Solvent protection of the hammerhead ribozyme in the ground state: Evidence for a cation-assisted conformational change leading to catalysis

Biochemistry

Volumn 42, Issue 15, 2003, Pages 4421-4429

  Hampel, Ken J ^a   Burke, John M ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HAMMERHEAD RIBOZYMES;

CATALYSIS; CONFORMATIONS; CRYSTAL STRUCTURE; GROUND STATE; POSITIVE IONS; SOLVENTS; TITRATION;

BIOCHEMISTRY;

CATION; HYDROXYL RADICAL; LITHIUM ION; MAGNESIUM ION; METAL ION; NUCLEOTIDE; RIBOZYME;

ARTICLE; BINDING AFFINITY; CALCULATION; CATALYSIS; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA CLEAVAGE; DNA FOOTPRINTING; ENZYME ANALYSIS; ENZYME CONFORMATION; GENE CONSTRUCT; GENE SEQUENCE; LYSIS; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN FOLDING; SHARK; STRUCTURE ACTIVITY RELATION; TITRIMETRY;

MAGNESIUM; NUCLEIC ACID CONFORMATION; RNA, CATALYTIC; SOLVENTS;

CHONDRICHTHYES;

EID: 0037461285     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi020659c     Document Type: Article

References (57)

1. Buzayan, J. M., Gerlach, W. L., and Breuning, G. (1986) Nonenzymatic cleavage and ligation of RNAs complementary to a plant virus satellite RNA, Nature 323, 349-353.
2. Epstein, L. M., and Gall, J. G. (1987) Self-cleaving transcripts of satellite DNA from the newt, Cell 48, 535-543.
3. Ferbeyre, G., Smith, J. M., and Cedergren, R. (1998) Schistosome satellite DNA encodes active hammerhead ribozymes, Mol. Cell. Biol. 18, 3880-3888.
4. Ferbeyre, G., Bourdeau, V., Pageau, M., Miramontes, P., and Cedergren, R. (2000) Distribution of hammerhead and hammerhead-like RNA motifs through the GenBank, Genome Res. 10, 1011-1019.
5. Salehi-Ashtiani, K., and Szostak, J. W. (2001) In vitro evolution suggests multiple origins for the hammerhead ribozyme, Nature 414, 82-84.
6. Hutchins, C. J., Rathjen, P. D., Forster, A. C., and Symons, R. H. (1986) Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid, Nucleic Acids Res. 14, 3627-3640.
7. Forster, A. C., and Symons, R. H. (1987) Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites, Cell 49, 211-220.
8. 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.
9. Hertel, K. J., and Uhlenbeck, O. C. (1995) The internal equilibrium of the hammerhead ribozyme reaction, Biochemistry 34, 1744-1749.
10. Stage-Zimmermann, T. K., and Uhlenbeck, O. C. (1998) Hammerhead ribozyme kinetics, RNA 4, 875-889.
11. Murray, J. B., Dunham, C. M., and Scott, W. G. (2002) A pH-dependent conformational change, rather than the chemical step, appears to be rate-limiting in the hammerhead ribozyme cleavage reaction, J. Mol. Biol. 315, 121-130.
12. Ruffner, D. E., Stormo, G. D., and Uhlenbeck, O. C. (1990) Sequence requirements of the hammerhead RNA self-cleavage reaction, Biochemistry 29, 10695-10702.
13. Pley, H. W., Flaherty, K. M., and McKay, D. B. (1994) Three-dimensional structure of a hammerhead ribozyme, Nature 372, 68-74.
14. Scott, W. G., Finch, J. T., and Klug, A. (1995) The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage, Cell 81, 991-1002.
15. Bassi, G. S., Mollegaard, N. E., Murchie, A. I., von Kitzing, E., and Lilley, D. M. (1995) Ionic interactions and the global conformations of the hammerhead ribozyme, Nat. Struct. Biol. 2, 45-55.
16. Bassi, G. S., Murchie, A. I., Walter, F., Clegg, R. M., and Lilley, D. M. (1997) Ion-induced folding of the hammerhead ribozyme: a fluorescence resonance energy transfer study, EMBO J. 16, 7481-7489.
