Arenavirus nucleoproteins prevent activation of nuclear factor kappa B

Journal of Virology

Volumn 86, Issue 15, 2012, Pages 8185-8197

  Rodrigo, W W Shanaka I ^a   Ortiz Riaño, Emilio ^a   Pythoud, Christelle ^b   Kunz, Stefan ^b   de la Torre, Juan C ^c   Martínez Sobrido, Luis ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; VIRUS NUCLEOPROTEIN;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; ANIMAL CELL; ARENAVIRUS INFECTION; ARTICLE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; INFLAMMATION; INHIBITION KINETICS; INNATE IMMUNITY; INTERFERON PRODUCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RESIDUE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; VIRUS CELL INTERACTION; VIRUS IMMUNITY; VIRUS REPLICATION; VIRUS VIRULENCE;

ARENAVIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; NEW WORLD ARENAVIRUSES; TACARIBE VIRUS;

EID: 84864386762     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.07240-11     Document Type: Article

References (97)

1. Alkalay I, et al. 1995. Stimulation-dependent I kappa B alpha phosphorylation marks the NF-kappa B inhibitor for degradation via the ubiquitinproteasome pathway. Proc. Natl. Acad. Sci. U. S. A. 92:10599-10603.
2. Barton LL. 1996. Lymphocytic choriomeningitis virus: a neglected central nervous system pathogen. Clin. Infect. Dis. 22:197. doi:10.1093/clinids/22.1.197.
3. Bonnard M, et al. 2000. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kappaB-dependent gene transcription.EMBOJ. 19:4976-4985.
4. Borrow P, Martinez-Sobrido L, de la Torre JC. 2010. Inhibition of the type I interferon antiviral response during areanvirus infection. Viruses 2:2443-2480.
5. Borrow P, Oldstone MB. 1994. Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 198:1-9.
6. Bowick GC, et al. 2007. Identification of differentially activated cellsignaling networks associated with pichinde virus pathogenesis by using systems kinomics. J. Virol. 81:1923-1933.
7. Bowick GC, et al. 2009. Attenuated and lethal variants of Pichinde virus induce differential patterns of NF-kappaB activation suggesting a potential target for novel therapeutics. Viral Immunol. 22:457-462.
8. Buchmeier MJ, de la Torre JC, Peters CJ. 2007. Arenaviridae: The viruses and their replication, p 1791-1827. In Knipe PD, Howley P, Griffin D, Lamb R, Martin M, Roizman B, Straus S (ed), Fields virology, 5th ed, vol II. Lippincott Williams & Wilkins, Philadelphia, PA.
9. Cárdenas WB, et al. 2006. Ebola virus VP35 protein binds doublestranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 80:5168-5178.
10. Carnec X, et al. 2011. Lassa virus nucleoprotein mutants generated by reverse genetics induce a robust type I interferon response in human dendritic cells and macrophages. J. Virol. 85:12093-12097.
11. Delhase M, et al. 2012. TANK-binding kinase 1 (TBK1) controls cell survival through PAI-2/serpinB2 and transglutaminase 2. Proc. Natl. Acad. Sci. U. S. A. 109:E177-E186.
12. Djavani MM, et al. 2007. Early blood profiles of virus infection in a monkey model for Lassa fever. J. Virol. 81:7960-7973.
13. Eichler R, et al. 2004. Characterization of the Lassa virus matrix protein Z: electron microscopic study of virus-like particles and interaction with the nucleoprotein (NP). Virus Res. 100:249-255.
14. Elco CP, Guenther JM, Williams BR, Sen GC. 2005. Analysis of genes induced by Sendai virus infection of mutant cell lines reveals essential roles of interferon regulatory factor 3, NF-kappaB, and interferon but not tolllike receptor 3. J. Virol. 79:3920-3929.
15. Fan L, Briese T, Lipkin WI. 2010. Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J. Virol. 84: 1785-1791.
16. Fischer SA, et al. 2006. Transmission of lymphocytic choriomeningitis virus by organ transplantation. N. Engl. J. Med. 354:2235-2249.
17. Fitzgerald KA, et al. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491-496.
18. Fujita F, et al. 2003. Identification of NAP1, a regulatory subunit of IkappaB kinase-related kinases that potentiates NF-kappaB signaling. Mol. Cell. Biol. 23:7780-7793.
