MeRNA: a database of metal ion binding sites in RNA structures
http://www.100md.com
《核酸研究医学期刊》
1Department of Structural Biology, Physical Biosciences Division, Lawrence Berkeley National Laboratory Berkeley, CA 94720, USA 2Department of Plant and Microbial Biology 111 Koshland Hall #3102 University of California at Berkeley Berkeley, CA 94720-3102, USA
*To whom correspondence should be addressed. Tel: +1 510 486 4304; Fax: +1 510 486 6798; Email: SRHolbrook@lbl.gov
ABSTRACT
Metal ions are essential for the folding of RNA into stable tertiary structures and for the catalytic activity of some RNA enzymes. To aid in the study of the roles of metal ions in RNA structural biology, we have created MeRNA (Metals in RNA), a comprehensive compilation of all metal binding sites identified in RNA 3D structures available from the PDB and Nucleic Acid Database. Currently, our database contains information relating to binding of 9764 metal ions corresponding to 23 distinct elements, in 256 RNA structures. The metal ion locations were confirmed and ligands characterized using original literature references. MeRNA includes eight manually identified metal-ion binding motifs, which are described in the literature. MeRNA is searchable by PDB identifier, metal ion, method of structure determination, resolution and R-values for X-ray structure and distance from metal to any RNA atom or to water. New structures with their respective binding motifs will be added to the database as they become available. The MeRNA database will further our understanding of the roles of metal ions in RNA folding and catalysis and have applications in structural and functional analysis, RNA design and engineering. The MeRNA database is accessible at http://merna.lbl.gov.
INTRODUCTION
The significance of metal ion interaction with RNA structures became apparent in the mid-1960s when Fresco et al. (1) discovered that cations are essential for the stabilization of the native structure of transfer RNA. Over a decade later, the first crystal structures of tRNAPhe revealed at least four specific magnesium ion binding sites that are important in maintaining the fold of the tRNA molecule (2–4). Since then, numerous studies have shown that metal ions play a crucial role in RNA 3D folding, structure stabilization and catalytic activity .
In order to analyze the binding of metal ions to RNA and the role metal ions play in overall RNA structure and function, we have created a comprehensive database, MeRNA (Metals in RNA), of all metal binding sites identified in RNA 3D structures available from the PDB (12) and Nucleic Acid Database (NDB) (13). The MeRNA database is an adjunct to the Structural Classification of RNA database (SCOR) (14), which focuses on RNA structural and functional motifs.
MeRNA catalogs 9764 metal ions corresponding to 23 elements that interact with RNA in 256 PDB entries solved by X-ray diffraction, NMR and fiber diffraction, with coordinates released before July 1, 2005 and containing one or more metal cations bound to RNA. An analysis of our data identifies the characteristic coordination geometries and role of specific RNA functional groups in binding particular metal ions, as well as the presence of specific RNA metal binding motifs.
DATABASE CONTENT AND INTERFACE
Content
For each PDB or NDB entry we have extracted the experimental method, resolution, quality of the model, and primary and secondary references. Distances from the metals in each structure to the nearest RNA atoms, as well as protein atoms and water molecules, are calculated from atomic coordinates. Only RNA and protein atoms which can serve as ligands for metal ions (e.g. N, O, S) are included in MeRNA analysis. These data are stored in a MySQL database. The binding motifs and types of binding were manually determined by analyzing each RNA structure and comparing to certain binding motifs previously described in the literature. In particular, eight well-characterized metal ion binding motifs were identified and included in the database. These eight include (i) the major groove of a G?U wobble base pair, followed by a Y?G pair (see Figure 1a) (15–21), (ii) sheared G?A pairs (22–25), (iii) magnesium clamp (26), (iv) metal ion zipper (25), (v) loop E motif (25,27–29), (vi) AA platform (see Figure 1b) (30–32), (vii) tetrads (33–36) and (viii) the G-phosphate Mg ion binding motif (37). The content of the database with respect to the cations included in the PDB entries and their preference for certain binding motifs is illustrated in Table 1.
Figure 1 (a) Major groove of G-U wobble pair binds a sodium ion (pdb code 1s72 ); (b) AA-platform motif from 23S RNA binds a sodium ion (pdb code 1s72 ). Thin black lines indicate direct bonding between the sodium ion and RNA atoms. Figures generated with Swiss-PdbViewer, version 7.5 (45).
