Nucleocytoplasmic shuttling of viral proteins in Borna disease virus infection

Viruses

Volumn 5, Issue 8, 2013, Pages 1978-1990

  Honda, Tomoyuki ^a   Tomonaga, Keizo ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Borna disease virus; NES; NLS; Replication; RNP

Indexed keywords

DIHYDROLIPOAMIDE DEHYDROGENASE; GLYCINE DEHYDROGENASE (DECARBOXYLATING); GUANINE NUCLEOTIDE BINDING PROTEIN; LARGE PROTEIN; NUCLEOPROTEIN; PHOSPHOPROTEIN; PROTEIN X; RIBONUCLEOPROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; X PROTEIN;

BORNA DISEASE; BORNA DISEASE VIRUS; CELL NUCLEUS; CYTOPLASM; MONONEGAVIRALES; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; RNA VIRUS; VIRUS REPLICATION;

BORNA DISEASE VIRUS; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION, VIRAL; PROTEIN TRANSPORT; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84881528677     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v5081978     Document Type: Review

References (50)

1. Pletnikov, M.V.; Rubin, S.A.; Vasudevan, K.; Moran, T.H.; Carbone, K.M. Developmental brain injury associated with abnormal play behavior in neonatally Borna disease virus-infected Lewis rats: A model of autism. Behav. Brain Res. 1999, 100, 43-50.
2. Hornig, M.; Solbrig, M.; Horscroft, N.; Weissenböck, H.; Lipkin, W.I. Borna disease virus infection of adult and neonatal rats: Models for neuropsychiatric disease. Curr. Top. Microbiol. Immunol. 2001, 253, 157-177.
3. Schwemmle, M. Interactions of the borna disease virus P, N, and X proteins and their functional implications. J. Biol. Chem. 1998, 273, 9007-9012.
4. Rudolph, M.G.; Kraus, I.; Dickmanns, A.; Eickmann, M.; Garten, W.; Ficner, R. Crystal structure of the borna disease virus nucleoprotein. Structure 2003, 11, 1219-1226.
5. Schneider, U.; Naegele, M.; Staeheli, P.; Schwemmle, M. Active borna disease virus polymerase complex requires a distinct nucleoprotein-to-phosphoprotein ratio but no viral X protein. J. Virol. 2003, 77, 11781-11789.
6. Perez, M.; Sanchez, A.; Cubitt, B.; Rosario, D.; de la Torre, J.C. A reverse genetics system for Borna disease virus. J. Gen. Virol. 2003, 84, 3099-3104.
7. Kraus, I.; Eickmann, M.; Kiermayer, S.; Scheffczik, H.; Fluess, M.; Richt, J.A.; Garten, W. Open reading frame III of borna disease virus encodes a nonglycosylated matrix protein. J. Virol. 2001, 75, 12098-12104.
8. Bajramovic, J.J.; Münter, S.; Syan, S.; Nehrbass, U.; Brahic, M.; Gonzalez-Dunia, D. Borna disease virus glycoprotein is required for viral dissemination in neurons. J. Virol. 2003, 77, 12222-12231.
9. Honda, T.; Horie, M.; Daito, T.; Ikuta, K.; Tomonaga, K. Molecular chaperone BiP interacts with Borna disease virus glycoprotein at the cell surface. J. Virol. 2009, 83, 12622-12625.
10. Matsumoto, Y.; Hayashi, Y.; Omori, H.; Honda, T.; Daito, T.; Horie, M.; Ikuta, K.; Fujino, K.; Nakamura, S.; Schneider, U.; Chase, G.; Yoshimori, T.; Schwemmle, M.; Tomonaga, K. Bornavirus closely associates and segregates with host chromosomes to ensure persistent intranuclear infection. Cell Host Microbe 2012, 11, 492-503.
11. Fulcher, A.J.; Jans, D.A. Regulation of nucleocytoplasmic trafficking of viral proteins: an integral role in pathogenesis? Biochim. Biophys. Acta 2011, 1813, 2176-2190.
12. Nakielny, S.; Dreyfuss, G. Transport of proteins and RNAs in and out of the nucleus. Cell 1999, 99, 677-690.
13. Whittaker, G.R.; Helenius, A. Nuclear import and export of viruses and virus genomes. Virology 1998, 246, 1-23.
14. Hutchinson, E.C.; Fodor, E. Nuclear import of the influenza A virus transcriptional machinery. Vaccine 2012, 30, 7353-7358.
15. Tomonaga, K.; Kobayashi, T.; Ikuta, K. Molecular and cellular biology of Borna disease virus infection. Microb. Infect. 2002, 4, 491-500.
