Crystal structure of the plant epigenetic protein arginine methyltransferase 10

Journal of Molecular Biology

Volumn 414, Issue 1, 2011, Pages 106-122

  Cheng, Yuan ^a,b,f   Frazier, Monica ^a,b   Lu, Falong ^c,d   Cao, Xiaofeng ^c   Redinbo, Matthew R ^a,b,e  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^e University of North Carolina at Chapel Hill   (United States)

^f UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Arabidopsis; epigenetics; flowering time; protein motion; protein structure

Indexed keywords

METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 10; S ADENOSYLHOMOCYSTEINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DIMERIZATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; EPIGENETICS; FLOWERING; METHYLATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 81055156654     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.09.040     Document Type: Article

References (51)

1. Bedford M.T., and Clarke S.G. Protein arginine methylation in mammals: who, what, and why Mol. Cell 33 2009 1 13
2. Sanchez S.E., Petrillo E., Beckwith E.J., Zhang X., Rugnone M.L., and Hernando C.E. A methyl transferase links the circadian clock to the regulation of alternative splicing Nature 468 2010 112 116
3. Stallcup M.R. Role of protein methylation in chromatin remodeling and transcriptional regulation Oncogene 20 2001 3014 3020 (Pubitemid 32553555)
4. Bedford M.T. Arginine methylation at a glance J. Cell Sci. 120 2007 4243 4246
5. Lake A.N., and Bedford M.T. Protein methylation and DNA repair Mutat. Res. 618 2007 91 101 (Pubitemid 46574739)
6. Smith B.C., and Denu J.M. Chemical mechanisms of histone lysine and arginine modifications Biochim. Biophys. Acta 1789 2009 45 57
7. Liu C., Lu F., Cui X., and Cao X. Histone methylation in higher plants Annu. Rev. Plant Biol. 61 2010 395 420
8. Deng X., Gu L., Liu C., Lu T., Lu F., and Lu Z. Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing Proc. Natl Acad. Sci. USA 107 2010 19114 19119
9. Wolf S.S. The protein arginine methyltransferase family: an update about function, new perspectives and the physiological role in humans Cell Mol. Life Sci. 66 2009 2109 2121
10. Teyssier C., Le Romancer M., Sentis S., Jalaguier S., Corbo L., and Cavailles V. Protein arginine methylation in estrogen signaling and estrogen-related cancers Trends Endocrinol. Metab. 21 2009 181 189
11. Aletta J.M., and Hu J.C. Protein arginine methylation in health and disease Biotechnol. Annu. Rev. 14 2008 203 224 (Pubitemid 351903455)
12. Boger R.H., Cooke J.P., and Vallance P. ADMA: an emerging cardiovascular risk factor Vasc. Med. 10 2005 S1 S2
13. Ueda S., Yamagishi S., Matsumoto Y., Fukami K., and Okuda S. Asymmetric dimethylarginine (ADMA) is a novel emerging risk factor for cardiovascular disease and the development of renal injury in chronic kidney disease Clin. Exp. Nephrol. 11 2007 115 121 (Pubitemid 47012517)
14. Pullamsetti S., Kiss L., Ghofrani H.A., Voswinckel R., Haredza P., and Klepetko W. Increased levels and reduced catabolism of asymmetric and symmetric dimethylarginines in pulmonary hypertension FASEB J. 19 2005 1175 1177 (Pubitemid 40946456)
15. Bedford M.T., and Richard S. Arginine methylation an emerging regulator of protein function Mol. Cell 18 2005 263 272 (Pubitemid 41350532)
16. Lin C.H., Hsieh M., Li Y.C., Li S.Y., Pearson D.L., Pollard K.M., and Li C. Protein N-arginine methylation in subcellular fractions of lymphoblastoid cells J. Biochem. 128 2000 493 498
17. Frankel A., and Clarke S. PRMT3 is a distinct member of the protein arginine N-methyltransferase family. Conferral of substrate specificity by a zinc-finger domain J. Biol. Chem. 275 2000 32974 32982
18. Weiss V.H., McBride A.E., Soriano M.A., Filman D.J., Silver P.A., and Hogle J.M. The structure and oligomerization of the yeast arginine methyltransferase, Hmt1 Nat. Struct. Biol. 7 2000 1165 1171
19. Zhang X., and Cheng X. Structure of the predominant protein arginine methyltransferase PRMT1 and analysis of its binding to substrate peptides Structure 11 2003 509 520 (Pubitemid 36579129)
20. Zhang X., Zhou L., and Cheng X. Crystal structure of the conserved core of protein arginine methyltransferase PRMT3 EMBO J. 19 2000 3509 3519 (Pubitemid 30462110)
21. Cheng X., Collins R.E., and Zhang X. Structural and sequence motifs of protein (histone) methylation enzymes Annu. Rev. Biophys. Biomol. Struct. 34 2005 267 294 (Pubitemid 40847726)
22. Troffer-Charlier N., Cura V., Hassenboehler P., Moras D., and Cavarelli J. Functional insights from structures of coactivator-associated arginine methyltransferase 1 domains EMBO J. 26 2007 4391 4401 (Pubitemid 47587658)
23. Yue W.W., Hassler M., Roe S.M., Thompson-Vale V., and Pearl L.H. Insights into histone code syntax from structural and biochemical studies of CARM1 methyltransferase EMBO J. 26 2007 4402 4412 (Pubitemid 47587659)
24. Kim S., Merrill B.M., Rajpurohit R., Kumar A., Stone K.L., and Papov V.V. Identification of N(G)-methylarginine residues in human heterogeneous RNP protein A1: Phe/Gly-Gly-Gly-Arg-Gly-Gly-Gly/Phe is a preferred recognition motif Biochemistry 36 1997 5185 5192 (Pubitemid 27199735)
