A conserved region of nonstructural protein 1 from alphacoronaviruses inhibits host gene expression and is critical for viral virulence

Journal of Biological Chemistry

Volumn 294, Issue 37, 2019, Pages 13606-13618

  Shen, Zhou ^a,b   Wang, Gang ^a,b   Yang, Yiling ^a,b   Shi, Jiale ^a,b   Fang, Liurong ^a,b   Li, Fang ^c   Xiao, Shaobo ^a,b   Fu, Zhen F ^a,b,d   Peng, Guiqing ^a,b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b Hubei Key Laboratory of Preventive Veterinary Medicine   (China)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CELL CULTURE; CRYSTAL STRUCTURE; GENE EXPRESSION; MAMMALS; PROTEINS; VIRUSES;

BIOCHEMICAL ANALYSIS; CONSERVED REGIONS; MULTIPLE FUNCTION; NONSTRUCTURAL PROTEINS; PORCINE EPIDEMIC DIARRHEA VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME CORONAVIRUS; SINGLE STRANDED RNA; TRANSMISSIBLE GASTROENTERITIS VIRUS;

DISEASES;

NONSTRUCTURAL PROTEIN 1; NSP1 PROTEIN, SARS CORONAVIRUS; RNA DIRECTED RNA POLYMERASE; SYNAPSIN; VIRAL PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CRISPR-CAS9 SYSTEM; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MOLECULAR CLONING; NONHUMAN; NSP1 GENE; PLASMID; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; SARS CORONAVIRUS; TRANSMISSIBLE GASTROENTERITIS VIRUS; VIROGENESIS; VIRUS REPLICATION; VIRUS VIRULENCE; ALPHACORONAVIRUS; ANIMAL; BETACORONAVIRUS; GENETICS; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PIG; PORCINE EPIDEMIC DIARRHEA VIRUS; ULTRASTRUCTURE; VIRULENCE;

ALPHACORONAVIRUS; ANIMALS; BETACORONAVIRUS; HOST MICROBIAL INTERACTIONS; HUMANS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; PORCINE EPIDEMIC DIARRHEA VIRUS; PROTEIN BIOSYNTHESIS; RNA REPLICASE; SARS VIRUS; SWINE; SYNAPSINS; TRANSMISSIBLE GASTROENTERITIS VIRUS; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 85072234645     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.RA119.009713     Document Type: Article

References (46)

