Encephalomyocarditis Virus 3C protease relieves TRAF family member-associated NF-KB activator (TANK) inhibitory effect on TRAF6-mediated NF-KB Signaling through cleavage of TANK

Journal of Biological Chemistry

Volumn 290, Issue 46, 2015, Pages 27618-27632

  Huang, Li ^a   Liu, Qinfang ^a   Zhang, Lijie ^a   Zhang, Quan ^a,b   Hu, Liang ^a   Li, Changyao ^a   Wang, Shengnan ^a   Li, Jiangnan ^a   Zhang, Yuanfeng ^a   Yu, Huibin ^a   Wang, Yan ^a,c   Zhong, Zhaohua ^d   Xiong, Tao ^b   Xia, Xueshan ^c   Wang, Xiaojun ^a   Yu, Li ^a   Deng, Guohua ^a   Cai, Xuehui ^a   Cui, Shangjin ^a   Weng, Changjiang ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b YANGTZE UNIVERSITY   (China)

^c KUNMING UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; CHEMICAL ACTIVATION; SIGNALING; TANKS (CONTAINERS); VIRUSES;

B CELL RECEPTOR; CYSTEINE PROTEASE ACTIVITY; ENCEPHALOMYOCARDITIS VIRUS; FOOT-AND-MOUTH DISEASE VIRUS; INHIBITORY EFFECT; NEGATIVE REGULATORS; TOLL-LIKE RECEPTORS; VIRAL INFECTIONS;

CELL SIGNALING;

3C PROTEASE; GLUTAMINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEINASE; REGULATOR PROTEIN; TRAF FAMILY MEMBER ASSOCIATED NK KAPPAB ACTIVATOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VIRUS ENZYME; 3C PROTEASES; CYSTEINE PROTEINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TANK PROTEIN, HUMAN; VIRAL PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CARDIOVIRUS INFECTION; EMBRYO; ENCEPHALOMYOCARDITIS VIRUS; ENCEPHALOMYOCARDITIS VIRUS INFECTION; ENZYME ACTIVITY; ENZYME STABILITY; FOOT AND MOUTH DISEASE VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; VIRUS STRAIN; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; ENZYMOLOGY; EQUINE ARTERITIS VIRUS; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; PROTEIN DEGRADATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ARTERITIS VIRUS, EQUINE; CYSTEINE ENDOPEPTIDASES; ENCEPHALOMYOCARDITIS VIRUS; FOOT-AND-MOUTH DISEASE VIRUS; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; PROTEOLYSIS; TNF RECEPTOR-ASSOCIATED FACTOR 6; VIRAL PROTEINS;

EID: 84946924644     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.660761     Document Type: Article

References (55)

