The Ligand-Free State of the TPP Riboswitch: A Partially Folded RNA Structure

Journal of Molecular Biology

Volumn 396, Issue 1, 2010, Pages 153-165

  Ali, Mona ^a   Lipfert, Jan ^b   Seifert, Soenke ^c   Herschlag, Daniel ^a   Doniach, Sebastian ^a  

^a STANFORD UNIVERSITY   (United States)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

riboswitch; RNA folding; RNA structure; small angle X ray scattering

Indexed keywords

COCARBOXYLASE;

ARTICLE; COMPUTER MODEL; COMPUTER PREDICTION; CONFORMATIONAL TRANSITION; DATA ANALYSIS SOFTWARE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RIBOSWITCH; RNA STRUCTURE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

EID: 74649084566     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.11.030     Document Type: Article

References (70)

1. Pyle A.M., and Green J.B. RNA folding. Curr. Opin. Struct. Biol. 5 (1995) 303-310
2. Coppins R.L., Hall K.B., and Groisman E.A. The intricate world of riboswitches. Curr. Opin. Microbiol. 10 (2007) 176-181
3. Nudler E., and Mironov A.S. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 29 (2004) 11-17
4. Schwalbe H., Buck J., Furtig B., Noeske J., and Wohnert J. Structures of RNA switches: insight into molecular recognition and tertiary structure. Angew. Chem. Int. Ed. Engl. 46 (2007) 1212-1219
5. Wakeman C.A., Winkler W.C., and Dann III C.E. Structural features of metabolite-sensing riboswitches. Trends Biochem. Sci. 32 (2007) 415-424
6. Mandal M., and Breaker R.R. Gene regulation by riboswitches. Nat. Rev. Mol. Cell Biol. 5 (2004) 451-463
7. Garst A.D., Heroux A., Rambo R.P., and Batey R.T. Crystal structure of the lysine riboswitch regulatory mRNA element. J. Biol. Chem. 283 (2008) 22347-22351
8. Batey R.T., Gilbert S.D., and Montange R.K. Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine. Nature 432 (2004) 411-415
9. Montange R.K., and Batey R.T. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441 (2006) 1172-1175
10. Dann III C.E., Wakeman C.A., Sieling C.L., Baker S.C., Irnov I., and Winkler W.C. Structure and mechanism of a metal-sensing regulatory RNA. Cell 130 (2007) 878-892
11. Serganov A., Polonskaia A., Phan A.T., Breaker R.R., and Patel D.J. Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 441 (2006) 1167-1171
12. Cochrane J.C., Lipchock S.V., and Strobel S.A. Structural investigation of the GlmS ribozyme bound to its catalytic cofactor. Chem. Biol. 14 (2007) 97-105
13. Serganov A., Huang L., and Patel D.J. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 458 (2009) 233-237
14. Klein D.J., and Ferre-D'Amare A.R. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313 (2006) 1752-1756
15. Ottink O.M., Rampersad S.M., Tessari M., Zaman G.J., Heus H.A., and Wijmenga S.S. Ligand-induced folding of the guanine-sensing riboswitch is controlled by a combined predetermined induced fit mechanism. RNA 13 (2007) 2202-2212
16. Lipfert J., Das R., Chu V.B., Kudaravalli M., Boyd N., Herschlag D., and Doniach S. Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. J. Mol. Biol. 365 (2007) 1393-1406
17. Greenleaf W.J., Frieda K.L., Foster D.A., Woodside M.T., and Block S.M. Direct observation of hierarchical folding in single riboswitch aptamers. Science 319 (2008) 630-633
18. Winkler W.C., Nahvi A., Sudarsan N., Barrick J.E., and Breaker R.R. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat. Struct. Biol. 10 (2003) 701-707
19. Thore S., Leibundgut M., and Ban N. Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 312 (2006) 1208-1211
20. Thore S., Frick C., and Ban N. Structural basis of thiamine pyrophosphate analogues binding to the eukaryotic riboswitch. J. Am. Chem. Soc. 130 (2008) 8116-8117
21. Lipfert J., and Doniach S. Small-angle X-ray scattering from RNA, proteins, and protein complexes. Annu. Rev. Biophys. Biomol. Struct. 36 (2007) 307-327
