Disruption of MDA5-mediated innate immune responses by the 3C proteins of coxsackievirus A16, coxsackievirus A6, and enterovirus D68

Journal of Virology

Volumn 91, Issue 13, 2017, Pages

  Rui, Yajuan ^a,b,c   Su, Jiaming ^a,b,c,d   Wang, Hong ^a   Chang, Junliang ^a   Wang, Shaohua ^a   Zheng, Wenwen ^a   Cai, Yong ^c   Wei, Wei ^a   Gordy, James T ^b   Markham, Richard ^b   Kong, Wei ^c   Zhang, Wenyan ^a   Yu, Xiao Fang ^a,b,d  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c JILIN UNIVERSITY   (China)

^d THE SECOND AFFILIATED HOSPITAL OF ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

3C protease; CV A16; CV A6; EV D68; HFMD; Innate immune response; MAVS; MDA5; TAK1

Indexed keywords

3C PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON INDUCED HELICASE C DOMAIN CONTAINING PROTEIN 1; RETINOIC ACID NDUCIBLE GENE I LIKE RECEPTOR; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG; VIRAL PROTEIN; 3C PROTEASES; CYSTEINE PROTEINASE; IFIH1 PROTEIN, HUMAN; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VISA PROTEIN, HUMAN;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; COXSACKIEVIRUS A16; COXSACKIEVIRUS A6; DISEASE ASSOCIATION; DISEASE SEVERITY; ENTEROVIRUS; ENTEROVIRUS D68; HAND FOOT AND MOUTH DISEASE; HUMAN; HUMAN CELL; IMMUNE EVASION; IMMUNOPRECIPITATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RESPIRATORY TRACT DISEASE; SIGNAL TRANSDUCTION; VIRUS LOAD; VIRUS STRAIN; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PROTEIN DEGRADATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CYSTEINE ENDOPEPTIDASES; ENTEROVIRUS; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; IMMUNITY, INNATE; INTERFERON-INDUCED HELICASE, IFIH1; MAP KINASE KINASE KINASES; PROTEOLYSIS; SIGNAL TRANSDUCTION; VIRAL PROTEINS;

EID: 85020396681     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00546-17     Document Type: Article

References (72)

