RNA virus capsid proteins: More than just a shell

Future Virology

Volumn 8, Issue 5, 2013, Pages 435-450

  Willows, Steven ^a   Hou, Shangmei ^a   Hobman, Tom C ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

apoptosis; capsid proteins; innate immunity; pathogenesis; replication; virus host

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CAPSID PROTEIN; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; DAXX PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; PROTEIN 14 3 3; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; TRANSFER RNA; VIRUS RNA;

APOPTOSIS; BLUETONGUE ORBIVIRUS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; COXSACKIE VIRUS; DENGUE VIRUS; DIMERIZATION; EASTERN EQUINE ENCEPHALOMYELITIS VIRUS; ENZYME ACTIVITY; FLAVIVIRUS; GENE CONTROL; GENE EXPRESSION; GENETIC VARIABILITY; HANTAVIRUS; HEPATITIS C VIRUS; HUMAN; INNATE IMMUNITY; JAPANESE ENCEPHALITIS VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; RNA STRUCTURE; RNA VIRUS; RUBELLA VIRUS; SARS CORONAVIRUS; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRAL CLEARANCE; VIRION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENOME; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

MIRIDAE; RNA VIRUSES;

EID: 84876889904     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.13.32     Document Type: Review

References (160)

1. Vozzolo L, Loh B, Gane PJ et al. Gyrase B inhibitor impairs HIV-1 replication by targeting Hsp90 and the capsid protein. J. Biol. Chem. 285(50), 39314-39328 (2010).
2. Price AJ, Fletcher AJ, Schaller T et al. CPSF6 defines a conserved capsid interface that modulates HIV-1 replication. PLoS Pathog. 8(8), e1002896 (2012).
3. Blair WS, Pickford C, Irving SL et al. HIV capsid is a tractable target for small molecule therapeutic intervention. PLoS Pathog. 6(12), e1001220 (2010).
4. Scheele CM, Pfefferkorn ER. Kinetics of incorporation of structural proteins into Sindbis virions. J. Virol. 3(4), 369-375 (1969).
5. Ruigrok RW, Crepin T, Kolakofsky D. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr. Opin. Microbiol. 14(4), 504-510 (2011).
6. Netherton C, Moffat K, Brooks E, Wileman T. A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv. Virus Res. 70, 101-182 (2007).
7. Thomas JA, Gorelick RJ. Nucleocapsid protein function in early infection processes. Virus Res. 134(1-2), 39-63 (2008).
8. Barat C, Lullien V, Schatz O et al. HIV-1 reverse transcriptase specifically interacts with the anticodon domain of its cognate primer tRNA. EMBO 8(11), 3279-3285 (1989).
9. Darlix JL, Vincent A, Gabus C, De Rocquigny H, Roques B. Trans-activation of the 5́ to 3́ viral DNA strand transfer by nucleocapsid protein during reverse transcription of HIV1 RNA. C. R. Acad. Sci. III 316(8), 763-771 (1993).
10. Ji X, Klarmann GJ, Preston BD. Effect of human immunodeficiency virus type 1 (HIV 1) nucleocapsid protein on HIV-1 reverse transcriptase activity in vitro. Biochemistry 35(1), 132-143 (1996)
11. Peliska JA, Balasubramanian S, Giedroc DP, Benkovic SJ. Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity. Biochemistry 33(46), 13817-13823 (1994).
12. Cristofari G, Ivanyi-Nagy R, Gabus C et al. The hepatitis C virus core protein is a potent nucleic acid chaperone that directs dimerization of the viral (+) strand RNA in vitro. Nucleic Acids Res. 32(8), 2623-2631 (2004).
13. Sharma KK, De Rocquigny H, Darlix JL et al. Analysis of the RNA chaperoning activity of the hepatitis C virus core protein on the conserved 3'X region of the viral genome. Nucleic Acids Res. 40(6), 2540-2553 (2012).
14. Ivanyi-Nagy R, Lavergne JP, Gabus C, Ficheux D, Darlix JL. RNA chaperoning and intrinsic disorder in the core proteins of Flaviviridae. Nucleic Acids Res. 36(3), 712-725 (2008).
15. Mir MA, Panganiban AT. The bunyavirus nucleocapsid protein is an RNA chaperone: possible roles in viral RNA panhandle formation and genome replication. RNA 12(2), 272-282 (2006).
