RNA induced polymerization of the Borna disease virus nucleoprotein

Virology

Volumn 397, Issue 1, 2010, Pages 64-72

  Hock, Miriam ^a   Kraus, Ina ^b   Schoehn, Guy ^a,c   Jamin, Marc ^a   Andrei Selmer, Cornelia ^d   Garten, Wolfgang ^b   Weissenhorn, Winfried ^a  

^a UNIV GRENOBLE ALPES   (France)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

Borna disease virus; Genomic ssRNA; Nucleocapsid; Nucleoprotein; Phosphoprotein

Indexed keywords

NUCLEOPROTEIN; PHOSPHOPROTEIN; POLYMER; VIRUS RNA;

5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ARTICLE; BORNA DISEASE VIRUS; CARBOXY TERMINAL SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN POLYMERIZATION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

BORNA DISEASE VIRUS; RABIES VIRUS; RNA VIRUSES; VESICULAR STOMATITIS VIRUS;

EID: 73949090555     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.11.016     Document Type: Article

References (94)

1. Albertini A.A.V., Wernimont A.K., Muziol T., Ravelli R.B.G., Clapier C.R., Schoehn G., Weissenhorn W., and Ruigrok R.W.H. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science (New York, N.Y.) 313 5785 (2006) 360-363
2. Albertini A.A.V., Clapier C.R., Wernimont A.K., Schoehn G., Weissenhorn W., and Ruigrok R.W.H. Isolation and crystallization of a unique size category of recombinant Rabies virus Nucleoprotein-RNA rings. J. Struct. Biol. 158 1 (2007) 129-133
3. Albertini A.A.V., Schoehn G., Weissenhorn W., and Ruigrok R.W.H. Structural aspects of rabies virus replication. Cell. Mol. Life Sci.: CMLS 65 2 (2008) 282-294
4. Baudin F., Bach C., Cusack S., and Ruigrok R.W. Structure of influenza virus RNP: I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. EMBO J. 13 13 (1994) 3158-3165
5. Berg M., Ehrenborg C., Blomberg J., Pipkorn R., and Berg A.L. Two domains of the Borna disease virus p40 protein are required for interaction with the p23 protein. J. Gen. Virol. 79 Pt. 12 (1998) 2957-2963
6. Blumberg B.M., Giorgi C., and Kolakofsky D. N protein of vesicular stomatitis virus selectively encapsidates leader RNA in vitro. Cell 32 2 (1983) 559-567
7. Bourhis J.-M., Canard B., and Longhi S. Structural disorder within the replicative complex of measles virus: functional implications. Virology 344 1 (2006) 94-110
8. Chase G., Mayer D., Hildebrand A., Frank R., Hayashi Y., Tomonaga K., and Schwemmle M. Borna disease virus matrix protein is an integral component of the viral ribonucleoprotein complex that does not interfere with polymerase activity. J. Virol. 81 2 (2007) 743-749
9. Chen Z., Green T.J., Luo M., and Li H. Visualizing the RNA molecule in the bacterially expressed vesicular stomatitis virus nucleoprotein-RNA complex. Structure (London, England: 1993) 12 2 (2004) 227-235
10. Choudhary S.K., Malur A.G., Huo Y., De B.P., and Banerjee A.K. Characterization of the oligomerization domain of the phosphoprotein of human parainfluenza virus type 3. Virology 302 2 (2002) 373-382
11. Cox R., Green T.J., Qiu S., Kang J., Tsao J., Prevelige P.E., He B., and Luo M. Characterization of a mumps virus nucleocapsid-like particle. J. Virol. 83 21 (2009) 11402-11406
12. Cubitt B., and de la Torre J.C. Borna disease virus (BDV), a nonsegmented RNA virus, replicates in the nuclei of infected cells where infectious BDV ribonucleoproteins are present. J. Virol. 68 3 (1994) 1371-1381
