Visualizing metal-ion-binding sites in group I introns by iron(II)-mediated Fenton reactions

Chemistry and Biology

Volumn 5, Issue 3, 1998, Pages 163-175

  Berens, Christian ^a,b   Streicher, Barbara ^b   Schroeder, Renée ^b   Hillen, Wolfgang ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Fenton chemistry; Group I intron; Metal ion binding site; Ribozyme

Indexed keywords

EID: 0032033759     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(98)90061-8     Document Type: Article

References (78)

1. Pan, T., Long, D.M. & Uhlenbeck, O.C. (1993) Divalent metal ions in RNA folding and catalysis. In The RNA World (Gesteland, R.F. & Atkins, J.F., eds), pp. 271-302, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
2. Pyle, A.M. (1993). Ribozymes: A distinct class of metalloenzymes. Science 261, 709-714.
3. Yarus, M. (1993). How many catalytic RNAs? Ions and the Cheshire cat conjecture. FASEB J. 7, 31-39.
4. Streicher, B. & Wailis, M.G. (1996) Metal ions as the key to the functioning of both the group I intron and the ribosome. In Ribosomal RNA and Group I Introns (Green, R. & Schroeder, R., eds), pp. 103-128, R.G. Landes, Austin.
5. Phe. J. Mol. Biol. 111, 315-318.
6. Pley, H.W., Flaherty, K.M. & McKay, D.B. (1994). Three-dimensional structure of a hammerhead ribozyme. Nature 372, 68-74.
7. Scott, W.G., Murray, J.B., Arnold, J.R.P., Stoddard, B.L & Klug, A. (1996). Capturing the structure of a catalytic RNA intermediate: the hammerhead ribozyme. Science 274, 2065-2069.
8. Cate, J.H., et al., & Doudna, J.A. (1996). Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 273, 1678-1685.
9. 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.
10. Dahm, S.C. & Uhlenbeck, O.C. (1991). Role of divalent metal ions in the hammerhead RNA cleavage reaction. Biochemistry 30, 9464-9469.
11. Christian, E.L & Yarus, M. (1993). Metal coordination sites that contribute to structure and catalysis in the group I intron from Tetrahymena. Biochemistry 32, 4475-4480.
12. Harris, M.E. & Pace, N.R. (1995). Identification of phosphates involved in catalysis by the ribozyme RNase P RNA. RNA 1, 210-218.
13. Cate, J.H., Hanna, R.L. & Doudna, J.A. (1997). A magnesium ion core at the heart of a ribozyme domain. Nat. Struct. Biol. 4, 553-558.
14. Phe - implications for lead toxicity and self-splicing RNA. Nature 303, 543-546.
15. Phe by specific metal ion-induced cleavages. FEBS Lett. 243, 293-298.
16. Streicher, B., von Ahsen, U. & Schroeder, R. (1993). Lead cleavage sites in the core structure of group I intron-RNA. Nucleic Acids Res. 21, 311-317.
17. Zito, K., Hüttenhofer, A. & Pace, N.R. (1993). Lead-catalyzed cleavage of ribonuclease P RNA as a probe for integrity of tertiary structure. Nucleic Acids Res. 21, 5916-5920.
18. Streicher, B., Westhof, E. & Schroeder, R. (1996). The environment of two metals ions surrounding the splice site of a group I intron. EMBO J. 15, 2556-2564.
19. Bassi, G.S., Mallegaard, N.E., Murchie, A.I., von Kitzing, E. & Lilley, D.M. (1995). Ionic interactions and the global conformations of the hammerhead ribozyme. Nat. Struct. Biol. 2, 45-55.
20. Celander, D.W. & Cech, T.R. (1991). Visualizing the higher order folding of a catalytic RNA molecule. Science 251, 401-407.
21. Brown, I.B. (1988). What factors determine cation coordination numbers? Acta Crystallogr. Sect. B 44, 545-553.
22. Glusker, J.P. (1991). Structural aspects of metal liganding to functional groups in proteins. Adv. Protein Chem. 42, 1-76.
23. Udenfried, S., Clark, C.T., Axelrod, J. & Brodie, R.B. (1954). Ascorbic acid in aromatic hydroxylation I. A model system for aromatic hydroxylation. J. Biol. Chem. 208, 731-739.
24. Burkhoff, A.M. & Tullius, T.D. (1987). The unusual conformation adopted by the adenine tracts in kinetoplast DNA. Cell 48, 935-943.
25. Tullius, T.D. & Dombroski, B.A. (1985). Iron(II) EDTA used to measure the helical twist along any DNA molecule. Science 230, 679-681.
26. Tullius, T.D. & Dombroski, B.A. (1986). Hydroxyl radical 'footprinting': high-resolution information about DNA-protein contacts and application to lambda repressor and Cro protein. Proc. Natl Acad. Sci. USA 83, 5469-5473.
