The structural and accessory proteins M, ORF 4a, ORF 4b, and ORF 5 of Middle East respiratory syndrome coronavirus (MERS-CoV) are potent interferon antagonists

Protein and Cell

Volumn 4, Issue 12, 2013, Pages 951-961

  Yang, Yang ^a   Zhang, Ling ^a   Geng, Heyuan ^a   Deng, Yao ^a   Huang, Baoying ^a   Guo, Yin ^b   Zhao, Zhengdong ^a   Tan, Wenjie ^a  

^a BEIJING HOSPITAL   (China)

^b INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

accessory proteins; interferon antagonists; MERS CoV; structural proteins

Indexed keywords

BETA ACTIN; BETA INTERFERON; E PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; M PROTEIN; ORF 3 PROTEIN; ORF 4A PROTEIN; ORF 4B PROTEIN; ORF 5 PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VITRONECTIN;

ARTICLE; CELL ORGANELLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CORONAVIRUS; CYTOPLASM; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTERFERON PRODUCTION; MIDDLE EAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CELL LINE; CORONAVIRUS; GENES, VIRAL; HUMANS; INTERFERONS; OPEN READING FRAMES; RECOMBINANT PROTEINS; VIRAL MATRIX PROTEINS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRAL STRUCTURAL PROTEINS;

EID: 84890049888     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-013-3096-8     Document Type: Article

References (51)