13. Cubitt B., Oldstone C., Valcarcel J., and Carlos de la Torre J. RNA splicing contributes to the generation of mature mRNAs of Borna disease virus, a non-segmented negative strand RNA virus. Virus Res. 34 1 (1994) 69-79
14. Curran J. A role for the Sendai virus P protein trimer in RNA synthesis. J. Virol. 72 5 (1998) 4274-4280
15. Curran J., Marq J.B., and Kolakofsky D. An N-terminal domain of the Sendai paramyxovirus P protein acts as a chaperone for the NP protein during the nascent chain assembly step of genome replication. J. Virol. 69 2 (1995) 849-855
16. Dolnik O., Kolesnikova L., and Becker S. Filoviruses: interactions with the host cell. Cell. Mol. Life Sci.: CMLS 65 5 (2008) 756-776
17. Duesberg P.H. Distinct subunits of the ribonucleoprotein of influenza virus. J. Mol. Biol. 42 3 (1969) 485-499
18. Emerson S.U., and Schubert M. Location of the binding domains for the RNA polymerase L and the ribonucleocapsid template within different halves of the NS phosphoprotein of vesicular stomatitis virus. Proc. Natl. Acad. Sci. U. S. A. 84 16 (1987) 5655-5659
19. Emerson S.U., and Wagner R.R. Dissociation and reconstitution of the transcriptase and template activities of vesicular stomatitis B and T virions. J. Virol. 10 2 (1972) 297-309
20. Emerson S.U., and Yu Y. Both NS and L proteins are required for in vitro RNA synthesis by vesicular stomatitis virus. J. Virol. 15 6 (1975) 1348-1356
21. Fooks A.R., Stephenson J.R., Warnes A., Dowsett A.B., Rima B.K., and Wilkinson G.W. Measles virus nucleocapsid protein expressed in insect cells assembles into nucleocapsid-like structures. J. Gen. Virol. 74 Pt. 7 (1993) 1439-1444
22. Gerard F.C.A., Ribeiro E.d.A., Albertini A.A.V., Gutsche I., Zaccai G., Ruigrok R.W.H., and Jamin M. Unphosphorylated rhabdoviridae phosphoproteins form elongated dimers in solution. Biochemistry 46 36 (2007) 10328-10338
23. Gerard F.C.A., Ribeiro E.d.A., Leyrat C., Ivanov I., Blondel D., Longhi S., Ruigrok R.W.H., and Jamin M. Modular organization of rabies virus phosphoprotein. J. Mol. Biol. 388 5 (2009) 978-996
24. Gigant B., Iseni F., Gaudin Y., Knossow M., and Blondel D. Neither phosphorylation nor the amino-terminal part of rabies virus phosphoprotein is required for its oligomerization. J. Gen. Virol. 81 Pt. 7 (2000) 1757-1761
25. Gomis-Rüth F.X., Dessen A., Timmins J., Bracher A., Kolesnikowa L., Becker S., Klenk H.D., and Weissenhorn W. The matrix protein VP40 from Ebola virus octamerizes into pore-like structures with specific RNA binding properties. Structure (London, England: 1993) 11 4 (2003) 423-433
26. Green T.J., and Luo M. Resolution improvement of X-ray diffraction data of crystals of a vesicular stomatitis virus nucleocapsid protein oligomer complexed with RNA. Acta Crystallogr., D Biol. Crystallogr. 62 Pt. 5 (2006) 498-504
27. Green T.J., Zhang X., Wertz G.W., and Luo M. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science (New York, N.Y.) 313 5785 (2006) 357-360
28. Günzl A., Palfi Z., and Bindereif A. Analysis of RNA-protein complexes by oligonucleotide-targeted RNase H digestion. Methods (San Diego, Calif.) 26 2 (2002) 162-169
