The nucleoprotein and the viral RNA of infectious salmon anemia virus (ISAV) are localized in the nucleolus of infected cells

Virology

Volumn 379, Issue 1, 2008, Pages 55-63

  Goić, Bertsy ^a,b,c   Bustamante, Juanita ^a   Miquel, Alvaro ^a   Alvarez, Marco ^b,c   Vera, M Ines ^b,c   Valenzuela, Pablo D T ^a,b,c   Burzio, Luis O ^a,b,c  

^a Grupo Bios SA   (Chile)

^b Fundacion Ciencia para la Vida   (Chile)

^c UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

In situ hybridization; ISAV; Nucleoli; Nucleolin; Nucleoprotein

Indexed keywords

GENOMIC RNA; MONOCLONAL ANTIBODY; NUCLEOLIN; NUCLEOPROTEIN; VIRUS RNA;

AGRICULTURAL WORKER; ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; CELL COMPARTMENTALIZATION; CELL LINE; GENOMICS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOLUS; ORTHOMYXOVIRUS; PRIORITY JOURNAL; PROTEIN INTERACTION; STAINING; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELL NUCLEOLUS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; ISAVIRUS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; NUCLEOPROTEINS; PHOSPHOPROTEINS; RNA, VIRAL; RNA-BINDING PROTEINS; SALMON; SEQUENCE ALIGNMENT; VIRUS ASSEMBLY; VIRUS REPLICATION;

INFECTIOUS SALMON ANEMIA VIRUS; ISAVIRUS; ORTHOMYXOVIRIDAE;

EID: 49049095668     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.05.036     Document Type: Article

References (48)

