Regulation of positive-strand RNA virus replication: The emerging role of phosphorylation

Virus Research

Volumn 129, Issue 2, 2007, Pages 73-79

  Jakubiec, Anna ^a   Jupin, Isabelle ^a  

^a INSTITUT JACQUES MONOD   (France)

Author keywords

Phosphorylation; Positive strand RNA virus; Regulation; Replication

Indexed keywords

VIRUS PROTEIN;

CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME STABILITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN RNA BINDING; REVIEW; RNA VIRUS; VIRUS REPLICATION;

ANIMALS; HUMANS; PHOSPHORYLATION; RNA REPLICASE; RNA VIRUSES; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

ANIMALIA; RNA VIRUSES;

EID: 35348816734     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2007.07.012     Document Type: Review

References (62)

1. Ahlquist P., Noueiry A.O., Lee W.M., Kushner D.B., and Dye B.T. Host factors in positive-strand RNA virus genome replication. J. Virol. 77 (2003) 8181-8186
2. Appel N., Pietschmann T., and Bartenschlager R. Mutational analysis of hepatitis C virus nonstructural protein 5A: potential role of differential phosphorylation in RNA replication and identification of a genetically flexible domain. J. Virol. 79 (2005) 3187-3194
3. Barton D.J., Sawicki S.G., and Sawicki D.L. Solubilization and immunoprecipitation of alphavirus replication complexes. J. Virol. 65 (1991) 1496-1506
4. Blight K.J., Kolykhalov A.A., and Rice C.M. Efficient initiation of HCV RNA replication in cell culture. Science 290 (2000) 1972-1974
5. Boyle W.J., Smeal T., Defize L.H., Angel P., Woodgett J.R., Karin M., and Hunter T. Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell 64 (1991) 573-584
6. Buck K.W. Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv. Virus Res. 47 (1996) 159-251
7. Cohen P. The regulation of protein function by multisite phosphorylation-a 25 year update. Trends Biochem. Sci. 25 (2000) 596-601
8. Cohen P. Protein kinases-the major drug targets of the twenty-first century?. Nat. Rev. Drug Discov. 1 (2002) 309-315
9. De I., Fata-Hartley C., Sawicki S.G., and Sawicki D.L. Functional analysis of nsP3 phosphoprotein mutants of Sindbis virus. J. Virol. 77 (2003) 13106-13116
10. de Groot R.J., Rumenapf T., Kuhn R.J., Strauss E.G., and Strauss J.H. Sindbis virus RNA polymerase is degraded by the N-end rule pathway. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 8967-8971
11. Evans M.J., Rice C.M., and Goff S.P. Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13038-13043
12. Ferrer-Orta C., Arias A., Escarmis C., and Verdaguer N. A comparison of viral RNA-dependent RNA polymerases. Curr. Opin. Struct. Biol. 16 (2006) 27-34
13. Gao L., Tu H., Shi S.T., Lee K.J., Asanaka M., Hwang S.B., and Lai M.M. Interaction with a ubiquitin-like protein enhances the ubiquitination and degradation of hepatitis C virus RNA-dependent RNA polymerase. J. Virol. 77 (2003) 4149-4159
14. Gao L., Aizaki H., He J.W., and Lai M.M. Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft. J. Virol. 78 (2004) 3480-3488
15. Héricourt F., Blanc S., Redeker V., and Jupin I. Evidence for phosphorylation and ubiquitinylation of the turnip yellow mosaic virus RNA-dependent RNA polymerase domain expressed in a baculovirus-insect cell system. Biochem. J. 349 (2000) 417-425
16. Hjerrild M., and Gammeltoft S. Phosphoproteomics toolbox: computational biology, protein chemistry and mass spectrometry. FEBS Lett. 580 (2006) 4764-4770
17. Huang L., Sineva E.V., Hargittai M.R., Sharma S.D., Suthar M., Raney K.D., and Cameron C.E. Purification and characterization of hepatitis C virus non-structural protein 5A expressed in Escherichia coli. Protein Expres. Purif. 37 (2004) 144-153
18. Huang L., Hwang J., Sharma S.D., Hargittai M.R., Chen Y., Arnold J.J., Raney K.D., and Cameron C.E. Hepatitis C virus nonstructural protein 5A (NS5A) is an RNA-binding protein. J. Biol. Chem. 280 (2005) 36417-36428
19. Hwang S.B., Park K.J., Kim Y.S., Sung Y.C., and Lai M.M. Hepatitis C virus NS5B protein is a membrane-associated phosphoprotein with a predominantly perinuclear localization. Virology 227 (1997) 439-446
