Identification of cellular proteome using two-dimensional difference gel electrophoresis in ST cells infected with transmissible gastroenteritis coronavirus

Proteome Science

Volumn 11, Issue 1, 2013, Pages

  Zhang, Xin ^a   Shi, Hong Yan ^a   Chen, Jian Fei ^a   Shi, Da ^a   Lang, Hong Wu ^b   Wang, Zhong Tian ^b   Feng, Li ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b CHINA INSTITUTE OF VETERINARY DRUG CONTROL   (China)

Author keywords

DIGE; Proteome; ST cell; TGEV

Indexed keywords

ACIDIC RIBOSOMAL PROTEIN P0; ALPHA TROPOMYOSIN; ALPHA TUBULIN; ANNEXIN A8; BETA ACTIN; BETA TUBULIN; CYTOCHROME; CYTOCHROME B C1 COMPLEX 1; CYTOKERATIN 19; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U; INITIATION FACTOR 4A; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE ISOENZYME 1; LIPOCORTIN 4; PHOSPHOPROTEIN PHOSPHATASE 2A; PROHIBITIN; PROTEIN; PROTEIN 14 3 3; THIOPURINE METHYLTRANSFERASE; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL CELL; ARTICLE; CELL LYSATE; CELL STRUCTURE; CONTROLLED STUDY; CORONAVIRUS INFECTION; CYTOPATHOGENIC EFFECT; DOWN REGULATION; HOST CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRION; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; PROTEOMICS; RNA PROCESSING; SIGNAL TRANSDUCTION; STROMA CELL; TRANSMISSIBLE GASTROENTERITIS VIRUS; TRANSPORT VESICLE; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION; VIRUS REPLICATION; WESTERN BLOTTING;

CORONAVIRUS; SUIDAE; TRANSMISSIBLE GASTROENTERITIS VIRUS;

EID: 84880088942     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-11-31     Document Type: Article

References (60)