1. Alvarez M., Quezada C., Navarro C., Molina A., Bouvet P., Krauskopf M., and Vera M.I. An increased expression of nucleolin is associated with a physiological nucleolar segregation. Biochem. Biophys. Res. Commun. 301 1 (2003) 152-158
2. Amorim M.-J., Read E.K., Dalton R.M., Medcalf L., and Digard P. Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity. Traffic 8 1 (2007) 1-11
3. Aspehaug V., Falk K., Krossoy B., Thevarajan J., Sanders L., Moore L., Endresen C., and Biering E. Infectious salmon anemia virus (ISAV) genomic segment 3 encodes the viral nucleoprotein (NP), an RNA-binding protein with two monopartite nuclear localization signals (NLS). Virus Res. 106 1 (2004) 51-60
4. Aspehaug V., Mikalsen A.B., Snow M., Biering E., and Villoing S. Characterization of the infectious salmon anemia virus fusion protein. J. Virol. 79 19 (2005) 12544-12553
5. Bierin E., Falk K., Hoel E., Thevarajan J., Joerink M., Nylund A., Endresen C., and Krossoyl B. Segment 8 encodes a structural protein of infectious salmon anaemia virus (ISAV); the co-linear transcript from segment 7 probably encodes a non-structural or minor structural protein. Dis. Aquat. Organ. 49 2 (2002) 117-122
6. Bouchard D., Keleher W., Opitz H.M., Blake S., Edwards K.C., and Nicholson B.L. Isolation of infectious salmon anemia virus (ISAV) from Atlantic salmon in New Brunswick, Canada. Dis. Aquat. Organ. 35 2 (1999) 131-137
7. Bouchard D.A., Brockway K., Giray C.W.K., and Merril P.L. First report of infectious salmon anemia (ISA) in United States. Bull. Eur. AQssc. Fish Pathol. 21 (2001) 86-88
8. Clouthier S.C., Rector T., Brown N.E., and Anderson E.D. Genomic organization of infectious salmon anaemia virus. J. Gen. Virol. 83 Pt 2 (2002) 421-428
9. Cros J.F., Garcia-Sastre A., and Palese P. An unconventional NLS is critical for the nuclear import of the influenza A virus nucleoprotein and ribonucleoprotein. Traffic 6 3 (2005) 205-213
10. Cunningham C.O., and Snow M. Genetic analysis of infectious salmon anaemia virus (ISAV) from Scotland. Dis. Aquat. Organ. 41 1 (2000) 1-8
11. Dannevig B.H., Falk K., and Namork E. Isolation of the causal virus of infectious salmon anaemia (ISA) in a long-term cell line from Atlantic salmon head kidney. J. Gen. Virol. 76 Pt 6 (1995) 1353-1359
12. Espinoza J.C., and Kunznar J. Rapid simultaneous detection and quantification of infectious pancreatic necrosis virus (IPNV). J. Virol. Methods 105 (2002) 81-85
13. Falk K., Namork E., Rimstad E., Mjaaland S., and Dannevig B.H. Characterization of infectious salmon anemia virus, an orthomyxo-like virus isolated from Atlantic salmon (Salmo salar L.). J. Virol. 71 12 (1997) 9016-9023
14. Falk K., Aspehaug V., Vlasak R., and Endresen C. Identification and characterization of viral structural proteins of infectious salmon anemia virus. J. Virol. 78 6 (2004) 3063-3071
15. Fijan N., Sulimanovic D., Bearzotti M., Muzinic D., Zwillenberg L.O., and Chilmonczyk S. Some properties of the Epithelioma papulosum cyprini (EPC) cell line from carp Cyprinus carpio. Ann. Virol. Inst. Pasteur 134E (1983) 207-220
16. Fryer J.L., Yusha A., and Pilcher K.S. The in vitro cultivation of tissue and cells of Pacific salmon and steelhead trout. Ann. N. Y. Acad. Sci. 126 1 (1965) 566-586
17. Herz C., Stavnezer E., Krug R., and Gurney Jr. T. Influenza virus, an RNA virus, synthesizes its messenger RNA in the nucleus of infected cells. Cell 26 3 Pt 1 (1981) 391-400
18. Hiscox J.A. The nucleolus-a gateway to viral infection?. Arch. Virol. 147 6 (2002) 1077-1089
19. Hiscox J.A. RNA viruses: hijacking the dynamic nucleolus. Nat. Rev. Microbiol. 5 2 (2007) 119-127
20. Jackson D.A., Caton A.J., McCready S.J., and Cook P.R. Influenza virus RNA is synthesized at fixed sites in the nucleus. Nature 296 5855 (1982) 366-368
21. Jamett A.A.J., Miquel A., Arriagada R., Becker M.I., Valenzuela P., and Burzio L.O. Characteristics of monoclonal antibodies against Piscirickettsia salmonis. J. Fish. Dis. 24 (2001) 205-215
22. Kawaoka Y.C.N.J., Haller O., Hongo S., Kaverin N., Klen H.D., Lamb R.A., McCauley J., Palese P., Rimstad E., and Webster R.G. Infectious salmon anaemia virus. In: Fauquet C.M., Mayo M.A., Maniloff J., and Desselberger U. (Eds). Virus Taxonomy-Eight Report of the International Comitee on Taxonomy Viruses (2005), LA Bull. Elsevier Academic Press, New York
23. Kibenge F.S., Kibenge M.J., McKenna P.K., Stothard P., Marshall R., Kibenge F.S., Lyaku J.R., Rainnie D., and Hammell K.L. Growth of infectious salmon anaemia virus in CHSE-214 cells and evidence for phenotypic differences between virus strains. J. Gen. Virol. 81 1 (2000) 143-150
