Proteomic analysis for Type I interferon antagonism of Japanese encephalitis virus NS5 protein

Proteomics

Volumn 13, Issue 23-24, 2013, Pages 3442-3456

  Yang, Tsuey Ching ^a   Li, Shih Wein ^b   Lai, Chien Chen ^c,d   Lu, Kai Zen ^b   Chiu, Man Tzu ^b   Hsieh, Tsung Han ^b   Wan, Lei ^c   Lin, Cheng Wen ^b,e  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^e ASIA UNIVERSITY   (Taiwan)

Author keywords

Calreticulin; Interferon; Japanese encephalitis virus; Microbiology; Non structural protein 5; STAT1

Indexed keywords

BETA INTERFERON; CALRETICULIN; CHAPERONIN 60; CHAPERONIN CONTAINING TCP1; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IBETA; CYCLOPHILIN A; HEAT SHOCK PROTEIN 27; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; INOSINATE DEHYDROGENASE; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 4; MESSENGER RNA; NONSTRUCTURAL PROTEIN 5; PEROXIREDOXIN 1; PHOSPHOGLYCERATE DEHYDROGENASE; STAT1 PROTEIN; THIOREDOXIN; TRANSCRIPTION FACTOR NFAT;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELLULAR DISTRIBUTION; DOWN REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; JAPANESE ENCEPHALITIS VIRUS; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; UPREGULATION; VECTOR CONTROL; VIRUS REPLICATION;

CALRETICULIN; INTERFERON; JAPANESE ENCEPHALITIS VIRUS; MICROBIOLOGY; NON-STRUCTURAL PROTEIN 5; STAT1;

AMINO ACID SEQUENCE; ANIMALS; CALCINEURIN; CELL LINE; CELL LINE, TUMOR; CRICETINAE; CYCLOSPORINE; ENCEPHALITIS VIRUS, JAPANESE; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INTERFERON-BETA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; RESPONSE ELEMENTS; STAT1 TRANSCRIPTION FACTOR; TANDEM MASS SPECTROMETRY; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84890259450     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300001     Document Type: Article

References (48)

