Johnston. 1994. A molecular genetic approach to the study of Venezuelan equine encephalitis virus pathogenesis. Arch. Virol. Suppl. 9: 99– 109.
23. Enserink, M. 2007. Epidemiology. Tropical disease follows mosquitoes to Europe. Science 317: 1485.
24. Favre, D.,, E. Studer, and, M. R. Michel. 1996. Semliki Forest virus capsid protein inhibits the initiation of translation by upregulating the double-stranded RNA-activated protein kinase (PKR). Biosci. Rep. 16: 485– 511.
25. Fazakerley, J. K. 2004. Semliki forest virus infection of laboratory mice: a model to study the pathogenesis of viral encephalitis. Arch. Virol. Suppl. 179– 190.
26. Finlay, B. B., and, G. McFadden. 2006. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124: 767– 782.
27. Finter, N. B. 1964. Interferon production and sensitivity of Semliki Forest virus variants. J. Hyg. (Lond.) 62: 337– 349.
28. Flexman, J. P.,, D. W. Smith,, J. S. Mackenzie,, J. R. Fraser,, S. P. Bass,, L. Hueston,, M. D. Lindsay, and, A. L. Cunningham. 1998. A comparison of the diseases caused by Ross River virus and Barmah Forest virus. Med. J. Aust. 169: 159– 163.
29. Friedman, R. M. 1968. Inhibition of arbovirus protein synthesis by interferon. J. Virol. 2: 1081– 1085.
30. Frolov, I.,, E. Agapov,, T. A. Hoffman, Jr.,, B. M. Pragai,, M. Lippa,, S. Schlesinger, and, C. M. Rice. 1999. Selection of RNA replicons capable of persistent noncytopathic replication in mammalian cells. J. Virol. 73: 3854– 3865.
31. Frolov, I.,, R. Hardy, and, C. M. Rice. 2001. Cis-acting RNA elements at the 5′ end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis. RNA 7: 1638– 1651.
32. Frolova, E. I.,, R. Z. Fayzulin,, S. H. Cook,, D. E. Griffin,, C. M. Rice, and, I. Frolov. 2002. Roles of nonstructural protein nsP2 and alpha/beta interferons in determining the outcome of Sindbis virus infection. J. Virol. 76: 11254– 11264.
33. Froshauer, S.,, J. Kartenbeck, and, A. Helenius. 1988. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J. Cell Biol. 107: 2075– 2086.
34. Garmashova, N.,, S. Atasheva,, W. Kang,, S. C. Weaver,, E. Frolova, and, I. Frolov. 2007. Analysis of Venezuelan eguine encephalitis virus capsid protein function in the inhibition of cellular transcription. J. Virol. 81: 13552– 13565.
35. Garmashova, N.,, R. Gorchakov,, E. Frolova, and, I. Frolov. 2006. Sindbis virus nonstructural protein nsP2 is cytotoxic and inhibits cellular transcription. J. Virol. 80: 5686– 5696.
36. Garmashova, N.,, R. Gorchakov,, E. Volkova,, S. Paessler,, E. Frolova, and, I. Frolov. 2007. The Old World and New World alphaviruses use different virus-specific proteins for induction of transcriptional shutoff. J. Virol. 81: 2472– 2484.
37. Giannakopoulos, N. V.,, J. K. Luo,, V. Papov,, W. Zou,, D. J. Lenschow,, B. S. Jacobs,, E. C. Borden,, J. Li,, H. W. Virgin, and, D. E. Zhang. 2005. Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem. Biophys. Res. Commun. 336: 496– 506.
38. Gilfoy, F. D., and, P. W. Mason. 2007. West Nile virus-induced interferon production is mediated by the double-stranded RNA-dependent protein kinase PKR. J. Virol. 81: 11148– 11158.
39. Gitlin, L.,, W. Barchet,, S. Gilfillan,, M. Cella,, B. Beutler,, R. A. Flavell,, M. S. Diamond, and, M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103: 8459– 8464.
40. Gomez de Cedron, M.,, N. Ehsani,, M. L. Mikkola,, J. A. Garcia, and, L. Kaariainen. 1999. RNA helicase activity of Semliki Forest virus replicase protein NSP2. FEBS Lett. 448: 19– 22.
