Emerging applications of riboswitches – from antibacterial targets to molecular tools

Journal of Applied Genetics

Volumn 57, Issue 4, 2016, Pages 531-541

  Machtel, Piotr ^a   Bąkowska Żywicka, Kamilla ^a   Żywicki, Marek ^b  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Aptamer; Aptazyme; Biosensor; Gene expression regulation; Riboselector; Riboswitch

Indexed keywords

ANTIINFECTIVE AGENT; COCARBOXYLASE; CYCLIC GMP; FLAVINE MONONUCLEOTIDE; PYRITHIAMINE; THEOPHYLLINE; BIS(3',5')-CYCLIC DIGUANYLIC ACID; LYSINE; PURINE DERIVATIVE; RIBOSWITCH; RNA;

ANTIBACTERIAL ACTIVITY; BACTERIAL GENE; BIOENGINEERING; BIOSENSOR; CELL MOTILITY; CHEMOTAXIS; DRUG TARGETING; GENE EXPRESSION REGULATION; GLMS GENE; HUMAN; LYSINE RIBOSWITCH; MYCOBACTERIUM; NONHUMAN; PURINE RIBOSWITCH; REGULATORY MECHANISM; REVIEW; RIBOSELECTOR; RIBOSWITCH; SYSTEMATIC EVOLUTION OF LIGANDS BY EXPONENTIAL ENRICHMENT APTAMER TECHNIQUE; VIRUS GENE; ANALOGS AND DERIVATIVES; BACTERIUM; CHEMISTRY; GENETIC PROCEDURES; GENETIC TRANSCRIPTION; GENETICS; PROTEIN SYNTHESIS; RNA SPLICING; VIRUS;

BACTERIA; BIOSENSING TECHNIQUES; CYCLIC GMP; GENE EXPRESSION REGULATION; LYSINE; PROTEIN BIOSYNTHESIS; PURINES; RIBOSWITCH; RNA; RNA SPLICING; THIAMINE PYROPHOSPHATE; TRANSCRIPTION, GENETIC; VIRUSES;

EID: 84961653881     PISSN: 12341983     EISSN: None     Source Type: Journal    
DOI: 10.1007/s13353-016-0341-x     Document Type: Review

References (77)