1. Burke, D. S., Monath, T. P., Flaviviruses, in: Fields, B. N., Knipe, D. M., Howley, P. M., Griffin, D. E. (Eds.), Fields Virology, Vol. 4, Lippincott Williams and Wilkins, Philadelphia, PA, 2001, pp. 1043-1125.
2. Lindenbach, B. D., Rice, C. M., Flaviviridae: the viruses and their replication, in: Knipe, D. M., Howley, P. M. (Eds.), Fields Virology, Vol. 4. Lippincott Williams & Wilkins, Philadelphia, PA, 2001, pp. 991-1041.
3. Kalita, J., Misra, U. K., Comparison of CT and MRI findings in the diagnosis of Japanese encephalitis. J. Neurol. Sci. 2000, 174, 3-8.
4. Misra, U. K., Kalita, J., Goel, D., Mathur, A., Clinical, radiological and neurophysiological spectrum of JEV encephalitis and other non-specific encephalitis during post-monsoon period in India. Neurol. India. 2003, 51, 55-59.
5. Liu, T. H., Liang, L. C., Wang, C. C., Liu, H. C., Chen, W. J., The blood-brain barrier in the cerebrum is the initial site for the Japanese encephalitis virus entering the central nervous system. J. Neurovirol. 2008, 14, 514-521.
6. Solomon, T. N., Dung, M. R., Kneen, R., Gainsborough, M. D., Vaughn, W., Khanh, V. T., Japanese encephalitis. J. Neurol. Neurosurg. Psychiatry 2000, 68, 405-415.
7. Tsai, T. F., Factors in the changing epidemiology of Japanese encephalitis and West Nile fever, in: Saluzzo, J. F., Dodet, B., eds. Factors in the Emergence of Arbovirus Diseases, Elselvier, Paris, 1997, pp. 179-189.
8. Park, G. S., Morris, K. L., Hallett, R. G., Bloom, M. E., Best, S. M., Identification of residues critical for the interferon antagonist function of Langat virus NS5 reveals a role for the RNA-dependent RNA polymerase domain. J. Virol. 2007, 81, 6936-6946.
9. Qi, W. B., Hua, R. H., Yan, L. P., Tong, G. Z. et al., Effective inhibition of Japanese encephalitis virus replication by small interfering RNAs targeting the NS5 gene. Virus Res. 2008, 132, 145-151.
10. Lin, R. J., Chang, B. L., Yu, H. P., Liao, C. L., Lin, Y. L., Blocking of interferon-induced Jak-Stat signaling by Japanese encephalitis virus NS5 through a protein tyrosine phosphatase-mediated mechanism. J. Virol. 2006, 80, 5908-5918.
11. Laurent-Rolle, M., Boer, E. F., Lubick, K. J., Wolfinbarger, J. B. et al., The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J. Virol. 2010, 84, 3503-3515.
12. Ashour, J., Laurent-Rolle, M., Shi, P. Y., García-Sastre, A., NS5 of dengue virus mediates STAT2 binding and degradation. J. Virol. 2009, 83, 5408-5418.
13. Mazzon, M., Jones, M., Davidson, A., Chain, B., Jacobs, M., Dengue virus NS5 inhibits interferon-alpha signaling by blocking signal transducer and activator of transcription 2 phosphorylation. J. Infect. Dis. 2009, 200, 1261-1270.
14. Best, S. M., Morris, K. L., Shannon, J. G., Robertson, S. J. et al., Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J. Virol. 2005, 79, 12828-12839.
15. Werme, K., Wigerius, M., Johansson, M., Tick-borne encephalitis virus NS5 associates with membrane protein scribble and impairs interferon-stimulated JAK-STAT signalling. Cell Microbiol. 2008, 10, 696-712.
16. Miller, C. A., Carrigan, D. R., Reversible repression and activation of measles virus infection in neural cells. Proc. Natl. Acad. Sci. USA 1982, 79, 1629-1633.
17. Ziegler, R. J., Stauffer, E. K., Mumps virus-induced alterations in cellular excitability during persistent infections. J. Gen. Virol. 1987, 68, 2501-2507.
18. Yang, T. C., Shiu, S. L., Chuang, P. H., Lin, Y. J. et al., Japanese encephalitis virus NS2B-NS3 protease induces caspase 3 activation and mitochondria-mediated apoptosis in human medulloblastoma cells. Virus Res. 2009, 143, 77-85.
19. Yang, T. C., Lai, C. C., Shiu, S. L., Chuang, P. H. et al., Japanese encephalitis virus down-regulates thioredoxin and induces ROS-mediated ASK1-ERK/p38 MAPK activation in human promonocyte cells. Microb. Infect. 2010, 12, 643-651.
20. Hsiao, N. W., Chen, J. W., Yang, T. C., Orloff, G. M. et al., ISG15 over-expression inhibits replication of the Japanese encephalitis virus in human medulloblastoma cells. Antivir. Res. 2010, 85, 504-511.
21. Lin, C. W., Lin, K. H., Lyu, P. C., Chen, W. J., Japanese encephalitis virus NS2B-NS3 protease binding to phage-displayed human brain proteins with the domain of trypsin inhibitor and basic region leucine zipper. Virus Res. 2006, 116, 106-113.
22. Li, S. W., Lai, C. C., Ping, J. F., Tsai, F. J. et al., 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. 2011, 92, 1127-1140.
23. Lin, C.W., Cheng, C.W., Yang, T.C., Li, S.W. et al., Interferon antagonist function of Japanese encephalitis virus NS4A and its interaction with DEAD-box RNA helicase DDX42. Virus Res. 2008, 137, 49-55.