41. Gorchakov, R.,, E. Frolova,, B. R. Williams,, C. M. Rice, and, I. Frolov. 2004. PKR-dependent and -independent mechanisms are involved in translational shutoff during Sindbis virus infection. J. Virol. 78: 8455– 8467.
42. Grieder, F. B., and, S. N. Vogel. 1999. Role of interferon and interferon regulatory factors in early protection against Venezuelan equine encephalitis virus infection. Virology 257: 106– 118.
43. Griffin, D. E. 1976. Role of the immune response in age-dependent resistance of mice to encephalitis due to Sindbis virus. J. Infect. Dis. 133: 456– 464.
44. Griffin, D. E. 2001. Alphaviruses, p. 917–962. In D. M. Knipe and, P. M. Howley (ed.), Fields Virology, 4th ed. Lippincott, Williams & Wilkins, Philadelphia, PA.
45. Grimley, P. M.,, J. G. Levin,, I. K. Berezesky, and, R. M. Friedman. 1972. Specific membranous structures associated with the replication of group A arboviruses. J. Virol. 10: 492– 503.
46. Guo, X.,, J. W. Carroll,, M. R. Macdonald,, S. P. Goff, and, G. Gao. 2004. The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J. Virol. 78: 12781– 12787.
47. Guo, X.,, J. Ma,, J. Sun, and, G. Gao. 2007. The zinc-finger antiviral protein recruits the RNA processing exo-some to degrade the target mRNA. Proc. Natl. Acad. Sci. USA 104: 151– 156.
48. Hardy, W. R., and, J. H. Strauss. 1989. Processing the non-structural polyproteins of Sindbis virus: nonstructural proteinase is in the C-terminal half of nsP2 and functions both in cis and in trans. J. Virol. 63: 4653– 4664.
49. Hefti, H. P.,, M. Frese,, H. Landis,, C. Di Paolo,, A. Aguzzi,, O. Haller, and, J. Pavlovic. 1999. Human MxA protein protects mice lacking a functional alpha/beta interferon system against La Crosse virus and other lethal viral infections. J. Virol. 73: 6984– 6991.
50. Heise, M. T.,, D. A. Simpson, and, R. E. Johnston. 2000. Sindbis-group alphavirus replication in periosteum and endosteum of long bones in adult mice. J. Virol. 74: 9294– 9299.
51. Hidmark, A. S.,, G. M. McInerney,, E. K. Nordstrom,, I. Douagi,, K. M. Werner,, P. Liljestrom, and, G. B. Karlsson Hedestam. 2005. Early alpha/beta interferon production by myeloid dendritic cells in response to UV-inactivated virus requires viral entry and interferon regulatory factor 3 but not MyD88. J. Virol. 79: 10376– 10385.
52. Hoenen, A.,, W. Liu,, G. Kochs,, A. A. Khromykh, and, J. M. Mackenzie. 2007. West Nile virus-induced cytoplasmic membrane structures provide partial protection against the interferon-induced antiviral MxA protein. J. Gen. Virol. 88: 3013– 3017.
53. Honda, K.,, A. Takaoka, and, T. Taniguchi. 2006. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349– 360.
54. Hornung, V.,, J. Ellegast,, S. Kim,, K. Brzózka,, A. Jung,, H. Kato,, H. Poeck,, S. Akira,, K. K. Conzelmann,, M. Schlee,, S. Endres, and, G. Hartmann. 2006. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314: 994– 997.
55. Hsieh, P., and, P. W. Robbins. 1984. Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells. J. Biol. Chem. 259: 2375– 2382.
56. Hsieh, P.,, M. R. Rosner, and, P. W. Robbins. 1983. Host-dependent variation of asparagine-linked oligosaccha-rides at individual glycosylation sites of Sindbis virus glycoproteins. J. Biol. Chem. 258: 2548– 2554.
57. Iwasaki, A., and, R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987– 995.
58. Jackson, A. C. and,, J. P. Rossiter. 1997. Apoptotic cell death is an important cause of neuronal injury in experimental Venezuelan equine encephalitis virus infection of mice. Acta Neuropathol. 93: 349– 353.
