The bulge region of HIV-1 TAR RNA binds metal ions in solution

Nucleic Acids Research

Volumn 30, Issue 19, 2002, Pages 4241-4249

  Olejniczak, Mikołaj ^a   Gdaniec, Zofia ^a   Fischer, Artur ^a   Grabarkiewicz, Tomasz ^a   Bielecki, Łukasz ^a   Adamiak, Ryszard W ^a  

^a POLISH ACADEMY OF SCIENCES   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; COBALT COMPLEX; FLUOROURIDINE; LEAD; LIGAND; MAGNESIUM ION; OLIGORIBONUCLEOTIDE; VIRUS RNA;

BINDING AFFINITY; CHEMICAL BOND; CHEMICAL LABELING; CONTROLLED STUDY; DISSOCIATION CONSTANT; HUMAN IMMUNODEFICIENCY VIRUS 1; METAL BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; RNA CLEAVAGE; RNA SEQUENCE; RNA STRUCTURE; SIMULATION; SYNTHESIS; TITRIMETRY;

ARGININE; BINDING SITES; BINDING, COMPETITIVE; CALCIUM; COBALT; FLUORINE; FLUOROURACIL; GENE PRODUCTS, TAT; HIV-1; HUMANS; MAGNESIUM; MAGNETIC RESONANCE SPECTROSCOPY; METALS; NUCLEIC ACID CONFORMATION; RNA, VIRAL;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0036798069     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkf541     Document Type: Review

References (58)

