Viral nucleolar localisation signals determine dynamic trafficking within the nucleolus

Virology

Volumn 380, Issue 2, 2008, Pages 191-202

  Emmott, Edward ^a   Dove, Brian K ^a   Howell, Gareth ^a   Chappell, Lucy A ^a   Reed, Mark L ^a   Boyne, James R ^a   You, Jae Hwan ^a   Brooks, Gavin ^b   Whitehouse, Adrian ^a   Hiscox, Julian A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

Coronavirus; FLIP; FRAP; Herpesvirus; HIV; Nucleolar trafficking; Nucleolus

Indexed keywords

CHIMERIC PROTEIN; VIRUS PROTEIN;

ARTICLE; BLEACHING; BRONCHITIS; CELL MIGRATION; CONFOCAL MICROSCOPY; CORONAVIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; VIRUS NUCLEOCAPSID;

ANIMALS; ARTIFICIAL GENE FUSION; CAPSID PROTEINS; CELL LINE; CELL NUCLEOLUS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; MICROSCOPY, CONFOCAL; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANS-ACTIVATORS; VIRAL PROTEINS;

AVIAN INFECTIOUS BRONCHITIS VIRUS; CORONAVIRUS; HERPESVIRIDAE; HUMAN IMMUNODEFICIENCY VIRUS 1; SAIMIRIINE HERPESVIRUS 2;

EID: 53249109348     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.05.032     Document Type: Article

References (81)

