Identification of host proteins involved in japanese encephalitis virus infection by quantitative proteomics analysis

Journal of Proteome Research

Volumn 12, Issue 6, 2013, Pages 2666-2678

  Zhang, Lei Ke ^a   Chai, Fan ^a,b   Li, Hao Yu ^a   Xiao, Gengfu ^a,b   Guo, Lin ^a  

^a WUHAN UNIVERSITY   (China)

^b WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

IFITM3; Japanese encephalitis virus; quantitative proteomics; RANBP2; SAMD9; siRNA; STRING; VAMP8

Indexed keywords

INTERFERON INDUCED TRANSMEMBRANE PROTEIN 3; MEMBRANE PROTEIN; NUCLEAR PROTEIN; RAN BINDING PROTEIN 2; STERILE ALPHA MOTIF DOMAIN CONTAINING PROTEIN 9; UBIQUITIN; UNCLASSIFIED DRUG; VESICLE ASSOCIATED MEMBRANE PROTEIN 8;

ARTICLE; BIOINFORMATICS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; INTRACELLULAR MEMBRANE; JAPANESE ENCEPHALITIS; JAPANESE ENCEPHALITIS VIRUS; LIPID METABOLISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; VIRUS CELL INTERACTION; VIRUS REPLICATION; WESTERN BLOTTING;

JAPANESE ENCEPHALITIS VIRUS;

EID: 84879348793     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400011k     Document Type: Article

References (78)