59. Jiang, Z.,, T. W. Mak,, G. Sen, and, X. Li. 2004. Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc. Natl. Acad. Sci. USA 101: 3533– 3538.
60. Jiang, Z.,, M. Zamanian-Daryoush,, H. Nie,, A. M. Silva,, B. R. Williams, and, X. Li. 2003. Poly(I-C)-induced Toll-like receptor 3 (TLR3)-mediated activation of NFkappa B and MAP kinase is through an interleukin-1 receptor-associated kinase (IRAK)-independent pathway employing the signaling components TLR3-TRAF6-TAK1-TAB2-PKR. J. Biol. Chem. 278: 16713– 16719.
61. Jin, Y.,, L. Fuller,, G. Ciancio,, G. W. Burke III,, A. G. Tzakis,, C. Ricordi,, J. Miller, and, V. Esquenzai. 2004. Antigen presentation and immune regulatory capacity of immature and mature-enriched antigen presenting (dendritic) cells derived from human bone marrow. Hum. Immunol. 65: 93– 103.
62. Johnson, R. T. 1965. Virus invasion of the central nervous system: a study of Sindbis virus infection in the mouse using fluorescent antibody. Am. J. Pathol. 70: 929– 943.
63. Johnson, R. T.,, H. F. McFarland, and, S. E. Levy. 1972. Age-dependent resistance to viral encephalitis: studies of infections due to Sindbis virus in mice. J. Infect. Dis. 125: 257– 262.
64. Kang, D. C.,, R. V. Gopalkrishnan,, Q. Wu,, E. Jankowsky,, A. M. Pyle, and, P. B. Fisher. 2002. mda-5: an interferoninducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. USA 99: 637– 642.
65. Kielian, M. 2002. Structural surprises from the flaviviruses and alphaviruses. Mol. Cell 9: 454– 456.
66. Klimstra, W. B.,, E. M. Nangle,, M. S. Smith,, A. D. Yurochko, and, K. D. Ryman. 2003. DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J. Virol. 77: 12022– 12032.
67. Klimstra, W. B.,, K. D. Ryman,, K. A. Bernard,, K. B. Nguyen,, C. A. Biron, and, R. E. Johnston. 1999. Infection of neonatal mice with Sindbis virus results in a systemic inflammatory response syndrome. J. Virol. 73: 10387– 10398.
68. Klimstra, W. B.,, K. D. Ryman, and, R. E. Johnston. 1998. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 72: 7357– 7366.
69. Landis, H.,, A. Simon-Jodicke,, A. Kloti,, C. Di Paolo,, J. J. Schnorr,, S. Schneider-Schaulies,, H. P. Hefti, and, J. Pavlovic. 1998. Human MxA protein confers resistance to Semliki Forest virus and inhibits the amplification of a Semliki Forest virus-based replicon in the absence of viral structural proteins. J. Virol. 72: 1516– 1522.
70. Lee, J. Y.,, J. A. Marshall, and, D. S. Bowden. 1994. Characterization of rubella virus replication complexes using antibodies to double-stranded RNA. Virology 200: 307– 312.
71. Lemm, J. A. and,, C. M. Rice. 1993. Assembly of functional Sindbis virus RNA replication complexes: requirement for coexpression of P123 and P34. J. Virol. 67: 1905– 1915.
72. Lemm, J. A. and,, C. M. Rice. 1993. Roles of nonstructural polyproteins and cleavage products in regulating Sindbis virus RNA replication and transcription. J. Virol. 67: 1916– 1926.
73. Lemm, J. A.,, T. Rumenapf,, E. G. Strauss,, J. H. Strauss, and, C. M. Rice. 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.
74. Lenschow, D. J.,, N. V. Giannakopoulos,, L. J. Gunn,, C. Johnston,, A. K. O’Guin,, R. E. Schmidt,, B. Levine, and, H. W. Virgin IV. 2005. Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. J. Virol. 79: 13974– 13983.
75. Lidbury, B. A., and, S. Mahalingam. 2000. Specific ablation of antiviral gene expression in macrophages by antibody-dependent enhancement of Ross River virus infection. J. Virol. 74: 8376– 8381.