1. McMinn PC. 2002. An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev 26:91-107. https://doi.org/10.1111/j.1574-6976.2002.tb00601.x
2. Qiu J. 2008. Enterovirus 71 infection: a new threat to global public health? Lancet Neurol 7:868-869. https://doi.org/10.1016/S1474-4422(08)70207-2
3. Bendig JW, Fleming DM. 1996. Epidemiological, virological, and clinical features of an epidemic of hand, foot, and mouth disease in England and Wales. Commun Dis Rep CDR Rev 6:R81-R86
4. Yen FB, Chang LY, Kao CL, Lee PI, Chen CM, Lee CY, Shao PL, Wang SC, Lu CY, Huang LM. 2009. Coxsackieviruses infection in northern Taiwan-epidemiology and clinical characteristics. J Microbiol Immunol Infect 42:38-46
5. Wang CY, Li Lu F, Wu MH, Lee CY, Huang LM. 2004. Fatal coxsackievirus A16 infection. Pediatr Infect Dis J 23:275-276. https://doi.org/10.1097/01.inf.0000115950.63906.78
6. Wright HT, Jr, Landing BH, Lennette EH, McAllister RM. 1963. Fatal infection in an infant associated with coxsackie virus group A, type. 16. N Engl J Med 268:1041-1044. https://doi.org/10.1056/NEJM196305092681904
7. Lancet Infectious Diseases. 2014. Enterovirus D68: the unexpected guest. Lancet Infect Dis 14:1023. https://doi.org/10.1016/S1473-3099(14)70968-5
8. Brown BA, Nix WA, Sheth M, Frace M, Oberste MS. 2014. Seven strains of enterovirus D68 detected in the United States during the 2014 severe respiratory disease outbreak. Genome Announc 2:e01201-14. https://doi .org/10.1128/genomeA.01201-14
9. Selvarangan R, Gerber SI, Midgley CM, Jackson MA, Turabelidze G, Obringer E, Johnson D, Giles BL, Patel A, Echols F. 2014. Severe respiratory illness associated with enterovirus D68-Missouri and Illinois, 2014. Am J Transplant 14:2662-2663. https://doi.org/10.1111/ajt.13035
10. Nelson R. 2014. Outbreaks of enterovirus D68 continue across the USA. Lancet Respir Med 2:791. https://doi.org/10.1016/S2213-2600(14)70190-0
11. Messacar K, Schreiner TL, Maloney JA, Wallace A, Ludke J, Oberste MS, Nix WA, Robinson CC, Glodé MP, Abzug MJ. 2015. A cluster of acute flaccid paralysis and cranial nerve dysfunction temporally associated with an outbreak of enterovirus D68 in children in Colorado, USA. Lancet 385:1662-1671. https://doi.org/10.1016/S0140-6736(14)62457-0
12. Oermann CM, Schuster JE, Conners GP, Newland JG, Selvarangan R, Jackson MA. 2015. Enterovirus D68. A focused review and clinical highlights from the 2014 U.S. outbreak. Ann Am Thorac Soc 12:775-781. https://doi.org/10.1513/AnnalsATS.201412-592FR
13. Sinclair C, Gaunt E, Simmonds P, Broomfield D, Nwafor N, Wellington L, Templeton K, Willocks L, Schofield O, Harvala H. 2014. Atypical hand, foot, and mouth disease associated with coxsackievirus A6 infection, Edinburgh, United Kingdom, January to February 2014. Euro Surveill 19:20745. https://doi.org/10.2807/1560-7917.ES2014.19.12.20745
14. Chong JH, Aan MK. 2014. An atypical dermatologic presentation of a child with hand, foot and mouth disease caused by coxsackievirus A6. Pediatr Infect Dis J 33:889. https://doi.org/10.1097/INF .0000000000000310
15. Downing C, Ramirez-Fort MK, Doan HQ, Benoist F, Oberste MS, Khan F, Tyring SK. 2014. Coxsackievirus A6 associated hand, foot and mouth disease in adults: clinical presentation and review of the literature. J Clin Virol 60:381-386. https://doi.org/10.1016/j.jcv.2014.04.023
16. Ben-Chetrit E, Wiener-Well Y, Shulman LM, Cohen MJ, Elinav H, Sofer D, Feldman I, Marva E, Wolf DG. 2014. Coxsackievirus A6-related hand foot and mouth disease: skin manifestations in a cluster of adult patients. J Clin Virol 59:201-203. https://doi.org/10.1016/j.jcv.2013.12.012
17. Feder HM, Jr, Bennett N, Modlin JF. 2014. Atypical hand, foot, and mouth disease: a vesiculobullous eruption caused by coxsackie virus A6. Lancet Infect Dis 14:83-86. https://doi.org/10.1016/S1473-3099(13)70264-0
