A crystallographic study of the binding of 13 metal ions of two related RNA duplexes

Nucleic Acids Research

Volumn 31, Issue 10, 2003, Pages 2671-2682

  Ennifar, Eric ^a   Walter, Philippe ^a   Dumas, Philippe ^a  

^a INST DE BIOL MOLEC ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BARIUM ION; CADMIUM; CALCIUM ION; COBALT; COBALT DERIVATIVE; CYTOSINE; DIVALENT CATION; DOUBLE STRANDED RNA; GOLD; GUANINE; LEAD; MAGNESIUM ION; MANGANESE; METAL ION; METHENAMINE; PLATINUM; POTASSIUM ION; RUTHENIUM DERIVATIVE; STRONTIUM; VIRUS RNA; ZINC ION; COBALT AMMONIUM COMPLEX; GOLD CHLORIDE; GOLD DERIVATIVE; HETERODUPLEX; MAGNESIUM; METAL; OLIGORIBONUCLEOTIDE; PLATINUM DERIVATIVE; PLATINUM TETRACHLORIDE; RNA; RUTHENIUM HEXAAMMINE;

ARTICLE; BASE PAIRING; BINDING AFFINITY; CONTROLLED STUDY; DIMERIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; METAL BINDING; MOLECULAR MIMICRY; PRIORITY JOURNAL; RNA SEQUENCE; RNA STRUCTURE; X RAY CRYSTALLOGRAPHY; BINDING COMPETITION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; CRYSTALLIZATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

BASE SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; CATIONS, DIVALENT; COBALT; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; GOLD COMPOUNDS; MAGNESIUM; METALS; MODELS, MOLECULAR; NUCLEIC ACID HETERODUPLEXES; OLIGORIBONUCLEOTIDES; PLATINUM COMPOUNDS; RNA; RUTHENIUM COMPOUNDS;

EID: 0038719800     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkg350     Document Type: Article

References (59)