76. Lidbury, B. A.,, C. Simeonovic,, G. E. Maxwell,, I. D. Marshall, and, A. J. Hapel. 2000. Macrophage-induced muscle pathology results in morbidity and mortality for Ross River virus-infected mice. J. Infect. Dis. 181: 27– 34.
77. MacDonald, G. H. and,, R. E. Johnston. 2000. Role of dendritic cell targeting in Venezuelan equine encephalitis virus pathogenesis. J. Virol. 74: 914– 922.
78. Macdonald, M. R.,, E. S. Machlin,, O. R. Albin, and, D. E. Levy. 2007. The zinc-finger antiviral protein acts synergistically with an interferon-induced factor for maximal activity against alphaviruses. J. Virol. 81: 13509– 13518.
79. Mahalingam, S., and, B. A. Lidbury. 2002. Suppression of lipopolysaccharide-induced antiviral transcription factor (Stat-1 and NF-kappa B) complexes by antibody-dependent enhancement of macrophage infection by Ross River virus. Proc. Natl. Acad. Sci. USA 99: 13819– 13824.
80. Marcus, P. I. and,, F. J. Fuller. 1979. Interferon induction by viruses. II. Sindbis virus: interferon induction requires one-quarter of the genome—genes G and A. J. Gen. Virol. 44: 169– 177.
81. Marland, G.,, A. B. Bakker,, G. J. Adema, and, C. G. Figdor. 1996. Dendritic cells in immune response induction. Stem Cells 14: 501– 507.
82. McGreal, E. P.,, L. Martinez-Pomares, and, S. Gordon. 2004. Divergent roles for C-type lectins expressed by cells of the innate immune system. Mol. Immunol. 41: 1109– 1121.
83. McWhirter, S. M.,, K. A. Fitzgerald,, J. Rosains,, D. C. Rowe,, D. T. Golenbock, and, T. Maniatis. 2004. IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. USA 101: 233– 238.
84. Mecs, E.,, J. A. Sonnabend,, E. M. Martin, and, K. H. Fantes. 1967. The effect of interferon on the synthesis of RNA in chick cells infected with Semliki forest virus. J. Gen. Virol. 1: 25– 40.
85. Meylan, E.,, J. Tschopp, and, M. Karin. 2006. Intracellular pattern recognition receptors in the host response. Nature 442: 39– 44.
86. Monlux, W. S.,, A. J. Luedke, and, J. Bowne. 1972. Central nervous system response of horses to Venezuelan equine encephalomyelitis vaccine (TC-83). J. Am. Vet. Med. Assoc. 161: 265– 269.
87. Morens, D. M., and, S. B. Halstead. 1990. Measurement of antibody-dependent infection enhancement of four dengue virus serotypes by monoclonal and polyclonal antibodies. J. Gen. Virol. 71(Pt. 12): 2909– 2914.
88. Morrison, T. E.,, A. C. Whitmore,, R. S. Shabman,, B. A. Lidbury,, S. Mahalingam, and, M. T. Heise. 2006. Characterization of Ross River virus tropism and virus-induced inflammation in a mouse model of viral arthritis and myositis. J. Virol. 80: 737– 749.
89. Muller, U.,, U. Steinhoff,, L. F. Reis,, S. Hemmi,, J. Pavlovic,, R. M. Zinkernagel, and, M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918– 1921.
90. Navarro-Sanchez, E.,, R. Altmeyer,, A. Amara,, O. Schwartz,, F. Fieschi,, J. L. Virelizier,, F. Arenzana-Seisdedos, and, P. Despres. 2003. Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep. 4: 723– 728.
91. Niesters, H. G., and, J. H. Strauss. 1990. Defined mutations in the 5′ nontranslated sequence of Sindbis virus RNA. J. Virol. 64: 4162– 4168.
92. Niesters, H. G., and, J. H. Strauss. 1990. Mutagenesis of the conserved 51-nucleotide region of Sindbis virus. J. Virol. 64: 1639– 1647.
93. Ou, J. H.,, E. G. Strauss, and, J. H. Strauss. 1981. Comparative studies of the 3′-terminal sequences of several alpha virus RNAs. Virology 109: 281– 289.
