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

Molecular and Cellular Proteomics

Volumn 9, Issue 9, 2010, Pages 1920-1936

  Emmott, Edward ^a   Rodgers, Mark A ^a   Macdonald, Andrew ^a   McCrory, Sarah ^a   Ajuh, Paul ^b   Hiscox, Julian A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b Dundee Cell Products Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID DERIVATIVE; CYTOPLASM PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LUCIFERASE; MYOSIN VI; NUCLEAR PROTEIN; NUCLEOCAPSID PROTEIN; PROTEOME; TRANSCRIPTION FACTOR AP 1; VIMENTIN; VIRUS PROTEIN;

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; AVIAN INFECTIOUS BRONCHITIS VIRUS; CELL COMPARTMENTALIZATION; CELL FRACTIONATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORONAVIRUS; CYTOPLASM; CYTOSKELETON; IMMUNOFLUORESCENCE; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEOMICS; QUANTITATIVE ANALYSIS; REPORTER GENE; RNA VIRUS; UPREGULATION; VALIDATION PROCESS; VERO CELL; VIRUS CELL INTERACTION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; CELL NUCLEOLUS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CHROMATOGRAPHY, LIQUID; CYTOPLASM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; INFECTIOUS BRONCHITIS VIRUS; ISOTOPE LABELING; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PROTEOMICS; TANDEM MASS SPECTROMETRY; VERO CELLS; VIRAL PROTEINS;

AVIAN INFECTIOUS BRONCHITIS VIRUS; CORONAVIRUS; RNA VIRUSES;

EID: 77956497028     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M900345-MCP200     Document Type: Article

References (85)

1. Dove, B., Brooks, G., Bicknell, K., Wurm, T., and Hiscox, J. A. (2006) Cell cycle perturbations induced by infection with the coronavirus infectious bronchitis virus and their effect on virus replication. J. Virol. 80, 4147-4156
2. Chen, C. J., and Makino, S. (2004) Murine coronavirus replication induces cell cycle arrest in G0/G1 phase. J. Virol. 78, 5658-5669
3. Chen, C. J., Sugiyama, K., Kubo, H., Huang, C., and Makino, S. (2004) Murine coronavirus nonstructural protein p28 arrests cell cycle in G0/G1 phase. J. Virol. 78, 10410-10419
4. Li, F. Q., Tam, J. P., and Liu, D. X. (2007) Cell cycle arrest and apoptosis induced by the coronavirus infectious bronchitis virus in the absence of p53. Virology 365, 435-445
5. Belyavsky, M., Belyavskaya, E., Levy, G. A., and Leibowitz, J. L. (1998) Coronavirus MHV-3-induced apoptosis in macrophages. Virology 250, 41-49
6. Eleouet, J. F., Chilmonczyk, S., Besnardeau, L., and Laude, H. (1998) Transmissible gastroenteritis coronavirus induces programmed cell death in infected cells through a caspase-dependent pathway. J. Virol. 72, 4918-4924
7. Versteeg, G. A., Slobodskaya, O., and Spaan, W. J. (2006) Transcriptional profiling of acute cytopathic murine hepatitis virus infection in fibroblast-like cells. J. Gen. Virol. 87, 1961-1975
8. Whitman, L., Zhou, H., Perlman, S., and Lane, T. E. (2009) IFN-gamma-mediated suppression of coronavirus replication in glial-committed progenitor cells. Virology 384, 209-215
9. Tohya, Y., Narayanan, K., Kamitani, W., Huang, C., Lokugamage, K., and Makino, S. (2009) Suppression of host gene expression by nsp1 proteins of group 2 bat coronaviruses. J. Virol. 83, 5282-5288
10. Peiris, J. S., Guan, Y., and Yuen, K. Y. (2004) Severe acute respiratory syndrome. Nat. Med. 10, S88-S97
11. Cavanagh, D. (2005) Coronaviruses in poultry and other birds. Avian Pathol. 34, 439-448
12. Sawicki, S. G., Sawicki, D. L., and Siddell, S. G. (2007) A contemporary view of coronavirus transcription. J. Virol. 81, 20-29
13. van Hemert, M. J., van den Worm, S. H., Knoops, K., Mommaas, A. M., Gorbalenya, A. E., and Snijder, E. J. (2008) SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathog. 4, e1000054
