Toward Understanding Molecular Recognition between PRMTs and their Substrates

Author(s): Owen M. Price, Joan M. Hevel*

Journal Name: Current Protein & Peptide Science

Volume 21 , Issue 7 , 2020

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Graphical Abstract:


Protein arginine methylation is a widespread eukaryotic posttranslational modification that occurs with as much frequency as ubiquitinylation. Yet, how the nine different human protein arginine methyltransferases (PRMTs) recognize their respective protein targets is not well understood. This review summarizes the progress that has been made over the last decade or more to resolve this significant biochemical question. A multipronged approach involving structural biology, substrate profiling, bioorthogonal chemistry and proteomics is discussed.

Keywords: PRMT, arginine methylation, substrate specificity, PRMT molecular recognition, arginine methylome, target recognition.

Fulton, M.D.; Brown, T.; Zheng, Y.G. Mechanisms and Inhibitors of Histone Arginine Methylation. Chem. Rec., 2018, 18(12), 1792-1807.
[] [PMID: 30230223]
Di Lorenzo, A.; Bedford, M.T. Histone arginine methylation. FEBS Lett., 2011, 585(13), 2024-2031.
[] [PMID: 21074527]
Wysocka, J.; Allis, C.D.; Coonrod, S. Histone arginine methylation and its dynamic regulation. Front. Biosci., 2006, 11, 344-355.
[] [PMID: 16146736]
Litt, M.; Qiu, Y.; Huang, S. Histone arginine methylations: their roles in chromatin dynamics and transcriptional regulation. Biosci. Rep., 2009, 29(2), 131-141.
[] [PMID: 19220199]
Fuhrmann, J.; Clancy, K.W.; Thompson, P.R. Chemical biology of protein arginine modifications in epigenetic regulation. Chem. Rev., 2015, 115(11), 5413-5461.
[] [PMID: 25970731]
Larsen, S.C.; Sylvestersen, K.B.; Mund, A.; Lyon, D.; Mullari, M.; Madsen, M.V.; Daniel, J.A.; Jensen, L.J.; Nielsen, M.L. Proteome-wide analysis of arginine monomethylation reveals widespread occurrence in human cells. Sci. Signal., 2016, 9(443), rs9-rs9.
[] [PMID: 27577262]
Lee, Y.H.; Stallcup, M.R. Minireview: protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol. Endocrinol., 2009, 23(4), 425-433.
[] [PMID: 19164444]
Raposo, A.E.; Piller, S.C. Protein arginine methylation: an emerging regulator of the cell cycle. Cell Div., 2018, 13(3), 3.
[] [PMID: 29568320]
Stouth, D.W.; vanLieshout, T.L.; Shen, N.Y.; Ljubicic, V. Regulation of Skeletal Muscle Plasticity by Protein Arginine Methyltransferases and Their Potential Roles in Neuromuscular Disorders. Front. Physiol., 2017, 8(870), 870.
[] [PMID: 29163212]
Blanc, R.S.; Richard, S. Arginine Methylation: The Coming of Age. Mol. Cell, 2017, 65(1), 8-24.
[] [PMID: 28061334]
Bedford, M.T.; Clarke, S.G. Protein arginine methylation in mammals: who, what, and why. Mol. Cell, 2009, 33(1), 1-13.
[] [PMID: 19150423]
Yang, Y.; Bedford, M.T. Protein arginine methyltransferases and cancer. Nat. Rev. Cancer, 2013, 13(1), 37-50.
[] [PMID: 23235912]
Morales, Y.; Cáceres, T.; May, K.; Hevel, J.M. Biochemistry and regulation of the protein arginine methyltransferases (PRMTs). Arch. Biochem. Biophys., 2016, 590, 138-152.