94. Paz, S.,, Q. Sun,, P. Nakhaei,, R. Romieu-Mourez,, D. Goubau,, I. Julkunen,, R. Lin, and, J. Hiscott. 2006. Induction of IRF3 and IRF7 phosphorylation following activation of the RIG-I pathway. Cell. Mol. Biol. (Noisy-le-grand) 52: 17– 28.
95. Peranen, J., and, L. Kaariainen. 1991. Biogenesis of type I cytopathic vacuoles in Semliki Forest virus-infected BHK cells. J. Virol. 65: 1623– 1627.
96. Peranen, J.,, M. Rikkonen,, P. Liljestrom, and, L. Kaariainen. 1990. Nuclear localization of Semliki Forest virus-specific nonstructural protein nsP2. J. Virol. 64: 1888– 1896.
97. Perera, R.,, K. E. Owen,, T. L. Tellinghuisen,, A. E. Gorbalenya, and, R. J. Kuhn. 2001. Alphavirus nucleocapsid protein contains a putative coiled coil alpha-helix important for core assembly. J. Virol. 75: 1– 10.
98. Pichlmair, A.,, O. Schulz,, C. P. Tan,, T. I. Naslund,, P. Liljestrom,, F. Weber, and, C. Reis e Sousa. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314: 997– 1001.
99. Pinheiro, F. P.,, R. B. Freitas,, J. F. Travassos da Rosa,, Y. B. Gabbay,, W. A. Mello, and, J. W. LeDuc. 1981. An outbreak of Mayaro virus disease in Belterra, Brazil. I. Clinical and virological findings. Am. J. Trop. Med. Hyg. 30: 674– 681.
100. Pletnev, S. V.,, W. Zhang,, S. Mukhopadhyay,, B. R. Fisher,, R. Hernandez,, D. T. Brown,, T. S. Baker,, M. G. Rossmann, and, R. J. Kuhn. 2001. Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold. Cell 105: 127– 136.
101. Pollara, G.,, D. R. Katz, and, B. M. Chain. 2005. LIGHTing up dendritic cell activation: immune regulation and viral exploitation. J. Cell. Physiol. 205: 161– 162.
102. Porterfield, J. S. 1986. Antibody-dependent enhancement of viral infectivity. Adv. Virus Res. 31: 335– 355.
103. Postic, B.,, C. J. Schleupner,, J. A. Armstrong, and, M. Ho. 1969. Two variants of Sindbis virus which differ in interferon induction and serum clearance. I. The phenomenon. J. Infect. Dis. 120: 339– 347.
104. Proll, S.,, G. Dobler,, M. Pfeffer,, T. Jelinek,, H. D. Nothdurft, and, T. Loscher. 1999. [Persistent arthralgias in Ross-River-Virus disease after travel to the South Pacific]. Dtsch. Med. Wochenschr. 124: 759– 762.
105. Rabinovich, S., and, C. Liu. 1968. Interferon content of organs and serum after intravenous inoculation of mice with Sindbis virus. Exp. Med. Surg. 26: 117– 123.
106. Rebello, M. C.,, M. E. Fonseca,, J. O. Marinho, and, M. A. Rebello. 1993. Interferon action on Mayaro virus replication. Acta Virol. 37: 223– 231.
107. Rikkonen, M. 1996. Functional significance of the nuclear-targeting and NTP-binding motifs of Semliki Forest virus nonstructural protein nsP2. Virology 218: 352– 361.
108. Rikkonen, M.,, J. Peranen, and, L. Kaariainen. 1994. ATPase and GTPase activities associated with Semliki Forest virus nonstructural protein nsP2. J. Virol. 68: 5804– 5810.
109. Ritchie, K. J.,, C. S. Hahn,, K. I. Kim,, M. Yan,, D. Rosario,, L. Li,, J. C. de la Torre, and, D. E. Zhang. 2004. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 10: 1374– 1378.
110. Ryman, K. D.,, C. L. Gardner,, C. W. Burke,, K. C. Meier,, J. M. Thompson, and, W. B. Klimstra. 2007. Heparan sulfate binding can contribute to the neurovirulence of neuroadapted and nonneuroadapted Sindbis viruses. J. Virol. 81: 3563– 3573.
