Probing the structural hierarchy and energy landscape of an RNA T-loop hairpin

Nucleic Acids Research

Volumn 35, Issue 20, 2007, Pages 6995-7002

  Zhuang, Zhuoyun ^a   Jaeger, Luc ^a   Shea, Joan Emma ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENERGY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN MOTIF; RNA STRUCTURE; SIMULATION;

HALOARCULA MARISMORTUI; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA; THERMODYNAMICS;

EID: 36749052211     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm719     Document Type: Article

References (60)

1. Mathews,D.H. (2006) Revolutions in RNA secondary structure prediction. J. Mol. Biol., 359, 526-532.
2. Brion,P. and Westhof,E. (1997) Hierarchy and dynamics of RNA folding. Annu. Rev. Biophys. Biomol. Struct., 26, 113-137.
3. Westhof,E. and Auffinger,P. (2000) RNA Tertiary Structure. Encyclopedia of Analytical Chemistry. John Wiley & Sons Ltd, Chichester, pp. 5222-5232.
4. Leontis,N.B. and Westhof,E. (2003) Analysis of RNA motifs. Curr. Opin. Struct. Biol., 13, 300-308.
5. Holbrook,S.R. (2005) RNA structure: The long and the short of it, Curr. Opin. Struct. Biol., 15, 302-308.
6. Batey,R.T., Rambo,R.P. and Doudna,J.A. (1999) Tertiary motifs in RNA structure and folding. Angew. Chem. Int. Ed. Engl., 38, 2326-2343.
7. Moore,P.B. (1999) Structural motifs in RNA. Annu. Rev. Biochem., 68, 287-300.
8. Hendrix,D.K., Brenner,S.E. and Holbrook,S.R. (2005) RNA structural motifs: Building blocks of a modular biomolecule. Q. Rev. Biophys. 38, 221-243.
9. Tinoco,I.Jr and Bustamante,C. (1999) How RNA folds. J. Mol. Biol., 293, 271-281.
10. Schroeder,R., Barta,A. and Semrad,K. (2004) Strategies for RNA folding and assembly. Nat. Rev. Mol. Cell Biol., 5, 908-919.
11. Russell,R., Millett,I.S., Tate,M.W., Kwok,L.W., Nakatani,B., Gruner,S.M., Mochrie,S.G., Pande,V.S., Doniach,S. et al. (2002) Rapid compaction during RNA folding. Proc. Natl Acad. Sci. USA, 99, 4266-4271.
12. Russell,R., Millett,I.S., Doniach,S. and Herschtag,D. (2000) Small angle X-ray scattering reveals a compact intermediate in RNA folding. Nat. Struct. Biol., 7, 367-370.
13. Buchmueller,K.L., Webb,A.E., Richardson,D.A. and Weeks,K.M. (2000) A collapsed non-native RNA folding state. Nat. Struct. Biol., 7 362-366.
14. Adilakshmi,T., Ramaswamy,P. and Woodson,S.A. (2005) Protein-independent folding pathway of the 16 S rRNA 5′ domain. J. Mol. Biol., 351, 508-519.
15. Uhlenbeck,O.C. (1990) Tetraloops and RNA folding. Nature, 346 613-614.
16. Nagaswamy,U. and Fox,G.E. (2002) Frequent occurrence of the T-loop RNA folding motif in ribosomal RNAs. RNA, 8, 1112-1119.
17. Gutell,R.R., Cannone,J.J., Konings,D. and Gautheret,D. (2000) Predicting U-turns in ribosomal RNA with comparative sequence analysis. J. Mol. Biol., 300, 791-803.
18. Jucker,F.M., Heus,H.A., Yip,P.F., Moors,E.H. and Pardi,A. (1996) A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. Mol. Biol., 264, 968-980.
19. Woese,C.R., Winker,S. and Gutell,R.R. (1990) Architecture of ribosomal RNA: Constraints on the sequence of "tetra-loops". Proc. Natl Acad. Sci. USA, 87, 8467-8471.
20. Krasilnikov,A.S. and Mondragon,A. (2003) On the occurrence of the T-loop RNA folding motif in large RNA molecules. RNA, 9, 640-643.
21. Jucker,F.M. and Pardi,A. (1995) GNRA tetraloops make a U-turn. RNA 1, 219-222.
22. Turek,J.P.G., Thermes,C., Groebe,D.R., Gayle,M., Guild,N., Stormo,G., D'Aubento-Carafa,Y., Uhlenbeck,O.C. et al. (1988) GUUCGG hairpins: extraordinarily stable RNA secondary structures associated with various biochemical processes. Proc. Natl Acad. Sci. USA, 85, 1364-1368.
23. Molinaro,M. and Tinoco,I.Jr (1995) Use of ultra stable UNCG tetraloop hairpins to fold RNA structures: Thermodynamic and spectroscopic applications. Nucleic Acids Res., 23, 3056-3063.
24. Jaeger,L., Michel,F. and Westhof,E. (1994) Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J. Mol. Biol., 236, 1271-1276.
25. Menger,M., Eckstein,F. and Porschke,D. (2000) Dynamics of the RNA hairpin GNRA tetraloop. Biochem. J., 39, 4500-4507.
26. Cheong,C., Varani,G. and Tinoco,I.Jr (1990) Solution structure of an unusually stable RNA hairpin, 5′GGAC(UUCG)GUCC. Nature, 346 680-682.
27. Heus,H.A. and Pardi,A. (1991) Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. Science, 253, 191-194.
28. Correll,C.C. and Swinger,K. (2003) Common and distinctive features of GNRA tetraloops based on a GUAA tetraloop structure at 1.4Å resolution. RNA, 9, 353-363.
29. Cate,J.H., Gooding,A.R., Podell,E., Zhou,K., Golden,B.L., Szewczak,A.A., Kundrot,C.E., Cech,T.R. and Doudna,J.A. (1996) RNA tertiary structure mediation by adenosine platforms. Science, 273, 1696-1699.
