The 3C protein of enterovirus 71 inhibits retinoid acid-inducible gene I-mediated interferon regulatory factor 3 activation and type I interferon responses

Journal of Virology

Volumn 84, Issue 16, 2010, Pages 8051-8061

  Lei, Xiaobo ^a   Liu, Xinlei ^a   Yijie, Ma ^b   Sun, Zhenmin ^a   Yang, Yaowu ^a   Jin, Qi ^a   He, Bin ^b   Wang, Jianwei ^a  

^a INSTITUTE OF PATHOGEN BIOLOGY   (China)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON A; B CELL ACTIVATING FACTOR RECEPTOR; BETA INTERFERON; CASPASE; INTERFERON; INTERFERON REGULATORY FACTOR 3; RETINOIC ACID INDUCIBLE PROTEIN I; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; DISEASE EXACERBATION; ENTEROVIRUS INFECTION; ENZYME ACTIVITY; GENETIC CODE; IMMUNIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TARGETING;

AMINO ACID SUBSTITUTION; DEAD-BOX RNA HELICASES; ENTEROVIRUS A, HUMAN; HUMANS; IMMUNE EVASION; IMMUNE TOLERANCE; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA; VIRAL PROTEINS; VIRULENCE FACTORS;

HUMAN ENTEROVIRUS 71; MAMMALIA; MURINAE;

EID: 77955006559     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02491-09     Document Type: Article

References (54)