111. Ryman, K. D.,, W. B. Klimstra, and, R. E. Johnston. 2004. Attenuation of Sindbis virus variants incorporating uncleaved PE2 glycoprotein is correlated with attachment to cell-surface heparan sulfate. Virology 322: 1– 12.
112. Ryman, K. D.,, W. B. Klimstra,, K. B. Nguyen,, C. A. Biron, and, R. E. Johnston. 2000. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J. Virol. 74: 3366– 3378.
113. Ryman, K. D.,, K. C. Meier,, C. L. Gardner, and, W. B. Klimstra. 2007. Non-pathogenic Sindbis virus causes viral hemorrhagic fever in the absence of alpha/beta and gamma interferons. Virology 368: 273– 285.
114. Ryman, K. D.,, K. C. Meier,, E. M. Nangle,, S. L. Ragsdale,, N. L. Korneeva,, R. E. Rhoads,, M. R. Macdonald, and, W. B. Klimstra. 2005. Sindbis virus translation is inhibited by a PKR/RNase L-independent effector induced by alpha/beta interferon priming of dendritic cells. J. Virol. 79: 1487– 1499.
115. Ryman, K. D.,, L. J. White,, R. E. Johnston, and, W. B. Klimstra. 2002. Effects of PKR/RNase L-dependent and alternative antiviral pathways on alphavirus replication and pathogenesis. Viral Immunol. 15: 53– 76.
117. Sawicki, D. L.,, R. H. Silverman,, B. R. Williams, and, S. G. Sawicki. 2003. Alphavirus minus-strand synthesis and persistence in mouse embryo fibroblasts derived from mice lacking RNase L and protein kinase R. J. Virol. 77: 1801– 1811.
118. Schafer, S. L.,, R. Lin,, P. A. Moore,, J. Hiscott, and, P. M. Pitha. 1998. Regulation of type I interferon gene expression by interferon regulatory factor-3. J. Biol. Chem. 273: 2714– 2720.
119. Schoneboom, B. A.,, J. S. Lee, and, F. B. Grieder. 2000. Early expression of IFN-alpha/beta and iNOS in the brains of Venezuelan equine encephalitis virus-infected mice. J. Interferon Cytokine Res. 20: 205– 215.
120. Schoub, B. D.,, C. J. Dommann,, S. Johnson,, C. Downie, and, P. L. Patel. 1990. Encephalitis in a 13-year-old boy following 17D yellow fever vaccine. J. Infect. 21: 105– 106.
121. Shabman, R. S.,, T. E. Morrison,, C. Moore,, L. White,, M. S. Suthar,, L. Hueston,, N. Rulli,, B. Lidbury,, J. P. Ting,, S. Mahalingam, and, M. T. Heise. 2007. Differential induction of type I interferon responses in myeloid dendritic cells by mosquito and mammalian-cell-derived alphaviruses. J. Virol. 81: 237– 247.
122. Sherman, L. A., and, D. E. Griffin. 1990. Pathogenesis of encephalitis induced in newborn mice by virulent and avirulent strains of Sindbis virus. J. Virol. 64: 2041– 2046.
123. Shirako, Y., and, J. H. Strauss. 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.
124. Sonnabend, J. A.,, E. M. Martin,, E. Mecs, and, K. H. Fantes. 1967. The effect of interferon on the synthesis and activity of an RNA polymerase isolated from chick cells infected with Semliki forest virus. J. Gen. Virol. 1: 41– 48.
125. Strahle, L.,, J. B. Marq,, A. Brini,, S. Hausmann,, D. Kolakofsky, and, D. Garcin. 2007. Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J. Virol. 81: 12227– 12237.
126. Strauss, E. G.,, C. M. Rice, and, J. H. Strauss. 1984. Complete nucleotide sequence of the genomic RNA of Sindbis virus. Virology 133: 92– 110.
127. Strauss, J. H., and, E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58: 491– 562.
128. Tassaneetrithep, B.,, T. H. Burgess,, A. Granelli-Piperno,, C. Trumpfheller,, J. Finke,, W. Sun,, M. A. Eller,, K. Pattanapanyasat,, S. Sarasombath,, D. L. Birx,, R. M. Steinman,, S. Schlesinger, and, M. A. Marovich. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197: 823– 829.