1. Carocci, M., and Bakkali-Kassimi, L. (2012) The encephalomyocarditis virus. Virulence 3, 351-367
2. Loughran, G., and Firth., A. E., and Atkins, J. F. (2011) Ribosomal frameshifting into an overlapping gene in the 2B-encoding region of the cardiovirus genome. Proc. Natl. Acad. Sci. U.S.A. 108, E1111-E1119
3. Ito, M., Yanagi, Y., and Ichinohe, T. (2012) Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLoS Pathog. 8, e1002857
4. Ng, C. S., Jogi, M., Yoo, J. S., Onomoto, K., Koike, S., Iwasaki, T., Yoneyama, M., Kato, H., and Fujita, T. (2013) Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J. Virol. 87, 9511-9522
5. Napetschnig, J., and Wu, H. (2013) Molecular basis of NF-KB signaling. Annu. Rev. Biophys. 42, 443-468
6. Kawai, T., and Akira, S. (2007) Signaling to NF-KB by Toll-like receptors. Trends Mol. Med. 13, 460-469
7. Israël, A. (2010) The IKK complex, a central regulator of NF-KB activation. Cold Spring Harb. Perspect. Biol. 2, a000158
8. Häcker, H., and Karin, M. (2006) Regulation and function of IKK and IKK-related kinases. Science's STKE 2006, re13
9. Sun, S. C. (2012) The noncanonical NF-KB pathway. Immunol. Rev. 246, 125-140
10. Chiu, Y. H., Zhao, M., and Chen, Z. J. (2009) Ubiquitin in NF-KB signaling. Chem. Rev. 109, 1549-1560
11. Cheng, G., and Baltimore, D. (1996) TANK, a co-inducer with TRAF2 of TNF- and CD 40L-mediated NF-KB activation. Genes Dev. 10, 963-973
12. Maruyama, K., Kawagoe, T., Kondo, T., Akira, S., and Takeuchi, O. (2012) TRAF family member-associated NF-KB activator (TANK) is a negative regulator of osteoclastogenesis and bone formation. J. Biol. Chem. 287, 29114-29124
13. Lomaga, M. A., Yeh, W. C, Sarosi, I., and Duncan., G. S., Furlonger, C, Ho, A., Morony, S., Capparelli, C, Van, G., Kaufman, S., van der Heiden, A., Itie, A., Wakeham, A., Khoo, W., Sasaki, T., et al. (1999) TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13, 1015-1024
14. Konno, H., Yamamoto, T., Yamazaki, K., Gohda, J., Akiyama, T., Semba, K., Goto, H., Kato, A., Yujiri, T., Imai, T., Kawaguchi, Y., Su, B., Takeuchi, O., Akira, S., Tsunetsugu-Yokota, Y., and Inoue, J. (2009) TRAF6 establishes innate immune responses by activating NF-KB and IRF7 upon sensing cytosolic viral RNA and DNA. PLoS One 4, e5674
15. Wu, H., and Arron, J. R. (2003) TRAF6, a molecular bridge spanning adaptive immunity, innate immunity and osteoimmunology. BioEssays 25, 1096-1105
16. Matsumura, T., Degawa, T., Takii, T., Hayashi, H., Okamoto, T., Inoue, J., and Onozaki, K. (2003) TRAF6-NF-KB pathway is essential for interleukin-1-induced TLR2 expression and its functional response to TLR2 li-gand in murine hepatocytes. Immunology 109, 127-136
17. Loiarro, M., Ruggiero, V., and Sette, C. Targeting TLR/IL-1R signalling in human diseases. Mediators Inflamm. 2010, 674363
18. Loiarro, M., Ruggiero, V., and Sette, C (2013) Targeting the Toll-like receptor/interleukin 1 receptor pathway in human diseases: rational design of MyD88 inhibitors. Clin. Lymphoma Myeloma Leuk. 13, 222-226
19. O'Neill, L. A. (2008) The interleukin-1 receptor/Toll-like receptor super-family: 10years of progress. Immunol. Rev. 226, 10-18
20. Oeckinghaus, A., and Hayden., M. S., and Ghosh, S. (2011) Crosstalk in NF-KB signaling pathways. Nat Immunol. 12, 695-708
21. Wang, Z., Liu, Y., Lin, W., and Cui, S. (2012) A real-time PCR to detect and analyze virulent EMCV loads in sows and piglets. Mol. Biol. Rep. 39, 10013-10017