25. Wooderchak W.L., Zang T., Zhou Z.S., Acuna M., Tahara S.M., and Hevel J.M. Substrate profiling of PRMT1 reveals amino acid sequences that extend beyond the "RGG" paradigm Biochemistry 47 2008 9456 9466
26. Gary J.D., and Clarke S. RNA and protein interactions modulated by protein arginine methylation Prog. Nucleic Acid Res. Mol. Biol. 61 1998 65 131
27. Osborne T.C., Obianyo O., Zhang X., Cheng X., and 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 46 2007 13370 13381 (Pubitemid 350136376)
28. Lin W.J., Gary J.D., Yang M.C., Clarke S., and Herschman H.R. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase J. Biol. Chem. 271 1996 15034 15044 (Pubitemid 26197578)
29. Singh V., Miranda T.B., Jiang W., Frankel A., Roemer M.E., and Robb V.A. DAL-1/4.1B tumor suppressor interacts with protein arginine N-methyltransferase 3 (PRMT3) and inhibits its ability to methylate substrates in vitro and in vivo Oncogene 23 2004 7761 7771 (Pubitemid 39457026)
30. Pal S., Vishwanath S.N., Erdjument-Bromage H., Tempst P., and Sif S. Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes Mol. Cell. Biol. 24 2004 9630 9645 (Pubitemid 39391698)
31. Xu W., Cho H., Kadam S., Banayo E.M., Anderson S., and Yates J.R. III A methylation-mediator complex in hormone signaling Genes Dev. 18 2004 144 156 (Pubitemid 38141783)
32. Niu L., Lu F., Pei Y., Liu C., and Cao X. Regulation of flowering time by the protein arginine methyltransferase AtPRMT10 EMBO Rep. 8 2007 1190 1195 (Pubitemid 350201739)
33. Fauman E.B., Blumenthal R.M., and Cheng X. Structure and evolution of AdoMet-dependent methyltransferase X Cheng, R.M. Blumenthal, S-Adenosylmethionine-Dependent Methyltransferase: Structures and Functions 1999 World Scientific, Inc. Singapore
34. Cheng X., and Roberts R.J. AdoMet-dependent methylation, DNA methyltransferases and base flipping Nucleic Acids Res. 29 2001 3784 3795 (Pubitemid 32910519)
35. Lee D.Y., Ianculescu I., Purcell D., Zhang X., Cheng X., and Stallcup M.R. Surface-scanning mutational analysis of protein arginine methyltransferase 1: roles of specific amino acids in methyltransferase substrate specificity, oligomerization, and coactivator function Mol. Endocrinol. 21 2007 1381 1393 (Pubitemid 46984744)
36. Smith J.J., Rucknagel K.P., Schierhorn A., Tang J., Nemeth A., and Linder M. Unusual sites of arginine methylation in poly(A)-binding protein II and in vitro methylation by protein arginine methyltransferases PRMT1 and PRMT3 J. Biol. Chem. 274 1999 13229 13234
37. Teotico D.G., Frazier M.L., Ding F., Dokholyan N.V., Temple B.R., and Redinbo M.R. Active nuclear receptors exhibit highly correlated AF-2 domain motions PLoS Comput. Biol. 4 2008 e1000111
38. Goulet I., Gauvin G., Boisvenue S., and Cote J. Alternative splicing yields protein arginine methyltransferase 1 isoforms with distinct activity, substrate specificity, and subcellular localization J. Biol. Chem. 282 2007 33009 33021 (Pubitemid 350159275)
39. Tang J., Gary J.D., Clarke S., and Herschman H.R. PRMT 3, a type I protein arginine N-methyltransferase that differs from PRMT1 in its oligomerization, subcellular localization, substrate specificity, and regulation J. Biol. Chem. 273 1998 16935 16945 (Pubitemid 28311725)
40. Pawlak M.R., Banik-Maiti S., Pietenpol J.A., and Ruley H.E. Protein arginine methyltransferase I: substrate specificity and role in hnRNP assembly J. Cell. Biochem. 87 2002 394 407 (Pubitemid 35231703)
41. Stols L., Gu M., Dieckman L., Raffen R., Collart F.R., and Donnelly M.I. A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site Protein Expression Purif. 25 2002 8 15 (Pubitemid 36034995)
42. Cheng Y., McNamara D.E., Miley M.J., Nash R.P., and Redinbo M.R. Functional characterization of the multi-domain F plasmid TraI relaxase-helicase J. Biol. Chem. 286 2011 12670 12682
43. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode C.W. Cater Jr. R.M. Sweet, Methods in Enzymology 276 1997 Academic Press New York, NY 307 326 (Pubitemid 27085611)
44. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., and Echols N. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 213 221
45. Collabroative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
46. Emsley P., Lohkamp B., Scott W.G., and Cowtan K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501
47. Duan Y., Wu C., Chowdhury S., Lee M.C., Xiong G., and Zhang W. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 24 2003 1999 2012
48. Case D.A., Darden T.A., Cheatham T.E.I., Simmerling C.L., and Wang J. AMBER 9 2006 University of California San Francisco, CA
49. Essman U., Perera L., Berkowita M.L., Darden T.A., and Lee H. A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
50. Sharma S., Ding F., and Dokholyan N.V. Multiscale modeling of nucleosome dynamics Biophys. J. 92 2007 1457 1470 (Pubitemid 46393459)
51. Everitt B.S., Landau S., and Leese M. Cluster Analysis 2001 Oxford University Press Oxford, UK