Riboswitches: Emerging themes in RNA structure and function

Annual Review of Biophysics

Volumn 37, Issue , 2008, Pages 117-133

  Montange, Rebecca K ^a   Batey, Robert T ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Aptamer; Crystallography; Gene regulation; Noncoding RNA; RNA folding

Indexed keywords

COCARBOXYLASE; PURINE; RNA; UNTRANSLATED RNA; RNA BINDING PROTEIN; ADENINE; CYANOCOBALAMIN; FLAVINE MONONUCLEOTIDE; GLUCOSAMINE PHOSPHATE ACETYLTRANSFERASE; GLYCINE; GUANINE; LYSINE; MAGNESIUM; S ADENOSYLMETHIONINE;

BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTALLOGRAPHY; GENE CONTROL; GENE EXPRESSION; PRIORITY JOURNAL; REVIEW; RIBOSWITCH; RNA BINDING; RNA STRUCTURE; BIOLOGICAL MODEL; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; PHYSIOLOGY; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE; LIGAND BINDING; PROTEIN FOLDING;

GENE EXPRESSION; GENE EXPRESSION REGULATION; MODELS, CHEMICAL; MODELS, GENETIC; MODELS, MOLECULAR; RNA; RNA-BINDING PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 48249104039     PISSN: 1936122X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.biophys.37.032807.130000     Document Type: Review

References (97)

