An energetically beneficial leader-linker interaction abolishes ligand-binding cooperativity in glycine riboswitches

RNA

Volumn 18, Issue 3, 2012, Pages 496-507

  Sherman, Eileen M ^a   Esquiaqui, Jackie ^a   Elsayed, Galal ^a   Ye, Jing Dong ^a  

^a UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Cooperativity; Glycine; Kink turn motif; Leader linker interaction; Riboswitch; Synergistic

Indexed keywords

APTAMER; GLYCINE; NUCLEOTIDE;

ARTICLE; BINDING AFFINITY; ENERGY TRANSFER; LEADER LINER INTERACTION; LIGAND BINDING; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN RNA BINDING; RIBOSWITCH;

5' UNTRANSLATED REGIONS; APTAMERS, NUCLEOTIDE; BASE PAIRING; BASE SEQUENCE; GLYCINE; LIGANDS; MUTATION; NUCLEIC ACID CONFORMATION; RIBOSWITCH; RNA, BACTERIAL; RNA, MESSENGER; SEQUENCE ALIGNMENT;

EID: 84857438025     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.031286.111     Document Type: Article

References (45)

1. Barrick JE, Corbino KA, Winkler WC, Nahvi A, Mandal M, Collins J, Lee M, Roth A, Sudarsan N, Jona I, et al. 2004. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc Natl Acad Sci 101: 6421-6426. (Pubitemid 38585989)
2. Birdsall DL, Finer-Moore J, Stroud RM. 1996. Entropy in bi-substrate enzymes: proposed role of an alternate site in chaperoning substrate into, and products out of, thymidylate synthase. J Mol Biol 255: 522-535. (Pubitemid 26105574)
3. Blouin S, Lafontaine DA. 2007. A loop loop interaction and a K-turn motif located in the lysine aptamer domain are important for the riboswitch gene regulation control. RNA 13: 1256-1267. (Pubitemid 47080471)
4. Breaker RR. 2010. Riboswitches and the RNA world. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a003566.
5. Breaker RR. 2011. Prospects for riboswitch discovery and analysis. Mol Cell 43: 867-879.
6. Brenowitz M, Chance MR, Dhavan G, Takamoto K. 2002. Probing the structural dynamics of nucleic acids by quantitative time-resolved and equilibrium hydroxyl radical "footprinting". Curr Opin Struct Biol 12: 648-653. (Pubitemid 35449074)
7. Butler EB, Xiong Y, Wang J, Strobel SA. 2011. Structural basis of cooperative ligand binding by the glycine riboswitch. Chem Biol 18: 293-298.
8. Cheah MT, Wachter A, Sudarsan N, Breaker RR. 2007. Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 447: 497-500. (Pubitemid 46816734)
9. Cilley CD, Williamson JR. 1999. PACE analysis of RNA-peptide interactions. Methods Mol Biol 118: 129-141.
10. Cruz JA, Westhof E. 2011. Sequence-based identification of 3D structural modules in RNA with RMDetect. Nat Methods 8: 513-521.
11. Erion TV, Strobel SA. 2011. Identification of a tertiary interaction important for cooperative ligand binding by the glycine riboswitch. RNA 17: 74-84.
12. Fujiwara K, Okamura-Ikeda K, Motokawa Y. 1984. Mechanism of the glycine cleavage reaction. Further characterization of the intermediate attached to H-protein and of the reaction catalyzed by T-protein. J Biol Chem 259: 10664-10668. (Pubitemid 14031187)
13. Gardner PP, Daub J, Tate J, Moore BL, Osuch IH, Griffiths-Jones S, Finn RD, Nawrocki EP, Kolbe DL, Eddy SR, et al. 2011. Rfam: Wikipedia, clans and the "decimal" release. Nucleic Acids Res 39: D141-D145.
14. Goody TA, Melcher SE, Norman DG, Lilley DM. 2004. The kink-turn motif in RNA is dimorphic, and metal ion-dependent. RNA 10: 254-264. (Pubitemid 38129830)
15. Gordon L, Chervonenkis AY, Gammerman AJ, Shahmuradov IA, Solovyev VV. 2003. Sequence alignment kernel for recognition of promoter regions. Bioinformatics 19: 1964-1971. (Pubitemid 37322341)
16. Huang L, Serganov A, Patel DJ. 2010. Structural insights into ligand recognition by a sensing domain of the cooperative glycine riboswitch. Mol Cell 40: 774-786.
17. Khvorova A, Lescoute A, Westhof E, Jayasena SD. 2003. Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat Struct Biol 10: 708-712. (Pubitemid 37052408)
18. Kladwang W, Chou FC, Das R. 2012. Automated RNA structure prediction uncovers a missing link in double glycine riboswitches. J Am Chem Soc (in press).