1. Weinstein,L.B., Jones,B.C., Cosstick,R. and Cech,T.R. (1997) A second catalytic metal ion in group I ribozyme. Nature, 388, 805-808.
2. Sood,V.D., Beattie,T.L. and Collins,R.A. (1998) Identification of phosphate groups involved in metal binding and tertiary interactions in the core of the Neurospora VS ribozyme. J. Mol. Biol., 282, 741-750.
3. Yoshida,A., Sun,S. and Piccirilli,J.A. (1999) A new metal ion interaction in the Tetrahymena ribozyme reaction revealed by double sulfur substitution. Nature Struct. Biol., 6, 318-321.
4. 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.
5. Colmenarejo,G. and Tinoco,I.,Jr (1999) Structure and thermodynamics of metal binding in the P5 helix of a group I intron ribozyme. J. Mol. Biol., 290, 119-135.
6. Gonzalez,R.L.,Jr and Tinoco,I.,Jr (1999) Solution structure and thermodynamics of a divalent metal ion binding site in an RNA pseudoknot. J. Mol. Biol., 289, 1267-1282.
7. Schmitz,M. and Tinoco,I.,Jr (2000) Solution structure and metal-ion binding of the P4 element from bacterial RNase P RNA. RNA, 6, 1212-1225.
8. Rudisser,S. and Tinoco,I.,Jr (2000) Solution structure of Cobalt(III)hexammine complexed to the GAAA tetraloop and metal-ion binding to G·A mismatches. J. Mol. Biol., 295, 1211-1223.
9. Tanaka,Y., Kojima,C., Morita,E.H., Kasai,Y., Yamasaki,K., Ono,A., Kainosho,M. and Taira,K. (2002) Identification of the metal ion binding site on an RNA motif from hammerhead ribozymes using (15)N NMR spectroscopy. J. Am. Chem. Soc., 124, 4595-4601.
10. Pilbrow,J.R. and Hanson,G.R. (1993) Electron paramagnetic resonance. In Riordan,J.F. and Vallee,B.L. (eds), Methods Enzymology, Vol. 227, pp. 330-353.
11. Hermann,T. and Westhof,E. (1998) Exploration of metal ion binding sites in RNA folds by Brownian-dynamics simulations. Structure, 6, 1303-1314.
12. Skripkin,E., Paillart,J.C., Marquet,R., Ehresmann,B. and Ehresmann,C. (1994) Identification of the primary site of the Human Immunodeficiency Virus Type I RNA dimerization in vitro. Proc. Natl Acad. Sci. USA, 91, 4945-4949.
13. Muriaux,D., Rocquigny,H.D., Roques,B.P. and Paoletti,J. (1996) NCP7 activates HIV-1 Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J. Biol. Chem., 271, 33686-33692.
14. Ennifar,E., Walter,P., Ehresmann,B., Ehresmann,C. and Dumas,P. (2001) Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nature Struct. Biol., 8, 1064-1068.
15. 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.
16. Otwinowski,Z. and Minor,W. (1996) Processing of X-ray diffraction data collected in oscillation mode. In Carter,C.W.,Jr and Sweet,R.M. (eds), Methods Enzymology. Vol. 276, pp. 307-326.
17. Brünger,A.T., Adams,P.D., Clore,G.M., DeLano,W.L., Gros,P., Grosse-Kunstleve,R.W., Jiang,J.S., Kuszewski,J., Nilges,M., Pannu,N.S. et al. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr., D54, 905-921.
18. Collaborative Computational Project Number 4. (1994) The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr., D50, 760-763.
19. Basu,S., Rambo,R.P., Strauss-Soukup,J., Cate,J.H., Ferré-D'Amaré,A.R., Strobel,S.A. and 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.
20. Tereshko,V., Wilds,C.J., Minasov,G., Prakash,T.P., Maier,M.A., Howard,A., Wawrzak,Z., Manoharan,M. and Egli,M. (2001) Detection of alkali metal ions in DNA crystals using state-of-the-art X-ray diffraction experiments. Nucleic Acids Res., 29, 1208-1215.
21. Ennifar,E., Walter,P. and Dumas,P. (2001) An efficient method for solving RNA structures: MAD phasing by replacing magnesium with zinc. Acta Crystallogr., D57, 330-332.
22. 2+ binding isotherms for nucleic acids using Poisson-Boltzmann theory. J. Mol. Biol., 294, 1135-1147.
23. Westhof,E. (1988) Water: an integral part of nucleic acid structure. Ann. Rev. Biophys. Biophys. Chem., 125-144.
24. Auffinger,P. and Westhof,E. (2000) RNA solvation: a molecular dynamics simulation perspective. Biopolymers, 56, 266-274.
25. Cate,J.H., Gooding,A.R., Podell,E., Zhou,K., Golden,B.L., Kundrot,C.E., Cech,T.R. and Doudna,J.A. (1996) Crystal structure of a group I ribozyme domain: principles of RNA packing. Science, 273, 1678-1685.
26. Wimberly,B.T., Brodersen,D.E., Clemons,W.M.,Jr, Morgan-Warren,R.J., Carter,A.P., Vonrhein,C., Hartsch,T. and Ramakrishnan,V. (2000) Structure of the 30S ribosomal subunit. Nature, 407, 327-339.
27. Cruse,W.B.T., Saludjan,P., Biala,E., Strazewski,P., Prangé,T. and Kennard,O. (1994) Structure of a mispaired RNA double helix at 1.6 Å resolution and implication for the prediction of RNA secondary structure. Proc. Natl Acad. Sci. USA, 91, 4160-4164.
28. Cruse,W., Saludjian,P., Neuman,A. and Prangé,T. (2001) Destabilizing effect of a fluorouracil extra base in a hybrid RNA duplex compared with bromo and chloro analogues. Acta Crystallogr., D57, 1609-1613.
29. Teplova,M., Minasov,G., Tereshko,V., Inamati,G.B., Cook,P.D., Manoharan,M. and Egli,M. (1999) Crystal structure and improved antisense properties of 2′-O-(2-methoxyethyl)-RNA. Nature Struct. Biol., 6, 535-539.
