Structural principles of nucleoside selectivity in a 2′- deoxyguanosine riboswitch

Nature Chemical Biology

Volumn 7, Issue 10, 2011, Pages 748-755

  Pikovskaya, Olga ^a   Polonskaia, Anna ^a   Patel, Dinshaw J ^a   Serganov, Alexander ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYGUANOSINE; DEOXYGUANOSINE PHOSPHATE; GUANOSINE; GUANOSINE PHOSPHATE; NUCLEIC ACID BASE; NUCLEOSIDE; PURINE; RNA;

ARTICLE; BIOENGINEERING; BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; COMPARATIVE STUDY; CRYSTAL STRUCTURE; LIGAND BINDING; MESOPLASMA FLORUM; PRIORITY JOURNAL; RIBOSWITCH;

BACTERIA (MICROORGANISMS); MESOPLASMA FLORUM;

EID: 80052967464     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.631     Document Type: Article

References (50)

1. Nudler, E. & Mironov, A. S. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 29, 11-17 (2004). (Pubitemid 38068475)
2. Roth, A. & Breaker, R. R. The structural and functional diversity of metabolite-binding riboswitches. Annu. Rev. Biochem. 78, 305-334 (2009).
3. Serganov, A. & Patel, D. J. Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat. Rev. Genet. 8, 776-790 (2007). (Pubitemid 47429208)
4. Montange, R. K. & Batey, R. T. Riboswitches: emerging themes in RNA structure and function. Annu. Rev. Biophys. 37, 117-133 (2008).
5. 1 contains an unusually small aptamer domain. Nat. Struct. Mol. Biol. 14, 308-317 (2007). (Pubitemid 46608347)
6. Corbino, K. A. et al. Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria. Genome Biol. 6, R70 (2005).
7. Epshtein, V., Mironov, A. S. & Nudler, E. The riboswitch-mediated control of sulfur metabolism in bacteria. Proc. Natl. Acad. Sci. USA 100, 5052-5056 (2003). (Pubitemid 36542656)
8. Fuchs, R. T., Grundy, F. J. & Henkin, T. M. The S (MK) box is a new SAM-binding RNA for translational regulation of SAM synthetase. Nat. Struct. Mol. Biol. 13, 226-233 (2006). (Pubitemid 43348508)
9. McDaniel, B. A., Grundy, F. J., Artsimovitch, I. & Henkin, T. M. Transcription termination control of the S box system: direct measurement of S-adenosylmethionine by the leader RNA. Proc. Natl. Acad. Sci. USA 100, 3083-3088 (2003). (Pubitemid 36356543)
10. Serganov, A. Determination of riboswitch structures: light at the end of the tunnel? RNA Biol. 7, 98-103 (2010).
11. Mandal, M. & Breaker, R. R. Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat. Struct. Mol. Biol. 11, 29-35 (2004). (Pubitemid 38173438)
12. Mandal, M., Boese, B., Barrick, J. E., Winkler, W. C. & Breaker, R. R. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113, 577-586 (2003). (Pubitemid 36694183)
13. Kim, J. N., Roth, A. & Breaker, R. R. Guanine riboswitch variants from Mesoplasma florum selectively recognize 2′-deoxyguanosine. Proc. Natl. Acad. Sci. USA 104, 16092-16097 (2007). (Pubitemid 350099369)
14. Batey, R. T., Gilbert, S. D. & Montange, R. K. Structure of a natural guanineresponsive riboswitch complexed with the metabolite hypoxanthine. Nature 432, 411-415 (2004). (Pubitemid 39551677)
15. Serganov, A. et al. Structural basis for discriminative regulation of gene expression by adenine-and guanine-sensing mRNAs. Chem. Biol. 11, 1729-1741 (2004). (Pubitemid 39651306)
16. Noeske, J. et al. An intermolecular base triple as the basis of ligand specificity and affinity in the guanine-and adenine-sensing riboswitch RNAs. Proc. Natl. Acad. Sci. USA 102, 1372-1377 (2005). (Pubitemid 40209177)
17. Edwards, A. L. & Batey, R. T. A structural basis for the recognition of 2′-deoxyguanosine by the purine riboswitch. J. Mol. Biol. 385, 938-948 (2009).
18. Gardner, P. P. et al. Rfam: updates to the RNA families database. Nucleic Acids Res. 37, D136-D140 (2009).
19. Lemay, J. F. & Lafontaine, D. A. Core requirements of the adenine riboswitch aptamer for ligand binding. RNA 13, 339-350 (2007).
20. Mulhbacher, J. & Lafontaine, D. A. Ligand recognition determinants of guanine riboswitches. Nucleic Acids Res. 35, 5568-5580 (2007). (Pubitemid 47423928)
21. De La Peña, M., Dufour, D. & Gallego, J. Three-way RNA junctions with remote tertiary contacts: a recurrent and highly versatile fold. RNA 15, 1949-1964 (2009).
22. Lemay, J. F., Penedo, J. C., Tremblay, R., Lilley, D. M. & Lafontaine, D. A. Folding of the adenine riboswitch. Chem. Biol. 13, 857-868 (2006). (Pubitemid 44247776)
23. Gilbert, S. D., Love, C. E., Edwards, A. L. & Batey, R. T. Mutational analysis of the purine riboswitch aptamer domain. Biochemistry 46, 13297-13309 (2007). (Pubitemid 350136370)