[] [PMID: 26612103]
Woodsmith, J.; Casado-Medrano, V.; Benlasfer, N.; Eccles, R.L.; Hutten, S.; Heine, C.L.; Thormann, V.; Abou-Ajram, C.; Rocks, O.; Dormann, D.; Stelzl, U. Interaction modulation through arrays of clustered methyl-arginine protein modifications. Life Sci Alliance, 2018, 1(5)e201800178
[] [PMID: 30456387]
Côté, J.; Boisvert, F-M.; Boulanger, M-C.; Bedford, M.T.; Richard, S. Sam68 RNA binding protein is an in vivo substrate for protein arginine N-methyltransferase 1. Mol. Biol. Cell, 2003, 14(1), 274-287.
[] [PMID: 12529443]
Lischwe, M.A.; Cook, R.G.; Ahn, Y.S.; Yeoman, L.C.; Busch, H. Clustering of glycine and NG,NG-dimethylarginine in nucleolar protein C23. Biochemistry, 1985, 24(22), 6025-6028.
[] [PMID: 4084504]
Fronz, K.; Güttinger, S.; Burkert, K.; Kühn, U.; Stöhr, N.; Schierhorn, A.; Wahle, E. Arginine methylation of the nuclear poly(a) binding protein weakens the interaction with its nuclear import receptor, transportin. J. Biol. Chem., 2011, 286(38), 32986-32994.
[] [PMID: 21808065]
Wei, Y.; Horng, J-C.; Vendel, A.C.; Raleigh, D.P.; Lumb, K.J. Contribution to stability and folding of a buried polar residue at the CARM1 methylation site of the KIX domain of CBP. Biochemistry, 2003, 42(23), 7044-7049.
[] [PMID: 12795599]
El-Andaloussi, N.; Valovka, T.; Toueille, M.; Steinacher, R.; Focke, F.; Gehrig, P.; Covic, M.; Hassa, P.O.; Schär, P.; Hübscher, U.; Hottiger, M.O. Arginine methylation regulates DNA polymerase β. Mol. Cell, 2006, 22(1), 51-62.
[] [PMID: 16600869]
Fulton, M.D.; Brown, T.; Zheng, Y.G. The Biological Axis of Protein Arginine Methylation and Asymmetric Dimethylarginine. Int. J. Mol. Sci., 2019, 20(13)E3322
[] [PMID: 31284549]
Chong, P.A.; Vernon, R.M.; Forman-Kay, J.D. RGG/RG Motif Regions in RNA Binding and Phase Separation. J. Mol. Biol., 2018, 430(23), 4650-4665.
[] [PMID: 29913160]
Yu, M.C. The Role of Protein Arginine Methylation in mRNP Dynamics. Mol. Biol. Int., 2011, 2011163827
[] [PMID: 22091396]
Lorton, B.M.; Shechter, D. Cellular consequences of arginine methylation. Cell. Mol. Life Sci., 2019, 76(15), 2933-2956.
[] [PMID: 31101937]
Cura, V.; Troffer-Charlier, N.; Wurtz, J-M.; Bonnefond, L.; Cavarelli, J. Structural insight into arginine methylation by the mouse protein arginine methyltransferase 7: a zinc finger freezes the mimic of the dimeric state into a single active site. Acta Crystallogr. D Biol. Crystallogr., 2014, 70(Pt 9), 2401-2412.
[] [PMID: 25195753]
Schapira, M.; Ferreira de Freitas, R. Structural biology and chemistry of protein arginine methyltransferases. MedChemComm, 2014, 5(12), 1779-1788.
[] [PMID: 26693001]
Antonysamy, S.; Bonday, Z.; Campbell, R.M.; Doyle, B.; Druzina, Z.; Gheyi, T.; Han, B.; Jungheim, L.N.; Qian, Y.; Rauch, C.; Russell, M.; Sauder, J.M.; Wasserman, S.R.; Weichert, K.; Willard, F.S.; Zhang, A.; Emtage, S. Crystal structure of the human PRMT5:MEP50 complex. Proc. Natl. Acad. Sci. USA, 2012, 109(44), 17960-17965.
