Large scale mass spectrometry-based identifications of enzyme-mediated protein methylation are subject to high false discovery rates

Molecular and Cellular Proteomics

Volumn 15, Issue 3, 2016, Pages 989-1006

  Hart Smith, Gene ^a   Yagoub, Daniel ^a   Tay, Aidan P ^a   Pickford, Russell ^a   Wilkins, Marc R ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

2 PROPANOL; AMINO ACID; ARGININE; ASPARTIC ACID; ENZYME; GLUTAMIC ACID; LYSINE; METHANOL; METHIONINE; PEPTIDE; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN METHYLATION; TANDEM MASS SPECTROMETRY; CHEMISTRY; DEVICES; FALSE POSITIVE RESULT; METABOLISM; METHYLATION; PROCEDURES; PROTEOMICS; SACCHAROMYCES CEREVISIAE;

FALSE POSITIVE REACTIONS; METHYLATION; PEPTIDES; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 84962534083     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.055384     Document Type: Article

References (57)

1. Khoury, G. A., Baliban, R. C, and Floudas, C. A. (2011) Proteome-wide post-translational modification statistics: frequency analysis and curation of the Swiss-Prot database. Sci. Rep. 1, srep00090
2. Zobel-Thropp, P., Gary, J. D., and Clarke, S. (1998) δ-N-Methylarginine is a novel posttranslational modification of arginine residues in yeast proteins. J. Biol. Chem. 273, 29283-29286
3. Lee, D. Y., Teyssier, C, Strahl, B. D., and Stallcup, M. R. (2005) Role of protein methylation in regulation of transcription. Endocr. Rev. 26, 147-170
4. Cao, X.-J., Arnaudo, A. M., and Garcia, B. A. (2013) Large scale global identification of protein lysine methylation in vivo. Epigenetics 8, 477-485
5. Fisk, J. C, Li, J., Wang, H., Aletta, J. M., Qu, J., and Read, L. K. (2013) Proteomic analysis reveals diverse classes of arginine methylproteins in mitochondria of trypanosomes. Mol. Cell. Proteomics 12, 302-311
6. Uhlmann, T., Geoghegan, V. L., Thomas, B., Ridlova, G., Trudgian, D. C, and Acuto, O. (2012) A method for large scale identification of protein arginine methylation. Mol. Cell. Proteomics 11, 1489-1499
7. Bremang, M., Cuomo, A., Agresta, A. M., Stugiewicz, M., Spadotto, V., and Bonaldi, T. (2013) Mass spectrometry-based identification and characterisation of lysine and arginine methylation in the human proteome. Mol. BioSyst. 9, 2231-2247
8. Guo, A., Gu, H., Zhou, J., Mulhern, D., Wang, Y., Lee, K. A., Yang, V., Aguiar, M., Kornhauser, J., Jia, X., Ren, J., Beausoleil, S. A., Silva, J. C, Vemulapalli, V., Bedford, M. T., and Comb, M. J. (2014) Immunoaffinity enrichment and mass spectrometry analysis of protein methylation. Mol. Cell. Proteomics 13, 372-387
9. Lott, K., Li, J., Fisk, J. C, Wang, H., Aletta, J. M., Qu, J., and Read, L. K. (2013) Global proteomic analysis in trypanosomes reveals unique proteins and conserved cellular processes impacted by arginine methylation. J. Proteomics 91, 210-225
10. Wang, K., Zhou, Y. J., Liu, H., Cheng, K., Mao, J., Wang, F., Liu, W., Ye, M., Zhao, Z. K., and Zou, H. (2015) Proteomic analysis of protein methylation in the yeast Saccharomyces cerevisiae. J. Proteomics 114, 226-233
11. Alban, C, Tardif, M., Mininno, M., Brugiere, S., Gilgen, A., Ma, S., Mazzoleni, M., Gigarel, O., Martin-Laffon, J., Ferro, M., and Ravanel, S. (2014) Uncovering the protein lysine and arginine methylation network in Arabidopsis chloroplasts. PLoS One 9, e95512
12. Wu, Z., Cheng, Z., Sun, M., Wan, X., Liu, P., He, T., Tan, M., and Zhao, Y. (2015) A chemical proteomics approach for global analysis of lysine monomethylome profiling. Mol. Cell. Proteomics 14, 329-339
13. Geoghegan, V., Guo, A., Trudgian, D., Thomas, B., and Acuto, O. (2015) Comprehensive identification of arginine methylation in primary T cells reveals regulatory roles in cell signalling. Nat. Commun. 6, 6758
14. Plank, M., Fischer, R., Geoghegan, V., Charles, P. D., Konietzny, R., Acuto, O., Pears, C., Schofield, C. J., and Kessler, B. M. (2015) Expanding the yeast protein arginine methylome. Proteomics 15, 3232-3243
15. Sylvestersen, K. B., Horn, H., Jungmichel, S., Jensen, L. J., and Nielsen, M. L. (2014) Proteomic analysis of arginine methylation sites in human cells reveals dynamic regulation during transcriptional arrest. Mol. Cell. Proteomics 13, 2072-2088
