Identification of host factors involved in coronavirus replication by quantitative proteomics analysis

Proteomics

Volumn 11, Issue 1, 2011, Pages 64-80

  Vogels, Mijke W ^a,b   Van Balkom, Bas W M ^c,d   Kaloyanova, Dora V ^a   Batenburg, Joseph J ^a   Heck, Albert J ^c   Helms, J Bernd ^a   Rottier, Peter J M ^b   De Haan, Cornelis A M ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Host pathogen interactions; Microbiology; Secretory pathway; SILAC

Indexed keywords

PROTEIN SECB; SMALL INTERFERING RNA; VIRUS GLYCOPROTEIN;

ARTICLE; CONTROLLED STUDY; CORONAVIRUS; GOLGI COMPLEX; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEOMICS; QUANTITATIVE ANALYSIS; VIRUS CELL INTERACTION; VIRUS REPLICATION;

CORONAVIRUS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MASS SPECTROMETRY; MURINE HEPATITIS VIRUS; PROTEOMICS; RECEPTORS, FIBROBLAST GROWTH FACTOR; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIALOGLYCOPROTEINS; VIRUS REPLICATION;

CORONAVIRUS; MURINE HEPATITIS VIRUS;

EID: 78650357434     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000309     Document Type: Article

References (69)

1. Belov, G. A., Altan-Bonnet, N., Kovtunovych, G., Jackson, C. L. et al., Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J. Virol. 2007, 81, 558-567.
2. Beske, O., Reichelt, M., Taylor, M. P., Kirkegaard, K., Andino, R., Poliovirus infection blocks ERGIC-to-Golgi trafficking and induces microtubule-dependent disruption of the Golgi complex. J. Cell. Sci. 2007, 120, 3207-3218.
3. Choe, S. S., Dodd, D. A., Kirkegaard, K., Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 2005, 337, 18-29.
4. Konan, K. V., Giddings, T. H., Jr., Ikeda, M., Li, K. et al., Nonstructural protein precursor NS4A/B from hepatitis C virus alters function and ultrastructure of host secretory apparatus. J. Virol. 2003, 77, 7843-7855.
5. Moffat, K., Knox, C., Howell, G., Clark, S. J. et al., Inhibition of the secretory pathway by foot-and-mouth disease virus 2BC protein is reproduced by coexpression of 2B with 2C, and the site of inhibition is determined by the subcellular location of 2C. J. Virol. 2007, 81, 1129-1139.
6. Oostra, M., te Lintelo, E. G., Deijs, M., Verheije, M. H. et al., Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J. Virol. 2007, 81, 12323-12336.
7. Sakaguchi, T., Leser, G. P., Lamb, R. A., The ion channel activity of the influenza virus M2 protein affects transport through the Golgi apparatus. J. Cell. Biol. 1996, 133, 733-747.
8. Drosten, C., Gunther, S., Preiser, W., van der Werf, S. et al., Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 2003, 348, 1967-1976.
9. Lai, M. M., Coronavirus: organization, replication and expression of genome. Ann. Rev. Microbiol. 1990, 44, 303-333.
10. Spaan, W., Cavanagh, D., Horzinek, M. C., Coronaviruses: structure and genome expression. J. Gen. Virol. 1988, 69, 2939-2952.
11. Goldsmith, C. S., Tatti, K. M., Ksiazek, T. G., Rollin, P. E. et al., Ultrastructural characterization of SARS coronavirus. Emerg. Infect. Dis. 2004, 10, 320-326.
12. Gosert, R., Kanjanahaluethai, A., Egger, D., Bienz, K., Baker, S. C., RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 2002, 76, 3697-3708.
13. Sims, A. C., Ostermann, J., Denison, M. R., Mouse hepatitis virus replicase proteins associate with two distinct populations of intracellular membranes. J. Virol. 2000, 74, 5647-5654.
