Porcine deltacoronavirus nsp5 antagonizes type I interferon signaling by cleaving STAT2

Journal of Virology

Volumn 91, Issue 10, 2017, Pages

  Zhu, Xinyu ^a,b   Wang, Dang ^a,b   Zhou, Junwei ^a,b   Pan, Ting ^a,b   Chen, Jiyao ^a,b   Yang, Yuting ^a,b   Lv, Mengting ^a,b   Ye, Xu ^a,b   Peng, Guiqing ^a,b   Fang, Liurong ^a,b   Xiao, Shaobo ^a,b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b THE COOPERATIVE INNOVATION CENTER FOR SUSTAINABLE PIG PRODUCTION   (China)

Author keywords

Immune suppression; Interferon signaling; Nonstructural protein 5 (nsp5); Porcine deltacoronavirus; STAT2

Indexed keywords

ALPHA INTERFERON; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 9; JANUS KINASE 1; JANUS KINASE 2; NONSTRUCTURAL PROTEIN 5; STAT2 PROTEIN; VIRAL PROTEIN;

ANIMAL CELL; ARTICLE; CHEMICAL PHENOMENA; CONTROLLED STUDY; DIARRHEA; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LUCIFERASE ASSAY; MOLECULAR WEIGHT; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PORCINE DELTACORONAVIRUS; PORCINE EPIDEMIC DIARRHEA VIRUS; PORCINE RESPIRATORY CORONAVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CHEMISTRY; CORONAVIRIDAE; CORONAVIRUS INFECTION; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; PIG;

ANIMALS; CORONAVIRUS; CORONAVIRUS INFECTIONS; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; PORCINE EPIDEMIC DIARRHEA VIRUS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STAT2 TRANSCRIPTION FACTOR; SWINE; VIRAL PROTEINS;

EID: 85018313703     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00003-17     Document Type: Article

References (58)