16. Yagoub, D., Hart-Smith, G., Moecking, J., Erce, M. A., and Wilkins, M. R. (2015) Yeast proteins Gar1p, Nop1p, Npl3p, Nsr1p, and Rps2p are natively methylated and are substrates of the arginine methyltransferase Hmt1p. Proteomics 15, 3209-3218
17. Low, J. K., Hart-Smith, G., Erce, M. A., and Wilkins, M. R. (2013) Analysis of the Proteome of Saccharomyces cerevisiae for methylarginine. J. Proteome Res. 12, 3884-3899
18. Bedford, M. T., and Clarke, S. (2009) Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1-13
19. Carlson, S. M., Moore, K. E., Green, E. M., Martín, G. M., and Gozani, O. (2014) Proteome-wide enrichment of proteins modified by lysine methylation. Nat. Protoc. 9, 37-50
20. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214
21. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A., Brunak, S., and Mann, M. (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3-ra3
22. Lundby, A., Lage, K., Weinert, B. T., Bekker-Jensen, D. B., Secher, A., Skovgaard, T., Kelstrup, C. D., Dmytriyev, A., Choudhary, C., Lundby, C., and Olsen, J. V. (2012) Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns. Cell Rep. 2, 419-431
23. Marx, H., Lemeer, S., Schliep, J. E., Matheron, L., Mohammed, S., Cox, J., Mann, M., Heck, A. J., and Kuster, B. (2013) A large synthetic peptide and phosphopeptide reference library for mass spectrometry-based proteomics. Nat. Biotechnol. 31, 557-564
24. Fu, Y., and Qian, X. (2014) Transferred subgroup false discovery rate for rare post-translational modifications detected by mass spectrometry. Mol. Cell. Proteomics 13, 1359-1368
25. Ong, S. E., Mittler, G., and Mann, M. (2004) Identifying and quantifying in vivo methylation sites by heavy-methyl SILAC. Nat. Methods 1, 119-126
26. Jung, S. Y., Li, Y., Wang, Y., Chen, Y., Zhao, Y., and Qin, J. (2008) Complications in the assignment of 14 and 28 Da mass shift detected by mass spectrometry as in vivo methylation from endogenous proteins. Anal. Chem. 80, 1721-1729
27. Chen, G., Liu, H., Wang, X., and Li, Z. (2010) In vitro methylation by methanol: proteomic screening and prevalence investigation. Anal. Chim. Acta 661, 67-75
28. Xing, G., Zhang, J., Chen, Y., and Zhao, Y. (2008) Identification of four novel types of in vitro protein modifications. J. Proteome Res. 7, 4603-4608
29. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
30. Hart-Smith, G., Chia, S. Z., Low, J. K., McKay, M. J., Molloy, M. P., and Wilkins, M. R. (2014) Stoichiometry of Saccharomyces cerevisiae lysine methylation: insights into non-histone protein lysine methyltransferase activity. J. Proteome Res. 13, 1744-1756
31. Hart-Smith, G., and Raftery, M. J. (2012) Detection and characterization of low abundance glycopeptides via higher-energy c-trap dissociation and orbitrap mass analysis. J. Am. Soc. Mass Spectrom. 23, 124-140
32. Hart-Smith, G., Low, J. K., Erce, M. A., and Wilkins, M. R. (2012) Enhanced methylarginine characterization by post-translational modification-specific targeted data acquisition and electron-transfer dissociation mass spectrometry. J. Am. Soc. Mass Spectrom. 23, 1376-1389
33. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
34. Erce, M. A., Pang, C. N., Hart-Smith, G., and Wilkins, M. R. (2012) The methylproteome and the intracellular methylation network. Proteomics 12, 564-586
35. Kall, L, Canterbury, J. D., Weston, J., Noble, W. S., and MacCoss, M. J. (2007) Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 4, 923-925
36. Couttas, T. A., Raftery, M. J., Padula, M. P., Herbert, B. R., and Wilkins, M. R. (2012) Methylation of translation-associated proteins in Saccharomyces cerevisiae: identification of methylated lysines and their methyltransferases. Proteomics 12, 960-972
37. Cavallius, J., Zoll, W., Chakraburtty, K., and Merrick, W. C. (1993) Characterization of yeast EF-1α: nonconservation of post-translational modifications. Biochim. Biophys. Acta 1163, 75-80
38. Itoh, T., and Wittmann-Liebold, B. (1978) The primary structure of protein 44 from the large subunit of yeast ribosomes. FEBS Lett. 96, 399-402
39. Webb, K. J., Laganowsky, A., Whitelegge, J. P., and Clarke, S. G. (2008) Identification of two SET domain proteins required for methylation of lysine residues in yeast ribosomal protein Rpl42ab. J. Biol. Chem. 283, 35561-35568
40. Low, J. K., and Wilkins, M. R. (2012) Protein arginine methylation in Saccharomyces cerevisiae. FEBS J. 279, 4423-4443
