A determinant of sindbis virus neurovirulence enables efficient disruption of Jak/STAT signaling

Journal of Virology

Volumn 84, Issue 21, 2010, Pages 11429-11439

  Simmons, Jason D ^a,b   Wollish, Amy C ^a,b   Heise, Mark T ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON; JANUS KINASE 1; JANUS KINASE 2; PROTEIN KINASE TYK2; STAT1 PROTEIN; STAT2 PROTEIN; THREONINE; INTERFERON; JANUS KINASE; STAT PROTEIN;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SINDBIS VIRUS; VERO CELL; VIRUS ACTIVATION; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE; ANIMAL; CHLOROCEBUS AETHIOPS; METABOLISM; MOUSE; PATHOGENICITY; PHOSPHORYLATION; SPECIES DIFFERENCE; VERO CELL LINE; VIRULENCE;

ANIMALS; CERCOPITHECUS AETHIOPS; DOWN-REGULATION; INTERFERON TYPE I; INTERFERON-GAMMA; JANUS KINASES; MICE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SINDBIS VIRUS; SPECIES SPECIFICITY; STAT TRANSCRIPTION FACTORS; VERO CELLS; VIRULENCE;

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

EID: 77957955050     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00577-10     Document Type: Article

References (63)

1. Aguilar, P. V., A. P. Adams, E. Wang, W. Kang, A. S. Carrara, M. Anishchenko, I. Frolov, and S. C. Weaver. 2008. Structural and nonstructural protein genome regions of eastern equine encephalitis virus are determinants of interferon sensitivity and murine virulence. J. Virol. 82:4920-4930.
2. 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 systems but not in mosquito cells. J. Virol. 82:6972-6983.
3. 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.
4. Best, S. M., K. L. Morris, J. G. Shannon, S. J. Robertson, D. N. Mitzel, G. S. Park, E. Boer, J. B. Wolfinbarger, and M. E. Bloom. 2005. Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J. Virol. 79:12828-12839.
5. Binder, G. K., and D. E. Griffin. 2001. Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons. Science 293:303-306.
6. Burdeinick-Kerr, R., D. Govindarajan, and D. E. Griffin. 2009. Noncytolytic clearance of Sindbis virus infection from neurons by gamma interferon is dependent on Jak/STAT signaling. J. Virol. 83:3429-3435.
7. Burdeinick-Kerr, R., and D. E. Griffin. 2005. Gamma interferon-dependent, noncytolytic clearance of Sindbis virus infection from neurons in vitro. J. Virol. 79:5374-5385.
8. Burdeinick-Kerr, R., J. Wind, and D. E. Griffin. 2007. Synergistic roles of antibody and interferon in noncytolytic clearance of Sindbis virus from different regions of the central nervous system. J. Virol. 81:5628-5636.
9. 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.
10. 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.
11. Colamonici, O. R., H. Uyttendaele, P. Domanski, H. Yan, and J. J. Krolewski. 1994. p135tyk2, an interferon-alpha-activated tyrosine kinase, is physically associated with an interferon-alpha receptor. J. Biol. Chem. 269:3518-3522.
12. Cruz, C. C., M. S. Suthar, S. A. Montgomery, R. Shabman, J. Simmons, R. E. Johnston, T. E. Morrison, and M. T. Heise. 2010. Modulation of type I IFN induction by a virulence determinant within the alphavirus nsP1 protein. Virology 399:1-10.
13. Diaz, M. O., S. Ziemin, M. M. Le Beau, P. Pitha, S. D. Smith, R. R. Chilcote, and J. D. Rowley. 1988. Homozygous deletion of the alpha- and beta 1-interferon genes in human leukemia and derived cell lines. Proc. Natl. Acad. Sci. U. S. A. 85:5259-5263.
14. Dubuisson, J., S. Lustig, N. Ruggli, Y. Akov, and C. M. Rice. 1997. Genetic determinants of Sindbis virus neuroinvasiveness. J. Virol. 71:2636-2646.
15. Friedman, R. L., S. P. Manly, M. McMahon, I. M. Kerr, and G. R. Stark. 1984. Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell 38:745-755.
16. Friedman, R. L., and G. R. Stark. 1985. Alpha-interferon-induced transcription of HLA and metallothionein genes containing homologous upstream sequences. Nature 314:637-639.
17. 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.
