Immunoaffinity enrichment and mass spectrometry analysis of protein methylation

Molecular and Cellular Proteomics

Volumn 13, Issue 1, 2014, Pages 372-387

  Guo, Ailan ^a   Gu, Hongbo ^a   Zhou, Jing ^a   Mulhern, Daniel ^a   Wang, Yi ^a   Lee, Kimberly A ^a   Yang, Vicky ^a   Aguiar, Mike ^a   Kornhauser, Jon ^a   Jia, Xiaoying ^a   Ren, Jianmin ^a   Beausoleil, Sean A ^a   Silva, Jeffrey C ^a   Vemulapalli, Vidyasiri ^b   Bedford, Mark T ^b   Comb, Michael J ^a  

^a CELL SIGNALING TECHNOLOGY   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 N N DIMETHYLARGININE; ARGININE; LYSINE; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ARTICLE; CELL STRAIN HCT116; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EMBRYO; EXPERIMENTAL RABBIT; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PURIFICATION; RNA PROCESSING; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION;

AMINO ACID MOTIFS; ANIMALS; ARGININE; BRAIN; CHROMATOGRAPHY, LIQUID; HCT116 CELLS; HUMANS; LYSINE; METHYLATION; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; TANDEM MASS SPECTROMETRY;

EID: 84891801106     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.O113.027870     Document Type: Article

References (59)