19. Klein DJ, Schmeing TM, Moore PB, Steitz TA. 2001. The kink-turn: a new RNA secondary structure motif. EMBO J 20: 4214-4221. (Pubitemid 32751837)
20. Kwon M, Strobel SA. 2008. Chemical basis of glycine riboswitch cooperativity. RNA 14: 25-34.
21. Latham JA, Cech TR. 1989. Defining the inside and outside of a catalytic RNA molecule. Science 245: 276-282. (Pubitemid 19196644)
22. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR. 2010. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329: 845-848.
23. Lipfert J, Das R, Chu VB, Kudaravalli M, Boyd N, Herschlag D, Doniach S. 2007. Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. J Mol Biol 365: 1393-1406. (Pubitemid 46048825)
24. Lipfert J, Sim AY, Herschlag D, Doniach S. 2010. Dissecting electrostatic screening, specific ion binding, and ligand binding in an energetic model for glycine riboswitch folding. RNA 16: 708-719.
25. Liu J, Lilley DM. 2007. The role of specific 2′-hydroxyl groups in the stabilization of the folded conformation of kink-turn RNA. RNA 13: 200-210. (Pubitemid 46147896)
26. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM, Ruzzo WL, Breaker RR. 2004. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306: 275-279. (Pubitemid 39336872)
27. Martick M, Scott WG. 2006. Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126: 309-320. (Pubitemid 44092962)
28. Montange RK, Batey RT. 2006. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441: 1172-1175. (Pubitemid 43990740)
29. Pizer LI, Potochny ML. 1964. Nutritional and regulatory aspects of serine metabolism in Escherichia coli. J Bacteriol 88: 611-619.
30. Ravindran PP, Heroux A, Ye JD. 2011. Improvement of the crystallizability and expression of an RNA crystallization chaperone. J Biochem 150: 535-543.
31. Ravnikar PD, Somerville RL. 1987. Genetic characterization of a highly efficient alternate pathway of serine biosynthesis in Escherichia coli. J Bacteriol 169: 2611-2617. (Pubitemid 17104322)
32. Regulski EE, Breaker RR. 2008. In-line probing analysis of riboswitches. Methods Mol Biol 419: 53-67.
33. Roth A, Breaker RR. 2009. The structural and functional diversity of metabolite-binding riboswitches. Annu Rev Biochem 78: 305-334.
34. Schroeder KT, Daldrop P, Lilley DM. 2011. RNA tertiary interactions in a riboswitch stabilize the structure of a kink turn. Structure 19: 1233-1240.
35. Sclavi B, Sullivan M, Chance MR, Brenowitz M, Woodson SA. 1998. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science 279: 1940-1943.
36. Smith KD, Strobel SA. 2011. Interactions of the c-di-GMP riboswitch with its second messenger ligand. Biochem Soc Trans 39: 647-651.
37. Soukup GA, Breaker RR. 1999. Relationship between internucleotide linkage geometry and the stability of RNA. RNA 5: 1308-1325. (Pubitemid 29489813)
38. Trausch JJ, Ceres P, Reyes FE, Batey RT. 2011. The structure of a tetrahydrofolate-sensing riboswitch reveals two ligand binding sites in a single aptamer. Structure 19: 1413-1423.
39. Tripp HJ, Schwalbach MS, Meyer MM, Kitner JB, Breaker RR, Giovannoni SJ. 2009. Unique glycine-activated riboswitch linked to glycine-serine auxotrophy in SAR11. Environ Microbiol 11: 230-238.
40. Turner B, Lilley DM. 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.
41. Turner B, Melcher SE, Wilson TJ, Norman DG, Lilley DM. 2005. Induced fit of RNA on binding the L7Ae protein to the kink-turn motif. RNA 11: 1192-1200.
42. Wachter A, Tunc-Ozdemir M, Grove BC, Green PJ, Shintani DK, Breaker RR. 2007. Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19: 3437-3450.
43. Wakeman CA, Winkler WC. 2009. Structural probing techniques on natural aptamers. Methods Mol Biol 535: 115-133.
44. Wickiser JK, Winkler WC, Breaker RR, Crothers DM. 2005. The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol Cell 18: 49-60. (Pubitemid 40444647)
45. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415. (Pubitemid 37442169)