Magnesium-binding architectures in RNA crystal structures: Validation, binding preferences, classification and motif detection

Nucleic Acids Research

Volumn 43, Issue 7, 2015, Pages 3789-3801

  Zheng, Heping ^a,b,c,d   Shabalin, Ivan G ^a,b,c,d,e   Handing, Katarzyna B ^a,c,d,f   Bujnicki, Janusz M ^f,g   Minor, Wladek ^a,b,c,d,e  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Center for Structural Genomics of Infectious Diseases (CSGID) Consortium   (United States)

^c Midwest Center for Structural Genomics (MCSG) Consortium   (United States)

^d New York Structural Genomics Research Consortium (NYSGRC)   (United States)

^e Enzyme Function Initiative ^*  (United States)

^f INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^g ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE; MAGNESIUM ION; NITROGEN; OXYGEN; MAGNESIUM; RNA;

ARTICLE; ATOM; BINDING SITE; CHEMICAL COMPOSITION; CLASSIFICATION; CRYSTAL STRUCTURE; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN DATA BANK; RNA STRUCTURE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; CHEMISTRY; CONFORMATION; METABOLISM; VALIDATION STUDY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MAGNESIUM; NUCLEIC ACID CONFORMATION; RNA;

EID: 84930632553     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv225     Document Type: Article

References (37)