19. GarcíA-Sastre A. 2004. Identification and characterization of viral antagonists of type I interferon in negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:249-280.
20. GarcíA-Sastre A. 2002. Mechanisms of inhibition of the host interferon alpha/beta-mediated antiviral responses by viruses. Microbes Infect. 4:647-655.
21. GarcíA-Sastre A, Sansonetti PJ. 2010. Host-pathogen interactions. Curr. Opin. Immunol. 22:425-427.
22. Groseth A, et al. 2011. Tacaribe virus but not junin virus infection induces cytokine release from primary human monocytes and macrophages. PLoS Negl. Trop. Dis. 5:e1137. doi:10.1371/journal. pntd.0001137.
23. Hastie KM, Kimberlin CR, Zandonatti MA, MacRae IJ, Saphire EO. 2011. Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3= to 5= exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. U. S. A. 108:2396-2401.
24. Hayden MS, Ghosh S. 2008. Shared principles in NF-kappaB signaling. Cell 132:344-362.
25. Heller MV, Saavedra MC, Falcoff R, Maiztegui JI, Molinas FC. 1992. Increased tumor necrosis factor-alpha levels in Argentine hemorrhagic fever. J. Infect. Dis. 166:1203-1204.
26. Hemmi H, et al. 2004. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199:1641-1650.
27. Herbein G, O'Brien WA. 2000. Tumor necrosis factor (TNF)-alpha and TNF receptors in viral pathogenesis. Proc. Soc. Exp. Biol. Med. 223:241-257.
28. Hiscott J. 2007. Convergence of the NF-kappaB and IRF pathways in the regulation of the innate antiviral response. Cytokine Growth Factor Rev. 18:483-490.
29. Hiscott J, et al. 2003. Convergence of the NF-kappaB and interferon signaling pathways in the regulation of antiviral defense and apoptosis. Ann. N. Y. Acad. Sci. 1010:237-248.
30. Hiscott J, Lin R, Nakhaei P, Paz S. 2006. MasterCARD: a priceless link to innate immunity. Trends Mol. Med. 12:53-56.
31. Hiscott J, Nguyen TL, Arguello M, Nakhaei P, Paz S. 2006. Manipulation of the nuclear factor-kappaB pathway and the innate immune response by viruses. Oncogene 25:6844-6867.
32. Honda K, Takaoka A, Taniguchi T. 2006. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25:349-360.
33. Israel, A. 2010. The IKK complex, a central regulator of NF-kappaB activation. Cold Spring Harb. Perspect. Biol. 2:a000158. doi:10.1101/cshperspect.a000158.
34. Jahrling PB, et al. 1980. Lassa virus infection of rhesus monkeys: pathogenesis and treatment with ribavirin. J. Infect. Dis. 141:580-589.
35. Jahrling PB, Peters CJ. 1992. Lymphocytic choriomeningitis virus. A neglected pathogen of man. Arch. Pathol. Lab. Med. 116:486-488.
36. Kawai T, et al. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988.
37. Kilgore PE, et al. 1997. Treatment of Bolivian hemorrhagic fever with intravenous ribavirin. Clin. Infect. Dis. 24:718-722.
38. Kishore N, et al. 2002. IKK-i and TBK-1 are enzymatically distinct from the homologous enzyme IKK-2: comparative analysis of recombinant human IKK-i, TBK-1, and IKK-2. J. Biol. Chem. 277:13840-13847.
39. Kochs G, Garcia-Sastre A, Martinez-Sobrido L. 2007. Multiple antiinterferon actions of the influenza A virus NS1 protein. J. Virol. 81:7011-7021.
40. Koop A, et al. 2011. Novel splice variants of human IKKepsilon negatively regulate IKKepsilon-induced IRF3 and NF-kB activation. Eur. J. Immunol. 41:224-234.
41. Koshiba T, Bashiruddin N, Kawabata S. 2011. Mitochondria and antiviral innate immunity. Int. J. Biochem. Mol. Biol. 2:257-262.
42. Kuai J, et al. 2004. NAK is recruited to the TNFR1 complex in a TNFalpha-dependent manner and mediates the production of RANTES: identification of endogenous TNFR-interacting proteins by a proteomic approach. J. Biol. Chem. 279:53266-53271.
43. Lan S, McLay L, Aronson J, Ly H, Liang Y. 2008. Genome comparison of virulent and avirulent strains of the Pichinde arenavirus. Arch. Virol. 153:1241-1250.
44. Levis SC, et al. 1985. Correlation between endogenous interferon and the clinical evolution of patients with Argentine hemorrhagic fever. J. Interferon Res. 5:383-389.
45. Lin R, et al. 2006. Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKepsilon molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J. Virol. 80:6072-6083.