29. Habjan M., Andersson I., Klingström J., Schümann M., Martin A., Zimmermann P., Wagner V., Pichlmair A., Schneider U., Mühlberger E., Mirazimi A., and Weber F. Processing of genome 5' termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS One 3 4 (2008) e2032
30. Hoenen T., Volchkov V., Kolesnikova L., Mittler E., Timmins J., Ottmann M., Reynard O., Becker S., and Weissenhorn W. VP40 octamers are essential for Ebola virus replication. J. Virol. 79 3 (2005) 1898-1905
31. Honkavuori K.S., Shivaprasad H.L., Williams B.L., Quan P.L., Hornig M., Street C., Palacios G., Hutchison S.K., Franca M., Egholm M., Briese T., and Lipkin W.I. Novel Borna virus in psittacine birds with proventricular dilatation disease. Emerg. Infect. Dis. 14 12 (2008) 1883-1886
32. Horikami S.M., and Moyer S.A. Alternative amino acids at a single site in the Sendai virus L protein produce multiple defects in RNA synthesis in vitro. Virology 211 2 (1995) 577-582
33. Houben K., Marion D., Tarbouriech N., Ruigrok R.W.H., and Blanchard L. Interaction of the C-terminal domains of Sendai virus N and P proteins: comparison of polymerase-nucleocapsid interactions within the paramyxovirus family. J. Virol. 81 13 (2007) 6807-6816
34. Imai Y., Matsushima Y., Sugimura T., and Terada M. A simple and rapid method for generating a deletion by PCR. Nucleic Acids Res. 19 10 (1991) 2785
35. Iseni F., Barge A., Baudin F., Blondel D., and Ruigrok R.W. Characterization of rabies virus nucleocapsids and recombinant nucleocapsid-like structures. J. Gen. Virol. 79 Pt. 12 (1998) 2909-2919
36. Karlin D., Ferron F., Canard B., and Longhi S. Structural disorder and modular organization in Paramyxovirinae N and P. J. Gen. Virol. 84 Pt. 12 (2003) 3239-3252
37. Kingston R.L., Baase W.A., and Gay L.S. Characterization of nucleocapsid binding by the measles virus and mumps virus phosphoproteins. J. Virol. 78 16 (2004) 8630-8640
38. Kliche S., Stitz L., Mangalam H., Shi L., Binz T., Niemann H., Briese T., and Lipkin W.I. Characterization of the Borna disease virus phosphoprotein, p23. J. Virol. 70 11 (1996) 8133-8137
39. Kobayashi T., Shoya Y., Koda T., Takashima I., Lai P.K., Ikuta K., Kakinuma M., and Kishi M. Nuclear targeting activity associated with the amino terminal region of the Borna disease virus nucleoprotein. Virology 243 1 (1998) 188-197
40. Kobayashi T., Watanabe M., Kamitani W., Tomonaga K., and Ikuta K. Translation initiation of a bicistronic mRNA of Borna disease virus: a 16-kDa phosphoprotein is initiated at an internal start codon. Virology 277 2 (2000) 296-305
41. Kohno T., Goto T., Takasaki T., Morita C., Nakaya T., Ikuta K., Kurane I., Sano K., and Nakai M. Fine structure and morphogenesis of Borna disease virus. J. Virol. 73 1 (1999) 760-766
42. Kolakofsky D., Le Mercier P., Iseni F., and Garcin D. Viral DNA polymerase scanning and the gymnastics of Sendai virus RNA synthesis. Virology 318 2 (2004) 463-473
43. Kouznetzoff A., Buckle M., and Tordo N. Identification of a region of the rabies virus N protein involved in direct binding to the viral RNA. J. Gen. Virol. 79 Pt. 5 (1998) 1005-1013
44. Lata S., Roessle M., Solomons J., Jamin M., Gottlinger H.G., Svergun D.I., and Weissenhorn W. Structural basis for autoinhibition of ESCRT-III CHMP3. J. Mol. Biol. 378 4 (2008) 818-827
45. Luo M., Green T.J., Zhang X., Tsao J., and Qiu S. Structural comparisons of the nucleoprotein from three negative strand RNA virus families. Virol. J. 4 (2007) 72