16. Mir MA, Panganiban AT. Characterization of the RNA chaperone activity of hantavirus nucleocapsid protein. J. Virol. 80(13), 6276-6285 (2006).
17. Ivanov I, Yabukarski F, Ruigrok RW, Jamin M. Structural insights into the rhabdovirus transcription/replication complex. Virus Res. 162(1-2), 126-137 (2011).
18. Patton JT, Davis NL, Wertz GW. N protein alone satisfies the requirement for protein synthesis during RNA replication of vesicular stomatitis virus. J. Virol. 49(2), 303-309 (1984).
19. Chen MH, Icenogle JP. Rubella virus capsid protein modulates viral genome replication and virus infectivity. J. Virol. 78(8), 4314-4322 (2004).
20. Patton JT, Vasquez-Del Carpio R, Tortorici MA, Taraporewala ZF. Coupling of rotavirus genome replication and capsid assembly. Adv. Virus Res. 69, 167-201 (2007).
21. Patton JT, Jones MT, Kalbach AN, He YW, Xiaobo J. Rotavirus RNA polymerase requires the core shell protein to synthesize the double-stranded RNA genome. J. Virol. 71(12), 9618-9626 (1997).
22. Trask SD, Mcdonald SM, Patton JT. Structural insights into the coupling of virion assembly and rotavirus replication. Nat. Rev. Microbiol. 10(3), 165-177 (2012).
23. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73(6), 1067-1078 (1993).
24. Cen S, Khorchid A, Javanbakht H et al. Incorporation of lysyl-tRNA synthetase into human immunodeficiency virus type 1. J. Virol. 75(11), 5043-5048 (2001).
25. Schaller T, Ocwieja KE, Rasaiyaah J et al. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog. 7(12), e1002439 (2011).
26. Franke EK, Yuan HE, Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372(6504), 359-362 (1994).
27. Thali M, Bukovsky A, Kondo E et al. Functional association of cyclophilin A with HIV-1 virions. Nature 372(6504), 363-365 (1994).
28. Mascarenhas AP, Musier-Forsyth K. The capsid protein of human immunodeficiency virus: interactions of HIV 1 capsid with host protein factors. FEBS J. 276(21), 6118-6127 (2009).
29. Wang X, Bai J, Zhang L, Wang X, Li Y, Jiang P. Poly(A)-binding protein interacts with the nucleocapsid protein of porcine reproductive and respiratory syndrome virus and participates in viral replication. Antiviral Res. 96(3), 315-323 (2012).
30. Collier B, Gray NK. Cleavage, a real turn-off? HIV-mediated proteolysis of PABP1. Biochem. J. 396(2), e9-e11 (2006).
31. Alvarez E, Castello A, Menendez-Arias L, Carrasco L. HIV protease cleaves poly(A)- binding protein. Biochem. J. 396(2), 219-226 (2006).
32. Bonderoff JM, Larey JL, Lloyd RE. Cleavage of poly(A)-binding protein by poliovirus 3C proteinase inhibits viral internal ribosome entry site-mediated translation. J. Virol. 82(19), 9389-9399 (2008).
33. Zhang B, Morace G, Gauss-Muller V, Kusov Y. Poly(A) binding protein, C-terminally truncated by the hepatitis A virus proteinase 3C, inhibits viral translation. Nucleic Acids Res. 35(17), 5975-5984 (2007).
34. Ilkow CS, Mancinelli V, Beatch MD, Hobman TC. Rubella virus capsid protein interacts with poly(a)-binding protein and inhibits translation. J. Virol. 82(9), 4284-4294 (2008).
35. Sharma A, Boris-Lawrie K. Determination of host RNA helicases activity in viral replication. Methods Enzymol. 511, 405-435 (2012).
36. Xu Z, Hobman TC. The helicase activity of DDX56 is required for its role in assembly of infectious West Nile virus particles. Virology 433(1), 226-235 (2012).
37. Xu Z, Anderson R, Hobman TC. The capsid-binding nucleolar helicase DDX56 is important for infectivity of West Nile virus. J. Virol. 85(11), 5571-5580 (2011).