30. Robinson,H., Gao,Y., Sanishvili,R., Joachimiak,A. and Wang,A.H.-J. (2000) Hexahydrated magnesium ions bind in the deep major groove and at the outer mouth of A-form nucleic acid duplexes. Nucleic Acids Res., 28, 1760-1766.
31. 2+(aq) binding sites. J. Inorg. Biochem., 49, 171-175.
32. Shriver,D.F. and Atkins,P.W. (1999) Inorganic Chemistry. Oxford University Press, Oxford.
33. Cate,J.H. and Doudna,J.A. (1996) Metal-binding sites in the major groove of a large ribozyme domain. Structure, 4, 1221-1229.
34. Juneau,K., Podell,E., Harrington,D.J. and Cech,T.R. (2001) Structural basis of the enhanced stability of a mutant ribozyme domain and a detailed view of RNA-solvent interactions. Structure, 9, 221-231.
35. Vargason,J.M., Eichman,B.F. and Ho,P.S. (2000) The extended and eccentric E-DNA structure induced by cytosine methylation or bromination. Nature Struct. Biol., 7, 758-761.
36. Martin,A. and Swaddle,T.W. (1974) Kinetics and mechanism of the thermal decomposition of hexaamminecobalt(III) and aquopentaamminecobalt(III) ions in acidic aqueous solutions. Can. J. Chem., 52, 2751-2759.
37. Ennifar,E., Carpentier,P., Pirocchi,M., Walter,P., Ferrer,J.L. and Dumas,P. (2002) X-ray-induced debromination of nucleic acids at the Br K-absorption edge and implications on MAD-phasing. Acta Crystallogr., D58, 1262-1268.
38. Rupert,P.B. and Ferré-D'Amaré,A.R. (2001) Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature, 410, 780-786.
39. Ippolito,J.A. and Steitz,T.A. (1998) A 1.3-Å resolution crystal structure of the HIV-1 trans-activation response region RNA stem reveals a metal ion-dependent bulge conformation. Proc. Natl Acad. Sci. USA, 95, 9819-9824.
40. Baugh,C., Grate,D. and Wilson,C. (2000) 2.8 Å crystal structure of the malachite green aptamer. J. Mol. Biol., 301, 117-128.
41. Mueller,U., Schubel,H., Sprinzl,M. and Heinemann,U. (1999) Crystal structure of acceptor stem of tRNA(Ala) from Escherichia coli shows unique G·U wobble base pair at 1.16 Å resolution. RNA, 5, 670-677.
42. Perbandt,M., Vallazza,M., Lippmann,C., Betzel,C. and Erdmann,V.A. (2001) Structure of an RNA duplex with an unusual G·C pair in wobble-like conformation at 1.6 Å resolution. Acta Crystallogr., D57, 219-224.
43. 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.
44. Paillart,J.C., Westhof,E., Ehresmann,C., Ehresmann,B. and Marquet,R. (1997) Non-canonical interactions in a kissing loop complex: the dimerization initiation site of HIV-1 genomic RNA. J. Mol. Biol., 270, 36-49.
45. Dahm,S.C., Derrick,W.B. and Uhlenbeck,O.C. (1993) Evidence for the role of solvated metal hydroxide in the hammerhead cleavage mechanism. Biochemistry, 32, 13040-13045.
46. Walter,F., Murchie,A.I., Thomson,J.B. and Lilley,D.M. (1998) Structure and activity of the hairpin ribozyme in its natural junction conformation: effect of metal ions. Biochemistry, 37, 14195-14203.
47. Brown,R.S., Hingerty,B.E., Dewan,J.C. and Klug,A. (1983) Pb(II)-catalysed cleavage of the sugar-phosphate backbone of yeast tRNAPhe - implications for lead toxicity and self-splicing RNA. Nature, 303, 543-546.
48. Wimberly,B.T., Guymon,R., McCutcheon,J.P., White,S.W. and Ramakrishnan,V. (1999) A detailed view of a ribosomal active site: the structure of the L11-RNA complex. Cell, 97, 491-502.
49. Conn,G.L., Gittis,A.G., Lattman,E.E., Misra,V.K. and Draper,D.E. (2002) A compact RNA tertiary structure contains a buried backbone-K+ complex. J. Mol. Biol., 318, 963-973.
50. Marcus,Y. (1988) Ionic radii in aqueous solutions. Chem. Rev., 88, 1475-1498.
51. Batey,R.T., Rambo,R.P., Lucast,L., Rha,B. and Doudna,J.A. (2000) Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science, 287, 1232-1239.
52. Kim,S.H., Shin,W.C. and Warrant,R.W. (1985) Heavy metal ion-nucleic acid interaction. Methods Enzymol., 114, 156-167.
53. Kosturko,L.D., Folzer,C. and Stewart,R.F. (1974) The crystal and molecular structure of a 2:1 complex of 1-methylthymine-mercury (II). Biochemistry, 13, 3949-3952.
54. Katz,S. (1963) The reversible reaction of Hg(II) and double-stranded polynucleotides. A step-function theory and its significance. Biochim. Biophys. Acta, 68, 240-253.
55. Sabbioni,E., Blanch,N., Baricevic,K. and Serra,M.A. (1999) Effects of trace metal compounds on HIV-1 reverse transcriptase: an in vitro study. Biol. Trace Elem. Res., 68, 107-119.
56. Pearson,R.G. (1963) Hard and soft acids and bases. J. Am. Chem. Soc., 85, 3533-3539.
57. Jack,A., Ladner,J.E., Rhodes,D., Brown,R.S. and Klug,A. (1977) A crystallographic study of metal-binding to yeast phenylalanine transfer RNA. J. Mol. Biol., 111, 315-328.
58. Scott,W.G., Murray,J.B., Arnold,J.R.P., Stoddard,B.L. and Klug,A. (1996) Capturing the structure of a catalytic RNA intermediate: the hammerhead ribozyme. Science, 274, 2065-2069.
59. Murray,J.B., Terwey,D.P., Maloney,L., Karpeisky,A., Usman,N., Beigelman,L. and Scott,W.G. (1998) The structural basis of hammerhead ribozyme self-cleavage. Cell, 92, 665-673.