1. Tsai, T. F. New initiatives for the control of Japanese encephalitis by vaccination: minutes of a WHO/CVI meeting, Bangkok, Thailand, 13-15 October 1998 Vaccine 2000, 18 (Suppl 2) 1-25
2. Misra, U. K.; Kalita, J. Overview: Japanese encephalitis Prog. Neurobiol. 2010, 91 (2) 108-20
3. van den Hurk, A. F.; Ritchie, S. A.; Mackenzie, J. S. Ecology and geographical expansion of Japanese encephalitis virus Annu. Rev. Entomol. 2009, 54, 17-35
4. Unni, S. K.; Ruzek, D.; Chhatbar, C.; Mishra, R.; Johri, M. K.; Singh, S. K. Japanese encephalitis virus: from genome to infectome Microbes Infect. 2011, 13 (4) 312-21
5. Mukhopadhyay, S.; Kuhn, R. J.; Rossmann, M. G. A structural perspective of the flavivirus life cycle Nat. Rev. Microbiol. 2005, 3 (1) 13-22
6. Smit, J. M.; Moesker, B.; Rodenhuis-Zybert, I.; Wilschut, J. Flavivirus cell entry and membrane fusion Viruses 2011, 3 (2) 160-71
7. Pastorino, B.; Nougairede, A.; Wurtz, N.; Gould, E.; de Lamballerie, X. Role of host cell factors in flavivirus infection: Implications for pathogenesis and development of antiviral drugs Antiviral Res. 2010, 87 (3) 281-94
8. Brinton, M. A. Host factors involved in West Nile virus replication Ann. N.Y. Acad. Sci. 2001, 951, 207-19
9. Ma-Lauer, Y.; Lei, J.; Hilgenfeld, R.; von Brunn, A. Virus-host interactomes-antiviral drug discovery Curr. Opin. Virol. 2012, 2 (5) 614-21
10. Munday, D. C.; Surtees, R.; Emmott, E.; Dove, B. K.; Digard, P.; Barr, J. N.; Whitehouse, A.; Matthews, D.; Hiscox, J. A. Using SILAC and quantitative proteomics to investigate the interactions between viral and host proteomes Proteomics 2012, 12 (4-5) 666-72
11. Pastorino, B.; Boucomont-Chapeaublanc, E.; Peyrefitte, C. N.; Belghazi, M.; Fusai, T.; Rogier, C.; Tolou, H. J.; Almeras, L. Identification of cellular proteome modifications in response to West Nile virus infection Mol. Cell. Proteomics 2009, 8 (7) 1623-37
12. Tchankouo-Nguetcheu, S.; Khun, H.; Pincet, L.; Roux, P.; Bahut, M.; Huerre, M.; Guette, C.; Choumet, V. Differential protein modulation in midguts of Aedes aegypti infected with chikungunya and dengue 2 viruses PLoS One 2010, 5 (10 e13149
13. Emmott, E.; Wise, H.; Loucaides, E. M.; Matthews, D. A.; Digard, P.; Hiscox, J. A. Quantitative proteomics using SILAC coupled to LC-MS/MS reveals changes in the nucleolar proteome in influenza A virus-infected cells J. Proteome Res. 2010, 9 (10) 5335-45
14. Coombs, K. M.; Berard, A.; Xu, W.; Krokhin, O.; Meng, X.; Cortens, J. P.; Kobasa, D.; Wilkins, J.; Brown, E. G. Quantitative proteomic analyses of influenza virus-infected cultured human lung cells J. Virol. 2010, 84 (20) 10888-906
15. Lam, Y. W.; Evans, V. C.; Heesom, K. J.; Lamond, A. I.; Matthews, D. A. Proteomics analysis of the nucleolus in adenovirus-infected cells Mol. Cell. Proteomics 2009, 9 (1) 117-30
16. Yu, J. L.; Guo, L. Quantitative proteomic analysis of Salmonella enterica serovar Typhimurium under PhoP/PhoQ activation conditions J. Proteome Res. 2011, 10 (7) 2992-3002
17. Jensen, L. J.; Kuhn, M.; Stark, M.; Chaffron, S.; Creevey, C.; Muller, J.; Doerks, T.; Julien, P.; Roth, A.; Simonovic, M.; Bork, P.; von Mering, C. STRING 8 - a global view on proteins and their functional interactions in 630 organisms Nucleic Acids Res. 2009, 37 (Database issue) D412-6
18. Lin, R. J.; Liao, C. L.; Lin, Y. L. Replication-incompetent virions of Japanese encephalitis virus trigger neuronal cell death by oxidative stress in a culture system J. Gen. Virol. 2004, 85 (Pt 2) 521-33
19. Konishi, E.; Mason, P. W. Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the premembrane protein J. Virol. 1993, 67 (3) 1672-5
20. Espada-Murao, L. A.; Morita, K. Delayed cytosolic exposure of Japanese encephalitis virus double-stranded RNA impedes interferon activation and enhances viral dissemination in porcine cells J. Virol. 2011, 85 (13) 6736-49
21. Himeda, T.; Hosomi, T.; Okuwa, T.; Muraki, Y.; Ohara, Y. Saffold virus type 3 (SAFV-3) persists in HeLa cells PLoS One 2013, 8 (1) e53194