1. Basler, C. F., Wang, X., Mühlberger, E., Volchkov, V., Paragas, J., and Klenk, H. D. (2000). The Ebola virus VP35 protein functions as a type I IFN an tagonist. Proc Natl Acad Sci U S A 97, 12289-12294.
2. Breban, R., Riou, J., and Fontanet, A. (2013). Interhuman transmissibility of Middle East respiratory syndrome coronavirus: estimation of pandemic risk. The Lancet 382, 694-649.
3. Corse, E., and Machamer, C. E. (2000). Infectious bronchitis virus E protein is targeted to the Golgi complex and directs release of viruslike particles. J Virol 74, 4319-4326.
4. Chan, R. W., Chan, M. C., Agnihothram, S., Chan, L. L., Kuok, D. I., and Fong, J. H. (2013). Tropism of and innate immune responses to the novel human betacoronavirus lineage C virus in human ex vivo respiratory organ cultures. J Virol 87, 6604-6614.
5. de Groot, R. J., Baker, S. C., Baric, R. S., Brown, C. S., Drosten, C., and Enjuanes, L. (2013). Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol 87, 7790-7792.
6. Devaraj, S. G., Wang, N., Chen, Z., Chen, Z., Tseng, M., and Barretto, N. (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.
7. de Wilde, A. H., Raj, V. S., Oudshoorn, D., Bestebroer, T. M., van Nieuwkoop, S., and Limpens, R. W. (2013). MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-α treatment. J Gen Virol 94, 1749-1760.
8. Freundt, E. C., Yu, L., Park, E., Lenardo, M. J., and Xu, X. N. (2009). Molecular determinants for subcellular localization of the severe acute respiratory syndrome coronavirus open reading frame 3b protein. J Virol 83, 6631-6640.
9. Frieman, M., Ratia, K., Johnston, R. E., Mesecar, A. D., and Baric, R. S. (2009). Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-kappaB signaling. J Virol 83, 6689-6705.
10. Frieman, M., Yount, B., Heise, M., Kopecky-Bromberg, S. A., Palese, P., and Baric, R. S. (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.
11. Frieman, M., and Baric, R. (2008). Mechanisms of severe acute respiratory syndrome pathogenesis and innate immunomodulation. Microbiol Mol Biol Rev 72, 672-685.
12. García-Sastre, A., and Biron, C. A. (2006). Type 1 interferons and the virus-host relationship a lesson in détente. Science 312, 879-882.
13. Hiscox, J. A., Wurm, T., Wilson, L., Britton, P., Cavanagh, D., and Brooks, G. (2001). The coronavirus infectious bronchitis virus nucleoprotein localizes to the nucleolus. J Virol 75, 506-512.
14. Huang, C., Lokugamage, K. G., Rozovics, J. M., Narayanan, K., Semler, B. L., and Makino, S. (2011). SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: viral mRNAs are resistant to nsp1-induced RNA cleavage. PLoS Pathog 7, e1002433.
15. Kamitani, W., Huang, C., Narayanan, K., Lokugamage, K. G., and Makino, S. (2009). A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat Struct Mol Biol 16, 1134-1140.
16. Khan, S., Fielding, B. C., Tan, T. H., Chou, C. F., Shen, S., and Lim, S. G. (2006). Over-expression of severe acute respiratory syndrome coronavirus 3b protein induces both apoptosis and necrosis in Vero E6 Cells. Virus Res 122, 20-27.
17. Kochs, G., García-Sastre, A., and Martínez-Sobrido, L. (2007). Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81, 7011-7021.
18. Kopecky-Bromberg, S. A., Martínez-Sobrido, L., Frieman, M., Baric, R. A., and Palese, P. (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.
19. Lai, M. M. C., Perlman, S., and Anderson, J. L. (2006). Coronaviridae. In: Knipe D. M., Howley P. M., eds. Fields Virology, 5th edition. Philadelphia: Lippincott Williams & Wilkins, pp. 1305-1335.
20. Lei, X, Liu, X, Ma, Y, Sun, Z, Yang, Y, and Jin, Q. (2010). The 3C protein of enterovirus 71 inhibits retinoid acid-inducible gene I-mediated interferon regulatory factor 3activation and type I interferon responses. J Virol 34, 8051-8061.
21. Lontok, E., Corse, E., and Machamer, C. E. (2004). Intracellular targeting signals contribute to localization of coronavirus spike proteins near the virus assembly site. J Virol 78, 5913-5922.
22. Lu, X., Pan, J., Tao, J., and Guo, D. (2011). SARS-CoV nucleocapsid protein antagonizes IFN-β response by targeting initial step of IFN-β induction pathway, and its C-terminal region is critical for the antagonism. Virus Genes 42, 37-45.
23. Lu, G, Hu, Y, Wang, Q, Qi, J, Gao, F, and Li, Y. (2013). Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 500, 227-231.
24. Koetzner, C. A., Kuo, L., Goebel, S. J., Dean, A. B., Parker, M. M., and Masters, P. S. (2010). MHV Accessory protein 5a is a major antagonist of the antiviral action of interferon against murine coronavirus. J Virol 84, 8262-8274.
25. Marra, M. A., Jones, S. J., Astell, C. R., Holt, R. A., Brooks-Wilson, A., and Butterfield, Y. S. (2003). The Ge nome sequence of the SARS-associated coronavirus. Science 300, 1399-1404.