1. Masters PS. The molecular biology of coronaviruses. Adv Virus Res 2006, 66:193-292.
2. Sestak K, Lanza I, Park SK, Weilnau PA, Saif LJ. Contribution of passive immunity to porcine respiratory coronavirus to protection against transmissible gastroenteritis virus challenge exposure in suckling pigs. Am J Vet Res 1996, 57:664-671.
3. Penzes Z, Gonzalez JM, Calvo E, Izeta A, Smerdou C, Mendez A, Sanchez CM, Sola I, Almazan F, Enjuanes L. Complete genome sequence of transmissible gastroenteritis coronavirus PUR46-MAD clone and evolution of the purdue virus cluster. Virus Genes 2001, 23:105-118. 10.1023/A:1011147832586, 11556396.
4. Schwegmann-Wessels C, Zimmer G, Laude H, Enjuanes L, Herrler G. Binding of transmissible gastroenteritis coronavirus to cell surface sialoglycoproteins. J Virol 2002, 76:6037-6043. 10.1128/JVI.76.12.6037-6043.2002, 136196, 12021336.
5. Escors D, Camafeita E, Ortego J, Laude H, Enjuanes L. Organization of two transmissible gastroenteritis coronavirus membrane protein topologies within the virion and core. J Virol 2001, 75:12228-12240. 10.1128/JVI.75.24.12228-12240.2001, 116120, 11711614.
6. Escors D, Ortego J, Laude H, Enjuanes L. The membrane M protein carboxy terminus binds to transmissible gastroenteritis coronavirus core and contributes to core stability. J Virol 2001, 75:1312-1324. 10.1128/JVI.75.3.1312-1324.2001, 114037, 11152504.
7. Godet M, L'Haridon R, Vautherot JF, Laude H. TGEV corona virus ORF4 encodes a membrane protein that is incorporated into virions. Virology 1992, 188:666-675. 10.1016/0042-6822(92)90521-P, 1316677.
8. Calvo E, Escors D, Lopez JA, Gonzalez JM, Alvarez A, Arza E, Enjuanes L. Phosphorylation and subcellular localization of transmissible gastroenteritis virus nucleocapsid protein in infected cells. J Gen Virol 2005, 86:2255-2267. 10.1099/vir.0.80975-0, 16033973.
9. Kapke PA, Brian DA. Sequence analysis of the porcine transmissible gastroenteritis coronavirus nucleocapsid protein gene. Virology 1986, 151:41-49. 10.1016/0042-6822(86)90102-9, 3008432.
10. Wurm T, Chen H, Hodgson T, Britton P, Brooks G, Hiscox JA. Localization to the nucleolus is a common feature of coronavirus nucleoproteins, and the protein may disrupt host cell division. J Virol 2001, 75:9345-9356. 10.1128/JVI.75.19.9345-9356.2001, 114503, 11533198.
11. Maxwell KL, Frappier L. Viral proteomics. Microbiol Mol Biol Rev 2007, 71:398-411. 10.1128/MMBR.00042-06, 1899879, 17554050.
12. Go EP, Wikoff WR, Shen Z, O'Maille G, Morita H, Conrads TP, Nordstrom A, Trauger SA, Uritboonthai W, Lucas DA, Chan KC, Veenstra TD, Lewicki H, Oldstone MB, Schneemann A, Siuzdak G. Mass spectrometry reveals specific and global molecular transformations during viral infection. J Proteome Res 2006, 5:2405-2416. 10.1021/pr060215t, 2566936, 16944953.
13. Unlu M, Morgan ME, Minden JS. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 1997, 18:2071-2077. 10.1002/elps.1150181133, 9420172.
14. Patton WF. Detection technologies in proteome analysis. J Chromatogr B Analyt Technol Biomed Life Sci 2002, 771:3-31. 10.1016/S1570-0232(02)00043-0, 12015990.
15. Vester D, Rapp E, Gade D, Genzel Y, Reichl U. Quantitative analysis of cellular proteome alterations in human influenza a virus-infected mammalian cell lines. Proteomics 2009, 9:3316-3327. 10.1002/pmic.200800893, 19504497.
16. Coiras M, Camafeita E, Urena T, Lopez JA, Caballero F, Fernandez B, Lopez-Huertas MR, Perez-Olmeda M, Alcami J. Modifications in the human T cell proteome induced by intracellular HIV-1 tat protein expression. Proteomics 2006, 6:63-73.
17. Huang Q, Wang L, Bai S, Lin W, Chen W, Lin J, Lin X. Global proteome analysis of hepatitis B virus expressing human hepatoblastoma cell line HepG2. J Med Virol 2009, 81:1539-1550. 10.1002/jmv.21593, 19626621.
18. De Re V, Simula MP, Cannizzaro R, Sansonno D, Canzonieri V, Gloghini A, Carbone A, Colombatti A, Marin MD, De Zorzi M, Toffoli G. HCV inhibits antigen processing and presentation and induces oxidative stress response in gastric mucosa. Proteomics Clin Appl 2008, 2:1290-1299. 10.1002/prca.200800059, 21136923.
19. Cao JY, Mansouri S, Frappier L. Changes in the nasopharyngeal carcinoma nuclear proteome induced by the EBNA1 protein of epstein-barr virus reveal potential roles for EBNA1 in metastasis and oxidative stress responses. J Virol 2012, 86:382-394. 10.1128/JVI.05648-11, 3255880, 22013061.