1. Chen Q, Gauger P, Stafne M, Thomas J, Arruda P, Burrough E, Madson D, Brodie J, Magstadt D, Derscheid R, Welch M, Zhang J. 2015. Pathogenicity and pathogenesis of a United States porcine deltacoronavirus cell culture isolate in 5-day-old neonatal piglets. Virology 482:51-59. https:// doi.org/10.1016/j.virol.2015.03.024.
2. Jung K, Hu H, Eyerly B, Lu Z, Chepngeno J, Saif LJ. 2015. Pathogenicity of 2 porcine deltacoronavirus strains in gnotobiotic pigs. Emerg Infect Dis 21:650-654. https://doi.org/10.3201/eid2104.141859.
3. Ma Y, Zhang Y, Liang X, Lou F, Oglesbee M, Krakowka S, Li J. 2015. Origin, evolution, and virulence of porcine deltacoronaviruses in the United States. mBio 6:e00064-15. https://doi.org/10.1128/mBio.00064-15.
4. Hu H, Jung K, Vlasova AN, Saif LJ. 2016. Experimental infection of gnotobiotic pigs with the cell-culture-adapted porcine deltacoronavirus strain OH-FD22. Arch Virol 161:3421-3434. https://doi.org/10.1007/ s00705-016-3056-8.
5. Woo PC, Lau SK, Lam CS, Lau CC, Tsang AK, Lau JH, Bai R, Teng JL, Tsang CC, Wang M, Zheng BJ, Chan KH, Yuen KY. 2012. Discovery of seven novel mammalian and avian coronaviruses in the genus Deltacoronavirus supports bat coronaviruses as the gene source of Alphacoronavirus and Betacoronavirus and avian coronaviruses as the gene source of Gammacoronavirus and Deltacoronavirus. J Virol 86:3995-4008. https:// doi.org/10.1128/JVI.06540-11.
6. Wang L, Byrum B, Zhang Y. 2014. Detection and genetic characterization of deltacoronavirus in pigs, Ohio, USA, 2014. Emerg Infect Dis 20: 1227-1230. https://doi.org/10.3201/eid2007.140296.
7. Wang L, Byrum B, Zhang Y. 2014. Porcine coronavirus HKU15 detected in 9 US states, 2014. Emerg Infect Dis 20:1594-1595. https://doi.org/10 .3201/eid2009.140756.
8. Homwong N, Jarvis MC, Lam HC, Diaz A, Rovira A, Nelson M, Marthaler D. 2016. Characterization and evolution of porcine deltacoronavirus in the United States. Prev Vet Med 123:168-174. https://doi.org/10.1016/j .prevetmed.2015.11.001.
9. Lee JH, Chung HC, Nguyen VG, Moon HJ, Kim HK, Park SJ, Lee CH, Lee GE, Park BK. 2016. Detection and phylogenetic analysis of porcine deltacoronavirus in Korean swine farms, 2015. Transbound Emerg Dis 63:248-252. https://doi.org/10.1111/tbed.12490.
10. Dong N, Fang L, Zeng S, Sun Q, Chen H, Xiao S. 2015. Porcine deltacoronavirus in mainland China. Emerg Infect Dis 21:2254-2255. https:// doi.org/10.3201/eid2112.150283.
11. Song D, Zhou X, Peng Q, Chen Y, Zhang F, Huang T, Zhang T, Li A, Huang D, Wu Q, He H, Tang Y. 2015. Newly emerged porcine deltacoronavirus associated with diarrhoea in swine in China: identification, prevalence and full-length genome sequence analysis. Transbound Emerg Dis 62: 575-580. https://doi.org/10.1111/tbed.12399.
12. Wang YW, Yue H, Fang W, Huang YW. 2015. Complete genome sequence of porcine deltacoronavirus strain CH/Sichuan/S27/2012 from mainland China. Genome Announc 3:e00945-15. https://doi.org/10 .1128/genomeA.00945-15.
13. Janetanakit T, Lumyai M, Bunpapong N, Boonyapisitsopa S, Chaiyawong S, Nonthabenjawan N, Kesdaengsakonwut S, Amonsin A. 2016. Porcine deltacoronavirus, Thailand, 2015. Emerg Infect Dis 22:757-759. https:// doi.org/10.3201/eid2204.151852.
14. Saeng-Chuto K, Lorsirigool A, Temeeyasen G, Vui DT, Stott CJ, Madapong A, Tripipat T, Wegner M, Intrakamhaeng M, Chongcharoen W, Tantituvanont A, Kaewprommal P, Piriyapongsa J, Nilubol D. 2017. Different lineage of porcine deltacoronavirus in Thailand, Vietnam and Lao PDR in 2015. Transbound Emerg Dis 64:3-10. https://doi.org/10.1111/tbed .12585.
15. Zhang J. 2016. Porcine deltacoronavirus: overview of infection dynamics, diagnostic methods, prevalence and genetic evolution. Virus Res 226: 71-84. https://doi.org/10.1016/j.virusres.2016.05.028.
16. Jung K, Hu H, Saif LJ. 2016. Porcine deltacoronavirus infection: etiology, cell culture for virus isolation and propagation, molecular epidemiology and pathogenesis. Virus Res 226:50-59. https://doi.org/10.1016/j.virusres .2016.04.009.
17. Woo PC, Lau SK, Huang Y, Yuen KY. 2009. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med (Maywood) 234:1117-1127. https://doi.org/10.3181/0903-MR-94.
18. Fang P, Fang L, Hong Y, Liu X, Dong N, Ma P, Bi J, Wang D, Xiao S. 20 December 2016. Discovery of a novel accessory protein NS7a encoded by porcine deltacoronavirus. J Gen Virol https://doi.org/10.1099/jgv .0.000690.
19. Fang P, Fang L, Liu X, Hong Y, Wang Y, Dong N, Ma P, Bi J, Wang D, Xiao S. 2016. Identification and subcellular localization of porcine deltacoronavirus accessory protein NS6. Virology 499:170-177. https://doi.org/10 .1016/j.virol.2016.09.015.
