The yjdF riboswitch candidate regulates gene expression by binding diverse azaaromatic compounds

RNA

Volumn 22, Issue 4, 2016, Pages 530-541

  Li, Sanshu ^a   Hwang, Xue Ying ^a   Stav, Shira ^a   Breaker, Ronald R ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Alkaloid; Chelerythrine; DUF2992; Noncoding RNA; Orphan riboswitch

Indexed keywords

APTAMER; AROMATIC COMPOUND; HETEROCYCLIC COMPOUND; NITROGEN DERIVATIVE; PHENOL DERIVATIVE; POLYCYCLIC HYDROCARBON; BACTERIAL RNA; RIBOSWITCH;

ARTICLE; CHEMICAL BINDING; DISSOCIATION CONSTANT; GENE; GENE AMPLIFICATION; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; LIGAND BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RIBOSWITCH; YJDF GENE; BACILLUS SUBTILIS; CONSENSUS SEQUENCE; DRUG EFFECTS; GENETICS; MOLECULAR GENETICS;

AZA COMPOUNDS; BACILLUS SUBTILIS; BASE SEQUENCE; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; RIBOSWITCH; RNA, BACTERIAL;

EID: 84962599121     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.054890.115     Document Type: Article

References (65)

1. Alekshun MN, Levy SB, Mealy TR, Seaton BA, Head JF. 2001. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 A resolution. Nat Struct Biol 8: 710-714.
2. Baker JL, Sudarsan N, Weinberg Z, Roth A, Stockbridge RB, Breaker RR. 2012. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335: 233-235.
3. 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.
4. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. 2008. GenBank. Nucleic Acids Res 36: D25-D30.
5. Block KF, Hammond MC, Breaker RR. 2010. Evidence for widespread gene control function by the ydaO riboswitch candidate. J Bacteriol 192: 3983-3989.
6. Blount KF, Wang JX, Lim J, Sudarsan N, Breaker RR. 2007. Antibacterial lysine analogs that target lysine riboswitches. Nat Chem Biol 3: 44-49.
7. Blount KF, Megyola C, Plummer M, Osterman D, O'Connell T, Aristoff P, Quinn C, Chrusciel RA, Poel TJ, Schostarez HJ, et al. 2015. Novel riboswitch-binding flavin analog that protects mice against Clostridium difficile infection without inhibiting cecal flora. Antimicrob Agents Chemother 59: 5736-5746.
8. Breaker RR. 2011. Prospects for riboswitch discovery and analysis. Mol Cell 43: 867-879.
9. Breaker RR. 2012. Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4: a003566.
10. Dambach M, Sandoval M, Updegrove TB, Anantharaman V, Aravind L, Waters LS, Storz G. 2015. The ubiquitous yybP-ykoY riboswitch is a manganese-responsive regulatory element. Mol Cell 57: 1099-1109.
11. De Silva RS, Kovacikova G, Lin W, Taylor RK, Skorupski K, Kull FJ. 2005. Crystal structure of the virulence gene activator AphA from Vibrio cholerae reveals it is a novel member of the winged helix transcription factor superfamily. J Biol Chem 280: 13779-13783.
12. Dong X, Dong M, Lu Y, Turley A, Jin T, Wu C. 2011. Antimicrobial and antioxidant activities of lignin from residue of corn stover to ethanol production. Ind Crops Prod 34: 1629-1634.
13. Finkelstein T, Weinstein IB. 1967. Proflavine binding to transfer ribonucleic acid, synthetic ribonucleic acids, and deoxyribonucleic acid. J Biol Chem 242: 3763-3768.
14. Furukawa K, Ramesh A, Zhou Z, Weinberg Z, Vallery T, Winkler WC, Breaker RR. 2015. Bacterial riboswitches cooperatively bind Ni2+ or Co2+ ions and control expression of heavy metal transporters. Mol Cell 57: 1088-1098.
15. Garst AD, Edwards AL, Batey RT. 2011. Riboswitches: structures and mechanisms. Cold Spring Harb Perspect Biol 3: a003533.
16. Guérout-Fleury AM, Frandsen N, Stragier P. 1996. Plasmids for ectopic integration in Bacillus subtilis. Gene 180: 57-61.
17. Gury J, Barthelmebs L, Tran NP, Diviès C, Cavin JF. 2004. Cloning, deletion, and characterization of PadR, the transcriptional repressor of the phenolic acid decarboxylase-encoding padA gene of Lactobacillus plantarum. Appl Environ Microbiol 70: 2146-2153.