18. Gardner, C. L., C. W. Burke, M. Z. Tesfay, P. J. Glass, W. B. Klimstra, and K. D. Ryman. 2008. Eastern and Venezuelan equine encephalitis viruses differ in their ability to infect dendritic cells and macrophages: impact of altered cell tropism on pathogenesis. J. Virol. 82:10634-10646.
19. Garmashova, N., S. Atasheva, W. Kang, S. C. Weaver, E. Frolova, and I. Frolov. 2007. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J. Virol. 81:13552-13565.
20. 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.
21. 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. (Pubitemid 46303363)
22. Gil, M. P., E. Bohn, A. K. O'Guin, C. V. Ramana, B. Levine, G. R. Stark, H. W. Virgin, and R. D. Schreiber. 2001. Biologic consequences of Stat1-independent IFN signaling. Proc. Natl. Acad. Sci. U. S. A. 98:6680-6685.
23. 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. U. S. A. 103:8459-8464.
24. Griffin, D. E. 2010. Recovery from viral encephalomyelitis: immune-mediated noncytolytic virus clearance from neurons. Immunol. Res. 47:123-133.
25. Guo, J. T., J. Hayashi, and C. Seeger. 2005. West Nile virus inhibits the signal transduction pathway of alpha interferon. J. Virol. 79:1343-1350. (Pubitemid 40459081)
26. 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.
27. Heise, M. T., D. A. Simpson, and R. E. Johnston. 2000. A single amino acid change in nsP1 attenuates neurovirulence of the Sindbis-group alphavirus S.A.AR86. J. Virol. 74:4207-4213.
28. Heise, M. T., L. J. White, D. A. Simpson, C. Leonard, K. A. Bernard, R. B. Meeker, and R. E. Johnston. 2003. An attenuating mutation in nsP1 of the Sindbis-group virus S.A.AR86 accelerates nonstructural protein processing and up-regulates viral 26S RNA synthesis. J. Virol. 77:1149-1156.
29. Heise, M. T., A. Whitmore, J. Thompson, M. Parsons, A. A. Grobbelaar, A. Kemp, J. T. Paweska, K. Madric, L. J. White, R. Swanepoel, and F. J. Burt. 2009. An alphavirus replicon-derived candidate vaccine against Rift Valley fever virus. Epidemiol. Infect. 137:1309-1318.
30. 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.
31. Jackson, A. C., T. R. Moench, B. D. Trapp, and D. E. Griffin. 1988. Basis of neurovirulence in Sindbis virus encephalomyelitis of mice. Lab. Invest. 58:503-509.
32. Johnson, K. E., and D. M. Knipe. 2010. Herpes simplex virus-1 infection causes the secretion of a type I interferon-antagonizing protein and inhibits signaling at or before Jak-1 activation. Virology 396:21-29.
33. 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.
34. 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.
35. Laurent-Rolle, M., E. F. Boer, K. J. Lubick, J. B. Wolfinbarger, A. B. Carmody, B. Rockx, W. Liu, J. Ashour, W. L. Shupert, M. R. Holbrook, A. D. Barrett, P. W. Mason, M. E. Bloom, A. Garcia-Sastre, A. A. Khromykh, and S. M. Best. 2010. The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J. Virol. 84:3503-3515.
36. Levine, B., and D. E. Griffin. 1992. Persistence of viral RNA in mouse brains after recovery from acute alphavirus encephalitis. J. Virol. 66:6429-6435.
37. Levine, B., J. M. Hardwick, B. D. Trapp, T. O. Crawford, R. C. Bollinger, and D. E. Griffin. 1991. Antibody-mediated clearance of alphavirus infection from neurons. Science 254:856-860.
38. Levy, D. E., and J. E. Darnell, Jr. 2002. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell. Biol. 3:651-662.
39. Lin, R. J., C. L. Liao, E. Lin, and Y. L. Lin. 2004. Blocking of the alpha interferon-induced Jak-Stat signaling pathway by Japanese encephalitis virus infection. J. Virol. 78:9285-9294.
40. Lustig, S., M. Halevy, D. Ben-Nathan, and Y. Akov. 1992. A novel variant of Sindbis virus is both neurovirulent and neuroinvasive in adult mice. Arch. Virol. 122:237-248.
41. Lustig, S., A. C. Jackson, C. S. Hahn, D. E. Griffin, E. G. Strauss, and J. H. Strauss. 1988. Molecular basis of Sindbis virus neurovirulence in mice. J. Virol. 62:2329-2336.
42. McKnight, K. L., D. A. Simpson, S. C. Lin, T. A. Knott, J. M. Polo, D. F. Pence, D. B. Johannsen, H. W. Heidner, N. L. Davis, and R. E. Johnston. 1996. Deduced consensus sequence of Sindbis virus strain AR339: mutations contained in laboratory strains which affect cell culture and in vivo phenotypes. J. Virol. 70:1981-1989.