1. Draper, D.E. (2008) RNA folding: Thermodynamic and molecular descriptions of the roles of ions. Biophys. J., 95, 5489-5495.
2. Tinoco, I. Jr and Kieft, J.S. (1997) The ion core in RNA folding. Nat. Struct. Biol., 4, 509-512.
3. Jenner, L., Demeshkina, N., Yusupova, G. and Yusupov, M. (2010) Structural rearrangements of the ribosome at the tRNA proofreading step. Nat. Struct. Mol. Biol., 17, 1072-1078.
4. Brannvall, M. and Kirsebom, L.A. (2001) Metal ion cooperativity in ribozyme cleavage of RNA. Proc. Natl Acad. Sci. U.S.A., 98, 12943-12947.
5. Scott, W.G., Finch, J.T. and Klug, A. (1995) The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage. Cell, 81, 991-1002.
6. Bowman, J.C., Lenz, T.K., Hud, N.V. and Williams, L.D. (2012) Cations in charge: magnesium ions in RNA folding and catalysis. Curr. Opin. Struct. Biol., 22, 262-272.
7. Ennifar, E., Yusupov, M., Walter, P., Marquet, R., Ehresmann, B., Ehresmann, C. and Dumas, P. (1999) The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges. Structure, 7, 1439-1449.
8. Correll, C.C., Freeborn, B., Moore, P.B. and Steitz, T.A. (1997) Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain. Cell, 91, 705-712.
9. Baeyens, K.J., De Bondt, H.L., Pardi, A. and Holbrook, S.R. (1996) A curved RNA helix incorporating an internal loop with G.A and A.A non-watson-crick base pairing. Proc. Natl Acad. Sci. U.S.A., 93, 12851-12855.
10. Klein, D.J., Moore, P.B. and Steitz, T.A. (2004) The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA, 10, 1366-1379.
11. Lippert, B. (2000) Multiplicity of metal ion binding patterns to nucleobases. Coordin. Chem. Rev., 200, 487-516.
12. Hsiao, C., Tannenbaum, E., VanDeusen, H., Hershkovitz, E., Perng, G., Tannenbaum, A.R. and Williams, L.D. (2009) Complexes of nucleic acids with group I and II cations. In: Hud, NV (ed). Nucleic Acid-Metal Ion Interactions. RSC Publishing, Cambridge, pp. 1-38.
13. Stefan, L.R., Zhang, R., Levitan, A.G., Hendrix, D.K., Brenner, S.E. and Holbrook, S.R. (2006) MeRNA: a database of metal ion binding sites in RNA structures. Nucleic Acids Res., 34, D131-D134.
14. Schnabl, J., Suter, P. and Sigel, R.K. (2012) MINAS-a database of metal ions in nucleic AcidS. Nucleic Acids Res., 40, D434-D438.
15. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The protein data bank. Nucleic Acids Res., 28, 235-242.
16. Cooper, D.R., Porebski, P.J., Chruszcz, M. and Minor, W. (2011) X-ray crystallography: assessment and validation of protein-small molecule complexes for drug discovery. Expert Opin. Drug Discov., 6, 771-782.
17. Pozharski, E., Weichenberger, C.X. and Rupp, B. (2013) Techniques, tools and best practices for ligand electron-density analysis and results from their application to deposited crystal structures. Acta Crystallogr. D, 69, 150-167.
18. Zheng, H., Chordia, M.D., Cooper, D.R., Chruszcz, M., Muller, P., Sheldrick, G.M. and Minor, W. (2014) Validation of metal-binding sites in macromolecular structures with the CheckMyMetal web server. Nat. Protoc., 9, 156-170.
19. Nayal, M. and Di Cera, E. (1996) Valence screening of water in protein crystals reveals potential na+ binding sites. J. Mol. Biol., 256, 228-234.
20. Zheng, H., Chruszcz, M., Lasota, P., Lebioda, L. and Minor, W. (2008) Data mining of metal ion environments present in protein structures. J. Inorg. Biochem., 102, 1765-1776.
21. Allen, F.H. (2002) The Cambridge structural database: a quarter of a million crystal structures and rising. Acta Cryst. B, 58, 380-388.
22. Permyakov, E. (2009) Metalloproteomics. Wiley & Sons, Inc., Hoboken, NJ.
23. Word, J.M., Lovell, S.C., LaBean, T.H., Taylor, H.C., Zalis, M.E., Presley, B.K., Richardson, J.S. and Richardson, D.C. (1999) Visualizing and quantifying molecular goodness-of-ft: small-probe contact dots with explicit hydrogen atoms. J. Mol. Biol., 285, 1711-1733.
24. Chen, V.B., Arendall, W.B. III, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D, 66, 12-21.
25. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G., McCoy, A. et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr., 67, 235-242.
26. Brese, N.E. and O'Keeffe, M. (1991) Bond-valence parameters for solids. Acta Cryst. B, 47, 192-197.
27. Müller, P., Köpke, S. and Sheldrick, G.M. (2003) Is the bond-valence method able to identify metal atoms in protein structures? Acta Cryst. D, 59, 32-37.
28. Borovinskaya, M.A., Pai, R.D., Zhang, W., Schuwirth, B.S., Holton, J.M., Hirokawa, G., Kaji, H., Kaji, A. and Cate, J.H. (2007) Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat. Struct. Mol. Biol., 14, 727-732.
29. Rabl, J., Leibundgut, M., Ataide, S.F., Haag, A. and Ban, N. (2011) Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science, 331, 730-736.
30. Petrov, A.S., Bowman, J.C., Harvey, S.C. and Williams, L.D. (2011) Bidentate RNA-magnesium clamps: on the origin of the special role of magnesium in RNA folding. RNA, 17, 291-297.
31. Szabó, Z. (2008) Multinuclear NMR studies of the interaction of metal ions with adenine-nucleotides. Coord. Chem. Rev., 252, 2362-2380.
32. Hawkins, P.C., Warren, G.L., Skillman, A.G. and Nicholls, A. (2008) How to do an evaluation: pitfalls and traps. J. Comput. Aided Mol. Des., 22, 179-190.
33. Andreini, C., Cavallaro, G., Lorenzini, S. and Rosato, A. (2013) MetalPDB: a database of metal sites in biological macromolecular structures. Nucleic Acids Res., 41, D312-D319.
34. Castagnetto, J.M., Hennessy, S.W., Roberts, V.A., Getzoff, E.D., Tainer, J.A. and Pique, M.E. (2002) MDB: the metalloprotein database and browser at the scripps research institute. Nucleic Acids Res., 30, 379-382.
35. Hsin, K., Sheng, Y., Harding, M.M., Taylor, P. and Walkinshaw, M.D. (2008) MESPEUS: a database of the geometry of metal sites in proteins. J. Appl. Crystallogr., 41, 963-968.
36. Philips, A., Milanowska, K., Lach, G., Boniecki, M., Rother, K. and Bujnicki, J.M. (2012) MetalionRNA: computational predictor of metal-binding sites in RNA structures. Bioinformatics, 28, 198-205.
37. Hanson, R.M. (2010) Jmol-a paradigm shift in crystallographic visualization. J. Appl. Crystallogr., 43, 1250-1260.