1. Arora N (2013) Recent Advances in Biosensors Technology: a review. Octa J Biosci 1:147–150
2. Ataide SF, Wilson SN, Dang S, Rogers TE, Roy B, Banerjee R, Henkin TM, Ibba M (2007) Mechanisms of resistance to an amino acid antibiotic that targets translation. ACS Chem Biol 2:819–827
3. Baker MD, Wolanin PM, Stock JB (2006) Signal transduction in bacterial chemotaxis. Bioessays 28:9–22
4. Benner SA, Ellington AD, Tauer A (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci U S A 86:7054–7058
5. Bian J, Shen H, Tu Y, Yu A, Li C (2011) The riboswitch regulates a thiamine pyrophosphate ABC transporter of the oral spirochete Treponema denticola. J Bacteriol 193:3912–3922. doi:10.1128/JB.00386-11
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. Breaker RR (2012) Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4
8. Brown AC, Parish T (2006) Instability of the acetamide-inducible expression vector pJAM2 in Mycobacterium tuberculosis. Plasmid 55(1):81–86
9. Caron MP, Bastet L, Lussier A, Simoneau-Roy M, Masse E, Lafontaine DA (2012) Dual-acting riboswitch control of translation initiation and mRNA decay. Proc Natl Acad Sci U S A 109:E3444–E3453. doi:10.1073/pnas.1214024109
10. Cheah MT, Wachter A, Sudarsan N, Breaker RR (2007) Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 447:497–500
11. Chen ZH, Schaap P (2012) The prokaryote messenger c-di-GMP triggers stalk cell differentiation in Dictyostelium. Nature 488:680–683. doi:10.1038/nature11313
12. Chen AG, Sudarsan N, Breaker RR (2011) Mechanism for gene control by a natural allosteric group I ribozyme. RNA 17:1967–1972. doi:10.1261/rna.2757311
13. Cochrane JC, Lipchock SV, Strobel SA (2007) Structural investigation of the GlmS ribozyme bound to Its catalytic cofactor. Chem Biol 14:97–105
14. Collins JA, Irnov I, Baker S, Winkler WC (2007) Mechanism of mRNA destabilization by the glmS ribozyme. Genes Dev 21:3356–3368
15. Di Girolamo M, Di Girolamo A, Cini C, Coccia R, De Marco C (1986) Thialysine utilization for protein synthesis by CHO cells. Physiol Chem Phys Med NMR 18:159–164
16. Di Girolamo M, Busiello V, Coccia R, Foppoli C (1990) Aspartokinase III repression and lysine analogs utilization for protein synthesis. Physiol Chem Phys Med NMR 22:241–245
17. 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 14:1459–1468
18. Ehrt S, Guo XV, Hickey CM, Ryou M, Monteleone M, Riley LW, Schnappinger D (2005) Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res 33:e21
19. Furukawa K, Gu H, Sudarsan N, Hayakawa Y, Hyodo M, Breaker RR (2012) Identification of ligand analogues that control c-di-GMP riboswitches. ACS Chem Biol 7:1436–1443. doi:10.1021/cb300138n
20. Furukawa K, Ramesh A, Zhou Z, Weinberg Z, Vallery T, Winkler WC, Breaker RR (2015) Bacterial riboswitches cooperatively bind Ni(2+) or Co(2+) ions and control expression of heavy metal transporters. Mol Cell 57:1088–1098. doi:10.1016/j.molcel.2015.02.009
21. Gilbert SD, Montange RK, Stoddard CD, Batey RT (2006) Structural studies of the purine and SAM binding riboswitches. Cold Spring Harb Symp Quant Biol 71:259–268
22. Gilbert SD, Rambo RP, Van Tyne D, Batey RT (2008) Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat Struct Mol Biol 15:177–182. doi:10.1038/nsmb.1371
23. Gilbert SD, Reyes FE, Edwards AL, Batey RT (2009) Adaptive ligand binding by the purine riboswitch in the recognition of guanine and adenine analogs. Structure 17:857–868. doi:10.1016/j.str.2009.04.009
24. Haller A, Rieder U, Aigner M, Blanchard SC, Micura R (2011) Conformational capture of the SAM-II riboswitch. Nat Chem Biol 7:393–400. doi:10.1038/nchembio.562
25. Han K, Liang Z, Zhou N (2010) Design strategies for aptamer-based biosensors. Sensors (Basel) 10:4541–4557. doi:10.3390/s100504541
26. Hollands K, Proshkin S, Sklyarova S, Epshtein V, Mironov A, Nudler E, Groisman EA (2012) Riboswitch control of Rho-dependent transcription termination. Proc Natl Acad Sci U S A 109:5376–5381. doi:10.1073/pnas.1112211109