18. Kawai T, Akira S. 2006. Innate immune recognition of viral infection. Nat Immunol 7:131-137. https://doi.org/10.1038/ni1303
19. Takeuchi O, Akira S. 2007. Recognition of viruses by innate immunity. Immunol Rev 220:214-224. https://doi.org/10.1111/j.1600-065X.2007 .00562.x
20. Wu J, Chen ZJ. 2014. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 32:461-488. https://doi.org/10.1146/annurev-immunol-032713-120156
21. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G. 2006. 5=-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997. https://doi.org/10.1126/science.1132505
22. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5=-phosphates. Science 314:997-1001. https://doi.org/10 .1126/science.1132998
23. Reikine S, Nguyen JB, Modis Y. 2014. Pattern recognition and signaling mechanisms of RIG-I and MDA5. Front Immunol 5:342. https://doi.org/10.3389/fimmu.2014.00342
24. Feng Q, Langereis MA, Olagnier D, Chiang C, van de Winkel R, van Essen P, Zoll J, Hiscott J, van Kuppeveld FJ. 2014. Coxsackievirus cloverleaf RNA containing a 5= triphosphate triggers an antiviral response via RIG-I activation. PLoS One 9:e95927. https://doi.org/10.1371/journal.pone .0095927
25. Feng Q, Hato SV, Langereis MA, Zoll J, Virgen-Slane R, Peisley A, Hur S, Semler BL, van Rij RP, van Kuppeveld FJ. 2012. MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep 2:1187-1196. https://doi.org/10.1016/j.celrep.2012.10.005
26. Takahasi K, Kumeta H, Tsuduki N, Narita R, Shigemoto T, Hirai R, Yoneyama M, Horiuchi M, Ogura K, Fujita T, Inagaki F. 2009. Solution structures of cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: identification of the RNA recognition loop in RIG-I-like receptors. J Biol Chem 284:17465-17474. https://doi.org/10.1074/jbc.M109.007179
27. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. 2005. IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat Immunol 6:981-988. https://doi.org/10 .1038/ni1243
28. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172. https://doi.org/10.1038/nature04193
29. Seth RB, Sun L, Ea CK, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NFkappaB and IRF 3. Cell 122:669-682. https://doi.org/10.1016/j.cell.2005 .08.012
30. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, Du F, Ren J, Wu YT, Grishin NV, Chen ZJ. 2015. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 347:aaa2630. https://doi.org/10.1126/science.aaa2630
31. Hayden MS, Ghosh S. 2008. Shared principles in NF-kappaB signaling. Cell 132:344-362. https://doi.org/10.1016/j.cell.2008.01.020
32. Li ML, Hsu TA, Chen TC, Chang SC, Lee JC, Chen CC, Stollar V, Shih SR. 2002. The 3C protease activity of enterovirus 71 induces human neural cell apoptosis. Virology 293:386-395. https://doi.org/10.1006/viro.2001 .1310
33. Shih SR, Chiang C, Chen TC, Wu CN, Hsu JT, Lee JC, Hwang MJ, Li ML, Chen GW, Ho MS. 2004. Mutations at KFRDI and VGK domains of enterovirus 71 3C protease affect its RNA binding and proteolytic activities. J Biomed Sci 11:239-248. https://doi.org/10.1007/BF02256567
34. Lei X, Han N, Xiao X, Jin Q, He B, Wang J. 2014. Enterovirus 71 3C inhibits cytokine expression through cleavage of the TAK1/TAB1/TAB2/TAB3 complex. J Virol 88:9830-9841. https://doi.org/10.1128/JVI.01425-14
35. Lei X, Liu X, Ma Y, Sun Z, Yang Y, Jin Q, He B, Wang J. 2010. The 3C protein of enterovirus 71 inhibits retinoid acid-inducible gene I-mediated interferon regulatory factor 3 activation and type I interferon responses. J Virol 84: 8051-8061. https://doi.org/10.1128/JVI.02491-09
36. Lei X, Sun Z, Liu X, Jin Q, He B, Wang J. 2011. Cleavage of the adaptor protein TRIF by enterovirus 71 3C inhibits antiviral responses mediated by Toll-like receptor 3. J Virol 85:8811-8818. https://doi.org/10.1128/JVI .00447-11
