Tertiary structure formation in the hairpin ribozyme monitored by fluorescence resonance energy transfer

EMBO Journal

Volumn 17, Issue 8, 1998, Pages 2378-2391

  Walter, Nils G ^a   Hampel, Ken J ^a   Brown, Kirk M ^a   Burke, John M ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

Catalytic RNA; Domain docking; Metal ions; Reaction mechanism; RNA folding

Indexed keywords

RIBOZYME; RNA;

ARTICLE; CONFORMATIONAL TRANSITION; FLUORESCENCE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE;

BASE COMPOSITION; BINDING SITES; GUANINE; HYDROGEN-ION CONCENTRATION; MAGNESIUM; METALS; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA, CATALYTIC; SPECTROMETRY, FLUORESCENCE; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 0032522574     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.8.2378     Document Type: Article

References (62)

1. Anderson,P., Monforte,J., Tritz,R., Nesbitt,S., Hearst,J. and Hampel,A. (1994) Mutagenesis of the hairpin ribozyme. Nucleic Acids Res., 22, 1096-1100.
2. Banerjee,A.R., Jaeger,J.A. and Turner,D.H. (1993) Thermal unfolding of a group I ribozyme: the low-temperature transition is primarily disruption of tertiary structure. Biochemistry, 32, 153-163.
3. Bassi,G.S., Murchie,A.I.H., Walter,F., Clegg,R.M. and Lilley,D.M.J. (1997) Ion-induced folding of the hammerhead ribozyme: a fluorescence resonance energy transfer study. EMBO J., 16, 7481-7489.
4. Berzal-Herranz,A., Joseph,S., Chowrira,B.M., Butcher,S.E. and Burke,J.M. (1993) Essential nucleotide sequences and secondary structure elements of the hairpin ribozyme. EMBO J., 12, 2567-2574.
5. Bevilacqua,P.C., Kierzek,R., Johnson,K.A. and Turner,D.H. (1992) Dynamics of ribozyme binding of substrate revealed by fluorescence-detected stopped-flow methods. Science, 258, 1355-1358.
6. Bjornson,K.P., Amaratunga,M., Moore,K.J.H. and Lohmann,T.M. (1994) Single-turnover kinetics of helicase-catalyzed DNA unwinding monitored continuously by fluorescence energy transfer. Biochemistry, 33, 14306-14316.
7. Burke,J.M., Butcher,S.E. and Sargueil,B. (1996) Structural analysis and modifications of the hairpin ribozyme. Nucleic Acids Mol. Biol., 10 129-143.
8. 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.
9. Butcher,S.E., Heckman,J.E. and Burke,J.M. (1995) Reconstitution of hairpin ribozyme activity following separation of functional domains J. Biol. Chem., 270, 29648-29651.
10. Buzayan,J.M., Gerlach,W.L. and Bruening,G. (1986) Non-enzymatic cleavage and ligation of RNAs complementary to a plant virus satellite RNA. Nature, 323, 349-353.
11. Cate,J.H., Gooding,A.R., Podell,E., Zhou,K., 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.
12. 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.
13. Chowrira,B.M. and Burke,J.M. (1992) Extensive phosphorothioate substitution yields highly active and nuclease-resistant hairpin ribozymes. Nucleic Acids Res., 20, 2835-2840.
14. Chowrira,B.M., Berzal-Herranz,A. and Burke,J.M. (1991) Novel guanosine requirement for catalysis by the hairpin ribozyme. Nature, 354, 320-322.
15. Chowrira,B.M., Berzal-Herranz,A. and Burke,J.M. (1993a) Ionic requirements for RNA binding, cleavage, and ligation by the hairpin ribozyme. Biochemistry, 32, 1088-1095.
16. Chowrira,B.M., Berzal-Herranz,A., Keller,C.F. and Burke,J.M. (1993b) Four ribose 2′-hydroxyl groups essential for catalytic function of the hairpin ribozyme. J. Biol. Chem., 268. 19458-19462.
17. DeYoung,M.B., Siwkowski,A.M., Lian,Y. and Hampel,A. (1995) Catalytic properties of hairpin ribozymes derived from chicory yellow mottle virus and arabis mosaic virus satellite RNAs. Biochemistry, 34, 15785-15791.