1. Teeter, M.M., Quigley, G.J. and Rich, A. (1980) Metal ions and transfer RNA. In Spiro, T.G. (ed.), Nucleic Acid-Metal Ion Interactions. Wiley, New York, pp. 145-177.
2. Feig, A.L. and Uhlenbeck, O.C. (1999) The role of metal ions in RNA biochemistry. In Gesteland, R.F., Cech, T. and Atkins, J.F. (eds), The RNA World. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 287-319.
3. Cate, J.H., Gooding, A.R., Podell, E., Zhou, K.H., 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.
4. Misra, V.K. and Draper, D.E. (1998) On the role of magnesium ions in RNA stability. Biopolymers, 48, 113-135.
5. 2+ binding to RNA. Proc. Natl Acad. Sci. USA, 98, 12456-12461.
6. 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.
7. Jovine, L., Djordjevic, S. and Rhodes, D. (2000) The crystal structure of yeast phenylalanine tRNA at 2.0 Å resolution: cleavage by Mg(2+) in 15-year old crystals. J. Mol. Biol., 301, 401-414.
8. Scott, W.G., Murray, J.B., Arnold, J.R., Stoddard, B.L. and Klug, A. (1996) Capturing the structure of a catalytic RNA intermediate: the hammerhead ribozyme. Science, 274, 2065-2069.
9. Cate, J.H., Hanna, R.L. and Doudna, J.A. (1997) A magnesium ion core at the heart of a ribozyme domain. Nature Struct. Biol., 4, 553-558.
10. 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.
11. 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.
12. Kieft, J.S. and Tinoco, I. (1997) Solution structure of a metal-binding site in the major groove of RNA complexed with cobalt (III) hexammine. Structure, 5, 713-721.
13. Gonzalez, R.L. and Tinoco, I. (2001) Identification and characterization of metal ion binding sites in RNA. Methods Enzymol., 338, 421-443.
14. Hardin, C.C., Gollnick, P., Kallenbach, N.R., Cohn, M. and Horowitz, J. (1986) Fluorine-19 nuclear magnetic resonance studies of the structure of 5-fluorouracil-substituted Escherichia coli transfer RNA. Biochemistry, 25, 5699-5709.
15. Chu, W.C., Kintanar, A. and Horowitz, J. (1992) Correlations between fluorine-19 nuclear magnetic resonance chemical shift and the secondary and tertiary structure of 5-fluorouracil-substituted tRNA. J. Mol. Biol., 227, 1173-1181.
16. Sahasrabudhe, P.V., Pon, R.T. and Gmeiner, W.H. (1995) Effects of site-specific substitution of 5-fluorouridine on the stabilities of duplex DNA and RNA. Nucleic Acids Res., 23, 3916-3921.
17. Fischer, A., Gdaniec, Z., Biala, E., Lozynski, M., Milecki, J. and Adamiak, R.W. (1996) F-19 NMR of RNA. The structural and chemical aspects of 5- fluoro-cytidine and -uridine labelling of oligoribonucleotides. Nucl. Nucl., 15, 477-488.
18. Kanyo, J.E., Duhamel, J. and Lu, P.Z. (1996) Secondary structure of the r(CUUCGG) tetraloop. Nucleic Acids Res., 24, 4015-4022.
19. Arnold, J.R.P. and Fisher, J. (2000) Structural equilibria in RNA as revealed by F-19 NMR. J. Biomol. Struct. Dyn., 17, 843-856.
20. Hammann, C., Norman, D.G. and Lilley, D.M.J. (2001) Dissection of the ion-induced folding of the hammerhead ribozyme using F-19 NMR. Proc. Natl Acad. Sci. USA, 98, 5503-5508.
21. Ciesiolka, J., Wrzesinski, J., Gornicki, P., Podkowinski, J. and Krzyzosiak, W.J. (1989) Analysis of magnesium, europium and lead binding sites in methionine initiator and elongator tRNAs by specific metal-ion-induced cleavages. Eur. J. Biochem., 186, 71-77.
22. Polacek, N. and Barta, A. (1998) Metal ion probing of rRNAs: evidence for evolutionarily conserved divalent cation binding pockets. RNA, 4, 1282-1294.
23. Matysiak, M. Wrzesinski, J. and Ciesiolka, J. (1999) Sequential folding of the genomic ribozyme of the hepatitis delta virus: structural analysis of RNA transcription intermediates. J. Mol. Biol., 291, 283-294.
24. Kazakov, S. and Altman, S. (1991) Site-specific cleavage by metal ion cofactors and inhibitors of M1 RNA, the catalytic subunit of RNase P from Escherichia coli. Proc. Natl Acad. Sci. USA, 88, 9193-9197.
25. Streicher, B., von Ahsen, U. and Schroeder, R. (1993) Lead cleavage sites in the core structure of group I intron-RNA. Nucleic Acids Res., 21, 311-317.
26. Ciesiolka, J. (1999) Metal ion-induced cleavages in probing of RNA structure. In Barciszewski, J. and Clarke, B.F.C. (eds), RNA Biochemistry and Biotechnology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 111-121.
27. Streicher, B. Westhof, E. and Schroeder, R (1996) The environment of two metal ions surrounding the splice site of a group I intron. EMBO J., 15, 2556-2564.
28. Winter, D., Polacek, N., Halama, I., Streicher, B. and Barta, A. (1997) Lead-catalysed specific cleavage of ribosomal RNAs. Nucleic Acids Res., 25, 1817-1824.
29. 19F-NMR and modelling studies. Nucleic Acids Symp. Ser., 42, 117-118.
30. Gdaniec, Z., Sierzputowska-Gracz, H. and Theil, E.C. (1998) Iron regulatory element and internal loop/bulge structure for ferritin mRNA studied by cobalt(III) hexammine binding, molecular modeling, and NMR spectroscopy. Biochemistry, 37, 1505-1512.
31. Hermann, T. and Westhof, E. (1998) Exploration of metal ion binding sites in RNA folds by Brownian-dynamics simulations. Struct. Fold. Des., 6, 1303-1314.