20. Li G, Chen Q, Harmon KM, Yoon KJ, Schwartz KJ, Hoogland MJ, Gauger PC, Main RG, Zhang J. 2014. Full-length genome sequence of porcine deltacoronavirus strain U S A/IA/2014/8734. Genome Announc 2:e00278-14. https://doi.org/10.1128/genomeA.00278-14.
21. Chen F, Zhu Y, Wu M, Ku X, Yao L, He Q. 2015. Full-length genome characterization of Chinese porcine deltacoronavirus strain CH/SXD1/ 2015. Genome Announc 3:e01284-15. https://doi.org/10.1128/genomeA .01284-15.
22. Anand K, Ziebuhr J, Wadhwani P, Mesters JR, Hilgenfeld R. 2003. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 300:1763-1767. https://doi.org/10.1126/science.1085658.
23. Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, Bayer S, Weissbrich B, Snijder EJ, Rabenau H, Doerr HW, Gorbalenya AE, Ziebuhr J. 2003. Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol 84:2305-2315. https://doi.org/10.1099/vir.0.19424-0.
24. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47. https://doi.org/10.1099/vir.0.83391-0.
25. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE, Kuestner R, Garrigues U, Birks C, Roraback J, Ostrander C, Dong D, Shin J, Presnell S, Fox B, Haldeman B, Cooper E, Taft D, Gilbert T, Grant FJ, Tackett M, Krivan W, McKnight G, Clegg C, Foster D, Klucher KM. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol 4:63-68. https://doi.org/10.1038/ni873.
26. Ihle JN. 1995. The Janus protein tyrosine kinase family and its role in cytokine signaling. Adv Immunol 60:1-35. https://doi.org/10.1016/S0065-2776(08)60582-9.
27. Darnell JE, Jr, Kerr IM, Stark GR. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1421. https://doi.org/10.1126/ science.8197455.
28. Qureshi SA, Salditt-Georgieff M, Darnell JE, Jr. 1995. Tyrosinephosphorylated Stat1 and Stat2 plus a 48-kDa protein all contact DNA in forming interferon-stimulated-gene factor 3. Proc Natl Acad Sci U S A 92:3829-3833. https://doi.org/10.1073/pnas.92.9.3829.
29. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. 1998. How cells respond to interferons. Annu Rev Biochem 67:227-264. https://doi .org/10.1146/annurev.biochem.67.1.227.
30. Grant A, Ponia SS, Tripathi S, Balasubramaniam V, Miorin L, Sourisseau M, Schwarz MC, Sanchez-Seco MP, Evans MJ, Best SM, Garcia-Sastre A. 2016. Zika virus targets human STAT2 to inhibit type I interferon signaling. Cell Host Microbe 19:882-890. https://doi.org/10.1016/j.chom.2016.05.009.
31. Ashour J, Laurent-Rolle M, Shi PY, Garcia-Sastre A. 2009. NS5 of dengue virus mediates STAT2 binding and degradation. J Virol 83:5408-5418. https://doi.org/10.1128/JVI.02188-08.
32. Lin W, Kim SS, Yeung E, Kamegaya Y, Blackard JT, Kim KA, Holtzman MJ, Chung RT. 2006. Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J Virol 80:9226-9235. https://doi.org/10.1128/JVI.00459-06.
33. Zhu X, Fang L, Wang D, Yang Y, Chen J, Ye X, Foda MF, Xiao S. 2017. Porcine deltacoronavirus nsp5 inhibits interferon-beta production through the cleavage of NEMO. Virology 502:33-38. https://doi.org/10 .1016/j.virol.2016.12.005.
34. Takaoka A, Yanai H. 2006. Interferon signalling network in innate defence. Cell Microbiol 8:907-922. https://doi.org/10.1111/j.1462-5822 .2006.00716.x.
35. Hsu MF, Kuo CJ, Chang KT, Chang HC, Chou CC, Ko TP, Shr HL, Chang GG, Wang AH, Liang PH. 2005. Mechanism of the maturation process of SARS-CoV 3CL protease. J Biol Chem 280:31257-31266. https://doi.org/ 10.1074/jbc.M502577200.
36. Ye G, Deng F, Shen Z, Luo R, Zhao L, Xiao S, Fu ZF, Peng G. 2016. Structural basis for the dimerization and substrate recognition specificity of porcine epidemic diarrhea virus 3C-like protease. Virology 494: 225-235. https://doi.org/10.1016/j.virol.2016.04.018.
37. Chuck CP, Chong LT, Chen C, Chow HF, Wan DC, Wong KB. 2010. Profiling of substrate specificity of SARS-CoV 3CL. PLoS One 5:e13197. https://doi.org/10.1371/journal.pone.0013197.
38. Gotoh B, Takeuchi K, Komatsu T, Yokoo J. 2003. The STAT2 activation process is a crucial target of Sendai virus C protein for the blockade of alpha interferon signaling. J Virol 77:3360-3370. https://doi.org/10 .1128/JVI.77.6.3360-3370.2003.
39. Laurent-Rolle M, Morrison J, Rajsbaum R, Macleod JM, Pisanelli G, Pham A, Ayllon J, Miorin L, Martinez-Romero C, ten Oever BR, Garcia-Sastre A. 2014. The interferon signaling antagonist function of yellow fever virus NS5 protein is activated by type I interferon. Cell Host Microbe 16: 314-327. https://doi.org/10.1016/j.chom.2014.07.015.
