Functional characterization of the major and minor phosphorylation sites of the P protein of borna disease virus

Journal of Virology

Volumn 81, Issue 11, 2007, Pages 5497-5507

  Schmid, Sonja ^a   Mayer, Daniel ^a   Schneider, Urs ^a   Schwemmle, Martin ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; CASEIN KINASE II; MUTANT PROTEIN; PHOSPHOPROTEIN P; PROTEIN KINASE C EPSILON; RNA DIRECTED RNA POLYMERASE; SERINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BORNA DISEASE VIRUS; CELL CULTURE; CULTURE MEDIUM; ENZYME ACTIVITY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REACTION ANALYSIS; SEQUENCE ANALYSIS; VIRUS RECOMBINANT;

AMINO ACID SUBSTITUTION; BORNA DISEASE VIRUS; CASEIN KINASE II; CELL LINE; COENZYMES; DOWN-REGULATION; HUMANS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE C-EPSILON; RNA REPLICASE; VIRAL STRUCTURAL PROTEINS;

BORNA DISEASE VIRUS;

EID: 34249794587     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02233-06     Document Type: Article

References (52)

1. Asenjo, A., L. Rodriguez, and N. Villanueva. 2005. Determination of phosphorylated residues from human respiratory syncytial virus P protein that are dynamically dcphosphorylated by cellular phosphatases: a possible role for serine 54. J. Gen. Virol. 86:1109-1120.
2. Barik, S., and A. K. Banerjee. 1992. Phosphorylation by cellular casein kinase II is essential for transcriptional activity of vesicular stomatitis virus phosphoprotein. Proc. Natl. Acad. Sci., USA 89:6570-6574.
3. Barik, S., and A. K. Banerjee. 1992. Sequential phosphorylation of the phosphoprotein of vesicular stomatitis virus by cellular and viral protein kinases is essential for transcription activation. J. Virol. 66:1109-1118.
4. Briese, T., J. C. de la Torre, A. Lewis, H. Ludwig, and W. I. Lipkin. 1992. Borna disease virus, a negative-strand RNA virus, transcribes in the nucleus of infected cells. Proc. Natl. Acad. Sci. USA 89:11486-11489.
5. Briese, T., A. Schneemann, A. J. Lewis, Y.-S. Park, S. Kim, H. Ludwig, and W. I. Lipkin. 1994. Genomic organization of Borna disease virus. Proc. Natl. Acad. Sci. USA 91:4362-4366.
6. Buchholz, U. J., S. Finke, and K. K. Conzelmann. 1999. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J. Virol. 73:251-259.
7. Byrappa, S., and K. C. Gupta. 1999. Human parainfluenza virus type 1 phosphoprotein is constitutively phosphorylated at Ser-120 and Ser-184. J. Gen. Virol. 80:1199-1209.
8. Byrappa, S., Y. B. Pan, and K. C. Gupta. 1996. Sendai virus P protein is constitutively phosphorylated at serine249: high phosphorylation potential of the P protein. Virology 216:228-234.
9. Chang, T. L., C. S. Reiss, and A. S. Huang. 1994. Inhibition of vesicular stomatitis virus RNA synthesis by protein hyperphosphorylation. J. Virol. 68:4980-4987.
10. Chen, J. L., T. Das, and A. K. Banerjee. 1997. Phosphorylated states of vesicular stomatitis virus P protein in vitro and in vivo. Virology 228:200-212.
11. Cubitt, B., C. Oldstone, V. Valcarel, and J. C. de la Torre. 1994. RNA splicing contributes to the generation of mature mRNAs of Borna disease virus, a non-segmented negative strand RNA virus. Virus Res. 34:69-79.
12. Das, D., A. K. Gupta, P. W. Sims, C. A. Gelfand, J. E. Jentoft, and A. K. Banerjee. 1995. Role of cellular casein kinase II in the function of the phosphoprotein (P) subunit of the RNA polymerase of vesicular stomatitis virus. J. Biol. Chem. 270:24100-24107.
13. Das, S. C., and A. K. Pattnaik. 2004. Phosphorylation of vesicular stomatitis virus phosphoprotein P is indispensable for virus growth. J. Virol. 78:6420-6430.
14. Das, T., A. Schuster, S. Schneider-Schaulies, and A. K. Banerjee. 1995. Involvement of cellular casein kinase II in the phosphorylation of measles virus P protein: identification of phosphorylation sites. Virology 211:218-226.