22. Xue, M., Wang, H, Li, W., Zhou, G., Tu, Y., and Yu, L. (2012) Effects of amino acid substitutions in the VP2 B-C loop on antigenicity and pathogenicity of serotype Asia1 foot-and-mouth disease virus. Virol. J. 9, 191
23. Zhang, Y., Li, Z., Ge, X., Guo, X., and Yang, H. (2011) Autophagy promotes the replication of encephalomyocarditis virus in host cells. Autophagy 7, 613-628
24. Jiang, J., and Tang, H. (2010) Mechanism of inhibiting type I interferon induction by hepatitis B virus X protein. Protein Cell 1, 1106-1117
25. Lei, X., Liu, X., Ma, Y., Sun, Z., Yang, Y., Jin, Q., He, B., and 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
26. Lei, X., Sun, Z., Liu, X., Jin, Q., He, B., and 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
27. Wang, B., Xi, X., Lei, X., Zhang, X., Cui, S., Wang, J., Jin, Q., and Zhao, Z. (2013) Enterovirus 71 protease 2Apro targets MAVS to inhibit anti-viral type I interferon responses. PLoS Pathog. 9, e1003231
28. Weng, C, Li, Y., Xu, D., Shi, Y., and Tang, H. (2005) Specific cleavage of Mcl-1 by caspase-3 in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in Jurkat leukemia T cells. J. Biol. Chem. 280, 10491-10500
29. Li, D., Li, S., Sun, Y., Dong, H, Li, Y., Zhao, B., Guo, D., Weng, C, and Qiu, H. J. (2013) Poly(C)-binding protein 1, a novel N(pro)-interacting protein involved in classical swine fever virus growth. J. Virol. 87, 2072-2080
30. Lei, X., Xiao, X., Xue, Q., Jin, Q., He, B., and Wang, J. (2013) Cleavage of interferon regulatory factor 7 by enterovirus 71 3C suppresses cellular responses. J. Virol. 87, 1690-1698
31. Mukherjee, A., and Morosky., S. A., Delorme-Axford, E., Dybdahl-Sissoko, N., Oberste, M. S., Wang, T., and Coyne, C. B. (2011) The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog. 7, e1001311
32. Wang, D., Fang, L., Li, K., Zhong, H., Fan, J., Ouyang, C, Zhang, H., Duan, E., Luo, R., Zhang, Z., Liu, X., Chen, H., and Xiao, S. (2012) Foot-and-mouth disease virus 3C protease cleaves NEMO to impair innate immune signaling. J. Virol. 86, 9311-9322
33. Li, X. D., Sun, L., Seth, R. B., Pineda, G., and Chen, Z. J. (2005) Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc. Natl. Acad. Sci. U.S.A. 102, 17717-17722
34. Hall, D. J., and Palmenberg, A. C. (1996) Cleavage site mutations in the encephalomyocarditis virus P3 region lethally abrogate the normal processing cascade. J. Virol. 70, 5954-5961
35. Sun, J. Y., and Liu., M. Q., Xu, Y. L., Xu, Z. R., Pan, L., and Gao, H. (2005) Improvement of the thermostability and catalytic activity of a mesophilic family 11 xylanase by N-terminus replacement. Protein Expr. Purif. 42, 122-130
36. Jakus, P. B., Kalman, N., Antus, C, Radnai, B., Tucsek, Z., Gallyas, F., Jr., Sumegi, B., and Veres, B. (2013) TRAF6 is functional in inhibition of TLR4-mediated NF-KB activation by resveratrol. J. Nutr. Biochem. 24, 819-823
37. Kawagoe, T., Takeuchi, O., Takabatake, Y., Kato, H, Isaka, Y., Tsujimura, T., and Akira, S. (2009) TANK is a negative regulator of Toll-like receptor signaling and is critical for the prevention of autoimmune nephritis. Nat. Immunol. 10, 965-972
38. Chen, Z. J. (2012) Ubiquitination in signaling to and activation of IKK. Immunol. Rev. 246, 95-106
39. Fang, Y., and Snijder, E. J. (2010) The PRRSV replicase: exploring the multifunctionalityof an intriguing set of nonstructural proteins. Virus Res. 154, 61-76
40. Snijder, E. J., Kikkert, M., and Fang, Y. (2013) Arterivirus molecular biology and pathogenesis. J. Gen. Virol. 94, 2141-2163
