Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-κB signaling

Journal of Virology

Volumn 83, Issue 13, 2009, Pages 6689-6705

  Frieman, Matthew ^a   Ratia, Kiira ^b   Johnston, Robert E ^c   Mesecar, Andrew D ^b   Baric, Ralph S ^a  

^a IL   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; PAPAIN; PAPAIN LIKE PROTEINASE; PROTEINASE; PROTEOME; STRUCTURAL PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; 3C LIKE PROTEASE, SARS CORONAVIRUS; 3C-LIKE PROTEASE, SARS CORONAVIRUS; CYSTEINE PROTEINASE; I KAPPA B; INTERFERON; IRF3 PROTEIN, HUMAN; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; SARS CORONAVIRUS; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS PATHOGENESIS; VIRUS REPLICATION; CELL LINE; DRUG ANTAGONISM; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION;

SARS CORONAVIRUS;

CELL LINE; CYSTEINE ENDOPEPTIDASES; HUMANS; I-KAPPA B PROTEINS; INTERFERON REGULATORY FACTOR-3; INTERFERONS; NF-KAPPA B; PHOSPHORYLATION; SARS VIRUS; VIRAL PROTEINS;

EID: 67449088510     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02220-08     Document Type: Article

References (59)

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. (Pubitemid 351657053)
2. Akira, S., and H. Hemmi. 2003. Recognition of pathogen-associated molecular patterns by TLR family. Immunol. Lett. 85:85-95.
3. Andrejeva, J., K. S. Childs, D. F. Young, T. S. Carlos, N. Stock, S. Goodbourn, and R. E. Randall. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. USA 101:17264-17269.
4. Balasuriya, U. B. R., H. W. Heidner, J. F. Hedges, J. C. Williams, N. L. Davis, R. E. Johnston, and N. J. MacLachlan. 2000. Expression of the two major envelope proteins of equine arteritis virus as a heterodimer is necessary for induction of neutralizing antibodies in mice immunized with recombinant Venezuelan equine encephalitis virus replicon particles. J. Virol. 74:10623-10630. (Pubitemid 30815383)
5. Barretto, N., D. Jukneliene, K. Ratia, Z. Chen, A. D. Mesecar, and S. C. Baker. 2006. Deubiquitinating activity of the SARS-CoV papain-like protease. Adv. Exp. Med. Biol. 581:37-41.
6. Barretto, N., D. Jukneliene, K. Ratia, Z. Chen, A. D. Mesecar, and S. C. Baker. 2005. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J. Virol. 79:15189-15198. (Pubitemid 43032301)
7. Basler, C. F., X. Wang, E. Muhlberger, V. Volchkov, J. Paragas, H. D. Klenk, A. Garcia-Sastre, and P. Palese. 2000. The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc. Natl. Acad. Sci. USA 97:12289-12294.
8. Cervantes-Barragan, L., R. Zust, F. Weber, M. Spiegel, K. S. Lang, S. Akira, V. Thiel, and B. Ludewig. 2006. Control of coronavirus infection through plasmacytoid dendritic cell-derived type I interferon. Blood 109:1131-1137.
9. Cornell, C. T., W. B. Kiosses, S. Harkins, and J. L. Whitton. 2006. Inhibition of protein trafficking by coxsackievirus B3: multiple viral proteins target a single organelle. J. Virol. 80:6637-6647. (Pubitemid 43927466)
10. Cruz, C. D., H. Palosaari, J.-P. Parisien, P. Devaux, R. Cattaneo, T. Ouchi, and C. M. Horvath. 2006. Measles virus V protein inhibits p53 family member p73. J. Virol. 80:5644-5650. (Pubitemid 43752811)
11. Davis, N. L., I. J. Caley, K. W. Brown, M. R. Betts, D. M. Irlbeck, K. M. McGrath, M. J. Connell, D. C. Montefiori, J. A. Frelinger, R. Swanstrom, P. R. Johnson, and R. E. Johnston. 2000. Vaccination of macaques against pathogenic simian immunodeficiency virus with Venezuelan equine encephalitis virus replicon particles. J. Virol. 74:371-378. (Pubitemid 30002918)
