The expression platform and the aptamer: Cooperativity between Mg 2+ and ligand in the SAM-I riboswitch

Nucleic Acids Research

Volumn 41, Issue 3, 2013, Pages 1922-1935

  Hennelly, Scott P ^a   Novikova, Irina V ^a   Sanbonmatsu, Karissa Y ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; MAGNESIUM ION; PHOSPHOROTHIOIC ACID;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONCENTRATION (PARAMETERS); CONFORMATION; CONTROLLED STUDY; LIGAND BINDING; MOLECULAR INTERACTION; MOLECULAR PROBE; PRIORITY JOURNAL; RIBOSWITCH; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

CATIONS, DIVALENT; LIGANDS; MAGNESIUM; NUCLEIC ACID CONFORMATION; RIBOSWITCH; RNA, BACTERIAL; S-ADENOSYLMETHIONINE; THERMOANAEROBACTER;

EID: 84873632585     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks978     Document Type: Article

References (49)

1. Mandal M. and Breaker R.R. (2004) Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat. Struct. Mol. Biol., 11, 29-35
2. Winkler W.C., Cohen-Chalamish S. and Breaker R.R. (2002) An mRNA structure that controls gene expression by binding FMN. Proc. Natl Acad. Sci. USA, 99, 15908-15913
3. Winkler W.C., Nahvi A., Sudarsan N., Barrick J.E. and Breaker R.R. (2003) An mRNA structure that controls gene expression by binding S- adenosylmethionine. Nat. Struct. Biol., 10, 701-707
4. Mandal M., Lee M., Barrick J.E., Weinberg Z., Emilsson G.M., Ruzzo W.L. and Breaker R.R. (2004) A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science, 306, 275-279
5. Sudarsan N., Wickiser J.K., Nakamura S., Ebert M.S. and Breaker R.R. (2003) An mRNA structure in bacteria that controls gene expression by binding lysine. Genes Dev., 17, 2688-2697
6. Sudarsan N., Lee E.R., Weinberg Z., Moy R.H., Kim J.N., Link K.H. and Breaker R.R. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science, 321, 411-413
7. Nahvi A., Barrick J.E. and Breaker R.R. (2004) Coenzyme B12 riboswitches are widespread genetic control elements in prokaryotes. Nucleic Acids Res., 32, 143-150
8. Winkler W., Nahvi A. and Breaker R.R. (2002) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature, 419, 952-956
9. Gong B., Klein D.J., Ferre-D'Amare A.R. and Carey P.R. The glmS ribozyme tunes the catalytically critical pK(a) of its coenzyme glucosamine-6-phosphate. J. Am. Chem. Soc., 133, 14188-14191
10. Chu V.B., Bai Y., Lipfert J., Herschlag D. and Doniach S. (2008) A repulsive field: advances in the electrostatics of the ion atmosphere. Curr. Opin. Chem. Biol., 12, 619-625
11. Baird N.J. and Ferre-D'Amare A.R. Idiosyncratically tuned switching behavior of riboswitch aptamer domains revealed by comparative small-angle X-ray scattering analysis. RNA, 16, 598-609
12. Kwon M. and Strobel S.A. (2008) Chemical basis of glycine riboswitch cooperativity. RNA, 14, 25-34
13. Chen B., Zuo X., Wang Y.X. and Dayie T.K. (2012) Multiple conformations of SAM-II riboswitch detected with SAXS and NMR spectroscopy. Nucleic Acids Res., 40, 3117-3130
14. Kulshina N., Edwards T.E. and Ferre-D'Amare A.R. Thermodynamic analysis of ligand binding and ligand binding-induced tertiary structure formation by the thiamine pyrophosphate riboswitch. RNA, 16, 186-196
15. Stoddard C.D., Montange R.K., Hennelly S.P., Rambo R.P., Sanbonmatsu K.Y. and Batey R.T. (2010) Free state conformational sampling of the SAM-I riboswitch aptamer domain. Structure, 18, 787-797
16. Heppell B. and Lafontaine D.A. (2008) Folding of the SAM aptamer is determined by the formation of a K-turn-dependent pseudoknot. Biochemistry, 47, 1490-1499
17. Lipfert J., Das R., Chu V.B., Kudaravalli M., Boyd N., Herschlag D. and Doniach S. (2007) Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. J. Mol. Biol., 365, 1393-1406
18. Lipfert J., Sim A.Y., Herschlag D. and Doniach S. Dissecting electrostatic screening, specific ion binding, and ligand binding in an energetic model for glycine riboswitch folding. RNA, 16, 708-719
19. Ali M., Lipfert J., Seifert S., Herschlag D. and Doniach S. (2010) The ligand-free state of the TPP riboswitch: a partially folded RNA structure. J. Mol. Biol., 396, 153-165
20. Hennelly S.P. and Sanbonmatsu K.Y. Tertiary contacts control switching of the SAM-I riboswitch. Nucleic Acids Res., 39, 2416-2431
21. Moghaddam S., Caliskan G., Chauhan S., Hyeon C., Briber R.M., Thirumalai D. and Woodson S.A. (2009) Metal ion dependence of cooperative collapse transitions in RNA. J. Mol. Biol., 393, 753-764
22. Heilman-Miller S.L., Pan J., Thirumalai D. and Woodson S.A. (2001) Role of counterion condensation in folding of the Tetrahymena ribozyme: part II. Counterion-dependence of folding kinetics. J. Mol. Biol., 309, 57-68