1. Weiss, S. R., and Navas-Martin, S. (2005) Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol. Mol. Biol. Rev. 69, 635- 664 CrossRef Medline
2. Weiss, S. R., and Leibowitz, J. L. (2011) Coronavirus pathogenesis. Adv. Virus. Res. 81, 85-164 CrossRef Medline
3. Jung, K., and Saif, L. J. (2015) Porcine epidemic diarrhea virus infection: etiology, epidemiology, pathogenesis and immunoprophylaxis. Vet. J. 204, 134 -143 CrossRef Medline
4. Zhou, P., Fan, H., Lan, T., Yang, X. L., Shi, W. F., Zhang, W., Zhu, Y., Zhang, Y. W., Xie, Q. M., Mani, S., Zheng, X. S., Li, B., Li, J. M., Guo, H., Pei, G. Q., et al. (2018) Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 556, 255-258 CrossRef Medline
5. Fehr, A. R., and Perlman, S. (2015) Coronaviruses: an overview of their replication and pathogenesis. Methods Mol. Biol. 1282, 1-23 CrossRef Medline
6. Woo, P. C., Huang, Y., Lau, S. K., and Yuen, K. Y. (2010) Coronavirus genomics and bioinformatics analysis. Viruses 2, 1804-1820 CrossRef Medline
7. Almeida, M. S., Johnson, M. A., and Wüthrich, K. (2006) NMR assignment of the SARS-CoV protein nsp1. J. Biomol. NMR 36, 46 CrossRef Medline
8. Jansson, A. M. (2013) Structure of alphacoronavirus transmissible gastroenteritis virus nsp1 has implications for coronavirus nsp1 function and evolution. J. Virol. 87, 2949 -2955 CrossRef Medline
9. Shen, Z., Ye, G., Deng, F., Wang, G., Cui, M., Fang, L., Xiao, S., Fu, Z. F., and Peng, G. (2018) Structural basis for the inhibition of host gene expression by porcine epidemic diarrhea virus nsp1. J. Virol. 92, e01896 CrossRef Medline
10. Narayanan, K., Huang, C., Lokugamage, K., Kamitani, W., Ikegami, T., Tseng, C. T., and Makino, S. (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 CrossRef Medline
11. Züst, R., Cervantes-Barragán, L., Kuri, T., Blakqori, G., Weber, F., Ludewig, B., and Thiel, V. (2007) Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLoS Pathog. 3, e109 CrossRef Medline
12. Zhang, Q., Ma, J., and Yoo, D. (2017) Inhibition of NF-κB activity by the porcine epidemic diarrhea virus nonstructural protein 1 for innate immune evasion. Virology 510, 111-126 CrossRef Medline
13. 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 CrossRef Medline
14. Lokugamage, K. G., Narayanan, K., Nakagawa, K., Terasaki, K., Ramirez, S. I., Tseng, C. T., and Makino, S. (2015) Middle East respiratory syndrome coronavirus nsp1 inhibits host gene expression by selectively targeting mRNAs transcribed in the nucleus while sparing mRNAs of cytoplasmic origin. J. Virol. 89, 10970 -10981 CrossRef Medline
15. Huang, C., Lokugamage, K. G., Rozovics, J. M., Narayanan, K., Semler, B. L., and Makino, S. (2011) Alphacoronavirus transmissible gastroenteritis virus nsp1 protein suppresses protein translation in mammalian cells and in cell-free HeLa cell extracts but not in rabbit reticulocyte lysate. J. Virol. 85, 638 - 643 CrossRef Medline
16. Wang, Y., Shi, H., Rigolet, P., Wu, N., Zhu, L., Xi, X. G., Vabret, A., Wang, X., and Wang, T. (2010) Nsp1 proteins of group I and SARS coronaviruses share structural and functional similarities. Infect. Genet. Evol. 10, 919 -924 CrossRef Medline
17. 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 CrossRef Medline
18. Zhang, Q., Shi, K., and Yoo, D. (2016) Suppression of type I interferon production by porcine epidemic diarrhea virus and degradation of CREB-binding protein by nsp1. Virology 489, 252-268 CrossRef Medline
19. Wang, G., Liang, R., Liu, Z., Shen, Z., Shi, J., Shi, Y., Deng, F., Xiao, S., Fu, Z. F., and Peng, G. (2019) The N-terminal domain of spike protein is not the enteric tropism determinant for transmissible gastroenteritis virus in piglets. Viruses 11, E313 CrossRef Medline
20. Lloyd, R. E. (2006) Translational control by viral proteinases. Virus Res. 119, 76 - 88 CrossRef Medline
21. Schneider, R. J., and Mohr, I. (2003) Translation initiation and viral tricks. Trends Biochem. Sci. 28, 130 -136 CrossRef Medline
22. Patnaik, S., Basu, D., Southall, N., Dehdashti, S., Wan, K. K., Zheng, W., Ferrer, M., Taylor, M., Engel, D. A., and Marugan, J. J. (2019) Identification, design and synthesis of novel pyrazolopyridine influenza virus nonstructural protein 1 antagonists. Bioorg. Med. Chem. Lett. 29, 1113-1119 CrossRef Medline
23. Park, H. S., Liu, G., Thulasi Raman, S. N., Landreth, S. L., Liu, Q., and Zhou, Y. (2018) NS1 protein of 2009 pandemic influenza a virus inhibits porcine NLRP3 Inflammasome-mediated interleukin-1β production by suppressing ASC ubiquitination. J. Virol. 92, e00022-18 CrossRef Medline
24. Nicolodi, C., Groiss, F., Kiselev, O., Wolschek, M., Seipelt, J., and Muster, T. (2019) Safety and immunogenicity of a replication-deficient H5N1 influenza virus vaccine lacking NS1. Vaccine 37, 3722-3729 CrossRef Medline
