Folding of the hammerhead ribozyme: Pyrrolo-cytosine fluorescence separates core folding from global folding and reveals a pH-dependent conformational change

RNA

Volumn 18, Issue 3, 2012, Pages 434-448

  Buskiewicz, Iwona A ^a   Burke, John M ^a  

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

Author keywords

Catalytic RNA; Hammerhead ribozyme; Pyrrolo cytosine; RNA folding

Indexed keywords

CYTOSINE; HAMMERHEAD RIBOZYME;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; EQUILIBRIUM CONSTANT; FLUORESCENCE; MUTATIONAL ANALYSIS; PH; PRIORITY JOURNAL; PROTEIN FOLDING;

BASE PAIRING; BASE SEQUENCE; CATALYTIC DOMAIN; CYTOSINE; FLUORESCENT DYES; HYDROGEN-ION CONCENTRATION; KINETICS; MUTATION; PYRROLES; RNA FOLDING; RNA, CATALYTIC;

EID: 84857431262     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.030999.111     Document Type: Article

References (69)

1. Bassi GS, Murchie AI, Walter F, Clegg RM, Lilley DM. 1997. Ion-induced folding of the hammerhead ribozyme: A fluorescence resonance energy transfer study. EMBO J 16: 7481-7489. (Pubitemid 28010507)
2. Berry DA, Jung K-Y, Wise DS, Sercel AD, Pearson WH, Mackie H, Randolph JB, Somers RL. 2004. Pyrrolo-dC and pyrrolo-C: Fluorescent analogs of cytidine and 2′-deoxycytidine for the study of oligonucleotides. Tetrahedron Lett 45: 2457-2461. (Pubitemid 38230354)
3. Bevilacqua PC, Brown TS, Chadalavada D, Lecomte J, Moody E, Nakano SI. 2005. Linkage between proton binding and folding in RNA: Implications for RNA catalysis. Biochem Soc Trans 33: 466-470. (Pubitemid 40873866)
4. Boots JL, Canny MD, Azimi E, Pardi A. 2008. Metal ion specificities for folding and cleavage activity in the Schistosoma hammerhead ribozyme. RNA 14: 2212-2222.
5. Brahms J, Maurizot JC, Michelson AM. 1967. Conformational stability of dinucleotides in solution. J Mol Biol 25: 481-495.
6. Brown D. 1971. Fused pyrimidines. Part II: Purines. Wiley, New York.
7. Butcher SE, Burke JM. 1994. Structure-mapping of the hairpin ribozyme. Magnesium-dependent folding and evidence for tertiary interactions within the ribozyme-substrate complex. J Mol Biol 244: 52-63.
8. Canny MD, Jucker FM, Kellogg E, Khvorova A, Jayasena SD, Pardi A. 2004. Fast cleavage kinetics of a natural hammerhead ribozyme. J Am Chem Soc 126: 10848-10849. (Pubitemid 39180563)
9. Carbonell A, De la Pena M, Flores R, Gago S. 2006. Effects of the trinucleotide preceding the self-cleavage site on eggplant latent viroid hammerheads: Differences in co- and post-transcriptional self-cleavage may explain the lack of trinucleotide AUC in most natural hammerheads. Nucleic Acids Res 34: 5613-5622. (Pubitemid 44742448)
10. Chartrand P, Harvey SC, Ferbeyre G, Usman N, Cedergren R. 1995. An oligodeoxyribonucleotide that supports catalytic activity in the hammerhead ribozyme domain. Nucleic Acids Res 23: 4092-4096.
11. Chi YI, Martick M, Lares M, Kim R, Scott WG, Kim SH. 2008. Capturing hammerhead ribozyme structures in action by modulating general base catalysis. PLoS Biol 6: e234. doi: 10.1371/journal.pbio.0060234.
12. Clouet-D'Orval B, Uhlenbeck OC. 1996. Kinetic characterization of two I/II format hammerhead ribozymes. RNA 2: 483-491. (Pubitemid 26374242)