14. Snijder, E. J., van der Meer, Y., Zevenhoven-Dobbe, J., Onderwater, J. J. et al., Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J. Virol. 2006, 80, 5927-5940.
15. Knoops, K., Kikkert, M., Worm, S. H., Zevenhoven-Dobbe, J. C. et al., SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol. 2008, 6, e226.
16. Verheije, M. H., Raaben, M., Mari, M., Te Lintelo, E. G. et al., Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathogens 2008, 4, e1000088.
17. Knoops, K., Swett-Tapia, C., van den Worm, S. H., Te Velthuis, A. J. et al., Integrity of the early secretory pathway promotes, but is not required for, severe acute respiratory syndrome coronavirus RNA synthesis and virus-induced remodeling of endoplasmic reticulum membranes. J. Virol. 2010, 84, 833-846.
18. de Haan, C. A., Rottier, P. J., Molecular interactions in the assembly of coronaviruses. Adv. Virus Res. 2005, 64, 165-230.
19. Klumperman, J., Locker, J. K., Meijer, A., Horzinek, M. C. et al., Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. J. Virol. 1994, 68, 6523-6534.
20. Kuo, L., Masters, P. S., Genetic evidence for a structural interaction between the carboxy termini of the membrane and nucleocapsid proteins of mouse hepatitis virus. J. Virol. 2002, 76, 4987-4999.
21. Narayanan, K., Chen, C. J., Maeda, J., Makino, S., Nucleocapsid-independent specific viral RNA packaging via viral envelope protein and viral RNA signal. J. Virol. 2003, 77, 2922-2927.
22. Narayanan, K., Maeda, A., Maeda, J., Makino, S., Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells. J. Virol. 2000, 74, 8127-8134.
23. Risco, C., Muntion, M., Enjuanes, L., Carrascosa, J. L., Two types of virus-related particles are found during transmissible gastroenteritis virus morphogenesis. J. Virol. 1998, 72, 4022-4031.
24. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B. et al., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1, 376-386.
25. Wurdinger, T., Verheije, M. H., Raaben, M., Bosch, B. J. et al., Targeting non-human coronaviruses to human cancer cells using a bispecific single-chain antibody. Gene Ther. 2005, 12, 1394-1404.
26. de Haan, C. A., van Genne, L., Stoop, J. N., Volders, H., Rottier, P. J., Coronaviruses as vectors: position dependence of foreign gene expression. J. Virol. 2003, 77, 11312-11323.
27. Sohn, K., Orci, L., Ravazzola, M., Amherdt, M. et al., A major transmembrane protein of Golgi-derived COPI-coated vesicles involved in coatomer binding. J. Cell. Biol. 1996, 135, 1239-1248.
28. Rottier, P. J., Horzinek, M. C., van der Zeijst, B. A., Viral protein synthesis in mouse hepatitis virus strain A59-infected cells: effect of tunicamycin. J. Virol. 1981, 40, 350-357.
29. van Balkom, B. W., van Gestel, R. A., Brouwers, J. F., Krijgsveld, J. et al., Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. J. Prot. Res. 2005, 4, 958-966.
30. Brügger, B., Sandhoff, R., Wegehingel, S., Gorgas, K. et al., Evidence for segregation of sphingomyelin and cholesterol during formation of COPI-coated vesicles. J. Cell. Biol. 2000, 151, 507-518.
31. Kersey, P. J., Duarte, J., Williams, A., Karavidopoulou, Y. et al., The International Protein Index: an integrated database for proteomics experiments. Proteomics 2004, 4, 1985-1988.
32. Perkins, D. N., Pappin, D. J., Creasy, D. M., Cottrell, J. S., Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20, 3551-3567.
33. Schulze, W. X., Mann, M., A novel proteomic screen for peptide-protein interactions. J. Biol. Chem. 2004, 279, 10756-10764.
