Emerging technologies to map the protein methylome

Journal of Molecular Biology

Volumn 426, Issue 20, 2014, Pages 3350-3362

  Carlson, Scott M ^a   Gozani, Or ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

arginine methylation; lysine methylation; methyltransferase; proteomics; signaling

Indexed keywords

ARGININE; BINDING PROTEIN; LYSINE; PROTEIN METHYLTRANSFERASE; HISTONE; NONHISTONE PROTEIN; PROTEOME;

AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; ARTICLE; CELL DIFFERENTIATION; CHEMICAL GENETICS; DRUG DEVELOPMENT; ENZYME SUBSTRATE COMPLEX; HIGH THROUGHPUT SCREENING; HIGH THROUGHPUT SEQUENCING; HISTONE MODIFICATION; HYDROPHILIC INTERACTION CHROMATOGRAPHY; ISOTOPE LABELING; MASS SPECTROMETRY; PEPTIDE LIBRARY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN METHYLATION; PROTEIN MICROARRAY; PROTEIN PROCESSING; PROTEIN TARGETING; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; ANIMAL; HUMAN; IMMUNOPRECIPITATION; METABOLISM; METHYLATION; PROCEDURES;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HISTONES; HUMANS; IMMUNOPRECIPITATION; METHYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS;

EID: 84907577266     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.04.024     Document Type: Review

References (82)

