The role of interferon antagonist, non-structural proteins in the pathogenesis and emergence of arboviruses

Viruses

Volumn 3, Issue 6, 2011, Pages 629-658

  Hollidge, Bradley S ^a   Weiss, Susan R ^a   Soldan, Samantha S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alphavirus; Arbovirus; Bunyavirus; Emergence; Flavivirus; Innate immune system; Interferon

Indexed keywords

INTERFERON; INTERFERON ANTAGONIST; MYXOVIRUS RESISTANCE PROTEIN A; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 2A; NONSTRUCTURAL PROTEIN 2B; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4A; NONSTRUCTURAL PROTEIN 4B; NONSTRUCTURAL PROTEIN 5; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALPHA VIRUS; ARBOVIRUS; BUNYAMWERA VIRUS; CHIKUNGUNYA ALPHAVIRUS; CYTOKINE RESPONSE; DENGUE VIRUS; DISEASE SEVERITY; FLAVIVIRUS; HUMAN; INNATE IMMUNITY; JAPANESE ENCEPHALITIS VIRUS; LA CROSSE VIRUS; MOSQUITO BORNE FLAVIVIRUS; NEW WORLD ALPHA VIRUS; NONHUMAN; OLD WORLD ALPHA VIRUS; ORTHOBUNYAVIRUS; REVIEW; RIFT VALLEY FEVER BUNYAVIRUS; RNA VIRUS INFECTION; ROSS RIVER ALPHA VIRUS; SINDBIS VIRUS; TICK BORNE FLAVIVIRUS; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRAL PHENOMENA AND FUNCTIONS; VIRUS CELL INTERACTION; VIRUS EMERGENCE; VIRUS PATHOGENESIS;

ANIMALS; ARBOVIRUS INFECTIONS; ARBOVIRUSES; HUMANS; INTERFERONS; VIRAL NONSTRUCTURAL PROTEINS;

ALPHAVIRUS; ARBOVIRUS; FLAVIVIRUS; ORTHOBUNYAVIRUS;

EID: 79959634863     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v3060629     Document Type: Review

References (148)

1. Weaver, S.C.; Reisen, W.K. Present and future arboviral threats. Antivir. Res. 2010, 85, 328-345.
2. Hollidge, B.S.; Gonzalez-Scarano, F.; Soldan, S.S. Arboviral encephalitides: Transmission, emergence, and pathogenesis. J. Neuroimmune Pharmacol. 2010, 5, 428-442.
3. Livieratos, I.C.; Eliasco, E.; Muller, G.; Olsthoorn, R.C.; Salazar, L.F.; Pleij, C.W.; Coutts, R.H. Analysis of the DNA of potato yellow vein virus: Evidence for a tripartite genome and conserved 3'-terminal structures among members of the genus crinivirus. J. Gen. Virol. 2004, 85, 2065-2075.
4. Ghanim, M.; Czosnek, H. Tomato yellow leaf curl geminivirus (tylcv-is) is transmitted among whiteflies (bemisia tabaci) in a sex-related manner. J. Virol. 2000, 74, 4738-4745.
5. Whitfield, A.E.; Ullman, D.E.; German, T.L. Tospovirus-thrips interactions. Annu. Rev. Phytopathol. 2005, 43, 459-489.
6. Jones, K.E.; Patel, N.G.; Levy, M.A.; Storeygard, A.; Balk, D.; Gittleman, J.L.; Daszak, P. Global trends in emerging infectious diseases. Nature 2008, 451, 990-993.
7. Gubler, D.J. The global emergence/resurgence of arboviral diseases as public health problems. Arch. Med. Res. 2002, 33, 330-342.
8. Elliott, R.M. Bunyaviruses and climate change. Clin. Microbiol. Infect. 2009, 15, 510-517.
9. Benedict, M.Q.; Levine, R.S.; Hawley, W.A.; Lounibos, L.P. Spread of the tiger: Global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis. 2007, 7, 76-85.
10. Fonseca, D.M.; Keyghobadi, N.; Malcolm, C.A.; Mehmet, C.; Schaffner, F.; Mogi, M.; Fleischer, R.C.; Wilkerson, R.C. Emerging vectors in the Culex pipiens complex. Science 2004, 303, 1535-1538.
11. Weaver, S.C.; Barrett, A.D. Transmission cycles, host range, evolution and emergence of arboviral disease. Nat. Rev. Microbiol. 2004, 2, 789-801.
12. Barrett, A.D.; Higgs, S. Yellow fever: A disease that has yet to be conquered. Annu. Rev. Entomol. 2007, 52, 209-229.
13. Nimmannitya, S.; Halstead, S.B.; Cohen, S.N.; Margiotta, M.R. Dengue and chikungunya virus infection in man in Thailand, 1962-1964. I. Observations on hospitalized patients with hemorrhagic fever. Am. J. Trop. Med. Hyg. 1969, 18, 954-971.
14. Padbidri, V.S.; Gnaneswar, T.T. Epidemiological investigations of chikungunya epidemic at Barsi, Maharashtra state, India. J. Hyg. Epidemiol. Microbiol. Immunol. 1979, 23, 445-451.