23. Heilman-Miller S.L., Thirumalai D. and Woodson S.A. (2001) Role of counterion condensation in folding of the Tetrahymena ribozyme: part I. Equilibrium stabilization by cations. J. Mol. Biol., 306, 1157-1166
24. Lipfert J., Herschlag D. and Doniach S. (2009) Riboswitch conformations revealed by small-angle X-ray scattering. Methods Mol. Biol., 540, 141-159
25. Rangan P. and Woodson S.A. (2003) Structural requirement for Mg2+binding in the group I intron core. J. Mol. Biol., 329, 229-238
26. Woodson S.A. Compact intermediates in RNA folding. Annu. Rev. Biophys., 39, 61-77
27. Mortimer S.A. and Weeks K.M. (2007) A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. J. Am. Chem. Soc., 129, 4144-4145
28. Heppell B., Blouin S., Dussault A.M., Mulhbacher J., Ennifar E., Penedo J.C. and Lafontaine D.A. Molecular insights into the ligand-controlled organization of the SAM-I riboswitch. Nat. Chem. Biol., 7, 384-392
29. McDaniel B.A., Grundy F.J. and Henkin T.M. (2005) A tertiary structural element in S box leader RNAs is required for S-adenosylmethionine-directed transcription termination. Mol. Microbiol., 57, 1008-1021
30. Tomsic J., McDaniel B.A., Grundy F.J. and Henkin T.M. (2008) 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, 823-833
31. Epshtein V., Mironov A.S. and Nudler E. (2003) The riboswitch-mediated control of sulfur metabolism in bacteria. Proc. Natl Acad. Sci. USA, 100, 5052-5056
32. Gherghe C.M., Shajani Z., Wilkinson K.A., Varani G. and Weeks K.M. (2008) Strong correlation between SHAPE chemistry and the generalized NMR order parameter (S2) in RNA. J. Am. Chem. Soc., 130, 12244-12245
33. Black C.B. and Cowan J.A. (1994) Magnesium Activation of Ribonuclease H Evidence for One Catalytic Metal Ion? Inorg. Chem., 33, 5805-5808
34. Brown I.D(1988) What factors determine cation coordination number? Acta Crystallogr., B44, 545-553
35. Christian E.L. and Yarus M. (1993) Metal coordination sites that contribute to structure and catalysis in the group I intron from Tetrahymena. Biochemistry, 32, 4475-4480
36. Christian E.L. and Yarus M. (1992) Analysis of the role of phosphate oxygens in the group I intron from Tetrahymena. J. Mol. Biol., 228, 743-758
37. Strauss-Soukup J.K. and Strobel S.A. (2000) A chemical phylogeny of group I introns based upon interference mapping of a bacterial ribozyme. J. Mol. Biol., 302, 339-358
38. Ryder S.P. and Strobel S.A. (1999) Nucleotide analog interference mapping. Methods, 18, 38-50
39. Montange R.K. and Batey R.T. (2006) Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature, 441, 1172-1175
40. Griffiths A.D., Potter B.V. and Eperon I.C. (1987) Stereospecificity of nucleases towards phosphorothioate-substituted RNA: stereochemistry of transcription by T7 RNA polymerase. Nucleic Acids Res., 15, 4145-4162
41. Turner B. and Lilley D.M. (2008) The importance of G.A hydrogen bonding in the metal ion- and protein-induced folding of a kink turn RNA. J. Mol. Biol., 381, 431-442
42. Grilley D., Misra V., Caliskan G. and Draper D.E. (2007) Importance of partially unfolded conformations for Mg(2+)- induced folding of RNA tertiary structure: structural models and free energies of Mg2+interactions. Biochemistry, 46, 10266-10278
43. Lambert D., Leipply D., Shiman R. and Draper D.E. (2009) The influence of monovalent cation size on the stability of RNA tertiary structures. J. Mol. Biol., 390, 791-804
44. Grilley D., Soto A.M. and Draper D.E. (2006) Mg2+-RNA interaction free energies and their relationship to the folding of RNA tertiary structures. Proc. Natl Acad. Sci. USA, 103, 14003-14008
45. Leipply D. and Draper D.E. Evidence for a thermodynamically distinct Mg2+ion associated with formation of an RNA tertiary structure. J. Am. Chem. Soc., 133, 13397-13405
46. Behrouzi R., Roh J.H., Kilburn D., Briber R.M. and Woodson S.A. (2012) Cooperative tertiary interaction network guides RNA folding. Cell, 149, 348-357
47. Hayes R.L., Noel J.K., Mohanty U., Whitford P.C., Hennelly S.P., Onuchic J.N. and Sanbonmatsu K.Y. (2012) Magnesium fluctuations modulate RNA dynamics in the SAM-I riboswitch. J. Am. Chem. Soc., 134, 12043-12053
48. Wickiser J.K., Winkler W.C., Breaker R.R. and Crothers D.M. (2005) The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol. Cell, 18, 49-60
49. Lemay J.F., Desnoyers G., Blouin S., Heppell B., Bastet L., St-Pierre P., Masse E. and Lafontaine D.A. (2011) Comparative study between transcriptionally- and translationally-acting adenine riboswitches reveals key differences in riboswitch regulatory mechanisms. PLoS Genet., 7, e1001278