14. Prentice, E., Jerome, W. G., Yoshimori, T., Mizushima, N., and Denison, M. R. (2004) Coronavirus replication complex formation utilizes components of cellular autophagy. J. Biol. Chem. 279, 10136-10141
15. de Haan, C. A., and Reggiori, F. (2008) Are nidoviruses hijacking the autophagy machinery? Autophagy 4, 276-279
16. Bost, A. G., Prentice, E., and Denison, M. R. (2001) Mouse hepatitis virus replicase protein complexes are translocated to sites of M protein accumulation in the ERGIC at late times of infection. Virology 285, 21-29
17. Cawood, R., Harrison, S. M., Dove, B. K., Reed, M. L., and Hiscox, J. A. (2007) Cell cycle dependent nucleolar localization of the coronavirus nucleocapsid protein. Cell Cycle 6, 863-867
18. Freundt, E. C., Yu, L., Park, E., Lenardo, M. J., and Xu, X. N. (2009) Molecular determinants for subcellular localization of the severe acute respiratory syndrome coronavirus open reading frame 3b protein. J. Virol. 83, 6631-6640
19. Spencer, K. A., Dee, M., Britton, P., and Hiscox, J. A. (2008) Role of phosphorylation clusters in the biology of the coronavirus infectious bronchitis virus nucleocapsid protein. Virology 370, 373-381
20. Spencer, K. A., and Hiscox, J. A. (2006) Characterisation of the RNA binding properties of the coronavirus infectious bronchitis virus nucleocapsid protein amino-terminal region. FEBS Lett. 580, 5993-5998
21. Chen, H., Gill, A., Dove, B. K., Emmett, S. R., Kemp, C. F., Ritchie, M. A., Dee, M., and Hiscox, J. A. (2005) Mass spectroscopic characterisation of the coronavirus infectious bronchitis virus nucleoprotein and elucidation of the role of phosphorylation in RNA binding using surface plasmon resonance. J. Virol. 79, 1164-1179
22. Zúñiga, S., Sola, I., Moreno, J. L., Sabella, P., Plana-Durán, J., and Enjuanes, L. (2007) Coronavirus nucleocapsid protein is an RNA chaperone. Virology 357, 215-227 (Pubitemid 44830061)
23. Hiscox, J. A. (2007) RNA viruses: hijacking the dynamic nucleolus. Nat. Rev. Microbiol. 5, 119-127
24. Hiscox, J. A. (2002) Brief review: the nucleolus - a gateway to viral infection? Arch. Virol. 147, 1077-1089
25. Greco, A. (2009) Involvement of the nucleolus in replication of human viruses. Rev. Med. Virol. 19, 201-214
26. Jiang, X. S., Tang, L. Y., Dai, J., Zhou, H., Li, S. J., Xia, Q. C., Wu, J. R., and Zeng, R. (2005) Quantitative analysis of severe acute respiratory syndrome (SARS)-associated coronavirus-infected cells using proteomic approaches: implications for cellular responses to virus infection. Mol. Cell. Proteomics 4, 902-913 (Pubitemid 41309148)
27. Yount, B., Curtis, K. M., Fritz, E. A., Hensley, L. E., Jahrling, P. B., Prentice, E., Denison, M. R., Geisbert, T. W., and Baric, R. S. (2003) Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. U.S.A. 100, 12995-13000 (Pubitemid 37340014)
28. Batonick, M., Oomens, A. G., and Wertz, G. W. (2008) Human respiratory syncytial virus glycoproteins are not required for apical targeting and release from polarized epithelial cells. J. Virol. 82, 8664-8672
29. Dauber, B., Heins, G., and Wolff, T. (2004) The influenza B virus nonstructural NS1 protein is essential for efficient viral growth and antagonizes beta interferon induction. J. Virol. 78, 1865-1872 (Pubitemid 38176718)
30. Carlos, T. S., Young, D. F., Schneider, M., Simas, J. P., and Randall, R. E. (2009) Parainfluenza virus 5 genomes are located in viral cytoplasmic bodies whilst the virus dismantles the interferon-induced antiviral state of cells. J. Gen. Virol. 90, 2147-2156