15. Revilla, Y.; Granja, A.G. Viral mechanisms involved in the transcriptional CBP/p300 regulation of inflammatory and immune responses. Crit. Rev. Immunol. 2009, 29, 131-154.
16. Garmashova, N.; Gorchakov, R.; Volkova, E.; Paessler, S.; Frolova, E.; Frolov, I. The Old World and New World alphaviruses use different virus-specific proteins for induction of transcriptional shutoff. J. Virol. 2007, 81, 2472-2484.
17. Garmashova, N.; Atasheva, S.; Kang, W.; Weaver, S.C.; Frolova, E.; Frolov, I. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J. Virol. 2007, 81, 13552-13565.
18. Hornung, V.; Ellegast, J.; Kim, S.; Brzozka, K.; Jung, A.; Kato, H.; Poeck, H.; Akira, S.; Conzelmann, K.K.; Schlee, M.; Endres, S.; Hartmann, G. 5'-triphosphate DNA is the ligand for RIG-I. Science 2006, 314, 994-997.
19. Pichlmair, A.; Schulz, O.; Tan, C.P.; Naslund, T.I.; Liljestrom, P.; Weber, F.; Reis e Sousa, C. RIG-I-mediated antiviral responses to single-stranded DNA bearing 5'-phosphates. Science 2006, 314, 997-1001.
20. Saito, T.; Owen, D.M.; Jiang, F.; Marcotrigiano, J.; Gale, M., Jr. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis c virus RNA. Nature 2008, 454, 523-527.
21. Kato, H.; Takeuchi, O.; Mikamo-Satoh, E.; Hirai, R.; Kawai, T.; Matsushita, K.; Hiiragi, A.; Dermody, T.S.; Fujita, T.; Akira, S. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 2008, 205, 1601-1610.
22. Saito, T.; Gale, M., Jr. Differential recognition of double-stranded DNA by RIG-I-like receptors in antiviral immunity. J. Exp. Med. 2008, 205, 1523-1527.
23. Kato, H.; Takeuchi, O.; Sato, S.; Yoneyama, M.; Yamamoto, M.; Matsui, K.; Uematsu, S.; Jung, A.; Kawai, T.; Ishii, K.J.; Yamaguchi, O.; Otsu, K.; Tsujimura, T.; Koh, C.S.; Reis e Sousa, C.; Matsuura, Y.; Fujita, T.; Akira, S. Differential roles of MDA5 and RIG-I helicases in the recognition of DNA viruses. Nature 2006, 441, 101-105.
24. Gitlin, L.; Barchet, W.; Gilfillan, S.; Cella, M.; Beutler, B.; Flavell, R.A.; Diamond, M.S.; Colonna, M. Essential role of MDA-5 in type I IFN responses to polyriboinosinic: Polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 8459-8464.
25. Pichlmair, A.; Schulz, O.; Tan, C.P.; Rehwinkel, J.; Kato, H.; Takeuchi, O.; Akira, S.; Way, M.; Schiavo, G.; Reis e Sousa, C. Activation of MDA5 requires higher-order DNA structures generated during virus infection. J. Virol. 2009, 83, 10761-10769.
26. Sharma, S.; tenOever, B.R.; Grandvaux, N.; Zhou, G.P.; Lin, R.; Hiscott, J. Triggering the interferon antiviral response through an IKK-related pathway. Science 2003, 300, 1148-1151.
27. Fitzgerald, K.A.; McWhirter, S.M.; Faia, K.L.; Rowe, D.C.; Latz, E.; Golenbock, D.T.; Coyle, A.J.; Liao, S.M.; Maniatis, T. Ikkepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4, 491-496.
28. Honda, K.; Yanai, H.; Negishi, H.; Asagiri, M.; Sato, M.; Mizutani, T.; Shimada, N.; Ohba, Y.; Takaoka, A.; Yoshida, N.; Taniguchi, T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434, 772-777.
29. Janeway, C.A., Jr.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20, 197-216.
30. Takeda, K.; Kaisho, T.; Akira, S. Toll-like receptors. Annu. Rev. Immunol. 2003, 21, 335-376.
31. Zhang, D.; Zhang, G.; Hayden, M.S.; Greenblatt, M.B.; Bussey, C.; Flavell, R.A.; Ghosh, S. A toll-like receptor that prevents infection by uropathogenic bacteria. Science 2004, 303, 1522-1526.
32. Iwasaki, A.; Medzhitov, R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5, 987-995.
33. Diebold, S.S.; Kaisho, T.; Hemmi, H.; Akira, S.; Reis e Sousa, C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303, 1529-1531.
34. Heil, F.; Hemmi, H.; Hochrein, H.; Ampenberger, F.; Kirschning, C.; Akira, S.; Lipford, G.; Wagner, H.; Bauer, S. Species-specific recognition of single-stranded DNA via toll-like receptor 7 and 8. Science 2004, 303, 1526-1529.
35. Lund, J.M.; Alexopoulou, L.; Sato, A.; Karow, M.; Adams, N.C.; Gale, N.W.; Iwasaki, A.; Flavell, R.A. Recognition of single-stranded DNA viruses by toll-like receptor 7. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 5598-5603.