1. Adams PL, Stahley MR, Kosek AB, Wang J, Strobel SA. 2004. Crystal structure of a self-splicing group I intron with both exons. Nature 430:45-50
2. Agalarov SC, Sridhar Prasad G, Funke PM, Stout CD, Williamson JR. 2000. Structure of the S15,S6,S18-rRNA complex: assembly of the 30S ribosome central domain. Science 288:107-13
3. Andreeva A, Howorth D, Brenner SE, Hubbard TJP, Chothia C, Murzin AG. 2004. SCOP database in 2004: Refinements integrate structure and sequence family data. Nucleic Acids Res. 32:D226-29
4. Batey RT, Gilbert SD, Montange RK. 2004. Structure of a natural guanine-responsive riboswitch complexed with the metabolite hypoxantbine. Nature 432:411-15
5. Berman HM, Westbrook J, Feng Z, Gililand G, Bhat TN, et al. 2007. The Protein Data Bank. http://www.pdb.org/pdb/home/home.do
6. Borovok I, Gorovitz B, Schreiber R, Aharonowitz Y, Cohen G. 2006. Coenzyme B12 controls transcription of the Streptomyces class Ia ribonucleotide reductase nrdABS operon via a riboswitch mechanism. J. Bacteriol. 188:2512-20
7. Canny MD, Jucker FM, Kellogg E, Khvorova A, Jayasena SD, Pardi A. 2004. Fast cleavage kinetics of a natural hammerhead ribozyme. J. Am. Chem. Soc. 126:10848-49
8. Cate JH, Hanna RL, Doudna JA. 1997. A magnesium ion core at the heart of a ribozyme domain. Nat. Struct. Biol. 4:553-58
9. Cheah MT, Wachter A, Sudarsan N, Breaker RR. 2007. Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 447:497-500
10. Cochrane JC, Lipchock SV, Strobel SA. 2007. Structural investigation of the GlmS ribozyme bound to its catalytic cofactor. Chem. Biol. 14:97-105
11. Corbino KA, Barrick JE, Lim J, Welz R, Tucker BJ, et al. 2005. Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria. Genome Biol. 6:R70
12. 2+. Cell 125:71-84
13. Dann CE 3rd, Wakeman CA, Sieling CL, Baker SC, Irnov I, Winkler WC. 2007. Structure and mechanism of a metal-sensing regulatory RNA. Cell 130:878-92
14. Dieckmann T, Suzuki E, Nakamura GK, Feigon J. 1996. Solution structure of an ATP-binding RNA aptamer reveals a novel fold. RNA 2:628-40
15. Edwards TE, Ferre-D'Amare AR. 2006. Crystal structures of the thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. Structure 14:1459-68
16. Edwards TE, Klein DJ, Ferré-D'Amaré AR. 2007. Riboswitches: small molecule recognition by gene regulatory RNAs. Curr. Opin. Struct. Biol. 17:273-79
17. Epshtein V, Mironov AS, Nudler E. 2003. The riboswitch-mediated control of sulfur metabolism in bacteria. Proc. Natl. Acad. Sci. USA 100:5052-56
18. Ferre-D'Amare AR, Zhou K, Doudna JA. 1998. Crystal structure of a hepatitis delta virus ribozyme. Nature 395:567-74
19. Fuchs RT, Grundy FJ, Henkin TM. 2006. The S(MK) box is a new SAM-binding RNA for translational regulation of SAM synthetase. Nat. Struct. Mol. Biol. 13:226-33
20. Gelfand MS, Mironov AA, Jomantas J, Kozlov YI, Perumov DA. 1999. A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. Trends Genet. 15:439-42
21. Gilbert SD, Batey RT. 2005. Riboswitches: natural SELEXion. Cell. Mol. Life Sci. 62:2401-4
22. Gilbert SD, Montange RK, Stoddard CD, Batey RT. 2006. Structural studies of the purine and SAM binding riboswitches. Cold Spring Horb. Symp. Quant. Biol. 71:259-68
23. Gilbert SD, Rambo RP, VanTyne D, Batey RT. 2008. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat. Struct. Mol. Biol. In press.
24. Gilbert SD, Stoddard CD, Wise SJ, Batey RT. 2006. Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain. J. Mol. Biol. 359:754-68
25. Golden BL, Gooding AR, Podell ER, Cech TR. 1998. A preorganized active site in the crystal structure of the Tetrabymena ribozyme. Science 282:259-64
26. Golden BL, Kim H, Chase E. 2005. Crystal structure of a phage Twort group I ribozyme-product complex. Nat. Struct. Mol. Biol. 12:82-89
27. Grundy FJ, Henkin TM. 2006. From ribosome to riboswitch: control of gene expression in bacteria by RNA structural rearrangements. Crit. Rev. Biochem. Mol. Biol. 41:329-38
28. Grundy FJ, Lehman SC, Henkin TM. 2003. The L box regulon: lysine sensing by leader RNAs of bacterial lysine biosynthesis genes. Proc. Natl. Acad. Sci. USA 100:12057-62
29. Hampel KJ, Tinsley MM. 2006. Evidence for preorganization of the glmS ribozyme ligand binding pocket. Biochemistry 45:7861-71
30. Hardin JW, Batey RT. 2006. The bipartite architecture of the sRNA in an archaeal box C/D complex is a primary determinant of specificity. Nucleic Acids Res. 34:5039-51
31. Houlberg U, Jensen KF. 1983. Role of hypoxanthine and guanine in regulation of Salmonella typhimurium pur gene expression. J. Bacteriol. 153:835-45
32. Jenison RD, Gill SC, Pardi A, Polisky B. 1994. High-resolution molecular discrimination by RNA. Science 263:1425-29
33. Jiang L, Patel DJ. 1998. Solution structure of the tobramycin-RNA aptamer complex. Nat. Struct. Biol. 5:769-74