13. Clouet-d'Orval B, Uhlenbeck OC. 1997. Hammerhead ribozymes with a faster cleavage rate. Biochemistry 36: 9087-9092. (Pubitemid 27329492)
14. Dash C, Rausch JW, Le Grice SF. 2004. Using pyrrolo-deoxycytosine to probe RNA/DNA hybrids containing the human immunodeficiency virus type-1 3′ polypurine tract. Nucleic Acids Res 32: 1539-1547. (Pubitemid 38864681)
15. De la Pena M, Gago S, Flores R. 2003. Peripheral regions of natural hammerhead ribozymes greatly increase their self-cleavage activity. EMBO J 22: 5561-5570. (Pubitemid 37279965)
16. Doudna JA, Cormack BP, Szostak JW. 1989. RNA structure, not sequence, determines the 5′ splice-site specificity of a group I intron. Proc Natl Acad Sci 86: 7402-7406. (Pubitemid 19254465)
17. Edwards EL, Patrick MH, Ratliff RL, Gray DM. 1990. A.T and C.C+ base pairs can form simultaneously in a novel multistranded DNA complex. Biochemistry 29: 828-836. (Pubitemid 20041969)
18. Ferbeyre G, Smith JM, Cedergren R. 1998. Schistosome satellite DNA encodes active hammerhead ribozymes.Mol Cell Biol 18: 3880-3888. (Pubitemid 28287911)
19. Flores R, Hernandez C, de la Pena M, Vera A, Daros JA. 2001. Hammerhead ribozyme structure and function in plant RNA replication. Methods Enzymol 341: 540-552. (Pubitemid 32928548)
20. Forster AC, Symons RH. 1987. Self-cleavage of virusoid RNA is performed by the proposed 55-nucleotide active site. Cell 50: 9-16.
21. Fu DJ, McLaughlin LW. 1992. Importance of specific purine amino and hydroxyl groups for efficient cleavage by a hammerhead ribozyme. Proc Natl Acad Sci 89: 3985-3989.
22. Gray DM, Cui T, Ratliff RL. 1984. Circular dichroism measurements show that C.C+ base pairs can coexist with A.T base pairs between antiparallel strands of an oligodeoxynucleotide double-helix. Nucleic Acids Res 12: 7565-7580.
23. Guschlbauer W. 1975. Protonated polynucleotide structures. 16. Thermodynamics of the melting of the acid form of polycytidylic acid. Nucleic Acids Res 2: 353-360.
24. Hammann C, Lilley DM. 2002. Folding and activity of the hammerhead ribozyme. ChemBioChem 3: 690-700. (Pubitemid 36004508)
25. Hampel KJ, Burke JM. 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. (Pubitemid 36457610)
26. Han J, Burke JM. 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. (Pubitemid 40740769)
27. Hardman SJ, Botchway SW, Thompson KC. 2008. Evidence for a nonbase stacking effect for the environment-sensitive fluorescent base pyrrolocytosine-comparison with 2-aminopurine. Photochem Photobiol 84: 1473-1479.
28. Heckman JE, Lambert D, Burke JM. 2005. Photocrosslinking detects a compact, active structure of the hammerhead ribozyme. Biochemistry 44: 4148-4156. (Pubitemid 40403954)
29. Hertel KJ, Pardi A, Uhlenbeck OC, Koizumi M, Ohtsuka E, Uesugi S, Cedergren R, Eckstein F, Gerlach WL, Hodgson R, et al. 1992. Numbering system for the hammerhead. Nucleic Acids Res 20: 3252.
30. Howard FB, Miles HT. 1984. 2NH2A X T helices in the ribo- and deoxypolynucleotide series. Structural and energetic consequences of 2NH2A substitution. Biochemistry 23: 6723-6732.
31. Howard FB, Frazier J, Singer MF, Miles HT. 1966. Helix formation between polyribonucleotides and purines, purine nucleosides and nucleotides. II. J Mol Biol 16: 415-439.
