Single-molecule RNA folding

Accounts of Chemical Research

Volumn 38, Issue 7, 2005, Pages 566-573

  Bokinsky, Gregory ^a,c   Zhuang, Xiaowei ^b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOZYME;

ARTICLE; CHEMISTRY; CONFORMATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; METHODOLOGY;

FLUORESCENCE RESONANCE ENERGY TRANSFER; NUCLEIC ACID CONFORMATION; RNA, CATALYTIC;

EID: 23744470902     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar040142o     Document Type: Article

References (67)

1. Kruger, K.; Grabowski, P. J.; Zaug, A. J.; Sands, J.; Gottschling, D. E. et al. Self-splicing RNA - Auto-excision and auto-cyclization of the ribosomal-RNA intervening sequence of Tetrahymena. Cell 1982, 31, 147-157.
2. Guerrier-Takada, C.; Gardinier, K.; Pace, T.; Altman, S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 1983, 35, 849-857.
3. Noller, H. F.; Hoffarth, V.; Zimniak, L. Unusual resistance of peptidyl transferase to protein extraction procedure. Science 1992, 265, 1709-1712.
4. Steitz, T. A.; Moore, P. B. RNA, the first macromolecular catalyst: the ribosome is a ribozyme. Trends Biochem. Sci. 2003, 28, 411-418.
5. Valadkhan, S.; Manley, J. L. Intrinsic metal binding by a spliceosomal RNA. Nat. Struct. Biol. 2002, 9, 498-9.
6. Villa, T.; Pleiss, J. A.; Guthrie, C. Spliceosomal snRNAs: Mg2+-dependent chemistry at the catalytic core? Cell 2002, 109, 149-152.
7. Famulok, M.; Verma, S. In vivo-applied functional RNAs as tools in proteomics and genomics research. Trends Biotechnol. 2002, 20, 462-6.
8. Sullenger, B. A.; Gilboa, E. Emerging clinical applications of RNA. Nature 2002, 418, 252-8.
9. Burgstaller, P.; Jenne, A.; Blind, M. Aptamers and aptazymes: accelerating small molecule drug discovery. Curr. Opin. Drug Discov. Devel. 2002, 5, 690-700.
10. Zarrinkar, P. P.; Williamson, J. R. Kinetic Intermediates in RNA Folding. Science 1994, 265, 918-924.
11. Zarrinkar, P. P.; Wang, J.; Williamson, J. R. Slow folding kinetic of RNase P RNA. RNA 1996, 2, 564-573.
12. Pan, T.; Sosnick, T. R. Intermediates and kinetics traps in the folding of a large ribozyme reveal by circular dichroism and Uv absorbance spectroscopies and catalytic activity. Nat. Struct. Biol. 1997, 4, 931-938.
13. Pan, J.; Thirumalai, D.; Woodson, S. A. Folding of RNA involves parallel pathways. J. Mol. Biol. 1997, 273, 7-13.
14. Sclavi, B.; Sullivan, M.; Chance, M. R.; Brenowitz, M.; Woodson, S. A. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science 1998, 279, 1940-1943.
15. Treiber, D. K.; Rook, M. S.; Zarrinkar, P. P.; Williamson, J. R. Kinetic intermediates trapped by native interactions in RNA folding. Science 1998, 279, 1943-6.
16. Rook, M. S.; Treiber, D. K.; Williamson, J. R. Fast folding mutants of the Tetrahymena group I ribozyme reveal a rugged folding energy landscape. J. Mol. Biol. 1998, 281, 609-20.
17. Pan, J.; Woodson, S. Folding intermediates of a self-splicing RNA: Mis-pairing of the catalytic core. J. Mol. Biol. 1998, 280, 597-609.
18. Pan, T.; Fang, X.; Sosnick, T. R. Pathway modulation, circular permutation and rapid folding under kinetic control. J. Mol. Biol. 1999, 286, 721-731.
19. Russell, R.; Herschlag, D. New pathways in folding of the Tetrahymena group I RNA enzyme. J. Mol. Biol. 1999, 291, 1155-1167.
20. Buchmueller, K. L.; Webb, A. E.; Richardson, D. A.; Weeks, K. M. A collapsed non-native RNA folding state. Nat. Struct. Biol. 2000, 7, 362-6.
21. Zhuang, X.; Bartley, L.; Babcock, H.; Russell, R.; Ha, T. et al. A single molecule study of RNA catalysis and folding. Science 2000, 288, 2048-2051.
22. Pan, J.; Deras, M. L.; Woodson, S. A. Fast folding of a ribozyme by stabilizing core interactions: Evidence for multiple folding pathways in RNA. J. Mol. Biol. 2000, 296, 133-144.