46. Maclellan K., Loney C., Yeo R.P., and Bhella D. The 24-angstrom structure of respiratory syncytial virus nucleocapsid protein-RNA decameric rings. J. Virol. 81 17 (2007) 9519-9524
47. Masters P.S., and Banerjee A.K. Complex formation with vesicular stomatitis virus phosphoprotein NS prevents binding of nucleocapsid protein N to nonspecific RNA. J. Virol. 62 8 (1988) 2658-2664
48. Mavrakis M., Kolesnikova L., Schoehn G., Becker S., and Ruigrok R.W.H. Morphology of Marburg virus NP-RNA. Virology 296 2 (2002) 300-307
49. Mavrakis M., Iseni F., Mazza C., Schoehn G., Ebel C., Gentzel M., Franz T., and Ruigrok R.W.H. Isolation and characterisation of the rabies virus N degrees-P complex produced in insect cells. Virology 305 2 (2003) 406-414
50. Mayer D., Baginsky S., and Schwemmle M. Isolation of viral ribonucleoprotein complexes from infected cells by tandem affinity purification. Proteomics 5 17 (2005) 4483-4487
51. Mellon M.G., and Emerson S.U. Rebinding of transcriptase components (L and NS proteins) to the nucleocapsid template of vesicular stomatitis virus. J. Virol. 27 3 (1978) 560-567
52. Möller P., Pariente N., Klenk H.-D., and Becker S. Homo-oligomerization of Marburg virus VP35 is essential for its function in replication and transcription. J. Virol. 79 23 (2005) 14876-14886
53. Money V.A., McPhee H.K., Mosely J.A., Sanderson J.M., and Yeo R.P. Surface features of a Mononegavirales matrix protein indicate sites of membrane interaction. Proc. Natl. Acad. Sci. U. S. A. 106 11 (2009) 4441-4446
54. Murphy M.F., and Lazzarini R.A. Synthesis of viral mRNA and polyadenylate by a ribonucleoprotein complex from extracts of VSV-infected cells. Cell 3 1 (1974) 77-84
55. Neumann P., Lieber D., Meyer S., Dautel P., Kerth A., Kraus I., Garten W., and Stubbs M.T. Crystal structure of the Borna disease virus matrix protein (BDV-M) reveals ssRNA binding properties. Proc. Natl. Acad. Sci. U. S. A. 106 10 (2009) 3710-3715
56. Pattnaik A.K., Ball L.A., LeGrone A.W., and Wertz G.W. Infectious defective interfering particles of VSV from transcripts of a cDNA clone. Cell 69 6 (1992) 1011-1020
57. Perez M., Sanchez A., Cubitt B., Rosario D., and de la Torre J.C. A reverse genetics system for Borna disease virus. J. Gen. Virol. 84 Pt. 11 (2003) 3099-3104
58. Pleschka S., Staeheli P., Kolodziejek J., Richt J.A., Nowotny N., and Schwemmle M. Conservation of coding potential and terminal sequences in four different isolates of Borna disease virus. J. Gen. Virol. 82 Pt. 11 (2001) 2681-2690
59. Poenisch M., Wille S., Ackermann A., Staeheli P., and Schneider U. The X protein of Borna disease virus serves essential functions in the viral multiplication cycle. J. Virol. 81 13 (2007) 7297-7299
60. Poenisch M., Staeheli P., and Schneider U. Viral accessory protein X stimulates the assembly of functional Borna disease virus polymerase complexes. J. Gen. Virol. 89 Pt. 6 (2008) 1442-1445
61. Portner A., and Murti K.G. Localization of P, NP, and M proteins on Sendai virus nucleocapsid using immunogold labeling. Virology 150 2 (1986) 469-478
62. Price S.R., Ito N., Oubridge C., Avis J.M., and Nagai K. Crystallization of RNA-protein complexes: I. Methods for the large-scale preparation of RNA suitable for crystallographic studies. J. Mol. Biol. 249 2 (1995) 398-408