15. De, B. P., and A. K. Banerjee. 1997. Role of host proteins in gene expression of nonsegmented negative strand RNA viruses. Adv. Virus Res. 48:169-204.
16. Desmyter, J., J. L. Melnick, and W. E. Rawls. 1968. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J. Virol. 2:955-961.
17. Gao, Y., and J. Lenard. 1995. Multimerization and transcriptional activation of the phosphoprotein (P) of vesicular stomatitis virus by casein kinase-II. EMBO J. 14:1240-1247.
18. Gonzalez-Dunia, D., R. Volmer, D. Mayer, and M. Schwemmle. 2005. Borna disease virus interference with neuronal plasticity. Virus Res. 111:224-234.
19. Hallensleben, W., and P. Staeheli. 1999. Inhibition of Borna disease virus multiplication by interferon: cell line differences in susceptibility. Arch. Virol. 144:1209-1216.
20. Hu, C., and K. C. Gupta. 2000. Functional significance of alternate phosphorylation in Sendai virus P protein. Virology 268:517-532.
21. Hu, C. J., A. Kato, M. C. Bowman, K. Kiyotani, T. Yoshida, S. A. Moyer, Y. Nagai, and K. C. Gupta. 1999. Role of primary constitutive phosphorylation of Sendai virus P and V proteins in viral replication and pathogenesis. Virology 263:195-208.
22. Huang, W., and R. L. Erikson. 1994. Constitutive activation of Mek1 by mutation of serine phosphorylation sites. Proc. Natl. Acad. Sci. USA 91: 8960-8963.
23. Hwang, L. N., N. Englund, T. Das, A. K. Banerjee, and A. K. Pattnaik. 1999. Optimal replication activity of vesicular stomatitis virus RNA polymerase requires phosphorylation of a residue(s) at carboxy-terminal domain II of its accessory subunit, phosphoprotein P. J. Virol. 73:5613-5620.
24. Jonscher, K. R., and J. R. Yates III. 1997. Matrix-assisted laser desorption ionization/quadrupole ion trap mass spectrometry of peptides. Application to the localization of phosphorylation sites on the P protein from Sendai virus. J. Biol. Chem. 272:1735-1741.
25. Kobayashi, T., G. Zhang, B. J. Lee, S. Baba, M. Yamashita, W. Kamitani, H. Yanai, K. Tomonaga, and K. Ikuta. 2003. Modulation of Borna disease virus phosphoprotein nuclear localization by the viral protein X encoded in the overlapping open reading frame. J. Virol. 77:8099-8107.
26. Laemmli, U. K., and M. Favre. 1973. Maturation of the head of bacteriophage T4. J. Mol. Biol. 80:575-581.
27. Landt, O., H. P. Grunert, and U. Hahn. 1990. A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene 96:125-128.
28. Lu, B., C. H. Ma, R. Brazas, and H. Jin. 2002. The major phosphorylation sites of the respiratory syncytial virus phosphoprotein are dispensable for virus replication in vitro. J. Virol. 76:10776-10784.
29. Martin, A., P. Staeheli, and U. Schneider. 2006. RNA polymerase II-controlled expression of antigenomic RNA enhances the rescue efficacies of two different members of the Mononegavirales independently of the site of viral genome replication. J. Virol. 80:5708-5715.
30. Mosca, J. D., and P. M. Pitha. 1986. Transcriptional and posttranscriptional regulation of exogenous human beta interferon gene in simian cells defective in interferon synthesis. Mol. Cell. Biol. 6:2279-2283.
31. Navarro, J., C. Lopez-Otin, and N. Villanueva. 1991. Location of phosphorylated residues in human respiratory syncytial virus phosphoprotein. J. Gen. Virol. 72:1455-1459.
32. Pattnaik, A. K., L. Hwang, T. Li, N. Englund, M. Mathur, T. Das, and A. K. Banerjee. 1997. Phosphorylation within the amino-terminal acidic domain I of the phosphoprotein of vesicular stomatitis virus is required for transcription but not for replication. J. Virol. 71:8167-8175.
33. Perez, M., A. Sanchez, B. Cubitt, D. Rosario, and J. C. de la Torre. 2003. A reverse genetics system for Borna disease virus. J. Gen. Virol. 84:3099-3104.
34. Poenisch, M., G. Unterstab, T. Wolff, P. Staeheli, and U. Schneider. 2004. The X protein of Borna disease virus regulates viral polymerase activity through interaction with the P protein. J. Gen. Virol. 85:1895-1898.