1. AbuBakar, S., H. Y. Chee, M. F. Al-Kobaisi, J. Xiaoshan, K. B. Chua, and S. K. Lam. 1999. Identification of enterovirus 71 isolates from an outbreak of hand, foot and mouth disease (HFMD) with fatal cases of encephalomyelitis in Malaysia. Virus Res. 61:1-9.
2. AbuBakar, S., I. C. Sam, J. Yusof, M. K. Lim, S. Misbah, N. MatRahim, and P. S. Hooi. 2009. Enterovirus 71 outbreak, Brunei. Emerg. Infect. Dis. 15:79-82.
3. Alexander, J. P., Jr., L. Baden, M. A. Pallansch, and L. J. Anderson. 1994. Enterovirus 71 infections and neurologic disease-United States, 1977-1991. J. Infect. Dis. 169:905-908.
4. Barral, P. M., J. M. Morrison, J. Drahos, P. Gupta, D. Sarkar, P. B. Fisher, and V. R. Racaniello. 2007. MDA-5 is cleaved in poliovirus-infected cells. J. Virol. 81:3677-3684.
5. Barral, P. M., D. Sarkar, P. B. Fisher, and V. R. Racaniello. 2009. RIG-I is cleaved during picornavirus infection. Virology 391:171-176.
6. Barro, M., and J. T. Patton. 2005. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc. Natl. Acad. Sci. U. S. A. 102:4114-4119.
7. Chang, L. Y., L. M. Huang, S. S. Gau, Y. Y. Wu, S. H. Hsia, T. Y. Fan, K. L. Lin, Y. C. Huang, C. Y. Lu, and T. Y. Lin. 2007. Neurodevelopment and cognition in children after enterovirus 71 infection. N. Engl. J. Med. 356:1226-1234.
8. Chen, Y. C., C. K. Yu, Y. F. Wang, C. C. Liu, I. J. Su, and H. Y. Lei. 2004. A murine oral enterovirus 71 infection model with central nervous system involvement. J. Gen. Virol. 85:69-77.
9. Feng, Z. D., M. Cerveny, Z. Yan, and B. He. 2007. The VP35 protein of Ebola virus inhibits the antiviral effect mediated by double-stranded RNA dependent protein kinase PKR. J. Virol. 81:182-192.
10. 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. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491-496.
11. Gilbert, G. L., K. E. Dickson, M. J. Waters, M. L. Kennett, S. A. Land, and M. Sneddon. 1988. Outbreak of enterovirus 71 infection in Victoria, Australia, with a high incidence of neurologic involvement. Pediatr. Infect. Dis. J. 7:484-488.
12. Gitlin, L., W. Barchet, S. Gilfillan, M. Cella, B. Beutler, R. A. Flavell, M. S. Diamond, and M. Colonna. 2006. Essential role of MDA-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U. S. A. 103:8459-8464.
13. Hacker, H., V. Redecke, B. Blagoev, I. Kratchmarova, L. C. Hsu, G. G. Wang, M. P. Kamps, E. Raz, H. Wagner, G. Hacker, M. Mann, and M. Karin. 2006. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439:204-207. (Pubitemid 43083141)
14. Ho, M., E. R. Chen, K. H. Hsu, S. J. Twu, K. T. Chen, S. F. Tsai, J. R. Wang, and S. R. Shih. 1999. An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N. Engl. J. Med. 341:929-935.
15. Honda, K., S. Sakaguchi, C. Nakajima, A. Watanabe, H. Yanai, M. Matsumoto, T. Ohteki, T. Kaisho, A. Takaoka, S. Akira, T. Seya, and T. Taniguchi. 2003. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc. Natl. Acad. Sci. U. S. A. 100:10872-10877.
16. Hornung, V., J. Ellegast, S. Kim, K. Brzozka, A. Jung, H. Kato, H. Poeck, S. Akira, K. K. Conzelmann, M. Schlee, S. Endres, and G. Hartmann. 2006. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
17. Huang, C. C., C. C. Liu, Y. C. Chang, C. Y. Chen, S. T. Wang, and T. F. Yeh. 1999. Neurologic complications in children with enterovirus 71 infection. N. Engl. J. Med. 341:936-942.
18. Jiang, Z., T. W. Mak, G. Sen, and X. Li. 2004. Toll-like receptor 3-mediated activation of NF-κB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-β. Proc. Natl. Acad. Sci. U. S. A. 101:3533-3538.
19. Jiang, Z., M. Zamanian-Daryoush, H. Nie, A. M. Silva, B. R. Williams, and X. Li. 2003. Poly(I-C)-induced Toll-like receptor 3 (TLR3)-mediated activation of NFκB and MAP kinase is through an interleukin-1 receptor-associated kinase (IRAK)-independent pathway employing the signaling components TLR3-TRAF6-TAK1-TAB2-PKR. J. Biol. Chem. 278:16713-16719.
20. Kato, H., O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, K. Matsushita, A. Hiiragi, T. S. Dermody, T. Fujita, and S. Akira. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205:1601-1610.
21. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, O. Yamaguchi, K. Otsu, T. Tsujimura, C. S. Koh, C. Reis e Sousa, Y. Matsuura, T. Fujita, and S. Akira. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
22. Kawai, T., and S. Akira. 2006. Innate immune recognition of viral infection. Nat. Immunol. 7:131-137.
23. Kawai, T., K. Takahashi, S. Sato, C. Coban, H. Kumar, H. Kato, K. J. Ishii, O. Takeuchi, and S. Akira. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988.
24. Kehle, J., B. Roth, C. Metzger, A. Pfitzner, and G. Enders. 2003. Molecular characterization of an enterovirus 71 causing neurological disease in Germany. J. Neurovirol. 9:126-128. (Pubitemid 36372552)
25. Le Bon, A., and D. F. Tough. 2002. Links between innate and adaptive immunity via type I interferon. Curr. Opin. Immunol. 14:432-436.