36. Alexopoulou, L.; Holt, A.C.; Medzhitov, R.; Flavell, R.A. Recognition of double-stranded DNA and activation of NF-kappab by toll-like receptor 3. Nature 2001, 413, 732-738.
37. Bauer, S.; Kirschning, C.J.; Hacker, H.; Redecke, V.; Hausmann, S.; Akira, S.; Wagner, H.; Lipford, G.B. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 9237-9242.
38. Yamamoto, M.; Sato, S.; Mori, K.; Hoshino, K.; Takeuchi, O.; Takeda, K.; Akira, S. Cutting edge: A novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the toll-like receptor signaling. J. Immunol. 2002, 169, 6668-6672.
39. Garcia, M.A.; Meurs, E.F.; Esteban, M. The dsRNA protein kinase PKR: Virus and cell control. Biochimie 2007, 89, 799-811.
40. Hovanessian, A.G. Interferon-induced and double-stranded RNA-activated enzymes: A specific protein kinase and 2',5'-oligoadenylate synthetases. J. Interferon. Res. 1991, 11, 199-205.
41. Novick, D.; Cohen, B.; Rubinstein, M. The human interferon alpha/beta receptor: Characterization and molecular cloning. Cell 1994, 77, 391-400.
42. Colamonici, O.; Yan, H.; Domanski, P.; Handa, R.; Smalley, D.; Mullersman, J.; Witte, M.; Krishnan, K.; Krolewski, J. Direct binding to and tyrosine phosphorylation of the alpha subunit of the type I interferon receptor by p135tyk2 tyrosine kinase. Mol. Cell Biol. 1994, 14, 8133-8142.
43. Colamonici, O.R.; Platanias, L.C.; Domanski, P.; Handa, R.; Gilmour, K.C.; Diaz, M.O.; Reich, N.; Pitha-Rowe, P. Transmembrane signaling by the alpha subunit of the type I interferon receptor is essential for activation of the JAK kinases and the transcriptional factor ISGF3. J. Biol. Chem. 1995, 270, 8188-8193.
44. Domanski, P.; Fish, E.; Nadeau, O.W.; Witte, M.; Platanias, L.C.; Yan, H.; Krolewski, J.; Pitha, P.; Colamonici, O.R. A region of the beta subunit of the interferon alpha receptor different from box 1 interacts with JAK1 and is sufficient to activate the JAK-STAT pathway and induce an antiviral state. J. Biol. Chem. 1997, 272, 26388-26393.
45. Nadeau, O.W.; Domanski, P.; Usacheva, A.; Uddin, S.; Platanias, L.C.; Pitha, P.; Raz, R.; Levy, D.; Majchrzak, B.; Fish, E.; Colamonici, O.R. The proximal tyrosines of the cytoplasmic domain of the beta chain of the type I interferon receptor are essential for signal transducer and activator of transcription (STAT) 2 activation. Evidence that two STAT2 sites are required to reach a threshold of interferon alpha-induced STAT2 tyrosine phosphorylation that allows normal formation of interferon-stimulated gene factor 3. J. Biol. Chem. 1999, 274, 4045-4052.
46. Gupta, S.; Yan, H.; Wong, L.H.; Ralph, S.; Krolewski, J.; Schindler, C. The SH2 domains of STAT1 and STAT2 mediate multiple interactions in the transduction of IFN-alpha signals. EMBO. J. 1996, 15, 1075-1084.
47. Fu, X.Y.; Kessler, D.S.; Veals, S.A.; Levy, D.E.; Darnell, J.E., Jr. ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 8555-8559.
48. Kessler, D.S.; Levy, D.E.; Darnell, J.E., Jr. Two interferon-induced nuclear factors bind a single promoter element in interferon-stimulated genes. Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 8521-8525.
49. Qureshi, S.A.; Salditt-Georgieff, M.; Darnell, J.E., Jr. Tyrosine-phosphorylated STAT1 and STAT2 plus a 48-kDa protein all contact DNA in forming interferon-stimulated-gene factor 3. Proc. Natl. Acad. Sci. U. S. A. 1995, 92, 3829-3833.
50. Calisher, C.H. History, classification, and taxonomy of viruses in the family Bunyaviridae. In The Bunyaviridae; Elliot, R., Ed.; Plenum Press: New York, NY, USA, 1996; pp. 11-17.
51. Plyusnin, A.; Morzunov, S.P. Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr. Top. Microbiol. Immunol. 2001, 256, 47-75.
52. Soldan, S.S.; Gonzalez-Scarano, F. Emerging infectious diseases: The Bunyaviridae. J. Neurovirol. 2005, 11, 412-423.
53. Dionisio, D.; Esperti, F.; Vivarelli, A.; Valassina, M. Epidemiological, clinical and laboratory aspects of sandfly fever. Curr. Opin. Infect. Dis. 2003, 16, 383-388.