1. Aletta, J. M., Cimato, T. R., and Ettinger, M. J. (1998) Protein methylation: a signal event in post-translational modification. Trends Biochem. Sci. 23, 89-91
2. Comb, D. G., Sarkar, N., and Pinzino, C. J. (1966) The methylation of lysine residues in protein. J. Biol. Chem. 241, 1857-1862
3. Bedford, M. T., and Clarke, S. G. (2009) Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1-13
4. Bedford, M. T., and Richard, S. (2005) Arginine methylation: an emerging regulator of protein function. Mol. Cell 18, 263-272
5. Bedford, M. T. (2007) Arginine methylation at a glance. J. Cell Sci. 120, 4243-4246
6. Dillon, S. C., Zhang, X., Trievel, R. C., and Cheng, X. (2005) The SETdomain protein superfamily: protein lysine methyltransferases. Genome Biol. 6, 227
7. Zhang, X., and Bruice, T. C. (2007) Histone lysine methyltransferase SET7/9: formation of a water channel precedes each methyl transfer. Biochemistry 46, 14838-14844
8. Lee, D. Y., Teyssier, C., Strahl, B. D., and Stallcup, M. R. (2005) Role of protein methylation in regulation of transcription. Endocrine Rev. 26, 147-170
9. Hyun, Y. L., Lew, D. B., Park, S. H., Kim, C. W., Paik, W. K., and Kim, S. (2000) Enzymic methylation of arginyl residues in -gly-arg-gly- peptides. Biochem. J. 348 Pt 3, 573-578
10. Cheng, D., Cote, J., Shaaban, S., and Bedford, M. T. (2007) The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol. Cell 25, 71-83
11. Trojer, P., and Reinberg, D. (2006) Histone lysine demethylases and their impact on epigenetics. Cell 125, 213-217
12. Anand, R., and Marmorstein, R. (2007) Structure and mechanism of lysinespecific demethylase enzymes. J. Biol. Chem. 282, 35425-35429
13. Liu, F., Zhao, X., Perna, F., Wang, L., Koppikar, P., Abdel-Wahab, O., Harr, M. W., Levine, R. L., Xu, H., Tefferi, A., Deblasio, A., Hatlen, M., Menendez, S., and Nimer, S. D. (2011) JAK2V617F-mediated phosphorylation of PRMT5 downregulates its methyltransferase activity and promotes myeloproliferation. Cancer Cell 19, 283-294
14. Higashimoto, K., Kuhn, P., Desai, D., Cheng, X., and Xu, W. (2007) Phosphorylation- mediated inactivation of coactivator-associated arginine methyltransferase 1. Proc. Natl. Acad. Sci. U.S.A. 104, 12318-12323
15. Pawlak, M. R., Scherer, C. A., Chen, J., Roshon, M. J., and Ruley, H. E. (2000) Arginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol. Cell. Biol. 20, 4859-4869
16. Yadav, N., Lee, J., Kim, J., Shen, J., Hu, M. C., Aldaz, C. M., and Bedford, M. T. (2003) Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 100, 6464-6468
17. Dambacher, S., Hahn, M., and Schotta, G. (2010) Epigenetic regulation of development by histone lysine methylation. Heredity 105, 24-37
18. Greer, E. L., and Shi, Y. (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genetics 13, 343-357
19. Yang, Y., and Bedford, M. T. (2013) Protein arginine methyltransferases and cancer. Nat. Rev. Cancer 13, 37-50
20. Majumder, S., Liu, Y., Ford, O. H., 3rd, Mohler, J. L., and Whang, Y. E. (2006) Involvement of arginine methyltransferase CARM1 in androgen receptor function and prostate cancer cell viability. Prostate 66, 1292-1301
21. Frietze, S., Lupien, M., Silver, P. A., and Brown, M. (2008) CARM1 regulates estrogen-stimulated breast cancer growth through up-regulation of E2F1. Cancer Res. 68, 301-306
22. Scorilas, A., Black, M. H., Talieri, M., and Diamandis, E. P. (2000) Genomic organization, physical mapping, and expression analysis of the human protein arginine methyltransferase 1 gene. Biochem. Biophys. Res. Commun. 278, 349-359
23. Mathioudaki, K., Papadokostopoulou, A., Scorilas, A., Xynopoulos, D., Agnanti, N., and Talieri, M. (2008) The PRMT1 gene expression pattern in colon cancer. Br. J. Cancer 99, 2094-2099
24. Kang, M. Y., Lee, B. B., Kim, Y. H., Chang, D. K., Kyu Park, S., Chun, H. K., Song, S. Y., Park, J., and Kim, D. H. (2007) Association of the SUV39H1 histone methyltransferase with the DNA methyltransferase 1 at mRNA expression level in primary colorectal cancer. Int. J. Cancer 121, 2192-2197
25. Simon, J. A., and Lange, C. A. (2008) Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat. Res. 647, 21-29
26. Tsang, D. P., and Cheng, A. S. (2011) Epigenetic regulation of signaling pathways in cancer: role of the histone methyltransferase EZH2. J. Gastroenterol. Hepatol. 26, 19-27
27. Yap, D. B., Chu, J., Berg, T., Schapira, M., Cheng, S. W., Moradian, A., Morin, R. D., Mungall, A. J., Meissner, B., Boyle, M., Marquez, V. E., Marra, M. A., Gascoyne, R. D., Humphries, R. K., Arrowsmith, C. H., Morin, G. B., and Aparicio, S. A. (2011) Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood 117, 2451-2459
28. Yost, J. M., Korboukh, I., Liu, F., Gao, C., and Jin, J. (2011) Targets in epigenetics: inhibiting the methyl writers of the histone code. Curr. Chem. Genomics 5, 72-84
29. Cheng, D., Yadav, N., King, R. W., Swanson, M. S., Weinstein, E. J., and Bedford, M. T. (2004) Small molecule regulators of protein arginine methyltransferases. J. Biol. Chem. 279, 23892-23899
30. Rush, J., Moritz, A., Lee, K. A., Guo, A., Goss, V. L., Spek, E. J., Zhang, H., Zha, X. M., Polakiewicz, R. D., and Comb, M. J. (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 23, 94-101
31. Villen, J., Beausoleil, S. A., Gerber, S. A., and Gygi, S. P. (2007) Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. U.S.A. 104, 1488-1493