12. de Lang, A., T. Baas, T. Teal, L. M. Leijten, B. Rain, A. D. Osterhaus, B. L. Haagmans, and M. G. Katze. 2007. Functional genomics highlights differential induction of antiviral pathways in the lungs of SARS-CoV-infected macaques. PLoS Pathog. 3:e112.
13. Devaraj, S. G., N. Wang, Z. Chen, Z. Chen, M. Tseng, N. Barretto, R. Lin, C. J. Peters, C. T. Tseng, S. C. Baker, and K. Li. 2007. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J. Biol. Chem. 282:32208-32221.
14. Dowell, S. F., and M. S. Ho. 2004. Seasonality of infectious diseases and severe acute respiratory syndrome - what we don't know can hurt us. Lancet Infect. Dis. 4:704-708.
15. Drosten, C., S. Gunther, W. Preiser, S. van der Werf, H. R. Brodt, S. Becker, H. Rabenau, M. Panning, L. Kolesnikova, R. A. Fouchier, A. Berger, A. M. Burguiere, J. Cinatl, M. Eickmann, N. Escriou, K. Grywna, S. Kramme, J. C. Manuguerra, S. Muller, V. Rickerts, M. Sturmer, S. Vieth, H. D. Klenk, A. D. Osterhaus, H. Schmitz, and H. W. Doerr. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967-1976.
16. Eckerle, L. D., X. Lu, S. M. Sperry, L. Choi, and M. R. Denison. 2007. High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J. Virol. 81:12135-12144. (Pubitemid 350085829)
17. Fitzgerald, K. A., S. M. McWhirter, K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S. M. Liao, and T. Maniatis. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491-496.
18. Frieman, M., B. Yount, M. Heise, S. A. Kopecky-Bromberg, P. Palese, and R. S. Baric. 2007. Severe acute respiratory syndrome coronavirus ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rough endoplasmic reticulum/Golgi membrane. J. Virol. 81:9812-9824. (Pubitemid 350067685)
19. Gale, M. J., Jr., M. J. Korth, N. M. Tang, S. L. Tan, D. A. Hopkins, T. E. Dever, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230:217-227. (Pubitemid 27211852)
20. Garcia-Sastre, A., A. Egorov, D. Matassov, S. Brandt, D. E. Levy, J. E. Durbin, P. Palese, and T. Muster. 1998. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324-330. (Pubitemid 29013414)
21. Gorbalenya, A. E., E. J. Snijder, and W. J. M. Spaan. 2004. Severe acute respiratory syndrome coronavirus phylogeny: toward consensus. J. Virol. 78:7863-7866. (Pubitemid 38944271)
22. Graham, R. L., A. C. Sims, S. M. Brockway, R. S. Baric, and M. R. Denison. 2005. The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication. J. Virol. 79:13399-13411. (Pubitemid 41508153)
23. Han, Y., H. Geng, W. Feng, X. Tang, A. Ou, Y. Lao, Y. Xu, H. Lin, H. Liu, and Y. Li. 2003. A follow-up study of 69 discharged SARS patients. J. Tradit. Chin. Med. 23:214-217.
24. Harcourt, B. H., D. Jukneliene, A. Kanjanahaluethai, J. Bechill, K. M. Severson, C. M. Smith, P. A. Rota, and S. C. Baker. 2004. Identification of severe acute respiratory syndrome coronavirus replicase products and characterization of papain-like protease activity. J. Virol. 78:13600-13612. (Pubitemid 39612760)
25. Hengel, H., U. H. Koszinowski, and K. K. Conzelmann. 2005. Viruses know it all: new insights into IFN networks. Trends Immunol. 26:396-401. (Pubitemid 40835846)
26. Hiscott, J., N. Grandvaux, S. Sharma, B. R. Tenoever, M. J. Servant, and R. Lin. 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.