35. Schneider, P. A., A. Schneemann, and W. I. Lipkin. 1994. RNA splicing in Borna disease virus, a nonsegmented, negative-strand RNA virus. J. Virol. 68:5007-5012.
36. Schneider, U. 2005. Novel insights into the regulation of the viral polymerase complex of neurotropic Borna disease virus. Virus Res. 111:148-160.
37. Schneider, U., K. Blechschmidt, M. Schwemmle, and P. Staeheli. 2004. 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. 279:55290-55296.
38. Schneider, U., M. Naegele, P. Staeheli, and M. Schwemmle. 2003. Active Borna disease virus polymerase complex requires a distinct nucleoprotein-to-phosphoprotein ratio but no viral X protein. J. Virol. 77:11781-11789.
39. Schneider, U., M. Schwemmle, and P. Staeheli. 2005. Genome trimming: a unique strategy for replication control employed by Borna disease virus. Proc. Natl. Acad. Sci. USA 102:3441-3446.
40. Schwardt, M., D. Mayer, R. Frank, U. Schneider, M. Eickmann, O. Planz, T. Wolff, and M. Schwemmle. 2005. The negative regulator of Borna disease virus polymerase is a non-structural protein. J. Gen. Virol. 86:3163-3169.
41. Schwemmle, M., B. De, L. Shi, A. Banerjee, and W. I. Lipkin. 1997. Borna disease virus P-protein is phosphorylated by protein kinase Cε and casein kinase II. J. Biol. Chem. 272:21818-21823.
42. Schwemmle, M., M. Salvatore, L. Shi, J. Richt, C. Lee, and W. Lipkin. 1998. Interactions of the Borna disease virus P, N, and X proteins and their functional implications. J. Biol. Chem. 273:9007-9012.
43. Spadafora, D., D. M. Canter, R. L. Jackson, and J. Perrault. 1996. Constitutive phosphorylation of the vesicular stomatitis virus P protein modulates polymerase complex formation but is not essential for transcription or replication. J. Virol. 70:4538-4548.
44. Staeheli, P., C. Sauder, J. Hausmann, F. Ehrensperger, and M. Schwemmle. 2000. Epidemiology of Borna disease virus. J. Gen. Virol. 81:2123-2135.
45. Takacs, A. M., S. Barik, T. Das, and A. K. Banerjee. 1992. Phosphorylation of specific serine residues within the acidic domain of the phosphoprotein of vesicular stomatitis virus regulates transcription in vitro. J. Virol. 66:5842-5848.
46. Tomonaga, K., T. Kobayashi, and K. Ikuta. 2002. Molecular and cellular biology of Borna disease virus infection. Microbes Infect. 4:491-500.
47. Unterstab, G., S. Ludwig, A. Anton, O. Planz, B. Dauber, D. Krappmann, G. Heins, C. Ehrhardt, and T. Wolff. 2005. Viral targeting of the interferon-β-inducing Traf family member-associated NF-κB activator (TANK)-binding kinase-1. Proc. Natl. Acad. Sci. USA 102:13640-13645.
48. Villanueva, N., R. Hardy, A. Asenjo, Q. Yu, and G. Wertz. 2000. The bulk of the phosphorylation of human respiratory syncytial virus phosphoprotein is not essential but modulates viral RNA transcription and replication. J. Gen. Virol. 81:129-133.
49. Villanueva, N., J. Navarro, E. Mendez, and I. Garcia-Albert. 1994. Identification of a protein kinase involved in the phosphorylation of the C-terminal region of human respiratory syncytial virus P protein. J Gen. Virol. 75:555-565.
50. Volmer, R., C. Monnet, and D. Gonzalez-Dunia. 2006. Borna disease virus blocks potentiation of presynaptic activity through inhibition of protein kinase C signaling. PLOS Pathog. 2:e19.
51. Wehner, T., A. Ruppert, C. Herden, K. Frese, H. Becht, and J. A. Richt. 1997. Detection of a novel Borna disease virus encoded 10 kilodalton protein in infected cells and tissues. J. Gen. Virol. 8:2459-2466.
52. Yanai, H., Y. Hayashi, Y. Watanabe, N. Ohtaki, T. Kobayashi, Y. Nozaki, K. Ikuta, and K. Tomonaga. 2006. Development of a novel Borna disease virus reverse genetics system using RNA polymerase II promoter and SV40 nuclear import signal. Microbes Infect. 8:1522-1529.