Structural determinants for the strict monomethylation activity by trypanosoma brucei protein arginine methyltransferase 7

Structure

Volumn 22, Issue 5, 2014, Pages 756-768

  Wang, Chongyuan ^a   Zhu, Yuwei ^a   Caceres, Tamar B ^b   Liu, Lei ^a   Peng, Junhui ^a   Wang, Junchen ^a   Chen, Jiajing ^a   Chen, Xuwen ^a   Zhang, Zhiyong ^a   Zuo, Xiaobing ^c   Gong, Qingguo ^a   Teng, Maikun ^a   Hevel, Joan M ^b   Wu, Jihui ^a   Shi, Yunyu ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UTAH STATE UNIVERSITY   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H4; N(G),N(G) DIMETHYLARGININE; PROTEIN ARGININE METHYLTRANSFERASE; S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE; TRYPANOSOMA BRUCEI PROTEIN ARGININE METHYLTRANSTYPE FERASE 7; UNCLASSIFIED DRUG; ARGININE; GUANIDINE; HISTONE; N,N'-DIMETHYLARGININE; N,N-DIMETHYLARGININE; PROTOZOAL PROTEIN;

ARTICLE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ISOTHERMAL TITRATION CALORIMETRY; METHYLATION; NONHUMAN; NUCLEOPHILICITY; PRIORITY JOURNAL; TRYPANOSOMA BRUCEI; TURNOVER TIME; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; TRYPANOSOMA BRUCEI BRUCEI; X RAY CRYSTALLOGRAPHY;

TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ARGININE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GUANIDINE; HISTONES; METHYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN-ARGININE N-METHYLTRANSFERASES; PROTOZOAN PROTEINS; S-ADENOSYLHOMOCYSTEINE; S-ADENOSYLMETHIONINE; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84899984348     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.03.003     Document Type: Article