27. Jang S, Yang J, Seo SW, Jung GY (2015) Riboselector: riboswitch-based synthetic selection device to expedite evolution of metabolite-producing microorganisms. Methods Enzymol 550:341–362. doi:10.1016/bs.mie.2014.10.039
28. Jo JJ, Shin JS (2009) Construction of intragenic synthetic riboswitches for detection of a small molecule. Biotechnol Lett 31:1577–1581. doi:10.1007/s10529-009-0058-6
29. Judson N, Mekalanos JJ (2000) Transposon-based approaches to identify essential bacterial genes. Trends Microbiol. 8:521-526. doi::10.1016/S0966-842X(00)01865-5
30. Kelly E, Russell SJ (2007) History of oncolytic viruses: genesis to genetic engineering. Mol Ther 15:651–659
31. Ketzer P, Kaufmann JK, Engelhardt S, Bossow S, von Kalle C, Hartig JS, Ungerechts G, Nettelbeck DM (2014) Artificial riboswitches for gene expression and replication control of DNA and RNA viruses. Proc Natl Acad Sci U S A 111:E554–E562. doi:10.1073/pnas.1318563111
32. 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. doi:10.1021/cb900146k
33. Klein DJ, Edwards TE, Ferre-D'Amare AR (2009) Cocrystal structure of a class I preQ1 riboswitch reveals a pseudoknot recognizing an essential hypermodified nucleobase. Nat Struct Mol Biol 16:343–344. doi:10.1038/nsmb.1563
34. Lee ER, Blount KF, Breaker RR (2009) Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression. RNA Biol 6:187–194
35. 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. doi:10.1126/science.1190713
36. Li S, Breaker RR (2012) Fluoride enhances the activity of fungicides that destabilize cell membranes. Bioorg Med Chem Lett 22:3317–3322. doi:10.1016/j.bmcl.2012.03.006
37. Liberman JA, Salim M, Krucinska J, Wedekind JE (2013) Structure of a class II preQ1 riboswitch reveals ligand recognition by a new fold. Nat Chem Biol 9:353–355. doi:10.1038/nchembio
38. Lünse CE, Schmidt MS, Wittmann V, Mayer G (2011) Carba-sugars activate the glmS-riboswitch of Staphylococcus aureus. ACS Chem Biol 6:675–678. doi:10.1021/cb200016d
39. Lünse CE, Schuller A, Mayer G (2014) The promise of riboswitches as potential antibacterial drug targets. Int J Med Microbiol 304:79–92. doi:10.1016/j.ijmm.2013.09.002
40. Mandal M, Breaker RR (2004) Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat Struct Mol Biol 11:29–35
41. Martini L, Mansy SS (2011) Cell-like systems with riboswitch controlled gene expression. Chem Commun (Camb) 47:10734–10736. doi:10.1039/c1cc13930d
42. McCown PJ, Roth A, Breaker RR (2011) An expanded collection and refined consensus model of glmS ribozymes. RNA 17:728–736. doi:10.1261/rna.2590811
43. 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
44. Miesel L, Greene J, Black TA (2003) Genetic strategies for antibacterial drug discovery. Nat Rev Genet 4:442–456
45. 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. doi:10.1371/journal.ppat.1000865
46. Ontiveros-Palacios N, Smith AM, Grundy FJ, Soberon M, Henkin TM, Miranda-Rios J (2008) Molecular basis of gene regulation by the THI-box riboswitch. Mol Microbiol 67:793–803. doi:10.1111/j.1365-2958.2007.06088.x
47. Ott E, Stolz J, Lehmann M, Mack M (2009) The RFN riboswitch of Bacillus subtilis is a target for the antibiotic roseoflavin produced by Streptomyces davawensis. RNA Biol 6:276–280
48. Park M, Tsai SL, Chen W (2013) Microbial biosensors: engineered microorganisms as the sensing machinery. Sensors Basel 13:5777–5795. doi:10.3390/s130505777
49. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL (2007) Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat Rev Drug Discov 6:29–40
50. Pedrolli DB, Matern A, Wang J, Ester M, Siedler K, Breaker R, Mack M (2012) A highly specialized flavin mononucleotide riboswitch responds differently to similar ligands and confers roseoflavin resistance to Streptomyces davawensis. Nucleic Acids Res 40:8662–8673
51. Pernites R, Ponnapati R, Felipe MJ, Advincula R (2011) Electropolymerization molecularly imprinted polymer (E-MIP) SPR sensing of drug molecules: pre-polymerization complexed terthiophene and carbazole electroactive monomers. Biosens Bioelectron 26(5):2766–2771. doi:10.1016/j.bios.2010.10.027