[] [PMID: 23071334]
Sun, L.; Wang, M.; Lv, Z.; Yang, N.; Liu, Y.; Bao, S.; Gong, W.; Xu, R-M. Structural insights into protein arginine symmetric dimethylation by PRMT5. Proc. Natl. Acad. Sci. USA, 2011, 108(51), 20538-20543.
[] [PMID: 22143770]
Tewary, S.K.; Zheng, Y.G.; Ho, M-C. Protein arginine methyltransferases: insights into the enzyme structure and mechanism at the atomic level. Cell. Mol. Life Sci., 2019, 76(15), 2917-2932.
[] [PMID: 31123777]
Zhang, X.; Cheng, X. Structure of the predominant protein arginine methyltransferase PRMT1 and analysis of its binding to substrate peptides. Structure, 2003, 11(5), 509-520.
[] [PMID: 12737817]
Cura, V.; Marechal, N.; Troffer-Charlier, N.; Strub, J-M.; van Haren, M.J.; Martin, N.I.; Cianférani, S.; Bonnefond, L.; Cavarelli, J. Structural studies of protein arginine methyltransferase 2 reveal its interactions with potential substrates and inhibitors. FEBS J., 2017, 284(1), 77-96.
[] [PMID: 27879050]
Zhang, X.; Zhou, L.; Cheng, X. Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J., 2000, 19(14), 3509-3519.
[] [PMID: 10899106]
Troffer-Charlier, N.; Cura, V.; Hassenboehler, P.; Moras, D.; Cavarelli, J. Functional insights from structures of coactivator-associated arginine methyltransferase 1 domains. EMBO J., 2007, 26(20), 4391-4401.
[] [PMID: 17882262]
Bonnefond, L.; Stojko, J.; Mailliot, J.; Troffer-Charlier, N.; Cura, V.; Wurtz, J-M.; Cianférani, S.; Cavarelli, J. Functional insights from high resolution structures of mouse protein arginine methyltransferase 6. J. Struct. Biol., 2015, 191(2), 175-183.
[] [PMID: 26094878]
Mitchell, L.H.; Drew, A.E.; Ribich, S.A.; Rioux, N.; Swinger, K.K.; Jacques, S.L.; Lingaraj, T.; Boriack-Sjodin, P.A.; Waters, N.J.; Wigle, T.J.; Moradei, O.; Jin, L.; Riera, T.; Porter-Scott, M.; Moyer, M.P.; Smith, J.J.; Chesworth, R.; Copeland, R.A. Aryl Pyrazoles as Potent Inhibitors of Arginine Methyltransferases: Identification of the First PRMT6 Tool Compound. ACS Med. Chem. Lett., 2015, 6(6), 655-659.
[] [PMID: 26101569]
Lee, W.C.; Lin, W.L.; Matsui, T.; Chen, E.S.W.; Wei, T.Y.W.; Lin, W.H.; Hu, H.; Zheng, Y.G.; Tsai, M.D.; Ho, M.C. Protein Arginine Methyltransferase 8: Tetrameric Structure and Protein Substrate Specificity. Biochemistry, 2015, 54(51), 7514-7523.
[] [PMID: 26529540]
Xu, W.; Chen, H.; Du, K.; Asahara, H.; Tini, M.; Emerson, B.M.; Montminy, M.; Evans, R.M. A transcriptional switch mediated by cofactor methylation. Science, 2001, 294(5551), 2507-2511.
[] [PMID: 11701890]
Pierce, B.G.; Wiehe, K.; Hwang, H.; Kim, B-H.; Vreven, T.; Weng, Z. ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers. Bioinformatics, 2014, 30(12), 1771-1773.
[] [PMID: 24532726]
Duhovny, D.; Nussinov, R.; Wolfson, H.J. Efficient Unbound Docking of Rigid Molecules., 2002.
Schneidman-Duhovny, D.; Inbar, Y.; Nussinov, R.; Wolfson, H.J. PatchDock and SymmDock: servers for rigid and symmetric docking., 2005.