38. Clarke P, Tyler KL. Apoptosis in animal models of virus-induced disease. Nat. Rev. Microbiol. 7(2), 144-155 (2009).
39. Mahmood Z, Shukla Y. Death receptors: targets for cancer therapy. Exp. Cell Res. 316(6), 887-899 (2010).
40. Estaquier J, Vallette F, Vayssiere JL, Mignotte B. The mitochondrial pathways of apoptosis. Adv. Exp. Med. Biol. 942, 157-183 (2012).
41. Roulston A, Marcellus RC, Branton PE. Viruses and apoptosis. Annu. Rev. Microbiol. 53, 577-628 (1999).
42. Hardestam J, Klingstrom J, Mattsson K, Lundkvist A. HFRS causing hantaviruses do not induce apoptosis in confluent Vero E6 and A-549 cells. J. Med. Virol. 76(2), 234-240 (2005).
43. Ontiveros SJ, Li Q, Jonsson CB. Modulation of apoptosis and immune signaling pathways by the Hantaan virus nucleocapsid protein. Virology 401(2), 165-178 (2010).
44. Li XD, Makela TP, Guo D et al. Hantavirus nucleocapsid protein interacts with the Fas-mediated apoptosis enhancer Daxx. J. Gen. Virol. 83(Pt 4), 759-766 (2002).
45. Yang X, Khosravi-Far R, Chang HY, Baltimore D. Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell 89(7), 1067-1076 (1997).
46. Salomoni P, Khelifi AF. Daxx: death or survival protein? Trends Cell Biol. 16(2), 97-104 (2006).
47. Bardeletti G, Tektoff J, Gautheron D. Rubella virus maturation and production in two host cell systems. Intervirology 11(2), 97-103 (1979).
48. Ilkow CS, Goping IS, Hobman TC. The rubella virus capsid is an anti-apoptotic protein that attenuates the pore-forming ability of Bax. PLoS Pathog. 7(2), e1001291 (2011).
49. Beatch MD, Hobman TC. Rubella virus capsid associates with host cell protein p32 and localizes to mitochondria. J. Virol. 74(12), 5569-5576 (2000).
50. Beatch MD, Everitt JC, Law LJ, Hobman TC. Interactions between rubella virus capsid and host protein p32 are important for virus replication. J. Virol. 79(16), 10807-10820 (2005).
51. Itahana K, Zhang Y. Mitochondrial p32 is a critical mediator of ARF-induced apoptosis. Cancer Cell 13(6), 542-553 (2008)
52. Sunayama J, Ando Y, Itoh N et al. Physical and functional interaction between BH3-only protein Hrk and mitochondrial pore-forming protein p32. Cell Death Differ. 11(7), 771-781 (2004).
53. Szabo J, Cervenak L, Toth FD et al. Soluble gC1q-R/p33, a cell protein that binds to the globular "heads" of C1q, effectively inhibits the growth of HIV-1 strains in cell cultures. Clin. Immunol. 99(2), 222-231 (2001).
54. Polyak SJ. Hepatitis C virus-cell interactions and their role in pathogenesis. Clin. Liver Dis. 7(1), 67-88 (2003).
55. Yasui K, Wakita T, Tsukiyama-Kohara K et al. The native form and maturation process of hepatitis C virus core protein. J. Virol. 72(7), 6048-6055 (1998).
56. Lo SY, Masiarz F, Hwang SB, Lai MM, Ou JH. Differential subcellular localization of hepatitis C virus core gene products. Virology 213(2), 455-461 (1995).
57. Urbanowski MD, Ilkow CS, Hobman TC. Modulation of signaling pathways by RNA virus capsid proteins. Cell. Signal. 20(7), 1227-1236 (2008).
58. Jahan S, Ashfaq UA, Khaliq S, Samreen B, Afzal N. Dual behavior of HCV core gene in regulation of apoptosis is important in progression of HCC. Infect. Genet. Evol. 12(2), 236-239 (2012).
59. Ray RB, Steele R, Basu A et al. Distinct functional role of hepatitis C virus core protein on NF-kB regulation is linked to genomic variation. Virus Res. 87(1), 21-29 (2002).
60. Zhu N, Khoshnan A, Schneider R et al. Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. J. Virol. 72(5), 3691-3697 (1998).
61. Lu W, Lo SY, Chen M, Wu K, Fung YK, Ou JH. Activation of p53 tumor suppressor by hepatitis C virus core protein. Virology 264(1), 134-141 (1999).
62. Otsuka M, Kato N, Lan K et al. Hepatitis C virus core protein enhances p53 function through augmentation of DNA binding affinity and transcriptional ability. J. Biol. Chem. 275(44), 34122-34130 (2000).
63. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 408(6810), 307-310 (2000).
64. Ray RB, Steele R, Meyer K, Ray R. Transcriptional repression of p53 promoter by hepatitis C virus core protein. J. Biol. Chem. 272(17), 10983-10986 (1997).
65. Kao CF, Chen SY, Chen JY, Wu Lee YH. Modulation of p53 transcription regulatory activity and post-translational modification by hepatitis C virus core protein. Oncogene 23(14), 2472-2483 (2004).
66. Lee SK, Park SO, Joe CO, Kim YS. Interaction of HCV core protein with 14-3-3epsilon protein releases Bax to activate apoptosis. Biochem. Biophys. Res. Commun. 352(3), 756-762 (2007).
67. Mohd-Ismail NK, Deng L, Sukumaran SK, Yu VC, Hotta H, Tan YJ. The hepatitis C virus core protein contains a BH3 domain that regulates apoptosis through specific interaction with human Mcl-1. J. Virol. 83(19), 9993-10006 (2009).
68. Marusawa H, Hijikata M, Chiba T, Shimotohno K. Hepatitis C virus core protein inhibits Fas- and tumor necrosis factor alpha-mediated apoptosis via NF-kB activation. J. Virol. 73(6), 4713-4720 (1999).
69. Yoshida H, Kato N, Shiratori Y et al. Hepatitis C virus core protein activates nuclear factor kappa B-dependent signaling through tumor necrosis factor receptor-associated factor. J. Biol. Chem. 276(19), 16399-16405 (2001).
70. Chung YM, Park KJ, Choi SY, Hwang SB, Lee SY. Hepatitis C virus core protein potentiates TNF-a-induced NF-kB activation through TRAF2-IKKbeta- dependent pathway. Biochem. Biophys. Res. Commun. 284(1), 15-19 (2001).
71. Tai DI, Tsai SL, Chen YM et al. Activation of nuclear factor kappaB in hepatitis C virus infection: implications for pathogenesis and hepatocarcinogenesis. Hepatology 31(3), 656-664 (2000).
72. Aoki H, Hayashi J, Moriyama M, Arakawa Y, Hino O. Hepatitis C virus core protein interacts with 14-3-3 protein and activates the kinase Raf-1. J. Virol. 74(4), 1736-1741 (2000).
73. Nakamura H, Aoki H, Hino O, Moriyama M. HCV core protein promotes heparin binding EGF-like growth factor expression and activates Akt. Hepatol. Res. 41(5), 455-462 (2011).
74. Otsuka M, Kato N, Taniguchi H et al. Hepatitis C virus core protein inhibits apoptosis via enhanced Bcl-xL expression. Virology 296(1), 84-93 (2002).
75. Saito K, Meyer K, Warner R, Basu A, Ray RB, Ray R. Hepatitis C virus core protein inhibits tumor necrosis factor a-mediated apoptosis by a protective effect involving cellular FLICE inhibitory protein. J. Virol. 80(9), 4372-4379 (2006).
76. WHO. Dengue and Dengue Haemorrhagic Fever: Factsheet No 117. WHO, Geneva, Switzerland (2008).
77. Makino Y, Tadano M, Anzai T, Ma SP, Yasuda S, Fukunaga T. Detection of dengue 4 virus core protein in the nucleus. II. Antibody against dengue 4 core protein produced by a recombinant baculovirus reacts with the antigen in the nucleus. J. Gen. Virol. 70(Pt 6), 1417-1425 (1989).
78. Li J, Huang R, Liao W, Chen Z, Zhang S, Huang R. Dengue virus utilizes calcium modulating cyclophilin-binding ligand to subvert apoptosis. Biochem. Biophys. Res. Commun. 418(4), 622-627 (2012).
79. Edgar CE, Lindquist LD, McKean DL, Strasser A, Bram RJ. CAML regulates Bim-dependent thymocyte death. Cell Death Differ. 17(10), 1566-1576 (2010).
80. Feng P, Park J, Lee BS, Lee SH, Bram RJ, Jung JU. Kaposi's sarcoma-associated herpesvirus mitochondrial K7 protein targets a cellular calcium-modulating cyclophilin ligand to modulate intracellular calcium concentration and inhibit apoptosis. J. Virol. 76(22), 11491-11504 (2002).
