Evidence for lysine acetylation in the coat protein of a polerovirus

Journal of General Virology

Volumn 95, Issue , 2014, Pages 2321-2329

  Cilia, Michelle ^a,b,c   Johnson, Richard ^d   Sweeney, Michelle ^c   DeBlasio, Stacy L ^a,c   Bruce, James E ^d   MacCoss, Michael J ^d   Gray, Stewart M ^a,b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; COAT PROTEIN; IMMONIUM ION; ION; LYSINE; MONOMER; UNCLASSIFIED DRUG; CAPSID PROTEIN;

ARTICLE; LYSINE ACETYLATION; NONHUMAN; POLEROVIRUS; PROTEIN ACETYLATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STABILITY; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS STRAIN; ACETYLATION; CHEMISTRY; LUTEOVIRIDAE; MASS SPECTROMETRY; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING;

ACETYLATION; CAPSID PROTEINS; LUTEOVIRIDAE; LYSINE; MASS SPECTROMETRY; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84907212877     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.066514-0     Document Type: Article

References (42)

1. Brault, V., van den Heuvel, J. F., Verbeek, M., Ziegler-Graff, V., Reutenauer, A., Herrbach, E., Garaud, J. C., Guilley, H., Richards, K. & Jonard, G. (1995). Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74. EMBO J 14, 650-659.
2. Brosch, M., Yu, L., Hubbard, T. & Choudhary, J. (2009). Accurate and sensitive peptide identification with Mascot Percolator. J Proteome Res 8, 3176-3181.
3. Bruce, J. E. (2012). In vivo protein complex topologies: sights through a cross-linking lens. Proteomics 12, 1565-1575.
4. Chavez, J. D., Cilia, M., Weisbrod, C. R., Ju, H. J., Eng, J. K., Gray, S. M. & Bruce, J. E. (2012). Cross-linking measurements of the Potato leafroll virus reveal protein interaction topologies required for virion stability, aphid transmission, and virus-plant interactions. J Proteome Res 11, 2968-2981.
5. Cheng, S. L., Domier, L. L. & D'Arcy, C. J. (1994). Detection of the readthrough protein of barley yellow dwarf virus. Virology 202, 1003- 1006.
6. Cilia, M., Howe, K., Fish, T., Smith, D., Mahoney, J., Tamborindeguy, C., Burd, J., Thannhauser, T. W. & Gray, S. (2011a). Biomarker discovery from the top down: protein biomarkers for efficient virus transmission by insects (Homoptera: Aphididae) discovered by coupling genetics and 2-D DIGE. Proteomics 11, 2440-2458.
7. Cilia, M., Tamborindeguy, C., Fish, T., Howe, K., Thannhauser, T. W. & Gray, S. (2011b). Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. J Virol 85, 2148-2166.
8. Cilia, M., Peter, K. A., Bereman, M. S., Howe, K., Fish, T., Smith, D., Gildow, F., MacCoss, M. J., Thannhauser, T. W. & Gray, S. M. (2012). Discovery and targeted LC-MS/MS of purified polerovirus reveals differences in the virus-host interactome associated with altered aphid transmission. PLoS ONE 7, e48177.
9. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. (2004). WebLogo: a sequence logo generator. Genome Res 14, 1188-1190.
10. Cueva, J. G., Hsin, J., Huang, K. C. & Goodman, M. B. (2012). Posttranslational acetylation of a-tubulin constrains protofilament number in native microtubules. Curr Biol 22, 1066-1074.
11. D'Orso, I. & Frankel, A. D. (2009). Tat acetylation modulates assembly of a viral-host RNA-protein transcription complex. Proc Natl Acad Sci U S A 106, 3101-3106.
12. Filichkin, S. A., Lister, R. M., McGrath, P. F. & Young, M. J. (1994). In vivo expression and mutational analysis of the barley yellow dwarf virus readthrough gene. Virology 205, 290-299.
13. Glozak, M. A., Sengupta, N., Zhang, X. & Seto, E. (2005). Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23.
14. Gray, S. M., Cilia, M. & Ghanim, M. (2014). Circulative, "nonpropagative'' virus transmission: an orchestra of virus-, insect-, and plant-derived instruments. Adv Virus Res 89, 141-199.
15. Kaplan, I. B., Lee, L., Ripoll, D. R., Palukaitis, P., Gildow, F. & Gray, S. M. (2007). Point mutations in the potato leafroll virus major capsid protein alter virion stability and aphid transmission. J Gen Virol 88, 1821-1830.
16. Kessner, D., Chambers, M., Burke, R., Agus, D. & Mallick, P. (2008). ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics 24, 2534-2536.
17. Lee, L., Kaplan, I. B., Ripoll, D. R., Liang, D., Palukaitis, P. & Gray, S. M. (2005). A surface loop of the potato leafroll virus coat protein is involved in virion assembly, systemic movement, and aphid transmission. J Virol 79, 1207-1214.
18. Li, T., Diner, B. A., Chen, J. & Cristea, I. M. (2012). Acetylation modulates cellular distribution and DNA sensing ability of interferoninducible protein IFI16. Proc Natl Acad Sci U S A 109, 10558- 10563.
19. Link, K., Vogel, F. & Sonnewald, U. (2011). PD trafficking of potato leafroll virus movement protein in Arabidopsis depends on site-specific protein phosphorylation. Front Plant Sci 2, 18.