1. Andersen J.S., Lam Y.W., Leung A.K., Ong S.E., Lyon C.E., Lamond A.I., and Mann M. Nucleolar proteome dynamics. Nature 433 (2005) 77-83
2. Angelier N., Tramier M., Louvet E., Coppey-Moisan M., Savino T.M., De Mey J.R., and Hernandez-Verdun D. Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Mol. Biol. Cell 16 (2005) 2862-2871
3. Axelrod D., Koppel D.E., Schlessinger J., Elson E., and Webb W.W. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J 16 (1976) 1055-1069
4. Bertrand L., and Pearson A. The conserved N-terminal domain of herpes simplex virus 1 UL24 protein is sufficient to induce the spatial redistribution of nucleolin. J. Gen. Virol 89 (2008) 1142-1151
5. Boyne J.R., Colgan K.J., and Whitehouse A. Herpesvirus saimiri ORF57: a post-transcriptional regulatory protein. Front. Biosci 13 (2008) 2928-2938
6. Boyne J.R., and Whitehouse A. Nucleolar trafficking is essential for nuclear export of intronless herpesvirus mRNA. Proc. Natl. Acad. Sci. USA 103 (2006) 15190-15195
7. Carmo-Fonseca M. The contribution of nuclear compartmentalization to gene regulation. Cell 108 (2002) 513-521
8. Carmo-Fonseca M., Mendes-Soares L., and Campos I. To be or not to be in the nucleolus. Nature Cell Biol 2 (2000) E107-E112
9. Cawood R., Harrison S.M., Dove B.K., Reed M.L., and Hiscox J.A. Cell cycle dependent localisation of the coronavirus nucleocapsid protein. Cell Cycle 6 (2007) 863-867
10. Chang J.H., and Olson M.O. A single gene codes for two forms of rat nucleolar protein B23 mRNA. J. Biol. Chem 264 (1989) 11732-11737
11. Chen D., and Huang S. Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J. Cell. Biol 153 (2001) 169-176
12. Chen H., Coote B., Attree S., and Hiscox J.A. Evaluation of a nucleoprotein-based enzyme-linked immunosorbent assay for the detection of antibodies against infectious bronchitis virus. Avian Path 32 (2003) 519-526
13. Chen H., Gill A., Dove B.K., Emmett S.R., Kemp F.C., Ritchie M.A., Dee M., and Hiscox J.A. 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 (2005) 1164-1179
14. Chen H., Wurm T., Britton P., Brooks G., and Hiscox J.A. Interaction of the coronavirus nucleoprotein with nucleolar antigens and the host cell. J. Virol 76 (2002) 5233-5250
15. Cochrane A.W., Perkins A., and Rosen C.A. Identification of sequences important in the nucleolar localization of human immunodeficiency virus Rev: relevance of nucleolar localization to function. J. Virol 64 (1990) 881-885
16. Cooper M., Goodwin D.J., Hall K.T., Stevenson A.J., Meredith D.M., Markham A.F., and Whitehouse A. The gene product encoded by ORF 57 of herpesvirus saimiri regulates the redistribution of the splicing factor SC-35. J. Gen. Virol 80 (1999) 1311-1316
17. Daelemans D., Costes S.V., Cho E.H., Erwin-Cohen R.A., Lockett S., and Pavlakis G.N. In vivo HIV-1 Rev multimerization in the nucleolus and cytoplasm identified by fluorescence resonance energy transfer. J. Biol. Chem 279 (2004) 50167-50175
18. Dove B.K., You J.-H., Reed M.L., Emmett S.R., Brooks G., and Hiscox J.A. Changes in nucleolar architecture and protein profile during coronavirus infection. Cellular Microbiol 8 (2006) 1147-1157
19. Dundr M., Leno G.H., Hammarskjold M.L., Rekosh D., Helga-Maria C., and Olson M.O. The roles of nucleolar structure and function in the subcellular location of the HIV-1 Rev protein. J. Cell. Sci 108 (1995) 2811-2823
20. Dundr M., Misteli T., and Olson M.O. The dynamics of postmitotic reassembly of the nucleolus. J. Cell Biol 150 (2000) 433-446
21. Goodwin D.J., Hall K.T., Stevenson A.J., Markham A.F., and Whitehouse A. The open reading frame 57 gene product of herpesvirus saimiri shuttles between the nucleus and cytoplasm and is involved in viral RNA nuclear export. J. Virol 73 (1999) 10519-10524
22. Goodwin D.J., and Whitehouse A. A gamma-2 herpesvirus nucleocytoplasmic shuttle protein interacts with importin alpha 1 and alpha 5. J. Biol. Chem 276 (2001) 19905-19912
23. Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17 (2003) 1691-1702
24. Hernandez-Verdun D. Nucleolus: from structure to dynamics. Histochem. Cell Biol 125 (2006) 127-137
25. Hernandez-Verdun D., and Roussel P. Regulators of nucleolar functions. Prog. Cell Cycle Res 5 (2003) 301-308
26. Hernandez-Verdun D., Roussel P., and Gebrane-Younes J. Emerging concepts of nucleolar assembly. J. Cell. Sci 115 (2002) 2265-2270
27. Hiscox J.A. Brief review: the nucleolus - a gateway to viral infection?. Arch. Virol 147 (2002) 1077-1089
28. Hiscox J.A. The interaction of animal cytoplasmic RNA viruses with the nucleus to facilitate replication. Virus Res 95 (2003) 13-22
29. Hiscox J.A. RNA viruses: hijacking the dynamic nucleolus. Nature Rev. Microbiol 5 (2007) 119-127
30. Hiscox J.A., Wurm T., Wilson L., Cavanagh D., Britton P., and Brooks G. The coronavirus infectious bronchitis virus nucleoprotein localizes to the nucleolus. J. Virol 75 (2001) 506-512