1. X. Zhang, H. Wen, and X. Shi Lysine methylation: beyond histones Acta Biochim Biophys Sin (Shanghai) 44 2012 14 27
2. A. Di Lorenzo, and M.T. Bedford Histone arginine methylation FEBS Lett 585 2011 2024 2031
3. Y. Yang, and M.T. Bedford Protein arginine methyltransferases and cancer Nat Rev Cancer 13 2013 37 50
4. K.A. Mowen, J. Tang, W. Zhu, B.T. Schurter, K. Shuai, and H.R. Herschman Arginine methylation of STAT1 modulates IFNalpha/beta-induced transcription Cell 104 2001 731 741
5. F.M. Boisvert, J. Cote, M.C. Boulanger, P. Cleroux, F. Bachand, and C. Autexier Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing J Cell Biol 159 2002 957 969
6. H. Iwasaki, and T. Yada Protein arginine methylation regulates insulin signaling in L6 skeletal muscle cells Biochem Biophys Res Commun 364 2007 1015 1021
7. M.T. Bedford, and S.G. Clarke Protein arginine methylation in mammals: who, what, and why Mol Cell 33 2009 1 13
8. M.T. Bedford, and S. Richard Arginine methylation an emerging regulator of protein function Mol Cell 18 2005 263 272
9. H.S. Han, C.Y. Jung, Y.S. Yoon, S. Choi, D. Choi, and G. Kang Arginine methylation of CRTC2 is critical in the transcriptional control of hepatic glucose metabolism Sci Signaling 7 2014 ra19
10. X. Shi, I. Kachirskaia, H. Yamaguchi, L.E. West, H. Wen, and E.W. Wang Modulation of p53 function by SET8-mediated methylation at lysine 382 Mol Cell 27 2007 636 646
11. D. Levy, A.J. Kuo, Y. Chang, U. Schaefer, C. Kitson, and P. Cheung Lysine methylation of the NF-κB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-κB signaling Nat Immunol 12 2011 29 36
12. J. Huang, and S.L. Berger The emerging field of dynamic lysine methylation of non-histone proteins Curr Opin Genet Dev 18 2008 152 158
13. T.C. Petrossian, and S.G. Clarke Uncovering the human methyltransferasome Mol Cell Proteomics 10 2011 [M110.000976]
14. T.C. Petrossian, and S.G. Clarke Multiple motif scanning to identify methyltransferases from the yeast proteome Mol Cell Proteomics 8 2009 1516 1526
15. B.D. Young, D.I. Weiss, C.I. Zurita-Lopez, K.J. Webb, S.G. Clarke, and A.E. McBride Identification of methylated proteins in the yeast small ribosomal subunit: a role for SPOUT methyltransferases in protein arginine methylation Biochemistry 51 2012 5091 5104
16. S.B. Ficarro, M.L. McCleland, P.T. Stukenberg, D.J. Burke, M.M. Ross, and J. Shabanowitz Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae Nat Biotechnol 20 2002 301 305
17. C. Choudhary, C. Kumar, F. Gnad, M. Nielsen, M. Rehman, and T. Walther Lysine acetylation targets protein complexes and co-regulates major cellular functions Science 325 2009 834 840
18. Y. Zhang, A. Wolf-Yadlin, P. Ross, D. Pappin, J. Rush, and D. Lauffenburger Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules Mol Cell Proteomics 4 2005 1240 1250
19. G. Xu, J. Paige, and S. Jaffrey Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling Nat Biotechnol 28 2010 868 873
20. L. Afjehi-Sadat, and B.A. Garcia Comprehending dynamic protein methylation with mass spectrometry Curr Opin Chem Biol 17 2013 12 19
21. A.F. Altelaar, J. Munoz, and A.J. Heck Next-generation proteomics: towards an integrative view of proteome dynamics Nat Rev Genet 14 2013 35 48
22. F.M. Boisvert, J. Côté, M.C. Boulanger, and S. Richard A proteomic analysis of arginine-methylated protein complexes Mol Cell Proteomics 2 2003 1319 1330
23. A. Guo, H. Gu, J. Zhou, D. Mulhern, Y. Wang, and K.A. Lee Immunoaffinity enrichment and mass spectrometry analysis of protein methylation Mol Cell Proteomics 13 2014 372 387
24. P. Bulau, D. Zakrzewicz, K. Kitowska, B. Wardega, J. Kreuder, and O. Eickelberg Quantitative assessment of arginine methylation in free versus protein-incorporated amino acids in vitro and in vivo using protein hydrolysis and high-performance liquid chromatography Biotechniques 40 2006 305 310
25. T. Uhlmann, V.L. Geoghegan, B. Thomas, G. Ridlova, D.C. Trudgian, and O. Acuto A method for large-scale identification of protein arginine methylation Mol Cell Proteomics 11 2012 1489 1499
26. S.E. Ong, G. Mittler, and M. Mann Identifying and quantifying in vivo methylation sites by heavy methyl SILAC Nat Methods 1 2004 119 126
27. X.J. Cao, A.M. Arnaudo, and B.A. Garcia Large-scale global identification of protein lysine methylation in vivo Epigenetics 8 2013 477 485
28. K.E. Moore, S.M. Carlson, N.D. Camp, P. Cheung, R.G. James, and K.F. Chua A general molecular affinity strategy for global detection and proteomic analysis of lysine methylation Mol Cell 50 2013 444 456
29. S.M. Carlson, K.E. Moore, E.M. Green, G.M. Martin, and O. Gozani Proteome-wide enrichment of proteins modified by lysine methylation Nat Protoc 9 2014 37 50