Wang, C.; Zhu, Y.; Caceres, T.B.; Liu, L.; Peng, J.; Wang, J.; Chen, J.; Chen, X.; Zhang, Z.; Zuo, X.; Gong, Q.; Teng, M.; Hevel, J.M.; Wu, J.; Shi, Y. Structural determinants for the strict monomethylation activity by trypanosoma brucei protein arginine methyltransferase 7. Structure, 2014, 22(5), 756-768.
[] [PMID: 24726341]
Boriack-Sjodin, P.A.; Jin, L.; Jacques, S.L.; Drew, A.; Sneeringer, C.; Scott, M.P.; Moyer, M.P.; Ribich, S.; Moradei, O.; Copeland, R.A. Structural Insights into Ternary Complex Formation of Human CARM1 with Various Substrates. ACS Chem. Biol., 2016, 11(3), 763-771.
[] [PMID: 26551522]
van Haren, M.J.; Marechal, N.; Troffer-Charlier, N.; Cianciulli, A.; Sbardella, G.; Cavarelli, J.; Martin, N.I. Transition state mimics are valuable mechanistic probes for structural studies with the arginine methyltransferase CARM1. Proc. Natl. Acad. Sci. USA, 2017, 114(14), 3625-3630.
[] [PMID: 28330993]
Mavrakis, K.J.; McDonald, E.R., III; Schlabach, M.R.; Billy, E.; Hoffman, G.R.; deWeck, A.; Ruddy, D.A.; Venkatesan, K.; Yu, J.; McAllister, G.; Stump, M.; deBeaumont, R.; Ho, S.; Yue, Y.; Liu, Y.; Yan-Neale, Y.; Yang, G.; Lin, F.; Yin, H.; Gao, H.; Kipp, D.R.; Zhao, S.; McNamara, J.T.; Sprague, E.R.; Zheng, B.; Lin, Y.; Cho, Y.S.; Gu, J.; Crawford, K.; Ciccone, D.; Vitari, A.C.; Lai, A.; Capka, V.; Hurov, K.; Porter, J.A.; Tallarico, J.; Mickanin, C.; Lees, E.; Pagliarini, R.; Keen, N.; Schmelzle, T.; Hofmann, F.; Stegmeier, F.; Sellers, W.R. Disordered methionine metabolism in MTAP/CDKN2A-deleted cancers leads to dependence on PRMT5. Science, 2016, 351(6278), 1208-1213.
[] [PMID: 26912361]
Feng, Y.; Xie, N.; Jin, M.; Stahley, M.R.; Stivers, J.T.; Zheng, Y.G. A transient kinetic analysis of PRMT1 catalysis. Biochemistry, 2011, 50(32), 7033-7044.
[] [PMID: 21736313]
Weiss, V.H.; McBride, A.E.; Soriano, M.A.; Filman, D.J.; Silver, P.A.; Hogle, J.M. The structure and oligomerization of the yeast arginine methyltransferase, Hmt1. Nat. Struct. Biol., 2000, 7(12), 1165-1171.
[] [PMID: 11101900]
Fedoriw, A.; Rajapurkar, S.R.; O’Brien, S.; Gerhart, S.V.; Mitchell, L.H.; Adams, N.D.; Rioux, N.; Lingaraj, T.; Ribich, S.A.; Pappalardi, M.B.; Shah, N.; Laraio, J.; Liu, Y.; Butticello, M.; Carpenter, C.L.; Creasy, C.; Korenchuk, S.; McCabe, M.T.; McHugh, C.F.; Nagarajan, R.; Wagner, C.; Zappacosta, F.; Annan, R.; Concha, N.O.; Thomas, R.A.; Hart, T.K.; Smith, J.J.; Copeland, R.A.; Moyer, M.P.; Campbell, J.; Stickland, K.; Mills, J.; Jacques-O’Hagan, S.; Allain, C.; Johnston, D.; Raimondi, A.; Porter Scott, M.; Waters, N.; Swinger, K.; Boriack-Sjodin, A.; Riera, T.; Shapiro, G.; Chesworth, R.; Prinjha, R.K.; Kruger, R.G.; Barbash, O.; Mohammad, H.P. Anti-tumor Activity of the Type I PRMT Inhibitor, GSK3368715, Synergizes with PRMT5 Inhibition through MTAP Loss. Cancer Cell, 2019, 36(1), 100-114.e25.
