The Osmolyte TMAO stabilizes native RNA tertiary structures in the absence of Mg2+: Evidence for a large barrier to folding from phosphate dehydration

Journal of Molecular Biology

Volumn 404, Issue 1, 2010, Pages 138-157

  Lambert, Dominic ^a   Leipply, Desirae ^b   Draper, David E ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dimethylphosphate; Hydration; Linkage relations; RNA folding

Indexed keywords

MAGNESIUM ION; PHOSPHATE; RNA; TRIMETHYLAMINE OXIDE; WATER;

ARTICLE; CHELATION; DESICCATION; ENERGY TRANSFER; MOLECULAR PROBE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; RADIATION SCATTERING; RNA SEQUENCE; RNA STABILITY; RNA STRUCTURE; TITRIMETRY; X RAY CRYSTALLOGRAPHY;

EID: 78049445847     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.09.043     Document Type: Article

References (69)

1. Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D., Somero G.N. Living with water stress: evolution of osmolyte systems. Science 1982, 217:1214-1222.
2. Cayley D.S., Guttman H.J., Record M.T. Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys. J. 2000, 78:1748-1764.
3. Liu Y., Bolen D.W. The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes. Biochemistry 1995, 34:12884-12891.
4. Timasheff S.N. Control of protein stability and reactions by weakly interacting cosolvents: the simplicity of the complicated. Adv. Protein Chem. 1998, 51:355-432.
5. Courtenay E.S., Capp M.W., Saecker R.M., Record M.T. Thermodynamic analysis of interactions between denaturants and protein surface exposed on unfolding: interpretation of urea and guanidinium chloride m-values and their correlation with changes in accessible surface area (ASA) using preferential interaction coefficients and the local-bulk domain model. Proteins Suppl. 2000, 4:72-85.
6. Bolen D.W., Baskakov I.V. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J. Mol. Biol. 2001, 310:955-963.
7. Felitsky D.J., Cannon J.G., Capp M.W., Hong J., Van Wynsberghe A.W., Anderson C.F., Record M.T. The exclusion of glycine betaine from anionic biopolymer surface: why glycine betaine is an effective osmoprotectant but also a compatible solute. Biochemistry 2004, 43:14732-14743.
8. Auton M., Bolen D.W. Predicting the energetics of osmolyte-induced protein folding/unfolding. Proc. Natl Acad. Sci. USA 2005, 102:15065-15068.
9. Bolen D.W., Rose G.D. Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu. Rev. Biochem. 2008, 77:339-362.
10. Baskakov I., Bolen D.W. Forcing thermodynamically unfolded proteins to fold. J. Biol. Chem. 1998, 273:4831-4834.
11. Baskakov I.V., Kumar R., Srinivasan G., Ji Y.S., Bolen D.W., Thompson E.B. Trimethylamine N-oxide-induced cooperative folding of an intrinsically unfolded transcription-activating fragment of human glucocorticoid receptor. J. Biol. Chem. 1999, 274:10693-10696.
12. 2+ interactions. J. Mol. Biol. 2007, 370:993-1005.
13. Pan T., Sosnick T.R. Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nat. Struct. Biol. 1997, 4:931-938.
14. Wyman J. Heme Proteins. Adv. Protein Chem. 1948, 4:407-531.
15. Record M.T., Zhang W., Anderson C.F. Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: a practical guide to recognizing and interpreting polyelectrolyte effects, Hofmeister effects, and osmotic effects of salts. Adv. Protein Chem. 1998, 51:281-353.
16. Leipply D., Lambert D., Draper D.E. Ion-RNA interactions: thermodynamic analysis of the effects of mono- and divalent ions on RNA conformational equilibria. Methods Enzymol. 2009, 469:433-463.
17. Hong J., Capp M.W., Saecker R.M., Record M.T. Use of urea and glycine betaine to quantify coupled folding and probe the burial of DNA phosphates in lac repressor-lac operator binding. Biochemistry 2005, 44:16896-16911.
18. Hong J. Solute Probes of Changes in Water-Accessible Biopolymer Surface: Development and Application to Lac Repressor 2004, University of Wisconsin, Madison.
19. Pace C.N. The stability of globular proteins. CRC Crit. Rev. Biochem. 1975, 3:1-43.
