1887

Abstract

Sobemoviruses possess a viral genome-linked protein (VPg) attached to the 5′ end of viral RNA. VPg is processed from the viral polyprotein. In the current study, Cocksfoot mottle virus (CfMV) and Rice yellow mottle virus (RYMV) VPgs were purified from virions and analysed by mass spectrometry. The cleavage sites in the polyprotein and thereof the termini of VPg were experimentally proven. The lengths of the mature VPgs were determined to be 78 and 79 aa residues, respectively. The amino acid residues covalently linked to RNA in the two VPgs were, surprisingly, not conserved; it is a tyrosine at position 5 of CfMV VPg and serine at position 1 of RYMV VPg. Phosphorylations were identified in CfMV and RYMV VPgs with two positionally similar locations T20/S14 and S71/S72, respectively. RYMV VPg contains an additional phosphorylation site at S41.

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2011-02-01
2024-03-29
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References

  1. Albar, L., Bangratz-Reyser, M., Hébrard, E., Ndjiondjop, M., Jones, M. & Ghesquière, A.(2006). Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant J 47, 417–426.[CrossRef] [Google Scholar]
  2. Ambros, V. & Baltimore, D.(1978). Protein is linked to the 5′ end of poliovirus RNA by a phosphodiester linkage to tyrosine. J Biol Chem 253, 5263–5266. [Google Scholar]
  3. Anindya, R., Chittori, S. & Savithri, H. S.(2005). Tyrosine 66 of Pepper vein banding virus genome-linked protein is uridylylated by RNA-dependent RNA polymerase. Virology 336, 154–162.[CrossRef] [Google Scholar]
  4. Belliot, G., Sosnovtsev, S. V., Chang, K. O., McPhie, P. & Green, K. Y.(2008). Nucleotidylylation of the VPg protein of a human norovirus by its proteinase-polymerase precursor protein. Virology 374, 33–49.[CrossRef] [Google Scholar]
  5. Carette, J. E., Kujawa, A., Gühl, K., Verver, J., Wellink, J. & Van Kammen, A.(2001). Mutational analysis of the genome-linked protein of cowpea mosaic virus. Virology 290, 21–29.[CrossRef] [Google Scholar]
  6. Daughenbaugh, K. F., Fraser, C. S., Hershey, J. W. B. & Hardy, M. E.(2003). The genome-linked protein VPg of the Norwalk virus binds eIF3, suggesting its role in translation initiation complex recruitment. EMBO J 22, 2852–2859.[CrossRef] [Google Scholar]
  7. Daughenbaugh, K. F., Wobus, C. E. & Hardy, M. E.(2006). VPg of murine norovirus binds translation initiation factors in infected cells. Virol J 3, 33.[CrossRef] [Google Scholar]
  8. Ghosh, A., Rutgers, T., Ke-Qiang, M. & Kaesberg, P.(1981). Characterization of the coat protein mRNA of Southern bean mosaic virus and its relationship to the genomic RNA. J Virol 39, 87–92. [Google Scholar]
  9. Goodfellow, I., Chaudhry, Y., Gioldasi, I., Gerondopoulos, A., Natoni, A., Labrie, L., Laliberté, J. & Roberts, L.(2005). Calicivirus translation initiation requires an interaction between VPg and eIF4E. EMBO Rep 6, 968–972.[CrossRef] [Google Scholar]
  10. Gorbalenya, A. E., Koonin, E. V., Blinov, V. M. & Donchenko, A. P.(1988). Sobemovirus genome appears to encode a serine protease related to cysteine proteases of picornaviruses. FEBS Lett 236, 287–290.[CrossRef] [Google Scholar]
  11. Govind, K. & Savithri, H. S.(2010). Primer-independent initiation of RNA synthesis by SeMV recombinant RNA-dependent RNA polymerase. Virology 401, 280–292.[CrossRef] [Google Scholar]
  12. Gruez, A., Selisko, B., Roberts, M., Bricogne, G., Bussetta, C., Jabafi, I., Coutard, B., De Palma, A. M., Neyts, J. & other authors(2008). The crystal structure of coxsackievirus B3 RNA-dependent RNA polymerase in complex with its protein primer VPg confirms the existence of a second VPg binding site on Picornaviridae polymerases. J Virol 82, 9577–9590.[CrossRef] [Google Scholar]
  13. Grzela, R., Szolajska, E., Ebel, C., Madern, D., Favier, A., Wojtal, I., Zagorski, W. & Chroboczek, J.(2008). Virulence factor of potato virus Y, genome-attached terminal protein VPg, is a highly disordered protein. J Biol Chem 283, 213–221.[CrossRef] [Google Scholar]