31. Molestina, R. E., and Sinai, A. P. (2005) Host and parasite-derived IKK activities direct distinct temporal phases of NF-kappaB activation and target gene expression following Toxoplasma gondii infection. J. Cell Sci. 118, 5785-5796
32. Hsu, J. T., Kuo, C. J., Hsieh, H. P., Wang, Y. C., Huang, K. K., Lin, C. P., Huang, P. F., Chen, X., and Liang, P. H. (2004) Evaluation of metal-conjugated compounds as inhibitors of 3CL protease of SARS-CoV. FEBS Lett. 574, 116-120
33. Keitel, W. A., Dekker, C. L., Mink, C., Campbell, J. D., Edwards, K. M., Patel, S. M., Ho, D. Y., Talbot, H. K., Guo, K., Noah, D. L., and Hill, H. (2009) Safety and immunogenicity of inactivated, Vero cell culture-derived whole virus influenza A/H5N1 vaccine given alone or with aluminum hydroxide adjuvant in healthy adults. Vaccine 27, 6642-6648
34. Andersen, J. S., Lyon, C. E., Fox, A. H., Leung, A. K., Lam, Y. W., Steen, H., Mann, M., and Lamond, A. I. (2002) Directed proteomic analysis of the human nucleolus. Curr. Biol. 12, 1-11 (Pubitemid 34063348)
35. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (Pubitemid 26101214)
36. Olsen, J. V., de Godoy, L. M., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S., and Mann, M. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021
37. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
38. Emmott, E., Dove, B. K., Howell, G., Chappell, L. A., Reed, M. L., Boyne, J. R., You, J. H., Brooks, G., Whitehouse, A., and Hiscox, J. A. (2008) Viral nucleolar localisation signals determine dynamic trafficking within the nucleolus. Virology 380, 191-202
39. Mann, M. (2006) Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 7, 952-958
40. Skiba, M., Mettenleiter, T. C., and Karger, A. (2008) Quantitative whole-cell proteome analysis of pseudorabies virus-infected cells. J. Virol. 82, 9689-9699
41. Li, D., and Cavanagh, D. (1992) Coronavirus IBV-induced membrane fusion occurs at near-neutral pH. Arch. Virol. 122, 307-316
42. Fang, X., Gao, J., Zheng, H., Li, B., Kong, L., Zhang, Y., Wang, W., Zeng, Y., and Ye, L. (2007) The membrane protein of SARS-CoV suppresses NF-kappaB activation. J. Med. Virol. 79, 1431-1439
43. Wang, W., Ye, L., Ye, L., Li, B., Gao, B., Zeng, Y., Kong, L., Fang, X., Zheng, H., Wu, Z., and She, Y. (2007) Up-regulation of IL-6 and TNF-alpha induced by SARS-coronavirus spike protein in murine macrophages via NF-kappaB pathway. Virus Res. 128, 1-8
44. Kopecky-Bromberg, S. A., Martínez-Sobrido, L., Frieman, M., Baric, R. A., and Palese, P. (2007) Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J. Virol. 81, 548-557
45. Shaulian, E., and Karin, M. (2002) AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4, E131-E136
46. Parcellier, A., Schmitt, E., Gurbuxani, S., Seigneurin-Berny, D., Pance, A., Chantôme, A., Plenchette, S., Khochbin, S., Solary, E., and Garrido, C. (2003) HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol. Cell. Biol. 23, 5790-5802
47. De, A. K., Kodys, K. M., Yeh, B. S., and Miller-Graziano, C. (2000) Exaggerated human monocyte IL-10 concomitant to minimal TNF-alpha induction by heat-shock protein 27 (Hsp27) suggests Hsp27 is primarily an antiinflammatory stimulus. J. Immunol. 165, 3951-3958
48. Alford, K. A., Glennie, S., Turrell, B. R., Rawlinson, L., Saklatvala, J., and Dean, J. L. (2007) Heat shock protein 27 functions in inflammatory gene expression and transforming growth factor-beta-activated kinase-1 (TAK1)-mediated signaling. J. Biol. Chem. 282, 6232-6241
49. Aschenbrenner, L., Lee, T., and Hasson, T. (2003) Myo6 facilitates the translocation of endocytic vesicles from cell peripheries. Mol. Biol. Cell 14, 2728-2743