18. Downs,W.D. and Cech,T.R. (1996) Kinetic pathway for folding of the Tetrahymena ribozyme revealed by three UV-inducible crosslinks. RNA, 2, 718-732.
19. Draper,D.E. (1996) Parallel worlds. Nature Struct. Biol., 3, 397-400.
20. Earnshaw,D.J. and Gait,M.J. (1997) Progress toward the structure and therapeutic use of the hairpin ribozyme. Antisense Nucleic Acid Drug Dev., 7, 403-41.
21. Earnshaw,D.J., Masquida,B., Müller,S., Sigurdsson,S.T., Eckstein,F., Westhof,E. and Gait,M.J. (1997) Inter-domain cross-linking and molecular modelling of the hairpin ribozyme. J. Mol. Biol., 247, 1-16.
22. Emerick,V.L., Pan,J. and Woodson,S.A. (1996) Analysis of rate-determining conformational changes during self-splicing of the Tetrahymena intron. Biochemistry, 35, 13469-13477.
23. Esteban,J.A., Banerjee,A.R. and Burke,J.M. (1997) Kinetic mechanism of the hairpin ribozyme. Identification and characterization of two nonexchangeable conformations. J. Biol. Chem., 272, 13629-13639.
24. Esteban,J.A., Walter,N.G., Kotzorek,G., Heckman,J.E. and Burke,J.M. (1998) Structural basis for heterogeneous kinetics: Re-engineering the hairpin ribozyme. Proc. Natl Acad. Sci. USA, in press.
25. Feldstein,P.A. and Bruening,G. (1993) Catalytically active geometry in the reversible circularization of mini-monomer RNAs derived from the complementary strand of tobacco ringspot virus satellite RNA. Nucleic Acids Res., 21, 1991-1998.
26. Feldstein,P.A., Buzayan,J.M. and Bruening,G. (1989) Two sequences participating in the autocatalytic processing of satellite tobacco ringspot virus complementary RNA. Gene, 82, 53-61.
27. Grainger,R.J., Murchie,A.I.H. and Lilley,D.M.J. (1998) Exchange between stacking conformers in a four-way DNA junction. Biochemistry, 37, 23-32.
28. 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.
29. Hampel,A. and Tritz,R. (1989) RNA catalytic properties of the minimum (-)sTRSV sequence. Biochemistry, 28, 4929-4933.
30. Hegg,L.A. and Fedor,M.J. (1995) Kinetics and thermodynamics of intermolecular catalysis by hairpin ribozymes. Biochemistry, 34, 15813-15828.
31. Johnson,K.A. (1992) Transient-state kinetic analysis of enzyme reaction pathways. In Sigman,D. (ed.), The Enzymes. Vol. 20. Academic Press, New York, NY, pp. 1-61.
32. Komatsu,Y., Koizumi,M., Nakamura,H. and Ohtsuka,E. (1994) Loop-size variation to probe a bent structure of a hairpin ribozyme. J. Am. Chem, Soc., 116, 3692-3696.
33. Lakowicz,J.R. (1983) Principles of Fluorescence Spectroscopy. Plenum Press, New York, NY.
34. Long,D.M. and Uhlenbeck,O.C. (1993) Self-cleaving catalytic RNA. FASEB J., 7, 25-30.
35. Miick,S.M., Fee,R.S., Millar,D.P. and Chazin,W.J. (1997) Crossover isomer bias is the primary sequence-dependent property of immobilized Holliday junctions. Proc. Natl Acad. Sci. USA, 94, 9080-9084.
36. Morrison,L.E. and Stols,L.M. (1993) Sensitive fluorescence-based thermodynamic and kinetic measurements of DNA hybridization in solution. Biochemists, 32, 3095-3104.
37. Narlikar,G.J. and Herschlag,D. (1996) Isolation of a local tertiary folding transition in the context of a globally folded RNA. Nature Struct. Biol., 3, 701-710.
38. Nesbitt,S., Hegg,L.A. and Fedor,M.J. (1997) An unusual mechanism for hairpin ribozyme catalysis: pH and metal ion independence. Chem. Biol., 4, 619-630.
39. Pan,J., Thirumalai,D. and Woodson,S.A. (1997) Folding of RNA involves parallel pathways. J. Mol. Biol., 273, 7-13.
40. Pan,T. and Sosnick,T.R. (1997) Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nature Struct. Biol., 4, 931-938.