Table 1 Metal ions bound to RNA structures
As expected, magnesium ions occur in the most structures and are most numerous in the database, followed by sodium ions. This is due to the abundance of structures containing these ions and the particularly important role they play in the structure and function of nucleic acids. For instance, magnesium ions play an essential role in the tertiary folding of tRNA (2–4) as well as in the structure and catalytic function of ribozymes (23,24,31,32,38–44). The large number of occurrences of tungsten is due to the use of the octadecatungstenyl diphosphate complex with the formula O62P2W18 for crystallographic phasing in large RNA structures.
Interface
The home page contains a simple search by either PDB ID or metal ion type. The advanced search page (shown below) contains a form allowing searches by any of the following: PDB or NDB IDs, metal ion, experimental method, resolution, R and free R-values, binding motif, distance to any RNA or protein atom or water molecule and any combination of the above. It is also possible to search by author name either in the primary or in additional references, or both. An example of the advanced search page and its result page is given in Figures 2 and 3.
Figure 2 A snapshot of MeRNA interface showing the advanced search page.
Figure 3 A snapshot of MeRNA interface showing the results of previous search query.
Applications
Using the information contained in our database, one can explore approaches to predict metal ion binding sites in RNA sequence and structure and to identify new RNA metal ion binding motifs.
MeRNA can also be used with the SCOR database to understand RNA 3D structures in a comprehensive way, on the basis of their structure and function. This can be achieved relating RNA structural and tertiary interaction motifs classified in the SCOR database to the metal ion binding motifs included in MeRNA.
As it develops, MeRNA will become an invaluable resource for understanding the role of metal ions in forming and maintaining RNA structure and RNA function. Such insight will ultimately aid in the design of RNA structures with specific properties.
According to the published descriptions, many RNA structures have been determined, for which the bound (localized) metal ion coordinates have not been deposited to the PDB or NDB. This is often the case for heavy atom derivatives of the native RNA prepared for crystallographic phasing. The availability of these additional metal ion coordinates in RNA structures should provide a better overall description and understanding of the roles of metal ion binding in RNA.
ACKNOWLEDGEMENTS
The authors would like to thank Makio Tamura for writing the first code to calculate distances from PDB coordinates and for useful discussions. L.R.S., D.K.H., S.E.B. and S.R.H. were supported by National Institutes of Health (NIGMS) grant 1R01GM66199 through the US Department of Energy under Contract No. DE-AC02-05CH11231. S.R.H. was also supported by NIH (NHGRI) grant 1R01HG002665. S.E.B. was also supported by NHGRI of the NIH grant K22 HG00056 and is a Searle Scholar. Funding to pay the Open Access publication charges for this article was provided by NIGMS.
REFERENCES
Fresco, J.R., Adams, A., Ascione, R., Henley, D., Lindahl, T. (1966) Tertiary structure in transfer ribonucleic acids Cold Spring Harb. Symp. Quant. Biol, . 31, 527–537 .
Holbrook, S.R., Sussman, J.L., Warrant, R.W., Church, G.M., Kim, S.H. (1977) RNA-ligand interactions. (I) magnesium binding sites in yeast tRNAphe Nucleic Acids Res, . 4, 2811–2820 .
Jack, A., Ladner, J.E., Rhodes, D., Brown, R.S., Klug, A. (1977) A crystallographic study of metal-binding to yeast phenylalanine transfer RNA J. Mol. Biol, . 111, 315–328 .
Quigley, G.J., Teeter, M.M., Rich, A. (1978) Structural analysis of spermine and magnesium ion binding to yeast phenylalanine transfer RNA Proc. Natl Acad. Sci. USA, 75, 64–68 .
Pyle, A.M. (1993) Ribozymes—a distinct class of metalloenzymes Science, 261, 709–714 .
Pyle, A.M. (2002) Metal ions in the structure and function of RNA J. Biol. Inorg. Chem, . 7, 679–690 .