41. Tian, X., Lu, G., Gao, F., Peng, H., Feng, Y., Ma, G., Bartlam, M., Tian, K., Yan, J., Hilgenfeld, R., and Gao, G. F. (2009) Structure and cleavage specificity of the chymotrypsin-like serine protease (3CLSP/Nsp4) of porcine reproductive and respiratory syndrome virus (PRRSV). J. Mol. Biol. 392, 977-993
42. Zaragoza, C, Saura, M., Padalko, E. Y., Lopez-Rivera, E., Lizarbe, T. R., Lamas, S., and Lowenstein, C. J. (2006) Viral protease cleavage of inhibitor of κBα triggers host cell apoptosis. Proc. Natl. Acad. Sci. U.S.A. 103, 19051-19056
43. Zhao, T., Yang, L., Sun, Q., Arguello, M., and Ballard., D. W., Hiscott, J., and Lin, R. (2007) The NEMO adaptor bridges the nuclear factor-κB and interferon regulatory factor signaling pathways. Nat. Immunol. 8, 592-600
44. Huang, C, Zhang, Q., Guo, X. K., Yu, Z. B., Xu, A. T., Tang, J., and Feng, W. H. (2014) Porcine reproductive and respiratory syndrome virus nonstructural protein 4 antagonizes beta interferon expression by targeting the NF-KB essential modulator. J. Virol. 88, 10934-10945
45. Barral, P. M., Sarkar, D., Fisher, P. B., and Racaniello, V. R. (2009) RIG-I is cleaved during picornavirus infection. Virology 391, 171-176
46. Kobayashi, M., Arias, C, Garabedian, A., Palmenberg, A. C, and Mohr, I. (2012) Site-specific cleavage of the host poly(A) binding protein by the encephalomyocarditis virus 3C proteinase stimulates viral replication. J. Virol. 86, 10686-10694
47. Sha, W. C, Liou, H. C, Tuomanen, E. I., and Baltimore, D. (1995) Targeted disruption of the p50 subunit of NF-KB leads to multifocal defects in immune responses. Cell 80, 321-330
48. Schwarz, E. M., Badorff, C, and Hiura., T. S., Wessely, R., Badorff, A., Verma, I.M., and Knowlton, K. U. (1998) NF-κB-mediated inhibition of apoptosis is required for encephalomyocarditis virus virulence: amechanism of resistance in p50 knockout mice. J. Virol. 72, 5654-5660
49. Rothe, M., Xiong, J., Shu, H. B., Williamson, K., Goddard, A., and Goeddel, D. V. (1996) I-TRAF is a novel TRAF-interacting protein that regulates TRAF-mediated signal transduction. Proc. Natl. Acad. Sci. U.S.A. 93, 8241-8246
50. Pomerantz, J. L., and Baltimore, D. (1999) NF-KB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBOJ. 18, 6694-6704
51. Bonif, M., and Meuwis., M. A., Close, P., Benoit, V., Heyninck, K., and Chapelle., J. P., Bours, V., Merville, M. P., Piette, J., Beyaert, R., and Chariot, A. (2006) TNFα- and IKKβ-mediated TANK/I-TRAF phosphorylation: implications for interaction with NEMO/IKK7 and NF-KB activation. Biochem. J. 394, 593-603
52. Gatot, J. S., Gioia, R., Chau, T. L., Patrascu, F., Warnier, M., Close, P., Chapelle, J. P., Muraille, E., Brown, K., Siebenlist, U., Piette, J., Dejardin, E., and Chariot, A. (2007) Lipopolysaccharide-mediated interferon regulatory factor activation involves TBK1-IKKe-dependent Lys(63)-linked polyubiquitination and phosphorylation of TANK/I-TRAF. J. Biol. Chem. 282, 31131-31146
53. Shi, H. X., Liu, X., Wang, Q., Tang, P. P., Liu, X. Y., Shan, Y. F., and Wang, C. (2011) Mitochondrial ubiquitin ligase MARCH5 promotes TLR7 signaling by attenuating TANK action. PLoS Pathog. 7, e1002057
54. Walsh, M. C, Kim, G. K., Maurizio, P. L., Molnar, E. E., and Choi, Y. (2008) TRAF6 autoubiquitination-independent activation of the NFkappaB and MAPK pathways in response to IL-1 and RANKL. PLoS One 3, e4064
55. Muroi, M., and Tanamoto, K. (2008) TRAF6 distinctively mediates MyD88- and IRAK-1-induced activation of NF-KB. J. Leukocyte Biol. 83, 702-707