22. Checkley, M. A.; Luttge, B. G.; Mercredi, P. Y.; Kyere, S. K.; Donlan, J.; Murakami, T.; Summers, M. F.; Cocklin, S.; Freed, E. O. Reevaluation of the requirement for TIP47 in Human Immunodeficiency Virus Type 1 envelope glycoprotein incorporation J. Virol. 2013, 87 (6) 3561-70
23. Netherton, C.; Moffat, K.; Brooks, E.; Wileman, T. A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication Adv. Virus Res. 2007, 70, 101-82
24. Mann, M. Functional and quantitative proteomics using SILAC Nat. Rev. Mol. Cell. Biol. 2006, 7 (12) 952-8
25. Brass, A. L.; Huang, I. C.; Benita, Y.; John, S. P.; Krishnan, M. N.; Feeley, E. M.; Ryan, B. J.; Weyer, J. L.; van der Weyden, L.; Fikrig, E.; Adams, D. J.; Xavier, R. J.; Farzan, M.; Elledge, S. J. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus Cell 2009, 139 (7) 1243-54
26. Munday, D. C.; Emmott, E.; Surtees, R.; Lardeau, C. H.; Wu, W.; Duprex, W. P.; Dove, B. K.; Barr, J. N.; Hiscox, J. A. Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus Mol. Cell. Proteomics 2010, 9 (11) 2438-59
27. Munday, D. C.; Hiscox, J. A.; Barr, J. N. Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus subgroup B using SILAC coupled to LC-MS/MS Proteomics 2010, 10 (23) 4320-34
28. Indraccolo, S.; Pfeffer, U.; Minuzzo, S.; Esposito, G.; Roni, V.; Mandruzzato, S.; Ferrari, N.; Anfosso, L.; Dell'Eva, R.; Noonan, D. M.; Chieco-Bianchi, L.; Albini, A.; Amadori, A. Identification of genes selectively regulated by IFNs in endothelial cells J. Immunol. 2007, 178 (2) 1122-35
29. Der, S. D.; Zhou, A.; Williams, B. R.; Silverman, R. H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (26) 15623-8
30. Hultcrantz, M.; Huhn, M. H.; Wolf, M.; Olsson, A.; Jacobson, S.; Williams, B. R.; Korsgren, O.; Flodstrom-Tullberg, M. Interferons induce an antiviral state in human pancreatic islet cells Virology 2007, 367 (1) 92-101
31. Lanford, R. E.; Guerra, B.; Lee, H.; Chavez, D.; Brasky, K. M.; Bigger, C. B. Genomic response to interferon-alpha in chimpanzees: implications of rapid downregulation for hepatitis C kinetics Hepatology 2006, 43 (5) 961-72
32. Rani, M. R.; Shrock, J.; Appachi, S.; Rudick, R. A.; Williams, B. R.; Ransohoff, R. M. Novel interferon-beta-induced gene expression in peripheral blood cells J. Leukocyte Biol. 2007, 82 (5) 1353-60
33. Schoggins, J. W.; Wilson, S. J.; Panis, M.; Murphy, M. Y.; Jones, C. T.; Bieniasz, P.; Rice, C. M. A diverse range of gene products are effectors of the type I interferon antiviral response Nature 2011, 472 (7344) 481-5
34. Zheng, X.; Hong, L.; Shi, L.; Guo, J.; Sun, Z.; Zhou, J. Proteomics analysis of host cells infected with infectious bursal disease virus Mol. Cell. Proteomics 2008, 7 (3) 612-25
35. Fan, H.; Ye, Y.; Luo, Y.; Tong, T.; Yan, G.; Liao, M. Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals protein and pathway regulation in Porcine Circovirus Type 2 infected PK-15 cells J. Proteome Res. 2011, 11 (2) 995-1008
36. Zhang, L.; Zhang, Z. P.; Zhang, X. E.; Lin, F. S.; Ge, F. Quantitative proteomics analysis reveals BAG3 as a potential target to suppress severe acute respiratory syndrome coronavirus replication J. Virol. 2010, 84 (12) 6050-9
37. Jiang, D.; Weidner, J. M.; Qing, M.; Pan, X. B.; Guo, H.; Xu, C.; Zhang, X.; Birk, A.; Chang, J.; Shi, P. Y.; Block, T. M.; Guo, J. T. Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections J. Virol. 2010, 84 (16) 8332-41
38. Liu, J.; Wennier, S.; Zhang, L.; McFadden, G. M062 is a host range factor essential for myxoma virus pathogenesis and functions as an antagonist of host SAMD9 in human cells J. Virol. 2011, 85 (7) 3270-82
39. Apcher, G. S.; Heink, S.; Zantopf, D.; Kloetzel, P. M.; Schmid, H. P.; Mayer, R. J.; Kruger, E. Human immunodeficiency virus-1 Tat protein interacts with distinct proteasomal alpha and beta subunits FEBS Lett. 2003, 553 (1-2) 200-4
40. Schaller, T.; Ocwieja, K. E.; Rasaiyaah, J.; Price, A. J.; Brady, T. L.; Roth, S. L.; Hue, S.; Fletcher, A. J.; Lee, K.; KewalRamani, V. N.; Noursadeghi, M.; Jenner, R. G.; James, L. C.; Bushman, F. D.; Towers, G. J. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency PLoS Pathog. 2011, 7 (12) e1002439