32. Johnson KA. 1992. The enzymes. In Transient state kinetic analysis of enzyme reaction pathways. pp. 1-61. Academic Press, San Diego.
33. Jorgensen WL, Pranata J. 1990. Importance of secondary interactions in triply hydrogen bonded complexes: Guanine cytosine vs uracil-2,6- diaminopyridine. J Am Chem Soc 112: 2008-2010. (Pubitemid 20217130)
34. Kelley SO, Barton JK. 1999. Electron transfer between bases in double helical DNA. Science 283: 375-381.
35. Khvorova A, Lescoute A, Westhof E, Jayasena SD. 2003. Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat Struct Biol 10: 708-712. (Pubitemid 37052408)
36. Kim NK, Murali A, DeRose VJ. 2005. Separate metal requirements for loop interactions and catalysis in the extended hammerhead ribozyme. J Am Chem Soc 127: 14134-14135. (Pubitemid 41457549)
37. Knitt DS, Narlikar GJ, Herschlag D. 1994. Dissection of the role of the conserved G·U pair in group I RNA self-splicing. Biochemistry 33: 13864-13879. (Pubitemid 24381951)
38. ++ ions to polyadenylate, polyuridylate, and their complexes. Biopolymers 10: 2459-2490.
39. Kyogoku Y, Lord RC, Rich A. 1967. The effect of substituents on the hydrogen bonding of adenine and uracil derivatives. Proc Natl Acad Sci 57: 250-257.
40. Lambert D, Heckman JE, Burke JM. 2006. Three conserved guanosines approach the reaction site in native and minimal hammerhead ribozymes. Biochemistry 45: 7140-7147. (Pubitemid 43877402)
41. 2+ in hammerhead ribozyme catalysis from molecular simulation. J Am Chem Soc 130: 3053-3064.
42. Martick M, Scott WG. 2006. Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126: 309-320. (Pubitemid 44092962)
43. Martick M, Lee TS, York DM, Scott WG. 2008. Solvent structure and hammerhead ribozyme catalysis. Chem Biol 15: 332-342. (Pubitemid 351508433)
44. Masquida B, Westhof E. 2000. On the wobble GoU and related pairs. RNA 6: 9-15. (Pubitemid 30069032)
45. McDowell SE, Jun JM, Walter NG. 2010. Long-range tertiary interactions in single hammerhead ribozymes bias motional sampling toward catalytically active conformations. RNA 16: 2414-2426.
46. Muraoka M, Miles HT, Howard FB. 1980. Copolymers of adenylic and 2-aminoadenylic acids. Effect of progressive changes in hydrogen bonding and stacking on interaction with poly(uridylic acid). Biochemistry 19: 2429-2439. (Pubitemid 10026415)
47. Murray JB, Dunham CM, Scott WG. 2002. A pH-dependent conformational change, rather than the chemical step, appears to be ratelimiting in the hammerhead ribozyme cleavage reaction. J Mol Biol 315: 121-130. (Pubitemid 34722116)
48. Nelson JA, Uhlenbeck OC. 2006. When to believe what you see. Mol Cell 23: 447-450. (Pubitemid 44205497)
49. Nelson JA, Uhlenbeck OC. 2008. Minimal and extended hammerheads utilize a similar dynamic reaction mechanism for catalysis. RNA 14: 43-54.
50. Nelson JA, Shepotinovskaya I, Uhlenbeck OC. 2005. Hammerheads derived from sTRSV show enhanced cleavage and ligation rate constants. Biochemistry 44: 14577-14585. (Pubitemid 41567465)
51. Penedo JC, Wilson TJ, Jayasena SD, Khvorova A, Lilley DM. 2004. Folding of the natural hammerhead ribozyme is enhanced by interaction of auxiliary elements. RNA 10: 880-888. (Pubitemid 38529750)
