A chemical proteomics approach for global analysis of lysine monomethylome profiling

Molecular and Cellular Proteomics

Volumn 14, Issue 2, 2015, Pages 329-339

  Wu, Zhixiang ^a   Cheng, Zhongyi ^b   Sun, Mingwei ^a   Wan, Xuelian ^a   Liu, Ping ^a   He, Tieming ^b   Tan, Minjia ^a   Zhao, Yingming ^a,c  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b Jingjie PTM BioLab (Hangzhou) Co Ltd   (China)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; LYSINE; ANTIBODY; PEPTIDE; PROTEOME;

ARTICLE; CELL NUCLEUS; CHROMATIN STRUCTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; METHYLATION; PRIORITY JOURNAL; PROPIONYLATION; PROTEIN PROCESSING; PROTEOMICS; SPLICEOSOME; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; BIOLOGY; CELL LINE; CHEMISTRY; ISOTOPE LABELING; METABOLISM; MOLECULAR GENETICS; PROCEDURES; REPRODUCIBILITY;

AMINO ACID SEQUENCE; ANTIBODIES; CELL LINE; COMPUTATIONAL BIOLOGY; HUMANS; ISOTOPE LABELING; LYSINE; METHYLATION; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS;

EID: 84921911446     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.044255     Document Type: Article

References (67)

