The structure of a methylated tetraloop in 16s ribosomal RNA

Structure

Volumn 6, Issue 6, 1998, Pages 747-756

  Rife, Jason P ^a   Moore, Peter B ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

16S rRNA; Methylation; NMR; Tetraloops

Indexed keywords

BACTERIA (MICROORGANISMS); EUKARYOTA; GEOBACILLUS STEAROTHERMOPHILUS; PROKARYOTA;

EID: 0032526960     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(98)00076-8     Document Type: Article

References (58)

1. Ehresmann, C., Fellner, P. & Ebel, JP. (1971). The 3′ terminal nucleotide sequence of the 16S ribosomal RNA from Escherichia coli. FEBS Lett. 13, 325-328.
2. Van Charldorp, R., Heus, H.A. & Van Knippenberg, P.H. (1981). 16S ribosomal RNA of Escherichia coli contains a N2-methylguanosine at 27 nucleotides from the 3′ end. Nucleic Acids Res. 9, 2717-2725.
3. Van Knippenberg, P.H., Van Kimmenade, J.M. & Heus, H.A. (1984). Phylogeny of the conserved 3′ terminal structure of the RNA of small ribosomal subunits. Nucleic Acids Res. 12, 2595-2604.
4. Poldermans, B., Bakker, H. & Van Knippenberg, P.H. (1980). Studies on the function of two adjacent N6,N6-dimethyladenosines near the 3' end of 16S ribosomal RNA of Escherichia coli. IV. The effect of the methylgroups on ribosomal subunit interaction. Nucleic Acids Res. 8, 143-151.
5. Poldermans, B., Van Buul, C.P. & Van Knippenberg, P.H. (1979). Studies on the function of two adjacent N6,N6-dimethyladenosines near the 3′ end of 16S ribosomal RNA of Escherichia coli. II. The effect of the absence of the methyl groups on initiation of protein biosynthesis. J. Biol. Chem. 254, 9090-9093.
6. van Knippenberg, P.H. (1986). Structural and functional aspects of the N6,N6 dimethyladenosines in 16S ribosomal RNA. In Structural and Functional Aspects of the N6,N6 Dimethyladenosines in 16S Ribosomal RNA. (Hardesty, B. & Gisela, K., eds), pp. 412-424, Spinger-Verlag, New York.
7. Mitchell, P., Osswald, M. & Brimacombe, R. (1992). Identification of intermolecular RNA cross-links at the subunit interface of the Escherichia coli ribosome. Biochemistry 31, 3004-3011.
8. Heiser, T.L., Davies, J.E. & Dahlberg, J.E. (1971). Change in methylation of 16S ribosomal RNA associated with mutation to kasugamycin resistance in Escherichia coli. Nat. New Biol. 233, 12-14.
9. Helser, T.L., Davies, J.E. & Dahlberg, J.E. (1972). Mechanism of kasugamycin resistance in Escherichia coli. Nat. New Biol 235, 6-9.
10. Lafontaine, D., Delcour, J., Glasser, A.L., Desgres, J. & Vandenhaute, J. (1994). The DIM1 gene responsible for the conserved m6(2)Am6(2)A dimethylation in the 3′-terminal loop of 18 S rRNA is essential in yeast. J. Mol. Biol. 241, 492-497.
11. Strobel, S.A., Cech, T.R., Usman, N. & Beigelman, L. (1994). The 2,6-diaminopurine riboside-5-methylisocytidine wobble base pair: an isoenergetic substitution for the study of G U pairs in RNA. Biochemistry 33, 13824-13835.
12. Rife, J.P., Cheng, C.S., Moore, P.B. & Strobel, S.A. (1998). The synthesis of RNA containing the modified nucleotides N2-methylguanosine and N6,N6-dimethyladenosine. Nucleosides Nucleotides, in press.
13. Heus, H.A., van Kimmenade, J.M., van Knippenberg, P.H., Haasnoot, C.A., de Bruin, S.H. & Hilbers, C.W. (1 983). High-resolution proton magnetic resonance studies of the 3′-terminal colicin fragment of 16S ribosomal RNA from Escherichia coli. Assignment of iminoproton resonances by nuclear Overhauser effect experiments and the influence of adenine dimethylation on the hairpin conformation. J. mol. Biol. 170, 939-956.
14. Heus, H.A., Van Kimmenade, J.M., van Knippenberg, P.H. & Hinz, H.J. (1983). Calorimetric measurements of the destabilisation of a ribosomal RNA hairpin by dimethylation of two adjacent adenosines. Nucleic Acids Res. 11, 203-210.