22. Koch M.H., Vachette P., and Svergun D.I. Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q. Rev. Biophys. 36 (2003) 147-227
23. Doniach S. Changes in biomolecular conformation seen by small angle X-ray scattering. Chem. Rev. 101 (2001) 1763-1778
24. Lipfert J., Herschlag D., and Doniach S. Riboswitch conformations revealed by small-angle X-ray scattering. Methods Mol. Biol. 540 (2009) 141-159
25. Russell R., Millett I.S., Doniach S., and Herschlag D. Small angle X-ray scattering reveals a compact intermediate in RNA folding. Nat. Struct. Biol. 7 (2000) 367-370
26. Phe and the catalytic domain of the B. subtilis RNase P RNA determined by small-angle X-ray scattering. Biochemistry 39 (2000) 11107-11113
27. Russell R., Millett I.S., Tate M.W., Kwok L.W., Nakatani B., Gruner S.M., et al. Rapid compaction during RNA folding. Proc. Natl Acad. Sci. USA 99 (2002) 4266-4271
28. Russell R., Zhuang X., Babcock H.P., Millett I.S., Doniach S., Chu S., and Herschlag D. Exploring the folding landscape of a structured RNA. Proc. Natl Acad. Sci. USA 99 (2002) 155-160
29. Das R., Kwok L.W., Millett I.S., Bai Y., Mills T.T., Jacob J., et al. The fastest global events in RNA folding: electrostatic relaxation and tertiary collapse of the Tetrahymena ribozyme. J. Mol. Biol. 332 (2003) 311-319
30. Das R., Mills T.T., Kwok L.W., Maskel G.S., Millett I.S., Doniach S., et al. Counterion distribution around DNA probed by solution X-ray scattering. Phys. Rev. Lett. 90 (2003) 188103
31. Takamoto K., Das R., He Q., Doniach S., Brenowitz M., Herschlag D., and 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. 343 (2004) 1195-1206
32. Kwok L.W., Shcherbakova I., Lamb J.S., Park H.Y., Andresen K., Smith H., et al. Concordant exploration of the kinetics of RNA folding from global and local perspectives. J. Mol. Biol. 355 (2006) 282-293
33. Glatter O., and Kratky O. Small Angle X-ray Scattering (1982), Academic Press, London, UK
34. Woodson S.A. Metal ions and RNA folding: a highly charged topic with a dynamic future. Curr. Opin. Chem. Biol. 9 (2005) 104-109
35. Draper D.E. RNA folding: thermodynamic and molecular descriptions of the roles of ions. Biophys. J. 95 (2008) 5489-5495
36. Draper D.E., Grilley D., and Soto A.M. Ions and RNA folding. Annu. Rev. Biophys. Biomol. Struct. 34 (2005) 221-243
37. Draper D.E. A guide to ions and RNA structure. RNA 10 (2004) 335-343
38. Chu V.B., Bai Y., Lipfert J., Herschlag D., and Doniach S. A repulsive field: advances in the electrostatics of the ion atmosphere. Curr. Opin. Chem. Biol. 12 (2008) 619-625
39. Aparicio R., Fischer H., Scott D.J., Verschueren K.H., Kulminskaya A.A., Eneiskaya E.V., et al. Structural insights into the beta-mannosidase from T. reesei obtained by synchrotron small-angle X-ray solution scattering enhanced by X-ray crystallography. Biochemistry 41 (2002) 9370-9375
40. Egea P.F., Rochel N., Birck C., Vachette P., Timmins P.A., and Moras D. Effects of ligand binding on the association properties and conformation in solution of retinoic acid receptors RXR and RAR. J. Mol. Biol. 307 (2001) 557-576
41. Fujisawa T., Kostyukova A., and Maeda Y. The shapes and sizes of two domains of tropomodulin, the P-end-capping protein of actin-tropomyosin. FEBS Lett. 498 (2001) 67-71
42. Lipfert J., Chu V.B., Bai Y., Herschlag D., and Doniach S. Low resolution models for nucleic acids from small-angle X-ray scattering with applications to electrostatic modeling. J. Appl. Crystallogr. 40 (2007) s229-s234
43. Lipfert J., Ouellet J., Norman D.G., Doniach S., and Lilley D.M. The complete VS ribozyme in solution studied by small-angle X-ray scattering. Structure 16 (2008) 1357-1367
44. Lukavsky P.J., Kim I., Otto G.A., and Puglisi J.D. Structure of HCV IRES domain II determined by NMR. Nat. Struct. Biol. 10 (2003) 1033-1038
45. Walter F., Murchie A.I., Thomson J.B., and Lilley D.M. Structure and activity of the hairpin ribozyme in its natural junction conformation: effect of metal ions. Biochemistry 37 (1998) 14195-14203