34. van Breukelen, B., van den Toorn, H. W., Drugan, M. M., Heck, A. J., StatQuant: a post-quantification analysis toolbox for improving quantitative mass spectrometry. Bioinformatics 2009, 25, 1472-1473.
35. Raaben, M., Groot Koerkamp, M. J., Rottier, P. J., de Haan, C. A., Mouse hepatitis coronavirus replication induces host translational shutoff and mRNA decay, with concomitant formation of stress granules and processing bodies. Cell. Microbiol. 2007, 9, 2218-2229.
36. Schonborn, J., Oberstrass, J., Breyel, E., Tittgen, J. et al., Monoclonal antibodies to double-stranded RNA as probes of RNA structure in crude nucleic acid extracts. Nucleic Acids Res. 1991, 19, 2993-3000.
37. Hagemeijer, M. C., Verheije, M. H., Ulasli, M., Shaltiel, I. A. et al., Dynamics of coronavirus replication-transcription complexes. J. Virol. 2010, 84, 2134-2149.
38. Balch, W. E., Dunphy, W. G., Braell, W. A., Rothman, J. E., Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell 1984, 39, 405-416.
39. Ulasli, M., Verheije, M. H., de Haan, C. A., Reggiori, F., Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cell. Microbiol. 2010, 12, 844-861.
40. Craig, R., Beavis, R. C., A method for reducing the time required to match protein sequences with tandem mass spectra. Rapid Commun. Mass Spectrom. 2003, 17, 2310-2316.
41. Fenyo, D., Beavis, R. C., A method for assessing the statistical significance of mass spectrometry-based protein identifications using general scoring schemes. Anal. Chem. 2003, 75, 768-774.
42. Thomas, P. D., Campbell, M. J., Kejariwal, A., Mi, H. et al., PANTHER: a library of protein families and subfamilies indexed by function. Genome Res. 2003, 13, 2129-2141.
43. Zhang, L., Zhang, Z. P., Zhang, X. E., Lin, F. S., Ge, F., Quantitative proteomics analysis reveals BAG3 as a potential target to suppress SARS-CoV replication. J. Virol. 2010, 84, 6050-6059.
44. Emmott, E., Wise, H., Loucaides, E. M., Matthews, D. A. et al., 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, 5335-5345.
45. Munday, D., Emmott, E., Surtees, R., Lardeau, C. H. et al., Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus. Mol. Cell. Proteomics 2010, Epub ahead of print, doi: 10.1074/mcp.M110.001859.
46. Emmott, E., Rodgers, M., Macdonald, A., McCrory, S. et al., Quantitative proteomics using stable isotope labeling with amino acids in cell culture (SILAC) reveals changes in the cytoplasmic, nuclear and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol. Cell. Proteomics 2010, 9, 1920-1936.
47. Coombs, K. M., Berard, A., Xu, W., Krokhin, O. et al., Quantitative Proteomic Analyses of Influenza virus-Infected Cultured Human Lung Cells. J. Virol. 2010, 84, 10888-10906.
48. Takatalo, M. S., Kouvonen, P., Corthals, G., Nyman, T. A., Ronnholm, R. H., Identification of new Golgi complex specific proteins by direct organelle proteomic analysis. Proteomics 2006, 6, 3502-3508.
49. Taylor, R. S., Wu, C. C., Hays, L. G., Eng, J. K. et al., Proteomics of rat liver Golgi complex: minor proteins are identified through sequential fractionation. Electrophoresis 2000, 21, 3441-3459.
50. Wu, C. C., MacCoss, M. J., Mardones, G., Finnigan, C. et al., Organellar proteomics reveals Golgi arginine dimethylation. Mol. Biol. Cell 2004, 15, 2907-2919.
51. Wu, C. C., Yates, J. R., 3rd, Neville, M. C., Howell, K. E., Proteomic analysis of two functional states of the Golgi complex in mammary epithelial cells. Traffic 2000, 1, 769-782.