18. Heravi KM, Lange J, Watzlawick H, Kalinowski J, Altenbuchner J. 2015. Transcriptional regulation of the vanillate utilization genes (vanABK operon) of Corynebacterium glutamicum by VanR, a PadR-like repressor. J Bacteriol 197: 959-972.
19. Howe JA, Wang H, Fischmann TO, Balibar CJ, Xiao L, Galgoci AM, Malinverni JC, Mayhood T, Villafania A, Nahvi A, et al. 2015. Selective small-molecule inhibition of an RNA structural element. Nature 526: 672-677.
20. Huillet E, Velge P, Vallaeys T, Pardon P. 2006. LadR, a new PadR-related transcriptional regulator from Listeria monocytogenes, negatively regulates the expression of the multidrug efflux pump MdrL. FEMS Microbiol Lett 254: 87-94.
21. Human Microbiome Project Consortium. 2012. A framework for human microbiome research. Nature 486: 215-221.
22. Keefer LK, Johnson DE. 1970. Magnesium hydroxide as a thin-layer chromatographic adsorbent. II. A unique system for separating polynuclear azaaromatic compounds. J Chromatogr 47: 20-26.
23. Kellenberger CA, Wilson SC, Hickey SF, Gonzalez TL, Su Y, Hallberg ZF, Brewer TF, Iavarone AT, Carlson HK, Hsieh YF, et al. 2015. GEMM-I riboswitches from Geobacter sense the bacterial second messenger cyclic AMP-GMP. Proc Natl Acad Sci 112: 5383-5388.
24. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10: 845-858.
25. Kim JN, Blount KF, Puskarz I, Lim J, Link KH, Breaker RR. 2009. Design and antimicrobial action of purine analogues that bind guanine riboswitches. ACS Chem Biol 4: 915-927.
26. Kim PB, Nelson JW, Breaker RR. 2015. An ancient riboswitch class in bacteria regulates purine biosynthesis and one-carbon metabolism. Mol Cell 57: 317-328.
27. Li S, Breaker RR. 2013. Eukaryotic TPP riboswitch regulation of alternative splicing involving long-distance base pairing. Nucleic Acids Res 41: 3022-3031.
28. Li S, Smith KD, Davis JH, Gordon PB, Breaker RR, Strobel SA. 2013. Eukaryotic resistance to fluoride toxicity mediated by a widespread family of fluoride export proteins. Proc Natl Acad Sci 110: 19018-19023.
29. Lubelski J, De Jong A, van Merkerk R, Agustiandari H, Kuipers OP, Kok J, Driessen AJ. 2006. LmrCD is a major multidrug resistance transporter in Lactococcus lactis. Mol Microbiol 61: 771-781.
30. Lünse CE, Schmidt MS, Wittmann V, Mayer G. 2011. Carba-sugars activate the glmS-riboswitch of Staphylococcus aureus. ACS Chem Biol 6: 675-678.
31. Madoori PK, Aqustiandari H, Driessen AJ, Thunnissen AM. 2009. Structure of the transcriptional regulator LmrR and its mechanism of multidrug recognition. EMBO J 28: 156-166.
32. Markowitz VM, Chen IM, Chu K, Szeto E, Palaniappan K, Grechkin Y, Ratner A, Jacob B, Pati A, Huntemann M, et al. 2012. IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Res 40: D123-D129.
33. McCown PJ, Liang JJ, Weinberg Z, Breaker RR. 2014. Structural, functional, and taxonomic diversity of three preQ1 riboswitch classes. Chem Biol 21: 880-889.
34. Merritt ME, Donaldson JR. 2009. Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol 58: 1533-1541.
35. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, et al. 2008. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386.
36. Meyer MM, Hammond MC, Salinas Y, Roth A, Sudarsan N, Breaker RR. 2011. Challenges of ligand identification for riboswitch candidates. RNA Biol 8: 5-10.
37. Mironov AS, Gusarov I, Rafikov R, Lopez LE, Shatalin K, Kreneva RA, Perumov DA, Nudler E. 2002. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111: 747-756.
38. Mulhbacher J, Brouillette E, Allard M, Fortier LC, Malouin F, Lafontaine DA. 2010. Novel riboswitch ligand analogs as selective inhibitors of guanine-related metabolic pathways. PLoS Pathog 6: e1000865.
39. Nawrocki EP, Eddy SR. 2013. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29: 2933-2935.
40. Nelson JW, Sudarsan N, Furukawa K, Weinberg Z, Wang JX, Breaker RR. 2013. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat Chem Biol 9: 834-839.