20. Patramool S, Surasombatpattana P, Luplertlop N, Seveno M, Choumet V, Thomas F, Misse D. Proteomic analysis of an aedes albopictus cell line infected with dengue serotypes 1 and 3 viruses. Parasit Vectors 2011, 4:138-145. 10.1186/1756-3305-4-138, 3151224, 21767351.
21. Yang Y, An T, Gong D, Li D, Peng J, Leng C, Yuan Z, Tong G, Tian Z, Zhang D. Identification of porcine serum proteins modified in response to HP-PRRSV HuN4 infection by two-dimensional differential gel electrophoresis. Vet Microbiol 2012, 158:237-246. 10.1016/j.vetmic.2012.01.021, 22503602.
22. Naghavi MH, Goff SP. Retroviral proteins that interact with the host cell cytoskeleton. Curr Opin Immunol 2007, 19:402-407. 10.1016/j.coi.2007.07.003, 2040053, 17707624.
23. Greber UF, Way M. A superhighway to virus infection. Cell 2006, 124:741-754. 10.1016/j.cell.2006.02.018, 16497585.
24. Soll DR. Researchers in cell motility and the cytoskeleton can play major roles in understanding AIDS. Cell Motil Cytoskeleton 1997, 37:91-97. 10.1002/(SICI)1097-0169(1997)37:2<91::AID-CM1>3.0.CO;2-K, 9186006.
25. Radtke K, Dohner K, Sodeik B. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol 2006, 8:387-400. 10.1111/j.1462-5822.2005.00679.x, 16469052.
26. Cudmore S, Reckmann I, Way M. Viral manipulations of the actin cytoskeleton. Trends Microbiol 1997, 5:142-148. 10.1016/S0966-842X(97)01011-1, 9141188.
27. Franke WW, Schmid E, Winter S, Osborn M, Weber K. Widespread occurrence of intermediate-sized filaments of the vimentin-type in cultured cells from diverse vertebrates. Exp Cell Res 1979, 123:25-46. 10.1016/0014-4827(79)90418-X, 114401.
28. Ivaska J, Pallari HM, Nevo J, Eriksson JE. Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res 2007, 313:2050-2062. 10.1016/j.yexcr.2007.03.040, 17512929.
29. Yoon M, Moir RD, Prahlad V, Goldman RD. Motile properties of vimentin intermediate filament networks in living cells. J Cell Biol 1998, 143:147-157. 10.1083/jcb.143.1.147, 2132819, 9763427.
30. Stefanovic S, Windsor M, Nagata KI, Inagaki M, Wileman T. Vimentin rearrangement during African swine fever virus infection involves retrograde transport along microtubules and phosphorylation of vimentin by calcium calmodulin kinase II. J Virol 2005, 79:11766-11775. 10.1128/JVI.79.18.11766-11775.2005, 1212593, 16140754.
31. Shoeman RL, Honer B, Stoller TJ, Kesselmeier C, Miedel MC, Traub P, Graves MC. Human immunodeficiency virus type 1 protease cleaves the intermediate filament proteins vimentin, desmin, and glial fibrillary acidic protein. Proc Natl Acad Sci USA 1990, 87:6336-6340. 10.1073/pnas.87.16.6336, 54528, 2201025.
32. 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, 7:612-625.
33. Wojdyla JA, Manolaridis I, van Kasteren PB, Kikkert M, Snijder EJ, Gorbalenya AE, Tucker PA. Papain-like protease 1 from transmissible gastroenteritis virus: crystal structure and enzymatic activity toward viral and cellular substrates. J Virol 2010, 84:10063-10073. 10.1128/JVI.00898-10, 2937765, 20668092.
34. Li HP, Huang P, Park S, Lai MM. Polypyrimidine tract-binding protein binds to the leader RNA of mouse hepatitis virus and serves as a regulator of viral transcription. J Virol 1999, 73:772-777. 103887, 9847386.
35. Pinol-Roma S, Dreyfuss G. hnRNP proteins: localization and transport between the nucleus and the cytoplasm. Trends Cell Biol 1993, 3:151-155. 10.1016/0962-8924(93)90135-N, 14731609.
36. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 2002, 3:195-205. 10.1038/nrm760, 11994740.
37. Valente ST, Goff SP. Inhibition of HIV-1 gene expression by a fragment of hnRNP U. Mol Cell 2006, 23:597-605. 10.1016/j.molcel.2006.07.021, 16916646.
38. Krynetski E, Evans WE. Drug methylation in cancer therapy: lessons from the TPMT polymorphism. Oncogene 2003, 22:7403-7413. 10.1038/sj.onc.1206944, 14576848.
39. Woodson LC, Weinshilboum RM. Human kidney thiopurine methyltransferase. purification and biochemical properties. Biochem Pharmacol 1983, 32:819-826. 10.1016/0006-2952(83)90582-8, 6838629.
40. Hoover S, Striker R. Thiopurines inhibit bovine viral diarrhea virus production in a thiopurine methyltransferase-dependent manner. J Gen Virol 2008, 89:1000-1009. 10.1099/vir.0.83381-0, 18343842.
41. Silverman RH, Williams BR. Translational control perks up. Nature 1999, 397:208-211. 10.1038/16586, 9930691.
42. Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P. Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci USA 2003, 100:15764-15769. 10.1073/pnas.2536857100, 307642, 14671320.