40. Wathelet MG, Orr M, Frieman MB, Baric RS. 2007. Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81:11620-11633. https:// doi.org/10.1128/JVI.00702-07.
41. Frieman M, Yount B, Heise M, Kopecky-Bromberg SA, Palese P, Baric RS. 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. https:// doi.org/10.1128/JVI.01012-07.
42. Li SW, Lai CC, Ping JF, Tsai FJ, Wan L, Lin YJ, Kung SH, Lin CW. 2011. Severe acute respiratory syndrome coronavirus papain-like protease suppressed alpha interferon-induced responses through downregulation of extracellular signal-regulated kinase 1-mediated signalling pathways. J Gen Virol 92:1127-1140. https://doi.org/10.1099/vir.0.028936-0.
43. Wang D, Fang L, Shi Y, Zhang H, Gao L, Peng G, Chen H, Li K, Xiao S. 2015. Porcine epidemic diarrhea virus 3C-like protease regulates its interferon antagonism by cleaving NEMO. J Virol 90:2090-2101. https:// doi.org/10.1128/JVI.02514-15.
44. Wang D, Fang L, Wei D, Zhang H, Luo R, Chen H, Li K, Xiao S. 2014. Hepatitis A virus 3C protease cleaves NEMO to impair induction of beta interferon. J Virol 88:10252-10258. https://doi.org/10.1128/JVI.00869-14.
45. Wang D, Fang L, Li K, Zhong H, Fan J, Ouyang C, Zhang H, Duan E, Luo R, Zhang Z, Liu X, Chen H, Xiao S. 2012. Foot-and-mouth disease virus 3C protease cleaves NEMO to impair innate immune signaling. J Virol 86:9311-9322. https://doi.org/10.1128/JVI.00722-12.
46. Huang C, Zhang Q, Guo X, Yu Z, Xu A, Tang J, Feng W. 2014. Porcine reproductive and respiratory syndrome virus nonstructural protein 4 antagonizes beta interferon expression by targeting the NF-κB essential modulator. J Virol 88:10934-10945. https://doi.org/10.1128/JVI.01396-14.
47. Bhattacharya S, Eckner R, Grossman S, Oldread E, Arany Z, D'Andrea A, Livingston DM. 1996. Cooperation of Stat2 and p300/CBP in signalling induced by interferon-alpha. Nature 383:344-347. https://doi.org/10 .1038/383344a0.
48. Qureshi SA, Leung S, Kerr IM, Stark GR, Darnell JE, Jr. 1996. Function of Stat2 protein in transcriptional activation by alpha interferon. Mol Cell Biol 16:288-293. https://doi.org/10.1128/MCB.16.1.288.
49. Schindler C, Shuai K, Prezioso VR, Darnell JE, Jr. 1992. Interferondependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257:809-813. https://doi.org/10.1126/science .1496401.
50. Ziebuhr J, Snijder EJ, Gorbalenya AE. 2000. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81:853-879. https://doi.org/10.1099/0022-1317-81-4-853.
51. Hsu WC, Chang HC, Chou CY, Tsai PJ, Lin PI, Chang GG. 2005. Critical assessment of important regions in the subunit association and catalytic action of the severe acute respiratory syndrome coronavirus main protease. J Biol Chem 280:22741-22748. https://doi.org/10.1074/jbc .M502556200.
52. Jaru-Ampornpan P, Jengarn J, Wanitchang A, Jongkaewwattana A. 2017. Porcine epidemic diarrhea virus (PEDV) 3C-like protease-mediated nucleocapsid processing: a possible link to viral cell-culture adaptability. J Virol 91:e01660-16. https://doi.org/10.1128/JVI.01660-16.
53. Zhang Q, Shi K, Yoo D. 2016. Suppression of type I interferon production by porcine epidemic diarrhea virus and degradation of CREBbinding protein by nsp1. Virology 489:252-268. https://doi.org/10 .1016/j.virol.2015.12.010.
54. Ding Z, Fang L, Jing H, Zeng S, Wang D, Liu L, Zhang H, Luo R, Chen H, Xiao S. 2014. Porcine epidemic diarrhea virus nucleocapsid protein antagonizes beta interferon production by sequestering the interaction between IRF3 and TBK1. J Virol 88:8936-8945. https://doi.org/10.1128/ JVI.00700-14.
55. Xing Y, Chen J, Tu J, Zhang B, Chen X, Shi H, Baker SC, Feng L, Chen Z. 2013. The papain-like protease of porcine epidemic diarrhea virus negatively regulates type I interferon pathway by acting as a viral deubiquitinase. J Gen Virol 94:1554-1567. https://doi.org/10.1099/vir.0.051169-0.
56. Dong N, Fang L, Yang H, Liu H, Du T, Fang P, Wang D, Chen H, Xiao S. 2016. Isolation, genomic characterization, and pathogenicity of a Chinese porcine deltacoronavirus strain CHN-HN-2014. Vet Microbiol 196: 98-106. https://doi.org/10.1016/j.vetmic.2016.10.022.
57. Zhong H, Wang D, Fang L, Zhang H, Luo R, Shang M, Ouyang C, Ouyang H, Chen H, Xiao S. 2013. Ubiquitin-specific proteases 25 negatively regulates virus-induced type I interferon signaling. PLoS One 8:e80976. https://doi.org/10.1371/journal.pone.0080976.
58. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779-815. https://doi.org/10.1006/ jmbi.1993.1626.