30. Pley,H.W., Flaherty,K.M. and McKay,D.B. (1994) Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix. Nature, 372, 111-113.
31. 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.
32. Davis,J.H., Tonelli,M., Scott,L.G., Jaeger,L., Williamson,J.R. and Butcher,S.E. (2005) RNA helical packing in solution: NMR structure of a 30 kDa GAAA tetraloop-receptor complex. J. Mol. Biol., 351, 371-382.
33. Ban,N., Nissen,P., Hansen,J., Moore,P.B. and Steitz,T.A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4Å resolution. Science, 289, 905-920.
34. Krasilnikov,A.S., Yang,X., Pan,T. and Mondragon,A. (2003) Crystal structure of the specificity domain of ribonuclease P. Nature, 421, 760-764.
35. Zhao,L. and Xia,T. (2007) Direct revelation of multiple conformations in RNA by femtosecond dynamics. J. Am. Chem. Soc., 129, 4118-4119.
36. Ma,H., Proctor,D.J., Kierzek,E., Kierzek,R., Bevilacqua,P.C. and Gruebele,M. (2006) Exploring the energy landscape of a small RNA hairpin. J. Am. Chem. Soc., 128, 1523-1530.
37. Nivon,L.G. and Shakhnovich,E.I. (2004) All-atom Monte Carlo simulation of GCAA RNA folding. J. Mol. Biol., 344, 29-45.
38. Sorin,E.J., Engelhardt,M.A., Herschlag,D. and Pande,V.S. (2002) RNA simulations: Probing hairpin unfolding and the dynamics of a GNRA tetraloop. J. Mol. Biol., 317, 493-506.
39. Sorin,E.J., Rhee,Y.M., Nakatani,B.J. and Pande,V.S. (2003) Insights into nucleic acid conformational dynamics from massively parallel stochastic simulations. Biophys. J., 85, 790-803.
40. Sorin,E.J., Rhee,Y.M. and Pande,V.S. (2005) Does water play a structural role in the folding of small nucleic acids? Biophys. J., 88, 2516-2524.
41. Li,W., Ma,B. and Shapiro,B. (2001) Molecular dynamics simulations of the denaturation and refolding of an RNA tetraloop. J. Biomol. Struct. Dyn., 19, 381-396.
42. Nagel,J.H., Flamm,C., Hofacker,I.L., Franke,K., de Smit,M.H., Schuster,P. and Pteij,C.W. (2006) Structural parameters affecting the kinetics of RNA hairpin formation. Nucleic Acids Res., 34, 3568-3576.
43. Hansmann,U.H.E. (1997) Parallel tempering algorithm for conformational studies of biological molecules. Chem. Phys. Lett., 281, 140-150.
44. Mitsutake,A., Sugita,Y. and Okamoto,Y. (2001) Generalized-ensemble algorithms for molecular simulations of biopolymers. Biopolymers, 60, 96-123.
45. Sugita,Y. and Okamoto,Y. (1999) Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett., 315, 141-151.
46. Klein,D.J., Schmeing,T.M., Moore,P.B. and Steitz,T.A. (2001) The kink-turn: A new RNA secondary structure motif. EMBO J., 20, 4214-4221.
47. Case,D.A., Darden,T.A., Cheatham,T.E.III, Simmerling,C.L., Wang,J., Duke,R.E., Luo,R., Merz,K.M., Wang,B. et al. (2004) AMBER 8. University of California, San Francisco.
48. Wang,J., Cieplak,P. and Kollman,P.A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem., 21, 1049-1074.
49. Jorgensen,W.L., Chandrasekhar,J., Madura,J.D., Impey,R.W. and Klein,M.L. (1993) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
50. Ryckaert,J.P., Ciccotti,G. and Berendsen,H.J.C. (1977) Numerical-integration of Cartesian equations of motion of a system with constraints - molecular-dynamics of n-alkanes. J. Comput. Phys., 23, 327-341.
51. Darden,T.A., York,D.A. and Pedersen,L. (1995) Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
52. Berendsen,H.J.C., Postma,W.F., DiNola,V.G.A. and Haak,J.R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690.
53. DeLano,W.L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.
54. Pettersen,E.F., Goddard,T.D., Huang,C.C., Couch,G.S., Greenblatt,D.M., Meng,E.C. and Ferrin,T.E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
55. Ferrenberg,A.M. and Swendsen,R.H. (1989) Optimized Monte Carlo data analysis. Phys. Rev. Lett., 63, 1195-1198.
56. Kumar,S., Bouzida,D., Swendsen,R.H., Kollman,P.A. and Rosenberg,J.M. (1992) The weighted histogram analysis method for free-energy calculations on biomolecules. I. The Method. J. Comput. Chem., 13, 11.
57. Ferrenberg,A.M. and Swendsen,R.H. (1988) New Monte Carlo technique for studying phase transitions. Phys. Rev. Lett., 61, 2635-2638.
58. Thirumalai,D., Lee,N., Woodson,S.A. and Klimov,D. (2001) Early events in RNA folding. Annu. Rev. Phys. Chem., 52, 751-762.
59. Chen,S.J. and Dill,K.A. (2000) RNA folding energy landscapes. Proc. Natl Acad. Sci. USA, 97, 646-651.
60. Lemieux,S. and Major,F. (2002) RNA canonical and non-canonical base pairing types: A recognition method and complete repertoire. Nucleic Acids Res., 30, 4250-4263.