26. McBride, R., and Fielding, B. C. (2012). The role of severe acute respiratory syndrome (SARS)-coronavirus accessory proteins in virus pathogenesis. Viruses 4, 2902-2923.
27. Nal, B., Chan, C., Kien, F., Siu, L., Tse, J., and Chu, K. (2005). Differential maturation and subcellular localization of severe acute respiratory syndrome coronavirus surface proteins S, M and E. J Gen Virol 86, 1423-1434.
28. Nieto-Torres, J. L., Dediego, M. L., Alvarez, E., Jiménez-Guardeño, J. M., Regla-Nava, J. A., and Llorente, M. (2011). Subcellular location and topology of severe acute respiratory syndrome coronavirus envelope protein. Virology 415, 69-82.
29. Niwa, H., Yamamura, K., and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
30. Raj, V. S., Mou, H., Smits, S. L., Dekkers, D. H., Müller, M. A., and Dijkman, R. (2013). Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495, 251-254.
31. Randall, R. E., and Goodbourn, S. (2008). Interferons and viruses: an interplay between induction, signaling, antiviral responses and virus countermeasures. J Gen Virol 89, 1-47.
32. Reid, S. P., Leung, L. W., Hartman, A. L., Martinez, O., Shaw, M. L., and Carbonnelle, C. (2006). Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J Virol 80, 5156-5167.
33. Shaw, M. L. 2009. Henipaviruses employ a multifaceted approach to evade the antiviral interferon response. Viruses 1, 1190-1203.
34. Siu, K. L., Kok, K. H., Ng, M. H., Poon, V. K., Yuen, K. Y., and Zheng, B. J. (2009). Severe acute respiratory syndrome coronavirus M protein inhibits type I interferon production by impeding the formation of TRAF3. TANK. TBK1/IKKepsilon complex. J Biol Chem 284, 16202-16209.
35. Sun, L., Xing, Y., Chen, X., Zheng, Y., Yang, Y., and Nichols, D. B. (2012). Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS One 7, e30802.
36. Sun, W., Li, Y., Chen, L., Chen, H., You, F., and Zhou, X. (2009). ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci U S A 106, 8653-8658.
37. Surjit, M., Kumar, R., Mishra, R. N., Reddy, M. K., Chow, V. T., and Lal, S. K. (2005). The sever e acute respiratory syndrome coronavirus nucleocapsid protein is phosphorylated and localizes in the cytoplasm by 14-3-3-mediated translocation. J Virol 79, 11476-11486.
38. Susan, R. W., and Julian, L. L. (2011). Coronavir us pathogenesis. Adv Virus Res 81, 95-164.
39. Taylor, K. E., and Mossman, K. L. (2013). Recent advances in understanding viral evasion of type I interferon. Immunology 138, 190-197.
40. Totura, A. L., and Baric, R. S. (2012). SARS coronavirus pathogenesis: host innate immune responses and viral antagonism of interferon. Curr Opin Virol 2, 264-275.
41. van Boheemen, S., de Graaf, M., Lauber, C., Bestebroer, TM., Raj, V. S., and Zaki, A. M. (2012). Genomic c haracterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio 3, pii: e00473-12.
42. Wang, B., Xi, X., Lei, X., Zhang, X., Cui, S., and Wang, J. (2013). Enterovir us 71 protease 2Apro targets MAVS to inhibit anti-viral type I interferon responses. PLoS Pathog 9, e1003231.
43. Wathelet, M. G., Orr, M., Frieman, M. B., and Baric, R. S. (2007). Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81, 11620-11633.
44. World Health Organization. (2013). Novel coronavirus inf1ection-update. http://www. who. int/csr/don/2013_08_01/en/index. html.
45. Wurm, T., Chen, H., Hodgson, T., Britton, P., Brooks, G., and Hiscox, J. A. (2001). Localization to the nucleolus is a common feature of coronavirus nucleoproteins, and the protein may disrupt host cell division. J Virol 75, 9345-9356.
46. Ye, Y., Hauns, K., Langland, J. O., Jacobs, B. L., and Hogue, B. G. (2007). Mouse hepatitis coronavirus A59 nucleocapsid protein is a type I interferon Antagonist. J Virol 81, 2554-2563.
47. You, J., Dove, B. K., Enjuanes, L., DeDiego, M. L., Alvarez, E., and Howell, G. (2005). Subcellular localization of the severe acute respiratory syndrome coronavirus nucleocapsid protein. J Gen Virol 86, 3303-3310.
48. Yuan, X., Yao, Z., Shan, Y., Chen, B., Yang, Z., and Wu, J. (2005a). Nucleolar localization of non-structural protein 3b, a protein specifically encoded by the severe acute respiratory syndrome coronavirus. Virus Res 114, 70-79.
49. Yuan, X., Shan, Y., Zhao, Z., Chen, J., and Cong, Y. (2005b). G0/G1 arr est and apoptosis induced by SARS-CoV 3b protein in transfected cells. Virol J 2, 66.
50. Zaki, A. M., van Boheemen, S., Bestebroer, T. M., Osterhaus, A. D., and Fouchier, R. A. (2012). Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367, 1814-1820.
51. Zhao, L., Rose, K. M., Elliott, R., van Rooijen, N., and Weiss, S. R. (2011). Cell-type-specific type I interferon antagonism influences organ tropism of murine coronavirus. J Virol 85, 10058-10068.