[] [PMID: 31257072]
Shishkova, E.; Zeng, H.; Liu, F.; Kwiecien, N.W.; Hebert, A.S.; Coon, J.J.; Xu, W. Global mapping of CARM1 substrates defines enzyme specificity and substrate recognition. Nat. Commun., 2017, 8, 15571.
[] [PMID: 28537268]
Swiercz, R.; Person, M.D.; Bedford, M.T. Ribosomal protein S2 is a substrate for mammalian PRMT3 (protein arginine methyltransferase 3). Biochem. J., 2005, 386(Pt 1), 85-91.
[] [PMID: 15473865]
Burgos, E.S.; Wilczek, C.; Onikubo, T.; Bonanno, J.B.; Jansong, J.; Reimer, U.; Shechter, D. Histone H2A and H4 N-terminal tails are positioned by the MEP50 WD repeat protein for efficient methylation by the PRMT5 arginine methyltransferase. J. Biol. Chem., 2015, 290(15), 9674-9689.
[] [PMID: 25713080]
Ho, M.C.; Wilczek, C.; Bonanno, J.B.; Xing, L.; Seznec, J.; Matsui, T.; Carter, L.G.; Onikubo, T.; Kumar, P.R.; Chan, M.K.; Brenowitz, M.; Cheng, R.H.; Reimer, U.; Almo, S.C.; Shechter, D. Structure of the arginine methyltransferase PRMT5-MEP50 reveals a mechanism for substrate specificity. PLoS One, 2013, 8(2)e57008
[] [PMID: 23451136]
Baldwin, R.M.; Morettin, A.; Côté, J. Role of PRMTs in cancer: Could minor isoforms be leaving a mark? World J. Biol. Chem., 2014, 5(2), 115-129.
Goulet, I.; Gauvin, G.; Boisvenue, S.; Côté, J. Alternative splicing yields protein arginine methyltransferase 1 isoforms with distinct activity, substrate specificity, and subcellular localization. J. Biol. Chem., 2007, 282(45), 33009-33021.
[] [PMID: 17848568]
Ivry, S.L.; Meyer, N.O.; Winter, M.B.; Bohn, M.F.; Knudsen, G.M.; O’Donoghue, A.J.; Craik, C.S. Global substrate specificity profiling of post-translational modifying enzymes. Protein Sci., 2018, 27(3), 584-594.
[] [PMID: 29168252]
Meyer, N.O.; O’Donoghue, A.J.; Schulze-Gahmen, U.; Ravalin, M.; Moss, S.M.; Winter, M.B.; Knudsen, G.M.; Craik, C.S. Multiplex Substrate Profiling by Mass Spectrometry for Kinases as a Method for Revealing Quantitative Substrate Motifs. Anal. Chem., 2017, 89(8), 4550-4558.
[] [PMID: 28322550]
Wooderchak, W.L.; Zang, T.; Zhou, Z.S.; Acuña, M.; Tahara, S.M.; Hevel, J.M. Substrate profiling of PRMT1 reveals amino acid sequences that extend beyond the “RGG” paradigm. Biochemistry, 2008, 47(36), 9456-9466.
[] [PMID: 18700728]
Kölbel, K.; Ihling, C.; Kühn, U.; Neundorf, I.; Otto, S.; Stichel, J.; Robaa, D.; Beck-Sickinger, A.G.; Sinz, A.; Wahle, E. Peptide backbone conformation affects the substrate preference of protein arginine methyltransferase I. Biochemistry, 2012, 51(27), 5463-5475.
