Nuclear localization of Beet black scorch virus capsid protein and its interaction with importin α

Virus Research

Volumn 155, Issue 1, 2011, Pages 307-315

  Zhang, Yanjing ^a   Zhang, Xiaofeng ^a   Niu, Shaofang ^a   Han, Chenggui ^a   Yu, Jialin ^a   Li, Dawei ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Beet black scorch virus; Capsid protein; GFP; Importin ; Nuclear localization

Indexed keywords

AMINO ACID; CAPSID PROTEIN; GREEN FLUORESCENT PROTEIN; KARYOPHERIN ALPHA; NUCLEIC ACID;

AMINO TERMINAL SEQUENCE; ARTICLE; BEET BLACK SCORCH VIRUS; BIOLISTIC TRANSFORMATION; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; EPIDERMIS CELL; MUTATIONAL ANALYSIS; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; ONION; PLANT LEAF; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA VIRUS;

ALPHA KARYOPHERINS; ARTIFICIAL GENE FUSION; CAPSID PROTEINS; CELL NUCLEUS; DNA MUTATIONAL ANALYSIS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MICROSCOPY, CONFOCAL; ONIONS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TOBACCO; TOMBUSVIRIDAE;

ALLIUM CEPA; BEET BLACK SCORCH VIRUS; MIRIDAE; NECROVIRUS; NICOTIANA BENTHAMIANA; RNA VIRUSES;

EID: 78650545074     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2010.10.029     Document Type: Article

References (62)