27. Powers, T. & Noller, H.F. (1995). Hydroxyl radical footprinting of ribosomal proteins on 16S rRNA. RNA 1, 194-209.
28. Hertzberg, R.P. & Dervan, P.B. (1984). Cleavage of DNA with Methidiumpropyl-EDTA-Iron(II): reaction conditions and product analyses. Biochemistry 23, 3934-3945.
29. Mah, S.C., Townsend, C.A. & Tullius, T.D. (1994). Hydroxyl radical footprinting of calicheamicin. Relationship of DNA binding to cleavage. Biochemistry 33, 614-621.
30. Latham, J.A. & Cech, T.R. (1989). Defining the inside and outside of a catalytic RNA molecule. Science 245, 276-282.
31. Farber, J.M. & Levine, R.L. (1986). Sequence of a peptide susceptible to mixed-function oxidation. Probable cation binding site in glutamine synthetase. J. Biol. Chem. 261, 4574-4578.
32. Wei, C.H., Chou, W.Y. & Chang, G.G. (1995). Identification of Asp258 as the metal coordinate of pigeon liver malic enzyme by site-specific mutagenesis. Biochemistry 34, 7949-7954.
33. Mustaev, A., Kozlov, M., Markovtsov, V., Zaychikov, E., Denissova, L & Goldfarb, A. (1997). Modular organization of the catalytic center of RNA polymerase. Proc. Natl Acad. Sci. USA 94, 6641-6645.
34. 2+-isocitrate. J. Biol. Chem. 268, 5264-5271.
35. 2+ complex by hydrogen peroxide mediated protein cleavage. Biochemistry 34, 22-31.
36. Zaychikov, E., et al., & Mustaev, A. (1996). Mapping of catalytic residues in the RNA polymerase active center. Science 273, 107-109.
37. Lykke-Andersen, J., Garrett, R.A. & Kjems, J. (1997). Mapping metal ions at the catalytic centres of two intron-encoded endonucleases. EMBO J. 16, 3272-3281.
38. Grosshans, C.A. & Cech, T.R. (1989). Metal ion requirements for sequence-specific endoribonuclease activity of the Tetrahymena ribozyme. Biochemistry 28, 6888-6894.
39. Wang, J.-F. & Cech, T.R. (1992). Tertiary structure around the guanosine-binding site of the Tetrahymena ribozyme. Science 256, 526-529.
40. Zhong, M. & Kallenbach, N.R. (1994). Mapping tRNA and 5S RNA tertiary structures by charge dependent Fe(II)-catalyzed cleavage. J. Biomol. Struct. Dyn. 11, 901-911.
41. Christian, E.L. & Yarus, M. (1992). Analysis of the role of phosphate oxygens in the group I intron from Tetrahymena. J. Mol. Biol. 228, 743-758.
42. Piccirilli, J.A., Vyle, J.S., Caruthers, M.H. & Cech, T.R. (1993). Metal ion catalysis in the Tetrahymena ribozyme reaction. Nature 361, 85-88.
43. Sjögren, A.S., Pettersson, E., Sjöberg, B.M. & Strömberg, R. (1997). Metal ion interaction with cosubstrate in self-splicing of group I introns. Nucleic Acids Res. 25, 648-653.
44. McConnell, T.S., Herschlag, D. & Cech, T.R. (1997). Effects of divalent metal ions on individual steps of the Tetrahymena ribozyme reaction. Biochemistry 36, 8293-8303.
45. Weinstein, L.B., Jones, B.C.N.M., Cosstick, R. & Cech, T.R. (1997). A second catalytic metal ion in a group I ribozyme. Nature 388, 805-808.
46. Jaeger, L., Westhof, E. & Michel, F. (1993). Monitoring of the cooperative unfolding of the sunY group I intron of bacteriophage T4. The active form of the sun Y ribozyme is stabilized by multiple interactions with 3′ terminal intron components. J. Mol. Biol. 234, 331-346.
47. Lehnert, V., Jaeger, L., Michel, F. & Westhof, E. (1996). New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. Chem. Biol. 3, 993-1009.
48. Cate, J.H. & Doudna, J.A. (1996). Metal-binding sites in the major groove of a large ribozyme domain. Structure 4, 1221-1229.
49. Heuer, T.S., Chandry, P.S., Belfort, M., Celander, D.W. & Cech, T.R. (1991). Folding of group I introns from bacteriophage T4 involves internalization of the catalytic core. Proc. Natl Acad. Sci. USA 88, 11105-11109.
50. Galloway Salvo, J.L., Coetzee, T. & Belfort, M. (1990). Deletiontolerance and trans-splicing of the bacteriophage T4 td intron: Analysis of the P6-L6a region. J. Mol. Biol. 211, 537-549.
51. Wank, H. & Schroeder, R. (1996). Antibiotic-induced oligomerisation of group I intron RNA. J. Mol. Biol. 258, 53-61.
52. Inoue, T. & Cech, T.R. (1985). Secondary structure of the circular form of the Tetrahymena rRNA intervening sequence: a technique for RNA structure analysis using chemical probes and reverse transcriptase. Proc. Natl Acad. Sci. USA 82, 648-652.