46. Lomvardas S, Thanos D. 2002. Modifying gene expression programs by altering core promoter chromatin architecture. Cell 110:261-271.
47. Lukashevich IS, et al. 1999. Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-alpha gene expression. J. Med. Virol. 59:552-560.
48. Lukashevich IS, et al. 2004. LCMV-mediated hepatitis in rhesus macaques: WE but not ARM strain activates hepatocytes and induces liver regeneration. Arch. Virol. 149:2319-2336.
49. Lukashevich IS, et al. 2003. Arenavirus-mediated liver pathology: acute lymphocytic choriomeningitis virus infection of rhesus macaques is characterized by high-level interleukin-6 expression and hepatocyte proliferation. J. Virol. 77:1727-1737.
50. Marta RF, et al. 1999. Proinflammatory cytokines and elastase-alpha-1-antitrypsin in Argentine hemorrhagic fever. Am. J. Trop. Med. Hyg. 60: 85-89.
51. Martínez-Sobrido L, et al. 2010. Hemagglutinin-pseudotyped green fluorescent protein-expressing influenza viruses for the detection of influenza virus neutralizing antibodies. J. Virol. 84:2157-2163.
52. Martínez-Sobrido L, et al. 2009. Identification of amino acid residues critical for the anti-interferon activity of the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 83:11330-11340.
53. Martínez-Sobrido L, Giannakas P, Cubitt B, Garcia-Sastre A, de la Torre JC. 2007. Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J. Virol. 81:12696-12703.
54. Martínez-Sobrido L, Zuniga EI, Rosario D, Garcia-Sastre A, de la Torre JC. 2006. Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 80:9192-9199.
55. McCormick JB, Fisher-Hoch SP. 2002. Lassa fever. Curr. Top. Microbiol. Immunol. 262:75-109.
56. McKee KT, Jr, Huggins JW, Trahan CJ, Mahlandt BG. 1988. Ribavirin prophylaxis and therapy for experimental argentine hemorrhagic fever. Antimicrob. Agents Chemother. 32:1304-1309.
57. Mets MB, Barton LL, Khan AS, Ksiazek TG. 2000. Lymphocytic choriomeningitis virus: an underdiagnosed cause of congenital chorioretinitis. Am. J. Ophthalmol. 130:209-215.
58. Meylan E, et al. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172.
59. Meylan E, et al. 2009. Requirement for NF-kappaB signalling in a mouse model of lung adenocarcinoma. Nature 462:104-107.
60. Mistry N, Shapero J, Crawford RI. 2009. A review of adverse cutaneous drug reactions resulting from the use of interferon and ribavirin. Can. J. Gastroenterol. 23:677-683.
61. Muñoz-Jordán JL, et al. 2005. Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J. Virol. 79:8004-8013.
62. Nomura F, Kawai T, Nakanishi K, Akira S. 2000. NF-kappaB activation through IKK-i-dependent I-TRAF/TANK phosphorylation. Genes Cells 5:191-202.
63. Ortiz-Riaño E, Cheng BYH, de la Torre JC, Martínez-Sobrido L. 2011. The C-terminal region of lymphocytic choriomeningitis virus nucleoprotein contains distinct and segregable functional domains involved in NP-Z interaction and counteraction of the type I interferon response. J. Virol. 85:13038-13048.
64. Palacios G, et al. 2008. A new arenavirus in a cluster of fatal transplantassociated diseases. N. Engl. J. Med. 358:991-998.
65. Pannetier D, Faure C, Georges-Courbot MC, Deubel V, Baize S. 2004. Human macrophages, but not dendritic cells, are activated and produce alpha/beta interferons in response to Mopeia virus infection. J. Virol. 78: 10516-10524.
66. Perez M, Greenwald DL, de la Torre JC. 2004. Myristoylation of the RING finger Z protein is essential for arenavirus budding. J. Virol. 78: 11443-11448.
67. Perry AK, Chow EK, Goodnough JB, Yeh WC, Cheng G. 2004. Differential requirement for TANK-binding kinase-1 in type I interferon responses to toll-like receptor activation and viral infection. J. Exp. Med. 199:1651-1658.
68. Peters CJ. 2002. Human infection with arenaviruses in the Americas. Curr. Top. Microbiol. Immunol. 262:65-74.
69. Peters RT, Liao SM, Maniatis T. 2000. IKKepsilon is part of a novel PMA-inducible IkappaB kinase complex. Mol. Cell 5:513-522.
70. Pomerantz JL, Baltimore D. 1999. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J. 18:6694-6704.