References (46)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. S. Antonysamy, Z. Bonday, R.M. Campbell, B. Doyle, Z. Druzina, T. Gheyi, B. Han, L.N. Jungheim, Y. Qian, and C. Rauch et al. Crystal structure of the human PRMT5:MEP50 complex Proc. Natl. Acad. Sci. USA 109 2012 17960 17965
3. M.T. Bedford, and S.G. Clarke Protein arginine methylation in mammals: who, what, and why Mol. Cell 33 2009 1 13
4. M.T. Bedford, and S. Richard Arginine methylation an emerging regulator of protein function Mol. Cell 18 2005 263 272
5. Y. Cheng, M. Frazier, F. Lu, X. Cao, and M.R. Redinbo Crystal structure of the plant epigenetic protein arginine methyltransferase 10 J. Mol. Biol. 414 2011 106 122
6. I.W. Davis, A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, X. Wang, L.W. Murray, W.B. Arendall 3rd, J. Snoeyink, J.S. Richardson, and D.C. Richardson MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 Web Server issue 2007 W375 W383
7. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA
8. S.S. Dhar, S.H. Lee, P.Y. Kan, P. Voigt, L. Ma, X. Shi, D. Reinberg, and M.G. Lee Trans-tail regulation of MLL4-catalyzed H3K4 methylation by H4R3 symmetric dimethylation is mediated by a tandem PHD of MLL4 Genes Dev. 26 2012 2749 2762
9. A. Di Lorenzo, and M.T. Bedford Histone arginine methylation FEBS Lett. 585 2011 2024 2031
10. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
11. Y. Feng, R. Maity, J.P. Whitelegge, A. Hadjikyriacou, Z. Li, C. Zurita-Lopez, Q. Al-Hadid, A.T. Clark, M.T. Bedford, J.Y. Masson, and S.G. Clarke Mammalian protein arginine methyltransferase 7 (PRMT7) specifically targets RXR sites in lysine- and arginine-rich regions J. Biol. Chem. 288 2013 37010 37025
12. H. Fischer, M.D. Neto, H.B. Napolitano, I. Polikarpov, and A.F. Craievich Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale J. Appl. Crystallogr. 43 2010 101 109
13. J.C. Fisk, J. Sayegh, C. Zurita-Lopez, S. Menon, V. Presnyak, S.G. Clarke, and L.K. Read A type III protein arginine methyltransferase from the protozoan parasite Trypanosoma brucei J. Biol. Chem. 284 2009 11590 11600
14. G.B. Gonsalvez, L. Tian, J.K. Ospina, F.M. Boisvert, A.I. Lamond, and A.G. Matera Two distinct arginine methyltransferases are required for biogenesis of Sm-class ribonucleoproteins J. Cell Biol. 178 2007 733 740
15. E. Guccione, C. Bassi, F. Casadio, F. Martinato, M. Cesaroni, H. Schuchlautz, B. Lüscher, and B. Amati Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive Nature 449 2007 933 937
16. M.C. Ho, C. Wilczek, J.B. Bonanno, L. Xing, J. Seznec, T. Matsui, L.G. Carter, T. Onikubo, P.R. Kumar, and M.K. Chan et al. Structure of the arginine methyltransferase PRMT5-MEP50 reveals a mechanism for substrate specificity PLoS One 8 e57008 2013
17. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
18. A.N. Iberg, A. Espejo, D.H. Cheng, D. Kim, J. Michaud-Levesque, S. Richard, and M.T. Bedford Arginine methylation of the histone H3 tail impedes effector binding J. Biol. Chem. 283 2008 3006 3010
19. P. Jelinic, J.C. Stehle, and P. Shaw The testis-specific factor CTCFL cooperates with the protein methyltransferase PRMT7 in H19 imprinting control region methylation PLoS Biol. 4 2006 e355
20. V. Karkhanis, L. Wang, S. Tae, Y.J. Hu, A.N. Imbalzano, and S. Sif Protein arginine methyltransferase 7 regulates cellular response to DNA damage by methylating promoter histones H2A and H4 of the polymerase δ catalytic subunit gene, POLD1 J. Biol. Chem. 287 2012 29801 29814
21. A. Kirmizis, H. Santos-Rosa, C.J. Penkett, M.A. Singer, R.D. Green, and T. Kouzarides Distinct transcriptional outputs associated with mono- and dimethylated histone H3 arginine 2 Nat. Struct. Mol. Biol. 16 2009 449 451
22. P.V. Konarev, V.V. Volkov, A.V. Sokolova, M.H.J. Koch, and D.I. Svergun PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36 2003 1277 1282
23. P.V. Konarev, M.V. Petoukhov, V.V. Volkov, and D.I. Svergun ATSAS 2.1, a program package for small-angle scattering data analysis J. Appl. Crystallogr. 39 2006 277 286
24. M.B. Kozin, and D.I. Svergun Automated matching of high- and low-resolution structural models J. Appl. Crystallogr. 34 2001 33 41
25. R.A. Laskowski, M.W. Macarthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
26. J.H. Lee, J.R. Cook, Z.H. Yang, O. Mirochnitchenko, S.I. Gunderson, A.M. Felix, N. Herth, R. Hoffmann, and S. Pestka PRMT7, a new protein arginine methyltransferase that synthesizes symmetric dimethylarginine J. Biol. Chem. 280 2005 3656 3664
27. V. Migliori, J. Müller, S. Phalke, D. Low, M. Bezzi, W.C. Mok, S.K. Sahu, J. Gunaratne, P. Capasso, and C. Bassi et al. Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance Nat. Struct. Mol. Biol. 19 2012 136 144
28. T.B. Miranda, M. Miranda, A. Frankel, and S.G. Clarke PRMT7 is a member of the protein arginine methyltransferase family with a distinct substrate specificity J. Biol. Chem. 279 2004 22902 22907
29. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
30. K. Nishioka, and D. Reinberg Methods and tips for the purification of human histone methyltransferases Methods 31 2003 49 58
31. H.L. Rust, C.I. Zurita-Lopez, S. Clarke, and P.R. Thompson Mechanistic studies on transcriptional coactivator protein arginine methyltransferase 1 Biochemistry 50 2011 3332 3345
32. A.V. Semenyuk, and D.I. Svergun GNOM-a program package for small-angle scattering data-processing J. Appl. Crystallogr. 24 1991 537 540
33. B.B. Suh-Lailam, and J.M. Hevel A fast and efficient method for quantitative measurement of S-adenosyl-L-methionine-dependent methyltransferase activity with protein substrates Anal. Biochem. 398 2010 218 224
34. L. Sun, M. Wang, Z. Lv, N. Yang, Y. Liu, S. Bao, W. Gong, and R.M. Xu Structural insights into protein arginine symmetric dimethylation by PRMT5 Proc. Natl. Acad. Sci. USA 108 2011 20538 20543
35. D.I. Svergun, M.V. Petoukhov, and M.H.J. Koch Determination of domain structure of proteins from X-ray solution scattering Biophys. J. 80 2001 2946 2953
36. N. Troffer-Charlier, V. Cura, P. Hassenboehler, D. Moras, and J. Cavarelli Functional insights from structures of coactivator-associated arginine methyltransferase 1 domains EMBO J. 26 2007 4391 4401
37. A. Vagin, and A. Teplyakov Molecular replacement with MOLREP Acta Crystallogr. D Biol. Crystallogr. 66 2010 22 25
38. C. Wang, Y. Zhu, J. Chen, X. Li, J. Peng, J. Chen, Y. Zou, Z. Zhang, H. Jin, and P. Yang et al. Crystal structure of arginine methyltransferase 6 from Trypanosoma brucei PLoS One 9 2014 e87267
39. V.H. Weiss, A.E. McBride, M.A. Soriano, D.J. Filman, P.A. Silver, and J.M. Hogle The structure and oligomerization of the yeast arginine methyltransferase, Hmt1 Nat. Struct. Biol. 7 2000 1165 1171
40. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, and A. McCoy et al. Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
41. X. Xu, S. Hoang, M.W. Mayo, and S. Bekiranov Application of machine learning methods to histone methylation ChIP-Seq data reveals H4R3me2 globally represses gene expression BMC Bioinformatics 11 2010 396
42. Y. Yang, and M.T. Bedford Protein arginine methyltransferases and cancer Nat. Rev. Cancer 13 2013 37 50
43. W.W. Yue, M. Hassler, S.M. Roe, V. Thompson-Vale, and L.H. Pearl Insights into histone code syntax from structural and biochemical studies of CARM1 methyltransferase EMBO J. 26 2007 4402 4412
44. X. Zhang, and X.D. Cheng Structure of the predominant protein arginine methyltransferase PRMT1 and analysis of its binding to substrate peptides Structure 11 2003 509 520
45. X. Zhang, L. Zhou, and X.D. Cheng Crystal structure of the conserved core of protein arginine methyltransferase PRMT3 EMBO J. 19 2000 3509 3519
46. G-monomethylated arginine residues J. Biol. Chem. 287 2012 7859 7870