Crystal Structure of the Human tRNA m1A58 Methyltransferase-tRNA3Lys Complex: Refolding of Substrate tRNA Allows Access to the Methylation Target

Journal of Molecular Biology

Volumn 427, Issue 24, 2015, Pages 3862-3876

  Finer Moore, Janet ^a   Czudnochowski, Nadine ^a   O'Connell, Joseph D ^a   Wang, Amy Liya ^a   Stroud, Robert M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

1 methyladenosine; HIV; RNA modification; S adenosyl l methionine; X ray

Indexed keywords

1 METHYLADENOSINE 58 METHYTRANSFERASE; ADENOSYLHOMOCYSTEINASE; DIMER; HETERODIMER; LYSINE; METHYLTRANSFERASE; PRIMER RNA; S ADENOSYLMETHIONINE; TETRAMER; TRANSFER RNA; UNCLASSIFIED DRUG; PROTEIN BINDING; TRANSFER RNA METHYLTRANSFERASE; TRM61 PROTEIN, HUMAN;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; HYDROGEN BOND; PRIORITY JOURNAL; RNA BINDING; RNA FOLDING; RNA METHYLATION; RNA STABILITY; RNA STRUCTURE; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE; CHEMISTRY; HUMAN; METHYLATION; MOLECULAR MODEL; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROGEN BONDING; METHYLATION; MODELS, MOLECULAR; PROTEIN BINDING; RNA FOLDING; RNA, TRANSFER; TRNA METHYLTRANSFERASES;

EID: 84948654550     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.10.005     Document Type: Article

References (44)

