Distinct reaction pathway promoted by non-divalent-metal cations in a tertiary stabilized hammerhead ribozyme

RNA

Volumn 13, Issue 6, 2007, Pages 841-848

  Roychowdhury Saha, Manami ^a,c   Burke, Donald H ^a,b  

^a INDIANA UNIVERSITY   (United States)

^b University of Missouri   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Catalytic mechanism; Cobalt hexammine; Divalent cations; Hammerhead ribozymes

Indexed keywords

HAMMERHEAD RIBOZYME; MAGNESIUM ION; METAL ION; SODIUM ION; SPERMIDINE;

ARTICLE; CATALYSIS; ION TRANSPORT; MOLECULAR INTERACTION; PRIORITY JOURNAL; RNA ANALYSIS; RNA BINDING; RNA STABILITY; SIGNAL TRANSDUCTION;

BASE SEQUENCE; BINDING, COMPETITIVE; CATIONS; COBALT; KINETICS; MAGNESIUM; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; RNA STABILITY; RNA, CATALYTIC; SODIUM; SPERMIDINE;

EID: 34249059298     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.339207     Document Type: Article

References (55)

1. Akashi, H., Kawasaki, H., Kim, W.J., Akaike, T., Taira, K., and Maruyama, A. 2002. Enhancement in the cleavage activity of a hammerhead ribozyme by cationic comb-type polymers and an RNA helicase in vitro. J. Biochem. 131: 687-692.
2. Alam, S., Grum-Tokars, V., Krucinska, J., Kundracik, M.L., and Wedekind, J.E. 2005. Conformational heterogeneity at position U37 of an all-RNA hairpin ribozyme with implications for metal binding and the catalytic structure of the S-turn. Biochemistry 44: 14396-14408.
3. Basolo, F. and Pearson, R.G. 1988. Mechanisms of inorganic reactions. Wiley, New York.
4. 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.
5. Canny, M.D., Jucker, F.M., Kellogg, E., Khvorova, A., Jayasena, S.D., and Pardi, A. 2004. Fast cleavage kinetics of a natural hammerhead ribozyme. J. Am. Chem. Soc. 126: 10848-10849.
6. Cho, B.R. and Burke, D.H. 2006. Topological rearrangement yields structural stabilization and interhelical distance constraints in the Kin.46 self-phosphorylating ribozyme. RNA 12: 2118-2125.
7. Curtis, E.A. and Bartel, D.P. 2001. The hammerhead cleavage reaction in monovalent cations. RNA 7: 546-552.
8. Dahm, S.C. and Uhlenbeck, O.C. 1991. Role of divalent metal ions in the hammerhead RNA cleavage reaction. Biochemistry 30: 9464-9469.
9. De la Pena, M., Gago, S., and Flores, R. 2003. Peripheral regions of natural hammerhead ribozymes greatly increase their self-cleavage activity. EMBO J. 22: 5561-5570.
10. Earnshaw, D.J. and Gait, M.J. 1998. Hairpin ribozyme cleavage catalyzed by aminoglycoside antibiotics and the polyamine spermine in the absence of metal ions. Nucleic Acids Res. 26: 5551-5561.
11. Gonzalez, R.L. and Tinoco, I. 1999. Solution structure and thermodynamics of a divalent metal ion binding site in an RNA pseudoknot. J. Mol. Biol. 289: 1267-1282.
12. Hammann, C. and Lilley, D.M.J. 2002. Folding and activity of the hammerhead ribozyme. ChemBioChem 3: 691-700.
13. Hampel, A. and Cowan, J.A. 1997. A unique mechanism for RNA catalysis: The role of metal cofactors in hairpin ribozyme cleavage. Chem. Biol. 4: 513-517.
14. Hampel, K.J. and Burke, J.M. 2003. Solvent protection of the hammerhead ribozyme in the ground state: Evidence for a cation-assisted conformational change leading to catalysis. Biochemistry 42: 4421-4429.
15. Han, J. and Burke, J.M. 2005. Model for general acid-base catalysis by the hammerhead ribozyme: pH-activity relationships of G8 and G12 variants at the putative active site. Biochemistry 44: 7864-7870.
