Enterovirus 71 2C protein inhibits TNF-α-mediated activation of NF-κB by suppressing IκB kinase β phosphorylation

Journal of Immunology

Volumn 187, Issue 5, 2011, Pages 2202-2212

  Zheng, Zhenhua ^a   Li, Hongxia ^a   Zhang, Zhenfeng ^a   Meng, Jin ^a   Mao, Da ^a   Bai, Bingke ^b   Lu, Baojing ^c   Mao, Panyong ^b   Hu, Qinxue ^a   Wang, Hanzhong ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b BEIJING 302 HOSPITAL   (China)

^c ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 1; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PROTEIN 2C; TRANSCRIPTION FACTOR RELA; TUBULIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA BINDING; ENTEROVIRUS 71; ENZYME PHOSPHORYLATION; GEL MOBILITY SHIFT ASSAY; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; VIRUS INFECTION;

BLOTTING, WESTERN; CARRIER PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; ENZYME ACTIVATION; HEK293 CELLS; HELA CELLS; HUMANS; I-KAPPA B KINASE; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; NF-KAPPA B; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA; VIRAL NONSTRUCTURAL PROTEINS;

EID: 80052675403     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100285     Document Type: Article

References (68)

1. Bible, J. M., P. Pantelidis, P. K. Chan, and C. Y. Tong. 2007. Genetic evolution of enterovirus 71: epidemiological and pathological implications. Rev. Med. Virol. 17: 371-379. (Pubitemid 350144562)
2. Palacios, G., and M. S. Oberste. 2005. Enteroviruses as agents of emerging infectious diseases. J. Neurovirol. 11: 424-433. (Pubitemid 43064681)
3. Rodríguez, P. L., and L. Carrasco. 1995. Poliovirus protein 2C contains two regions involved in RNA binding activity. J. Biol. Chem. 270: 10105-10112.
4. Rodríguez, P. L., and L. Carrasco. 1993. Poliovirus protein 2C has ATPase and GTPase activities. J. Biol. Chem. 268: 8105-8110. (Pubitemid 23120393)
5. Echeverri, A., R. Banerjee, and A. Dasgupta. 1998. Amino-terminal region of poliovirus 2C protein is sufficient for membrane binding. Virus Res. 54: 217-223. (Pubitemid 28288964)
6. Echeverri, A. C., and A. Dasgupta. 1995. Amino terminal regions of poliovirus 2C protein mediate membrane binding. Virology 208: 540-553.
7. Banerjee, R., A. Echeverri, and A. Dasgupta. 1997. Poliovirus-encoded 2C polypeptide specifically binds to the 3′-terminal sequences of viral negative-strand RNA. J. Virol. 71: 9570-9578. (Pubitemid 27492404)
8. Racaniello, V. R. 2007. Picornaviridae: the viruses and their replication. In Fields Virology, 5th Ed. D. M. Knipe, and P. M. Howley, eds., eds. Lippincott Williams & Wilkins, Philadelphia, p. 796-839.
9. Tang, W. F., S. Y. Yang, B.W.Wu, J. R. Jheng, Y. L. Chen, C. H. Shih, K. H. Lin, H. C. Lai, P. Tang, and J. T. Horng. 2007. Reticulon 3 binds the 2C protein of enterovirus 71 and is required for viral replication. J. Biol. Chem. 282: 5888-5898. (Pubitemid 47093796)
10. Ghosh, S., M. J. May, and E. B. Kopp. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225-260. (Pubitemid 28183365)
11. Campbell, K. J., and N. D. Perkins. 2006. Regulation of NF-kappaB function. Biochem. Soc. Symp. 73: 165-180.
12. Baeuerle, P. A., and D. Baltimore. 1996. NF-kappa B: ten years after. Cell 87: 13-20.
13. Barkett, M., and T. D. Gilmore. 1999. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18: 6910-6924.
14. Pahl, H. L. 1999. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866.