24. Gilbert, S. D., Mediatore, S. J. & Batey, R. T. Modified pyrimidines specifically bind the purine riboswitch. J. Am. Chem. Soc. 128, 14214-14215 (2006). (Pubitemid 44707704)
25. Gilbert, S. D., Reyes, F. E., Edwards, A. L. & Batey, R. T. Adaptive ligand binding by the purine riboswitch in the recognition of guanine and adenine analogs. Structure 17, 857-868 (2009).
26. Gilbert, S. D., Stoddard, C. D., Wise, S. J. & Batey, R. T. Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain. J. Mol. Biol. 359, 754-768 (2006). (Pubitemid 43767264)
27. Jain, N., Zhao, L., Liu, J. D. & Xia, T. Heterogeneity and dynamics of the ligand recognition mode in purine-sensing riboswitches. Biochemistry 49, 3703-3714 (2010).
28. Gilbert, S. D., Rambo, R. P., Van Tyne, D. & Batey, R. T. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat. Struct. Mol. Biol. 15, 177-182 (2008). (Pubitemid 351207508)
29. MK riboswitch reveal the SAM-dependent translation inhibition mechanism. Nat. Struct. Mol. Biol. 15, 1076-1083 (2008).
30. Montange, R. K. & Batey, R. T. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441, 1172-1175 (2006). (Pubitemid 43990740)
31. Edwards, A. L., Reyes, F. E., Heroux, A. & Batey, R. T. Structural basis for recognition of S-adenosylhomocysteine by riboswitches. RNA 16, 2144-2155 (2010).
32. Wacker, A. et al. Structure and dynamics of the deoxyguanosine-sensing riboswitch studied by NMR-spectroscopy. Nucleic Acids Res. published online, doi:10.1093/nar/gkr238 (16 May 2011).
33. Stoddard, C. D., Gilbert, S. D. & Batey, R. T. Ligand-dependent folding of the three-way junction in the purine riboswitch. RNA 14, 675-684 (2008). (Pubitemid 351480880)
34. Greenleaf, W. J., Frieda, K. L., Foster, D. A., Woodside, M. T. & Block, S. M. Direct observation of hierarchical folding in single riboswitch aptamers. Science 319, 630-633 (2008). (Pubitemid 351197067)
35. Brenner, M. D., Scanlan, M. S., Nahas, M. K., Ha, T. & Silverman, S. K. Multivector fluorescence analysis of the xpt guanine riboswitch aptamer domain and the conformational role of guanine. Biochemistry 49, 1596-1605 (2010).
36. Ottink, O. M. et al. Ligand-induced folding of the guanine-sensing riboswitch is controlled by a combined predetermined induced fit mechanism. RNA 13, 2202-2212 (2007). (Pubitemid 350127561)
37. Noeske, J., Schwalbe, H. & Wohnert, J. Metal-ion binding and metal-ion induced folding of the adenine-sensing riboswitch aptamer domain. Nucleic Acids Res. 35, 5262-5273 (2007). (Pubitemid 47394209)
38. Rieder, R., Lang, K., Graber, D. & Micura, R. Ligand-induced folding of the adenosine deaminase A-riboswitch and implications on riboswitch translational control. ChemBioChem 8, 896-902 (2007). (Pubitemid 47194838)
39. Noeske, J. et al. Interplay of 'induced fit' and preorganization in the ligand induced folding of the aptamer domain of the guanine binding riboswitch. Nucleic Acids Res. 35, 572-583 (2007). (Pubitemid 46232073)
40. Buck, J., Noeske, J., Wohnert, J. & Schwalbe, H. Dissecting the influence of Mg2+ on 3D architecture and ligand-binding of the guanine-sensing riboswitch aptamer domain. Nucleic Acids Res. 38, 4143-4153 (2010).
41. Serganov, A., Huang, L. & Patel, D. J. Structural insights into amino acid binding and gene control by a lysine riboswitch. Nature 455, 1263-1267 (2008).
42. Serganov, A., Huang, L. & Patel, D. J. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 458, 233-237 (2009).
43. Delfosse, V. et al. Riboswitch structure: an internal residue mimicking the purine ligand. Nucleic Acids Res. 38, 2057-2068 (2010).
44. Dixon, N. et al. Reengineering orthogonally selective riboswitches. Proc. Natl. Acad. Sci. USA 107, 2830-2835 (2010).
45. Kim, J. N. et al. Design and antimicrobial action of purine analogues that bind guanine riboswitches. ACS Chem. Biol. 4, 915-927 (2009).
46. Mulhbacher, J. et al. Novel riboswitch ligand analogs as selective inhibitors of guanine-related metabolic pathways. PLoS Pathog. 6, e1000865 (2010).
47. Schneider, T. R. & Sheldrick, G. M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (2002). (Pubitemid 35169744)
48. De La Fortelle, E. I. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494 (1997). (Pubitemid 27085618)
49. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002). (Pubitemid 35337293)
50. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997). (Pubitemid 27235885)