24. Kibenge F.S., Garate O.N., Johnson G., Arriagada R., Kibenge M.J., and Wadowska D. Isolation and identification of infectious salmon anaemia virus (ISAV) from Coho salmon in Chile. Dis. Aquat. Organ 45 1 (2001) 9-18
25. Krossoy B., Hordvik I., Nilsen F., Nylund A., and Endresen C. The putative polymerase sequence of infectious salmon anemia virus suggests a new genus within the Orthomyxoviridae. J. Virol. 73 3 (1999) 2136-2142
26. 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 13 (1998) 7650-7656
27. Mayer D., Molawi K., Martinez-Sobrido L., Ghanem A., Thomas S., Baginsky S., Grossmann J., Garcia-Sastre A., and Schwemmle M. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J. Proteome Res. 6 2 (2007) 672-682
28. McBeath A.J., Collet B., Paley R., Duraffour S., Aspehaug V., Biering E., Secombes C.J., and Snow M. Identification of an interferon antagonist protein encoded by segment 7 of infectious salmon anaemia virus. Virus Res. 115 2 (2006) 176-184
29. Mjaaland S., Rimstad E., Falk K., and Dannevig B.H. Genomic characterization of the virus causing infectious salmon anemia in Atlantic salmon (Salmo salar L.): an orthomyxo-like virus in a teleost. J. Virol. 71 10 (1997) 7681-7686
30. Osorio M., Espinoza J.C., and Kuznar J. Visualization of infectious pancreatic necrosis virus (IPNV) particles labeled with fluorescent probes. J. Virol. Meth. 120 1-2 (2005) 140-144
31. 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 1 (2007) 30-41
32. Portela A., and Digard P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 83 4 (2002) 723-734
33. Pyper J.M., Clements J.E., and Zink M.C. The nucleolus is the site of Borna disease virus RNA transcription and replication. J. Virol. 72 9 (1998) 7697-7702
34. Rimstad E., Mjaaland S., Snow M., Mikalsen A.B., and Cunningham C.O. Characterization of the infectious salmon anemia virus genomic segment that encodes the putative hemagglutinin. J. Virol. 75 11 (2001) 5352-5356
35. Ritchie R.J., Heppell J., Cook M.B., Jones S., and Griffiths S.G. Identification and characterization of segments 3 and 4 of the ISAV genome. Virus Genes 22 3 (2001) 289-297
36. Schyth B.D., Olesen J.N., Ostergard P., and Falk K. Laboratory diagnosis of infectious salmon anemia (ISA): experience gained from the outbreaks on the Faroe Islands 2000-2003. Diseases of Fishand Shellfish, 11th International Conference of the EAFP 11 (2003) 0-79
37. Snow M., and Cunningham C.O. Characterisation of the putative nucleoprotein gene of infectious salmon anaemia virus (ISAV). Virus Res. 74 1-2 (2001) 111-118
38. Thorud K., and Djubvik H.O. Infectious anemia in Atlantic salmon (Salmo salar). Bull. Eur. Assoc. Fish Pathol. 8 (1988) 109-111
39. Tischler N.D., Galeno H., Rosemblatt M., and Valenzuela P.D. Human and rodent humoral immune responses to Andes virus structural proteins. Virology 334 2 (2005) 319-326
40. Ugrinova I., Monier K., Ivaldi C., Thiry M., Storck S., Mongelard F., and Bouvet P. Inactivation of nucleolin leads to nucleolar disruption, cell cycle arrest and defects in centrosome duplication. BMC Mol. Biol. 8 1 (2007) 1-16
41. Villegas J., Zarraga A.M., Muller I., Montecinos L., Werner E., Brito M., Meneses A.M., and Burzio L.O. A novel chimeric mitochondrial RNA localized in the nucleus of mouse sperm. DNA Cell Biol. 19 9 (2000) 579-588
42. Villegas J., Araya P., Bustos-Obregon E., and Burzio L.O. Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells. Mol. Hum. Reprod. 8 11 (2002) 977-983
43. Villegas J., Burzio V., Villota C., Landerer E., Martinez R., Santander M., Martinez R., Pinto R., Vera M.I., Boccardo E., Villa L.L., and Burzio L.O. Expression of a novel non-coding mitochondrial RNA in human proliferating cells. Nucleic Acids Res. 35 21 (2007) 7336-7347
44. Weber J.D., Kuo M.L., Bothner B., DiGiammarino E.L., Kriwacki R.W., Roussel M.F., and Sherr C.J. Cooperative signals governing ARF-mdm2 interaction and nucleolar localization of the complex. Mol. Cell. Biol. 20 7 (2000) 2517-2528
45. Wergeland H.I., and Jakobsen R.A. A salmonid cell line (TO) for production of infectious salmon anaemia virus (ISAV). Dis. Aquat. Organ. 44 3 (2001) 183-190
46. Wilhelm V., Soza C., Martinez R., Rosemblatt M., Burzio L.O., and Valenzuela P.D. Production and immune response of recombinant Hsp60 and Hsp70 from the salmon pathogen Piscirickettsia salmonis. Biol. Res. 38 1 (2005) 69-82
47. Wilhelm V., Miquel A., Burzio L.O., Rosemblatt M., Engel E., Valenzuela S., Parada G., and Valenzuela P.D. A vaccine against the salmonid pathogen Piscirickettsia salmonis based on recombinant proteins. Vaccine 24 23 (2006) 5083-5091
48. Wu W.W., Sun Y.H., and Pante N. Nuclear import of influenza A viral ribonucleoprotein complexes is mediated by two nuclear localization sequences on viral nucleoprotein. Virol. J. 4 (2007) 1-12