41. Parkhurst,K.M. and Parkhurst,L.J. (1995) Kinetic studies by fluorescence resonance energy transfer employing a double-labeled oligonucleotide: hybridization to the oligonucleotide complement and a single-stranded DNA. Biochemistry, 34, 285-292.
42. Perkins,T.A., Wolf,D.E. and Goodchild,J. (1996) Fluorescence resonance energy transfer analysis of ribozyme kinetics reveals the mode of action of a facilitator oligonucleotide. Biochemistry, 35, 16370-16377.
43. Sclavi,B., Woodson,S., Sullivan,M., Chance,M.R. and Brenowitz,M. (1997) Time-resolved synchrotron X-ray 'footprinting', a new approach to the study of nucleic acid structure and function: application to protein-DNA interactions and RNA folding. J. Mol. Biol., 266, 144-159.
44. Sclavi,B., Woodson,S., Sullivan,M., Chance,M.R. and Brenowitz,M. (1998) Visualizing RNA folding at millisecond intervals by X-ray footprinting. Science, in press.
45. Sigurdsson,S.T., Thomson,J.B. and Eckstein,F. (1998) Small ribozymes. In Simons,R.W. (ed.), RNA Structure and Function. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 339-376.
46. Song,L., Varma,C.A.G.O., Verhoeven,J.W. and Tanke,H.J. (1996) Influence of the triplet excited state on the photobleaching kinetics of fluorescein in microscopy. Biophys. J., 70, 2959-2968.
47. Sproat,B., Colonna,F., Mullah,B., Tsou,D., Andrus,A., Hample,A. and Vinayak,R. (1995) An efficient method for isolation and purification of oligoribonucleotides. Nucl. Nucl., 14, 255-273.
48. Strobel,S.A. and Cech,T.R. (1994) Translocation of an RNA duplex on a ribozyme. Nature Struct. Biol., 1, 13-17.
49. Szewczak,A.A. and Cech,T.R. (1997) An RNA internal loop acts as a hinge to facilitate ribozyme folding and catalysis. RNA, 3, 838-849.
50. Turner,D.H., Li,Y., Fountain,M., Profenno,L. and Bevilacqua,P.C. (1996) Dynamics of a group I ribozyme detected by spectroscopic methods. Nucleic Acids Mol. Biol., 10, 19-32.
51. Tuschl,T., Gohlke,C., Jovin,T.M., Westhof,E. and Eckstein,E (1994) A three-dimensional model for the hammerhead ribozyme based on fluorescence measurements. Science, 266, 785-789.
52. Walter,N.G. and Burke,J.M. (1997) Real-time monitoring of hairpin ribozyme kinetics through base-specific quenching of fluorescein-labeled substrates. RNA, 3, 392-404.
53. Walter,N.G. and Burke,J.M. (1998) The hairpin ribozyme: structure, assembly and catalysis. Curr. Opin. Chem. Biol., 2, 24-30.
54. Walter,N.G., Albinson,E. and Burke,J.M. (1997) Probing structure formation in the hairpin ribozyme using fluorescent substrate analogs. Nucleic Acids Symp. Ser., 36, 175-177.
55. Welch,P.J., Hampel,A., Barber,J., Wong-Staal,F. and Yu,M. (1996) Inhibition of HIV replication by the hairpin ribozyme. Nucleic Acids Mol. Bio., 10, 315-327.
56. Wincott,F. et al. (1995) Synthesis, deprotection, analysis and purification of RNA and ribozymes. Nucleic Acids Res., 23, 2677-2684.
57. Wu,P. and Brand,L. (1994) Resonance energy transfer: methods and applications. Anal. Biochem., 218, 1-13.
58. Yang,M., Ghosh,S.S. and Millar,D.P. (1994) Direct measurement of thermodynamic and kinetic parameters of DNA triple helix formation by fluorescence Spectroscopy. Biochemistry, 33, 15329-15337.
59. Young,K.J., Gill,F. and Grasby,J.A. (1997) Metal ions play a passive role in the hairpin ribozyme catalysed reaction. Nucleic Acids Res., 25, 3760-3766.
60. Zarrinkar,P.P. and Williamson,J.R. (1994) Kinetic intermediates in RNA folding. Science, 265, 918-924.
61. Zarrinkar,P.P. and Williamson,J.R. (1996) The kinetic folding pathway of the Tetrahymena ribozyme reveals possible similarities between RNA and protein folding. Nature Struct. Biol., 3, 432-438.
62. Zarrinkar,P.P., Wang,J. and Williamson,J.R. (1996) Slow folding kinetics of RNase P RNA. RNA, 2, 564-573.