41. Erce, M. A., Abeygunawardena, D., Low, J. K., Hart-Smith, G., and Wilkins, M. R. (2013) Interactions affected by arginine methylation in the yeast protein-protein interaction network. Mol. Cell. Proteomics 12, 3184-3198
42. Low, J. K., Hart-Smith, G., Erce, M. A., and Wilkins, M. R. (2014) The Saccharomyces cerevisiae poly (A)-binding protein is subject to multiple post-translational modifications, including the methylation of glutamic acid. Biochem. Biophys. Res. Commun. 443, 543-548
43. Sprung, R., Chen, Y., Zhang, K., Cheng, D., Zhang, T., Peng, J., and Zhao, Y. (2008) Identification and validation of eukaryotic aspartate and glutamate methylation in proteins. J. Proteome Res. 7, 1001-1006
44. Wilhelm, M., Schlegl, J., Hahne, H., MoghaddasGholami, A., Lieberenz, M., Savitski, M. M., Ziegler, E., Butzmann, L., Gessulat, S., Marx, H., Mathieson, T., Lemeer, S., Schnatbaum, K., Reimer, U., Wenschuh, H., Mollenhauer, M., Slotta-Huspenina, J., Boese, J. H., Bantscheff, M., Gerstmair, A., Faerber, F., and Kuster, B. (2014) Mass-spectrometrybased draft of the human proteome. Nature 509, 582-587
45. Fu, Y. (2012) Bayesian false discovery rates for post-translational modification proteomics. Statistics Interface 5, 47-59
46. Clauser, K. R., Hall, S. C, Smith, D. M., Webb, J. W., Andrews, L. E., Tran, H. M., Epstein, L. B., and Burlingame, A. L. (1995) Rapid mass spectrometric peptide sequencing and mass matching for characterization of human melanoma proteins isolated by two-dimensional PAGE. Proc. Natl. Acad. Sci. U. S. A. 92, 5072-5076
47. 2+ ATPase. Anal. Biochem. 214, 50-57
48. Haebel, S., Jensen, C, Andersen, S. O., and Roepstorff, P. (1995) Isoforms of a cuticular protein from larvae of the meal beetle, Tenebrio molitor, studied by mass spectrometry in combination with Edman degradation and two-dimensional polyacrylamide gel electrophoresis. Protein Sci. 4, 394-404
49. Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J., and Gevaert, K. (2009) Improved visualization of protein consensus sequences by ice-Logo. Nat. Methods 6, 786-787
50. G-methylated and unmodified arginine residues in peptides studied by ESI-MS/MS and MALDI-MS. J. Am. Soc. Mass Spectrom. 15, 142-149
51. Brame, C. J., Moran, M. F., and McBroom-Cerajewski, L. D. (2004) A mass spectrometry based method for distinguishing between symmetrically and asymmetrically dimethylated arginine residues. Rapid Commun. Mass Spectrom. 18, 877-881
52. Rappsilber, J., Friesen, W. J., Paushkin, S., Dreyfuss, G., and Mann, M. (2003) Detection of arginine dimethylated peptides by parallel precursor ion scanning mass spectrometry in positive ion mode. Anal. Chem. 75, 3107-3114
53. Snijders, A. P., Hung, M. L., Wilson, S. A., and Dickman, M. J. (2010) Analysis of arginine and lysine methylation utilizing peptide separations at neutral pH and electron transfer dissociation mass spectrometry. J. Am. Soc. Mass Spectrom. 21, 88-96
54. Zhang, K., Tang, H., Huang, L., Blankenship, J. W., Jones, P. R., Xiang, F., Yau, P. M., and Burlingame, A. L. (2002) Identification of acetylation and methylation sites of histone H3 from chicken erythrocytes by highaccuracy matrix-assisted laser desorption ionization-time-of-flight, matrix-assisted laser desorption ionization-postsource decay, and nanoelectrospray ionization tandem mass spectrometry. Anal. Biochem. 306, 259-269
55. Zhang, K., Yau, P. M., Chandrasekhar, B., New, R., Kondrat, R., Imai, B. S., and Bradbury, M. E. (2004) Differentiation between peptides containing acetylated or tri-methylated lysines by mass spectroscopy: an application for determining lysine 9 acetylation and methylation of histone H3. Proteomics 4, 1-10
56. Vizcaíno, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Ríos, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P. A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H. J., Albar, J. P., Martinez-Bartolome, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) Proteome-Xchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223-226
57. Ferro, M., Brugiere, S., Salvi, D., Seigneurin-Berny, D., Court, M., Moyet, L., Ramus, C, Miras, S., Mellal, M., Le Gall, S., Kieffer-Jaquinod, S., Bruley, C, Garin, J., Joyard, J., Masselon, C, Rolland, N. (2010) AT-CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell. Proteomics 9, 1063-1084