20. Jakubiec A., Tournier V., Drugeon G., Pflieger S., Camborde L., Vinh J., Héricourt F., Redeker V., and Jupin I. Phosphorylation of viral RNA-dependent RNA polymerase and its role in replication of a plus-strand RNA virus. J. Biol. Chem. 281 (2006) 21236-21249
21. Johansson M., Brooks A.J., Jans D.A., and Vasudevan S.G. A small region of the dengue virus-encoded RNA-dependent RNA polymerase, NS5, confers interaction with both the nuclear transport receptor importin-beta and the viral helicase, NS3. J. Gen. Virol. 82 (2001) 735-745
22. Kaariainen L., and Ahola T. Functions of alphavirus nonstructural proteins in RNA replication. Prog. Nucleic Acid Res. Mol. Biol. 71 (2002) 187-222
23. Kaneko T., Tanji Y., Satoh S., Hijikata M., Asabe S., Kimura K., and Shimotohno K. Production of two phosphoproteins from the NS5A region of the hepatitis C viral genome. Biochem. Biophys. Res. Commun. 205 (1994) 320-326
24. Kapoor M., Zhang L., Ramachandra M., Kusukawa J., Ebner K.E., and Padmanabhan R. Association between NS3 and NS5 proteins of dengue virus type 2 in the putative RNA replicase is linked to differential phosphorylation of NS5. J. Biol. Chem. 270 (1995) 19100-19106
25. Kim S.H., Palukaitis P., and Park Y.I. Phosphorylation of cucumber mosaic virus RNA polymerase 2a protein inhibits formation of replicase complex. EMBO J. 21 (2002) 2292-2300
26. Kim S.J., Kim J.H., Kim Y.G., Lim H.S., and Oh J.W. Protein kinase C-related kinase 2 regulates hepatitis C virus RNA polymerase function by phosphorylation. J. Biol. Chem. 279 (2004) 50031-50041
27. Kim M.J., Ham B.K., and Paek K.H. Novel protein kinase interacts with the Cucumber mosaic virus 1a methyltransferase domain. Biochem. Biophys. Res. Commun. 340 (2006) 228-235
28. Koonin E.V. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72 (1991) 2197-2206
29. LaStarza M.W., Grakoui A., and Rice C.M. Deletion and duplication mutations in the C-terminal nonconserved region of Sindbis virus nsP3: effects on phosphorylation and on virus replication in vertebrate and invertebrate cells. Virology 202 (1994) 224-232
30. Lemm J.A., Rumenapf T., Strauss E.G., Strauss J.H., and Rice C.M. Polypeptide requirements for assembly of functional Sindbis virus replication complexes: a model for the temporal regulation of minus- and plus-strand RNA synthesis. EMBO J. 13 (1994) 2925-2934
31. Lenard J. Host cell protein kinases in nonsegmented negative-strand virus (mononegavirales) infection. Pharmacol. Ther. 83 (1999) 39-48
32. Li G.P., LaStarza M.W., Hardy W.R., Strauss J.H., and Rice C.M. Phosphorylation of Sindbis virus nsP3 in vivo and in vitro. Virology 179 (1990) 416-427
33. Losick V.P., Schlax P.E., Emmons R.A., and Lawson T.G. Signals in hepatitis A virus P3 region proteins recognized by the ubiquitin-mediated proteolytic system. Virology 309 (2003) 306-319
34. Macdonald A., and Harris M. Hepatitis C virus NS5A: tales of a promiscuous protein. J. Gen. Virol. 85 (2004) 2485-2502
35. Mayrand S.H., Dwen P., and Pederson T. Serine/threonine phosphorylation regulates binding of C hnRNP proteins to pre-mRNA. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 7764-7768
36. Merits A., Vasiljeva L., Ahola T., Kaariainen L., and Auvinen P. Proteolytic processing of Semliki Forest virus-specific non-structural polyprotein by nsP2 protease. J. Gen. Virol. 82 (2001) 765-773
37. Morozova O.V., Tsekhanovskaya N.A., Maksimova T.G., Bachvalova V.N., Matveeva V.A., and Kit Y. Phosphorylation of tick-borne encephalitis virus NS5 protein. Virus Res. 49 (1997) 9-15
38. Nagy P.D., and Pogany J. Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology 344 (2006) 211-220
39. Neddermann P., Quintavalle M., Di Pietro C., Clementi A., Cerretani M., Altamura S., Bartholomew L., and De Francesco R. Reduction of hepatitis C virus NS5A hyperphosphorylation by selective inhibition of cellular kinases activates viral RNA replication in cell culture. J. Virol. 78 (2004) 13306-13314
40. Peranen J., Takkinen K., Kalkkinen N., and Kaariainen L. Semliki Forest virus-specific non-structural protein nsP3 is a phosphoprotein. J. Gen. Virol. 69 (1988) 2165-2178