1. Aparicio F.A., Sanchez-Navarro J., Pallas V. In vitro and in vivo mapping of the Prunus necrotic ringspot virus coat protein C-terminal dimerization domain by bimolecular fluorescence complementation. J. Gen. Virol. 2006, 87:1745-1750.
2. Appiano A., Redolfi P. Ultrastructure and cytochemistry of Phaseolus leaf tissues infected with an isolate of tobacco necrosis virus inducing localized wilting. Protoplasma 1993, 174:116-127.
3. Bortolamiol D., Pazhouhandeh M., Marrocco K., Genschik P., Ziegler-Graff V. The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 2007, 17:1615-1621.
4. Canto T., Uhrig J.F., Swanson M., Wright K.M., MacFarlane S.A. Translocation of Tomato bushy stunt virus P19 protein into the nucleus by ALY proteins compromises its silencing suppressor activity. J. Virol. 2006, 80:9064-9072.
5. Cao Y.H., Cai Z.N., Ding Q., Li D.W., Han C.G., Yu J.L., Liu Y. The complete nucleotide sequence of Beet black scorch virus (BBSV), a new member of the genus Necrovirus. Arch. Virol. 2002, 147:2431-2435.
6. Cao Y.H., Yuan X.F., Wang X.X., Guo L.H., Cai Z.N., Han C.G., Li D.W., Yu J.L. Effect on viral pathogenicity of Beet black scorch virus coat protein. Prog. Biochem. Biophys. 2006, 33:127-134.
7. Castellano M., Di Franco A., Martelli G. Electron microscopy of two olive viruses in host tissues. J. Submicrosc. Cytol. Pathol. 1987, 19:495-508.
8. Castellano M.A., Loconsole G., Grieco F., Di Sansebastiano G.P., Martelli G.P. Subcellular localization and immunodetection of movement proteins of olive latent virus 1. Arch. Virol. 2005, 150:1369-1381.
9. Conti E., Kuriyan J. Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin α. Structure 2000, 8:329-338.
10. Esau K., Hoefert L.L. Development of infection with beet western yellows virus in the sugarbeet. Virology 1972, 48:724-738.
11. Félix M.d.R., Cardoso J.M.S., Oliveira S., Clara M.I.E. Biological and molecular characterization of Olive latent virus 1. Plant Viruses 2007, 1:170-177.
12. Finch J.T., Klug A., Leberman R. The structures of turnip crinkle and tomato bushy stunt viruses. II. The surface structure: dimer clustering patterns. J. Mol. Biol. 1970, 50:215-216.
13. Fuentes A.L., Hamilton R.I. Failure of long-distance movement of southern bean mosaic virus in a resistant host is correlated with lack of normal virion formation. J. Gen. Virol. 1993, 74:1903-1910.
14. Gill C.C., Chong J. Development of the infection in oat leaves inoculated with barley yellow dwarf virus. Virology 1975, 66:440-453.
15. González-Vázquez M., Ayala J., García-Arenal F., Fraile A. Occurrence of Beet black scorch virus infecting sugar beet in Europe. Plant Dis. 2009, 93:21-24.
16. Goodin M., Dietzgen R., Schichnes D., Ruzin S., Jackson A. pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J. 2002, 31:375-383.
17. Gorlich D., Kostka S., Kraft R., Dingwall C., Laskey R.A., Hartmann E., Prehn S. Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol. 1995, 5:383-392.
18. Gorlich D., Vogel F., Mills A.D., Hartmann E., Laskey R.A. Distinct functions for the two importin subunits in nuclear protein import. Nature 1995, 377:246-248.
19. Guerra-Peraza O., Kirk D., Seltzer V., Veluthambi K., Schmit A.C., Hohn T., Herzog E. Coat proteins of Rice tungro bacilliform virus and Mungbean yellow mosaic virus contain multiple nuclear-localization signals and interact with importin α. J. Gen. Virol. 2005, 86:1815-1826.
20. Guo L.H., Cao Y.H., Li D.W., Niu S.N., Cai Z.N., Han C.G., Zhai Y.F., Yu J.L. Analysis of nucleotide sequences and multimeric forms of a novel satellite RNA associated with beet black scorch virus. J. Virol. 2005, 79:3664-3674.
21. Haupt S., Stroganova T., Ryabov E., Kim S.H., Fraser G., Duncan G., Mayo M.A., Barker H., Taliansky M. Nucleolar localization of potato leafroll virus capsid proteins. J. Gen. Virol. 2005, 86:2891-2896.
22. Hodel M.R., Corbett A.H., Hodel A.E. Dissection of a nuclear localization signal. J. Biol. Chem. 2001, 276:1317-1325.
23. Kanneganti T.D., Bai X., Tsai C.W., Win J., Meulia T., Goodin M., Kamoun S., Hogenhout S.A. A functional genetic assay for nuclear trafficking in plants. Plant J. 2007, 50:149-158.
24. Karsies A., Merkle T., Szurek B., Bonas U., Hohn T., Leclerc D. Regulated nuclear targeting of Cauliflower mosaic virus. J. Gen. Virol. 2002, 83:1783-1790.
25. Kassanis B., Vince D.A., Woods R.D. Light and electron microscopy of cells infected with tobacco necrosis and satellite viruses. J. Gen. Virol. 1970, 7:143-151.
26. Kim S.H., Macfarlane S., Kalinina N.O., Rakitina D.V., Ryabov E.V., Gillespie T., Haupt S., Brown J.W., Taliansky M. Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:11115-11120.
27. Kim S.H., Ryabov E.V., Kalinina N.O., Rakitina D.V., Gillespie T., MacFarlane S., Haupt S., Brown J.W., Taliansky M. Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO J. 2007, 26:2169-2179.
28. Koenig R., Valizadeh J. Molecular and serological characterization of an Iranian isolate of Beet black scorch virus. Arch. Virol. 2008, 153:1397-1400.
29. Kosugi S., Hasebe M., Matsumura N., Takashima H., Miyamoto-Sato E., Tomita M., Yanagawa H. Six classes of nuclear localization signals specific to different binding grooves of importin α. J. Biol. Chem. 2009, 284:478-485.
30. Krichevsky A., Kozlovsky S.V., Gafni Y., Citovsky V. Nuclear import and export of plant virus proteins and genomes. Mol. Plant Pathol. 2006, 7:131-146.
31. Kunik T., Mizrachy L., Citovsky V., Gafni Y. Characterization of a tomato karyopherin α that interacts with the Tomato yellow leaf curl virus (TYLCV) capsid protein. J. Exp. Bot. 1999, 50:731-732.