16. Yanai, H.; Kobayashi, T.; Hayashi, Y.; Ohtaki, N.; Zhang, G.; De, J.C.; Ikuta, K.; Tomonaga, K.; Watanabe, Y.; Carlos, J.; Torre, D. A methionine-rich domain mediates CRM1-dependent nuclear export activity of borna disease virus phosphoprotein a methionine-rich domain mediates CRM1-dependent nuclear export activity of borna disease virus phosphoprotein. J. Virol. 2006, 80, 1121-1129.
17. Kobayashi, T.; Zhang, G.; Lee, B.-J.; Baba, S.; Yamashita, M.; Kamitani, W.; Yanai, H.; Tomonaga, K.; Ikuta, K. Modulation of borna disease virus phosphoprotein nuclear localization by the viral protein X encoded in the overlapping open reading frame. J. Virol. 2003, 77, 8099-8107.
18. Pyper, J.M.; Gartner, A.E. Molecular basis for the differential subcellular localization of the 38-and 39-kilodalton structural proteins of Borna disease virus. J. Virol. 1997, 71, 5133-5139.
19. Kobayashi, T.; Shoya, Y.; Koda, T.; Takashima, I.; Lai, P.K.; Ikuta, K.; Kakinuma, M.; Kishi, M. Nuclear targeting activity associated with the amino terminal region of the Borna disease virus nucleoprotein. Virology 1998, 243, 188-197.
20. Kobayashi, T.; Kamitani, W.; Zhang, G.; Watanabe, M.; Tomonaga, K.; Ikuta, K. Borna disease virus nucleoprotein requires both nuclear localization and export activities for viral nucleocytoplasmic shuttling. J. Virol. 2001, 75, 3404-3412.
21. Berg, M.; Ehrenborg, C.; Blomberg, J.; Pipkorn, R.; Berg, A.L. Two domains of the Borna disease virus p40 protein are required for interaction with the p23 protein. J. Gen. Virol. 1998, 79, 2957-2963.
22. Schwemmle, M. Borna disease virus P-protein is phosphorylated by protein kinase cepsilon and casein kinase II. J. Biol. Chem. 1997, 272, 21818-21823.
23. Schmid, S.; Mayer, D.; Schneider, U.; Schwemmle, M. Functional characterization of the major and minor phosphorylation sites of the P protein of Borna disease virus. J. Virol. 2007, 81, 5497-5507.
24. Kamitani, W.; Ono, E.; Yoshino, S.; Kobayashi, T.; Taharaguchi, S.; Lee, B.-J.; Yamashita, M.; Kobayashi, T.; Okamoto, M.; Taniyama, H.; Tomonaga, K.; Ikuta, K. Glial expression of Borna disease virus phosphoprotein induces behavioral and neurological abnormalities in transgenic mice. Proc. Natl. Acad. Sci. USA 2003, 100, 8969-8974.
25. Honda, T.; Fujino, K.; Okuzaki, D.; Ohtaki, N.; Matsumoto, Y.; Horie, M.; Daito, T.; Itoh, M.; Tomonaga, K. Upregulation of insulin-like growth factor binding protein 3 in astrocytes of transgenic mice that express Borna disease virus phosphoprotein. J. Virol. 2011, 85, 4567-4571.
26. Shoya, Y.; Kobayashi, T.; Koda, T.; Ikuta, K.; Kakinuma, M.; Kishi, M. Two proline-rich nuclear localization signals in the amino-and Carboxyl-terminal regions of the borna disease virus phosphoprotein. J. Virol. 1998, 72, 9755-9762.
27. Schwemmle, M.; Jehle, C.; Shoemaker, T.; Lipkin, W.I. Characterization of the major nuclear localization signal of the Borna disease virus phosphoprotein. J. Gen. Virol. 1999, 80, 97-100.
28. Schneider, U.; Blechschmidt, K.; Schwemmle, M.; 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. 2004, 279, 55290-55296.
29. Poenisch, M.; Unterstab, G.; Wolff, T.; Staeheli, P.; Schneider, U. The X protein of Borna disease virus regulates viral polymerase activity through interaction with the P protein. J. Gen. Virol. 2004, 85, 1895-1898.
30. Poenisch, M.; Wille, S.; Ackermann, A.; Staeheli, P.; Schneider, U. The X protein of borna disease virus serves essential functions in the viral multiplication cycle. J. Virol. 2007, 81, 7297-7299.
31. Hayashi, Y.; Horie, M.; Daito, T.; Honda, T.; Ikuta, K.; Tomonaga, K. Heat shock cognate protein 70 controls Borna disease virus replication via interaction with the viral non-structural protein X. Microb. Infect. 2009, 11, 394-402.