27. Ikeda, F., C. M. Hecker, A. Rozenknop, R. D. Nordmeier, V. Rogov, K. Hofmann, S. Akira, V. Dotsch, and I. Dikic. 2007. Involvement of the ubiquitin- like domain of TBK1/IKK-i kinases in regulation of IFN-inducible genes. EMBO J. 26:3451-3462. (Pubitemid 47123538)
28. Kash, J. C., E. Mühlberger, V. Carter, M. Grosch, O. Perwitasari, S. C. Proll, M. J. Thomas, F. Weber, H.-D. Klenk, and M. G. Katze. 2006. Global suppression of the host antiviral response by Ebola- and Marburgviruses: increased antagonism of the type I interferon response is associated with enhanced virulence. J. Virol. 80:3009-3020. (Pubitemid 43346396)
29. Kopecky-Bromberg, S. A., L. Martinez-Sobrido, M. Frieman, R. A. Baric, and P. Palese. 2007. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J. Virol. 81:548-557. (Pubitemid 46067882)
30. Ksiazek, T. G., D. Erdman, C. S. Goldsmith, S. R. Zaki, T. Peret, S. Emery, S. Tong, C. Urbani, J. A. Comer, W. Lim, P. E. Rollin, S. F. Dowell, A. E. Ling, C. D. Humphrey, W. J. Shieh, J. Guarner, C. D. Paddock, P. Rota, B. Fields, J. DeRisi, J. Y. Yang, N. Cox, J. M. Hughes, J. W. LeDuc, W. J. Bellini, and L. J. Anderson. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-1966.
31. Lau, S. K., P. C. Woo, K. S. Li, Y. Huang, H. W. Tsoi, B. H. Wong, S. S. Wong, S. Y. Leung, K. H. Chan, and K. Y. Yuen. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA 102:14040-14045.
32. Levy, D. E., and A. Garcia-Sastre. 2001. The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev. 12:143-156. (Pubitemid 32590836)
33. May, M. J., S. E. Larsen, J. H. Shim, L. A. Madge, and S. Ghosh. 2004. A novel ubiquitin-like domain in IkappaB kinase beta is required for functional activity of the kinase. J. Biol. Chem. 279:45528-45539.
34. McWhirter, S. M., B. R. Tenoever, and T. Maniatis. 2005. Connecting mitochondria and innate immunity. Cell 122:645-647. (Pubitemid 41242626)
35. Meylan, E., J. Curran, K. Hofmann, D. Moradpour, M. Binder, R. Bartenschlager, and J. Tschopp. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172. (Pubitemid 41509355)
36. Narayanan, K., C. Huang, K. Lokugamage, W. Kamitani, T. Ikegami, C.-T. K. Tseng, and S. Makino. 2008. Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J. Virol. 82:4471-4479. (Pubitemid 351563683)
37. Parisien, J. P., J. F. Lau, J. J. Rodriguez, B. M. Sullivan, A. Moscona, G. D. Parks, R. A. Lamb, and C. M. Horvath. 2001. The V protein of human parainfluenza virus 2 antagonizes type I interferon responses by destabilizing signal transducer and activator of transcription 2. Virology 283:230-239. (Pubitemid 32881170)
38. Park, M.-S., M. L. Shaw, J. Muñoz-Jordan, J. F. Cros, T. Nakaya, N. Bouvier, P. Palese, A. Garcia-Sastre, and C. F. Basler. 2003. Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J. Virol. 77:1501-1511. (Pubitemid 36055570)
39. Poon, L. L. M., D. K. W. Chu, K. H. Chan, O. K. Wong, T. M. Ellis, Y. H. C. Leung, S. K. P. Lau, P. C. Y. Woo, K. Y. Suen, K. Y. Yuen, Y. Guan, and J. S. Peiris. 2005. Identification of a novel coronavirus in bats. J. Virol. 79:2001-2009. (Pubitemid 40204557)
40. Pushko, P., M. Parker, G. V. Ludwig, N. L. Davis, R. E. Johnston, and J. F. Smith. 1997. Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology 239:389-401. (Pubitemid 28105644)