31. Huang W.H., Yung B.Y., Syu W.J., and Lee Y.H. The nucleolar phosphoprotein B23 interacts with hepatitis delta antigens and modulates the hepatitis delta virus RNA replication. J. Biol. Chem 276 (2001) 25166-25175
32. Kim S.H., Macfarlane S., Kalinina N.O., Rakitina D.V., Ryabov E.V., Gillespie T., Haupt S., Brown J.W., and 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. USA 104 (2007) 11115-11120
33. Kim S.H., Ryabov E.V., Kalinina N.O., Rakitina D.V., Gillespie T., MacFarlane S., Haupt S., Brown J.W., and Taliansky M. Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO J 26 (2007) 2169-2179
34. Kim S.H., Ryabov E.V., Brown J.W., and Taliansky M. Involvement of the nucleolus in plant virus systemic infection. Biochem. Soc. Trans 32 (2004) 557-560
35. Kubota S., Siomi H., Satoh T., Endo S., Maki M., and Hatanaka M. Functional similarity of HIV-I rev and HTLV-I rex proteins: identification of a new nucleolar-targeting signal in rev protein. Biochem. Biophys. Res. Commun 162 (1989) 963-970
36. Kuppuswamy M., Subramanian T., Srinivasan A., and Chinnadurai G. Multiple functional domains of Tat, the trans-activator of HIV-1, defined by mutational analysis. Nuc. Acid. Res 17 (1989) 3551-3561
37. Lam Y.W., Trinkle-Mulcahy L., and Lamond A.I. The nucleolus. J. Cell Sci 118 (2005) 1335-1337
38. Lamond A.I., and Sleeman J.E. Nuclear substructure and dynamics. Current Biol 13 (2003) R825
39. Lee C., Hodgins D., Calvert J.G., Welch S.K., Jolie R., and Yoo D. Mutations within the nuclear localization signal of the porcine reproductive and respiratory syndrome virus nucleocapsid protein attenuate virus replication. Virology 346 (2006) 238-250
40. Lee C.H., Chang S.C., Chen C.J., and Chang M.F. The nucleolin binding activity of hepatitis delta antigen is associated with nucleolus targeting. J. Biol. Chem 273 (1998) 7650-7656
41. Leung A.K., Andersen J.S., Mann M., and Lamond A.I. Bioinformatic analysis of the nucleolus. Biochem J 376 (2003) 553-569
42. Leung A.K., and Lamond A.I. The dynamics of the nucleolus. Crit. Rev. Eukaryot. Gene Expr 13 (2003) 39-54
43. Leung A.K., Trinkle-Mulcahy L., Lam Y.W., Andersen J.S., Mann M., and Lamond A.I. NOPdb: Nucleolar Proteome Database. Nuc. Acid. Res 34 (2006) D218-D220
44. Li Y.P. Protein B23 is an important human factor for the nucleolar localization of the human immunodeficiency virus protein Tat. J. Virol 71 (1997) 4098-4102
45. Louvet E., Junera H.R., Le Panse S., and Hernandez-Verdun D. Dynamics and compartmentation of the nucleolar processing machinery. Exp. Cell Res 304 (2005) 457-470
46. Lymberopoulos M.H., and Pearson A. Involvement of UL24 in herpes-simplex-virus-1-induced dispersal of nucleolin. Virology 363 (2007) 397-409
47. Malik P., and Clements J.B. Protein kinase CK2 phosphorylation regulates the interaction of Kaposi's sarcoma-associated herpesvirus regulatory protein ORF57 with its multifunctional partner hnRNP K. Nuc. Acid. Res 32 (2004) 5553-5569
48. Marasco W.A., Szilvay A.M., Kalland K.H., Helland D.G., Reyes H.M., and Walter R.J. Spatial association of HIV-1 tat protein and the nucleolar transport protein B23 in stably transfected Jurkat T-cells. Arch. Virol 139 (1994) 133-154
49. Matthews D.A., and Olson M.O. What's new in the nucleolus?. EMBO Reports 7 (2006) 1-4
50. Melen K., Kinnunen L., Fagerlund R., Ikonen N., Twu K.Y., Krug R.M., and Julkunen I. Nuclear and nucleolar targeting of influenza A virus NS1 protein: striking differences between different virus subtypes. J. Virol 81 (2007) 5995-6006
51. Michienzi A., Cagnon L., Bahner I., and Rossi J.J. Ribozyme-mediated inhibition of HIV 1 suggests nucleolar trafficking of HIV-1 RNA. Proc. Natl. Acad. Sci. U S A 97 (2000) 8955-8960
52. Michienzi A., De Angelis F.G., Bozzoni I., and Rossi J.J. A nucleolar localizing Rev binding element inhibits HIV replication. AIDS Res. Ther 3 (2006) 13
53. Michienzi A., Li S., Zaia J.A., and Rossi J.J. A nucleolar TAR decoy inhibitor of HIV-1 replication. Proc. Natl. Acad. Sci. USA 99 (2002) 14047-14052
54. Misteli T. Protein dynamics: implications for nuclear architecture and gene expression. Science 291 (2001) 843-847
55. Miyazaki Y., Nosaka T., and Hatanaka M. The post-transcriptional regulator Rev of HIV: implications for its interaction with the nucleolar protein B23. Biochimie 78 (1996) 1081-1086
56. Murayama R., Harada Y., Shibata T., Kuroda K., Hayakawa S., Shimizu K., and Tanaka T. Influenza A virus non-structural protein 1 (NS1) interacts with cellular multifunctional protein nucleolin during infection. Biochem. Biophys. Res. Commun 362 (2007) 880-885
57. Ozawa M., Fujii K., Muramoto Y., Yamada S., Yamayoshi S., Takada A., Goto H., Horimoto T., and Kawaoka Y. Contributions of two nuclear localization signals of influenza A virus nucleoprotein to viral replication. J. Virol 81 (2007) 30-41