15. Hiscott, J., T. L. Nguyen, M. Arguello, P. Nakhaei, and S. Paz. 2006. Manipulation of the nuclear factor-kappaB pathway and the innate immune response by viruses. Oncogene 25: 6844-6867. (Pubitemid 44657856)
16. Unterholzner, L., and A. G. Bowie. 2008. The interplay between viruses and innate immune signaling: recent insights and therapeutic opportunities. Biochem. Pharmacol. 75: 589-602.
17. Herbein, G., and W. A. O'Brien. 2000. Tumor necrosis factor (TNF)-alpha and TNF receptors in viral pathogenesis. Proc. Soc. Exp. Biol. Med. 223: 241-257. (Pubitemid 30337778)
18. Chen, G., and D. V. Goeddel. 2002. TNF-R1 signaling: a beautiful pathway. Science 296: 1634-1635. (Pubitemid 34579145)
19. Scheidereit, C. 2006. IkappaB kinase complexes: gateways to NF-kappaB activation and transcription. Oncogene 25: 6685-6705. (Pubitemid 44657846)
20. DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388: 548-554. (Pubitemid 27339997)
21. Mercurio, F., H. Y. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. W. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278: 860-866. (Pubitemid 27467923)
22. Hayden, M. S., and S. Ghosh. 2004. Signaling to NF-kappaB. Genes Dev. 18: 2195-2224.
23. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18: 621-663. (Pubitemid 30365393)
24. Chen, F., L. M. Demers, and X. Shi. 2002. Upstream signal transduction of NF-kappaB activation. Curr. Drug Targets Inflamm. Allergy 1: 137-149.
25. Zaragoza, C., M. Saura, E. Y. Padalko, E. Lopez-Rivera, T. R. Lizarbe, S. Lamas, and C. J. Lowenstein. 2006. Viral protease cleavage of inhibitor of kappaBalpha triggers host cell apoptosis. Proc. Natl. Acad. Sci. USA 103: 19051-19056. (Pubitemid 350002826)
26. De Los Santos, T., F. Diaz-San Segundo, and M. J. Grubman. 2007. Degradation of nuclear factor kappa B during foot-and-mouth disease virus infection. J. Virol. 81: 12803-12815. (Pubitemid 350156918)
27. Lin, T. Y., S. H. Hsia, Y. C. Huang, C. T. Wu, and L. Y. Chang. 2003. Proinflammatory cytokine reactions in enterovirus 71 infections of the central nervous system. Clin. Infect. Dis. 36: 269-274.
28. Lin, T. Y., L. Y. Chang, Y. C. Huang, K. H. Hsu, C. H. Chiu, and K. D. Yang. 2002. Different proinflammatory reactions in fatal and non-fatal enterovirus 71 infections: implications for early recognition and therapy. Acta Paediatr. 91: 632-635.
29. Chen, Z., Y. Sahashi, K. Matsuo, H. Asanuma, H. Takahashi, T. Iwasaki, Y. Suzuki, C. Aizawa, T. Kurata, and S.-i. Tamura. 1998. Comparison of the ability of viral protein-expressing plasmid DNAs to protect against influenza. Vaccine 16: 1544-1549. (Pubitemid 28366091)
30. Li, X., Y. Yang, and J. D. Ashwell. 2002. TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature 416: 345-347.
31. Park, K. A., H. S. Byun, M. Won, K.-J. Yang, S. Shin, L. Piao, J. M. Kim, W.-H. Yoon, E. Junn, J. Park, et al. 2007. Sustained activation of protein kinase C downregulates nuclear factor-kappaB signaling by dissociation of IKK-gamma and Hsp90 complex in human colonic epithelial cells. Carcinogenesis 28: 71-80. (Pubitemid 44942628)
32. Chen, C. S., Y. C. Yao, S. C. Lin, Y. P. Lee, Y. F. Wang, J. R. Wang, C. C. Liu, H. Y. Lei, and C. K. Yu. 2007. Retrograde axonal transport: a major transmission route of enterovirus 71 in mice. J. Virol. 81: 8996-9003.
33. Schmid, J. A., and A. Birbach. 2008. IkappaB kinase beta (IKKbeta/IKK2/IKBKB): a key molecule in signaling to the transcription factor NF-kappaB. Cytokine Growth Factor Rev. 19: 157-165. (Pubitemid 351382281)
34. Santoro, M. G., A. Rossi, and C. Amici. 2003. NF-kappaB and virus infection: who controls whom. EMBO J. 22: 2552-2560. (Pubitemid 36712353)