54. Ergonul, O. Crimean-Congo haemorrhagic fever. Lancet Infect. Dis. 2006, 6, 203-214.
55. Hoogstraal, H. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J. Med. Entomol. 1979, 15, 307-417.
56. Schmaljohn, C.S. Bunyaviridae: The viruses and their replication. In Fields Virology, 4th ed.; Howley, D.M., Ed.; Lippincott Williams and Wilkins: Philadelphia, PA, USA, 2001.
57. Mohamed, M.; McLees, A.; Elliott, R.M. Viruses in the Anopheles A, Anopheles B, and Tete serogroups in the orthobunyavirus genus (family Bunyaviridae) do not encode an NSs protein. J. Virol. 2009, 83, 7612-7618.
58. Borucki, M.K.; Kempf, B.J.; Blitvich, B.J.; Blair, C.D.; Beaty, B.J. La Crosse virus: Replication in vertebrate and invertebrate hosts. Microbes Infect. 2002, 4, 341-350.
59. Pekosz, A.; Phillips, J.; Pleasure, D.; Merry, D.; Gonzalez-Scarano, F. Induction of apoptosis by La Crosse virus infection and role of neuronal differentiation and human bcl-2 expression in its prevention. J. Virol. 1996, 70, 5329-5335.
60. De Gregorio, E.; Spellman, P.T.; Tzou, P.; Rubin, G.M.; Lemaitre, B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO. J. 2002, 21, 2568-2579.
61. Dostert, C.; Jouanguy, E.; Irving, P.; Troxler, L.; Galiana-Arnoux, D.; Hetru, C.; Hoffmann, J.A.; Imler, J.L. The JAK-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat. Immunol. 2005, 6, 946-953.
62. Tanji, T. Activation of the drosophila innate immunity by the toll and IMD pathways. Seikagaku 2006, 78, 413-417.
63. Tanji, T.; Hu, X.; Weber, A.N.; Ip, Y.T. Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol. Cell Biol. 2007, 27, 4578-4588.
64. Tanji, T.; Ip, Y.T. Regulators of the toll and IMD pathways in the drosophila innate immune response. Trends Immunol. 2005, 26, 193-198.
65. Soldan, S.S.; Plassmeyer, M.L.; Matukonis, M.K.; Gonzalez-Scarano, F. La Crosse virus nonstructural protein NSs counteracts the effects of short interfering RNA. J. Virol. 2005, 79, 234-244.
66. Habjan, M.; Andersson, I.; Klingstrom, J.; Schumann, M.; Martin, A.; Zimmermann, P.; Wagner, V.; Pichlmair, A.; Schneider, U.; Muhlberger, E.; Mirazimi, A.; Weber, F. Processing of genome 5' termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE 2008, 3, 2032.
67. Griot, C.; Gonzalez-Scarano, F.; Nathanson, N. Molecular determinants of the virulence and infectivity of california serogroup bunyaviruses. Annu. Rev. Microbiol. 1993, 47, 117-138.
68. Haddow, A.D.; Odoi, A. The incidence risk, clustering, and clinical presentation of La Crosse virus infections in the Eastern United States, 2003-2007. PLoS ONE 2009, 4, e6145.
69. McJunkin, J.E.; de los Reyes, E.C.; Irazuzta, J.E.; Caceres, M.J.; Khan, R.R.; Minnich, L.L.; Fu, K.D.; Lovett, G.D.; Tsai, T.; Thompson, A. La Crosse encephalitis in children. N. Engl. J. Med. 2001, 344, 801-807.
70. Lambert, A.J.; Blair, C.D.; D'Anton, M.; Ewing, W.; Harborth, M.; Seiferth, R.; Xiang, J.; Lanciotti, R.S. La Crosse virus in Aedes albopictus mosquitoes, Texas, USA, 2009. Emerg. Infect. Dis. 2010, 16, 856-858.
71. Blakqori, G.; Delhaye, S.; Habjan, M.; Blair, C.D.; Sanchez-Vargas, I.; Olson, K.E.; Attarzadeh-Yazdi, G.; Fragkoudis, R.; Kohl, A.; Kalinke, U.; Weiss, S.; Michiels, T.; Staeheli, P.; Weber, F. La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J. Virol. 2007, 81, 4991-4999.
72. Verbruggen, P.; Ruf, M.; Blakqori, G.; Overby, A.K.; Heidemann, M.; Eick, D.; Weber, F. Interferon antagonist NSs of La Crosse virus triggers a DNA damage response-like degradation of transcribing RNA polymerase II. J. Biol. Chem. 2011, 286, 3681-3692.
73. Haller, O.; Frese, M.; Kochs, G. Mx proteins: Mediators of innate resistance to RNA viruses. Rev. Sci. Tech. 1998, 17, 220-230.
74. Hefti, H.P.; Frese, M.; Landis, H.; Di Paolo, C.; Aguzzi, A.; Haller, O.; Pavlovic, J. Human MxA protein protects mice lacking a functional alpha/beta interferon system against La Crosse virus and other lethal viral infections. J. Virol. 1999, 73, 6984-6991.
75. Staeheli, P.; Sutcliffe, J.G. Identification of a second interferon-regulated murine Mx gene. Mol. Cell Biol. 1988, 8, 4524-4528.