34. Johansen LE, Nygaard P, Lassen C, Agerso Y, Saxild HH. 2003. Definition of a second Bacillus subtilis pur regulon comprising the pur and xpt-pbuX operons plus pbuG, nupG (yxjA), and pbuE (ydhL). J. Bacteriol. 185:5200-9
35. Khvorova A, Lescoute A, Westhof E, Jayasena SD. 2003. Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat. Struct. Biol. 10:708-12
36. Klein DJ, Ferré-D'Amaré AR. 2006. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313:1752-56
37. Kubodera T, Watanabe M, Yoshiuchi K, Yamashita N, Nishimura A, et al. 2003. Thiamine-regulated gene expression of Aspergillus oryzae thiA requires splicing of the intron containing a riboswitch-like domain in the 5′-UTR. FEBS Lett. 555:516-20
38. Lang K, Rieder R, Micura R. 2007. Ligand-induced folding of the thiM TPP riboswitch investigated by a structure-based fluorescence spectroscopic approach. Nucleic Acids Res. 35:5370-78
39. Lemay JF, Lafontaine DA. 2007. Core requirements of the adenine riboswitch aptamer for ligand binding. RNA 13:339-50
40. Lemay JF, Penedo JC, Tremblay R, Lilley DMJ, Lafontaine DA. 2006. Folding of the adenine riboswitch. Chem. Biol. 13:857-68
41. Leontis NB, Airman RB, Berman HM, Brenner SE, Brown JW, et al. 2006. The RNA Ontology Consortium: an open invitation to the RNA community. RNA 12:533-41
42. Lescoute A, Westhof E. 2005. Riboswitch structures: Purine ligands replace tertiary contacts. Chem. Biol. 12:10-13
43. Leulliot N, Varani G. 2001. Current topics in RNA-protein recognition: control of specificity and biological function through induced fit and conformational capture. Biochemistry 40:7947-56
44. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR. 2003. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113:577-86
45. Mandal M, Breaker RR. 2004. Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat. Struct. Mol. Biol. 11:29-35
46. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM, et al. 2004. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306:275-79
47. Martick M, Scott WG. 2006. Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126:309-20
48. McDaniel BA, Grundy FJ, Artsimovitch I, Henkin TM. 2003. Transcription termination control of the S box system: direct measurement of S-adenosylmethionine by the leader RNA. Proc. Natl. Acad. Sci. USA 100:3083-88
49. Merino EJ, Wilkinson KA, Coughlan JL, Weeks KM. 2005. RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). J. Am. Chem. Soc. 127:4223-31
50. Miranda-Ríos J. 2007. The THI-box riboswitch, or how RNA binds thiamin pyrophosphate. Structure 15:259-65
51. Mironov AS, Gusarov I, Rafikov R, Lopez LE, Shatalin K, et al. 2002. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111:747-56
52. Montange RK, Batey RT. 2006. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441:1172-75
53. Moore T, Zhang Y, Fenley MO, Li H. 2004. Molecular basis of box C/D RNA-protein interactions; cocrystal structure of archaeal L7Ae and a box C/D RNA. Structure 12:807-18
54. Nahvi A, Sudarsan N, Ebert MS, Zou X, Brown KL, Breaker RR. 2002. Genetic control by a metabolite binding mRNA. Chem. Biol. 9:1043
55. Noeske J, Buck J, Furtig B, Nasiri HR, Schwalbe H, Wohnert J. 2007. Interplay of 'induced fit' and preorganization in the ligand induced folding of the aptamer domain of the guanine binding riboswitch. Nucleic Acids Res. 35:572-83
56. Noeske J, Richter C, Stirnal E, Schwalbe H, Wöhnert J. 2006. Phosphate-group recognition by the aptamer domain of the thiamine pyrophosphate sensing riboswitch. Chembiochem 7:1451-56
57. Nudler E, Mironov AS. 2004. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 29:11-17
58. Rentmeister A, Mayer G, Kuhn N, Famulok M. 2007. Conformational changes in the expression domain of the Escherichia coli thiM riboswitch. Nucleic Acids Res. 35:3713-22
59. Rieder R, Lang K, Graber D, Micura R. 2007. Ligand-induced folding of the adenosine deaminase A-riboswitch and implications on riboswitch translational control. Chembiochem 8:896-902
60. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS. 2002. Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J. Biol. Chem. 277:48949-59
61. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS. 2003. Regulation of lysine biosynthesis and transport genes in bacteria: yet another RNA riboswitch? Nucleic Acids foi. 31:6748-57
62. Roth A, Winkler WC, Regulski EE, Lee BW, Lim J, et al. 2007. A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat. Struct. Mol. Biol. 14:308-17
63. Rueda D, Bokinsky G, Rhodes MM, Rust MJ, Zhuang X, Walter NG. 2004. Single-molecule enzymology of RNA: Essential functional groups impact catalysis from a distance. Proc. Natl. Acad. Sci. USA 101:10066-71