[] [PMID: 22697391]
Nguyen, H.C.; Wang, M.; Salsburg, A.; Knuckley, B. Development of a Plate-Based Screening Assay to Investigate the Substrate Specificity of the PRMT Family of Enzymes. ACS Comb. Sci., 2015, 17(9), 500-505.
[] [PMID: 26252756]
Bicker, K.L.; Obianyo, O.; Rust, H.L.; Thompson, P.R. A combinatorial approach to characterize the substrate specificity of protein arginine methyltransferase 1. Mol. Biosyst., 2011, 7(1), 48-51.
[] [PMID: 20607165]
Hamey, J.J.; Separovich, R.J.; Wilkins, M.R. MT-MAMS: Protein Methyltransferase Motif Analysis by Mass Spectrometry. J. Proteome Res., 2018, 17(10), 3485-3491.
[] [PMID: 30156103]
Wang, M.; Xu, R-M.; Thompson, P.R. Substrate specificity, processivity, and kinetic mechanism of protein arginine methyltransferase 5. Biochemistry, 2013, 52(32), 5430-5440.
[] [PMID: 23866019]
Feng, Y.; Maity, R.; Whitelegge, J.P.; Hadjikyriacou, A.; Li, Z.; Zurita-Lopez, C.; Al-Hadid, Q.; Clark, A.T.; Bedford, M.T.; Masson, J-Y.; Clarke, S.G. Mammalian protein arginine methyltransferase 7 (PRMT7) specifically targets RXR sites in lysine- and arginine-rich regions. J. Biol. Chem., 2013, 288(52), 37010-37025.
[] [PMID: 24247247]
Cáceres, T.B.; Thakur, A.; Price, O.M.; Ippolito, N.; Li, J.; Qu, J.; Acevedo, O.; Hevel, J.M. Phe71 in Type III Trypanosomal Protein Arginine Methyltransferase 7 (TbPRMT7) Restricts the Enzyme to Monomethylation. Biochemistry, 2018, 57(8), 1349-1359.
[] [PMID: 29378138]
Hadjikyriacou, A.; Yang, Y.; Espejo, A.; Bedford, M.T.; Clarke, S.G. Unique Features of Human Protein Arginine Methyltransferase 9 (PRMT9) and Its Substrate RNA Splicing Factor SF3B2. J. Biol. Chem., 2015, 290(27), 16723-16743.
[] [PMID: 25979344]
Osborne, T.C.; Obianyo, O.; Zhang, X.; Cheng, X.; Thompson, P.R. Protein arginine methyltransferase 1: positively charged residues in substrate peptides distal to the site of methylation are important for substrate binding and catalysis. Biochemistry, 2007, 46(46), 13370-13381.
[] [PMID: 17960915]
Yamagata, K.; Daitoku, H.; Takahashi, Y.; Namiki, K.; Hisatake, K.; Kako, K.; Mukai, H.; Kasuya, Y.; Fukamizu, A. Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol. Cell, 2008, 32(2), 221-231.
[] [PMID: 18951090]
Sakamaki, J.; Daitoku, H.; Ueno, K.; Hagiwara, A.; Yamagata, K.; Fukamizu, A. Arginine methylation of BCL-2 antagonist of cell death (BAD) counteracts its phosphorylation and inactivation by Akt. Proc. Natl. Acad. Sci. USA, 2011, 108(15), 6085-6090.
[] [PMID: 21444773]
Rust, H.L.; Thompson, P.R. Kinase consensus sequences: a breeding ground for crosstalk. ACS Chem. Biol., 2011, 6(9), 881-892.