76. Pavlovic, J.; Arzet, H.A.; Hefti, H.P.; Frese, M.; Rost, D.; Ernst, B.; Kolb, E.; Staeheli, P.; Haller, O. Enhanced virus resistance of transgenic mice expressing the human MxA protein. J. Virol. 1995, 69, 4506-4510.
77. Andersson, I.; Lundkvist, A.; Haller, O.; Mirazimi, A. Type I interferon inhibits Crimean-Congo hemorrhagic fever virus in human target cells. J. Med. Virol. 2006, 78, 216-222.
78. Habjan, M.; Pichlmair, A.; Elliott, R.M.; Overby, A.K.; Glatter, T.; Gstaiger, M.; Superti-Furga, G.; Unger, H.; Weber, F. NSs protein of Rift Valley fever virus induces the specific degradation of the double-stranded RNA-dependent protein kinase. J. Virol. 2009, 83, 4365-4375.
79. Oelschlegel, R.; Kruger, D.H.; Rang, A. MxA-independent inhibition of hantaan virus replication induced by type I and type II interferon in vitro. Virus Res. 2007, 127, 100-105.
80. Bouloy, M.; Janzen, C.; Vialat, P.; Khun, H.; Pavlovic, J.; Huerre, M.; Haller, O. Genetic evidence for an interferon-antagonistic function of Rift Valley fever virus nonstructural protein NSs. J. Virol. 2001, 75, 1371-1377.
81. Streitenfeld, H.; Boyd, A.; Fazakerley, J.K.; Bridgen, A.; Elliott, R.M.; Weber, F. Activation of PKR by bunyamwera virus is independent of the viral interferon antagonist NSs. J. Virol. 2003, 77, 5507-5511.
82. Blakqori, G.; Weber, F. Efficient cDNA-based rescue of La Crosse bunyaviruses expressing or lacking the nonstructural protein NSs. J. Virol. 2005, 79, 10420-10428.
83. Le May, N.; Dubaele, S.; Proietti De Santis, L.; Billecocq, A.; Bouloy, M.; Egly, J.M. TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 2004, 116, 541-550.
84. Leonard, V.H.; Kohl, A.; Hart, T.J.; Elliott, R.M. Interaction of bunyamwera orthobunyavirus NSs protein with mediator protein MED8: A mechanism for inhibiting the interferon response. J. Virol. 2006, 80, 9667-9675.
85. Thomas, D.; Blakqori, G.; Wagner, V.; Banholzer, M.; Kessler, N.; Elliott, R.M.; Haller, O.; Weber, F. Inhibition of RNA polymerase II phosphorylation by a viral interferon antagonist. J. Biol. Chem. 2004, 279, 31471-31477.
86. Zhang, M.; Siedow, M.; Saia, G.; Chakravarti, A. Inhibition of p21-activated kinase 6 (PAK6) increases radiosensitivity of prostate cancer cells. Prostate 2010, 70, 807-816.
87. Ratner, J.N.; Balasubramanian, B.; Corden, J.; Warren, S.L.; Bregman, D.B. Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of RNA polymerase II. Implications for transcription-coupled DNA repair. J. Biol. Chem. 1998, 273, 5184-5189.
88. Beaudenon, S.L.; Huacani, M.R.; Wang, G.; McDonnell, D.P.; Huibregtse, J.M. RSP5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell Biol. 1999, 19, 6972-6979.
89. Harreman, M.; Taschner, M.; Sigurdsson, S.; Anindya, R.; Reid, J.; Somesh, B.; Kong, S.E.; Banks, C.A.; Conaway, R.C.; Conaway, J.W.; Svejstrup, J.Q. Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 20705-20710.
90. Heine, G.F.; Horwitz, A.A.; Parvin, J.D. Multiple mechanisms contribute to inhibit transcription in response to DNA damage. J. Biol. Chem. 2008, 283, 9555-9561.
91. Somesh, B.P.; Reid, J.; Liu, W.F.; Sogaard, T.M.; Erdjument-Bromage, H.; Tempst, P.; Svejstrup, J.Q. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 2005, 121, 913-923.
92. Kohl, A.; Clayton, R.F.; Weber, F.; Bridgen, A.; Randall, R.E.; Elliott, R.M. Bunyamwera virus nonstructural protein NSs counteracts interferon regulatory factor 3-mediated induction of early cell death. J. Virol. 2003, 77, 7999-8008.
93. Blazek, E.; Mittler, G.; Meisterernst, M. The mediator of RNA polymerase II. Chromosoma 2005, 113, 399-408.
94. Conaway, R.C.; Sato, S.; Tomomori-Sato, C.; Yao, T.; Conaway, J.W. The mammalian mediator complex and its role in transcriptional regulation. Trends Biochem. Sci. 2005, 30, 250-255.
95. Kornberg, R.D. Mediator and the mechanism of transcriptional activation. Trends Biochem. Sci. 2005, 30, 235-239.
96. Myers, L.C.; Gustafsson, C.M.; Bushnell, D.A.; Lui, M.; Erdjument-Bromage, H.; Tempst, P.; Kornberg, R.D. The MED proteins of yeast and their function through the RNA polymerase II carboxy-terminal domain. Genes Dev. 1998, 12, 45-54.