41. Kato, H.; Takeuchi, O.; Sato, S.; Yoneyama, M.; Yamamoto, M.; Matsui, K.; Uematsu, S.; Jung, A.; Kawai, T.; Ishii, K. J.; Yamaguchi, O.; Otsu, K.; Tsujimura, T.; Koh, C. S.; Reis e Sousa, C.; Matsuura, Y.; Fujita, T.; Akira, S. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature 2006, 441 (7089) 101-5
42. Pinto, A. K.; Daffis, S.; Brien, J. D.; Gainey, M. D.; Yokoyama, W. M.; Sheehan, K. C.; Murphy, K. M.; Schreiber, R. D.; Diamond, M. S. A temporal role of type I interferon signaling in CD8+ T cell maturation during acute West Nile virus infection PLoS Pathog. 2011, 7 (12) e1002407
43. Li, Y.; Li, C.; Xue, P.; Zhong, B.; Mao, A. P.; Ran, Y.; Chen, H.; Wang, Y. Y.; Yang, F.; Shu, H. B. ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (19) 7945-50
44. Chen, R.; Zhang, L.; Zhong, B.; Tan, B.; Liu, Y.; Shu, H. B. The ubiquitin-specific protease 17 is involved in virus-triggered type I IFN signaling Cell Res. 2010, 20 (7) 802-11
45. Zheng, J.; Sugrue, R. J.; Tang, K. Mass spectrometry based proteomic studies on viruses and hosts-a review Anal. Chim. Acta 2011, 702 (2) 149-59
46. Komarova, A. V.; Combredet, C.; Meyniel-Schicklin, L.; Chapelle, M.; Caignard, G.; Camadro, J. M.; Lotteau, V.; Vidalain, P. O.; Tangy, F. Proteomic analysis of virus-host interactions in an infectious context using recombinant viruses Mol. Cell. Proteomics 2011, 10 (12) M110 007443
47. Emmott, E.; Rodgers, M. A.; Macdonald, A.; McCrory, S.; Ajuh, P.; Hiscox, J. A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus Mol. Cell. Proteomics 2010, 9 (9) 1920-36
48. Gupta, N.; Santhosh, S. R.; Babu, J. P.; Parida, M. M.; Rao, P. V. Chemokine profiling of Japanese encephalitis virus-infected mouse neuroblastoma cells by microarray and real-time RT-PCR: implication in neuropathogenesis Virus Res. 2009, 147 (1) 107-12
49. Yang, Y.; Ye, J.; Yang, X.; Jiang, R.; Chen, H.; Cao, S. Japanese encephalitis virus infection induces changes of mRNA profile of mouse spleen and brain Virol. J. 2011, 8, 80
50. Ghazalpour, A.; Bennett, B.; Petyuk, V. A.; Orozco, L.; Hagopian, R.; Mungrue, I. N.; Farber, C. R.; Sinsheimer, J.; Kang, H. M.; Furlotte, N.; Park, C. C.; Wen, P. Z.; Brewer, H.; Weitz, K.; Camp, D. G., 2nd; Pan, C.; Yordanova, R.; Neuhaus, I.; Tilford, C.; Siemers, N.; Gargalovic, P.; Eskin, E.; Kirchgessner, T.; Smith, D. J.; Smith, R. D.; Lusis, A. J. Comparative analysis of proteome and transcriptome variation in mouse PLoS Genet. 2011, 7 (6) e1001393
51. Nie, L.; Wu, G.; Culley, D. E.; Scholten, J. C.; Zhang, W. Integrative analysis of transcriptomic and proteomic data: challenges, solutions and applications Crit. Rev. Biotechnol. 2007, 27 (2) 63-75
52. Takeuchi, O.; Akira, S. Innate immunity to virus infection Immunol. Rev. 2009, 227 (1) 75-86
53. Sadler, A. J.; Williams, B. R. Interferon-inducible antiviral effectors Nat. Rev. Immunol. 2008, 8 (7) 559-68
54. Biswas, N.; Wang, T.; Ding, M.; Tumne, A.; Chen, Y.; Wang, Q.; Gupta, P. ADAR1 is a novel multi targeted anti-HIV-1 cellular protein Virology 2011, 422 (2) 265-77
55. Pichlmair, A.; Lassnig, C.; Eberle, C. A.; Gorna, M. W.; Baumann, C. L.; Burkard, T. R.; Burckstummer, T.; Stefanovic, A.; Krieger, S.; Bennett, K. L.; Rulicke, T.; Weber, F.; Colinge, J.; Muller, M.; Superti-Furga, G. IFIT1 is an antiviral protein that recognizes 5′-triphosphate RNA Nat. Immunol. 2011, 12 (7) 624-30
56. Gao, G.; Guo, X.; Goff, S. P. Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein Science 2002, 297 (5587) 1703-6
57. Guo, X.; Carroll, J. W.; Macdonald, M. R.; Goff, S. P.; Gao, G. The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs J. Virol. 2004, 78 (23) 12781-7
58. Fitzpatrick, K.; Skasko, M.; Deerinck, T. J.; Crum, J.; Ellisman, M. H.; Guatelli, J. Direct restriction of virus release and incorporation of the interferon-induced protein BST-2 into HIV-1 particles PLoS Pathog. 2010, 6 (3) e1000701