43. Greco A, Laurent AM, Madjar JJ. Repression of beta-actin synthesis and persistence of ribosomal protein synthesis after infection of HeLa cells by herpes simplex virus type 1 infection are under translational control. Mol Gen Genet 1997, 256:320-327. 10.1007/s004380050575, 9393457.
44. Wool IG, Chan YL, Gluck A, Suzuki K. The primary structure of rat ribosomal proteins P0, P1, and P2 and a proposal for a uniform nomenclature for mammalian and yeast ribosomal proteins. Biochimie 1991, 73:861-870. 10.1016/0300-9084(91)90127-M, 1742361.
45. Skiba M, Mettenleiter TC, Karger A. Quantitative whole-cell proteome analysis of pseudorabies virus-infected cells. J Virol 2008, 82:9689-9699. 10.1128/JVI.00995-08, 2546971, 18653448.
46. Schlee M, Krug T, Gires O, Zeidler R, Hammerschmidt W, Mailhammer R, Laux G, Sauer G, Lovric J, Bornkamm GW. Identification of epstein-barr virus (EBV) nuclear antigen 2 (EBNA2) target proteins by proteome analysis: activation of EBNA2 in conditionally immortalized B cells reflects early events after infection of primary B cells by EBV. J Virol 2004, 78:3941-3952. 10.1128/JVI.78.8.3941-3952.2004, 374249, 15047810.
47. Ahmed M, McKenzie MO, Puckett S, Hojnacki M, Poliquin L, Lyles DS. Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J Virol 2003, 77:4646-4657. 10.1128/JVI.77.8.4646-4657.2003, 152115, 12663771.
48. Xiao H, Xu LH, Yamada Y, Liu DX. Coronavirus spike protein inhibits host cell translation by interaction with eIF3f. PLoS One 2008, 3:1494-1499.
49. Labib K, Nurse P. Cell cycle: bring on the phosphatases. Curr Biol 1993, 3:164-166. 10.1016/0960-9822(93)90261-L, 15335787.
50. Garcia A, Cayla X, Sontag E. Protein phosphatase 2A: a definite player in viral and parasitic regulation. Microbes Infect 2000, 2:401-407. 10.1016/S1286-4579(00)00327-0, 10817642.
51. Chen J, Martin BL, Brautigan DL. Regulation of protein serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 1992, 57:1261-1264.
52. Chen J, Parsons S, Brautigan DL. Tyrosine phosphorylation of protein phosphatase 2A in response to growth stimulation and v-src transformation of fibroblasts. J Biol Chem 1994, 269:7957-7962.
53. Santamaria E, Mora MI, Potel C, Fernandez-Irigoyen J, Carro-Roldan E, Hernandez-Alcoceba R, Prieto J, Epstein AL, Corrales FJ. Identification of replication-competent HSV-1 Cgal + strain signaling targets in human hepatoma cells by functional organelle proteomics. Mol Cell Proteomics 2009, 8:805-815. 10.1074/mcp.M800202-MCP200, 2667359, 19098277.
54. Jiang X, Tang L, Dai J, Zhou H, Li S, Xia Q, Wu J, Zeng R. Quantitative analysis of severe acute respiratory syndrome (SARS)-associated coronavirus-infected cells using proteomic approaches. Mol Cell Proteomics 2005, 4:902-913. 10.1074/mcp.M400112-MCP200, 15784933.
55. Emmott E, Rodgers MA, Macdonald A, McCrory S, Ajuh P, Hiscox JA. 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. 10.1074/mcp.M900345-MCP200, 2938107, 20467043.
56. Cao Z, Han Z, Shao Y, Liu X, Sun J, Yu D, Kong X, Liu S. Proteomics analysis of differentially expressed proteins in chicken trachea and kidney after infection with the highly virulent and attenuated coronavirus infectious bronchitis virus in vivo. Proteome Science 2012, 10:24-43. 10.1186/1477-5956-10-24, 3342233, 22463732.
57. Vogels MW, van Balkom BW, Kaloyanova DV, Batenburg JJ, Heck AJ, Helms JB, Rottier PJ, de Haan CA. Identification of host factors involved in coronavirus replication by quantitative proteomics analysis. Proteomics 2011, 11:64-80. 10.1002/pmic.201000309, 21182195.
58. Wang C, Chen J, Shi H, Qiu H, Xue F, Liu C, Zhu Y, Liu S, Almazan F, Enjuanes L, Feng L. Molecular characterization of a Chinese vaccine strain of transmissible gastroenteritis virus: mutations that may contribute to attenuation. Virus Genes 2010, 40:403-409. 10.1007/s11262-010-0467-6, 20229183.
59. Zhang X, Zhou J, Wu Y, Zheng X, Ma G, Wang Z, Jin Y, He J, Yan Y. Differential proteome analysis of host cells infected with porcine circovirus type 2. J Proteome Res 2009, 8:5111-5119. 10.1021/pr900488q, 19708719.
60. Cao Z, Han Z, Shao Y, Geng H, Kong X, Liu S. Proteomic analysis of chicken embryonic trachea and kidney tissues after infection in ovo by avian infectious bronchitis coronavirus. Proteome Sci 2011, 9:11-18. 10.1186/1477-5956-9-11, 3060854, 21385394.