1. Ambler, R. P., and Rees, M. W. (1959) Epsilon-N-Methyl-lysine in bacterial flagellar protein. Nature 184, 56-57
2. Allfrey, V. G., Faulkner, R., and Mirsky, A. E. (1964) Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. U.S.A. 51, 786-794
3. Rice, J. C., and Allis, C. D. (2001) Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13, 263-273
4. Martin, C., and Zhang, Y. (2005) The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6, 838-849
5. Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B. D., Sun, Z. W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C. P., Allis, C. D., and Jenuwein, T. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-599
6. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., Casero, R. A., and Shi, Y. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953
7. Copeland, R. A., Solomon, M. E., and Richon, V. M. (2009) Protein methyltransferases as a target class for drug discovery. Nat. Rev. Drug Discov. 8, 724-732
8. Schapira, M. (2011) Structural chemistry of human SET domain protein methyltransferases. Curr. Chem. Genomics 5, 85-94
9. Pedersen, M. T., and Helin, K. (2010) Histone demethylases in development and disease. Trends Cell Biol. 20, 662-671
10. Copeland, R. A., Moyer, M. P., and Richon, V. M. (2013) Targeting genetic alterations in protein methyltransferases for personalized cancer therapeutics. Oncogene 32, 939-946
11. Arrowsmith, C. H., Bountra, C., Fish, P. V., Lee, K., and Schapira, M. (2012) Epigenetic protein families: a new frontier for drug discovery. Nat. Rev. Drug Discov. 11, 384-400
12. Clarke, S. G. (2013) Protein methylation at the surface and buried deep: thinking outside the histone box. Trends Biochem. Sci. 38, 243-252
13. Huang, J., and Berger, S. L. (2008) The emerging field of dynamic lysine methylation of non-histone proteins. Curr. Opin. Genet. Dev. 18, 152-158
14. Jakobsson, M. E., Moen, A., Bousset, L., Egge-Jacobsen, W., Kernstock, S., Melki, R., and Falnes, P. O. (2013) Identification and characterization of a novel human methyltransferase modulating Hsp70 protein function through lysine methylation. J. Biol. Chem. 288, 27752-27763
15. Gu, W., and Roeder, R. G. (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90, 595-606
16. Kim, S. C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J., Cheng, T., Kho, Y., Xiao, H., Xiao, L., Grishin, N. V., White, M., Yang, X. J., and Zhao, Y. (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 23, 607-618
17. 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
18. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H., Li, Y., Shi, J., An, W., Hancock, S. M., He, F., Qin, L., Chin, J., Yang, P., Chen, X., Lei, Q., Xiong, Y., and Guan, K. L. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327, 1000-1004
19. Chen, Y., Zhao, W., Yang, J. S., Cheng, Z., Luo, H., Lu, Z., Tan, M., Gu, W., and Zhao, Y. (2012) Quantitative acetylome analysis reveals the roles of SIRT1 in regulating diverse substrates and cellular pathways. Mol. Cell. Proteomics 11, 1048-1062
20. Kelman, Z., Naktinis, V., and O'Donnell, M. (1995) Radiolabeling of proteins for biochemical studies. Methods Enzymol. 262, 430-442
21. Ficarro, S. B., McCleland, M. L., Stukenberg, P. T., Burke, D. J., Ross, M. M., Shabanowitz, J., Hunt, D. F., and White, F. M. (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20, 301-305
22. 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
23. Carlson, S. M., Moore, K. E., Green, E. M., Martin, G. M., and Gozani, O. (2014) Proteome-wide enrichment of proteins modified by lysine methylation. Nat. Protoc. 9, 37-50
24. Bremang, M., Cuomo, A., Agresta, A. M., Stugiewicz, M., Spadotto, V., and Bonaldi, T. (2013) Mass spectrometry-based identification and characterization of lysine and arginine methylation in the human proteome. Mol. Biosyst. 9, 2231-2247
25. 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
26. Moore, K. E., Carlson, S. M., Camp, N. D., Cheung, P., James, R. G., Chua, K. F., Wolf-Yadlin, A., and Gozani, O. (2013) A general molecular affinity strategy for global detection and proteomic analysis of lysine methylation. Mol. Cell 50, 444-456
27. Garcia, B. A., Mollah, S., Ueberheide, B. M., Busby, S. A., Muratore, T. L., Shabanowitz, J., and Hunt, D. F. (2007) Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nat. Protoc. 2, 933-938
28. Kim, S. C., Chen, Y., Mirza, S., Xu, Y., Lee, J., Liu, P., and Zhao, Y. (2006) A clean, more efficient method for in-solution digestion of protein mixtures without detergent or urea. J. Proteome Res. 5, 3446-3452
29. Wang, Y., Yang, F., Gritsenko, M. A., Wang, Y., Clauss, T., Liu, T., Shen, Y., Monroe, M. E., Lopez-Ferrer, D., Reno, T., Moore, R. J., Klemke, R. L., Camp, D. G., 2nd, and Smith, R. D. (2011) Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells. Proteomics 11, 2019-2026
30. Chen, Y., Kwon, S. W., Kim, S. C., and Zhao, Y. (2005) Integrated approach for manual evaluation of peptides identified by searching protein sequence databases with tandem mass spectra. J. Proteome Res. 4, 998-1005
31. Wu, Z., Moghaddas Gholami, A., and Kuster, B. (2012) Systematic identification of the HSP90 candidate regulated proteome. Mol. Cell. Proteo-mics 11, M111 016675
32. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene Ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
33. Kanehisa, M., and Goto, S. (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30
34. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2008) The Pfam protein families database. Nucleic Acids Res. 36, D281-D288
35. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13
36. Hochberg, Y. B. a. Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B 57, 12
37. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504
38. Bader, G. D., and Hogue, C. W. (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4, 2
39. Ruepp, A., Brauner, B., Dunger-Kaltenbach, I., Frishman, G., Montrone, C., Stransky, M., Waegele, B., Schmidt, T., Doudieu, O. N., Stumpflen, V., and Mewes, H. W. (2008) CORUM: the comprehensive resource of mammalian protein complexes. Nucleic Acids Res. 36, D646-D650
40. 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
41. Olsen, J. V., and Mann, M. (2013) Status of large-scale analysis of posttranslational modifications by mass spectrometry. Mol. Cell. Proteomics 12, 3444-3452
42. Zhao, Y., and Jensen, O. N. (2009) Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques. Proteomics 9, 4632-4641
43. Chen, Y., Sprung, R., Tang, Y., Ball, H., Sangras, B., Kim, S. C., Falck, J. R., Peng, J., Gu, W., and Zhao, Y. (2007) Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol. Cell. Proteomics 6, 812-819
44. http://www.unimod.org/modifications-list.php?
45. http://www.uniprot.org/.
46. Liu, M., Liu, Y., Cheng, J., Zhang, S. L., Wang, L., Shao, Q., Zhang, J., and Yang, Q. (2004) Transactivating effect of hepatitis C virus core protein: a suppression subtractive hybridization study. World J. Gastroenterol. 10, 1746-1749
47. Greer, E. L., and Shi, Y. (2012) Histone methylation: a dynamic mark in health, disease, and inheritance. Nat. Rev. Genet. 13, 343-357
48. Garcia, B. A., Hake, S. B., Diaz, R. L., Kauer, M., Morris, S. A., Recht, J., Shabanowitz, J., Mishra, N., Strahl, B. D., Allis, C. D., and Hunt, D. F. (2007) Organismal differences in post-translational modifications in histones H3 and H4. J. Biol. Chem. 282, 7641-7655
49. Boudrez, A., Beullens, M., Groenen, P., Van Eynde, A., Vulsteke, V., Jagiello, I., Murray, M., Krainer, A. R., Stalmans, W., and Bollen, M. (2000) NIPP1-mediated interaction of protein phosphatase-1 with CDC5L, a regulator of pre-mRNA splicing and mitotic entry. J. Biol. Chem. 275, 25411-25417
50. Palmieri, F. (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch. 447, 689-709
51. Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., Bork, P., and von Mering, C. (2009) STRING 8-A global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-D416
52. Musselman, C. A., Lalonde, M. E., Cote, J., and Kutateladze, T. G. (2012) Perceiving the epigenetic landscape through histone readers. Nat. Struct. Mol. Biol. 19, 1218-1227
53. Park, J., Chen, Y., Tishkoff, D. X., Peng, C., Tan, M., Dai, L., Xie, Z., Zhang, Y., Zwaans, B. M., Skinner, M. E., Lombard, D. B., and Zhao, Y. (2013) SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. Mol. Cell 50, 919-930
54. Bothwell, I. R., Islam, K., Chen, Y., Zheng, W., Blum, G., Deng, H., and Luo, M. (2012) Se-adenosyl-L-selenomethionine cofactor analog as a reporter of protein methylation. J. Am. Chem. Soc. 134, 14905-14912
55. Liu, H., Galka, M., Mori, E., Liu, X., Lin, Y. F., Wei, R., Pittock, P., Voss, C., Dhami, G., Li, X., Miyaji, M., Lajoie, G., Chen, B., and Li, S. S. (2013) A method for systematic mapping of protein lysine methylation identifies functions for HP1beta in DNA damage response. Mol. Cell 50, 723-735
56. 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
57. Witze, E. S., Old, W. M., Resing, K. A., and Ahn, N. G. (2007) Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 4, 798-806
58. Chin, H. G., Esteve, P. O., Pradhan, M., Benner, J., Patnaik, D., Carey, M. F., and Pradhan, S. (2007) Automethylation of G9a and its implication in wider substrate specificity and HP1 binding. Nucleic Acids Res. 35, 7313-7323
59. Sarraf, S. A., and Stancheva, I. (2004) Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell 15, 595-605
60. Loyola, A., Tagami, H., Bonaldi, T., Roche, D., Quivy, J. P., Imhof, A., Nakatani, Y., Dent, S. Y., and Almouzni, G. (2009) The HP1alpha-CAF1-SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep. 10, 769-775
61. Downward, J., Parker, P., and Waterfield, M. D. (1984) Autophosphorylation sites on the epidermal growth factor receptor. Nature 311, 483-485
62. Jain, S., Wei, J., Mitrani, L. R., and Bishopric, N. H. (2012) Auto-acetylation stabilizes p300 in cardiac myocytes during acute oxidative stress, promoting STAT3 accumulation and cell survival. Breast Cancer Res. Treat. 135, 103-114
63. Yang, Y., and Bedford, M. T. (2013) Protein arginine methyltransferases and cancer. Nat. Rev. Cancer 13, 37-50
64. Hunter, T. (2007) The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 28, 730-738
65. Guillemette, B., Drogaris, P., Lin, H. H., Armstrong, H., Hiragami-Hamada, K., Imhof, A., Bonneil, E., Thibault, P., Verreault, A., and Festenstein, R. J. (2011) H3 lysine 4 is acetylated at active gene promoters and is regulated by H3 lysine 4 methylation. PLoS Genet. 7, e1001354
66. Wagner, T., and Jung, M. (2012) New lysine methyltransferase drug targets in cancer. Nat. Biotechnol. 30, 622-623
67. Chuikov, S., Kurash, J. K., Wilson, J. R., Xiao, B., Justin, N., Ivanov, G. S., McKinney, K., Tempst, P., Prives, C., Gamblin, S. J., Barlev, N. A., and Reinberg, D. (2004) Regulation of p53 activity through lysine methylation. Nature 432, 353-360