32. Lange A., Mills R., Lange C., Stewart M., Devine S., Corbett A. Classical nuclear localization signals: definition, function, and interaction with importin α. J. Biol. Chem. 2007, 282:5101-5105.
33. Li J., Li M., Li C., Gao Y., Li D.W., Han C.G., Yu J.L. Effects on the local symptoms of subgenomic RNAs expressions and their translational products of Tobacco necrosis virus A Chinese isolate. Chin. Sci. Bull. 2008, 53:1682-1690.
34. Lin N., Hsieh C., Hsu Y. Capsid protein of cucumber mosaic virus accumulates in the nuclei and at the periphery of the nucleoli in infected cells. Arch. Virol. 1996, 141:727-732.
35. Liu H., Wei C., Zhong Y., Li Y. Rice black-streaked dwarf virus minor core protein P8 is a nuclear dimeric protein and represses transcription in tobacco protoplasts. FEBS Lett. 2007, 581:2534-2540.
36. Lommel S.A., Martelli G.P., Rubino L., Russo M. Family Tombusviridae. Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses 2005, 907-936. Elsevier Academic Press, San Diego, CA. C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Eds.).
37. Lot H., Rubino L., Delecolle B., Jacquemond M., Turturo C., Russo M. Characterization, nucleotide sequence and genome organization of leek white stripe virus, a putative new species of the genus Necrovirus. Arch. Virol. 1996, 141:2375-2386.
38. Lucy A.P., Guo H.S., Li W.X., Ding S.W. Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J. 2000, 19:1672-1680.
39. Molnar A., Havelda Z., Dalmay T., Szutorisz H., Burgyan J. Complete nucleotide sequence of tobacco necrosis virus strain DH and genes required for RNA replication and virus movement. J. Gen. Virol. 1997, 78:1235-1239.
40. Nass P., Jakstys B., D'Arcy C. In situ localization of barley yellow dwarf virus coat protein in oats. Phytopathology 1995, 85:556-560.
41. Olspert A., Paves H., Toomela R., Tamm T., Truve E. Cocksfoot mottle sobemovirus coat protein contains two nuclear localization signals. Virus Genes 2010, 40:423-431.
42. Opalka N., Brugidou C., Bonneau C., Nicole M., Beachy R., Yeager M., Fauquet C. Movement of rice yellow mottle virus between xylem cells through pit membranes. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3323-3328.
43. Orit K., Assaf F., Nehama Z., Chaim G., Abraham L. A peptide derived from the N-terminal region of HIV-1 Vpr promotes nuclear import in permeabilized cells: elucidation of the NLS region of the Vpr. FEBS Lett. 1998, 429:421-425.
44. Palmeri D., Malim M.H. Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha. Mol. Cell. Biol. 1999, 19:1218-1225.
45. Pantaleo V., Grieco F., Di Franco A., Martelli G. The role of the C-terminal region of olive latent virus 1 coat protein in host systemic infection. Arch. Virol. 2006, 151:1973-1983.
46. Qi D., Omarov R.T., Scholthof K.-B.G. The complex subcellular distribution of satellite panicum mosaic virus capsid protein reflects its multifunctional role during infection. Virology 2008, 376:154-164.
47. Rajamaki M.L., Valkonen J.P.T. Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Potato virus A in Nicotiana species. Plant Cell 2009, 21:2485-2502.
48. Rao A.L.N. Genome packaging by spherical plant RNA viruses. Annu. Rev. Phytopathol. 2006, 44:61-87.
49. Rexach M., Blobel G. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 1995, 83:683-692.
50. Sacher R., Ahlquist P. Effects of deletions in the N-terminal basic arm of brome mosaic virus coat protein on RNA packaging and systemic infection. J. Virol. 1989, 63:4545-4552.
51. Stockley P.G., Kirsh A.L., Chow E.P., Smart J.E., Harrison S.C. Structure of turnip crinkle virus. III. Identification of a unique coat protein dimer. J. Mol. Biol. 1986, 191:721-725.
52. Tamm T., Truve E. Sobemoviruses. J. Virol. 2000, 74:6231-6241.
53. Truant R., Cullen B.R. The arginine-rich domains present in Human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol. Cell. Biol. 1999, 19:1210-1217.
54. Vaewhongs A.A., Lommel S.A. Virion formation is required for the long-distance movement of Red clover necrotic mosaic virus in movement protein transgenic plants. Virology 1995, 212:607-613.
55. Walter M., Chaban C., Schutze K., Batistic O., Weckermann K., Nake C., Blazevic D., Grefen C., Schumacher K., Oecking C., Harter K., Kudla J. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 2004, 40:428-438.
56. Wang Y., Tzfira T., Gaba V., Citovsky V., Palukaitis P., Gal-On A. Functional analysis of the Cucumber mosaic virus 2b protein: pathogenicity and nuclear localization. J. Gen. Virol. 2004, 85:3135-3147.
57. Weiland J.J., Larson R.L., Freeman T.P., Edwards M.C. First report of Beet black scorch virus in the United States. Plant Dis. 2006, 90:828-1828.
58. Weiland J.J., Van Winkle D., Edwards M.C., Larson R.L., Shelver W.L., Freeman T.P., Liu H.Y. Characterization of a U.S. isolate of Beet black scorch virus. Phytopathology 2007, 97:1245-1254.
59. Whittaker G., Helenius A. Nuclear import and export of viruses and virus genomes. Virology 1998, 246:1-23.
60. Xi D.H., Li J., Han C.G., Li D.W., Yu J.L., Zhou X.P. Complete nucleotide sequence of a new strain of Tobacco necrosis virus A infecting soybean in China and infectivity of its full-length cDNA clone. Virus Genes 2008, 36:259-266.
61. Yuan X.F., Cao Y.H., Xi D.H., Guo L.H., Han C.G., Li D.W., Zhai Y.F., Yu J.L. Analysis of the subgenomic RNAs and the small open reading frames of Beet black scorch virus. J. Gen. Virol. 2006, 87:3077-3086.
62. Zhang X.R., Yuan Y.R., Pei Y., Lin S.S., Tuschl T., Patel D.J., Chua N.H. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006, 20:3255-3268.