71. Potter JA, Randall RE, Taylor GL. 2008. Crystal structure of human IPS-1/MAVS/VISA/Cardif caspase activation recruitment domain. BMC Struct. Biol. 8:11.
72. Pythoud C, et al. 2012. Arenavirus nucleoprotein targets interferon regulatory factor-activating kinase IKK∑. J. Virol. 86:7728-7738.
73. Qi X, et al. 2010. Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468:779-783.
74. Reis LF, Ho Lee T, Vilcek J. 1989. Tumor necrosis factor acts synergistically with autocrine interferon-beta and increases interferon-beta mRNA levels in human fibroblasts. J. Biol. Chem. 264:16351-16354.
75. Rodrigo WW, de la Torre JC, Martinez-Sobrido L. 2011. Use of singlecycle infectious lymphocytic choriomeningitis virus to study hemorrhagic fever arenaviruses. J. Virol. 85:1684-1695.
76. Rodríguez M, McCormick JB, Weissenbacher MC. 1986. Antiviral effect of ribavirin on Junin virus replication in vitro. Rev. Argent Microbiol. 18:69-74.
77. Sankar S, Chan H, Romanow WJ, Li J, Bates RJ. 2006. IKK-i signals through IRF3 and NFkappaB to mediate the production of inflammatory cytokines. Cell. Signal. 18:982-993.
78. Saron MF, Riviere Y, Hovanessian AG, Guillon JC. 1982. Chronic production of interferon in carrier mice congenitally infected with lymphocytic choriomeningitis virus. Virology 117:253-256.
79. Sasai M, Matsumoto M, Seya T. 2006. The kinase complex responsible for IRF-3-mediated IFN-beta production in myeloid dendritic cells (mDC). J. Biochem. 139:171-175.
80. Schuhmann KM, Pfaller CK, Conzelmann KK. 2011. The measles virus V protein binds to p65 (RelA) to suppress NF-kappaB activity. J. Virol. 85:3162-3171.
81. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, Hiscott J. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148-1151.
82. Shimada T, et al. 1999. IKK-i, a novel lipopolysaccharide-inducible kinase that is related to IkappaB kinases. Int. Immunol. 11:1357-1362.
83. Snell N. 1988. Ribavirin therapy for Lassa fever. Practitioner 232:432.
84. Stasakova J, et al. 2005. Influenza A mutant viruses with altered NS1 protein function provoke caspase-1 activation in primary human macrophages, resulting in fast apoptosis and release of high levels of interleukins 1beta and 18. J. Gen. Virol. 86(Pt 1):185-195.
85. Symeonidou I, et al. 2010. Modulation of NF-kappaBeta signalling pathways by parasites. J. Biol. Regul. Homeost. Agents 24:471-479.
86. Taylor SL, Frias-Staheli N, Garcia-Sastre A, Schmaljohn CS. 2009. Hantaan virus nucleocapsid protein binds to importin alpha proteins and inhibits tumor necrosis factor alpha-induced activation of nuclear factor kappa B. J. Virol. 83:1271-1279.
87. Tojima Y, et al. 2000. NAK is an IkappaB kinase-activating kinase. Nature 404:778-782.
88. Urata S, Yasuda J, de la Torre JC. 2009. The Z protein of the new world arenavirus tacaribe virus has bona fide budding activity that does not depend on known late domain motifs. J. Virol. 83:12651-12655.
89. Wajant H, Pfizenmaier K, Scheurich P. 2003. Tumor necrosis factor signaling. Cell Death Differ. 10:45-65.
90. Wajant H, Scheurich P. 2001. Tumor necrosis factor receptor-associated factor (TRAF) 2 and its role in TNF signaling. Int. J. Biochem. Cell Biol. 33:19-32.
91. Wang X, et al. 2000. Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J. Virol. 74:11566-11573.
92. Weber F, Kochs G, Haller O. 2004. Inverse interference: how viruses fight the interferon system. Viral Immunol. 17:498-515.
93. Weber F, Kochs G, Haller O, Staeheli P. 2003. Viral evasion of the interferon system: old viruses, new tricks. J. Interferon Cytokine Res. 23: 209-213.
94. Weissenbacher MC, Calello MA, Merani MS, McCormick JB, Rodriguez M. 1986. Therapeutic effect of the antiviral agent ribavirin in Junin virus infection of primates. J. Med. Virol. 20:261-267.
95. Weissenbacher MC, Laguens RP, Coto CE. 1987. Argentine hemorrhagic fever. Curr. Top. Microbiol. Immunol. 134:79-116.
96. Xu LG, et al. 2005. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19:727-740.
97. Zhou S, et al. 2010. Induction and inhibition of type I interferon responses by distinct components of lymphocytic choriomeningitis virus. J. Virol. 84:9452-9462.