16. Heckman, J.E., Lambert, D., and Burke, J.M. 2005. Photo-crosslinking detects a compact, active structure of the hammerhead ribozyme. Biochemistry 44: 4148-4156.
17. Horton, T.E. and DeRose, V.J. 2000. Cobalt hexammine inhibition of the hammerhead ribozyme. Biochemistry 39: 11408-11416.
18. Hunsicker, L.M. and DeRose, V.J. 2000. Activities and relative affinities of divalent metals in unmodified and phosphorothioate-substituted hammerhead ribozymes. J. Inorg. Biochem. 80: 271-281.
19. Khvorova, A., Lescoute, A., Westhof, E., and Jayasena, S.D. 2003. Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat. Struct. Biol. 10: 708-712.
20. 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.
21. Kim, N.K., Murali, A., and DeRose, V.J. 2005. Separate metal requirements for loop interactions and catalysis in the extended hammerhead ribozyme. J. Am. Chem. Soc. 127: 14134-14135.
22. Koculi, E., Lee, N.K., Thirumalai, D., and Woodson, S.A. 2004. Folding of the Tetrahymena ribozyme by polyamines: Importance of counterion valence and size. J. Mol. Biol. 341: 27-36.
23. Lambert, D., Heckman, J.E., and Burke, J.M. 2006a. Cation-specific structural accommodation within a catalytic RNA. Biochemistry 45: 829-838.
24. Lambert, D., Heckman, J.E., and Burke, J.M. 2006b. Three conserved guanosines approach the reaction site in native and minimal hammerhead ribozymes. Biochemistry 45: 7140-7147.
25. Maderia, M., Hunsicker, L.M., and DeRose, V.J. 2000. Metalphosphate interactions in the hammerhead ribozyme observed by P-31 NMR and phosphorothioate substitutions. Biochemistry 39: 12113-12120.
26. Maguire, J.L. and Collins, R.A. 2001. Effects of cobalt hexammine on folding and self-cleavage of the Neurospora VS ribozyme. J. Mol. Biol. 309: 45-56.
27. Martick, M. and Scott, W.G. 2006. Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126: 309-320.
28. Mikulecky, P.J., Takach, J.C., and Feig, A.L. 2004. Entropy-driven folding of an RNA helical junction: An isothermal titration calorimetric analysis of the hammerhead ribozyme. Biochemistry 43: 5870-5881.
29. 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.
30. Nakano, S., Chadalavada, D.M., and Bevilacqua, P.C. 2000. General acid-base catalysis in the mechanism of a hepatitis δ virus ribozyme. Science 287: 1493-1497.
31. Nakano, S., Proctor, D.J., and Bevilacqua, P.C. 2001. Mechanistic characterization of the HDV genomic ribozyme: Assessing the catalytic and structural contributions of divalent metal ions within a multichannel reaction mechanism. Biochemistry 40: 12022-12038.
32. Nakano, S., Cerrone, A.L., and Bevilacqua, P.C. 2003. Mechanistic characterization of the HDV genomic ribozyme: Classifying the catalytic and structural metal ion sites within a multichannel reaction mechanism. Biochemistry 42: 2982-2994.
33. Nelson, J.A., Shepotinovskaya, I., and Uhlenbeck, O.C. 2005. Hammerheads derived from sTRSV show enhanced cleavage and ligation rate constants. Biochemistry 44: 14577-14585.
34. Nixon, P.L., Theimer, C.A., and Giedroc, D.P. 1999. Thermodynamics of stabilization of RNA pseudoknots by cobalt(III) hexaammine. Biopolymers 50: 443-458.
35. 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.
36. Osborne, E.M., Schaak, J.E., and DeRose, V.J. 2005. Characterization of a native hammerhead ribozyme derived from schistosomes. RNA 11: 187-196.