37. Lei X, Xiao X, Xue Q, Jin Q, He B, Wang J. 2013. Cleavage of interferon regulatory factor 7 by enterovirus 71 3C suppresses cellular responses. J Virol 87:1690-1698. https://doi.org/10.1128/JVI.01855-12
38. Wang H, Lei X, Xiao X, Yang C, Lu W, Huang Z, Leng Q, Jin Q, He B, Meng G, Wang J. 2015. Reciprocal regulation between enterovirus 71 and the NLRP3 inflammasome. Cell Rep 12:42-48. https://doi.org/10.1016/j .celrep.2015.05.047
39. Xiang Z, Liu L, Lei X, Zhou Z, He B, Wang J. 2016. 3C protease of enterovirus D68 inhibits cellular defense mediated by interferon regulatory factor 7. J Virol 90:1613-1621. https://doi.org/10.1128/JVI.02395-15
40. Xiang Z, Li L, Lei X, Zhou H, Zhou Z, He B, Wang J. 2014. Enterovirus 68 3C protease cleaves TRIF to attenuate antiviral responses mediated by Toll-like receptor 3. J Virol 88:6650-6659. https://doi.org/10.1128/JVI .03138-13
41. Strahle L, Garcin D, Le Mercier P, Schlaak JF, Kolakofsky D. 2003. Sendai virus targets inflammatory responses, as well as the interferon-induced antiviral state, in a multifaceted manner. J Virol 77:7903-7913. https://doi.org/10.1128/JVI.77.14.7903-7913.2003
42. Lin R, Heylbroeck C, Pitha PM, Hiscott J. 1998. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol Cell Biol 18:2986-2996. https://doi.org/10.1128/MCB.18.5.2986
43. Lu J, Yi L, Zhao J, Yu J, Chen Y, Lin MC, Kung HF, He ML. 2012. Enterovirus 71 disrupts interferon signaling by reducing the level of interferon receptor 1. J Virol 86:3767-3776. https://doi.org/10.1128/JVI.06687-11
44. Kräusslich HG, Nicklin MJ, Toyoda H, Etchison D, Wimmer E. 1987. Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4F polypeptide p220. J Virol 61:2711-2718
45. Liebig HD, Seipelt J, Vassilieva E, Gradi A, Kuechler E. 2002. A thermosensitive mutant of HRV2 2A proteinase: evidence for direct cleavage of eIF4GI and eIF4GII. FEBS Lett 523:53-57. https://doi.org/10.1016/S0014-5793(02)02933-2
46. Liebig HD, Ziegler E, Yan R, Hartmuth K, Klump H, Kowalski H, Blaas D, Sommergruber W, Frasel L, Lamphear B, Rhoads R, Kuechler E, Skern T. 1993. Purification of two picornaviral 2A proteinases: interaction with eIF-4 gamma and influence on in vitro translation. Biochemistry 32: 7581-7588. https://doi.org/10.1021/bi00080a033
47. Mukherjee A, Morosky SA, Delorme-Axford E, Dybdahl-Sissoko N, Oberste MS, Wang T, Coyne CB. 2011. The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog 7:e1001311. https://doi.org/10.1371/journal.ppat .1001311
48. Barral PM, Sarkar D, Fisher PB, Racaniello VR. 2009. RIG-I is cleaved during picornavirus infection. Virology 391:171-176. https://doi.org/10.1016/j .virol.2009.06.045
49. Barral PM, Morrison JM, Drahos J, Gupta P, Sarkar D, Fisher PB, Racaniello VR. 2007. MDA-5 is cleaved in poliovirus-infected cells. J Virol 81: 3677-3684. https://doi.org/10.1128/JVI.01360-06
50. Papon L, Oteiza A, Imaizumi T, Kato H, Brocchi E, Lawson TG, Akira S, Mechti N. 2009. The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology 393: 311-318. https://doi.org/10.1016/j.virol.2009.08.009
51. Huang L, Liu Q, Zhang L, Zhang Q, Hu L, Li C, Wang S, Li J, Zhang Y, Yu H, Wang Y, Zhong Z, Xiong T, Xia X, Wang X, Yu L, Deng G, Cai X, Cui S, Weng C. 2015. Encephalomyocarditis virus 3C protease relieves TRAF family member-associated NF-kappaB activator (TANK) inhibitory effect on TRAF6-mediated NF-kappaB signaling through cleavage of TANK. J Biol Chem 290:27618-27632. https://doi.org/10.1074/jbc.M115.660761
52. Feng Q, Langereis MA, Lork M, Nguyen M, Hato SV, Lanke K, Emdad L, Bhoopathi P, Fisher PB, Lloyd RE, van Kuppeveld FJ. 2014. Enterovirus 2Apro targets MDA5 and MAVS in infected cells. J Virol 88:3369-3378. https://doi.org/10.1128/JVI.02712-13