41. Nelson JW, Sudarsan N, Phillips GE, Stav S, Lünse CE, McCown PJ, Breaker RR. 2015. Control of bacterial exoelectrogenesis by c- AMP-GMP. Proc Natl Acad Sci 112: 5389-5394.
42. Nguyen TK, Tran NP, Cavin JF. 2011. Genetic and biochemical analysis of PadR-padC promoter interactions during the phenolic acid stress response in Bacillus subtilis 168. J Bacteriol 193: 4180-4191.
43. Östman CE, Colmsjö AL. 1987. Backflush HPLCfor the isolation of polycyclic aromatic compounds - a comparative study. Chromatographia 23: 903-908.
44. Price IR, Gaballa A, Ding F, Helmann JD, Ke A. 2015. Mn2+-sensing mechanisms of yybP-ykoY orphan riboswitches. Mol Cell 57: 1110-1123.
45. Pruitt KD, Tatusova T, Maglott DR. 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35: D61-D65.
46. Regulski EE, Breaker RR. 2008. In-line probing analysis of riboswitches. Methods Mol Biol 419: 53-67.
47. Ren A, Wang XC, Kellenberger CA, Rajashankar KR, Jones RA, Hammond MC, Patel D. 2015. Structural basis for molecular discrimination by a 3′,3′-cGAMP sensing riboswitch. Cell Rep 11: 1-12.
48. Serganov A, Nudler E. 2013. A decade of riboswitches. Cell 152: 17-24.
49. Serganov A, Patel DJ. 2012. Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys 41: 343-370.
50. Serganov A, Huang L, Patel DJ. 2009. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 458: 233-237.
51. Soukup GA, Breaker RR. 1999. Relationship between internucleotide linkage geometry and the stability of RNA. RNA 5: 1308-1325.
52. 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: 2688-2697.
53. Sulavik MC, Gambino LF, Miller PF. 1995. The MarR repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli: prototypic member of a family of bacterial regulatory proteins involved in sensing phenolic compounds. Mol Med 1: 436-446.
54. Sun S, Chen J, Li W, Altintas I, Lin A, Peltier S, Stocks K, Allen EE, Ellisman M, Grethe J, et al. 2011. Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucleic Acids Res 39: D546-D551.
55. Sung JY, Shaffer EA, Costerton JW. 1993. Antibacterial activity of bile salts against common biliary pathogens. Effects of hydrophobicity of the molecule and in the presence of phospholipids. Dig Dis Sci 38: 2104-2112.
56. Vidal-Aroca F, Giannattasio M, Brunelli E, Vezzoli A, Plevani P, Muzi- Falconi M, Bertoni G. 2006. One-step high-throughput assay for quantitative detection of β-galactosidase activity in intact Gram-negative bacteria, yeast, and mammalian cells. Biotechniques 40: 433-440.
57. Wang JX, Lee ER, Morales DR, Lim J, Breaker RR. 2008. Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol Cell 29: 691-702.
58. Weinberg Z, Breaker RR. 2011. R2R-software to speed the depiction of aesthetic consensus RNA secondary structures. BMC Bioinformatics 12: 3.
59. Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K, Moy RH, Breaker RR. 2010. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11: R31.
60. Weinberg Z, Kim PB, Chen TH, Li S, Harris KA, Lunse CE, Breaker RR. 2015. New classes of self-cleaving ribozymes revealed by comparative genomics analysis. Nat Chem Biol 11: 606-610.
61. Winkler WC, Cohen-Chalamish S, Breaker RR. 2002. An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci 99: 15908-15913.
62. Zeigler DR, Prágai Z, Rodriguez S, Chevreux B, Muffler A, Albert T, Bai R, Wyss M, Perkins JB. 2008. The origins of 168, W23, and other Bacillus subtilis legacy strains. J Bacteriol 190: 6983-6995.
63. Zemek J, Košíková B, Augustín J, Joniak D. 1979. Antibiotic properties of lignin components. Folia Microbiol (Praha) 24: 483-486.
64. Zhang J, Lau MW, Ferré-D'Amaré AR. 2010. Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 49: 9123-9131.
65. Zheng G, Zhang Z, Lockman PR, Geldenhuys WJ, Allen DD, Dwoskin LP, Crooks PA. 2010. Bis-azaaromatic quaternary ammonium salts as ligands for the blood-brain barrier choline transporter. Bioorg Med Chem Lett 20: 3208-3210.