81. Limjindaporn T, Netsawang J, Noisakran S et al. Sensitization to Fas-mediated apoptosis by dengue virus capsid protein. Biochem. Biophys. Res. Commun. 362(2), 334-339 (2007).
82. Netsawang J, Noisakran S, Puttikhunt C et al. Nuclear localization of dengue virus capsid protein is required for DAXX interaction and apoptosis. Virus Res. 147(2), 275-283 (2010).
83. Strand S, Hofmann WJ, Hug H et al. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells - a mechanism of immune evasion? Nat. Med. 2(12), 1361-1366 (1996).
84. Nagila A, Netsawang J, Srisawat C et al. Role of CD137 signaling in dengue virus-mediated apoptosis. Biochem. Biophys. Res. Commun. 410(3), 428-433 (2011).
85. Yang JS, Ramanathan MP, Muthumani K et al. Induction of inflammation by West Nile virus capsid through the caspase-9 apoptotic pathway. Emerg. Infect. Dis. 8(12), 1379-1384 (2002).
86. Yang MR, Lee SR, Oh W et al. West Nile virus capsid protein induces p53-mediated apoptosis via the sequestration of HDM2 to the nucleolus. Cell. Microbiol. 10(1), 165-176 (2008).
87. Scherbik SV, Brinton MA. Virus-induced Ca2+ influx extends survival of West Nile virus-infected cells. J. Virol. 84(17), 8721-8731 (2010).
88. Das S, Chakraborty S, Basu A. Critical role of lipid rafts in virus entry and activation of phosphoinositide 3́ kinase/Akt signaling during early stages of Japanese encephalitis virus infection in neural stem/progenitor cells. J. Neurochem. 115(2), 537-549 (2010).
89. Lee CJ, Liao CL, Lin YL. Flavivirus activates phosphatidylinositol 3-kinase signaling to block caspase-dependent apoptotic cell death at the early stage of virus infection. J. Virol. 79(13), 8388-8399 (2005).
90. Yang CM, Lin CC, Lee IT et al. Japanese encephalitis virus induces matrix metalloproteinase-9 expression via a ROS/c Src/PDGFR/PI3K/Akt/MAPKs-dependent AP-1 pathway in rat brain astrocytes. J. Neuroinflamm. 9, 12 (2012).
91. Urbanowski MD, Hobman TC. The West Nile virus capsid protein blocks apoptosis through a phosphatidylinositol 3-kinase-dependent mechanism. J. Virol. 87(2), 872-881 (2012).
92. Henke A, Launhardt H, Klement K, Stelzner A, Zell R, Munder T. Apoptosis in coxsackievirus B3-caused diseases: interaction between the capsid protein VP2 and the proapoptotic protein Siva. J. Virol. 74(9), 4284-4290 (2000).
93. Mei Y, Wu M. Multifaceted functions of Siva 1: more than an Indian god of destruction. Protein Cell 3(2), 117-122 (2012).
94. Martin U, Nestler M, Munder T, Zell R, Sigusch HH, Henke A. Characterization of coxsackievirus B3-caused apoptosis under in vitro conditions. Med. Microbiol. Immunol. 193(2-3), 133-139 (2004).
95. Henke A, Nestler M, Strunze S et al. The apoptotic capability of coxsackievirus B3 is influenced by the efficient interaction between the capsid protein VP2 and the proapoptotic host protein Siva. Virology 289(1), 15-22 (2001).
96. Emmett SR, Dove B, Mahoney L, Wurm T, Hiscox JA. The cell cycle and virus infection. Methods Mol. Biol. 296, 197-218 (2005).
97. Dove B, Brooks G, Bicknell K, Wurm T, Hiscox JA. Cell cycle perturbations induced by infection with the coronavirus infectious bronchitis virus and their effect on virus replication. J. Virol. 80(8), 4147-4156 (2006).
98. Pines J. Cyclins and cyclin-dependent kinases: a biochemical view. Biochem. J. 308(Pt 3), 697-711 (1995).
99. Viallard JF, Lacombe F, Belloc F, Pellegrin JL, Reiffers J. Molecular mechanisms controlling the cell cycle: fundamental aspects and implications for oncology. Cancer Radiother. 5(2), 109-129 (2001).