30. H. Liu, M. Galka, E. Mori, X. Liu, Y.F. Lin, and R. Wei A method for systematic mapping of protein lysine methylation identifies functions for HP1β in DNA damage response Mol Cell 50 2013 723 735
31. F.M. Boisvert, U. Déry, J.Y. Masson, and S. Richard Arginine methylation of MRE11 by PRMT1 is required for DNA damage checkpoint control Genes Dev 19 2005 671 676
32. S.Y. Jung, Y. Li, Y. Wang, Y. Chen, Y. Zhao, and J. Qin 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 2008 1721 1729
33. C.J. Hung, Y.J. Lee, D.H. Chen, and C. Li Proteomic analysis of methylarginine-containing proteins in HeLa cells by two-dimensional gel electrophoresis and immunoblotting with a methylarginine-specific antibody Protein J 28 2009 139 147
34. Y.Y. Chiou, S.L. Fu, W.J. Lin, and C.H. Lin Proteomics analysis of in vitro protein methylation during Src-induced transformation Electrophoresis 33 2012 451 461
35. J.C. Fisk, J. Li, H. Wang, J.M. Aletta, J. Qu, and L.K. Read Proteomic analysis reveals diverse classes of arginine methylproteins in mitochondria of trypanosomes Mol Cell Proteomics 12 2013 302 311
36. K. Lott, J. Li, J.C. Fisk, H. Wang, J.M. Aletta, and J. Qu Global proteomic analysis in trypanosomes reveals unique proteins and conserved cellular processes impacted by arginine methylation J Proteomics 91 2013 210 225
37. K.B. Sylvestersen, H. Horn, S. Jungmichel, L.J. Jensen, and M.L. Nielsen Proteomic analysis of arginine methylation sites in human cells reveals dynamic regulation during transcriptional arrest Mol Cell Proteomics 2014 [Epub ahead of print]
38. S. Ong, B. Blagoev, I. Kratchmarova, D. Kristensen, H. Steen, and A. Pandey Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol Cell Proteomics 1 2002 376 386
39. M. Bremang, A. Cuomo, A.M. Agresta, M. Stugiewicz, V. Spadotto, and T. Bonaldi Mass spectrometry-based identification and characterisation of lysine and arginine methylation in the human proteome Mol BioSyst 9 2013 2231 2247
40. J. Min, A. Allali-Hassani, N. Nady, C. Qi, H. Ouyang, and Y. Liu L3MBTL1 recognition of mono- and dimethylated histones Nat Struct Mol Biol 14 2007 1229 1230
41. N. Nady, L. Krichevsky, N. Zhong, S. Duan, W. Tempel, and M.F. Amaya Histone recognition by human malignant brain tumor domains J Mol Biol 423 2012 702 718
42. M. Vedadi, D. Barsyte-Lovejoy, F. Liu, S. Rival-Gervier, A. Allali-Hassani, and V. Labrie A chemical probe selectively inhibits G9a and GLP methyltransferase activity in cells Nat Chem Biol 7 2011 566 574
43. M. Tachibana, K. Sugimoto, T. Fukushima, and Y. Shinkai Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3 J Biol Chem 276 2001 25309 25317
44. Y. Shinkai, and M. Tachibana H3K9 methyltransferase G9a and the related molecule GLP Genes Dev 25 2011 781 788
45. P. Rathert, A. Dhayalan, M. Murakami, X. Zhang, R. Tamas, and R. Jurkowska Protein lysine methyltransferase G9a acts on non-histone targets Nat Chem Biol 4 2008 344 346
46. S.C. Sampath, I. Marazzi, K.L. Yap, A.N. Krutchinsky, I. Mecklenbräuker, and A. Viale Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly Mol Cell 27 2007 596 608
47. D. Berwick, and J. Tavaré Identifying protein kinase substrates: hunting for the organ-grinder's monkeys Trends Biochem Sci 29 2004 227 232
48. H.H. Ng, Q. Feng, H. Wang, H. Erdjument-Bromage, P. Tempst, and Y. Zhang Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association Genes Dev 16 2002 1518 1527
49. S. Kernstock, E. Davydova, M. Jakobsson, A. Moen, S. Pettersen, and G.M. Mælandsmo Lysine methylation of VCP by a member of a novel human protein methyltransferase family Nat Commun 3 2012 1038
50. M.E. Jakobsson, A. Moen, L. Bousset, W. Egge-Jacobsen, S. Kernstock, and R. Melki Identification and characterization of a novel human methyltransferase modulating Hsp70 protein function through lysine methylation J Biol Chem 288 2013 27752 27763
51. H. Zhu, J.F. Klemic, S. Chang, P. Bertone, A. Casamayor, and K.G. Klemic Analysis of yeast protein kinases using protein chips Nat Genet 26 2000 283 289
52. H. Zhu, M. Bilgin, R. Bangham, D. Hall, A. Casamayor, and P. Bertone Global analysis of protein activities using proteome chips Science 293 2001 2101 2105
53. L. Meng, G.A. Michaud, J.S. Merkel, F. Zhou, J. Huang, and D.R. Mattoon Protein kinase substrate identification on functional protein arrays BMC Biotechnol 8 2008 22
54. S.V. Del Rincón, J. Rogers, M. Widschwendter, D. Sun, H.B. Sieburg, and C. Spruck Development and validation of a method for profiling post-translational modification activities using protein microarrays PLoS One 5 2010 e11332
55. J. Lee, and M.T. Bedford PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays EMBO Rep 3 2002 268 273
56. D. Levy, C.L. Liu, Z. Yang, A.M. Newman, A.A. Alizadeh, and P.J. Utz A proteomic approach for the identification of novel lysine methyltransferase substrates Epigenetics Chromatin 4 2011 19