[] [PMID: 21721511]
Scaramuzzino, C.; Casci, I.; Parodi, S.; Lievens, P.M.J.; Polanco, M.J.; Milioto, C.; Chivet, M.; Monaghan, J.; Mishra, A.; Badders, N.; Aggarwal, T.; Grunseich, C.; Sambataro, F.; Basso, M.; Fackelmayer, F.O.; Taylor, J.P.; Pandey, U.B.; Pennuto, M. Protein arginine methyltransferase 6 enhances polyglutamine-expanded androgen receptor function and toxicity in spinal and bulbar muscular atrophy. Neuron, 2015, 85(1), 88-100.
[] [PMID: 25569348]
Deen, J.; Vranken, C.; Leen, V.; Neely, R.K.; Janssen, K.P.F.; Hofkens, J. Methyltransferase-Directed Labeling of Biomolecules and its Applications. Angew. Chem. Int. Ed. Engl., 2017, 56(19), 5182-5200.
[] [PMID: 27943567]
Catcott, K.C.; Yan, J.; Qu, W.; Wysocki, V.H.; Zhou, Z.S. Identifying Unknown Enzyme-Substrate Pairs from the Cellular Milieu with Native Mass Spectrometry. ChemBioChem, 2017, 18(7), 613-617.
[] [PMID: 28140508]
Wang, R.; Zheng, W.; Yu, H.; Deng, H.; Luo, M. Labeling substrates of protein arginine methyltransferase with engineered enzymes and matched S-adenosyl-L-methionine analogues. J. Am. Chem. Soc., 2011, 133(20), 7648-7651.
[] [PMID: 21539310]
Shimazu, T.; Barjau, J.; Sohtome, Y.; Sodeoka, M.; Shinkai, Y. Selenium-based S-adenosylmethionine analog reveals the mammalian seven-beta-strand methyltransferase METTL10 to be an EF1A1 lysine methyltransferase. PLoS One, 2014, 9(8)e105394
[] [PMID: 25144183]
Guo, H.; Wang, R.; Zheng, W.; Chen, Y.; Blum, G.; Deng, H.; Luo, M. Profiling substrates of protein arginine N-methyltransferase 3 with S-adenosyl-L-methionine analogues. ACS Chem. Biol., 2014, 9(2), 476-484.
[] [PMID: 24320160]
Hymbaugh Bergman, S.J.; Comstock, L.R. N-mustard analogs of S-adenosyl-L-methionine as biochemical probes of protein arginine methylation. Bioorg. Med. Chem., 2015, 23(15), 5050-5055.
[] [PMID: 26037613]
Hoegl, A.; Nodwell, M.B.; Kirsch, V.C.; Bach, N.C.; Pfanzelt, M.; Stahl, M.; Schneider, S.; Sieber, S.A. Mining the cellular inventory of pyridoxal phosphate-dependent enzymes with functionalized cofactor mimics. Nat. Chem., 2018, 10(12), 1234-1245.
[] [PMID: 30297752]
Evich, M.; Stroeva, E.; Zheng, Y.G.; Germann, M.W. Effect of methylation on the side-chain pKa value of arginine. Protein Sci., 2016, 25(2), 479-486.
[] [PMID: 26540340]
Boisvert, F-M.; Côté, J.; Boulanger, M-C.; Richard, S. A proteomic analysis of arginine-methylated protein complexes. Mol. Cell. Proteomics, 2003, 2(12), 1319-1330.
[] [PMID: 14534352]
Ong, S-E.; Mittler, G.; Mann, M. Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat. Methods, 2004, 1(2), 119-126.
[] [PMID: 15782174]
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.; Comb, M.J. Immunoaffinity enrichment and mass spectrometry analysis of protein methylation. Mol. Cell. Proteomics, 2014, 13(1), 372-387.
[] [PMID: 24129315]
Geoghegan, V.; Guo, A.; Trudgian, D.; Thomas, B.; Acuto, O. Comprehensive identification of arginine methylation in primary T cells reveals regulatory roles in cell signalling. Nat. Commun., 2015, 6, 6758.
