From static to dynamic: The need for structural ensembles and a predictive model of RNA folding and function

Current Opinion in Structural Biology

Volumn 30, Issue , 2015, Pages 125-133

  Herschlag, Daniel ^a,b,c   Allred, Benjamin E ^a   Gowrishankar, Seshadri ^c  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Stanford University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITY; CRYSTAL STRUCTURE; ENTROPY; GENE EXPRESSION; GENE FUNCTION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; RNA FOLDING; RNA PROCESSING; RNA STRUCTURE; THERMODYNAMICS; CHEMISTRY; CONFORMATION; GENETICS; KINETICS; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY; RIBOSOME;

RNA;

KINETICS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RIBOSOMES; RNA; RNA FOLDING; THERMODYNAMICS;

EID: 84924977596     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.02.006     Document Type: Review

References (53)

1. Crick F.H. On protein synthesis. Symp Soc Exp Biol 1958, 12:138-163.
2. Crick F. Central dogma of molecular biology. Nature 1970, 227:561-563.
3. Temin H.M., Mizutani S. RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 1970, 226:1211-1213.
4. Autexier C., Lue N.F. The structure and function of telomerase reverse transcriptase. Annu Rev Biochem 2006, 75:493-517.
5. Fresco J.R., Adams A., Ascione R., Henley D., Lindahl T. Tertiary structure in transfer ribonucleic acids. Cold Spring Harb Symp Quant 1966, 31:527-537.
6. Cech T.R., Steitz J.A. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 2014, 157:77-94.
7. Kraus A., Groveman B.R., Caughey B. Prions and the potential transmissibility of protein misfolding diseases. Annu Rev Microbiol 2013, 67:543-564.
8. Woese C. The Genetic Code: The Molecular Basis for Genetic Expression 1967, Harper and Row, New York.
9. Crick F.H.C. The origin of the genetic code. J Mol Biol 1968, 38:367-379.
10. Orgel L.E. Evolution of genetic apparatus. J Mol Biol 1968, 38:381-393.
11. Dwars T., Paetzold E., Oehme G. Reactions in micellar systems. Angew Chem Int Ed 2005, 44:7174-7199.
12. Akopian D., Shen K., Zhang X., Shan S. Signal recognition particle: an essential protein-targeting machine. Annu Rev Biochem 2013, 82:693-721.
13. Voorhees R.M., Ramakrishnan V. Structural basis of the translational elongation cycle. Annu Rev Biochem 2013, 82:203-236.
14. Sanbonmatsu K.Y. Computational studies of molecular machines: the ribosome. Curr Opin Struct Biol 2012, 22:168-174.
15. Mitra K., Frank J. Ribosome dynamics: insights from atomic structure modeling into cryo-electron microscopy maps. Annu Rev Biophys Biomol Struct 2006, 35:299-317.
16. Freier S.M., Kierzek R., Jaeger J.A., Sugimoto N., Caruthers M.H., Neilson T., Turner D.H. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci USA 1986, 83:9373-9377.
17. Sugimoto N., Kierzek R., Turner D.H. Sequence dependence for the energetics of terminal mismatches in ribooligonucleotides. Biochemistry 1987, 26:4559-4562.
18. Mathews D.H., Sabina J., Zuker M., Turner D.H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 1999, 288:911-940.
19. Murchie A.I.H., Clegg R.M., von Krtzing E., Duckett D.R., Diekmann S., Lilley D.M. Fluorescence energy transfer shows that the four-way DNA junction is a right-handed cross of antiparallel molecules. Nature 1989, 341:763-766.
20. Battacharyya A., Murchie A.I., Lilley D.M. RNA bulges and the helical periodicity of double-stranded RNA. Nature 1990, 343:484-487.
21. Duckett D.R., Murchie A.I., Lilley D.M. The global folding of four-way helical junctions in RNA, including that in U1 snRNA. Cell 1995, 83:1027-1036.
22. Lilley D.M. Structures of helical junctions in nucleic acids. Q Rev Biophys 2000, 33:109-159.
23. Lilley D.M.J. The structure and folding of kink turns in RNA. WIREs RNA 2012, 3:797-805.
24. Chu V.B., Lipfert J., Bai Y., Pande V.S., Doniach S., Herschlag D. Do conformational biases of simple helical junctions influence RNA folding stability and specificity?. RNA 2009, 15:2195-2205.
25. Bothe J.R., Nikolova E.N., Eichhorn C.D., Chugh J., Hansen A.L., Al-Hashimi H.M. Characterizing RNA dynamics at atomic resolution using solution-state NMR spectroscopy. Nat Methods 2011, 8:919-931.