23. Heilman-Miller, S. L.; Pan, J.; Thirumalai, D.; Woodson, S. A. Role of counterion condensation in folding of the Tetrahymena ribozyme II. Counterion-dependence of folding kinetics. J. Mol. Biol. 2001, 309, 57-68.
24. Zhuang, X.; Kim, H.; Pereira, M.; Babcock, H.; Walter, N. et al. Correlating of Structural Dynamics and Function in Single Ribozyme Molecules. Science 2002, 296, 1473-1477.
25. Russell, R.; Zhuang, X.; Babcock, H.; Millett, I. S.; Doniach, S. et al. Exploring the Folding Landscape of a Structured RNA. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 155-160.
26. Russell, R.; Millett, I. S.; Tate, M. W.; Kwok, L. W.; Nakatani, B. et al. Rapid compaction during RNA folding. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 4266-71.
27. Takamoto, K.; He, Q.; Morris, S.; Chance, M. R.; Brenowitz, M. Monovalent cations mediate formation of native tertiary structures of the Tetrahymena thermophila ribozyme. Nat. Struct. Biol. 2002, 9, 928-933.
28. Bartley, L. E.; Zhuang, X.; Das, R.; Chu, S.; Herschlag, D. Exploration of the transition state for tertiary structure formation between RNA helix and a large structured RNA. J. Mol. Biol. 2003, 328, 1011-1026.
29. Bokinsky, G.; Rueda, D.; Misra, V. K.; Gordus, A.; Rhodes, M. M.; Babcock, H. P.; Walter, N. G.; Zhuang, X. Single-molecule transition-state analysis of RNA folding. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 9302-9307.
30. Tan, E.; Wilson, T. J.; Nahas, M. K.; Clegg, R. M.; Lilley, D. M. et al. A four-way junction accelerates hairpin ribozyme folding via a discrete intermediate. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 9308-9313.
31. Xie, Z.; Srividya, N.; Sosnick, T. R.; Pan, T.; Scherer, N. F. Single-molecule studies highlight conformational heterogeneity in the early folding steps of a large ribozyme. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 534-539.
32. Brion, P.; Westhof, E. Hierarchy and dynamics of RNA folding. Annu. Rev. Biophys. Biomol. Struct. 1997, 26, 113-37.
33. Treiber, D. K.; Williamson, J. R. Concerted kinetic folding of a multidomain ribozyme with a disrupted loop-receptor interaction. J. Mol. Biol. 2001, 305.
34. Rueda, D.; Bokinsky, G.; Rhodes, M. M.; Rust, M. J.; Zhuang, X. et al. Single-molecule enzymology of RNA: Essential functional groups impact catalysis from a distance. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 10066-10071.
35. Nahas, M. K.; Wilson, T. J.; Hohng, S. C.; Jarvie, K.; Lilley, D. M. J. et al. Observation of internal cleavage and ligation reactions of a ribozyme. Nat Struct. Mol. Biol 2004, 11, 1107-1113.
36. Pljevaljcic, G.; Millar, D. P.; Deniz, A. A. Freely diffusing single hairpin ribozymes provide insights into the role of secondary structure and partially folded states in RNA folding. Biophys. J. 2004, 87, 457-467.
37. Kim, H. D.; Nienhaus, G. U.; Ha, T.; Orr, J. W.; Williamson, J. R. et al. Mg2+-dependent conformational change of RNA studied by fluorescence correlation and FRET on immobilized single molecules. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 4284-4289.
38. Liphardt, J.; Onoa, B.; Smith, S. B.; Tinoco, I.; Bustamante, C. Reversible unfolding of single RNA molecules by mechanical force. Science 2001, 292, 733-737.
39. Onoa, B.; Dumont, S.; Liphardt, J.; Smith, S. B.; Tinoco, I. et al. Identifying kinetic barriers to mechanical unfolding of the T-thermophila ribozyme. Science 2003, 299, 1892-1895.
40. Tinoco, I. Force as a useful variable in reaction: unfolding RNA. Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 363-385.