43. Mosca, J. D., and P. M. Pitha. 1986. Transcriptional and posttranscriptional regulation of exogenous human beta interferon gene in simian cells defective in interferon synthesis. Mol. Cell. Biol. 6:2279-2283.
44. Pearse, R. N., R. Feinman, K. Shuai, J. E. Darnell, Jr., and J. V. Ravetch. 1993. Interferon gamma-induced transcription of the high-affinity Fc receptor for IgG requires assembly of a complex that includes the 91-kDa subunit of transcription factor ISGF3. Proc. Natl. Acad. Sci. U. S. A. 90:4314-4318.
45. Pichlmair, A., O. Schulz, C. P. Tan, J. Rehwinkel, H. Kato, O. Takeuchi, S. Akira, M. Way, G. Schiavo, and C. Reis e Sousa. 2009. Activation of MDA5 requires higher-order RNA structures generated during virus infection. J. Virol. 83:10761-10769.
46. Platanias, L. C. 2005. Mechanisms of type-I- and type-II-interferon- mediated signalling. Nat. Rev. Immunol. 5:375-386.
47. Platanias, L. C., S. Uddin, P. Domanski, and O. R. Colamonici. 1996. Differences in interferon alpha and beta signaling. Interferon beta selectively induces the interaction of the alpha and beta L subunits of the type I interferon receptor. J. Biol. Chem. 271:23630-23633.
48. Reid, S. P., L. W. Leung, A. L. Hartman, O. Martinez, M. L. Shaw, C. Carbonnelle, V. E. Volchkov, S. T. Nichol, and C. F. Basler. 2006. Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J. Virol. 80:5156-5167.
49. Ryman, K. D., and W. B. Klimstra. 2008. Host responses to alphavirus infection. Immunol. Rev. 225:27-45.
50. 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.
51. Ryman, K. D., K. C. Meier, C. L. Gardner, P. A. Adegboyega, and W. B. Klimstra. 2007. Non-pathogenic Sindbis virus causes hemorrhagic fever in the absence of alpha/beta and gamma interferons. Virology 368:273-285.
52. 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.
53. Schindler, C., D. E. Levy, and T. Decker. 2007. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282:20059-20063.
54. 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.
55. Shuai, K., A. Ziemiecki, A. F. Wilks, A. G. Harpur, H. B. Sadowski, M. Z. Gilman, and J. E. Darnell. 1993. Polypeptide signalling to the nucleus through tyrosine phosphorylation of Jak and Stat proteins. Nature 366:580-583.
56. Silvennoinen, O., J. N. Ihle, J. Schlessinger, and D. E. Levy. 1993. Interferon-induced nuclear signalling by Jak protein tyrosine kinases. Nature 366:583-585.
57. Simmons, J. D., L. J. White, T. E. Morrison, S. A. Montgomery, A. C. Whitmore, R. E. Johnston, and M. T. Heise. 2009. Venezuelan equine encephalitis virus disrupts STAT1 signaling by distinct mechanisms independent of host shutoff. J. Virol. 83:10571-10581.
58. Simpson, D. A., N. L. Davis, S. C. Lin, D. Russell, and R. E. Johnston. 1996. Complete nucleotide sequence and full-length cDNA clone of S.A.AR86 a South African alphavirus related to Sindbis. Virology 222:464-469.
59. Spotts, D. R., R. M. Reich, M. A. Kalkhan, R. M. Kinney, and J. T. Roehrig. 1998. Resistance to alpha/beta interferons correlates with the epizootic and virulence potential of Venezuelan equine encephalitis viruses and is determined by the 5′ noncoding region and glycoproteins. J. Virol. 72:10286-10291.
60. Suthar, M. S., R. Shabman, K. Madric, C. Lambeth, and M. T. Heise. 2005. Identification of adult mouse neurovirulence determinants of the Sindbis virus strain AR86. J. Virol. 79:4219-4228.
61. Watling, D., D. Guschin, M. Muller, O. Silvennoinen, B. A. Witthuhn, F. W. Quelle, N. C. Rogers, C. Schindler, G. R. Stark, J. N. Ihle, et al. 1993. Complementation by the protein tyrosine kinase JAK2 of a mutant cell line defective in the interferon-gamma signal transduction pathway. Nature 366:166-170.
62. 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.
63. Yin, J., C. L. Gardner, C. W. Burke, K. D. Ryman, and W. B. Klimstra. 2009. Similarities and differences in antagonism of neuron alpha/beta interferon responses by Venezuelan equine encephalitis and Sindbis alphaviruses. J. Virol. 83:10036-10047.