A disconnect between high-affinity binding and efficient regulation by antifolates and purines in the tetrahydrofolate riboswitch

Chemistry and Biology

Volumn 21, Issue 2, 2014, Pages 205-216

  Trausch, Jeremiah J ^a   Batey, Robert T ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; BINDING SITES; FOLIC ACID ANTAGONISTS; LEUCOVORIN; METHOTREXATE; MOLECULAR DOCKING SIMULATION; NUCLEIC ACID CONFORMATION; PURINES; RIBOSWITCH; TETRAHYDROFOLATES; TRANSCRIPTION TERMINATION, GENETIC;

EID: 84894462887     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.11.012     Document Type: Article

References (51)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. T.D. Ames, D.A. Rodionov, Z. Weinberg, and R.R. Breaker A eubacterial riboswitch class that senses the coenzyme tetrahydrofolate Chem. Biol. 17 2010 681 685
3. J.E. Barrick, and R.R. Breaker The distributions, mechanisms, and structures of metabolite-binding riboswitches Genome Biol. 8 2007 R239
4. R.T. Batey, S.D. Gilbert, and R.K. Montange Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxanthine Nature 432 2004 411 415
5. T.G. Battye, L. Kontogiannis, O. Johnson, H.R. Powell, and A.G. Leslie iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM Acta Crystallogr. D Biol. Crystallogr. 67 2011 271 281
6. B.D. Bennett, E.H. Kimball, M. Gao, R. Osterhout, S.J. Van Dien, and J.D. Rabinowitz Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli Nat. Chem. Biol. 5 2009 593 599
7. A. Bermingham, and J.P. Derrick The folic acid biosynthesis pathway in bacteria: evaluation of potential for antibacterial drug discovery BioEssays 24 2002 637 648
8. K.F. Blount, and R.R. Breaker Riboswitches as antibacterial drug targets Nat. Biotechnol. 24 2006 1558 1564
9. J.T. Bolin, D.J. Filman, D.A. Matthews, R.C. Hamlin, and J. Kraut Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 A resolution. I. General features and binding of methotrexate J. Biol. Chem. 257 1982 13650 13662
10. R.R. Breaker Riboswitches and the RNA world Cold Spring Harb. Perspect. Biol. 4 2012 4
11. A.T. Brünger, and L.M. Rice Crystallographic refinement by simulated annealing: methods and applications Methods Enzymol. 277 1997 243 269
12. C. Bystroff, S.J. Oatley, and J. Kraut Crystal structures of Escherichia coli dihydrofolate reductase: the NADP+ holoenzyme and the folate.NADP+ ternary complex. Substrate binding and a model for the transition state Biochemistry 29 1990 3263 3277
13. P. Ceres, A.D. Garst, J.G. Marcano-Velazquez, and R.T. Batey Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices ACS Synth. Biol 2 2013 463 472
14. P. Ceres, J.J. Trausch, and R.T. Batey Engineering modular 'ON' RNA switches using biological components Nucleic Acids Res. 41 2013 10449 10461
15. E. Cressina, L.H. Chen, C. Abell, F.J. Leeper, and A.G. Smith Fragment screening against the thiamine pyrophosphate riboswitch thiM Chem. Sci. 2 2011 157 165
16. P. Daldrop, F.E. Reyes, D.A. Robinson, C.M. Hammond, D.M. Lilley, R.T. Batey, and R. Brenk Novel ligands for a purine riboswitch discovered by RNA-ligand docking Chem. Biol. 18 2011 324 335
17. C.E. Dann 3rd, C.A. Wakeman, C.L. Sieling, S.C. Baker, I. Irnov, and W.C. Winkler Structure and mechanism of a metal-sensing regulatory RNA Cell 130 2007 878 892
18. K.E. Deigan, and A.R. Ferré-D'Amaré Riboswitches: discovery of drugs that target bacterial gene-regulatory RNAs Acc. Chem. Res. 44 2011 1329 1338
19. N. Dixon, J.N. Duncan, T. Geerlings, M.S. Dunstan, J.E. McCarthy, D. Leys, and J. Micklefield Reengineering orthogonally selective riboswitches Proc. Natl. Acad. Sci. USA 107 2010 2830 2835
20. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
21. A.D. Garst, and R.T. Batey A switch in time: detailing the life of a riboswitch Biochim. Biophys. Acta 1789 2009 584 591
22. A.D. Garst, A. Héroux, R.P. Rambo, and R.T. Batey Crystal structure of the lysine riboswitch regulatory mRNA element J. Biol. Chem. 283 2008 22347 22351
23. A.D. Garst, E.B. Porter, and R.T. Batey Insights into the regulatory landscape of the lysine riboswitch J. Mol. Biol. 423 2012 17 33
24. S.D. Gilbert, and R.T. Batey Monitoring RNA-ligand interactions using isothermal titration calorimetry Methods Mol. Biol. 540 2009 97 114
25. S.D. Gilbert, S.J. Mediatore, and R.T. Batey Modified pyrimidines specifically bind the purine riboswitch J. Am. Chem. Soc. 128 2006 14214 14215