37. Penedo, J.C., Wilson, T.J., Jayasena, S.D., Khvorova, A., and Lilley, D.M. 2004. Folding of the natural hammerhead ribozyme is enhanced by interaction of auxiliary elements. RNA 10: 880-888.
38. Peracchi, A., Beigelman, L., Scott, E.C., Uhlenbeck, O.C., and Herschlag, D. 1997. Involvement of a specific metal ion in the transition of the hammerhead ribozyme to its catalytic conformation. J. Biol. Chem. 272: 26822-26826.
39. Pley, H.W., Flaherty, K.M., and McKay, D.B. 1994. Three-dimensional structure of a hammerhead ribozyme. Nature 372: 68-74.
40. Roychowdhury-Saha, M. and Burke, D.H. 2006. Extraordinary rates of transition metal ion-mediated ribozyme catalysis. RNA 12: 1846-1852.
41. Rudisser, S. and Tinoco, I. 2000. Solution structure of cobalt(III)hexammine complexed to the GAAA tetraloop, and metal-ion binding to G center dot A mismatches. J. Mol. Biol. 295: 1211-1223.
42. 2+ ions slightly reorient stems I and II of the hammerhead ribozyme to increase the probability of formation of the catalytic core. Biochemistry 42: 9924-9936.
43. Rupert, P.B. and Ferre-D'Amare, A.R. 2001. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410: 780-786.
44. Saksmerprome, V., Roychowdhury-Saha, M., Jayasena, S., Khvorova, A., and Burke, D.H. 2004. Artificial tertiary motifs stabilize trans-cleaving hammerhead ribozymes under conditions of submillimolar divalent ions and high temperatures. RNA 10: 1916-1924.
45. 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.
46. Suga, H., Cowan, J.A., and Szostak, J.W. 1998. Unusual metal ion catalysis in an acyl-transferase ribozyme. Biochemistry 37: 10118-10125.
47. Suh, Y.A., Kumar, P.K.R., Taira, K., and Nishikawa, S. 1993. Self-cleavage activity of the genomic Hdv ribozyme in the presence of various divalent metal ions. Nucleic Acids Res. 21: 3277-3280.
48. Takagi, Y., Inoue, A., and Taira, K. 2004. Analysis on a cooperative pathway involving multiple cations in hammerhead reactions. J. Am. Chem. Soc. 126: 12856-12864.
49. Tuschl, T., Gohlke, C., Jovin, T.M., Westhof, E., and Eckstein, F. 1994. A three-dimensional model for the hammerhead ribozyme based on fluorescence measurements. Science 266: 785-789.
50. Vogt, M., Hunsicker, L., Cosper, N., Scott, R., and DeRose, V.J. 2003. Spectroscopic probes for metals and catalysis in the hammerhead ribozyme. Biophys. J. 84: 180A-181A.
51. Wang, S.L., 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.
52. Wedekind, J.E. and McKay, D.B. 1998. Crystallographic structures of the hammerhead ribozyme: Relationship to ribozyme folding and catalysis. Annu. Rev. Biophys. Biomol. Struct. 27: 475-502.
53. Yen, L., Svendsen, J., Lee, J.S., Gray, J.T., Magnier, M., Baba, T., D'Amato, R.J., and Mulligan, R.C. 2004. Exogenous control of mammalian gene expression through modulation of RNA selfcleavage. Nature 431: 471-476.
54. Zamel, R., Poon, A., Jaikaran, D., Andersen, A., Olive, J., De Abreu, D., and Collins, R.A. 2004. Exceptionally fast self-cleavage by a Neurospora Varkud satellite ribozyme. Proc. Natl. Acad. Sci. 101: 1467-1472.
55. Zhou, J.M., Zhou, D.M., Takagi, Y., Kasai, Y., Inoue, A., Baba, T., and Taira, K. 2002. Existence of efficient divalent metal ion-catalyzed and inefficient divalent metal ion-independent channels in reactions catalyzed by a hammerhead ribozyme. Nucleic Acids Res. 30: 2374-2382.