35. Taylor, S. L., N. Frias-Staheli, A. García-Sastre, and C. S. Schmaljohn. 2009. Hantaan virus nucleocapsid protein binds to importin alpha proteins and inhibits tumor necrosis factor alpha-induced activation of nuclear factor kappa B. J. Virol. 83: 1271-1279.
36. Shao, R. P., M. C. T. Hu, B. P. Zhou, S. Y. Lin, P. J. Chiao, R. H. Von Lindern, B. Spohn, and M. C. Hung. 1999. E1A sensitizes cells to tumor necrosis factor-induced apoptosis through inhibition of IkappaB kinases and nuclear factor kappaB activities. J. Biol. Chem. 274: 21495-21498.
37. Holloway, G., T. T. Truong, and B. S. Coulson. 2009. Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kappaB. J. Virol. 83: 4942-4951.
38. Graff, J. W., K. Ettayebi, and M. E. Hardy. 2009. Rotavirus NSP1 inhibits NFkappaB activation by inducing proteasome-dependent degradation of beta-TrCP: a novel mechanism of IFN antagonism. PLoS Pathog. 5: e1000280.
39. Tung, W. H., C. C. Sun, H. L. Hsieh, S. W. Wang, J. T. Horng, and C. M. Yang. 2007. EV71 induces VCAM-1 expression via PDGF receptor, PI3-K/Akt, p38 MAPK, JNK and NF-kappaB in vascular smooth muscle cells. Cell. Signal. 19: 2127-2137.
40. Tung, W. H., H. L. Hsieh, and C. M. Yang. 2010. Enterovirus 71 induces COX-2 expression via MAPKs, NF-kappaB, and AP-1 in SK-N-SH cells: role of PGE(2) in viral replication. Cell. Signal. 22: 234-246.
41. Tung, W. H., I. T. Lee, H. L. Hsieh, and C. M. Yang. 2010. EV71 induces COX-2 expression via c-Src/PDGFR/PI3K/Akt/p42/p44 MAPK/AP-1 and NF-kappaB in rat brain astrocytes. J. Cell. Physiol. 224: 376-386.
42. Neznanov, N., A. Kondratova, K. M. Chumakov, B. Angres, B. Zhumabayeva, V. I. Agol, and A. V. Gudkov. 2001. Poliovirus protein 3A inhibits tumor necrosis factor (TNF)-induced apoptosis by eliminating the TNF receptor from the cell surface. J. Virol. 75: 10409-10420. (Pubitemid 32948071)
43. Li, J. P., and D. Baltimore. 1990. An intragenic revertant of a poliovirus 2C mutant has an uncoating defect. J. Virol. 64: 1102-1107. (Pubitemid 20087747)
44. Cho, M. W., N. Teterina, D. Egger, K. Bienz, and E. Ehrenfeld. 1994. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells. Virology 202: 129-145. (Pubitemid 24241985)
45. Wimmer, E., C. U. Hellen, and X. Cao. 1993. Genetics of poliovirus. Annu. Rev. Genet. 27: 353-436. (Pubitemid 24011358)
46. Vance, L. M., N. Moscufo, M. Chow, and B. A. Heinz. 1997. Poliovirus 2C region functions during encapsidation of viral RNA. J. Virol. 71: 8759-8765. (Pubitemid 27446459)
47. Liu, Y., C. L. Wang, S. Mueller, A. V. Paul, E. Wimmer, and P. Jiang. 2010. Direct interaction between two viral proteins, the nonstructural protein 2C and the capsid protein VP3, is required for enterovirus morphogenesis. PLoS Pathog. 6: e1001066.
48. Liu, J., T. Wei, and J. Kwang. 2004. Avian encephalomyelitis virus nonstructural protein 2C induces apoptosis by activating cytochrome c/caspase-9 pathway. Virology 318: 169-182. (Pubitemid 38234271)
49. Karin, M. 2005. The IkappaB kinase (IKK) complex as a critical regulator of immune responses. Int. Congr. Ser. 1285: 97-103. (Pubitemid 43694177)
50. Perkins, N. D. 2006. Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene 25: 6717-6730. (Pubitemid 44657848)
51. Chen, Z. J. 2005. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 7: 758-765.
52. Krappmann, D., and C. Scheidereit. 2005. A pervasive role of ubiquitin conjugation in activation and termination of IkappaB kinase pathways. EMBO Rep. 6: 321-326. (Pubitemid 40561623)