[] [PMID: 25849564]
Musiani, D.; Bok, J.; Massignani, E.; Wu, L.; Tabaglio, T.; Ippolito, M.R.; Cuomo, A.; Ozbek, U.; Zorgati, H.; Ghoshdastider, U.; Robinson, R.C.; Guccione, E.; Bonaldi, T. Proteomics profiling of arginine methylation defines PRMT5 substrate specificity. Sci. Signal., 2019, 12(575)eaat8388
[] [PMID: 30940768]
Cheng, D.; Côté, J.; Shaaban, S.; Bedford, M.T. The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol. Cell, 2007, 25(1), 71-83.
[] [PMID: 17218272]
Pei, J.; Kim, B-H.; Grishin, N.V. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res., 2008, 36(7), 2295-2300.
[] [PMID: 18287115]
Drozdetskiy, A.; Cole, C.; Procter, J.; Barton, G.J. JPred4: a protein secondary structure prediction server. Nucleic Acids Res., 2015, 43(W1)W389-94
[] [PMID: 25883141]
Reidt, U.; Wahl, M.C.; Fasshauer, D.; Horowitz, D.S.; Lührmann, R.; Ficner, R. Crystal structure of a complex between human spliceosomal cyclophilin H and a U4/U6 snRNP-60K peptide. J. Mol. Biol., 2003, 331(1), 45-56.
[] [PMID: 12875835]
Vitali, J.; Ding, J.; Jiang, J.; Zhang, Y.; Krainer, A.R.; Xu, R-M. Correlated alternative side chain conformations in the RNA-recognition motif of heterogeneous nuclear ribonucleoprotein A1. Nucleic Acids Res., 2002, 30(7), 1531-1538.
[] [PMID: 11917013]
Hsu, M-C.; Tsai, Y-L.; Lin, C-H.; Pan, M-R.; Shan, Y-S.; Cheng, T-Y.; Cheng, S.H-C.; Chen, L-T.; Hung, W-C. Protein arginine methyltransferase 3-induced metabolic reprogramming is a vulnerable target of pancreatic cancer. J. Hematol. Oncol., 2019, 12(1), 79.
[] [PMID: 31324208]
Hsu, M-C.; Pan, M-R.; Chu, P-Y.; Tsai, Y-L.; Tsai, C-H.; Shan, Y-S.; Chen, L-T.; Hung, W-C. Protein Arginine Methyltransferase 3 Enhances Chemoresistance in Pancreatic Cancer by Methylating hnRNPA1 to Increase ABCG2 Expression. Cancers (Basel), 2018, 11(1)E8
[] [PMID: 30577570]
Frankel, A.; Yadav, N.; Lee, J.; Branscombe, T.L.; Clarke, S.; Bedford, M.T. The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J. Biol. Chem., 2002, 277(5), 3537-3543.
[] [PMID: 11724789]
Chan, L.H.; Zhou, L.; Ng, K.Y.; Wong, T.L.; Lee, T.K.; Sharma, R.; Loong, J.H.; Ching, Y.P.; Yuan, Y-F.; Xie, D.; Lo, C.M.; Man, K.; Artegiani, B.; Clevers, H.; Yan, H.H.; Leung, S.Y.; Richard, S.; Guan, X-Y.; Huen, M.S.Y.; Ma, S. PRMT6 Regulates RAS/RAF Binding and MEK/ERK-Mediated Cancer Stemness Activities in Hepatocellular Carcinoma through CRAF Methylation. Cell Rep., 2018, 25(3), 690-701.e8.
[] [PMID: 30332648]
Feng, Y.; Hadjikyriacou, A.; Clarke, S.G. Substrate specificity of human protein arginine methyltransferase 7 (PRMT7): the importance of acidic residues in the double E loop. J. Biol. Chem., 2014, 289(47), 32604-32616.
[] [PMID: 25294873]

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Article Details

Year: 2020
Page: [713 - 724]
Pages: 12
DOI: 10.2174/1389203721666200124143145
Price: $65

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