52. Neuman, B. W., Joseph, J. S., Saikatendu, K. S., Serrano, P. et al., Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J. Virol. 2008, 82, 5279-5294.
53. Hoshino, D., Tomari, T., Nagano, M., Koshikawa, N., Seiki, M., A novel protein associated with membrane-type 1 matrix metalloproteinase binds p27(kip1) and regulates RhoA activation, actin remodeling, and matrigel invasion. J. Biol. Chem. 2009, 284, 27315-27326.
54. Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A. L. et al., Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010, 141, 290-303.
55. Nada, S., Hondo, A., Kasai, A., Koike, M. et al., The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. EMBO J. 2009, 28, 477-489.
56. Guillaumot, P., Luquain, C., Malek, M., Huber, A. L. et al., Pdro, a protein associated with late endosomes and lysosomes and implicated in cellular cholesterol homeostasis. PLoS One 2010, 5, e10977.
57. Mannová, P., Fang, R., Wang, H., Deng, B. et al., Modification of host lipid raft proteome upon hepatitis C virus replication. Mol. Cell. Proteomics 2006, 5, 2319-2325.
58. Cordeiro, J. V., Guerra, S., Arakawa, Y., Dodding, M. P. et al., F11-mediated inhibition of RhoA signalling enhances the spread of vaccinia virus in vitro and in vivo in an intranasal mouse model of infection. PLoS One 2009, 4, e8506.
59. Glende, J., Schwegmann-Wessels, C., Al-Falah, M., Pfefferle, S. et al., Importance of cholesterol-rich membrane microdomains in the interaction of the S protein of SARS-coronavirus with the cellular receptor angiotensin-converting enzyme 2. Virology 2008, 381, 215-221.
60. Ren, X., Glende, J., Yin, J., Schwegmann-Wessels, C., Herrler, G., Importance of cholesterol for infection of cells by transmissible gastroenteritis virus. Virus Res. 2008, 137, 220-224.
61. Thorp, E. B., Gallagher, T. M., Requirements for CEACAMs and cholesterol during murine coronavirus cell entry. J. Virol. 2004, 78, 2682-2692.
62. Mourelatos, Z., Gonatas, J. O., Nycum, L. M., Gonatas, N. K., Biegel, J. A., Assignment of the GLG1 gene for MGF-160, a fibroblast growth factor and E-selectin binding membrane sialoglycoprotein of the Golgi apparatus, to chromosome 16q22-q23 by fluorescence in situ hybridization. Genomics 1995, 28, 354-355.
63. Burrus, L. W., Zuber, M. E., Lueddecke, B. A., Olwin, B. B., Identification of a cysteine-rich receptor for fibroblast growth factors. Mol. Cell. Biol. 1992, 12, 5600-5609.
64. Zuber, M. E., Zhou, Z., Burrus, L. W., Olwin, B. B., Cysteine-rich FGF receptor regulates intracellular FGF-1 and FGF-2 levels. J. Cell. Physiol. 1997, 170, 217-227.
65. Steegmaier, M., Borges, E., Berger, J., Schwarz, H., Vestweber, D., The E-selectin-ligand ESL-1 is located in the Golgi as well as on microvilli on the cell surface. J. Cell. Sci. 1997, 110, 687-694.
66. Steegmaier, M., Levinovitz, A., Isenmann, S., Borges, E. et al., The E-selectin-ligand ESL-1 is a variant of a receptor for fibroblast growth factor. Nature 1995, 373, 615-620.
67. Gonatas, J. O., Mezitis, S. G., Stieber, A., Fleischer, B., Gonatas, N. K., MG-160. A novel sialoglycoprotein of the medial cisternae of the Golgi apparatus. J. Biol. Chem. 1989, 264, 646-653.
68. Hay, J. C., Klumperman, J., Oorschot, V., Steegmaier, M. et al., Localization, dynamics, and protein interactions reveal distinct roles for ER and Golgi SNAREs. J. Cell. Biol. 1998, 141, 1489-1502.
69. Spang, A., Schekman, R., Reconstitution of retrograde transport from the Golgi to the ER in vitro. J. Cell. Biol. 1998, 143, 589-599.