97. Ahn, S.H.; Kim, M.; Buratowski, S. Phosphorylation of serine 2 within the RNA polymerase II c-terminal domain couples transcription and 3' end processing. Mol. Cell 2004, 13, 67-76.
98. Kobor, M.S.; Greenblatt, J. Regulation of transcription elongation by phosphorylation. Biochim. Biophys. Acta 2002, 1577, 261-275.
99. Yadani, F.Z.; Kohl, A.; Prehaud, C.; Billecocq, A.; Bouloy, M. The carboxy-terminal acidic domain of Rift Valley fever virus NSs protein is essential for the formation of filamentous structures but not for the nuclear localization of the protein. J. Virol. 1999, 73, 5018-5025.
100. Le May, N.; Mansuroglu, Z.; Leger, P.; Josse, T.; Blot, G.; Billecocq, A.; Flick, R.; Jacob, Y.; Bonnefoy, E.; Bouloy, M. A SAP30 complex inhibits IFN-beta expression in Rift Valley fever virus infected cells. PLoS Pathog. 2008, 4, e13.
101. Billecocq, A.; Spiegel, M.; Vialat, P.; Kohl, A.; Weber, F.; Bouloy, M.; Haller, O. NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J. Virol. 2004, 78, 9798-9806.
102. Jaaskelainen, K.M.; Kaukinen, P.; Minskaya, E.S.; Plyusnina, A.; Vapalahti, O.; Elliott, R.M.; Weber, F.; Vaheri, A.; Plyusnin, A. Tula and puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-beta promoter. J. Med. Virol. 2007, 79, 1527-1536.
103. Perrone, L.A.; Narayanan, K.; Worthy, M.; Peters, C.J. The S segment of punta toro virus (Bunyaviridae, phlebovirus) is a major determinant of lethality in the syrian hamster and codes for a type I interferon antagonist. J. Virol. 2007, 81, 884-892.
104. Black, T.L.; Safer, B.; Hovanessian, A.; Katze, M.G. The cellular 68,000-mr protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: Implications for translational regulation. J. Virol. 1989, 63, 2244-2251.
105. Nallagatla, S.R.; Hwang, J.; Toroney, R.; Zheng, X.; Cameron, C.E.; Bevilacqua, P.C. 5'-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 2007, 318, 1455-1458.
106. van Knippenberg, I.; Carlton-Smith, C.; Elliott, R.M. The N-terminus of bunyamwera orthobunyavirus NSs protein is essential for interferon antagonism. J. Gen. Virol. 2010, 91, 2002-2006.
107. Peters, C.J.; Dalrymple, J.M. Alphaviruses. In Virology, 2nd ed.; Fields, B.N., Knipe, D.M., Chanok, R.M., Eds.; Raven Press: New York, NY, USA, 1990.
108. Strauss, J.H.; Strauss, E.G. The alphaviruses: Gene expression, replication, and evolution. Microbiol. Rev. 1994, 58, 491-562.
109. Zacks, M.A.; Paessler, S. Encephalitic alphaviruses. Vet. Microbiol. 2010, 140, 281-286.
110. Kuhn, R.J. Togaviridae: The viruses and their replication. In Fields Virology, 5th ed.; Knipe, D.M., Howley, P.M., Griffin, D.E., Lamb, R.A., Martin, M.A., Roizman, B., Straus, S.E., Eds.; Lippincott-Raven Publishers: Philadelphia, PA, USA, 2007; pp. 1001-1022.
111. Simmons, J.D.; White, L.J.; Morrison, T.E.; Montgomery, S.A.; Whitmore, A.C.; Johnston, R.E.; Heise, M.T. Venezuelan equine encephalitis virus disrupts STAT1 signaling by distinct mechanisms independent of host shutoff. J. Virol. 2009, 83, 10571-10581.
112. Aguilar, P.V.; Weaver, S.C.; Basler, C.F. Capsid protein of Eastern equine encephalitis virus inhibits host cell gene expression. J. Virol. 2007, 81, 3866-3876.
113. Fros, J.J.; Liu, W.J.; Prow, N.A.; Geertsema, C.; Ligtenberg, M.; Vanlandingham, D.L.; Schnettler, E.; Vlak, J.M.; Suhrbier, A.; Khromykh, A.A.; Pijlman, G.P. Chikungunya virus nonstructural protein 2 inhibits type I/II interferon-stimulated JAK-STAT signaling. J. Virol. 2010, 84, 10877-10887.
114. Gardner, J.; Anraku, I.; Le, T.T.; Larcher, T.; Major, L.; Roques, P.; Schroder, W.A.; Higgs, S.; Suhrbier, A. Chikungunya virus arthritis in adult wild-type mice. J. Virol. 2010, 84, 8021-8032.
115. White, L.K.; Sali, T.; Alvarado, D.; Gatti, E.; Pierre, P.; Streblow, D.; Defilippis, V.R. Chikungunya virus induces IPS-1-dependent innate immune activation and protein kinase R-independent translational shutoff. J. Virol. 2011, 85, 606-620.