41. Stryer, L.; Haugland, R. P. Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. U.S.A. 1967, 58, 719-726.
42. Selvin, P. R. Fluorescence resonance energy-transfer. Methods Enzymol. 1995, 246, 6264-6268.
43. Weiss, S. Measuring conformational dynamics of biomolecules by single molecule fluorescence spectroscopy. Nat. Struct. Biol. 2000, 7, 724-729.
44. Ha, T.; Enderle, T.; Ogletree, D. F.; Chemla, D. S.; Selvin, P. R. et al. Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 6264-6268.
45. Schutz, G. J.; Trabesinger, W.; Schmidt, T. Direct observation of ligand colocalization on individual receptor molecules. Biophys. J. 1998, 74, 2223-2226.
46. Ha, T.; Zhuang, X.; Kim, H.; Orr, J. W.; Williamson, J. R. et al. Ligand-induced conformational changes observed in single RNA molecules. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 9077-9082.
47. Pley, H. W.; Flaherty, K. M.; McKay, D. B. Three-dimensional structure of a hammerhead ribozyme. Nature 1994, 372, 68-74.
48. Scott, W. G.; Finch, J. T.; Klug, A. The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage. Cell 1995, 81, 991-1002.
49. Ferre-D'Amare, A. R.; Zhou, K.; Doudna, J. A. Crystal Structure of a Hepatitis Delta Virus Ribozyme. Nature 1998, 395, 567-574.
50. Rupert, P. B.; Ferre-D'Amare, A. R. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 2001, 410, 780-6.
51. Rupert, P. B.; Massey, A. P.; Sigurdsson, S. T.; Ferre-D'Amare, A. R. Transition state stabilization by a catalytic RNA. Science 2002, 298, 1421-1424.
52. Walter, N. G.; Burke, J. M. The hairpin ribozyme: structure, assembly and catalysis. Curr. Opin. Chem. Biol. 1998, 2, 24-30.
53. Fedor, M. J. Structure and function of the hairpin ribozyme. J. Mol. Biol. 2000, 297, 269-91.
54. Walter, N. G.; Burke, J. M. Real-time monitoring of hairpin ribozyme kinetics through base-specific quenching of fluorescein-labeled substrates. RNA 1997, 3, 392-404.
55. Walter, N. G.; Burke, J. M.; Millar, D. P. Stability of hairpin ribozyme tertiary structure is governed by the interdomain junction. Nat. Struct. Biol. 1999, 6, 544-9.
56. Okumus, B.; Ha, T. How intrinsic are molecular heterogeneities observed in single molecule measurements?: Vesicle encapsulation studies. Biophys. J. 2004, 86, 601A-610A.
57. Lu, H. P.; Xun, L. Y.; Xie, X. S. Single-molecule enzymatic dynamics. Science 1998, 282, 1877-1882.
58. Edman, L.; Rigler, R. Memory landscapes of single-enzyme molecules. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 8266-8271.
59. Fersht, A. Structure and Mechanism in Protein Science; Freeman: New York, 1999.
60. Cai, Z. P.; Tinoco, I. Solution structure of loop a from the hairpin ribozyme from tobacco ringspot virus satellite. Biochemistry 1996, 35, 6026-6036.
61. Butcher, S. E.; Allain, F. H. T.; Feigon, J. Solution structure of the loop B domain from the hairpin ribozyme. Nat. Struct. Biol. 1999, 6, 212-216.
62. Pan, J.; Woodson, S. A. The effect of long-range loop-loop interactions on folding of the Tetrahymena self-splicng RNA. J. Mol. Biol. 1999, 294, 955-965.
63. Herschlag, D. RNA chaperones and the RNA folding problem. J. Biol. Chem. 1995, 270, 20871-20874.
64. Weeks, K. M. Protein-facilitated RNA folding. Curr. Opin. Struct. Biol. 1997, 7, 336-342.
65. Hsien, J.; Andrews, A. J.; Ferike, C. A. Roles of protein subunit in RNA-protein complexes: Lessons from Ribonuclease P. Biopolymers 2004, 73, 79-89.
66. Sorin, E. J.; Rhee, Y. M.; Nakatani, B. J.; Pande, V. S. Insights into nucleic acid conformational dynamics from massively parallel stochastic simulations. Biophys. J. 2003, 85, 790-803.
67. Nivon, L. G.; Shakhnovich, E. I. All-atom Monte Carlo simulation of GCAA RNA folding. J. Mol. Biol. 2004, 344, 29-45.