100. Ohkawa K, Ishida H, Nakanishi F et al. Hepatitis C virus core functions as a suppressor of cyclin-dependent kinase-activating kinase and impairs cell cycle progression. J. Biol. Chem. 279(12), 11719-11726 (2004).
101. Satyanarayana A, Kaldis P. Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28(33), 2925-2939 (2009).
102. Wang F, Yoshida I, Takamatsu M et al. Complex formation between hepatitis C virus core protein and p21Waf1/Cip1/Sdi1. Biochem. Biophys. Res. Commun. 273(2), 479-484 (2000).
103. Surjit M, Liu B, Chow VT, Lal SK. The nucleocapsid protein of severe acute respiratory syndrome-coronavirus inhibits the activity of cyclin-cyclin-dependent kinase complex and blocks S phase progression in mammalian cells. J. Biol. Chem. 281(16), 10669-10681 (2006).
104. Zeng Y, Ye L, Zhu S et al. The nucleocapsid protein of SARS-associated coronavirus inhibits B23 phosphorylation. Biochem. Biophys. Res. Commun. 369(2), 287-291 (2008).
105. Okuda M, Horn HF, Tarapore P et al. Nucleophosmin/B23 is a target of CDK2/ cyclin E in centrosome duplication. Cell 103(1), 127-140 (2000).
106. Zhou B, Liu J, Wang Q et al. The nucleocapsid protein of severe acute respiratory syndrome coronavirus inhibits cell cytokinesis and proliferation by interacting with translation elongation factor 1a. J. Virol. 82(14), 6962-6971 (2008).
107. Moriishi K, Mori Y, Matsuura Y. Processing and pathogenicity of HCV core protein. Uirusu 58(2), 183-190 (2008).
108. Yoshida T, Hanada T, Tokuhisa T et al. Activation of STAT3 by the hepatitis C virus core protein leads to cellular transformation. J. Exp. Med. 196(5), 641-653 (2002).
109. Ihle JN, Kerr IM. Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet. 11(2), 69-74 (1995).
110. Moriishi K, Mochizuki R, Moriya K et al. Critical role of PA28gamma in hepatitis C virus-associated steatogenesis and hepatocarcinogenesis. Proc. Natl Acad. Sci. USA 104(5), 1661-1666 (2007).
111. Yoshikawa T, Shimano H, Amemiya-Kudo M et al. Identification of liver X receptor-retinoid X receptor as an activator of the sterol regulatory element-binding protein 1c gene promoter. Mol. Cell. Biol. 21(9), 2991-3000 (2001).
112. Versteeg GA, Garcia-Sastre A. Viral tricks to grid-lock the type I interferon system. Curr. Opin. Mol. Biol. 13(4), 508-516 (2010).
113. Hosui A, Ohkawa K, Ishida H et al. Hepatitis C virus core protein differently regulates the JAK-STAT signaling pathway under interleukin-6 and interferon-gamma stimuli. J. Biol. Chem. 278(31), 28562-28571 (2003).
114. Lin W, Kim SS, Yeung E et al. Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J. Virol. 80(18), 9226-9235 (2006).
115. Ciccaglione AR, Stellacci E, Marcantonio C et al. Repression of interferon regulatory factor 1 by hepatitis C virus core protein results in inhibition of antiviral and immunomodulatory genes. J. Virol. 81(1), 202-214 (2007).
116. De Lucas S, Bartolome J, Carreno V. Hepatitis C virus core protein down-regulates transcription of interferon-induced antiviral genes. J. Infect. Dis. 191(1), 93-99 (2005).
117. Basu A, Meyer K, Ray RB, Ray R. Hepatitis C virus core protein modulates the interferon-induced transacting factors of Jak/Stat signaling pathway but does not affect the activation of downstream IRF-1 or 561 gene. Virology 288(2), 379-390 (2001).
118. Takayama I, Sato H, Watanabe A et al. The nucleocapsid protein of measles virus blocks host interferon response. Virology 424(1), 45-55 (2012).
119. Sagong M, Lee C. Porcine reproductive and respiratory syndrome virus nucleocapsid protein modulates interferon-beta production by inhibiting IRF3 activation in immortalized porcine alveolar macrophages. Arch. Virol. 156(12), 2187-2195 (2011).
120. Luo R, Fang L, Jiang Y et al. Activation of NF-kappaB by nucleocapsid protein of the porcine reproductive and respiratory syndrome virus. Virus Genes 42(1), 76-81 (2011).