52. Peselis A, Serganov A (2014) Themes and variations in riboswitch structure and function. Biochim Biophys Acta 1839:908–918. doi:10.1016/j.bbagrm.2014.02.012
53. Price IR, Gaballa A, Ding F, Helmann JD, Ke A (2015) Mn(2+)-Sensing Mechanisms of yybP-ykoY Orphan Riboswitches. Mol Cell 57:1110–1123. doi:10.1016/j.molcel.2015.02.016
54. Reining A, Nozinovic S, Schlepckow K, Buhr F, Furtig B, Schwalbe H (2013) Three-state mechanism couples ligand and temperature sensing in riboswitches. Nature 499:355–359. doi:10.1038/nature12378
55. Seeliger JC, Topp S, Sogi KM, Previti ML, Gallivan JP, Bertozzi CR (2012) A riboswitch-based inducible gene expression system for mycobacteria. PLoS One 7:e29266. doi:10.1371/journal.pone.0029266
56. Serganov A, Nudler E (2013) A decade of riboswitches. Cell 152(1-2):17–24. doi:10.1016/j.cell.2012.12.024
57. Serganov A, Patel DJ (2009) Amino acid recognition and gene regulation by riboswitches. Biochim Biophys Acta 1789:592–611. doi:10.1016/j.bbagrm.2009.07.002
58. Serganov A, Yuan YR, Pikovskaya O, Polonskaia A, Malinina L, Phan AT, Hobartner C, Micura R, Breaker RR, Patel DJ (2004) Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem Biol 11:1729–1741
59. Serganov A, Polonskaia A, Phan AT, Breaker RR, Patel DJ (2006) Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 441:1167–1171
60. Shanahan CA, Gaffney BL, Jones RA, Strobel SA (2011) Differential analogue binding by two classes of c-di-GMP riboswitches. J Am Chem Soc 133:15578–15592. doi:10.1021/ja204650q
61. Ster C, Allard M, Boulanger S, Lamontagne Boulet M, Mulhbacher J, Lafontaine DA, Marsault E, Lacasse P, Malouin F (2013) Experimental treatment of Staphylococcus aureus bovine intramammary infection using a guanine riboswitch ligand analog. J Dairy Sci 96:1000–1008. doi:10.3168/jds.2012-5890
62. Su L, Jia W, Hou C, Lei Y (2011) Microbial biosensors: a review. Biosens Bioelectron 26:1788–1799. doi:10.1016/j.bios.2010.09.005
63. 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
64. Sudarsan N, Cohen-Chalamish S, Nakamura S, Emilsson GM, Breaker RR (2005) Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine. Chem Biol 12:1325–1335
65. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411–413. doi:10.1126/science.1159519
66. Thore S, Leibundgut M, Ban N (2006) Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 312:1208–1211
67. Thore S, Frick C, Ban N (2008) Structural basis of thiamine pyrophosphate analogues binding to the eukaryotic riboswitch. J Am Chem Soc 130:8116–8117. doi:10.1021/ja801708e
68. Topp S, Gallivan JP (2007) Guiding bacteria with small molecules and RNA. J Am Chem Soc 129(21):6807–6811
69. van Kessel JC, Marinelli LJ, Hatfull GF (2008) Recombineering mycobacteria and their phages. Nat Rev Microbiol 6:851–857. doi:10.1038/nrmicro2014
70. 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
71. 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. doi:10.1186/gb-2010-11-3-r31
72. Winkler W, Nahvi A, Breaker RR (2002a) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419:952–956
73. Winkler WC, Cohen-Chalamish S, Breaker RR (2002b) An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci U S A 99:15908–15913
74. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR (2004) Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281–286
75. Wong HH, Lemoine NR, Wang Y (2010) Oncolytic viruses for cancer therapy. Overcoming the obstacles. Viruses 2:78–106
76. Yang J, Seo SW, Jang S, Shin SI, Lim CH, Roh TY, Jung GY (2013) Synthetic RNA devices to expedite the evolution of metabolite-producing microbes. Nat Commun 4:1413. doi:10.1038/ncomms2404
77. Zhou J, Sayre DA, Wang J, Pahadi N, Sintim HO (2012) Endo-S-c-di-GMP analogues-polymorphism and binding studies with class I riboswitch. Molecules 17:13376–13389. doi:10.3390/molecules171113376