129. Tesfay, M.,, J. Yin,, C. L. Gardner,, M. Khoretonenko,, N. Korneeva,, R. E. Rhoads,, K. D. Ryman, and, W. B. Klimstra. 2008. Interferon alpha/beta inhibits cap-dependent translation of viral but not cellular mRNA by a PKR-independent mechanism. J. Virol. 82: 2620– 2630.
130. Tesh, R. B.,, D. M. Watts,, K. L. Russell,, C. Damodaran,, C. Calampa,, C. Cabezas,, G. Ramirez,, B. Vasquez,, C. G. Hayes,, C. A. Rossi,, A. M. Powers,, C. L. Hice,, L. J. Chandler,, B. C. Cropp,, N. Karabatsos,, J. T. Roehrig, and, D. J. Gubler. 1999. Mayaro virus disease: an emerging mosquito-borne zoonosis in tropical South America. Clin. Infect. Dis. 28: 67– 73.
131. Trgovcich, J.,, J. F. Aronson, and, R. E. Johnston. 1996. Fatal Sindbis virus infection of neonatal mice in the absence of encephalitis. Virology 224: 73– 83.
132. Trischmann, H.,, D. Davis, and, P. J. Lachmann. 1995. Lymphocytotropic strains of HIV type 1 when complexed with enhancing antibodies can infect macrophages via Fc gamma RIII, independently of CD4. AIDS Res. Hum. Retroviruses 11: 343– 352.
133. Vasiljeva, L.,, A. Merits,, P. Auvinen, and, L. Kaariainen. 2000. Identification of a novel function of the alphavirus capping apparatus. RNA 5′-triphosphatase activity of Nsp2. J. Biol. Chem. 275: 17281– 17287.
134. Ventoso, I.,, M. A. Sanz,, S. Molina,, J. J. Berlanga,, L. Carrasco, and, M. Esteban. 2006. Translational resistance of late alphavirus mRNA to eIF2alpha phosphorylation: a strategy to overcome the antiviral effect of protein kinase PKR. Genes Dev. 20: 87– 100.
135. Vogel, P.,, W. M. Kell,, D. L. Fritz,, M. D. Parker, and, R. J. Schoepp. 2005. Early events in the pathogenesis of eastern equine encephalitis virus in mice. Am. J. Pathol. 166: 159– 171.
136. Watts, D. M.,, J. Callahan,, C. Rossi,, M. S. Oberste,, J. T. Roehrig,, M. T. Wooster,, J. F. Smith,, C. B. Cropp,, E. M. Gentrau,, N. Karabatsos,, D. Gubler, and, C. G. Hayes. 1998. Venezuelan equine encephalitis febrile cases among humans in the Peruvian Amazon River region. Am. J. Trop. Med. Hyg. 58: 35– 40.
137. Wesselingh, S. L.,, B. Levine,, R. J. Fox,, S. Choi, and, D. E. Griffin. 1994. Intracerebral cytokine mRNA expression during fatal and nonfatal alphavirus encephalitis suggests a predominant type 2 T cell response. J. Immunol. 152: 1289– 1297.
138. White, L. J.,, J. G. Wang,, N. L. Davis, and, R. E. Johnston. 2001. Role of alpha/beta interferon in Venezuelan equine encephalitis virus pathogenesis: effect of an attenuating mutation in the 5′ untranslated region. J. Virol. 75: 3706– 3718.
139. Yoneyama, M.,, M. Kikuchi,, T. Natsukawa,, N. Shinobu,, T. Imaizumi,, M. Miyagishi,, K. Taira,, S. Akira, and, T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5: 730– 737.
140. Zhang, Y.,, C. W. Burke,, K. D. Ryman, and, W. B. Klimstra. 2007. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J. Virol. 81: 11246– 11255.
141. Zhou, H., and, S. Perlman. 2007. Mouse hepatitis virus does not induce beta interferon synthesis and does not inhibit its induction by double-stranded RNA. J. Virol. 81: 568– 574.

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