116. Dryga, S.A.; Dryga, O.A.; Schlesinger, S. Identification of mutations in a sindbis virus variant able to establish persistent infection in BHK cells: The importance of a mutation in the nsP2 gene. Virology 1997, 228, 74-83.
117. Frolova, E.I.; Fayzulin, R.Z.; Cook, S.H.; Griffin, D.E.; Rice, C.M.; Frolov, I. Roles of nonstructural protein nsP2 and alpha/beta interferons in determining the outcome of sindbis virus infection. J. Virol. 2002, 76, 11254-11264.
118. Burke, C.W.; Gardner, C.L.; Steffan, J.J.; Ryman, K.D.; Klimstra, W.B. Characteristics of alpha/beta interferon induction after infection of murine fibroblasts with wild-type and mutant alphaviruses. Virology 2009, 395, 121-132.
119. Griffin, D.E. Alphaviruses. In Field Virology; Knipe, D.M., Howley, P.M., Eds.; Lippincott, Williams & Wilkins: Philadelphia, PA, USA, 2001; pp. 917-962.
120. Breakwell, L.; Dosenovic, P.; Karlsson Hedestam, G.B.; D'Amato, M.; Liljestrom, P.; Fazakerley, J.; McInerney, G.M. Semliki Forest virus nonstructural protein 2 is involved in suppression of the type I interferon response. J. Virol. 2007, 81, 8677-8684.
121. Merits, A.; Vasiljeva, L.; Ahola, T.; Kaariainen, L.; Auvinen, P. Proteolytic processing of Semliki Forest virus-specific non-structural polyprotein by nsP2 protease. J. Gen. Virol. 2001, 82, 765-773.
122. Vasiljeva, L.; Merits, A.; Golubtsov, A.; Sizemskaja, V.; Kaariainen, L.; Ahola, T. Regulation of the sequential processing of Semliki Forest virus replicase polyprotein. J. Biol. Chem. 2003, 278, 41636-41645.
123. Amineva, S.P.; Aminev, A.G.; Palmenberg, A.C.; Gern, J.E. Rhinovirus 3C protease precursors 3CD and 3CD' localize to the nuclei of infected cells. J. Gen. Virol. 2004, 85, 2969-2979.
124. Cruz, C.C.; Suthar, M.S.; Montgomery, S.A.; Shabman, R.; Simmons, J.; Johnston, R.E.; Morrison, T.E.; Heise, M.T. Modulation of type I IFN induction by a virulence determinant within the alphavirus nsP1 protein. Virology 2010, 399, 1-10.
125. Chambers, T.J.; Hahn, C.S.; Galler, R.; Rice, C.M. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 1990, 44, 649-688.
126. Kapoor, M.; Zhang, L.; Ramachandra, M.; Kusukawa, J.; Ebner, K.E.; Padmanabhan, R. Association between NS3 and NS5 proteins of dengue virus type 2 in the putative RNA replicase is linked to differential phosphorylation of NS5. J. Biol. Chem. 1995, 270, 19100-19106.
127. Li, H.; Clum, S.; You, S.; Ebner, K.E.; Padmanabhan, R. The serine protease and RNA-stimulated nucleoside triphosphatase and RNA helicase functional domains of dengue virus type 2 NS3 converge within a region of 20 amino acids. J. Virol. 1999, 73, 3108-3116.
128. Mackenzie, J.M.; Jones, M.K.; Westaway, E.G. Markers for trans-golgi membranes and the intermediate compartment localize to induced membranes with distinct replication functions in flavivirus-infected cells. J. Virol. 1999, 73, 9555-9567.
129. Heinz, F.X.; Collett, M.S.; Purcell, R.H.; Gould, E.A.; Howard, C.R.; Houghton, M.; Moormann, R.J.M.; Rice, C.M.; Thiel, H.J. Family flaviviridae. In Virus Taxonomy: 7th Report of the Internation Committee for the Taxonomy of Viruses; van Regenmortel, M.H., Fauquet, C.M., Bishop, D.H.L., Carstens, E., Estes, M.K., Lemon, S., Maniloff, J., Mayo, M.A., McGeoch, D., Pringle, C.R., Wickner, R.B., Eds.; Academic Press: San Diego, CA, USA, 2000.
130. Billoir, F.; de Chesse, R.; Tolou, H.; de Micco, P.; Gould, E.A.; de Lamballerie, X. Phylogeny of the genus flavivirus using complete coding sequences of arthropod-borne viruses and viruses with no known vector. J. Gen. Virol. 2000, 81, 781-790.
131. Werme, K.; Wigerius, M.; Johansson, M. Tick-borne encephalitis virus NS5 associates with membrane protein Scribble and impairs interferon-stimulated JAK-STAT signalling. Cell Microbiol. 2008, 10, 696-712.
132. Best, S.M.; Morris, K.L.; Shannon, J.G.; Robertson, S.J.; Mitzel, D.N.; Park, G.S.; Boer, E.; Wolfinbarger, J.B.; Bloom, M.E. Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J. Virol. 2005, 79, 12828-12839.
133. Ashour, J.; Laurent-Rolle, M.; Shi, P.Y.; Garcia-Sastre, A. NS5 of dengue virus mediates STAT2 binding and degradation. J. Virol. 2009, 83, 5408-5418.