17. Sigurdsson, S. T., Tuschl, T., and Eckstein, F. (1995) Probing RNA tertiary structure: interhelical crosslinking of the hammerhead ribozyme, RNA 1, 575-583.
18. Stage-Zimmermann, T. K., and Uhlenbeck, O. C. (2001) A covalent cross-link converts the hammerhead ribozyme from a ribonuclease to an RNA ligase, Nat. Struct. Biol. 8, 863-867.
19. Amiri, K. M., and Hagerman, P. J. (1994) Global conformation of a self-cleaving hammerhead RNA, Biochemistry 33, 13172-13177.
20. Fu, D. J., and McLaughlin, L. W. (1992) Importance of specific purine amino and hydroxyl groups for efficient cleavage by a hammerhead ribozyme, Proc. Natl. Acad. Sci. U.S.A. 89, 3985-3989.
21. Bassi, G. S., Murchie, A. I., and Lilley, D. M. (1996) The ion-induced folding of the hammerhead ribozyme: core sequence changes that perturb folding into the active conformation, RNA 2, 756-768.
22. Dahm, S. C., and Uhlenbeck, O. C. (1991) Role of divalent metal ions in the hammerhead RNA cleavage reaction, Biochemistry 30, 9464-9469.
23. Murray, J. B., Seyhan, A. A., Walter, N. G., Burke, J. M., and Scott, W. G. (1998) The hammerhead, hairpin and VS ribozymes are catalytically proficient in monovalent cations alone, Chem. Biol. 5, 587-595.
24. Curtis, E. A., and Bartel, D. P. (2001) The hammerhead cleavage reaction in monovalent cations, RNA 7, 546-552.
25. O'Rear, J. L., Wang, S., Feig, A. L., Beigelman, L., Uhlenbeck, O. C., and Herschlag, D. (2001) Comparison of the hammerhead cleavage reactions stimulated by monovalent and divalent cations, RNA 7, 537-545.
26. 2+-dependent conformational changes in the hammerhead ribozyme, Biochemistry 35, 14710-14716.
27. Wang, S., Karbstein, K., Peracchi, A., Beigelman, L., and Herschlag, D. (1999) Identification of the hammerhead ribozyme metal ion binding site responsible for rescue of the deleterious effect of a cleavage site phosphorothioate, Biochemistry 38, 14363-14378.
28. Russell, R., and Herschlag, D. (1999) New pathways in folding of the Tetrahymena group I RNA enzyme, J. Mol. Biol. 291, 1155-1167.
29. Woisard, A., Fourrey, J. L., and Favre, A. (1994) Multiple folded conformations of a hammerhead ribozyme domain under cleavage conditions, J. Mol. Biol. 239, 366-370.
30. Wang, L., and Ruffner, D. E. (1997) An ultraviolet crosslink in the hammerhead ribozyme dependent on 2-thiocytidine or 4-thiouridine substitution, Nucleic Acids Res. 25, 4355-4361.
31. Galas, D. J., and Schmitz, A. (1978) DNAse foot-printing: a simple method for the detection of protein-DNA binding specificity, Nucleic Acids Res. 5, 3157-3170.
32. Ehresmann, C., Baudin, F., Mougel, M., Romby, P., Ebel, J. P., and Ehresmann, B. (1987) Probing the structure of RNAs in solution, Nucleic Acids Res. 15, 9109-9128.
33. Krol, A., and Carbon, P. (1989) A guide for probing native small nuclear RNA and ribonucleoprotein structures, Methods Enzymol. 180, 212-227.
34. Sclavi, B., Sullivan, M., Chance, M. R., Brenowitz, M., and Woodson, S. A. (1998) RNA folding at millisecond intervals by synchrotron hydroxyl radical foot-printing, Science 279, 1940-1943.
35. Rose, M. A., and Weeks, K. M. (2001) Visualizing induced fit in early assembly of the human signal recognition particle, Nat. Struct. Biol. 8, 515-520.
36. Latham, J. A., and Cech, T. R. (1989) Defining the inside and outside of a catalytic RNA molecule, Science 245, 276-282.
37. Hampel, K. J., Walter, N. G., and Burke, J. M. (1998) The solvent-protected core of the hairpin ribozyme-substrate complex, Biochemistry 37, 14672-14682.