57. Q. Liu, and G. Dreyfuss in vivo and in vitro arginine methylation of RNA-binding proteins Mol Cell Biol 15 1995 2800 2808
58. A.D. Sharrocks, S.H. Yang, and A. Galanis Docking domains and substrate-specificity determination for MAP kinases Trends Biochem Sci 25 2000 448 453
59. A.M. Al-Ayoubi, H. Zheng, Y. Liu, T. Bai, and S.T. Eblen Mitogen-activated protein kinase phosphorylation of splicing factor 45 (SPF45) regulates SPF45 alternative splicing site utilization, proliferation, and cell adhesion Mol Cell Biol 32 2012 2880 2893
60. R. Swiercz, M.D. Person, and M.T. Bedford Ribosomal protein S2 is a substrate for mammalian PRMT3 (protein arginine methyltransferase 3) Biochem J 386 2005 85 91
61. N. El-Andaloussi, T. Valovka, M. Toueille, R. Steinacher, F. Focke, and P. Gehrig Arginine methylation regulates DNA polymerase beta Mol Cell 22 2006 51 62
62. S.S. Koh, H. Li, Y.H. Lee, R.B. Widelitz, C.M. Chuong, and M.R. Stallcup Synergistic coactivator function by coactivator-associated arginine methyltransferase (CARM) 1 and beta-catenin with two different classes of DNA-binding transcriptional activators J Biol Chem 277 2002 26031 26035
63. M. Le Romancer, I. Treilleux, N. Leconte, Y. Robin-Lespinasse, S. Sentis, and K. Bouchekioua-Bouzaghou Regulation of estrogen rapid signaling through arginine methylation by PRMT1 Mol Cell 31 2008 212 221
64. J. Ren, Y. Wang, Y. Liang, Y. Zhang, S. Bao, and Z. Xu Methylation of ribosomal protein S10 by protein-arginine methyltransferase 5 regulates ribosome biogenesis J Biol Chem 285 2010 12695 12705
65. M. Abu-Farha, S. Lanouette, F. Elisma, V. Tremblay, J. Butson, and D. Figeys Proteomic analyses of the SMYD family interactomes identify HSP90 as a novel target for SMYD2 J Mol Cell Biol 3 2011 301 308
66. K. Shah, Y. Liu, C. Deirmengian, and K. Shokat Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates Proc Natl Acad Sci U S A 94 1997 3565 3570
67. A. Bishop, K. Shah, Y. Liu, L. Witucki, C. Kung, and K. Shokat Design of allele-specific inhibitors to probe protein kinase signaling Curr Biol 8 1998 257 266
68. Y. Liu, K. Shah, F. Yang, L. Witucki, and K. Shokat Engineering Src family protein kinases with unnatural nucleotide specificity Chem Biol 5 1998 91 101
69. J. Allen, S. Lazerwith, and K. Shokat Bio-orthogonal affinity purification of direct kinase substrates J Am Chem Soc 127 2005 5288 5289
70. J. Blethrow, J. Glavy, D. Morgan, and K. Shokat Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates Proc Natl Acad Sci U S A 105 2008 1442 1447
71. S.M. Carlson, C.R. Chouinard, A. Labadorf, C.J. Lam, K. Schmelzle, and E. Fraenkel Large-scale discovery of ERK2 substrates identifies ERK-mediated transcriptional regulation by ETV3 Sci Signaling 4 2011 rs11
72. M.R. Banko, J.J. Allen, B.E. Schaffer, E.W. Wilker, P. Tsou, and J.L. White Chemical genetic screen for AMPKα2 substrates uncovers a network of proteins involved in mitosis Mol Cell 44 2011 878 892
73. L.E. Berchowitz, A.S. Gajadhar, F.J. van Werven, A.A. De Rosa, M.L. Samoylova, and G.A. Brar A developmentally regulated translational control pathway establishes the meiotic chromosome segregation pattern Genes Dev 27 2013 2147 2163
74. Q. Lin, F. Jiang, P.G. Schultz, and N.S. Gray Design of allele-specific protein methyltransferase inhibitors J Am Chem Soc 123 2001 11608 11613
75. O. Binda, M. Boyce, J.S. Rush, K.K. Palaniappan, C.R. Bertozzi, and O. Gozani A chemical method for labeling lysine methyltransferase substrates ChemBioChem 12 2011 330 334
76. H.C. Kolb, M.G. Finn, and K.B. Sharpless Click chemistry: diverse chemical function from a few good reactions Angew Chem Int Ed Engl 40 2001 2004 2021
77. M.D. Best Click chemistry and bioorthogonal reactions: unprecedented selectivity in the labeling of biological molecules Biochemistry 48 2009 6571 6584
78. K. Islam, W. Zheng, H. Yu, H. Deng, and M. Luo Expanding cofactor repertoire of protein lysine methyltransferase for substrate labeling ACS Chem Biol 6 2011 679 684
79. R. Wang, G. Ibáñez, K. Islam, W. Zheng, G. Blum, and C. Sengelaub Formulating a fluorogenic assay to evaluate S-adenosyl-l-methionine analogues as protein methyltransferase cofactors Mol BioSyst 7 2011 2970 2981
80. R. Wang, W. Zheng, H. Yu, H. Deng, and M. Luo Labeling substrates of protein arginine methyltransferase with engineered enzymes and matched S-adenosyl-l-methionine analogues J Am Chem Soc 133 2011 7648 7651
81. K. Islam, I. Bothwell, Y. Chen, C.A. Sengelaub, R. Wang, and H. Deng Bioorthogonal profiling of protein methylation (BPPM) using azido derivative of S-adenosyl-l-methionine J Am Chem Soc 134 2012 5909 5915
82. H. Guo, R. Wang, W. Zheng, Y. Chen, G. Blum, and H. Deng Profiling substrates of protein arginine N-methyltransferase 3 with S-adenosyl-l-methionine analogues ACS Chem Biol 9 2014 476 484