41. Qian, X.-Y., F. Alonso-Caplen, and R. M. Krug. 1994. Two functional domains of the influenza virus NS1 protein are required for regulation of nuclear export of mRNA. J. Virol. 68:2433-2441. (Pubitemid 24091923)
42. Ratia, K., K. S. Saikatendu, B. D. Santarsiero, N. Barretto, S. C. Baker, R. C. Stevens, and A. D. Mesecar. 2006. Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc. Natl. Acad. Sci. USA 103:5717-5722.
43. 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 α1 and blocks STAT1 nuclear accumulation. J. Virol. 80:5156-5167. (Pubitemid 43752761)
44. Rivas, C., J. Gil, Z. Melkova, M. Esteban, and M. Diaz-Guerra. 1998. Vaccinia virus E3L protein is an inhibitor of the interferon (i.f.n.)-induced 2-5A synthetase enzyme. Virology 243:406-414. (Pubitemid 28384157)
45. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
46. Schijns, V. E., C. M. Wierda, M. van Hoeij, and M. C. Horzinek. 1996. Exacerbated viral hepatitis in IFN-gamma receptor-deficient mice is not suppressed by IL-12. J. Immunol. 157:815-821. (Pubitemid 26231387)
47. Schoneboom, B. A., J. S. Lee, and F. B. Grieder. 2000. Early expression of IFN-alpha/beta and iNOS in the brains of Venezuelan equine encephalitis virus-infected mice. J. Interferon Cytokine Res. 20:205-215. (Pubitemid 30123750)
48. Shabman, R. S., T. E. Morrison, C. Moore, L. White, M. S. Suthar, L. Hueston, N. Rulli, B. Lidbury, J. P.-Y. 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. (Pubitemid 44975164)
49. Symons, J. A., A. Alcami, and G. L. Smith. 1995. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81:551-560.
50. Terzic, J., I. Marinovic-Terzic, F. Ikeda, and I. Dikic. 2007. Ubiquitin signals in the NF-kappaB pathway. Biochem. Soc. Trans. 35:942-945.
51. Theofilopoulos, A. N., R. Baccala, B. Beutler, and D. H. Kono. 2005. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 23:307-336.
52. Warfield, K. L., C. M. Bosio, B. C. Welcher, E. M. Deal, M. Mohamadzadeh, A. Schmaljohn, M. J. Aman, and S. Bavari. 2003. Ebola virus-like particles protect from lethal Ebola virus infection. Proc. Natl. Acad. Sci. USA 100:15889-15894.
53. Wathelet, M. G., M. Orr, M. B. Frieman, and R. S. Baric. 2007. Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J. Virol. 81:11620-11633. (Pubitemid 47623794)
54. Webster, R. G. 2004. Wet markets - a continuing source of severe acute respiratory syndrome and influenza? Lancet 363:234-236.
55. Xiang, Y., R. C. Condit, S. Vijaysri, B. Jacobs, B. R. G. Williams, and R. H. Silverman. 2002. Blockade of interferon induction and action by the E3L double-stranded RNA binding proteins of vaccinia virus. J. Virol. 76:5251-5259. (Pubitemid 34441727)
56. Ye, Y., K. Hauns, J. O. Langland, B. L. Jacobs, and B. G. Hogue. 2007. Mouse hepatitis coronavirus A59 nucleocapsid protein is a type I interferon antagonist. J. Virol. 81:2554-2563. (Pubitemid 46447021)
57. Yount, B., K. M. Curtis, E. A. Fritz, L. E. Hensley, P. B. Jahrling, E. Prentice, M. R. Denison, T. W. Geisbert, and R. S. Baric. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 100:12995-13000.
58. Zheng, D., G. Chen, B. Guo, G. Cheng, and H. Tang. 2008. PLP2, a potent deubiquitinase from murine hepatitis virus, strongly inhibits cellular type I interferon production. Cell Res. 18:1105-1113.
59. Zhou, Z., K. Hoebe, X. Du, Z. Jiang, L. Shamel, and B. Beutler. 2005. Antagonism between MyD88- and TRIF-dependent signals in B7RP-1 upregulation. Eur. J. Immunol. 35:1918-1927.