20. Robinson R.A., Sinclair D.A. The activity coefficients of the alkali chlorides and of lithium iodide in aqueous solution from vapor pressure measurements. J. Am. Chem. Soc. 1934, 59:1830-1835.
21. Pitzer K.S. Thermodynamics 1995, McGraw-Hill, Inc., New York. 3rd edit.
22. Robinson C.V., Stokes R.H. Activity coefficients in aqueous solutions of sucrose, mannitol and their mixtures at 25 J. Phys. Chem. 1961, 65:1954-1958.
23. Cannon J.G., Anderson C.F., Record M.T. Urea-amide preferential interactions in water: quantitative comparison of model compound data with biopolymer results using water accessible surface areas. J. Phys. Chem. B 2007, 111:9675-9685.
24. Capp M.W., Pegram L.M., Saecker R.M., Kratz M., Riccardi D., Wendorff T., et al. Interactions of the osmolyte glycine betaine with molecular surfaces in water: thermodynamics, structural interpretation, and prediction of m-values. Biochemistry 2009, 48:10372-10379.
25. Hong J., Capp M.W., Anderson C.F., Record M.T. Preferential interactions in aqueous solutions of urea and KCl. Biophys. Chem. 2003, 105:517-532.
26. Chang K.Y., Tinoco I. The structure of an RNA "kissing" hairpin complex of the HIV TAR hairpin loop and its complement. J. Mol. Biol. 1997, 269:52-66.
27. Davis J.H., Tonelli M., Scott L.G., Jaeger L., Williamson J.R., Butcher S.E. RNA helical packing in solution: NMR structure of a 30 kDa GAAA tetraloop-receptor complex. J. Mol. Biol. 2005, 351:371-382.
28. Zuo X., Wang J., Foster T.R., Schwieters C.D., Tiede D.M., Butcher S.E., Wang Y.X. Global molecular structure and interfaces: refining an RNA:RNA complex structure using solution X-ray scattering data. J. Am. Chem. Soc. 2008, 130:3292-3293.
29. Lambert D., Leipply D., Shiman R., Draper D.E. The influence of monovalent cation size on the stability of RNA tertiary structures. J. Mol. Biol. 2009, 390:791-804.
30. Serganov A., Yuan Y.R., Pikovskaya O., Polonskaia A., Malinina L., Phan A.T., et al. Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem. Biol. 2004, 11:1729-1741.
31. 2+ concentration: interpretation of the Hill equation and coefficient. Biochemistry 2010, 49:1843-1853.
32. + complex. J. Mol. Biol. 2002, 318:963-973.
33. 2+-RNA interaction free energies and their relationship to the folding of RNA tertiary structures. Proc. Natl Acad. Sci. USA 2006, 103:14003-14008.
34. 2+ binding to RNA. Proc. Natl Acad. Sci. USA 2001, 98:12456-12461.
35. Bukhman Y.V., Draper D.E. Affinities and selectivities of divalent cation binding sites within an RNA tertiary structure. J. Mol. Biol. 1997, 273:1020-1031.
36. Shiman R., Draper D.E. Stabilization of RNA tertiary structure by monovalent cations. J. Mol. Biol. 2000, 302:79-91.
37. Lu M., Draper D.E. Bases defining an ammonium and magnesium ion-dependent tertiary structure within the large subunit ribosomal RNA. J. Mol. Biol. 1994, 244:572-585.
38. Ts'o P.O.P., Melvin I.S., Olson A.C. Interaction and association of bases and nucleosides in aqueous solutions. J. Am. Chem. Soc. 1963, 85:1289-1296.
39. Qu Y., Bolen C.L., Bolen D.W. Osmolyte-driven contraction of a random coil protein. Proc. Natl Acad. Sci. USA 1998, 95:9268-9273.
40. Allen S.H., Wong K.P. The role of magnesium and potassium ions in the molecular mechanism of ribosome assembly: hydrodynamic, conformational, and thermal stability studies of 16 S RNA from Escherichia coli ribosomes. Arch. Biochem. Biophys. 1986, 249:137-147.
41. Buchmueller K.L., Webb A.E., Richardson D.A., Weeks K.M. A collapsed non-native RNA folding state. Nat. Struct. Biol. 2000, 7:362-366.
42. Perez-Salas U.A., Rangan P., Krueger S., Briber R.M., Thirumalai D., Woodson S.A. Compaction of a bacterial group I ribozyme coincides with the assembly of core helices. Biochemistry 2004, 43:1746-1753.
43. Takamoto K., Das R., He Q., Doniach S., Brenowitz M., Herschlag D., Chance M.R. Principles of RNA compaction: insights from the equilibrium folding pathway of the P4-P6 RNA domain in monovalent cations. J. Mol. Biol. 2004, 343:1195-1206.
44. 2+ interactions. Biochemistry 2007, 46:10266-10278.
45. Lemay J.F., Penedo J.C., Tremblay R., Lilley D.M., Lafontaine D.A. Folding of the adenine riboswitch. Chem. Biol. 2006, 13:857-868.