15. Van Charldorp, R., Heus, H.A., Van Knippenberg, P.H., Joordens, J., De Bruin, S.H. & Hilbers, C.W. (1981). Destabilization of secondary structure in 16S ribosomal RNA by dimethylation of two adjacent adenosines. Nucleic Acids Res. 9, 4413-4422.
16. Heus, H.A., Formenoy, L.J. &Van Knippenberg, P.H. (1990). Conformational and thermodynamic effects of naturally occurring base methylations in a ribosomal RNA hairpin of Bacillus stearothermophilus. Eur. J. Biochem. 188, 275-281.
17. 1H heteronuclear NMR. FEBS Lett. 347, 261-264.
18. Lapham, J., Rife, J.P., Moore, P.B. & Crothers, D.M. (1997). Measurement of diffusion constants for nucleic acids by NMR. J. Biomol. NMR 10, 255-262.
19. Varani, G., Aboul-ela, F. & Allain, F.H.T. (1996). NMR investigation of RNA structure. Prog. Nucl. Magn. Reson. Sp. 29, 51-127.
20. Zwahlen, C., Vincent, S.J.F., Di Bari, L., Levitt, M.H. & Bodenhausen, G. (1994). Quenching spin diffusion in selective measurements of transient Overhauser effects in nuclear magnetic resonance. Applications to oligonucleotides. J. Am. Chem. Soc. 116, 362-368.
21. Vincent, S.J.F., Zwalen, C. & Bodenhausen, G. (1996). Suppression of spin diffusion in selected frequency bands of nuclear Overhauser spectra. J. Biomol. NMR 7, 169-172.
22. 1H resonances in oligonucleotides by two-dimensional NMR spectroscopy. FEBS Lett. 208, 94-98.
23. Kellogg, G.W. (1992). Proton-detected hetero-TOCSY experiments with applications in nucleic acids. J. Magn. Reson. 98, 179-182.
24. 1H resonances in RNA. J. Am. Chem. Soc. 114, 2727-2728.
25. Kim, Y. & Prestegard, J.H. (1989). Measurements of vicinal couplings from cross peaks in COSY spectra. J. Magn. Reson. 84, 9-13.
26. van den Hoogen, F. (1988). NMR Studies Concerning Base-Base Interactions in Oligonucleotides. PhD Thesis, Leiden.
27. Engel, J.D. & von Hippel, P.H. (1978). Effects of methylation on the stability of nucleic acid conformations. Studies at the polymer level. J. Biol. Chem. 253, 927-934.
28. Stein, E.G., Rice, L.M. & Brünger, AT. (1997). Torsional-angle molecular dynamics as a new efficient tool for NMR structure calculation. J. Magn. Reson. 124, 154-164.
29. Rice, L.M. & Brünger, AT. (1994). Torsion angle dynamics: reduced variable conformational sampling enhances crystallographic structure refinement. Proteins 19, 277-290.
30. Stallings, S.C. & Moore, P.B. (1997). The structure of an essential splicing element: stem loop lla from yeast U2 snRNA. Structure 5, 1173-1185.
31. Rich, A. (1977). Three-dimensional structure of transfer RNA. Acc. Chem. Res. 10, 388-402.
32. Ginell, S.L. & Parthasarathy, R. (1978). Conformation of N2-methylguanosine, a modified nucleoside of tRNA. Biochem. Biophys. Res. Commun. 84, 886-894.
33. Pley, H.W., Flaherty, K.M. & McKay, D.B. (1994). Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix. Nature 372, 111-113.
34. Pley, H.W., Flaherty, K.M. & McKay, D.B. (1994). Three-dimensional structure of a hammerhead ribozyme. Nature 372, 68-74.
35. Jucker, P.M. & Pardi, A. (1995). GNRA tetraloops make a U-turn. RNA 1, 219-222.
36. Olsthoorn, C.S., Haasnoot, C.A. & Altona, C. (1980). Circular dichroism studies of 6-N-methylated adenylyladenosine and adenylyluridine and their parent compounds. Thermodynamics of stacking. Eur. J. Biochem. 106, 85-95.
37. Tazawa, I., Koike, T. & Inoue, Y. (1980). Stacking properties of a highly hydrophobic dinucleotide sequence, N6, N6-dimethyladenylyl(3′ leads to 5′)N6, N6-dimethyladenosine, occurring in 16-18S ribosomal RNA. Eur. J. Biochem. 109, 33-38.
38. Varani, G. (1995). Exceptionally stable nucleic acid hairpins. Annu. Rev. Biophys. Biomol. Struct. 24, 379-404.