50. Hertzano, R., Shalit, E., Rzadzinska, A. K., Dror, A. A., Song, L., Ron, U., Tan, J. T., Shitrit, A. S., Fuchs, H., Hasson, T., Ben-Tal, N., Sweeney, H. L., de Angelis, M. H., Steel, K. P., and Avraham, K. B. (2008) A Myo6 mutation destroys coordination between the myosin heads, revealing new functions of myosin VI in the stereocilia of mammalian inner ear hair cells. PLoS Genet. 4, e1000207
51. Dove, B. K., You, J. H., Reed, M. L., Emmett, S. R., Brooks, G., and Hiscox, J. A. (2006) Changes in nucleolar morphology and proteins during infection with the coronavirus infectious bronchitis virus. Cell. Microbiol. 8, 1147-1157
52. Lam, Y. W., Evans, V. C., Heesom, K. J., Lamond, A. I., and Matthews, D. A. (2010) Proteomics analysis of the nucleolus in adenovirus-infected cells. Mol. Cell. Proteomics 9, 117-130
53. Mannová, P., Fang, R., Wang, H., Deng, B., McIntosh, M. W., Hanash, S. M., and Beretta, L. (2006) Modification of host lipid raft proteome upon hepatitis C virus replication. Mol. Cell. Proteomics 5, 2319-2325
54. Brasier, A. R., Spratt, H., Wu, Z., Boldogh, I., Zhang, Y., Garofalo, R. P., Casola, A., Pashmi, J., Haag, A., Luxon, B., and Kurosky, A. (2004) Nuclear heat shock response and novel nuclear domain 10 reorganization in respiratory syncytial virus-infected A549 cells identified by high-resolution two-dimensional gel electrophoresis. J. Virol. 78, 11461-11476
55. Zheng, X., Hong, L., Shi, L., Guo, J., Sun, Z., and Zhou, J. (2008) Proteomics analysis of host cells infected with infectious bursal disease virus. Mol. Cell. Proteomics 7, 612-625
56. Pattanakitsakul, S. N., Rungrojcharoenkit, K., Kanlaya, R., Sinchaikul, S., Noisakran, S., Chen, S. T., Malasit, P., and Thongboonkerd, V. (2007) Proteomic analysis of host responses in HepG2 cells during dengue virus infection. J. Proteome Res. 6, 4592-4600
57. Reed, M. L., Dove, B. K., Jackson, R. M., Collins, R., Brooks, G., and Hiscox, J. A. (2006) Delineation and modelling of a nucleolar retention signal in the coronavirus nucleocapsid protein. Traffic 7, 833-848
58. Reed, M. L., Howell, G., Harrison, S. M., Spencer, K. A., and Hiscox, J. A. (2007) Characterization of the nuclear export signal in the coronavirus infectious bronchitis virus nucleocapsid protein. J. Virol. 81, 4298-4304
59. Hiscox, J. A., Wurm, T., Wilson, L., Britton, P., Cavanagh, D., and Brooks, G. (2001) The coronavirus infectious bronchitis virus nucleoprotein localizes to the nucleolus. J. Virol. 75, 506-512
60. Wurm, T., Chen, H., Hodgson., T, Britton, P., Brooks, G., and Hiscox, J. A. (2001) Localisation to the nucleolus is a common feature of coronavirus nucleoproteins and the protein may disrupt host cell division. J. Virol. 75, 9345-9356
61. Chen, H., Wurm, T., Britton, P., Brooks, G., and Hiscox, J. A. (2002) Interaction of the coronavirus nucleoprotein with nucleolar antigens and the host cell. J. Virol. 76, 5233-5250
62. Corse, E., and Machamer, C. E. (2003) The cytoplasmic tails of infectious bronchitis virus E and M proteins mediate their interaction. Virology 312, 25-34
63. Corse, E., and Machamer, C. E. (2000) Infectious bronchitis virus E protein is targeted to the Golgi complex and directs release of virus-like particles. J. Virol. 74, 4319-4326
64. Frieman, M., Ratia, K., Johnston, R. E., Mesecar, A. D., and Baric, R. S. (2009) Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-kappaB signaling. J. Virol. 83, 6689-6705
65. Chang, Y. J., Liu, C. Y., Chiang, B. L., Chao, Y. C., and Chen, C. C. (2004) Induction of IL-8 release in lung cells via activator protein-1 by recombinant baculovirus displaying severe acute respiratory syndrome-coronavirus spike proteins: identification of two functional regions. J. Immunol. 173, 7602-7614