32. Wolff, T.; Unterstab, G.; Heins, G.; Richt, J.A.; Kann, M. Characterization of an unusual importin alpha binding motif in the borna disease virus p10 protein that directs nuclear import. J. Biol. Chem. 2002, 277, 12151-12157.
33. Wolff, T.; Pfleger, R.; Wehner, T.; Reinhardt, J.; Richt, J.A. A short leucine-rich sequence in the Borna disease virus p10 protein mediates association with the viral phospho-and nucleoproteins. J. Gen. Virol. 2000, 81, 939-947.
34. Malik, T.H.; Kishi, M.; Lai, P.K. Characterization of the P protein-binding domain on the 10-kilodalton protein of Borna disease virus. J. Virol. 2000, 74, 3413-3417.
35. Watanabe, Y.; Ohtaki, N.; Hayashi, Y.; Ikuta, K.; Tomonaga, K. Autogenous translational regulation of the Borna disease virus negative control factor X from polycistronic mRNA using host RNA helicases. PLoS Pathog. 2009, 5, e1000654.
36. Briese, T.; Schneemann, A.; Lewis, A.J.; Park, Y.S.; Kim, S.; Ludwig, H.; Lipkin, W.I. Genomic organization of Borna disease virus. Proc. Natl. Acad. Sci. USA 1994, 91, 4362-4366.
37. Walker, M.P.; Jordan, I.; Briese, T.; Fischer, N.; Lipkin, W.I. Expression and characterization of the Borna disease virus polymerase. J. Virol. 2000, 74, 4425-4428.
38. Walker, M.P.; Lipkin, W.I. Characterization of the nuclear localization signal of the borna disease virus polymerase. J. Virol. 2002, 76, 8460-8467.
39. Gonzalez-Dunia, D.; Cubitt, B.; de la Torre, J.C. Mechanism of Borna disease virus entry into cells. J. Virol. 1998, 72, 783-788.
40. Vreede, F.T.; Jung, T.E.; Brownlee, G.G. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J. Virol. 2004, 78, 9568-9572.
41. Resa-Infante, P.; Jorba, N.; Zamarreño, N.; Fernández, Y.; Juárez, S.; Ortín, J. The host-dependent interaction of alpha-importins with influenza PB2 polymerase subunit is required for virus RNA replication. PLoS One 2008, 3, e3904.
42. Hutchinson, E.C.; Orr, O.E.; Man Liu, S.; Engelhardt, O.G.; Fodor, E. Characterization of the interaction between the influenza A virus polymerase subunit PB1 and the host nuclear import factor Ran-binding protein 5. J. Gen. Virol. 2011, 92, 1859-1869.
43. Schneider, U. Novel insights into the regulation of the viral polymerase complex of neurotropic Borna disease virus. Virus Res. 2005, 111, 148-160.
44. Curran, J. A role for the Sendai virus P protein trimer in RNA synthesis. J. Virol. 1998, 72, 4274-4280.
45. Watanabe, M.; Zhong, Q.; Kobayashi, T.; Kamitani, W.; Tomonaga, K.; Ikuta, K. Molecular ratio between borna disease viral-p40 and-p24 proteins in infected cells determined by quantitative antigen capture ELISA. Microbiol. Immunol. 2000, 44, 765-772.
46. Schneider, U.; Naegele, M.; Staeheli, P. Regulation of the Borna disease virus polymerase complex by the viral nucleoprotein p38 isoform. Brief Report. Arch. Virol. 2004, 149, 1409-1414.
47. Bui, M.; Wills, E.G.; Helenius, A.; Whittaker, G.R. Role of the influenza virus M1 protein in nuclear export of viral ribonucleoproteins. J. Virol. 2000, 74, 1781-1786.
48. Mayer, D.; Baginsky, S.; Schwemmle, M. Isolation of viral ribonucleoprotein complexes from infected cells by tandem affinity purification. Proteomics 2005, 5, 4483-4487.
49. Chase, G.; Mayer, D.; Hildebrand, A.; Frank, R.; Hayashi, Y.; Tomonaga, K.; 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. 2007, 81, 743-749.
50. Neumann, P.; Lieber, D.; Meyer, S.; Dautel, P.; Kerth, A.; Kraus, I.; Garten, W.; Stubbs, M.T. Crystal structure of the Borna disease virus matrix protein (BDV-M) reveals ssRNA binding properties. Proc. Natl. Acad. Sci. USA 2009, 106, 3710-3715.