53. Choi, S. H., K. J. Park, B. Y. Ahn, G. Jung, M. M. Lai, and S. B. Hwang. 2006. Hepatitis C virus nonstructural 5B protein regulates tumor necrosis factor alpha signaling through effects on cellular IkappaB kinase. Mol. Cell. Biol. 26: 3048-3059.
54. Chen, R. A. J., G. Ryzhakov, S. Cooray, F. Randow, and G. L. Smith. 2008. Inhibition of IkappaB kinase by vaccinia virus virulence factor B14. PLoS Pathog. 4: e22.
55. Nichols, D. B., and J. L. Shisler. 2006. The MC160 protein expressed by the dermatotropic poxvirus molluscum contagiosum virus prevents tumor necrosis factor alpha-induced NF-kappaB activation via inhibition of I kappa kinase complex formation. J. Virol. 80: 578-586. (Pubitemid 43062870)
56. Nichols, D. B., and J. L. Shisler. 2009. Poxvirus MC160 protein utilizes multiple mechanisms to inhibit NF-kappaB activation mediated via components of the tumor necrosis factor receptor 1 signal transduction pathway. J. Virol. 83: 3162-3174.
57. DiPerna, G., J. Stack, A. G. Bowie, A. Boyd, G. Kotwal, Z. Zhang, S. Arvikar, E. Latz, K. A. Fitzgerald, and W. L. Marshall. 2004. Poxvirus protein N1L targets the I-kappaB kinase complex, inhibits signaling to NF-kappaB by the tumor necrosis factor superfamily of receptors, and inhibits NF-kappaB and IRF3 signaling by Toll-like receptors. J. Biol. Chem. 279: 36570-36578. (Pubitemid 39129000)
58. Yin, M. J., Y. Yamamoto, and R. B. Gaynor. 1998. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature 396: 77-80. (Pubitemid 28520452)
59. Yamamoto, Y., M. J. Yin, K. M. Lin, and R. B. Gaynor. 1999. Sulindac inhibits activation of the NF-kappaB pathway. J. Biol. Chem. 274: 27307-27314.
60. Cárcamo, J. M., A. Pedraza, O. Bórquez-Ojeda, B. Zhang, R. Sanchez, and D. W. Golde. 2004. Vitamin C is a kinase inhibitor: dehydroascorbic acid inhibits IkappaBalpha kinase beta. Mol. Cell. Biol. 24: 6645-6652. (Pubitemid 38944344)
61. Jeon, K. I., J.-Y. Jeong, and D.-M. Jue. 2000. Thiol-reactive metal compounds inhibit NF-kappa B activation by blocking I kappa B kinase. J. Immunol. 164: 5981-5989. (Pubitemid 30389846)
62. Kwok, B. H., B. Koh, M. I. Ndubuisi, M. Elofsson, and C. M. Crews. 2001. The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IkappaB kinase. Chem. Biol. 8: 759-766. (Pubitemid 32752455)
63. Reynaert, N. L., A. Van der Vliet, A. S. Guala, T. McGovern, M. Hristova, C. Pantano, N. H. Heintz, J. Heim, Y. S. Ho, D. E. Matthews, et al. 2006. Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc. Natl. Acad. Sci. USA 103: 13086-13091. (Pubitemid 44338920)
64. Xu, G., Y.-C. Lo, Q. Li, G. Napolitano, X. Wu, X. Jiang, M. Dreano, M. Karin, and H. Wu. 2011. Crystal structure of inhibitor of κB kinase β. Nature 472: 325-330.
65. Li, H.-Y., H. Liu, C.-H. Wang, J.-Y. Zhang, J.-H. Man, Y.-F. Gao, P.-J. Zhang, W.-H. Li, J. Zhao, X. Pan, et al. 2008. Deactivation of the kinase IKK by CUEDC2 through recruitment of the phosphatase PP1. Nat. Immunol. 9: 533-541. (Pubitemid 351560522)
66. Cui, J., L. Zhu, X. Xia, H. Y. Wang, X. Legras, J. Hong, J. Ji, P. Shen, S. Zheng, Z. J. Chen, and R. F. Wang. 2010. NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways. Cell 141: 483-496.
67. Liu, J., and A. Lin. 2007. Wiring the cell signaling circuitry by the NF-kappa B and JNK1 crosstalk and its applications in human diseases. Oncogene 26: 3267-3278. (Pubitemid 46763020)
68. Lei, X., X. Liu, Y. Ma, Z. Sun, Y. Yang, Q. Jin, B. He, and J.Wang. 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.