46. Celander D.W., Cech T.R. Visualizing the higher order folding of a catalytic RNA molecule. Science 1991, 251:401-407.
47. Balasubramanian B., Pogozelski W.K., Tullius T.D. DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc. Natl Acad. Sci. USA 1998, 95:9738-9743.
48. Noto R., Martorana V., Emanuele A., Fornill S.L. Comparison of the water perturbations induced by two small organic solutes: ab initio calculations and molecular dynamics simulation. J. Chem. Soc. Faraday Trans. 1995, 91:3803-3808.
49. Schwinefus J.J., Kuprian M.J., Lamppa J.W., Merker W.E., Dorn K.N., Muth G.W. Human telomerase RNA pseudoknot and hairpin thermal stability with glycine betaine and urea: preferential interactions with RNA secondary and tertiary structures. Biochemistry 2007, 46:9068-9079.
50. Hong J., Capp M.W., Anderson C.F., Saecker R.M., Felitsky D.J., Anderson M.W., Record M.T. Preferential interactions of glycine betaine and of urea with DNA: implications for DNA hydration and for effects of these solutes on DNA stability. Biochemistry 2004, 43:14744-14758.
51. Costa M., Deme E., Jacquier A., Michel F. Multiple tertiary interactions involving domain II of group II self-splicing introns. J. Mol. Biol. 1997, 267:520-536.
52. Cate J.H., Gooding A.R., Podell E., Zhou K., Golden B.L., Kundrot C.E., et al. Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 1996, 273:1678-1685.
53. Adams P.L., Stahley M.R., Kosek A.B., Wang J., Strobel S.A. Crystal structure of a self-splicing group I intron with both exons. Nature 2004, 430:45-50.
54. Lebars I., Legrand P., Aime A., Pinaud N., Fribourg S., Di Primo C. Exploring TAR-RNA aptamer loop-loop interaction by X-ray crystallography, UV spectroscopy and surface plasmon resonance. Nucleic Acids Res. 2008, 36:7146-7156.
55. Creamer T.P., Srinivasan R., Rose G.D. Modeling unfolded states of peptides and proteins. Biochemistry 1995, 34:16245-16250.
56. Shortle D., Ackerman M.S. Persistence of native-like topology in a denatured protein in 8 M urea. Science 2001, 293:487-489.
57. Stein A., Crothers D.M. Conformational changes of transfer RNA. The role of magnesium(II). Biochemistry 1976, 15:160-167.
58. Robinson C.V., Stokes R.H. Electrolyte Solutions 2002, Dover Publications, Minoeola, NY. 2nd revised edit.
59. McIvor R.A., McCarthy G.D., Grant G.A. Preparation and toxicity of some alkyl thiophosphates. Can. J. Chem. 1956, 34:1819-1832.
60. Petersheim M., Turner D.H. Base-stacking and base-pairing contributions to helix stability: thermodynamics of double-helix formation with CCGG, CCGGp, CCGGAp, CCGGUp, and ACCGGUp. Biochemistry 1983, 22:256-263.
61. Draper D.E., Bukhman Y.V., Gluick T.C. Thermal methods for the analysis of RNA folding pathways. Current Protocols in Nucleic Acid Chemistry 2000, John Wiley & Sons, New York, section 11.3. S.L. Beaucage, D.E. Bergstrom, G.D. Glick, R.A. Jones (Eds.).
62. Press W.H., Teukolsky S.A., Vetterling W.T., Flannery B.P. Numerical Recipes in C 1992, Cambridge University Press, Cambridge, MA.
63. Das R., Laederach A., Pearlman S.M., Herschlag D., Altman R.B. SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA 2005, 11:344-354.
64. Svergun D.I., Koch M.J.H. Small-angle scattering studies of biological macromolecules in solution. Rep. Prog. Phys. 2003, 66:1735-1782.
65. Svergun D.I., Barberato C., Koch M.J.H. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 1995, 25:495-503.
66. Tsodikov O.V., Record M.T., Sergeev Y.V. Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. J. Comput. Chem. 2002, 23:600-609.
67. Richmond T.J., Richards F.M. Packing of α-helices: geometrical constraints and contact areas. J. Mol. Biol. 1978, 119:537-555.
68. Courtenay E.S., Capp M.W., Anderson C.F., Record M.T. Vapor pressure osmometry studies of osmolyte-protein interactions: implications for the action of osmoprotectants in vivo and for the interpretation of "osmotic stress" experiments in vitro. Biochemistry 2000, 39:4455-4471.
69. Pauling L. The Nature of the Chemical Bond 1960, Cornell University Press, Ithaca, NY.