20. Miller, W. A., Dinesh-Kumar, S. P. & Paul, C. P. (1995). Luteovirus gene expression. Crit Rev Plant Sci 14, 179-211.
21. Mu, J. J., Tsay, Y. G., Juan, L. J., Fu, T. F., Huang, W. H., Chen, D. S. & Chen, P. J. (2004). The small delta antigen of hepatitis delta virus is an acetylated protein and acetylation of lysine 72 may influence its cellular localization and viral RNA synthesis. Virology 319, 60-70.
22. Nallamilli, B. R., Edelmann, M. J., Zhong, X., Tan, F., Mujahid, H., Zhang, J., Nanduri, B. & Peng, Z. (2014). Global analysis of lysine acetylation suggests the involvement of protein acetylation in diverse biological processes in rice (Oryza sativa). PLoS ONE 9, e89283.
23. 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.
24. Peter, K. A., Liang, D., Palukaitis, P. & Gray, S. M. (2008). Small deletions in the potato leafroll virus readthrough protein affect particle morphology, aphid transmission, virus movement and accumulation. J Gen Virol 89, 2037-2045.
25. Peter, K. A., Gildow, F., Palukaitis, P. & Gray, S. M. (2009). The C terminus of the polerovirus p5 readthrough domain limits virus infection to the phloem. J Virol 83, 5419-5429.
26. Pinheiro, P., Bereman, M. S., Burd, J., Pals, M., Armstrong, S., Howe, K. J., Thannhauser, T. W., MacCoss, M. J., Gray, S. M. & Cilia, M. (2014). Evidence of the biochemical basis of host virulence in the greenbug aphid, Schizaphis graminum (Homoptera: Aphididae). J Proteome Res 13, 2094-2108.
27. Radkiewicz, J. L., Zipse, H., Clarke, S. & Houk, K. N. (2001). Neighboring side chain effects on asparaginyl and aspartyl degradation: an ab initio study of the relationship between peptide conformation and backbone NH acidity. J Am Chem Soc 123, 3499- 3506.
28. Revollon, S., Strub, J. M., Fitchette, A. C., Wiss, L., Gomord, V., Van Dorsselaer, A. & Brault, V. (2010). A reinvestigation provides no evidence for sugar residues on structural proteins of poleroviruses and argues against a role for glycosylation of virus structural proteins in aphid transmission. Virology 402, 303-314.
29. Robinson, N. E., Robinson, Z. W., Robinson, B. R., Robinson, A. L., Robinson, J. A., Robinson, M. L. & Robinson, A. B. (2004). Structuredependent nonenzymatic deamidation of glutaminyl and asparaginyl pentapeptides. J Pept Res 63, 426-436.
30. Rochow, W. F. (1970). Barley yellow dwarf virus: phenotypic mixing and vector specificity. Science 167, 875-878.
31. Seddas, P. & Boissinot, S. (2006). Glycosylation of beet western yellows virus proteins is implicated in the aphid transmission of the virus. Arch Virol 151, 967-984.
32. Spivak, M., Weston, J., Bottou, L., Käll, L. & Noble, W. S. (2009). Improvements to the Percolator algorithm for peptide identification from shotgun proteomics data sets. J Proteome Res 8, 3737-3745.
33. Tamborindeguy, C., Bereman, M. S., DeBlasio, S., Igwe, D., Smith, D. M., White, F., MacCoss, M. J., Gray, S. M. & Cilia, M. (2013). Genomic and proteomic analysis of Schizaphis graminum reveals cyclophilin proteins are involved in the transmission of Cereal yellow dwarf virus. PLoS ONE 8, e71620.
34. Thompson, J. D., Gibson, T. J. & Higgins, D. G. (2002). Multiple sequence alignment using Clustal W and Clustal_X. Curr. Protocols Bioinform 2002, Unit 2.3.
35. Torrance, L. (1992). Analysis of epitopes on potato leafroll virus capsid protein. Virology 191, 485-489.
36. Trelle, M. B. & Jensen, O. N. (2008). Utility of immonium ions for assignment of e-N-acetyllysine-containing peptides by tandem mass spectrometry. Anal Chem 80, 3422-3430.
37. Wang, J. Y., Chay, C., Gildow, F. E. & Gray, S. M. (1995). Readthrough protein associated with virions of barley yellow dwarf luteovirus and its potential role in regulating the efficiency of aphid transmission. Virology 206, 954-962.
38. Wu, X., Oh, M. H., Schwarz, E. M., Larue, C. T., Sivaguru, M., Imai, B. S., Yau, P. M., Ort, D. R. & Huber, S. C. (2011). Lysine acetylation is a widespread protein modification for diverse proteins in Arabidopsis. Plant Physiol 155, 1769-1778.
39. Xing, S. & Poirier, Y. (2012). The protein acetylome and the regulation of metabolism. Trends Plant Sci 17, 423-430.
40. Xue, B., Jeffers, V., Sullivan, W. J. & Uversky, V. N. (2013). Protein intrinsic disorder in the acetylome of intracellular and extracellular Toxoplasma gondii. Mol Biosyst 9, 645-657.
41. Yang, X., Thannhauser, T. W., Burrows, M., Cox-Foster, D., Gildow, F. E. & Gray, S. M. (2008). Coupling genetics and proteomics to identify aphid proteins associated with vector-specific transmission of polerovirus (Luteoviridae). J Virol 82, 291-299.
42. Yang, L., Vaitheesvaran, B., Hartil, K., Robinson, A. J.,Hoopmann,M. R., Eng, J. K., Kurland, I. J. & Bruce, J. E. (2011). The fasted/fed mouse metabolic acetylome: N6-acetylation differences suggest acetylation coordinates organ-specific fuel switching. J Proteome Res 10, 4134-4149.