25. Liu, Y. F., Tsai, P. Y., Chulakasian, S., Lin, F. Y., and Hsu, W. L. (2016) The pseudorabies virus vhs protein cleaves RNA containing an IRES sequence. FEBS J. 283, 899 -911 CrossRef Medline
26. Pasieka, T. J., Lu, B., Crosby, S. D., Wylie, K. M., Morrison, L. A., Alexander, D. E., Menachery, V. D., and Leib, D. A. (2008) Herpes simplex virus virion host shutoff attenuates establishment of the antiviral state. J. Virol. 82, 5527-5535 CrossRef Medline
27. Cai, H., Zhang, Y., Lu, M., Liang, X., Jennings, R., Niewiesk, S., and Li, J. (2016) Phosphorylation of human metapneumovirus M2-1 protein up-regulates viral replication and pathogenesis. J. Virol. 90, 7323-7338 CrossRef Medline
28. Jimenez-Guardeño, J. M., Nieto-Torres, J. L., DeDiego, M. L., Regla-Nava, J. A., Fernandez-Delgado, R., Castaño-Rodriguez, C., and Enjuanes, L. (2014) The PDZ-binding motif of severe acute respiratory syndrome coronavirus envelope protein is a determinant of viral pathogenesis. PLoS Pathog. 10, e1004320 CrossRef Medline
29. DeDiego, M. L., Nieto-Torres, J. L., Jimenez-Guardeño, J. M., Regla-Nava, J. A., Castaño-Rodriguez, C., Fernandez-Delgado, R., Usera, F., and Enjuanes, L. (2014) Coronavirus virulence genes with main focus on SARS-CoV envelope gene. Virus. Res. 194, 124 -137 CrossRef Medline
30. Su, S., Wong, G., Shi, W., Liu, J., Lai, A. C. K., Zhou, J., Liu, W., Bi, Y., and Gao, G. F. (2016) Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol. 24, 490 -502 CrossRef Medline
31. Lamirande, E. W., DeDiego, M. L., Roberts, A., Jackson, J. P., Alvarez, E., Sheahan, T., Shieh, W. J., Zaki, S. R., Baric, R., Enjuanes, L., and Subbarao, K. (2008) A live attenuated severe acute respiratory syndrome coronavirus is immunogenic and efficacious in golden Syrian hamsters. J. Virol. 82, 7721-7724CrossRef Medline
32. Netland, J., DeDiego, M. L., Zhao, J., Fett, C., Álvarez, E., Nieto-Torres, J. L., Enjuanes, L., and Perlman, S. (2010) Immunization with an attenuated severe acute respiratory syndrome coronavirus deleted in E protein protects against lethal respiratory disease. Virology 399, 120 -128 CrossRef Medline
33. Fett, C., DeDiego, M. L., Regla-Nava, J. A., Enjuanes, L., and Perlman, S. (2013) Complete protection against severe acute respiratory syndrome coronavirus-mediated lethal respiratory disease in aged mice by immunization with a mouse-adapted virus lacking E protein. J. Virol. 87, 6551- 6559 CrossRef Medline
34. Graham, R. L., Donaldson, E. F., and Baric, R. S. (2013) A decade after SARS: strategies for controlling emerging coronaviruses. Nat. Rev. Microbiol. 11, 836 - 848 CrossRef Medline
35. Lei, L., Ying, S., Baojun, L., Yi, Y., Xiang, H., Wenli, S., Zounan, S., Deyin, G., Qingyu, Z., Jingmei, L., and Guohui, C. (2013) Attenuation of mouse hepatitis virus by deletion of the LLRKxGxKG region of Nsp1. PLoS One 8, e61166 CrossRef Medline
36. Tohya, Y., Narayanan, K., Kamitani, W., Huang, C., Lokugamage, K., and Makino, S. (2009) Suppression of host gene expression by nsp1 proteins of group 2 bat coronaviruses. J. Virol. 83, 5282-5288 CrossRef Medline
37. Gustin, K. M., Guan, B. J., Dziduszko, A., and Brian, D. A. (2009) Bovine coronavirus nonstructural protein 1 (p28) is an RNA binding protein that binds terminal genomic cis-replication elements. J. Virol. 83, 6087- 6097 CrossRef Medline
38. Guan, B. J., Su, Y. P., Wu, H. Y., and Brian, D. A. (2012) Genetic evidence of a long-range RNA-RNA interaction between the genomic 5' untranslated region and the nonstructural protein 1 coding region in murine and bovine coronaviruses. J. Virol. 86, 4631- 4643 CrossRef Medline
39. Minor, W., Cymborowski, M., Otwinowski, Z., and Chruszcz, M. (2006) HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr. D Biol. Crystallogr. 62, 859 - 866 CrossRef Medline
40. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658 - 674 CrossRef Medline
41. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126 -2132 CrossRef Medline
42. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948 -1954 CrossRef Medline
43. Grell, L., Parkin, C., Slatest, L., and Craig, P. A. (2006) EZ-Viz, a tool for simplifying molecular viewing in PyMOL. Biochem. Mol. Biol. Educ. 34, 402- 407 CrossRef Medline
44. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 CrossRef Medline
45. Schmidt, E. K., Clavarino, G., Ceppi, M., and Pierre, P. (2009) SUnSET, a nonradioactive method to monitor protein synthesis. Nat. Methods 6, 275-277 CrossRef Medline
46. Robert, X., and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320 -W324 CrossRef Medline