26. Salmon L., Bascom G., Andricioaei I., Al-Hashimi H.M. A general method for constructing atomic-resolution RNA ensembles using NMR residual dipolar couplings: the basis for interhelical motions revealed. J Am Chem Soc 2013, 135:5457-5466.
27. 2+-induced conformational stabilization. J Mol Biol 2004, 338:7-16.
28. Zhang Q., Stelzer A.C., Fisher C.K., Al-Hashimi H.M. Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 2007, 450:1263-1267.
29. Mustoe A.M., Bailor M.H., Teixeira R.M., Brooks C.L., Al-Hashimi H.M. New insights into the fundamental role of topological constraints as a determinant of two-way junction conformation. Nucl Acids Res 2012, 40:892-904.
30. Bailor M.H., Mustoe A.M., Brooks C.L., Al-Hashimi H.M. 3D maps of RNA interhelical junctions. Nat Protoc 2011, 6:1536-1545.
31. Bailor M.H., Sun X., Al-Hashimi H.M. Topology links RNA secondary structure with global conformation, dynamics, and adaption. Science 2010, 327:202-206.
32. Bai Y., Chu V.B., Lipfert J., Pande V.S., Herschlag D., Doniach S. Critical assessment of nucleic acid electrostatics via experimental and computational investigation of an unfolded state ensemble. J Am Chem Soc 2008, 130:12334-12341.
33. Lipfert J., Doniach S., Das R., Herschlag D. Understanding nucleic acid-ion interactions. Annu Rev Biochem 2014, 83:813-841.
34. Chu V.B., Bai Y., Lipfert J., Herschlag D., Doniach S. A repulsive field: advances in the electrostatics of the ion atmosphere. Curr Opin Chem Biol 2008, 12:619-625.
35. Mathew-Fenn R.S., Das R., Harbury P.B. Remeasuring the double helix. Science 2008, 322:446-449.
36. Shi X., Herschlag D., Harbury P.B. Structural ensemble and microscopic elasticity of freely diffusing DNA by direct measurement of fluctuations. Proc Natl Acad Sci USA 2013, 110:E1444-E1451.
37. Shi X., Beauchamp K.A., Harbury P.B., Herschlag D. From a structural average to the conformational ensemble of a DNA bulge. Proc Natl Acad Sci USA 2014, 111:E1473-E1480.
38. Lee J., Dethoff E.A., Al-Hashimi H.M. Invisible RNA state dynamically couples distant motifs. Proc Natl Acad Sci USA 2014, 111:9485-9490.
39. Dethoff E.A., Petzold K., Chugh J., Casiano-Negroni A., Al-Hashimi H.M. Visualizing transient low-populated structures of RNA. Nature 2012, 491:724-728.
40. Cruz J.A., Blanchet M.F., Boniecki M., Bujnicki J.M., Chen S.J., Cao S., Das R., Ding F., Dokholyan N.V., Flores S.C., et al. RNA-Puzzles: a CASP-like evaluation of RNA three-dimensional structure prediction. RNA 2012, 18:610-625.
41. Jaeger L., Michel F., Westhof E. Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J Mol Biol 1994, 236:1271-1276.
42. Fiore J.L., Nesbitt D.J. An RNA folding motif: GNRA tetraloop-receptor interactions. Q Rev Biophys 2013, 46:223-264.
43. Battiste J.L., Tan R., Frankel A.D., Williamson J.R. Binding of an HIV Rev peptide to Rev responsive element RNA induces formation of purine-purine base pairs. Biochemistry 1994, 33:2741-2747.
44. Puglisi J.D., Tan R., Calnan B.J., Frankel A.D., Williamson J.R. Conformation of the TAR RNA-arginine complex by NMR spectroscopy. Science 1992, 257:76-80.
45. Winkler W.C., Breaker R.R. Regulation of bacterial gene expression by riboswitches. Annu Rev Microbiol 2005, 59:487-517.
46. Zarrinkar P.P., Williamson J.R. Kinetic intermediates in RNA folding. Science 1994, 265:918-924.
47. Zarrinkar P.P., Wang J., Williamson J.R. Slow folding kinetics of RNase P RNA. RNA 1996, 2:564-573.
48. Cate J.H., Gooding A.R., Podell E., Zhou K., Golden B.L., Kundrot C.E., Cech T.R., Doudna J.A. Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 1996, 273:1678-1685.
49. Butcher S.E., Dieckmann T., Feigon J. Solution structure of a GAAA tetraloop receptor RNA. EMBO J 1997, 16:7490-7499.
50. Jucker F.M., Heus H.A., Yip P.F., Moors E.H.M., Pardi A. A network of heterogenous hydrogen bonds in GNRA tetraloops. J Mol Biol 1996, 264:968-980.
51. Qin P.Z., Butcher S.E., Feigon J., Hubbell W.L. Quantitative analysis of the isolated GAAA tetraloop/receptor interaction in solution: a site-directed spin labeling study. Biochemistry 2001, 40:6929-6936.
52. Hodak J.H., Downey C.D., Fiore J.L., Pardi A., Nesbitt D.J. Docking kinetics and equilibrium of a GAAA tetraloop-receptor motif probed by single-molecule FRET. Proc Natl Acad Sci USA 2005, 102:10505-10510.
53. 2+-facilitated RNA folding. Proc Natl Acad Sci USA 2012, 109:2902-2907.