Pan, T., Long, D.M., Uhlenbeck, O.C. (1993) Divalent metal ions in RNA folding and catalysis In Gesteland, R.F. and Atkins, J.F. (Eds.). The RNA world, NY Cold Spring Harbor Laboratory Press pp. 271–302 .
Lilley, D.M. (1999) Folding and catalysis by the hairpin ribozyme FEBS Lett, . 452, 26–30 .
Hanna, R. and Doudna, J.A. (2000) Metal ions in ribozyme folding and catalysis Curr. Opin. Chem. Biol, . 4, 166–170 .
Ferre-D'Amare, A.R. and Doudna, J.A. (1999) RNA folds: insights from recent crystal structures Annu. Rev. of Biophys. Biomol. Struct, . 28, 57–73 .
DeRose, V.J. (2003) Metal ion binding to catalytic RNA molecules Curr. Opin. Struct. Biol, . 13, 317–324 .
Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E. (2000) The protein data bank Nucleic Acids Res, . 28, 235–242 .
Berman, H.M., Olson, W.K., Beveridge, D.L., Westbrook, J., Gelbin, A., Demeny, T., Hsieh, S.H., Srinivasan, A.R., Schneider, B. (1992) The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids Biophys. J, . 63, 751–759 .
Klosterman, P.S., Tamura, M., Holbrook, S.R., Brenner, S.E. (2002) SCOR: a structural classification of RNA database Nucleic Acids Res, . 30, 392–394 .
Gautheret, D., Konings, D., Gutell, R.R. (1995) G.U. base pairing motifs in ribosomal RNA RNA, 1, 807–814 .
Cate, J.H. and Doudna, J.A. (1996) Metal-binding sites in the major groove of a large ribozyme domain Structure, 4, 1221–1229 .
Hermann, T. and Westhof, E. (1998) Exploration of metal ion binding sites in RNA folds by brownian-dynamics simulations Structure, 6, 1303–1314 .
Westhof, E., Dumas, P., Moras, D. (1985) Crystallographic refinement of yeast aspartic acid transfer RNA J. Mol. Biol, . 184, 119–145 .
Cate, J.H., Gooding, A.R., Podell, E., Zhou, K., Golden, B.L., Kundrot, C.E., Cech, T.R., Doudna, J.A. (1996) Crystal structure of a group I ribozyme domain: principles of RNA packing Science, 273, 1678–1685 .
Kieft, J.S. and Tinoco, I., Jr. (1997) Solution structure of a metal-binding site in the major groove of RNA complexed with cobalt (III) hexammine Structure, 5, 713–721 .
Colmenarejo, G. and Tinoco, I.J. (1999) Structure and thermodynamics of metal binding in the P5 helix of a group I intron ribozyme J. Mol. Biol, . 290, 119–135 .
Baeyens, K.J., De Bondt, H.L., Pardi, A., 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. USA, 93, 12851–12855 .
Pley, H.W., Flaherty, K.M., McKay, D.B. (1994) Three-dimensional structure of a hammerhead ribozyme Nature, 372, 68–74 .
Scott, W.G., Finch, J.T., Klug, A. (1995) The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage Cell, 81, 991–1002 .
Correll, C.C., Freeborn, B., Moore, P.B., Steitz, T.A. (1997) Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain Cell, 91, 705–712 .
Ennifar, E., Yusupov, M., Walter, P., Marquet, R., Ehresmann, B., Ehresmann, C., 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 .
Leontis, N.B. and Westhof, E. (1998) The 5S rRNA loop E: chemical probing and phylogenetic data versus crystal structure RNA, 4, 1134–1153 .
Auffinger, P., Bielecki, L., Westhof, E. (2004) Symmetric K+ and Mg2+ ion-binding sites in the 5S rRNA loop E inferred from molecular dynamics simulations J. Mol. Biol, . 335, 555–571 .
Reblova, K., Spackova, N., Stefl, R., Csaszar, K., Koca, J., Leontis, N.B., Sponer, J. (2003) Non-Watson–Crick base pairing and hydration in RNA motifs: Molecular dynamics of 5S rRNA loop E Biophys. J, . 84, 3564–3582 .
Costa, M. and Michel, F. (1995) Frequent use of the same tertiary motif by self-folding RNAs EMBO J, . 14, 1276–1285 .