52. Perreault J, Weinberg Z, Roth A, Popescu O, Chartrand P, Ferbeyre G, Breaker RR. 2011. Identification of hammerhead ribozymes in all domains of life reveals novel structural variations. PLoS Comput Biol 7: e1002031. doi: 10.1371/journal.pcbi.1002031.
53. Prody GA, Bakos JT, Buzayan JM, Schneider IR, Breuning G. 1986. Autolytic processing of dimeric plant virus satellite RNA. Science 231: 1577-1580.
54. Przybilski R, Hammann C. 2007a. Idiosyncratic cleavage and ligation activity of individual hammerhead ribozymes and core sequence variants thereof. Biol Chem 388: 737-741. (Pubitemid 46934160)
55. Przybilski R, Hammann C. 2007b. The tolerance to exchanges of the Watson-Crick base pair in the hammerhead ribozyme core is determined by surrounding elements. RNA 13: 1625-1630. (Pubitemid 47481670)
56. Roychowdhury-Saha M, Burke DH. 2006. Extraordinary rates of transition metal ion-mediated ribozyme catalysis. RNA 12: 1846-1852. (Pubitemid 44484258)
57. Rueda D, Wick K, McDowell SE, Walter NG. 2003. Diffusely bound Mg2+ 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. (Pubitemid 37012868)
58. Ruffner DE, Stormo GD, Uhlenbeck OC. 1990. Sequence requirements of the hammerhead RNA self-cleavage reaction. Biochemistry 29: 10695-10702.
59. Saksmerprome V, Roychowdhury-Saha M, Jayasena S, Khvorova A, Burke DH. 2004. Artificial tertiary motifs stabilize trans-cleaving hammerhead ribozymes under conditions of submillimolar divalent ions and high temperatures. RNA 10: 1916-1924. (Pubitemid 39557829)
60. Sander C, Ts'o PO. 1971. Interaction of nucleic acids. 8. Binding of magnesium ions by nucleic acids. J Mol Biol 55: 1-21.
61. SantaLucia J Jr, Kierzek R, Turner DH. 1991. Stabilities of consecutive A·C, C·C, G·G, U·C, and U·U mismatches in RNA internal loops: Evidence for stable hydrogen-bonded U·U and C·C+ pairs. Biochemistry 30: 8242-8251.
62. Sashital DG, Cornilescu G, McManus CJ, Brow DA, Butcher SE. 2004. U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat Struct Mol Biol 11: 1237-1242.
63. Scott WG, Murray JB, Arnold JR, Stoddard BL, Klug A. 1996. Capturing the structure of a catalytic RNA intermediate: The hammerhead ribozyme. Science 274: 2065-2069. (Pubitemid 27020698)
64. Strobel SA, Cech TR, 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. (Pubitemid 24381947)
65. Thompson KC, Miyake N. 2005. Properties of a new fluorescent cytosine analogue, pyrrolocytosine. J Phys Chem B 109: 6012-6019. (Pubitemid 40519511)
66. Tinsley RA, Walter NG. 2006. Pyrrolo-C as a fluorescent probe for monitoring RNA secondary structure formation. RNA 12: 522-529. (Pubitemid 43290878)
67. Tuschl T, Ng MM, Pieken W, Benseler F, Eckstein F. 1993. Importance of exocyclic base functional groups of central core guanosines for hammerhead ribozyme activity. Biochemistry 32: 11658-11668. (Pubitemid 23341444)
68. Walter NG, Burke JM. 1997. Real-time monitoring of hairpin ribozyme kinetics through base-specific quenching of fluorescein-labeled substrates. RNA 3: 392-404. (Pubitemid 27157672)
69. Zhang X, Wadkins RM. 2009. DNA hairpins containing the cytidine analog pyrrolo-dC: Structural, thermodynamic, and spectroscopic studies. Biophys J 96: 1884-1891.