134. Mazzon, M.; Jones, M.; Davidson, A.; Chain, B.; Jacobs, M. Dengue virus NS5 inhibits interferon-alpha signaling by blocking signal transducer and activator of transcription 2 phosphorylation. J. Infect. Dis. 2009, 200, 1261-1270.
135. Munoz-Jordan, J.L.; Sanchez-Burgos, G.G.; Laurent-Rolle, M.; Garcia-Sastre, A. Inhibition of interferon signaling by dengue virus. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 14333-14338.
136. Liu, W.J.; Chen, H.B.; Wang, X.J.; Huang, H.; Khromykh, A.A. Analysis of adaptive mutations in kunjin virus replicon RNA reveals a novel role for the flavivirus nonstructural protein NS2A in inhibition of beta interferon promoter-driven transcription. J. Virol. 2004, 78, 12225-12235.
137. Charrel, R.N.; Attoui, H.; Butenko, A.M.; Clegg, J.C.; Deubel, V.; Frolova, T.V.; Gould, E.A.; Gritsun, T.S.; Heinz, F.X.; Labuda, M.; Lashkevich, V.A.; Loktev, V.; Lundkvist, A.; Lvov, D.V.; Mandl, C.W.; Niedrig, M.; Papa, A.; Petrov, V.S.; Plyusnin, A.; Randolph, S.; Suss, J.; Zlobin, V.I.; de Lamballerie, X. Tick-borne virus diseases of human interest in Europe. Clin. Microbiol. Infect. 2004, 10, 1040-1055.
138. Pugliese, A.; Beltramo, T.; Torre, D. Emerging and re-emerging viral infections in Europe. Cell Biochem. Funct. 2007, 25, 11-13.
139. Cinco, M.; Barbone, F.; Grazia Ciufolini, M.; Mascioli, M.; Anguero Rosenfeld, M.; Stefanel, P.; Luzzati, R. Seroprevalence of tick-borne infections in forestry rangers from Northeastern Italy. Clin. Microbiol. Infect. 2004, 10, 1056-1061.
140. Haglund, M.; Vene, S.; Forsgren, M.; Gunther, G.; Johansson, B.; Niedrig, M.; Plyusnin, A.; Lindquist, L.; Lundkvist, A. Characterisation of human tick-borne encephalitis virus from Sweden. J. Med. Virol. 2003, 71, 610-621.
141. Diaz, M.O.; Ziemin, S.; Le Beau, M.M.; Pitha, P.; Smith, S.D.; Chilcote, R.R.; Rowley, J.D. Homozygous deletion of the alpha- and beta 1-interferon genes in human leukemia and derived cell lines. Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 5259-5263.
142. Bilder, D.; Birnbaum, D.; Borg, J.P.; Bryant, P.; Huigbretse, J.; Jansen, E.; Kennedy, M.B.; Labouesse, M.; Legouis, R.; Mechler, B.; Perrimon, N.; Petit, M.; Sinha, P. Collective nomenclature for lap proteins. Nat. Cell Biol. 2000, 2, E114.
143. Navarro, C.; Nola, S.; Audebert, S.; Santoni, M.J.; Arsanto, J.P.; Ginestier, C.; Marchetto, S.; Jacquemier, J.; Isnardon, D.; Le Bivic, A.; Birnbaum, D.; Borg, J.P. Junctional recruitment of mammalian Scribble relies on E-Cadherin engagement. Oncogene 2005, 24, 4330-4339.
144. Luplertlop, N.; Misse, D.; Bray, D.; Deleuze, V.; Gonzalez, J.P.; Leardkamolkarn, V.; Yssel, H.; Veas, F. Dengue-virus-infected dendritic cells trigger vascular leakage through metalloproteinase overproduction. EMBO Rep. 2006, 7, 1176-1181.
145. Lin, R.J.; Chang, B.L.; Yu, H.P.; Liao, C.L.; Lin, Y.L. Blocking of interferon-induced JAK-STAT signaling by Japanese encephalitis virus NS5 through a protein tyrosine phosphatase-mediated mechanism. J. Virol. 2006, 80, 5908-5918.
146. Liu, W.J.; Chen, H.B.; Khromykh, A.A. Molecular and functional analyses of Kunjin virus infectious cDNA clones demonstrate the essential roles for NS2A in virus assembly and for a nonconservative residue in NS3 in RNA replication. J. Virol. 2003, 77, 7804-7813.
147. Hall, R.A.; Nisbet, D.J.; Pham, K.B.; Pyke, A.T.; Smith, G.A.; Khromykh, A.A. DNA vaccine coding for the full-length infectious Kunjin virus RNA protects mice against the New York strain of West Nile virus. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 10460-10464.
148. Liu, W.J.; Wang, X.J.; Clark, D.C.; Lobigs, M.; Hall, R.A.; Khromykh, A.A. A single amino acid substitution in the West Nile virus nonstructural protein NS2A disables its ability to inhibit alpha/beta interferon induction and attenuates virus virulence in mice. J. Virol. 2006, 80, 2396-2404.