121. Fu Y, Quan R, Zhang H, Hou J, Tang J, Feng WH. Porcine reproductive and respiratory syndrome virus induces interleukin-15 through the NF-kappaB signaling pathway. J. Virol. 86(14), 7625-7636 (2012).
122. Kopecky-Bromberg SA, Martinez-Sobrido L, Frieman M, Baric RA, Palese P. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J. Virol. 81(2), 548-557 (2007).
123. Lu X, Pan J, Tao J, Guo D. SARS-CoV nucleocapsid protein antagonizes IFN-beta response by targeting initial step of IFN-beta induction pathway, and its C-terminal region is critical for the antagonism. Virus Genes 42(1), 37-45 (2011).
124. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, Makino S. Dual functions of Rift Valley fever virus NSs protein: inhibition of host mRNA transcription and post-transcriptional downregulation of protein kinase PKR. Ann. N. Y. Acad. Sci. 1171(Suppl. 1), E75-E85 (2009).
125. Garmashova N, Atasheva S, Kang W, Weaver SC, Frolova E, Frolov I. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J. Virol. 81(24), 13552-13565 (2007).
126. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, Makino S. Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog. 5(2), e1000287 (2009).
127. Gustin KE. Inhibition of nucleo-cytoplasmic trafficking by RNA viruses: targeting the nuclear pore complex. Virus Res. 95(1-2), 35-44 (2003).
128. Verbruggen P, Ruf M, Blakqori G et al. Interferon antagonist NSs of La Crosse virus triggers a DNA damage response-like degradation of transcribing RNA polymerase II. J. Biol. Chem. 286(5), 3681-3692 (2011).
129. Easley R, Van Duyne R, Coley W et al. Chromatin dynamics associated with HIV-1 Tat-activated transcription. Biochim. Biophys. Acta 1799(3-4), 275-285 (2010).
130. 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. 81(5), 2472-2484 (2007).
131. Ruiz A. Epidemic of Venezuelan equine encephalitis. Rev. Panam. Salud Publica 1(1), 78-83 (1997).
132. Atasheva S, Fish A, Fornerod M, Frolova EI. Venezuelan equine encephalitis virus capsid protein forms a tetrameric complex with CRM1 and importin a/b that obstructs nuclear pore complex function. J. Virol. 84(9), 4158-4171 (2010).
133. Kato J, Kato N, Shiratori Y, Omata M. HCV proteins suppress translation. Nihon Rinsho 59(7), 1254-1258 (2001).
134. Lokugamage KG, Narayanan K, Huang C, Makino S. Severe acute respiratory syndrome coronavirus protein nsp1 is a novel eukaryotic translation inhibitor that represses multiple steps of translation initiation. J. Virol. 86(24), 13598-13608 (2012).
135. Gainey MD, Dillon PJ, Clark KM, Manuse MJ, Parks GD. Paramyxovirus- induced shutoff of host and viral protein synthesis: role of the P and V proteins in limiting PKR activation. J. Virol. 82(2), 828-839 (2008).
136. Kou YH, Chou SM, Wang YM et al. Hepatitis C virus NS4A inhibits cap-dependent and the viral IRES-mediated translation through interacting with eukaryotic elongation factor 1A. J. Biochem. Sci. 13(6), 861-874 (2006).
137. Kuyumcu-Martinez NM, Van Eden ME, Younan P, Lloyd RE. Cleavage of poly(A)- binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol. Cell. Biol. 24(4), 1779-1790 (2004).
138. Favre D, Studer E, Michel MR. Semliki Forest virus capsid protein inhibits the initiation of translation by upregulating the double-stranded RNA-activated protein kinase (PKR). Biosci. Rep. 16(6), 485-511 (1996).
139. Mortola E, Noad R, Roy P. Bluetongue virus outer capsid proteins are sufficient to trigger apoptosis in mammalian cells. J. Virol. 78(6), 2875-2883 (2004).
140. Wang T, Yu B, Lin L et al. A functional nuclear localization sequence in the VP1 capsid protein of coxsackievirus B3. Virology 433(2), 513-521 (2012).
141. Bhuvanakantham R, Li J, Tan TT, Ng ML. Human Sec3 protein is a novel transcriptional and translational repressor of flavivirus. Cell. Microbiol. 12(4), 453-472 (2010).