1. Met in S. cerevisiae Genes Dev. 18 2004 1227 1240
2. R. Marquet, C. Isel, C. Ehresmann, and B. Ehresmann tRNAs as primer of reverse transcriptases Biochimie 77 1995 113 124
3. M.J. Renda, B. Bradel-Tretheway, V. Planelles, R.A. Bambara, and S. Dewhurst Inhibition of HIV type 1 replication using lentiviral-mediated delivery of mutant tRNA(Lys3)A58U AIDS Res. Hum. Retrovir. 20 2004 1324 1334
4. W. Yu, A. McCulley, and C.D. Morrow Mutations in the TPsiC loop of E. coli tRNALys,3 have varied effects on in trans complementation of HIV-1 replication Virol. J. 4 2007 5
5. 1A58 methyltransferase from S. cerevisiae is conserved in humans RNA 11 2005 1281 1290
6. 1A58 methyltransferase and biophysical characterization of its interaction with tRNA J. Mol. Biol. 377 2008 535 550
7. A. Gupta, P.H. Kumar, T.K. Dineshkumar, U. Varshney, and H.S. Subramanya Crystal structure of Rv2118c: An AdoMet-dependent methyltransferase from Mycobacterium tuberculosis H37Rv J. Mol. Biol. 312 2001 381 391
8. 1A57/58 methyltransferase Nucleic Acids Res. 38 2010 6206 6218
9. M. Kuratani, T. Yanagisawa, R. Ishii, M. Matsuno, S.Y. Si, K. Katsura, R. Ushikoshi-Nakayama, R. Shibata, M. Shirouzu, Y. Bessho, and S. Yokoyama Crystal structure of tRNA m(1)A58 methyltransferase TrmI from Aquifex aeolicus in complex with S-adenosyl-l-methionine J. Struct. Funct. Genom. 15 2014 173 180
10. 1A58) methyltransferase (TrmI) J. Biol. Chem. 290 2015 5912 5925
11. J.D. Robertus, J.E. Ladner, J.T. Finch, D. Rhodes, R.S. Brown, B.F. Clark, and A. Klug Structure of yeast phenylalanine tRNA at 3 Å resolution Nature 250 1974 546 551
12. R. Ishitani, O. Nureki, N. Nameki, N. Okada, S. Nishimura, and S. Yokoyama Alternative tertiary structure of tRNA for recognition by a posttranscriptional modification enzyme Cell 113 2003 383 394
13. 1A58 methyltransferase family: Homology-based fold prediction and identification of new members from Eubacteria and Archaea FEBS Lett. 507 2001 123 127
14. J.L. Chambers, and R.M. Stroud Difference Fourier refinement of the structure of DIP-trypsin at 1.5 Å with a minicomputer technique Acta Crystallogr., Sect. B: Struct. Sci., Cryst. Eng. Mater. 33 1977 1824 1837
15. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
16. 1A58 MTase from Saccharomyces cerevisiae contribute to tRNA binding Nucleic Acids Res. 35 2007 6808 6819
17. R. Mosca, B. Brannetti, and T.R. Schneider Alignment of protein structures in the presence of domain motions BMC Bioinf. 9 2008 352
18. R. Mosca, and T.R. Schneider RAPIDO: A Web server for the alignment of protein structures in the presence of conformational changes Nucleic Acids Res. 36 2008 W42 W46
19. T. Malone, R.M. Blumenthal, and X. Cheng Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes J. Mol. Biol. 253 1995 618 632
20. G. Schluckebier, M. O'Gara, W. Saenger, and X. Cheng Universal catalytic domain structure of AdoMet-dependent methyltransferases J. Mol. Biol. 247 1995 16 20
21. S.H. Kim, G.J. Quigley, F.L. Suddath, A. McPherson, D. Sneden, J.J. Kim, J. Weinzierl, and A. Rich Three-dimensional structure of yeast phenylalanine transfer RNA: Folding of the polynucleotide chain Science 179 1973 285 288
22. F. Juhling, M. Morl, R.K. Hartmann, M. Sprinzl, P.F. Stadler, and J. Putz tRNAdb 2009: Compilation of tRNA sequences and tRNA genes Nucleic Acids Res. 37 2009 D159 D162
23. M. Saikia, Y. Fu, M. Pavon-Eternod, C. He, and T. Pan Genome-wide analysis of N1-methyl-adenosine modification in human tRNAs RNA 16 2010 1317 1327
24. J.A. Dunkle, K. Vinal, P.M. Desai, N. Zelinskaya, M. Savic, D.M. West, G.L. Conn, and C.M. Dunham Molecular recognition and modification of the 30S ribosome by the aminoglycoside-resistance methyltransferase NpmA Proc. Natl. Acad. Sci. U. S. A. 111 2014 6275 6280
25. S. Hur, R.M. Stroud, and J. Finer-Moore Substrate recognition by RNA 5-methyluridine methyltransferases and pseudouridine synthases: A structural perspective J. Biol. Chem. 281 2006 38969 38973
26. H. Grosjean, J. Edqvist, K.B. Straby, and R. Giege Enzymatic formation of modified nucleosides in tRNA: Dependence on tRNA architecture J. Mol. Biol. 255 1996 67 85
27. T. Ito, I. Masuda, K. Yoshida, S. Goto-Ito, S. Sekine, S.W. Suh, Y.M. Hou, and S. Yokoyama Structural basis for methyl-donor-dependent and sequence-specific binding to tRNA substrates by knotted methyltransferase TrmD Proc. Natl. Acad. Sci. U. S. A. 112 2015 E4197 E4205
28. T.M. Schmeing, R.M. Voorhees, A.C. Kelley, Y.G. Gao, F.V. Murphy, J.R. Weir, and V. Ramakrishnan The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA Science 326 2009 688 694
29. R.T. Byrne, A.L. Konevega, M.V. Rodnina, and A.A. Antson The crystal structure of unmodified tRNAPhe from Escherichia coli Nucleic Acids Res. 38 2010 4154 4162
30. A. Guelorget, P. Barraud, C. Tisne, and B. Golinelli-Pimpaneau Structural comparison of tRNA m(1)A58 methyltransferases revealed different molecular strategies to maintain their oligomeric architecture under extreme conditions BMC Struct. Biol. 11 2011 48
31. N. Yamazaki, H. Hori, K. Ozawa, S. Nakanishi, T. Ueda, I. Kumagai, K. Watanabe, and K. Nishikawa Substrate specificity of tRNA (adenine-1-)-methyltransferase from Thermus thermophilus HB27 Biosci. Biotechnol. Biochem. 58 1994 1128 1133
32. D. Hamdane, A. Guelorget, V. Guerineau, and B. Golinelli-Pimpaneau Dynamics of RNA modification by a multi-site-specific tRNA methyltransferase Nucleic Acids Res. 42 2014 11697 11706
33. S.C. Walker, J.M. Avis, and G.L. Conn General plasmids for producing RNA in vitro transcripts with homogeneous ends Nucleic Acids Res. 31 2003 e82
34. W. Kabsch Xds Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 125 132
35. P.A. Karplus, and K. Diederichs Linking crystallographic model and data quality Science 336 2012 1030 1033
36. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
37. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 213 221
38. P. Emsley, and K. Cowtan Coot: Model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132
39. K.S. Keating, and A.M. Pyle RCrane: Semi-automated RNA model building Acta Crystallogr., Sect. D: Biol. Crystallogr. 68 2012 985 995
40. V.B. Chen, W.B. Arendall III, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 12 21
41. P. Gouet, E. Courcelle, D.I. Stuart, and F. Metoz ESPript: Analysis of multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308
42. T.J. Dolinsky, J.E. Nielsen, J.A. McCammon, and N.A. Baker PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32 2004 W665 W667
43. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - A visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
44. K. Diederichs, and P.A. Karplus Improved R-factors for diffraction data analysis in macromolecular crystallography Nat. Struct. Biol. 4 1997 269 275