26. Li, L., Y. He, H. Yang, J. Zhu, X. Xu, J. Dong, Y. Zhu, and Q. Jin. 2005. Genetic characteristics of human enterovirus 71 and coxsackievirus A16 circulating from 1999 to 2004 in Shenzhen, People's Republic of China. J. Clin. Microbiol. 43:3835-3839.
27. Li, M. L., T. A. Hsu, T. C. Chen, S. C. Chang, J. C. Lee, C. C. Chen, V. Stollar, and S. R. Shih. 2002. The 3C protease activity of enterovirus 71 induces human neural cell apoptosis. Virology 293:386-395.
28. Lin, Y. W., K. C. Chang, C. M. Kao, S. P. Chang, Y. Y. Tung, and S. H. Chen. 2009. Lymphocyte and antibody responses reduce enterovirus 71 lethality in mice by decreasing tissue viral loads. J. Virol. 83:6477-6483.
29. Liu, M. L., Y. P. Lee, Y. F. Wang, H. Y. Lei, C. C. Liu, S. M. Wang, I. J. Su, J. R. Wang, T. M. Yeh, S. H. Chen, and C. K. Yu. 2005. Type I interferons protect mice against enterovirus 71 infection. J. Gen. Virol. 86:3263-3269.
30. McMinn, P., K. Lindsay, D. Perera, H. M. Chan, K. P. Chan, and M. J. Cardosa. 2001. Phylogenetic analysis of enterovirus 71 strains isolated during linked epidemics in Malaysia, Singapore, and Western Australia. J. Virol. 75:7732-7738. (Pubitemid 32738033)
31. McMinn, P., I. Stratov, L. Nagarajan, and S. Davis. 2001. Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clin. Infect. Dis. 32:236-242.
32. McMinn, P. C. 2002. An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol. Rev. 26:91-107.
33. McWhirter, S. M., K. A. Fitzgerald, J. Rosains, D. C. Rowe, D. T. Golenbock, and T. Maniatis. 2004. IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 101:233-238.
34. 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)
35. Mibayashi, M., L. Martinez-Sobrido, Y. M. Loo, W. B. Cardenas, M. Gale, Jr., and A. Garcia-Sastre. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 81:514-524. (Pubitemid 46067878)
36. Oganesyan, G., S. K. Saha, B. Guo, J. Q. He, A. Shahangian, B. Zarnegar, A. Perry, and G. Cheng. 2006. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 439:208-211. (Pubitemid 43083142)
37. Oshiumi, H., M. Matsumoto, K. Funami, T. Akazawa, and T. Seya. 2003. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 4:161-167.
38. Papon, L., A. Oteiza, T. Imaizumi, H. Kato, E. Brocchi, T. G. Lawson, S. Akira, and N. Mechti. 2009. The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology 393:311-318.
39. Peters, K. L., H. L. Smith, G. R. Stark, and G. C. Sen. 2002. IRF-3-dependent, NFκB- and JNK-independent activation of the 561 and IFN-beta genes in response to double-stranded RNA. Proc. Natl. Acad. Sci. U. S. A. 99:6322-6327.
40. Pichlmair, A., O. Schulz, C. P. Tan, T. I. Naslund, P. Liljestrom, F. Weber, and C. Reis e Sousa. 2006. RIG-I-mediated antiviral responses to singlestranded RNA bearing 5′-phosphates. Science 314:997-1001.
41. Prins, K. C., W. B. Cardenas, and C. F. Basler. 2009. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKε and TBK-1. J. Virol. 83:3069-3077.
42. Qiu, J. 2008. Enterovirus 71 infection: a new threat to global public health? Lancet Neurol. 7:868-869.
43. Saito, T., D. M. Owen, F. Jiang, J. Marcotrigiao, and M. Gale, Jr. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454:523-527.
44. Selkirk, J. V., L. M. Nottebaum, I. C. Ford, M. Santos, S. Malany, A. C. Foster, and S. M. Lechner. 2006. A novel cell-based assay for G-protein-coupled receptor-mediated cyclic adenosine monophosphate response element binding protein phosphorylation. J. Biomol. Screen. 11:351-358.
45. Sharma, S., B. R. tenOever, N. Grandvaux, G. P. Zhou, R. Lin, and J. Hiscott. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148-1151.
46. Shih, S. R., C. Chiang, T. C. Chen, C. N. Wu, J. T. Hsu, J. C. Lee, M. J. Hwang, M. L. Li, G. W. Chen, and M. S. Ho. 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.
47. Sumpter, R., Jr., Y. M. Loo, E. Foy, K. Li, M. Yoneyama, T. Fujita, S. M. Lemon, and M. Gale, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-2699.
48. γ134.5 protein of herpes simplex virus 1. J. Biol. Chem. 284:1097-1105.
49. Vollstedt, S., S. Arnold, C. Schwerdel, M. Franchini, G. Alber, J. P. Di Santo, M. Ackermann, and M. Suter. 2004. Interplay between alpha/beta and gamma interferons with B, T, and natural killer cells in the defense against herpes simplex virus type 1. J. Virol. 78:3846-3850. (Pubitemid 38437190)
50. Weng, K. F., M. L. Li, C. T. Huang, and S. R. Shih. 2009. Enterovirus 71 3C protease cleaves a novel target CstF-64 and inhibits cellular polyadenylation. PLoS pathogens 5:e1000593.
51. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301:640-643. (Pubitemid 36927946)
52. Yang, F., L. Ren, Z. Xiong, J. Li, Y. Xiao, R. Zhao, Y. He, G. Bu, S. Zhou, J. Wang, and J. Qi. 2009. Enterovirus 71 outbreak in the People's Republic of China in 2008. J. Clin. Microbiol. 47:2351-2352.
53. Yang, Y., Y. Liang, L. Qu, Z. Chen, M. Yi, K. Li, and S. M. Lemon. 2007. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc. Natl. Acad. Sci. U. S. A. 104:7253-7258.
54. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737.