64. Rupert PB, Ferre-D'Amare AR. 2001. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410:780-86
65. Saint-Girons I, Belfaiza J, Guillou Y, Perrin D, Guiso N, et al. 1986. Interactions of the Escherichia coli methionine repressor with the metF operator and with its corepressor, S-adenosylmethionine. J. Biol. Chem. 261:10936-40
66. Salehi-Ashtiani K, Luptik A, Litovchick A, Szostak JW. 2006. A genomewide search for ribozymes reveals an HDV-like sequence in the human CPEB3 gene. Science 313:1788-92
67. Sashital DG, Butcher SE. 2006. Flipping off the riboswitch: RNA structures that control gene expression. ACS Cbem. Biol. 1:341-45
68. Sassanfar M, Szostak JW. 1993. An RNA motif that binds ATP. Nature 364:550-53
69. Schwalbe H, Buck J, Fürtig B, Noeske J, Wöhnert J. 2007. Structures of RNA switches: insight into molecular recognition and tertiary structure. Ang. Chem. Int. Ed. Eng. 46:1212-19
70. Seelig B, Jäschke A. 1999. A small catalytic RNA motif with Diels-Alderase activity. Chem. Biol. 6:167-76
71. Serganov A, Keiper S, Malinina L, Tereshko V, Skripkin E, et al. 2005. Structural basis for Diels-Alder ribozyme-catalyzed carbon-carbon bond formation. Nat. Struct. Mol. Biol. 12:218-24
72. Serganov A, Polonskaia A, Phan AT, Breaker RR, Patel DJ. 2006. Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 441:1167-71
73. Serganov A, Yuan YR, Pikovskaya O, Polonskaia A, Malinina L, et al. 2004. Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem. Biol. 11:1729-41
74. Stoddard CD, Batey RT. 2006. Mix-and-match riboswitches. ACS Chem. Biol. 1:751-54
75. Sudarsan N, Barrick JE, Breaker RR. 2003. Metabolite-binding RNA domains are present in the genes of eukaryotes. RNA 9:644-47
76. Sudarsan N, Cohen-Chalamish S, Nakamura S, Emilsson GM, Breaker RR. 2005. Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine. Chem. Biol. 12:1325-35
77. Sudarsan N, Wickiser JK, Nakamura S, Ebert MS, Breaker RR. 2003. An mRNA structure in bacteria that controls gene expression by binding lysine. Genes Dev. 17:2688-97
78. Szewczak AA, Cech TR. 1997. An RNA internal loop acts as a hinge to facilitate ribozyme folding and catalysis. RNA 3:838-49
79. Talkington MWT, Siuzdak G, Williamson JR. 2005. An assembly landscape for the 30S ribosomal subunit. Nature 438:628-32
80. Thore S, Leibundgut M, Ban N. 2006. Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 312:1208-11
81. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS. 2003. Regulation of the vitamin B12 metabolism and transport in bacteria by a conserved RNA structural element. RNA 9:1084-97
82. Wakeman CA, Winkler WC, Dann CE 3rd. 2007. Structural features of metabolite-sensing riboswitches. Trends Biochem. Sci. 32:415-24
83. Wang Y, Rando RR. 1995. Specific binding of aminoglycoside antibiotics to RNA. Chem. Biol. 2:281-90
84. Warner DF, Savvi S, Mizrahi V, Dawes SS. 2007. A riboswitch regulates expression of the coenzyme B12-independent methionine synthase in Mycobacterium tuberculosis: implications for differential methionine synthase function in strains H37Rv and CDC1551. J. Bacteriol. 189:3655-59
85. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, et al. 2007. Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res. 35:4809-19
86. Westhof E, Patel DJ. 1997. Nucleic acids. From self-assembly to induced-fit recognition. Curr. Opin. Struct. Biol. 7:305-9
87. Williamson JR. 2000. Induced fit in RNA-protein recognition. Nat. Struct. Biol. 7:834-37
88. Winkler W, Nahvi A, Breaker RR. 2002. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952-56
89. Winkler WC. 2005. Riboswitches and the role of noncoding RNAs in bacterial metabolic control. Curr. Opin. Chem. Biol. 9:594-602
90. Winkler WC, Breaker RR. 2003. Genetic control by metabolite-binding riboswitches. Chembiochem 4:1024-32
91. Winkler WC, Breaker RR. 2005. Regulation of bacterial gene expression by riboswitches. Annu. Rev. Microbiol. 59:487-517
92. Winkler WC, Cohen-Chalamish S, Breaker RR. 2002. An mRNA structure that controls gene expression by binding FMN. Proc. Natl. Acad. Sci. USA 99:15908-13
93. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. 2004. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281-86
94. Winkler WC, Nahvi A, Sudarsan N, Barrick JE, Breaker RR. 2003. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat. Struct. Biol. 10:701-7
95. 2+ on TPP-dependent riboswitch. FEBS Lett. 579:2583-88
96. Zimmermann GR, Jenison RD, Wick CL, Simorre JP, Pardi A. 1997. Interlocking structural motifs mediate molecular discrimination by a theophylline-binding RNA. Nat. Struct. Biol. 4:644-49
97. Stoddard CD, Gilbert SD, Batey RT. 2008. Ligand-dependent folding of the three-way junction in the purine riboswitch. RNA In press