59. Lu, J.; Pan, Q.; Rong, L.; He, W.; Liu, S. L.; Liang, C. The IFITM proteins inhibit HIV-1 infection J. Virol. 2010, 85 (5) 2126-37
60. Yao, L.; Dong, H.; Zhu, H.; Nelson, D.; Liu, C.; Lambiase, L.; Li, X. Identification of the IFITM3 gene as an inhibitor of hepatitis C viral translation in a stable STAT1 cell line J. Viral Hepat. 2011, 18 (10) e523-9
61. Yount, J. S.; Moltedo, B.; Yang, Y. Y.; Charron, G.; Moran, T. M.; Lopez, C. B.; Hang, H. C. Palmitoylome profiling reveals S-palmitoylation-dependent antiviral activity of IFITM3 Nat. Chem. Biol. 2010, 6 (8) 610-4
62. Tanaka, M.; Shimbo, T.; Kikuchi, Y.; Matsuda, M.; Kaneda, Y. Sterile alpha motif containing domain 9 is involved in death signaling of malignant glioma treated with inactivated Sendai virus particle (HVJ-E) or type I interferon Int. J. Cancer 2009, 126 (8) 1982-91
63. Viswanathan, K.; Fruh, K.; DeFilippis, V. Viral hijacking of the host ubiquitin system to evade interferon responses Curr. Opin. Microbiol. 2010, 13 (4) 517-23
64. Wimmer, P.; Schreiner, S.; Dobner, T. Human pathogens and the host cell SUMOylation system J. Virol. 2011, 86 (2) 642-54
65. Chiu, M. W.; Shih, H. M.; Yang, T. H.; Yang, Y. L. The type 2 dengue virus envelope protein interacts with small ubiquitin-like modifier-1 (SUMO-1) conjugating enzyme 9 (Ubc9) J. Biomed. Sci. 2007, 14 (3) 429-44
66. Fink, J.; Gu, F.; Ling, L.; Tolfvenstam, T.; Olfat, F.; Chin, K. C.; Aw, P.; George, J.; Kuznetsov, V. A.; Schreiber, M.; Vasudevan, S. G.; Hibberd, M. L. Host gene expression profiling of dengue virus infection in cell lines and patients PLoS Neglected Trop. Dis. 2007, 1 (2) e86
67. Kanlaya, R.; Pattanakitsakul, S. N.; Sinchaikul, S.; Chen, S. T.; Thongboonkerd, V. The ubiquitin-proteasome pathway is important for dengue virus infection in primary human endothelial cells J. Proteome Res. 2010, 9 (10) 4960-71
68. Khadka, S.; Vangeloff, A. D.; Zhang, C.; Siddavatam, P.; Heaton, N. S.; Wang, L.; Sengupta, R.; Sahasrabudhe, S.; Randall, G.; Gribskov, M.; Kuhn, R. J.; Perera, R.; LaCount, D. J. A physical interaction network of dengue virus and human proteins Mol. Cell. Proteomics 2011, 10 (12) M111 012187
69. Werner, A.; Flotho, A.; Melchior, F. The RanBP2/RanGAP1*SUMO1/Ubc9 complex is a multisubunit SUMO E3 ligase Mol. Cell 2012, 46 (3) 287-98
70. Welsch, S.; Miller, S.; Romero-Brey, I.; Merz, A.; Bleck, C. K.; Walther, P.; Fuller, S. D.; Antony, C.; Krijnse-Locker, J.; Bartenschlager, R. Composition and three-dimensional architecture of the dengue virus replication and assembly sites Cell Host Microbe 2009, 5 (4) 365-75
71. Miller, S.; Krijnse-Locker, J. Modification of intracellular membrane structures for virus replication Nat. Rev. Microbiol. 2008, 6 (5) 363-74
72. Gao, L.; Aizaki, H.; He, J. W.; Lai, M. M. Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft J. Virol. 2004, 78 (7) 3480-8
73. Helbig, K. J.; Eyre, N. S.; Yip, E.; Narayana, S.; Li, K.; Fiches, G.; McCartney, E. M.; Jangra, R. K.; Lemon, S. M.; Beard, M. R. The antiviral protein viperin inhibits hepatitis C virus replication via interaction with nonstructural protein 5A Hepatology 2011, 54 (5) 1506-17
74. Wong, S. H.; Zhang, T.; Xu, Y.; Subramaniam, V. N.; Griffiths, G.; Hong, W. Endobrevin, a novel synaptobrevin/VAMP-like protein preferentially associated with the early endosome Mol. Biol. Cell 1998, 9 (6) 1549-63
75. Lee, C. J.; Lin, H. R.; Liao, C. L.; Lin, Y. L. Cholesterol effectively blocks entry of flavivirus J. Virol. 2008, 82 (13) 6470-80
76. Mackenzie, J. M.; Khromykh, A. A.; Parton, R. G. Cholesterol manipulation by West Nile virus perturbs the cellular immune response Cell Host Microbe 2007, 2 (4) 229-39
77. Rodgers, M. A.; Villareal, V. A.; Schaefer, E. A.; Peng, L. F.; Corey, K. E.; Chung, R. T.; Yang, P. L. Lipid metabolite profiling identifies desmosterol metabolism as a new antiviral target for hepatitis C virus J. Am. Chem. Soc. 2012, 134 (16) 6896-9
78. Sharma, M.; Sasvari, Z.; Nagy, P. D. Inhibition of sterol biosynthesis reduces tombusvirus replication in yeast and plants J. Virol. 2009, 84 (5) 2270-81