  14. Hébrard, E., Pinel-Galzi, A., Bersoult, A., Siré, C. & Fargette, D.(2006). Emergence of a resistance-breaking isolate of Rice yellow mottle virus during serial inoculations is due to a single substitution in the genome-linked viral protein VPg. J Gen Virol 87, 1369–1373.[CrossRef] [Google Scholar]
  15. Hébrard, E., Pinel-Galzi, A. & Fargette, D.(2008). Virulence domain of the RYMV genome-linked viral protein VPg towards rice rymv1–2-mediated resistance. Arch Virol 153, 1161–1164.[CrossRef] [Google Scholar]
  16. Hébrard, E., Bessin, Y., Michon, T., Longhi, S., Uversky, V. N., Delalande, F., Van Dorsselaer, A., Romero, P., Walter, J. & other authors(2009). Intrinsic disorder in viral proteins genome-linked: experimental and predictive analyses. Virol J 6, 23.[CrossRef] [Google Scholar]
  17. Hébrard, E, Poulicard, N, Gérard, C, Traoré, O, Albar, L, Fargette, D, Bessin, Y & Vignols, F.(2010). Direct interaction between the Rice yellow mottle virus VPg and the central domain of the rice eIF(iso)4G1 factor correlates with rice susceptibility and RYMV virulence. Mol Plant Microbe Interact 23, 1506–1513.[CrossRef] [Google Scholar]
  18. Jaegle, M., Wellink, J. & Goldbach, R.(1987). The genome-linked protein of Cowpea mosaic virus is bound to the 5′ terminus of virus RNA by phosphodiester linkage to serine. J Gen Virol 68, 627–632.[CrossRef] [Google Scholar]
  19. Jakubiec, A. & Jupin, I.(2007). Regulation of positive-strand RNA virus replication: the emerging role of phosphorylation. Virus Res 129, 73–79.[CrossRef] [Google Scholar]
  20. Khan, M. A., Miyoshi, H., Gallie, D. R. & Goss, D. J.(2008). Potyvirus genome-linked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J Biol Chem 283, 1340–1349.[CrossRef] [Google Scholar]
  21. Kosakovsky Pond, S. L. K. & Frost, S. D. W.(2005a). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531–2533.[CrossRef] [Google Scholar]
  22. Kosakovsky Pond, S. L. & Frost, S. D. W.(2005b). Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22, 1208–1222.[CrossRef] [Google Scholar]
  23. Lin, L., Shi, Y., Luo, Z., Lu, Y., Zheng, H., Yan, F., Chen, J., Chen, J., Adams, M. J. & other authors(2009). Protein–protein interactions in two potyviruses using the yeast two-hybrid system. Virus Res 142, 36–40.[CrossRef] [Google Scholar]
  24. Ma, B., Zhang, K., Hendrie, C., Liang, C., Li, M., Doherty-Kirby, A. & Lajoie, G.(2003).peaks: powerful software for peptide de novo sequencing by tandem mass spectrometry. Rapid Commun Mass Spectrom 17, 2337–2342.[CrossRef] [Google Scholar]
  25. Mäkinen, K., Tamm, T., Naess, V., Truve, E., Puurand, Ü., Munthe, T. & Saarma, M.(1995). Characterization of cocksfoot mottle sobemovirus genomic RNA and sequence comparison with related viruses. J Gen Virol 76, 2817–2825.[CrossRef] [Google Scholar]
  26. Mäkinen, K., Mäkeläinen, K., Arshava, N., Tamm, T., Merits, A., Truve, E., Zavriev, S. & Saarma, M.(2000). Characterization of VPg and the polyprotein processing of cocksfoot mottle virus (genus Sobemovirus). J Gen Virol 81, 2783–2789. [Google Scholar]
  27. Mang, K. Q., Ghosh, A. & Kaesberg, P.(1982). A comparative study of the cowpea and bean strains of southern bean mosaic virus. Virology 116, 264–274.[CrossRef] [Google Scholar]
  28. Meggio, F. & Pinna, L. A.(2003). One-thousand-and-one substrates of protein kinase CK2? FASEB J 17, 349–368.[CrossRef] [Google Scholar]
  29. Michon, T., Estevez, Y., Walter, J., German-Retana, S. & Le Gall, O.(2006). The potyviral virus genome-linked protein VPg forms a ternary complex with the eukaryotic initiation factors eIF4E and eIF4G and reduces eIF4E affinity for a mRNA cap analogue. FEBS J 273, 1312–1322.[CrossRef] [Google Scholar]
  30. Mittag, T., Kay, L. E. & Forman-Kay, J. D.(2010). Protein dynamics and conformational disorder in molecular recognition. J Mol Recognit 23, 105–116. [Google Scholar]
  31. Miyoshi, H., Suehiro, N., Tomoo, K., Muto, S., Takahashi, T., Tsukamoto, T., Ohmori, T. & Natsuaki, T.(2006). Binding analyses for the interaction between plant virus genome-linked protein (VPg) and plant translational initiation factors. Biochimie 88, 329–340.[CrossRef] [Google Scholar]