Basu, S., Rambo, R.P., Strauss-Soukup, J., Cate, J.H., Ferre-D'Amare, A.R., Strobel, S.A., Doudna, J.A. (1998) A specific monovalent metal ion integral to the AA platform of the RNA tetraloop receptor Nature Struct. Biol, . 5, 986–992 .
Cate, J.H., Gooding, A.R., Podell, E., Zhou, K., Golden, B.L., Szewczak, A.A., Kundrot, C.E., Cech, T.R., Doudna, J.A. (1996) RNA tertiary structure mediation by adenosine platforms Science, 273, 1696–1699 .
Cheong, C. and Moore, P.B. (1992) Solution structure of an unusually stable RNA tetraplex containing G- and U-quartet structures Biochemistry, 31, 8406–8414 .
Pan, B., Xiong, Y., Shi, K., Deng, J., Sundaralingam, M. (2003) Crystal structure of an RNA purine-rich tetraplex containing adenine tetrads: implications for specific binding in RNA tetraplexes Structure, 11, 815–823 .
Pan, B., Xiong, Y., Shi, K., Sundaralingam, M. (2003) Crystal structure of a bulged RNA tetraplex at 1.1 a resolution: implications for a novel binding site in RNA tetraplex Structure, 11, 1423–1430 .
Pan, B., Xiong, Y., Shi, K., Sundaralingam, M. (2003) An eight-stranded helical fragment in RNA crystal structure: Implications for tetraplex interaction Structure (Camb.), 11, 825–831 .
Klein, D.J., Moore, P.B., Steitz, T.A. (2004) The contribution of metal ions to the structural stability of the large ribosomal subunit RNA, 10, 1366–1379 .
Streicher, B., Westhof, E., Schroeder, R. (1996) The environment of two metal ions surrounding the splice site of a group I intron EMBO J, . 15, 2556–2564 .
Deme, E., Nolte, A., Jacquier, A. (1999) Unexpected metal ion requirements specific for catalysis of the branching reaction in a group II intron Biochemistry, 38, 3157–3167 .
Scott, W.G. (1999) Biophysical and biochemical investigations of RNA catalysis in the hammerhead ribozyme Quart. Rev. Biophys, . 32, 241–284 .
Wedekind, J.E. and McKay, D.B. (1999) Crystal structure of a lead-dependent ribozyme revealing metal binding sites relevant to catalysis Nature Struct. Biol, . 6, 261–268 .
Scott, W.G. and Klug, A. (1996) Ribozymes—structure and mechanism in RNA catalysis Trends Biochem. Sci, . 21, 220–224 .
Steitz, T.A. and Steitz, J.A. (1993) A general two-metal-ion mechanism for catalytic RNA Proc. Natl Acad. Sci. USA, 90, 6498–6502 .
Pan, T. and Uhlenbeck, O.C. (1992) A small metalloribozyme with a two-step mechanism Nature, 358, 560–563 .
Guex, N. and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis, 18, 2714–2723 .
Shannon, R. (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides Acta Crystallogr. A, . A32, 751–767 .(Liliana R. Stefan1, Rui Zhang1, Aaron G.)
*To whom correspondence should be addressed. Tel: +1 510 486 4304; Fax: +1 510 486 6798; Email: SRHolbrook@lbl.gov
ABSTRACT
Metal ions are essential for the folding of RNA into stable tertiary structures and for the catalytic activity of some RNA enzymes. To aid in the study of the roles of metal ions in RNA structural biology, we have created MeRNA (Metals in RNA), a comprehensive compilation of all metal binding sites identified in RNA 3D structures available from the PDB and Nucleic Acid Database. Currently, our database contains information relating to binding of 9764 metal ions corresponding to 23 distinct elements, in 256 RNA structures. The metal ion locations were confirmed and ligands characterized using original literature references. MeRNA includes eight manually identified metal-ion binding motifs, which are described in the literature. MeRNA is searchable by PDB identifier, metal ion, method of structure determination, resolution and R-values for X-ray structure and distance from metal to any RNA atom or to water. New structures with their respective binding motifs will be added to the database as they become available. The MeRNA database will further our understanding of the roles of metal ions in RNA folding and catalysis and have applications in structural and functional analysis, RNA design and engineering. The MeRNA database is accessible at http://merna.lbl.gov.