39. Jucker, F.M., Heus, H.A., Yip, P.P., Moors, E.H. & Pardi, A. (1996). A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. mol. Biol. 264, 968-980.
40. Butcher, S.E., Diekmann, T. & Feigon, J. (1997). Solution structure of the conserved 16 S-like ribosomal RNA UGAA tetraloop. J. mol. Biol. 268, 348-358.
41. Gornicki, P., et al. & Ehresmann, B. (1989). Use of lead(ll) to probe the structure of large RNAs. Conformation of the 3' terminal domain of E. coli 16S rRNA and its involvement in building the tRNA binding sites. J. Biomol. Struct. Dyn. 6, 971-984.
42. Chapman, N.M. & Noller, H.F. (1977). Protection of specific sites in 16S RNA from chemical modification by association of 30S and 50S ribosomes. J. mol. Biol. 109, 131-149.
43. Wickstrom, E. (1983). Nuclease mapping of the secondary structure of the 49-nucleotide 3' terminal cloacin fragment of Escherichia coli 16S RNA and its interactions with initiation factor 3. Nucleic Acids Res. 11, 2035-2052.
44. Heus, H.A. & van Knippenberg, P.H. (1988). The 3′ terminal colicin fragment of Escherichia coli 16S ribosomal RNA. Conformational details revealed by enzymic and chemical probing. J. Biomol. Struct. Dyn. 5, 951-963.
45. Lykke-Anderson, J. & Garrett, R. (1997). RNA-protein interactions of an archaeal homotetrameric splicing endoribonuclease with an exceptional evolutionary history. EMBO J. 16, 6290-6300.
46. Wickstrom, E., Heus, H.A., Haasnoot, C.A. & van Knippenberg, P.H. (1986). Circular dichroism and 500-MHz proton magnetic resonance studies of the interaction of Escherichia coli translational initiation factor 3 protein with the 16S ribosomal RNA 3′ cloacin fragment. Biochemistry 25, 2770-2777.
47. Ehresmann, C., et al. & Ehresmann, B. (1986). Cross-linking of initiation factor IF3 to Escherichia coli 30S ribosomal subunit by transdiamminedichloroplatinum(ll): characterization of two cross-linking sites in 16S rRNA; a possible way of functioning for IF3. Nucleic Acids Res. 14, 4803-4821.
48. Poldermans, B., Goosen, N. & Van Knippenberg, P.H. (1979). Studies on the function of two adjacent N6,N6-dimethyladenosines near the 3′ end of 16S ribosomal RNA of Escherichia coli. I. The effect of kasugamycin on initiation of protein synthesis. J. Biol. Chem. 254, 9085-9089.
49. Milligan, J.F. & Uhlenbeck, O.C. (1989). Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol. 180, 51-62.
50. White, S.A., Nilges, M., Huang, A., Brünger, A.T. & Moore, P.B. (1992). NMR analysis of helix I from the 5S RNA of Escherichia coli. Biochemistry 31, 1610-1621.
51. Dallas, A. & Moore, P.B. (1997). The loop E-loop D region of Escherichia coli 5S rRNA: the solution structure reveals an unusual loop that may be important for binding ribosomal proteins. Structure 5, 1639-1653.
52. Chang, K.-Y. & Tinoco, I., Jr. (1997). The structure of an RNA "kissing" hairpin complex of the HIV TAR hairpin loop and its complement. J. mol. Biol. 269, 52-66.
53. Gorenstein, D.G. (1984). Phosphorus-31 Chemical Shifts: Principles and Empirical Observations. (Gorenstein, D.G., ed.), pp. 7-36, Academic Press, Orlando, FL.
54. Parkinson, G., Vojtechovsky, J., Clowney, L., Brünger, A.T. & Berman, H.M. (1996). New parameters for the refinement of nucleic acid-containing structures. Acta. Cryst. D 52, 57-64.
55. Cornell, W.D., et al. & Kollman, P.A. (1995). A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117, 5179-5197.
56. Saenger, W. (1984). Principles of Nucleic Acid Structure, Springer-Verlag, New York.
57. Padmaja, N., Ramakumar, S. & Viswamitra, M.A. (1988). Structure of puromycin aminoglycosine. Acta Cryst C 44, 2176-2178.
58. MidasPlus. Molecular graphics images were produced using the MidasPlus package from the Computer Graphics Laboratory, University of California, San Francisco.