53. Michel, F., et al., & Shub, D.A. (1992). Activation of the catalytic core of a group I intron by a remote 3′ splice junction. Genes Dev. 6, 1373-1385.
54. Brenowitz, M.D., Senear, D.F., Shea, M.A. & Ackers, G.K. (1986). Quantitative DNase I footprint titration: a method for studying protein-DNA interactions. Methods Enzymol. 130, 132-181.
55. Brown, R.S., Dewan, J.C. & Klug, A. (1985). Crystallographic and biochemical investigation of the lead(II)-catalyzed hydrolysis of yeast phenylalanine tRNA. Biochemistry 24, 4785-4801.
56. Phe mutants. Biochemistry 29, 2515-2523.
57. Rogers, J., Chang, A.H., von Ahsen, U., Schroeder, R. & Davies, J. (1996). Inhibition of the self-cleavage reaction of the human hepatitis delta virus ribozyme by antibiotics. J. Mol. Biol. 259, 916-925.
58. Tullius, T.D., Dombroski, B.A., Churchill, M.E. & Kam, L. (1987). Hydroxyl radical footprinting: a high-resolution method for mapping protein-DNA contacts. Methods Enzymol. 155, 537-558.
59. Celander, D.W. & Cech, T.R. (1990). Iron(II)-Ethylenediaminetetraacetic acid catalyzed cleavage of RNA and DNA oligonucleotides: similar reactivity toward single- and double-stranded forms. Biochemistry 29, 1355-1361.
60. Brunel, C., Romby, P., Westhof, E., Ehresmann, C. & Ehresmann, B. (1991). Three-dimensional model of Escherichia coli ribosomal 5 S RNA as deduced from structure probing in solution and computer modeling. J. Mol. Biol. 221, 293-308.
61. Michel, F. & Westhof, E. (1990). Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol. 216, 585-610.
62. Laggerbauer, B., Murphy, F.L. & Cech, T.R. (1994). Two major tertiary folding transitions of the Tetrahymena catalytic RNA. EMBO J. 13, 2669-2676.
63. Jaeger, L., Michel, F. & Westhof, E. (1994). Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J. Mol. Biol. 236, 1271-1276.
64. 2+, and in the presence of substrate. Biochemistry 29, 10147-10158.
65. Pyle, A.M., Murphy, F.L & Cech, T.R. (1992). RNA substrate binding site in the catalytic core of the Tetrahymena ribozyme. Nature 358, 123-128.
66. Williamson, C.L., Tierney, W.M., Kerker, B.J. & Burke, J.M. (1987). Site-directed mutagenesis of core sequence elements 9R′, 9L, 9R, and 2 in self-splicing Tetrahymena pre-rRNA. J. Biol. Chem. 262, 14672-14682.
67. Kieft, J.S. & Tinoco, I. (1997). Solution structure of a metal-binding site in the major groove of RNA complexed with cobalt (III) hexammine. Structures 5, 713-721.
68. Prigodich, R.V. & Martin, C.T. (1990). Reaction of single-stranded DNA with hydroxyl radical generated by Iron(II)-Ethylenediaminetetraacetic acid. Biochemistry 29, 8017-8019.
69. Henle, E.S., Luo, Y., Gassmann, W. & Linn, S. (1996). Oxidative damage to DNA constituents by iron-mediated Fenton reactions. The deoxyguanosine family. J. Biol. Chem. 271, 21177-21186.
70. Luo, Y., Henle, E.S. & Linn, S. (1996). Oxidative damage to DNA constituents by iron-mediated Fenton reactions. The deoxycytidine family. J. Biol. Chem. 271, 21167-21176.
71. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual (2nd edn.). Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
72. Lingner, J. & Keller, W. (1993). 3′-end labeling of RNA with recombinant yeast poly(A) polymerase. Nucleic Acids Res. 21, 2917-2920.
73. Donis-Keller, H., Maxam, A.M. & Gilbert, W. (1977). Mapping adenines, guanines and pyrimidines in RNA. Nucleic Acids Res. 4, 2527-2538.
74. Been, M.D. & Cech, T.R. (1986). One binding site determines sequence specificity of Tetrahymena pre-rRNA self-splicing, transsplicing, and RNA enzyme activity. Cell 47, 207-216.
75. Inoue, T., Sullivan, F.X. & Cech, T.R. (1986). New reactions of the ribosomal RNA precursor of Tetrahymena and the mechanism of self-splicing. J. Mol. Biol. 189, 143-165.
76. Burke, J.M., et. al., & Tabak, H.W. (1987). Structural conventions for group I introns. Nucleic Acids Res. 15, 7217-7221.
77. Cech, T.R., Damberger, S.H. & Gutell, R.R. (1994). Representation of the secondary and tertiary structure of group I introns. Nat. Struct. Biol. 1, 273-280.
78. Richmond, T.J. (1984). Solvent accessible surface area and excluded volume in proteins. Analytical equations for overlapping spheres and implications for the Hydrophobic effect. J. Mol. Biol. 178, 63-89.