53. Wang B, Xi X, Lei X, Zhang X, Cui S, Wang J, Jin Q, Zhao Z. 2013. Enterovirus 71 protease 2Apro targets MAVS to inhibit anti-viral type I interferon responses. PLoS Pathog 9:e1003231. https://doi.org/10.1371/journal.ppat.1003231
54. Wang LC, Chen SO, Chang SP, Lee YP, Yu CK, Chen CL, Tseng PC, Hsieh CY, Chen SH. 2015. Enterovirus 71 proteins 2A and 3D antagonize the antiviral activity of gamma interferon via signaling attenuation. J Virol 89:7028-7037. https://doi.org/10.1128/JVI.00205-15
55. Liu Y, Zhang Z, Zhao X, Yu R, Zhang X, Wu S, Liu J, Chi X, Song X, Fu L, Yu Y, Hou L, Chen W. 2014. Enterovirus 71 inhibits cellular type I interferon signaling by downregulating JAK1 protein expression. Viral Immunol 27:267-276. https://doi.org/10.1089/vim.2013.0127
56. Lei X, Xiao X, Wang J. 2016. Innate immunity evasion by enteroviruses: insights into virus-host interaction. Viruses 8:E22. https://doi.org/10 .3390/v8010022
57. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao SM, Maniatis T. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4:491-496. https://doi.org/10.1038/ni921
58. 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. https://doi.org/10.1126/science.1081315
59. Xu L, Xiao N, Liu F, Ren H, Gu J. 2009. Inhibition of RIG-I and MDA5-dependent antiviral response by gC1qR at mitochondria. Proc Natl Acad Sci U S A 106:1530-1535. https://doi.org/10.1073/pnas.0811029106
60. Jiang X, Kinch LN, Brautigam CA, Chen X, Du F, Grishin NV, Chen ZJ. 2012. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36: 959-973. https://doi.org/10.1016/j.immuni.2012.03.022
61. Zhang W, Du J, Evans SL, Yu Y, Yu XF. 2012. T-cell differentiation factor CBF-beta regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481:376-379. https://doi.org/10.1038/nature10718
62. Berke IC, Modis Y. 2012. MDA5 cooperatively forms dimers and ATPsensitive filaments upon binding double-stranded RNA. EMBO J 31: 1714-1726. https://doi.org/10.1038/emboj.2012.19
63. Hou F, Sun L, Zheng H, Skaug B, Jiang QX, Chen ZJ. 2011. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146:448-461. https://doi.org/10.1016/j .cell.2011.06.041
64. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446:916-920. https://doi.org/10.1038/nature05732
65. Pham AM, Santa Maria FG, Lahiri T, Friedman E, Marie IJ, Levy DE. 2016. PKR transduces MDA5-dependent signals for type I IFN induction. PLoS Pathog 12:e1005489. https://doi.org/10.1371/journal.ppat.1005489
66. Wang S, Wang K, Lin R, Zheng C. 2013. Herpes simplex virus 1 serine/threonine kinase US3 hyperphosphorylates IRF3 and inhibits beta interferon production. J Virol 87:12814-12827. https://doi.org/10.1128/JVI .02355-13
67. Dai L, Thu CA, Liu XY, Xi J, Cheung PC. 2012. TAK1, more than just innate immunity. IUBMB Life 64:825-834. https://doi.org/10.1002/iub.1078
68. Abe Y, Fujii K, Nagata N, Takeuchi O, Akira S, Oshiumi H, Matsumoto M, Seya T, Koike S. 2012. The Toll-like receptor 3-mediated antiviral response is important for protection against poliovirus infection in poliovirus receptor transgenic mice. J Virol 86:185-194. https://doi.org/10 .1128/JVI.05245-11
69. Wang JP, Cerny A, Asher DR, Kurt-Jones EA, Bronson RT, Finberg RW. 2010. MDA5 and MAVS mediate type I interferon responses to coxsackie B virus. J Virol 84:254-260. https://doi.org/10.1128/JVI.00631-09
70. Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, Shimizu H. 2009. Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 15:794-797. https://doi.org/10.1038/nm.1961
71. Fan Y, Mao R, Yu Y, Liu S, Shi Z, Cheng J, Zhang H, An L, Zhao Y, Xu X, Chen Z, Kogiso M, Zhang D, Zhang H, Zhang P, Jung JU, Li X, Xu G, Yang J. 2014. USP21 negatively regulates antiviral response by acting as a RIG-I deubiquitinase. J Exp Med 211:313-328. https://doi.org/10.1084/jem.20122844
72. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493-497. https://doi.org/10.1093/oxfordjournals.aje.a118408