41. Pietschmann T., Lohmann V., Rutter G., Kurpanek K., and Bartenschlager R. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol. 75 (2001) 1252-1264
42. Poch O., Sauvaget I., Delarue M., and Tordo N. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J. 8 (1989) 3867-3874
43. Puustinen P., Rajamaki M.L., Ivanov K.I., Valkonen J.P., and Makinen K. Detection of the potyviral genome-linked protein VPg in virions and its phosphorylation by host kinases. J. Virol. 76 (2002) 12703-12711
44. Ransone L.J., and Dasgupta A. Multiple isoelectric forms of poliovirus RNA-dependent RNA polymerase: evidence for phosphorylation. J. Virol. 63 (1989) 4563-4568
45. Rechsteiner M., and Rogers S.W. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21 (1996) 267-271
46. Reed K.E., Gorbalenya A.E., and Rice C.M. The NS5A/NS5 proteins of viruses from three genera of the family flaviviridae are phosphorylated by associated serine/threonine kinases. J. Virol. 72 (1998) 6199-6206
47. Reinders J., and Sickmann A. State-of-the-art in phosphoproteomics. Proteomics 5 (2005) 4052-4061
48. Salonen A., Ahola T., and Kaariainen L. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285 (2005) 139-173
49. Sanfaçon H. Replication of positive-strand RNA viruses in plants: contact points between plant and virus components. Can. J. Bot. 83 (2005) 1529-1549
50. Sawyer T.K., Shakespeare W.C., Wang Y., Sundaramoorthi R., Huang W.S., Metcalf III C.A., Thomas M., Lawrence B.M., Rozamus L., Noehre J., Zhu X., Narula S., Bohacek R.S., Weigele M., and Dalgarno D.C. Protein phosphorylation and signal transduction modulation: chemistry perspectives for small-molecule drug discovery. Med. Chem. 1 (2005) 293-319
51. Schwartz M., Chen J., Lee W.M., Janda M., and Ahlquist P. Alternate, virus-induced membrane rearrangements support positive-strand RNA virus genome replication. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 11263-11268
52. Shapka N., Stork J., and Nagy P.D. Phosphorylation of the p33 replication protein of Cucumber necrosis tombusvirus adjacent to the RNA binding site affects viral RNA replication. Virology 343 (2005) 65-78
53. Shi S.T., Lee K.J., Aizaki H., Hwang S.B., and Lai M.M. Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J. Virol. 77 (2003) 4160-4168
54. Stork J., Panaviene Z., and Nagy P.D. Inhibition of in vitro RNA binding and replicase activity by phosphorylation of the p33 replication protein of Cucumber necrosis tombusvirus. Virology 343 (2005) 79-92
55. Suzuki M., Yoshida M., Yoshinuma T., and Hibi T. Interaction of replicase components between Cucumber mosaic virus and Peanut stunt virus. J. Gen. Virol. 84 (2003) 1931-1939
56. Tanji Y., Kaneko T., Satoh S., and Shimotohno K. Phosphorylation of hepatitis C virus-encoded nonstructural protein NS5A. J. Virol. 69 (1995) 3980-3986
57. Tu H., Gao L., Shi S.T., Taylor D.R., Yang T., Mircheff A.K., Wen Y., Gorbalenya A.E., Hwang S.B., and Lai M.M. Hepatitis C virus RNA polymerase and NS5A complex with a SNARE-like protein. Virology 263 (1999) 30-41
58. Tuittila M.T., Santagati M.G., Roytta M., Maatta J.A., and Hinkkanen A.E. Replicase complex genes of Semliki Forest virus confer lethal neurovirulence. J. Virol. 74 (2000) 4579-4589
59. van Regenmortel M.H.V., Fauquet C.M., Bishop D.H.L., Carstens E.B., Estes M.K., Lemon S.M., Maniloff J., Mayo M.A., McGeoch D.J., Pringle C.R., and Wickner R.B. The Seventh Report of the International Committee on Taxonomy of Viruses (2000), Academic Press, SanDiego, USA
60. Vihinen H., and Saarinen J. Phosphorylation site analysis of Semliki forest virus nonstructural protein 3. J. Biol. Chem. 275 (2000) 27775-27783
61. Vihinen H., Ahola T., Tuittila M., Merits A., and Kaariainen L. Elimination of phosphorylation sites of Semliki Forest virus replicase protein nsP3. J. Biol. Chem. 276 (2001) 5745-5752
62. Waris G., Sarker S., and Siddiqui A. Two-step affinity purification of the hepatitis C virus ribonucleoprotein complex. RNA 10 (2004) 321-329