32. Macek, B., Mann, M., and Olsen, J. V. (2009) Global and site-specific quantitative phosphoproteomics: principles and applications. Annu. Rev. Pharmacol. Toxicol. 49, 199-221
33. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840
34. Kim, W., Bennett, E. J., Huttlin, E. L., Guo, A., Li, J., Possemato, A., Sowa, M. E., Rad, R., Rush, J., Comb, M. J., Harper, J. W., and Gygi, S. P. (2011) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44, 325-340
35. Emanuele, M. J., Elia, A. E., Xu, Q., Thoma, C. R., Izhar, L., Leng, Y., Guo, A., Chen, Y. N., Rush, J., Hsu, P. W., Yen, H. C., and Elledge, S. J. (2011) Global identification of modular cullin-RING ligase substrates. Cell 147, 459-474
36. Boisvert, F. M., Cote, J., Boulanger, M. C., and Richard, S. (2003) A proteomic analysis of arginine-methylated protein complexes. Mol. Cell. Proteomics 2, 1319-1330
37. 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
38. Pang, C. N., Gasteiger, E., and Wilkins, M. R. (2010) Identification of arginine- and lysine-methylation in the proteome of Saccharomyces cerevisiae and its functional implications. BMC Genomics 11, 92
39. 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
40. Huttlin, E. L., Jedrychowski, M. P., Elias, J. E., Goswami, T., Rad, R., Beausoleil, S. A., Villen, J., Haas, W., Sowa, M. E., and Gygi, S. P. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189
41. Beausoleil, S. A., Villen, J., Gerber, S. A., Rush, J., and Gygi, S. P. (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292
42. Schilling, B., Rardin, M. J., MacLean, B. X., Zawadzka, A. M., Frewen, B. E., Cusack, M. P., Sorensen, D. J., Bereman, M. S., Jing, E., Wu, C. C., Verdin, E., Kahn, C. R., Maccoss, M. J., and Gibson, B. W. (2012) Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in skyline: application to protein acetylation and phosphorylation. Mol. Cell. Proteomics 11, 202-214
43. Zhang, H., Zha, X., Tan, Y., Hornbeck, P. V., Mastrangelo, A. J., Alessi, D. R., Polakiewicz, R. D., and Comb, M. J. (2002) Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 277, 39379-39387
44. Dhar, S., Vemulapalli, V., Patananan, A. N., Huang, G. L., Di Lorenzo, A., Richard, S., Comb, M. J., Guo, A., Clarke, S. G., and Bedford, M. T. (2013) Loss of the major Type I arginine methyltransferase PRMT1 causes substrate scavenging by other PRMTs. Sci. Rep. 3, 1311
45. Moritz, A., Li, Y., Guo, A., Villen, J., Wang, Y., MacNeill, J., Kornhauser, J., Sprott, K., Zhou, J., Possemato, A., Ren, J. M., Hornbeck, P., Cantley, L. C., Gygi, S. P., Rush, J., and Comb, M. J. (2010) Akt-RSK-S6 kinase signaling networks activated by oncogenic receptor tyrosine kinases. Sci. Signal. 3, ra64
46. Hsu, J. L., Huang, S. Y., Chow, N. H., and Chen, S. H. (2003) Stable-isotope dimethyl labeling for quantitative proteomics. Anal. Chem. 75, 6843-6852
47. Donlin, L. T., Andresen, C., Just, S., Rudensky, E., Pappas, C. T., Kruger, M., Jacobs, E. Y., Unger, A., Zieseniss, A., Dobenecker, M. W., Voelkel, T., Chait, B. T., Gregorio, C. C., Rottbauer, W., Tarakhovsky, A., and Linke, W. A. (2012) Smyd2 controls cytoplasmic lysine methylation of Hsp90 and myofilament organization. Genes Dev. 26, 114-119
48. Dhayalan, A., Kudithipudi, S., Rathert, P., and Jeltsch, A. (2011) Specificity analysis-based identification of new methylation targets of the SET7/9 protein lysine methyltransferase. Chem. Biol. 18, 111-120
49. Couture, J. F., Collazo, E., Hauk, G., and Trievel, R. C. (2006) Structural basis for the methylation site specificity of SET7/9. Nat. Struct. Mol. Biol. 13, 140-146
50. Schwartz, D., and Gygi, S. P. (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398
51. Brostoff, S., and Eylar, E. H. (1971) Localization of methylated arginine in the A1 protein from myelin. Proc. Natl. Acad. Sci. U.S.A. 68, 765-769
52. Cheng, D., Vemulapalli, V., and Bedford, M. T. (2012) Methods applied to the study of protein arginine methylation. Methods Enzymol. 512, 71-92
53. Najbauer, J., and Aswad, D. W. (1990) Diversity of methyl acceptor proteins in rat pheochromocytoma (PC12) cells revealed after treatment with adenosine dialdehyde. J. Biol. Chem. 265, 12717-12721
54. Sims, R. J., 3rd, Nishioka, K., and Reinberg, D. (2003) Histone lysine methylation: a signature for chromatin function. Trends Genet. 19, 629-639
55. Torres-Padilla, M. E., Parfitt, D. E., Kouzarides, T., and Zernicka-Goetz, M. (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445, 214-218
56. Beltran-Alvarez, P., Pagans, S., and Brugada, R. (2011) The cardiac sodium channel is post-translationally modified by arginine methylation. J. Proteome Res. 10, 3712-3719
57. Vosseller, K., Trinidad, J. C., Chalkley, R. J., Specht, C. G., Thalhammer, A., Lynn, A. J., Snedecor, J. O., Guan, S., Medzihradszky, K. F., Maltby, D. A., Schoepfer, R., and Burlingame, A. L. (2006) O-linked N-acetylglucosamine proteomics of postsynaptic density preparations using lectin weak affinity chromatography and mass spectrometry. Mol. Cell. Proteomics 5, 923-934
58. Tallent, M. K., Varghis, N., Skorobogatko, Y., Hernandez-Cuebas, L., Whelan, K., Vocadlo, D. J., and Vosseller, K. (2009) In vivo modulation of O-GlcNAc levels regulates hippocampal synaptic plasticity through interplay with phosphorylation. J. Biol. Chem. 284, 174-181
59. Lee, J., Sayegh, J., Daniel, J., Clarke, S., and Bedford, M. T. (2005) PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J. Biol. Chem. 280, 32890-32896