26. S.D. Gilbert, C.D. Stoddard, S.J. Wise, and R.T. Batey Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain J. Mol. Biol. 359 2006 754 768
27. N. Gonen, and Y.G. Assaraf Antifolates in cancer therapy: structure, activity and mechanisms of drug resistance Drug resistance updates: reviews and commentaries in antimicrobial and anticancer chemotherapy 15 2012 183 210
28. L. Guan, and M.D. Disney Recent advances in developing small molecules targeting RNA ACS Chem. Biol. 7 2012 73 86
29. A. Haller, M.F. Soulière, and R. Micura The dynamic nature of RNA as key to understanding riboswitch mechanisms Acc. Chem. Res. 44 2011 1339 1348
30. L. Huang, S. Ishibe-Murakami, D.J. Patel, and A. Serganov Long-range pseudoknot interactions dictate the regulatory response in the tetrahydrofolate riboswitch Proc. Natl. Acad. Sci. USA 108 2011 14801 14806
31. V. Illarionova, W. Eisenreich, M. Fischer, C. Haussmann, W. Romisch, G. Richter, and A. Bacher Biosynthesis of tetrahydrofolate. Stereochemistry of dihydroneopterin aldolase J. Biol. Chem. 277 2002 28841 28847
32. S. Jabrin, S. Ravanel, B. Gambonnet, R. Douce, and F. Rébeillé One-carbon metabolism in plants. Regulation of tetrahydrofolate synthesis during germination and seedling development Plant Physiol. 131 2003 1431 1439
33. S. Kariluoto, M. Edelmann, M. Herranen, A.M. Lampi, A. Shmelev, H. Salovaara, M. Korhola, and V. Piironen Production of folate by bacteria isolated from oat bran Int. J. Food Microbiol. 143 2010 41 47
34. C. Keshava, N. Keshava, W.Z. Whong, J. Nath, and T.M. Ong Inhibition of methotrexate-induced chromosomal damage by folinic acid in V79 cells Mutat. Res. 397 1998 221 228
35. E.R. Lee, K.F. Blount, and R.R. Breaker Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression RNA Biol. 6 2009 187 194
36. J.F. Lemay, G. Desnoyers, S. Blouin, B. Heppell, L. Bastet, P. St-Pierre, E. Massé, and D.A. Lafontaine Comparative study between transcriptionally- and translationally-acting adenine riboswitches reveals key differences in riboswitch regulatory mechanisms PLoS Genet. 7 2011 e1001278
37. J. Mulhbacher, E. Brouillette, M. Allard, L.C. Fortier, F. Malouin, and D.A. Lafontaine Novel riboswitch ligand analogs as selective inhibitors of guanine-related metabolic pathways PLoS Pathog. 6 2010 e1000865
38. L.S. Reed, and M.C. Archer Oxidation of tetrahydrofolic acid by air J. Agric. Food Chem. 28 1980 801 805
39. F.E. Reyes, A.D. Garst, and R.T. Batey Strategies in RNA crystallography Methods Enzymol. 469 2009 119 139
40. M. Saraste, and A. Musacchio Backwards and forwards binding Nat. Struct. Biol. 1 1994 835 837
41. J.M. Scott, and D.G. Weir Folic acid, homocysteine and one-carbon metabolism: a review of the essential biochemistry J. Cardiovasc. Risk 5 1998 223 227
42. A. Serganov, and E. Nudler A decade of riboswitches Cell 152 2013 17 24
43. A. Serganov, and D.J. Patel Metabolite recognition principles and molecular mechanisms underlying riboswitch function Annu. Rev. Biophys. 41 2012 343 370
44. A. Serganov, L. Huang, and D.J. Patel Structural insights into amino acid binding and gene control by a lysine riboswitch Nature 455 2008 1263 1267
45. N. Sudarsan, S. Cohen-Chalamish, S. Nakamura, G.M. Emilsson, and R.R. Breaker Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine Chem. Biol. 12 2005 1325 1335
46. S. Thore, C. Frick, and N. Ban Structural basis of thiamine pyrophosphate analogues binding to the eukaryotic riboswitch J. Am. Chem. Soc. 130 2008 8116 8117
47. J. Tomsic, B.A. McDaniel, F.J. Grundy, and T.M. Henkin Natural variability in S-adenosylmethionine (SAM)-dependent riboswitches: S-box elements in bacillus subtilis exhibit differential sensitivity to SAM In vivo and in vitro J. Bacteriol. 190 2008 823 833
48. J.J. Trausch, P. Ceres, F.E. Reyes, and R.T. Batey The structure of a tetrahydrofolate-sensing riboswitch reveals two ligand binding sites in a single aptamer Structure 19 2011 1413 1423
49. P.Y. Watson, and M.J. Fedor The glmS riboswitch integrates signals from activating and inhibitory metabolites in vivo Nat. Struct. Mol. Biol. 18 2011 359 363
50. J.K. Wickiser, W.C. Winkler, R.R. Breaker, and D.M. Crothers The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch Mol. Cell 18 2005 49 60
51. S.N. Wilson-Mitchell, F.J. Grundy, and T.M. Henkin Analysis of lysine recognition and specificity of the Bacillus subtilis L box riboswitch Nucleic Acids Res. 40 2012 5706 5717