INTRODUCTION
The significance of metal ion interaction with RNA structures became apparent in the mid-1960s when Fresco et al. (1) discovered that cations are essential for the stabilization of the native structure of transfer RNA. Over a decade later, the first crystal structures of tRNAPhe revealed at least four specific magnesium ion binding sites that are important in maintaining the fold of the tRNA molecule (2–4). Since then, numerous studies have shown that metal ions play a crucial role in RNA 3D folding, structure stabilization and catalytic activity .
In order to analyze the binding of metal ions to RNA and the role metal ions play in overall RNA structure and function, we have created a comprehensive database, MeRNA (Metals in RNA), of all metal binding sites identified in RNA 3D structures available from the PDB (12) and Nucleic Acid Database (NDB) (13). The MeRNA database is an adjunct to the Structural Classification of RNA database (SCOR) (14), which focuses on RNA structural and functional motifs.
MeRNA catalogs 9764 metal ions corresponding to 23 elements that interact with RNA in 256 PDB entries solved by X-ray diffraction, NMR and fiber diffraction, with coordinates released before July 1, 2005 and containing one or more metal cations bound to RNA. An analysis of our data identifies the characteristic coordination geometries and role of specific RNA functional groups in binding particular metal ions, as well as the presence of specific RNA metal binding motifs.
DATABASE CONTENT AND INTERFACE
Content
For each PDB or NDB entry we have extracted the experimental method, resolution, quality of the model, and primary and secondary references. Distances from the metals in each structure to the nearest RNA atoms, as well as protein atoms and water molecules, are calculated from atomic coordinates. Only RNA and protein atoms which can serve as ligands for metal ions (e.g. N, O, S) are included in MeRNA analysis. These data are stored in a MySQL database. The binding motifs and types of binding were manually determined by analyzing each RNA structure and comparing to certain binding motifs previously described in the literature. In particular, eight well-characterized metal ion binding motifs were identified and included in the database. These eight include (i) the major groove of a G?U wobble base pair, followed by a Y?G pair (see Figure 1a) (15–21), (ii) sheared G?A pairs (22–25), (iii) magnesium clamp (26), (iv) metal ion zipper (25), (v) loop E motif (25,27–29), (vi) AA platform (see Figure 1b) (30–32), (vii) tetrads (33–36) and (viii) the G-phosphate Mg ion binding motif (37). The content of the database with respect to the cations included in the PDB entries and their preference for certain binding motifs is illustrated in Table 1.
Figure 1 (a) Major groove of G-U wobble pair binds a sodium ion (pdb code 1s72 ); (b) AA-platform motif from 23S RNA binds a sodium ion (pdb code 1s72 ). Thin black lines indicate direct bonding between the sodium ion and RNA atoms. Figures generated with Swiss-PdbViewer, version 7.5 (45).
Table 1 Metal ions bound to RNA structures
As expected, magnesium ions occur in the most structures and are most numerous in the database, followed by sodium ions. This is due to the abundance of structures containing these ions and the particularly important role they play in the structure and function of nucleic acids. For instance, magnesium ions play an essential role in the tertiary folding of tRNA (2–4) as well as in the structure and catalytic function of ribozymes (23,24,31,32,38–44). The large number of occurrences of tungsten is due to the use of the octadecatungstenyl diphosphate complex with the formula O62P2W18 for crystallographic phasing in large RNA structures.
Interface
The home page contains a simple search by either PDB ID or metal ion type. The advanced search page (shown below) contains a form allowing searches by any of the following: PDB or NDB IDs, metal ion, experimental method, resolution, R and free R-values, binding motif, distance to any RNA or protein atom or water molecule and any combination of the above. It is also possible to search by author name either in the primary or in additional references, or both. An example of the advanced search page and its result page is given in Figures 2 and 3.
Figure 2 A snapshot of MeRNA interface showing the advanced search page.
Figure 3 A snapshot of MeRNA interface showing the results of previous search query.
Applications
Using the information contained in our database, one can explore approaches to predict metal ion binding sites in RNA sequence and structure and to identify new RNA metal ion binding motifs.