63. Pyper J.M., and Gartner A.E. Molecular basis for the differential subcellular localization of the 38- and 39-kilodalton structural proteins of Borna disease virus. J. Virol. 71 7 (1997) 5133-5139
64. Richt J.A., and Rott R. Borna disease virus: a mystery as an emerging zoonotic pathogen. Vet. J. (Lond. Eng., 1997) 161 1 (2001) 24-40
65. Richt J.A., Clements J.E., Herzog S., Pyper J., Wahn K., and Becht H. Analysis of virus-specific RNA species and proteins in Freon-113 preparations of the Borna disease virus. Med. Microbiol. Immunol. 182 5 (1993) 271-280
66. Rott R., and Becht H. Natural and experimental Borna disease in animals. Curr. Top. Microbiol. Immunol. 190 (1995) 17-30
67. Rudolph M.G., Kraus I., Dickmanns A., Eickmann M., Garten W., and Ficner R. Crystal structure of the Borna disease virus nucleoprotein. Structure (Lond. Eng., 1993) 11 10 (2003) 1219-1226
68. Schmid S., Mayer D., Schneider U., and Schwemmle M. Functional characterization of the major and minor phosphorylation sites of the P protein of Borna disease virus. J. Virol. 81 11 (2007) 5497-5507
69. Schneider U. Novel insights into the regulation of the viral polymerase complex of neurotropic Borna disease virus. Virus Res. 111 2 (2005) 148-160
70. Schneider P.A., Schneemann A., and Lipkin W.I. RNA splicing in Borna disease virus, a nonsegmented, negative-strand RNA virus. J. Virol. 68 8 (1994) 5007-5012
71. Schneider U., Naegele M., Staeheli P., and Schwemmle M. Active Borna disease virus polymerase complex requires a distinct nucleoprotein-to-phosphoprotein ratio but no viral X protein. J. Virol. 77 21 (2003) 11781-11789
72. Schneider U., Blechschmidt K., Schwemmle M., and Staeheli P. Overlap of interaction domains indicates a central role of the P protein in assembly and regulation of the Borna disease virus polymerase complex. J. Biol. Chem. 279 53 (2004) 55290-55296
73. Schneider U., Naegele M., and Staeheli P. Regulation of the Borna disease virus polymerase complex by the viral nucleoprotein p38 isoform. Brief Report. Arch. Virol. 149 7 (2004) 1409-1414
74. Schneider U., Schwemmle M., and Staeheli P. Genome trimming: a unique strategy for replication control employed by Borna disease virus. Proc. Natl. Acad. Sci. U. S. A. 102 9 (2005) 3441-3446
75. Schneider U., Martin A., Schwemmle M., and Staeheli P. Genome trimming by Borna disease viruses: viral replication control or escape from cellular surveillance?. Cell. Mol. Life Sci.: CMLS 64 9 (2007) 1038-1042
76. Schoehn G., Iseni F., Mavrakis M., Blondel D., and Ruigrok R.W. Structure of recombinant rabies virus nucleoprotein-RNA complex and identification of the phosphoprotein binding site. J. Virol. 75 1 (2001) 490-498
77. Schoehn G., Mavrakis M., Albertini A., Wade R., Hoenger A., and Ruigrok R.W.H. The 12 A structure of trypsin-treated measles virus N-RNA. J. Mol. Biol. 339 2 (2004) 301-312
78. Schoehn G., El Bakkouri M., Fabry C.M.S., Billet O., Estrozi L.F., Le L., Curiel D.T., Kajava A.V., Ruigrok R.W.H., and Kremer E.J. Three-dimensional structure of canine adenovirus serotype 2 capsid. J. Virol. 82 7 (2008) 3192-3203