142. Colpitts TM, Barthel S, Wang P, Fikrig E. Dengue virus capsid protein binds core histones and inhibits nucleosome formation in human liver cells. PLoS ONE 6(9), e24365 (2011).
143. Aguilar PV, Weaver SC, Basler CF. Capsid protein of eastern equine encephalitis virus inhibits host cell gene expression. J. Virol. 81(8), 3866-3876 (2007).
144. Owsianka AM, Patel AH. Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology 257(2), 330-340 (1999).
145. Oshiumi H, Ikeda M, Matsumoto M et al. Hepatitis C virus core protein abrogates the DDX3 function that enhances IPS-1- mediated IFN-beta induction. PLoS ONE 5(12), e14258 (2010).
146. Ait-Goughoulte M, Banerjee A, Meyer K et al. Hepatitis C virus core protein interacts with fibrinogen-beta and attenuates cytokine stimulated acute-phase response. Hepatology 51(5), 1505-1513 (2010).
147. Waggoner SN, Hall CH, Hahn YS. HCV core protein interaction with gC1q receptor inhibits Th1 differentiation of CD4+ T cells via suppression of dendritic cell IL-12 production. J. Leuk. Biol. 82(6), 1407-1419 (2007).
148. Kang SM, Kim SJ, Kim JH et al. Interaction of hepatitis C virus core protein with Hsp60 triggers the production of reactive oxygen species and enhances TNF-a-mediated apoptosis. Cancer Lett. 279(2), 230-237 (2009).
149. Alisi A, Giambartolomei S, Cupelli F et al. Physical and functional interaction between HCV core protein and the different p73 isoforms. Oncogene 22(17), 2573-2580 (2003).
150. Cheng PL, Chang MH, Chao CH, Lee YH. Hepatitis C viral proteins interact with Smad3 and differentially regulate TGF-beta/Smad3-mediated transcriptional activation. Oncogene 23(47), 7821-7838 (2004).
151. Chen H, Wurm T, Britton P, Brooks G, Hiscox JA. Interaction of the coronavirus nucleoprotein with nucleolar antigens and the host cell. J. Virol. 76(10), 5233-5250 (2002).
152. Mori Y, Okabayashi T, Yamashita T et al. Nuclear localization of Japanese encephalitis virus core protein enhances viral replication. J. Virol. 79(6), 3448-3458 (2005).
153. Kolokithas A, Rosenke K, Malik F et al. The glycosylated Gag protein of a murine leukemia virus inhibits the antiretroviral function of APOBEC3. J. Virol. 84(20), 10933-10936 (2010).
154. Wisniewski ML, Werner BG, Hom LG, Anguish LJ, Coffey CM, Parker JS. Reovirus infection or ectopic expression of outer capsid protein micro1 induces apoptosis independently of the cellular proapoptotic proteins Bax and Bak. J. Virol. 85(1), 296-304 (2011).
155. Ilkow CS, Weckbecker D, Cho WJ et al. The rubella virus capsid protein inhibits mitochondrial import. J. Virol. 84(1), 119-130 (2010).
156. Yan X, Hao Q, Mu Y et al. Nucleocapsid protein of SARS-CoV activates the expression of cyclooxygenase-2 by binding directly to regulatory elements for nuclear factor-kappa B and CCAAT/enhancer binding protein. Int. J. Biochem. Cell Biol. 38(8), 1417-1428 (2006).
157. Wei WY, Li HC, Chen CY et al. SARS-CoV nucleocapsid protein interacts with cellular pyruvate kinase protein and inhibits its activity. Arch. Virol. 157(4), 635-645 (2012).
158. Surjit M, Liu B, Jameel S, Chow VT, Lal SK. The SARS coronavirus nucleocapsid protein induces actin reorganization and apoptosis in COS-1 cells in the absence of growth factors. Biochem. J. 383(Pt 1), 13-18 (2004).
159. Atasheva S, Garmashova N, Frolov I, Frolova E. Venezuelan equine encephalitis virus capsid protein inhibits nuclear import in mammalian but not in mosquito cells. J. Virol. 82(8), 4028-4041 (2008).
160. Hunt TA, Urbanowski MD, Kakani K, Law LM, Brinton MA, Hobman TC. Interactions between the West Nile virus capsid protein and the host cell-encoded phosphatase inhibitor, I2PP2A. Cell. Microbiol. 9(11), 2756-2766 (2007).