24. Lai, C. C., Jou, M. J., Huang, S. Y., Li, S. W. et al., Proteomic analysis of up-regulated proteins in human promonocyte cells expressing severe acute respiratory syndrome coronavirus 3c-like protease. Proteomics 2007, 7, 1446-1460.
25. Tsang, K. W., Ho, P. L., Ooi, G. C., Yee, W. K. et al., A Cluster of Cases of Severe Acute Respiratory Syndrome in Hong Kong. N. Engl. J. Med. 2003, 348, 1977-1985.
26. Pryor, M. J., Rawlinson, S. M., Butcher, R. E., Barton, C. L. et al., Nuclear localization of dengue virus nonstructural protein 5 through its importin alpha/beta-recognized nuclear localization sequences is integral to viral infection. Traffic 2007, 8, 795-807.
27. Buckley, A., Gaidamovich, S., Turchinskaya, A., Gould, E. A., Monoclonal antibodies identify the NS5 yellow fever virus non-structural protein in the nuclei of infected cells. J. Gen. Virol. 1992, 73, 1125-1130.
28. Uchil, P. D., Kumar, A. V., Satchidanandam, V., Nuclear localization of flavivirus RNA synthesis in infected cells. J. Virol. 2006, 80, 5451-5464.
29. Groenendyk, J., Lynch, J., Michalak, M., Calreticulin, Ca2+, and calcineurin-signaling from the endoplasmic reticulum. Mol. Cells 2004, 17, 383-389.
30. Hermann-Kleiter, N., Baier, G., NFAT pulls the strings during CD4+ T helper cell effector functions. Blood 2010, 115, 2989-2997.
31. Moffatt, S. D., Cockman, M., Metcalfe, S. M., STAT 6 up-regulation by FK506 in the presence of interleukin-4. Transplantation 2000, 69, 1521-1523.
32. Woetmann, A., Nielsen, M., Christensen, S. T., Brockdorff, J. et al., Inhibition of protein phosphatase 2A induces serine/threonine phosphorylation, subcellular redistribution, and functional inhibition of STAT3. Proc. Natl. Acad. Sci. USA 1999, 96, 10620-10625.
33. Nakaya, T., Sato, M., Hata, N., Asagiri, M. et al., Gene induction pathways mediated by distinct IRFs during viral infection. Biochem. Biophys. Res. Commun. 2001, 283, 1150-1156.
34. Grandvaux, N., Servant, M. J., tenOever, B., Sen, G. C. et al., Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J. Virol. 2002, 76, 5532-5539.
35. Qing, M., Yang, F., Zhang, B., Zou, G. et al., Cyclosporine inhibits flavivirus replication through blocking the interaction between host cyclophilins and viral NS5 protein. Antimicrob. Agents Chemother. 2009, 53, 3226-3235.
36. Lynch, J., Michalak, M., Calreticulin is an upstream regulator of calcineurin. Biochem. Biophys. Res. Commun. 2003, 311, 1173-1179.
37. McCauliffe, D. P., Yang, Y. S., Wilson, J., Sontheimer, R. D., Capra, J. D., The 5'-flanking region of the human calreticulin gene shares homology with the human GRP78, GRP94, and protein disulfide isomerase promoters. J. Biol. Chem. 1992, 267, 2557-2562.
38. Waser, M., Mesaeli, N., Spencer, C., Michalak, M., Regulation of calreticulin gene expression by calcium. J. Cell Biol. 1997, 138, 547-557.
39. Keyes, L. R., Bego, M. G., Soland, M., St-Jeor, S., Cyclophilin A is required for efficient human cytomegalovirus DNA replication and reactivation. J. Gen. Virol. 2012, 93, 722-732.
40. Liu, J., Farmer, J. D., Jr., Lane, W. S., Friedman, J. et al., Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 1991, 66, 807-815.
41. Pfefferle, S., Schöpf, J., Kögl, M., Friedel, C. C. et al., The SARS-coronavirus-host interactome: identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog. 2011, 7, e1002331.
42. Li, W., Handschumacher, R. E., Identification of two calcineurin B-binding proteins: tubulin and heat shock protein 60. Biochim. Biophys. Acta 2002, 1599, 72-81.
43. Someren, J. S., Faber, L. E., Klein, J. D., Tumlin, J. A., Heat shock proteins 70 and 90 increase calcineurin activity in vitro through calmodulin-dependent and independent mechanisms. Biochem. Biophys. Res. Commun. 1999, 1260, 619-625.
44. Yue, X., Wang, H., Zhao, F., Liu, S. et al., Hepatitis B virus-induced calreticulin protein is involved in IFN resistance. J. Immunol. 2012, 189, 279-286.
45. Liu, Z., Yang, F., Robotham, J. M., Tang, H., Critical role of cyclophilin A and its prolyl-peptidyl isomerase activity in the structure and function of the hepatitis C virus replication complex. J. Virol. 2009, 83, 6554-6565.
46. Burch, A. D., Weller, S. K., Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone hsp90 for proper localization to the nucleus. J. Virol. 2005, 79, 10740-10749.
47. Stahl, M., Beck, J., Nassal, M., Chaperones activate hepadnavirus reverse transcriptase by transiently exposing a C-proximal region in the terminal protein domain that contributes to RNA binding. J. Virol. 2007, 81, 13354-13364.
48. He, H., Zhou, D., Fan, W., Fu, X. et al., Cyclophilin A inhibits rotavirus replication by facilitating host IFN-I production. Biochem. Biophys. Res. Commun. 2012, 422, 664-669.