79. Schwardt M., Mayer D., Frank R., Schneider U., Eickmann M., Planz O., Wolff T., and Schwemmle M. The negative regulator of Borna disease virus polymerase is a non-structural protein. J. Gen. Virol. 86 Pt. 11 (2005) 3163-3169
80. Schwemmle M., De B., Shi L., Banerjee A., and Lipkin W.I. Borna disease virus P-protein is phosphorylated by protein kinase C epsilon and casein kinase II. J. Biol. Chem. 272 35 (1997) 21818-21823
81. Schwemmle M., Salvatore M., Shi L., Richt J., Lee C.H., and Lipkin W.I. Interactions of the Borna disease virus P, N, and X proteins and their functional implications. J. Biol. Chem. 273 15 (1998) 9007-9012
82. Schwemmle M., Jehle C., Shoemaker T., and Lipkin W.I. Characterization of the major nuclear localization signal of the Borna disease virus phosphoprotein. J. Gen. Virol. 80 Pt. 1 (1999) 97-100
83. Shoya Y., Kobayashi T., Koda T., Ikuta K., Kakinuma M., and Kishi M. Two proline-rich nuclear localization signals in the amino- and carboxyl-terminal regions of the Borna disease virus phosphoprotein. J. Virol. 72 12 (1998) 9755-9762
84. Spehner D., Kirn A., and Drillien R. Assembly of nucleocapsidlike structures in animal cells infected with a vaccinia virus recombinant encoding the measles virus nucleoprotein. J. Virol. 65 11 (1991) 6296-6300
85. Szilágyi J.F., and Uryvayev L. Isolation of an infectious ribonucleoprotein from vesicular stomatitis virus containing an active RNA transcriptase. J. Virol. 11 2 (1973) 279-286
86. Tarbouriech N., Curran J., Ebel C., Ruigrok R.W., and Burmeister W.P. On the domain structure and the polymerization state of the Sendai virus P protein. Virology 266 1 (2000) 99-109
87. Tarbouriech N., Curran J., Ruigrok R.W., and Burmeister W.P. Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat. Struct. Biol. 7 9 (2000) 777-781
88. Tomonaga K., Kobayashi T., Lee B.-J., Watanabe M., Kamitani W., and Ikuta K. Identification of alternative splicing and negative splicing activity of a nonsegmented negative-strand RNA virus, Borna disease virus. Proc. Natl. Acad. Sci. U. S. A. 97 23 (2000) 12788-12793
89. Toriumi H., and Kawai A. Association of rabies virus nominal phosphoprotein (P) with viral nucleocapsid (NC) is enhanced by phosphorylation of the viral nucleoprotein (N). Microbiol. Immunol. 48 5 (2004) 399-409
90. Walker M.P., Jordan I., Briese T., Fischer N., and Lipkin W.I. Expression and characterization of the Borna disease virus polymerase. J. Virol. 74 9 (2000) 4425-4428
91. Yanai H., Hayashi Y., Watanabe Y., Ohtaki N., Kobayashi T., Nozaki Y., Ikuta K., and Tomonaga K. Development of a novel Borna disease virus reverse genetics system using RNA polymerase II promoter and SV40 nuclear import signal. Microbes Infect./Institut Pasteur 8 6 (2006) 1522-1529
92. Yanai H., Kobayashi T., Hayashi Y., Watanabe Y., Ohtaki N., Zhang G., de la Torre J.C., Ikuta K., and Tomonaga K. A methionine-rich domain mediates CRM1-dependent nuclear export activity of Borna disease virus phosphoprotein. J. Virol. 80 3 (2006) 1121-1129
93. Yang J., Hooper D.C., Wunner W.H., Koprowski H., Dietzschold B., and Fu Z.F. The specificity of rabies virus RNA encapsidation by nucleoprotein. Virology 242 1 (1998) 107-117
94. Zhang X., Green T.J., Tsao J., Qiu S., and Luo M. Role of intermolecular interactions of vesicular stomatitis virus nucleoprotein in RNA encapsidation. J. Virol. 82 2 (2008) 674-682