58. Pei Y., Hodgins D.C., Lee C., Calvert J.G., Welch S.K., Jolie R., Keith M., and Yoo D. Functional mapping of the porcine reproductive and respiratory syndrome virus capsid protein nuclear localization signal and its pathogenic association. Virus Res 135 (2008) 107-114
59. Perkins A., Cochrane A.W., Ruben S.M., and Rosen C.A. Structural and functional characterization of the human immunodeficiency virus rev protein. J. Acquir. Immune Defic. Syndr 2 (1989) 256-263
60. Phair R.D., and Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature 404 (2000) 604-609
61. Pollard V.W., and Malim M.H. The HIV-1 Rev protein. Annu. Rev. Microbiol 52 (1998) 491-532
62. Reed M.L., Dove B.K., Jackson R.M., Collins R., Brooks G., and Hiscox J.A. Delineation and modelling of a nucleolar retention signal in the coronavirus nucleocapsid protein. Traffic 7 (2006) 833-848
63. Reed M.L., Howell G., Harrison S.M., Spencer K.A., and Hiscox J.A. Characterization of the nuclear export signal in the coronavirus infectious bronchitis virus nucleocapsid protein. J. Virol 81 (2007) 4298-4304
64. Rossi J.J., June C.H., and Kohn D.B. Genetic therapies against HIV. Nat. Biotechnol 25 (2007) 1444-1454
65. Rowland R.R., Kerwin R., Kuckleburg C., Sperlich A., and Benfield D.A. The localisation of porcine reproductive and respiratory syndrome virus nucleocapsid protein to the nucleolus of infected cells and identification of a potential nucleolar localization signal sequence. Virus Res 64 (1999) 1-12
66. Rowland R.R.R., and Yoo D. Nucleolar-cytoplasmic shuttling of PRRSV nucleocapsid protein: a simple case of molecular mimicry or the complex regulation by nuclear import, nucleolar localization and nuclear export signal sequences. Virus Res 95 (2003) 23-33
67. Rubbi C.P., and Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22 (2003) 6068-6077
68. Ruben S., Perkins A., Purcell R., Joung K., Sia R., Burghoff R., Haseltine W.A., and Rosen C.A. Structural and functional characterization of human immunodeficiency virus tat protein. J Virol 63 (1989) 1-8
69. Sheval E.V., Polzikov M.A., Olson M.O.J., and Zatsepina O.V. A higher concentration of an antigen within the nucleolus may prevent its proper recognition by specific antibodies. Eur. J. Histochem. 49 (2005) 117-123
70. Spencer K.A., Dee M., Britton P., and Hiscox J.A. Role of phosphorylation clusters in the biology of the coronavirus infectious bronchitis virus nucleocapsid protein. Virology 370 (2008) 373-381
71. Spencer K.A., and Hiscox J.A. Characterisation of the RNA binding properties of the coronavirus infectious bronchitis virus nucleocapsid protein amino-terminal region. FEBS Lett 580 (2006) 5993-5998
72. Stauber R.H., Afonina E., Gulnik S., Erickson J., and Pavlakis G.N. Analysis of intracellular trafficking and interactions of cytoplasmic HIV-1 Rev mutants in living cells. Virology 251 (1998) 38-48
73. Stenoien D.L., Mielke M., and Mancini M.A. Intranuclear ataxin1 inclusions contain both fast- and slow-exchanging components. Nat. Cell Biol 4 (2002) 806-810
74. Taliansky M.E., and Robinson D.J. Molecular biology of umbraviruses: phantom warriors. J. Gen. Virol 84 (2003) 1951-1960
75. Tijms M.A., van der Meer Y., and Snijder E.J. Nuclear localization of non-structural protein 1 and nucleocapsid protein of equine arteritis virus. J. Gen. Virol 83 (2002) 795-800
76. Weidman M.K., Sharma R., Raychaudhuri S., Kundu P., Tsai W., and Dasgupta A. The interaction of cytoplasmic RNA viruses with the nucleus. Virus Res 95 (2003) 75-85
77. Williams B.J., Boyne J.R., Goodwin D.J., Roaden L., Hautbergue G.M., Wilson S.A., and Whitehouse A. The prototype gamma-2 herpesvirus nucleocytoplasmic shuttling protein, ORF 57, transports viral RNA through the cellular mRNA export pathway. Biochem. J 387 (2005) 295-308
78. Wurm T., Chen H., Britton P., Brooks G., and Hiscox J.A. Localisation to the nucleolus is a common feature of coronavirus nucleoproteins and the protein may disrupt host cell division. J. Virol 75 (2001) 9345-9356
79. Yoo D., Wootton S.K., Li G., Song C., and Rowland R.R. Colocalization and interaction of the porcine arterivirus nucleocapsid protein with the small nucleolar RNA-associated protein fibrillarin. J. Virol 77 (2003) 12173-12183
80. You J.H., Dove B.K., Enjuanes L., DeDiego M.L., Alvarez E., Howell G., Heinen P., Zambon M., and Hiscox J.A. Sub-cellular localisation of the severe acute respiratory syndrome coronavirus nucleocapsid protein. J. Gen. Virol 86 (2005) 3303-3310
81. You J.H., Howell G., Pattnaik A.K., Osorio F.A., and Hiscox J.A. A model for the dynamic nuclear/nucleolar/cytoplasmic trafficking of the porcine reproductive and respiratory syndrome virus (PRRSV) nucleocapsid protein based on live cell imaging. Virology 378 (2008) 34-47