MeRNA can also be used with the SCOR database to understand RNA 3D structures in a comprehensive way, on the basis of their structure and function. This can be achieved relating RNA structural and tertiary interaction motifs classified in the SCOR database to the metal ion binding motifs included in MeRNA.
As it develops, MeRNA will become an invaluable resource for understanding the role of metal ions in forming and maintaining RNA structure and RNA function. Such insight will ultimately aid in the design of RNA structures with specific properties.
According to the published descriptions, many RNA structures have been determined, for which the bound (localized) metal ion coordinates have not been deposited to the PDB or NDB. This is often the case for heavy atom derivatives of the native RNA prepared for crystallographic phasing. The availability of these additional metal ion coordinates in RNA structures should provide a better overall description and understanding of the roles of metal ion binding in RNA.
ACKNOWLEDGEMENTS
The authors would like to thank Makio Tamura for writing the first code to calculate distances from PDB coordinates and for useful discussions. L.R.S., D.K.H., S.E.B. and S.R.H. were supported by National Institutes of Health (NIGMS) grant 1R01GM66199 through the US Department of Energy under Contract No. DE-AC02-05CH11231. S.R.H. was also supported by NIH (NHGRI) grant 1R01HG002665. S.E.B. was also supported by NHGRI of the NIH grant K22 HG00056 and is a Searle Scholar. Funding to pay the Open Access publication charges for this article was provided by NIGMS.
REFERENCES
Fresco, J.R., Adams, A., Ascione, R., Henley, D., Lindahl, T. (1966) Tertiary structure in transfer ribonucleic acids Cold Spring Harb. Symp. Quant. Biol, . 31, 527–537 .
Holbrook, S.R., Sussman, J.L., Warrant, R.W., Church, G.M., Kim, S.H. (1977) RNA-ligand interactions. (I) magnesium binding sites in yeast tRNAphe Nucleic Acids Res, . 4, 2811–2820 .
Jack, A., Ladner, J.E., Rhodes, D., Brown, R.S., Klug, A. (1977) A crystallographic study of metal-binding to yeast phenylalanine transfer RNA J. Mol. Biol, . 111, 315–328 .
Quigley, G.J., Teeter, M.M., Rich, A. (1978) Structural analysis of spermine and magnesium ion binding to yeast phenylalanine transfer RNA Proc. Natl Acad. Sci. USA, 75, 64–68 .
Pyle, A.M. (1993) Ribozymes—a distinct class of metalloenzymes Science, 261, 709–714 .
Pyle, A.M. (2002) Metal ions in the structure and function of RNA J. Biol. Inorg. Chem, . 7, 679–690 .
Pan, T., Long, D.M., Uhlenbeck, O.C. (1993) Divalent metal ions in RNA folding and catalysis In Gesteland, R.F. and Atkins, J.F. (Eds.). The RNA world, NY Cold Spring Harbor Laboratory Press pp. 271–302 .
Lilley, D.M. (1999) Folding and catalysis by the hairpin ribozyme FEBS Lett, . 452, 26–30 .
Hanna, R. and Doudna, J.A. (2000) Metal ions in ribozyme folding and catalysis Curr. Opin. Chem. Biol, . 4, 166–170 .
Ferre-D'Amare, A.R. and Doudna, J.A. (1999) RNA folds: insights from recent crystal structures Annu. Rev. of Biophys. Biomol. Struct, . 28, 57–73 .
DeRose, V.J. (2003) Metal ion binding to catalytic RNA molecules Curr. Opin. Struct. Biol, . 13, 317–324 .
Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E. (2000) The protein data bank Nucleic Acids Res, . 28, 235–242 .
Berman, H.M., Olson, W.K., Beveridge, D.L., Westbrook, J., Gelbin, A., Demeny, T., Hsieh, S.H., Srinivasan, A.R., Schneider, B. (1992) The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids Biophys. J, . 63, 751–759 .
Klosterman, P.S., Tamura, M., Holbrook, S.R., Brenner, S.E. (2002) SCOR: a structural classification of RNA database Nucleic Acids Res, . 30, 392–394 .
Gautheret, D., Konings, D., Gutell, R.R. (1995) G.U. base pairing motifs in ribosomal RNA RNA, 1, 807–814 .