66. He, R., Leeson, A., Andonov, A., Li, Y., Bastien, N., Cao, J., Osiowy, C., Dobie, F., Cutts, T., Ballantine, M., and Li, X. (2003) Activation of AP-1 signal transduction pathway by SARS coronavirus nucleocapsid protein. Biochem. Biophys. Res. Commun. 311, 870-876
67. Shaulian, E., and Karin, M. (2001) AP-1 in cell proliferation and survival. Oncogene 20, 2390-2400
68. Harrison, S. M., Dove, B. K., Rothwell, L., Kaiser, P., Tarpey, I., Brooks, G., and Hiscox, J. A. (2007) Characterisation of cyclin D1 down-regulation in coronavirus infected cells. FEBS Lett. 581, 1275-1286
69. Lavi, E., Wang, Q., Weiss, S. R., and Gonatas, N. K. (1996) Syncytia formation induced by coronavirus infection is associated with fragmentation and rearrangement of the Golgi apparatus. Virology 221, 325-334
70. Kalicharran, K., and Dales, S. (1996) The murine coronavirus as a model of trafficking and assembly of viral proteins in neural tissue. Trends Microbiol. 4, 264-269
71. Wang, J., Fang, S., Xiao, H., Chen, B., Tam, J. P., and Liu, D. X. (2009) Interaction of the coronavirus infectious bronchitis virus membrane protein with beta-actin and its implication in virion assembly and budding. PLoS One 4, e4908
72. Vreugde, S., Ferrai, C., Miluzio, A., Hauben, E., Marchisio, P. C., Crippa, M. P., Bussi, M., and Biffo, S. (2006) Nuclear myosin VI enhances RNA polymerase II-dependent transcription. Mol. Cell 23, 749-755
73. Jung, E. J., Liu, G., Zhou, W., and Chen, X. (2006) Myosin VI is a mediator of the p53-dependent cell survival pathway. Mol. Cell. Biol. 26, 2175-2186
74. Bhattacharya, B., Noad, R. J., and Roy, P. (2007) Interaction between Bluetongue virus outer capsid protein VP2 and vimentin is necessary for virus egress. Virol. J. 4, 7
75. Chen, W., Gao, N., Wang, J. L., Tian, Y. P., Chen, Z. T., and An, J. (2008) Vimentin is required for dengue virus serotype 2 infection but microtubules are not necessary for this process. Arch. Virol. 153, 1777-1781
76. Stefanovic, S., Windsor, M., Nagata, K. I., Inagaki, M., and Wileman, T. (2005) Vimentin rearrangement during African swine fever virus infection involves retrograde transport along microtubules and phosphorylation of vimentin by calcium calmodulin kinase II. J. Virol. 79, 11766-11775
77. Risco, C., Rodríguez, J. R., López-Iglesias, C., Carrascosa, J. L., Esteban, M., and Rodríguez, D. (2002) Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76, 1839-1855
78. Emmott, E., and Hiscox, J. A. (2009) Nucleolar targetting: the hub of the matter. EMBO Rep. 10, 231-238
79. Salsman, J., Zimmerman, N., Chen, T., Domagala, M., and Frappier, L. (2008) Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies. PLoS Pathog. 4, e1000100
80. Boyne, J. R., and Whitehouse, A. (2006) Nucleolar trafficking is essential for nuclear export of intronless herpesvirus mRNA. Proc. Natl. Acad. Sci. U.S.A. 103, 15190-15195
81. Lymberopoulos, M. H., and Pearson, A. (2007) Involvement of UL24 in herpes-simplex-virus-1-induced dispersal of nucleolin. Virology 363, 397-409
82. Callé, A., Ugrinova, I., Epstein, A. L., Bouvet, P., Diaz, J. J., and Greco, A. (2008) Nucleolin is required for an efficient herpes simplex virus type 1 infection. J. Virol. 82, 4762-4773
83. Matthews, D. A. (2001) Adenovirus protein V induces redistribution of nucleolin and B23 from nucleolus to cytoplasm. J. Virol. 75, 1031-1038
84. Lawrence, F. J., McStay, B., and Matthews, D. A. (2006) Nucleolar protein upstream binding factor is sequestered into adenovirus DNA replication centres during infection without affecting RNA polymerase I location or ablating rRNA synthesis. J. Cell Sci. 119, 2621-2631
85. Enjuanes, L., Almazán, F., Sola, I., and Zuñiga, S. (2006) Biochemical aspects of coronavirus replication and virus-host interaction. Annu. Rev. Microbiol. 60, 211-230 (Pubitemid 44627947)