38. Hampel, K. J., and Burke, J. M. (2001) A conformational change in the "loop E-like" motif of the hairpin ribozyme is coincidental with domain docking and is essential for catalysis, Biochemistry 40, 3723-3729.
39. Walter, N. G., Yang, N., and Burke, J. M. (2000) Probing nonselective cation binding in the hairpin ribozyme with Tb(III), J. Mol. Biol. 298, 539-555.
40. Butcher, S. E., and Burke, J. M. (1994) A photo-cross-linkable tertiary structure motif found in functionally distinct RNA molecules is essential for catalytic function of the hairpin ribozyme, Biochemistry 33, 992-999.
41. Hampel, K. J., and Burke, J. M. (2001) Time-resolved hydroxyl-radical foot-printing of RNA using Fe(II)-EDTA, Methods 23, 233-239.
42. Hertel, K. J., Herschlag, D., and Uhlenbeck, O. C. (1994) A kinetic and thermodynamic framework for the hammerhead ribozyme reaction, Biochemistry 33, 3374-3385.
43. Clouet-D'Orval, B., and Uhlenbeck, O. C. (1996) Kinetic characterization of two I/II format hammerhead ribozymes, RNA 2, 483-491.
44. Scott, W. G., Finch, J. T., Grenfell, R., Fogg, J., Smith, T., Gait, M. J., and Klug, A. (1995) Rapid crystallization of chemically synthesized hammerhead RNAs using a double screening procedure, J. Mol. Biol. 250, 327-332.
45. Bassi, G. S., Mollegaard, N. E., Murchie, A. I., and Lilley, D. M. (1999) RNA folding and misfolding of the hammerhead ribozyme. Biochemistry 38, 3345-3354.
46. Amiri, K. M., and Hagerman, P. J. (1996) The global conformation of an active hammerhead RNA during the process of self-cleavage, J. Mol. Biol. 261, 125-134.
47. 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.
48. Walter, N. G., Burke, J. M., and Millar, D. P. (1999) Stability of hairpin ribozyme tertiary structure is governed by the interdomain junction, Nat. Struct. Biol. 6, 544-549.
49. Walter, N. G., Hampel, K. J., Brown, K. M., and Burke, J. M. (1998) Tertiary structure formation in the hairpin ribozyme monitored by fluorescence resonance energy transfer, EMBO J. 17, 2378-2391.
50. Zhuang, X., Kim, H., Pereira, M. J., Babcock, H. P., Walter, N. G., and Chu, S. (2002) Correlating structural dynamics and function in single ribozyme molecules. Science 296, 1473-1476.
51. Clouet-d'Orval, B., and Uhlenbeck, O. C. (1997) Hammerhead ribozymes with a faster cleavage rate, Biochemistry 36, 9087-9092.
52. 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.
53. Feig, A. L., Scott, W. G., and Uhlenbeck, O. C. (1998) Inhibition of the hammerhead ribozyme cleavage reaction by site-specific binding of Tb, Science 279, 81-84.
54. Hansen, M. R., Simorre, J. P., Hanson, P., Mokler, V., Bellon, L., Beigelman, L., and Pardi, A. (1999) Identification and characterization of a novel high affinity metal-binding site in the hammerhead ribozyme, RNA 5, 1099-1104.
55. Maderia, M., Hunsicker, L. M., and DeRose, V. J. (2000) Metal-phosphate interactions in the hammerhead ribozyme observed by 31P NMR and phosphorothioate substitutions, Biochemistry 39, 12113-12120.
56. Murray, J. B., and Scott, W. G. (2000) Does a single metal ion bridge the A-9 and scissile phosphate groups in the catalytically active hammerhead ribozyme structure?, J. Mol. Biol. 296, 33-41.
57. Hertel, K. J., Pardi, A., Uhlenbeck, O. C., Koizumi, M., Ohtsuka, E., Uesugi, S., Cedergren, R., Eckstein, F., Gerlach, W. L., Hodgson, R., and Symons, R. H. (1992) Numbering system for the hammerhead, Nucleic Acids Res. 20, 3252.