32. Jossinet, F., Paillart, J.C., Westhof, E., Hermann, T., Skripkin, E., Lodmell, J.S. Ehresmann, C., Ehresmann, B. and Marquet, R. (1999) Dimerization of HIV-1 genomic RNA of subtypes A and B: RNA loop structure and magnesium binding. RNA, 5, 1222-1234.
33. van Buuren, B.N.M., Hermann, T., Wijmenga, S.S. and Westhof, E. (2002) Brownian-dynamics simulations of metal-ion binding to four-way junctions. Nucleic Acids Res., 30, 507-514.
34. Jones, K.A. and Peterlin, B.M. (1994) Control of RNA initiation and elongation at the HIV-1 promoter. Annu. Rev. Biochem., 63, 717-743.
35. Hamy, F., Felder, E.R., Heizmann, G., Lazdins, J., Aboul-ela, F., Varani, G., Karn, J. and Klimkait, T. (1997) An inhibitor of the Tat/TAR RNA interaction that effectively suppresses HIV-1 replication. Proc. Natl Acad. Sci. USA, 94, 3548-3553.
36. Aboul-ela, F., Karn, J. and Varani, G. (1996) Structure of HIV-1 TAR RNA in the absence of ligands reveals a novel conformation of the trinucleotide bulge. Nucleic Acids Res., 24, 3974-3981.
37. Aboul-ela, F., Karn, J. and Varani, G. (1995) The structure of the human immunodeficiency virus type-1 TAR RNA reveals principles of RNA recognition by Tat protein. J. Mol. Biol., 253, 313-332.
38. Nifosi, R., Reyes, C.M. and Kollman, P.A. (2000) Molecular dynamics studies of the HIV-1 TAR and its complex with argininamide. Nucleic Acids Res., 28, 4944-4955.
39. Puglisi, J.D., Tan, R., Calnan, B.J., Frankel, A.D. and Williamson, J.R. (1992) Conformation of the TAR RNA-arginine complex by NMR spectroscopy. Science, 257, 76-80.
40. Long, K-S. and Crothers, D.M. (1999) Characterization of the solution conformations of unbound and Tat peptide-bound forms of HIV-1 TAR RNA. Biochemistry, 38, 10059-10069.
41. Faber, C., Sticht, H., Schweimer, K. and Rosch, P. (2000) Structural rearrangements of HIV-1 Tat-responsive RNA upon binding of neomycin B. J. Biol. Chem., 275, 20660-20666.
42. Hermann, T. and Westhof, E. (1999) Docking of cationic antibiotics to negatively charged pockets in RNA folds. J. Med Chem., 42, 1250-1261.
43. Al-Hashimi, H.M., Gosser, Y., Gorin, A., Majumdar, W.H.A. and Patel, D.J. (2002) Concerted motions in HIV-1 TAR RNA may allow access to bound state conformations: RNA dynamics from NMR residual dipolar couplings. J. Mol. Biol., 315, 95-102.
44. Ippolito, J.A. and Steitz, T.A (1998) A 1.3-angstrom 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.
45. Zacharias, M. and Hagerman, P.J. (1995) The bend in RNA created by the trans-activation response element bulge of human immunodeficiency virus is straightened by arginine and by Tat-derived peptide. Proc. Natl Acad. Sci. USA, 92, 6052-6056.
46. Arzumanov, A, Godde, F, Moreau, S., Toulme, J.J., Weeds, A. and Gait, M.J. (2000) Use of the fluorescent nucleoside analogue benzo[g]quinazoline 2′-O-methyl-beta-D-ribofuranoside to monitor the binding of the HIV-1 Tat protein or of antisense oligonucleotides to the TAR RNA stem-loop. Helv. Chim. Acta, 83, 1424-1436.
47. Usman, N., Ogilvie, K.K., Jiang, M.-Y. and Cedergren, R.J. (1987) Automated chemical synthesis of long oligoribonucleotides using 2′-O-silylated ribonucleotide 3′-O-phosphoramidites on a controlled-pore glass support: synthesis of a 43-nucleotide sequence similar to the 3′ half of an Escherichia coli formylmethionine tRNA. J. Am. Chem. Soc., 109, 7845-7854.
48. Fielding, L. (2000) Determination of association constants (K-a) from solution NMR data Tetrahedron, 56, 6151-6170.
49. Gonzalez, R.L. and Tinocol, I. (1999) Solution structure and thermodynamics of a divalent metal ion binding site in an RNA pseudoknot. J. Mol. Biol., 289, 1267-1282.
50. Madura, J.D., Davis, M.E., Gilson, M.K., Wade, R.C., Luty, B.A. and McCammon, J.A. (1994) Biological applications of electrostatic calculations and Brownian-dynamics simulations. Rev. Comp. Chem., 5, 229-267.
51. Sahasrabudhe, P.V. and Gmeiner, W.H. (1997) Solution structures of 5-fluorouracil-substituted RNA duplexes containing G-U wobble base pairs. Biochemistry, 36, 5981-5991.
52. Colmenarejo, G. and Tinoco, I. (1999) Structure and thermodynamics of metal binding in the P5 helix of a group I intron ribozyme. J. Mol. Biol., 290, 119-135.
53. Traut, T.W. (1994) Physiological concentrations of purines and pyrimidines. Mol. Cell. Biochem., 140, 1-22.
54. Cowan, J.A. (1993) Metallobiochemistry of RNA Co(NH3)6(3+) as a probe for Mg2+(aq) binding sites. J. Inorg. Biochem, 49, 171-175.
55. Butcher, S.E., Allain, F.H.T. and Feigon, J. (2000) Determination of metal ion binding sites within the hairpin ribozyme domains by NMR. Biochemistry, 39, 2174-2182.
56. Rudisser, S. and Tinoco, I. (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.
57. Kierzek, R. (2001) Nonezymatic cleavage of oligoribonucleotides. Methods Enzymol., 341, 657-675.
58. Kaukinen, U., Lyytikainen, S., Mikkola, S. and Lonnberg, H. (2002) The reactivity of phosphodiester bonds within linear single-stranded oligoribonucleotides is strongly dependent on the base sequence. Nucleic Acids res., 30, 468-474.