Cate, J.H. and Doudna, J.A. (1996) Metal-binding sites in the major groove of a large ribozyme domain Structure, 4, 1221–1229 .
Hermann, T. and Westhof, E. (1998) Exploration of metal ion binding sites in RNA folds by brownian-dynamics simulations Structure, 6, 1303–1314 .
Westhof, E., Dumas, P., Moras, D. (1985) Crystallographic refinement of yeast aspartic acid transfer RNA J. Mol. Biol, . 184, 119–145 .
Cate, J.H., Gooding, A.R., Podell, E., Zhou, K., Golden, B.L., Kundrot, C.E., Cech, T.R., Doudna, J.A. (1996) Crystal structure of a group I ribozyme domain: principles of RNA packing Science, 273, 1678–1685 .
Kieft, J.S. and Tinoco, I., Jr. (1997) Solution structure of a metal-binding site in the major groove of RNA complexed with cobalt (III) hexammine Structure, 5, 713–721 .
Colmenarejo, G. and Tinoco, I.J. (1999) Structure and thermodynamics of metal binding in the P5 helix of a group I intron ribozyme J. Mol. Biol, . 290, 119–135 .
Baeyens, K.J., De Bondt, H.L., Pardi, A., 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. USA, 93, 12851–12855 .
Pley, H.W., Flaherty, K.M., McKay, D.B. (1994) Three-dimensional structure of a hammerhead ribozyme Nature, 372, 68–74 .
Scott, W.G., Finch, J.T., Klug, A. (1995) The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage Cell, 81, 991–1002 .
Correll, C.C., Freeborn, B., Moore, P.B., Steitz, T.A. (1997) Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain Cell, 91, 705–712 .
Ennifar, E., Yusupov, M., Walter, P., Marquet, R., Ehresmann, B., Ehresmann, C., 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 .
Leontis, N.B. and Westhof, E. (1998) The 5S rRNA loop E: chemical probing and phylogenetic data versus crystal structure RNA, 4, 1134–1153 .
Auffinger, P., Bielecki, L., Westhof, E. (2004) Symmetric K+ and Mg2+ ion-binding sites in the 5S rRNA loop E inferred from molecular dynamics simulations J. Mol. Biol, . 335, 555–571 .
Reblova, K., Spackova, N., Stefl, R., Csaszar, K., Koca, J., Leontis, N.B., Sponer, J. (2003) Non-Watson–Crick base pairing and hydration in RNA motifs: Molecular dynamics of 5S rRNA loop E Biophys. J, . 84, 3564–3582 .
Costa, M. and Michel, F. (1995) Frequent use of the same tertiary motif by self-folding RNAs EMBO J, . 14, 1276–1285 .
Basu, S., Rambo, R.P., Strauss-Soukup, J., Cate, J.H., Ferre-D'Amare, A.R., Strobel, S.A., Doudna, J.A. (1998) A specific monovalent metal ion integral to the AA platform of the RNA tetraloop receptor Nature Struct. Biol, . 5, 986–992 .
Cate, J.H., Gooding, A.R., Podell, E., Zhou, K., Golden, B.L., Szewczak, A.A., Kundrot, C.E., Cech, T.R., Doudna, J.A. (1996) RNA tertiary structure mediation by adenosine platforms Science, 273, 1696–1699 .
Cheong, C. and Moore, P.B. (1992) Solution structure of an unusually stable RNA tetraplex containing G- and U-quartet structures Biochemistry, 31, 8406–8414 .
Pan, B., Xiong, Y., Shi, K., Deng, J., Sundaralingam, M. (2003) Crystal structure of an RNA purine-rich tetraplex containing adenine tetrads: implications for specific binding in RNA tetraplexes Structure, 11, 815–823 .
Pan, B., Xiong, Y., Shi, K., Sundaralingam, M. (2003) Crystal structure of a bulged RNA tetraplex at 1.1 a resolution: implications for a novel binding site in RNA tetraplex Structure, 11, 1423–1430 .
Pan, B., Xiong, Y., Shi, K., Sundaralingam, M. (2003) An eight-stranded helical fragment in RNA crystal structure: Implications for tetraplex interaction Structure (Camb.), 11, 825–831 .
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