  32. Murphy, J. F., Rychlik, W., Rhoads, R. E., Hunt, A. G. & Shaw, J. G.(1991). A tyrosine residue in the small nuclear inclusion protein of tobacco vein mottling virus links the VPg to the viral RNA. J Virol 65, 511–513. [Google Scholar]
  33. Murphy, J. F., Klein, P. G., Hunt, A. G. & Shaw, J. G.(1996). Replacement of the tyrosine residue that links a potyviral VPg to the viral RNA is lethal. Virology 220, 535–538.[CrossRef] [Google Scholar]
  34. Nair, S. & Savithri, H. S.(2010). Processing of SeMV polyproteins revisited. Virology 396, 106–117.[CrossRef] [Google Scholar]
  35. Olsen, J. V., de Godoy, L. M. F., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S. & other authors(2005). Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 4, 2010–2021.[CrossRef] [Google Scholar]
  36. Perkins, D. N., Pappin, D. J., Creasy, D. M. & Cottrell, J. S.(1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551–3567.[CrossRef] [Google Scholar]
  37. Pinel-Galzi, A., Mpunami, A., Sangu, E., Rakotomalala, M., Traoré, O., Sérémé, D., Sorho, F., Séré, Y., Kanyeka, Z. & other authors(2009). Recombination, selection and clock-like evolution of Rice yellow mottle virus. Virology 394, 164–172.[CrossRef] [Google Scholar]
  38. Puustinen, P., Rajamäki, M., Ivanov, K. I., Valkonen, J. P. T. & Mäkinen, K.(2002). Detection of the potyviral genome-linked protein VPg in virions and its phosphorylation by host kinases. J Virol 76, 12703–12711.[CrossRef] [Google Scholar]
  39. Rantalainen, K. I., Uversky, V. N., Permi, P., Kalkkinen, N., Dunker, A. K. & Mäkinen, K.(2008). Potato virus A genome-linked protein VPg is an intrinsically disordered molten globule-like protein with a hydrophobic core. Virology 377, 280–288.[CrossRef] [Google Scholar]
  40. Rappsilber, J., Mann, M. & Ishihama, Y.(2007). Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2, 1896–1906.[CrossRef] [Google Scholar]
  41. Receveur-Bréchot, V., Bourhis, J., Uversky, V. N., Canard, B. & Longhi, S.(2006). Assessing protein disorder and induced folding. Proteins 62, 24–45. [Google Scholar]
  42. Rothberg, P. G., Harris, T. J., Nomoto, A. & Wimmer, E.(1978). O4-(5′-uridylyl)tyrosine is the bond between the genome-linked protein and the RNA of poliovirus. Proc Natl Acad Sci U S A 75, 4868–4872.[CrossRef] [Google Scholar]
  43. Satheshkumar, P. S., Gayathri, P., Prasad, K. & Savithri, H. S.(2005). Natively unfolded VPg is essential for Sesbania mosaic virus serine protease activity. J Biol Chem 280, 30291–30300.[CrossRef] [Google Scholar]
  44. Schein, C. H., Oezguen, N., Volk, D. E., Garimella, R., Paul, A. & Braun, W.(2006). NMR structure of the viral peptide linked to the genome (VPg) of poliovirus. Peptides 27, 1676–1684.[CrossRef] [Google Scholar]
  45. Stadtman, E. R. & Levine, R. L.(2003). Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25, 207–218.[CrossRef] [Google Scholar]
  46. Stein, A., Pache, R. A., Bernadó, P., Pons, M. & Aloy, P.(2009). Dynamic interactions of proteins in complex networks: a more structured view. FEBS J 276, 5390–5405.[CrossRef] [Google Scholar]
  47. Tars, K., Zeltins, A. & Liljas, L.(2003). The three-dimensional structure of Cocksfoot mottle virus at 2.7 Å resolution. Virology 310, 287–297.[CrossRef] [Google Scholar]
  48. van der Wilk, F., Verbeek, M., Dullemans, A. & van den Heuvel, J.(1998). The genome-linked protein (VPg) of southern bean mosaic virus is encoded by the ORF2. Virus Genes 17, 21–24.[CrossRef] [Google Scholar]
  49. Wright, P. E. & Dyson, H. J.(2009). Linking folding and binding. Curr Opin Struct Biol 19, 31–38.[CrossRef] [Google Scholar]
  50. Xing, G., Zhang, J., Chen, Y. & Zhao, Y.(2008). Identification of four novel types of in vitro protein modifications. J Proteome Res 7, 4603–4608.[CrossRef] [Google Scholar]
  51. Zalloua, P. A., Buzayan, J. M. & Bruening, G.(1996). Chemical cleavage of 5′-linked protein from tobacco ringspot virus genomic RNAs and characterization of the protein-RNA linkage. Virology 219, 1–8.[CrossRef] [Google Scholar]
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vol. , part 2, pp. 445 - 452

Examples of detected peptides identified by fragmentation spectra [PDF](13 KB)



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