46. Murchie A.I., Thomson J.B., Walter F., and Lilley D.M. Folding of the hairpin ribozyme in its natural conformation achieves close physical proximity of the loops. Mol. Cell 1 (1998) 873-881
47. Shen Z., and Hagerman P.J. Conformation of the central, three-helix junction of the 5 S ribosomal RNA of Sulfolobus acidocaldarius. J. Mol. Biol. 241 (1994) 415-430
48. Serganov A.A., Masquida B., Westhof E., Cachia C., Portier C., Garber M., et al. The 16 S rRNA binding site of Thermus thermophilus ribosomal protein S15: comparison with Escherichia coli S15, minimum site and structure. RNA 2 (1996) 1124-1138
49. Tuschl T., Gohlke C., Jovin T.M., Westhof E., and Eckstein F. A three-dimensional model for the hammerhead ribozyme based on fluorescence measurements. Science 266 (1994) 785-789
50. Bassi G.S., Mollegaard N.E., Murchie A.I., von Kitzing E., and Lilley D.M. Ionic interactions and the global conformations of the hammerhead ribozyme. Nat. Struct. Biol. 2 (1995) 45-55
51. Brion P., and Westhof E. Hierarchy and dynamics of RNA folding. Annu. Rev. Biophys. Biomol. Struct. 26 (1997) 113-137
52. Lynch S.R., Gonzalez R.L., and Puglisi J.D. Comparison of X-ray crystal structure of the 30 S subunit-antibiotic complex with NMR structure of decoding site oligonucleotide-paromomycin complex. Structure 11 (2003) 43-53
53. Lafontaine D.A., Norman D.G., and Lilley D.M. The global structure of the VS ribozyme. EMBO J. 21 (2002) 2461-2471
54. Lilley D.M. Structures of helical junctions in nucleic acids. Q. Rev. Biophys. 33 (2000) 109-159
55. Parisien M., and Major F. The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452 (2008) 51-55
56. Das R., and Baker D. Automated de novo prediction of native-like RNA tertiary structures. Proc. Natl Acad. Sci. USA 104 (2007) 14664-14669
57. Jonikas M.A., Radmer R.J., Laederach A., Das R., Pearlman S., Herschlag D., and Altman R.B. Coarse-grained modeling of large RNA molecules with knowledge-based potentials and structural filters. RNA 15 (2009) 189-199
58. Svergun D., Barberato C., and Koch M.H. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28 (1995) 768-773
59. Garst A.D., and Batey R.T. A switch in time: detailing the life of a riboswitch. Biochim. Biophys. Acta 1789 (2009) 584-591
60. Lang K., Rieder R., and Micura R. Ligand-induced folding of the thiM TPP riboswitch investigated by a structure-based fluorescence spectroscopic approach. Nucleic Acids Res. 35 (2007) 5370-5378
61. Wachter A., Tunc-Ozdemir M., Grove B.C., Green P.J., Shintani D.K., and Breaker R.R. Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19 (2007) 3437-3450
62. Lipfert J., Millett I., Seifert S., and Doniach S. A sample holder for small-angle X-ray scattering static and flow cell measurements. Rev. Sci. Instrum. 77 (2006) 046108
63. Svergun D. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25 (1992) 495-503
64. Svergun D.I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76 (1999) 2879-2886
65. Kozin M., and Svergun D. Automated matching of high and low resolution structural models. J. Appl. Crystallogr. 34 (2001) 33-41
66. Volkov V., and Svergun D. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36 (2003) 860-864
67. Wriggers W., Milligan R.A., and McCammon J.A. Situs: a package for docking crystal structures into low-resolution maps from electron microscopy. J. Struct. Biol. 125 (1999) 185-195
68. Wriggers W., and Chacon P. Using Situs for the registration of protein structures with low-resolution bead models from X-ray solution scattering. J. Appl. Crystallogr. 34 (2001) 773-776
69. Pettersen E., Goddard T., Huang C., Couch G., Greenblatt M., Meng E., and Ferrin E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 13 (2004) 1605-1612
70. Humphrey, W., Dalke, A. & Schulten, K. (1996). VMD: Visual Molecular Dynamics. J. Mol. Graphics 14, 27-28, 33-38.