Transcriptional pausing at the translation start site operates as a critical checkpoint for riboswitch regulation

Nature Communications

Volumn 8, Issue , 2017, Pages

  Chauvier, Adrien ^a   Picard Jean, Frederic ^a   Berger Dancause, Jean Christophe ^a   Bastet, Laurene ^a   Naghdi, Mohammad Reza ^b   Dubé, Audrey ^a   Turcotte, Pierre ^a   Perreault, Jonathan ^b   Lafontaine, Daniel A ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; MESSENGER RNA; NUCLEASE S1; PYROPHOSPHATE; RNA POLYMERASE; THIAMINE DERIVATIVE; BACTERIAL PROTEIN; COCARBOXYLASE; ESCHERICHIA COLI PROTEIN; RHO PROTEIN, E COLI; RIBONUCLEASE H; THIC PROTEIN, BACTERIA;

BIOCHEMISTRY; COLIFORM BACTERIUM; GENE EXPRESSION; GENETIC ANALYSIS; METABOLITE; RNA;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENE REPRESSION; IN VITRO STUDY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE BINDING SITE; PROTEIN SECONDARY STRUCTURE; RIBOSWITCH; RNA CONFORMATION; RNA PROCESSING; RNA TRANSLATION; START CODON; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; TRANSLATION INITIATION; CHEMISTRY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; PROTEIN CONFORMATION; PROTEIN SYNTHESIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL PROTEINS; CODON, INITIATOR; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; RIBONUCLEASE H; RIBOSWITCH; THIAMINE PYROPHOSPHATE; TRANSCRIPTION, GENETIC;

EID: 85009274805     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13892     Document Type: Article

References (62)

1. Waters, L. S., & Storz, G. Regulatory RNAs in bacteria. Cell 136, 615-628 (2009).
2. Serganov, A., & Nudler, E. A decade of riboswitches. Cell 152, 17-24 (2013).
3. Irnov, I., Sharma, C. M., Vogel, J., & Winkler, W. C. Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res. 38, 6637-6651 (2010).
4. Weinberg, Z., et al. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol. 11, R31 (2010).
5. Caron, M. P., et al. Dual-Acting riboswitch control of translation initiation and mRNA decay. Proc. Natl Acad. Sci. USA 109, E3444-E3453 (2012).
6. Hollands, K., et al. Riboswitch control of Rho-dependent transcription termination. Proc. Natl Acad. Sci. USA 109, 5376-5381 (2012).
7. Hollands, K., Sevostiyanova, A., & Groisman, E. A. Unusually long-lived pause required for regulation of a Rho-dependent transcription terminator. Proc. Natl Acad. Sci. USA 111, E1999-E2007 (2014).
8. Bernstein, J. A., Lin, P. H., Cohen, S. N., & Lin-Chao, S. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl Acad. Sci. USA 101, 2758-2763 (2004).
9. Peters, J. M., et al. Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev. 26, 2621-2633 (2012).
10. Larson, M. H., et al. A pause sequence enriched at translation start sites drives transcription dynamics in vivo. Science 344, 1042-1047 (2014).
11. Begley, T. P., et al. Thiamin biosynthesis in prokaryotes. Arch. Microbiol. 171, 293-300 (1999).
12. Winkler, W., Nahvi, A., & Breaker, R. R. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419, 952-956 (2002).
13. Rodionov, D. A., Vitreschak, A. G., Mironov, A. A., & Gelfand, M. S. Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J. Biol. Chem. 277, 48949-48959 (2002).
14. Ontiveros-Palacios, N., et al. Molecular basis of gene regulation by the THI-box riboswitch. Mol. Microbiol. 67, 793-803 (2008).
15. Kido, M., et al. RNase E polypeptides lacking a carboxyl-Terminal half suppress a mukB mutation in Escherichia coli. J. Bacteriol. 178, 3917-3925 (1996).
16. Kohn, H., & Widger, W. The molecular basis for the mode of action of bicyclomycin. Curr. Drug Targets Infect. Disord. 5, 273-295 (2005).
17. Shashni, R., Qayyum, M. Z., Vishalini, V., Dey, D., & Sen, R. Redundancy of primary RNA-binding functions of the bacterial transcription terminator Rho. Nucleic Acids Res. 42, 9677-9690 (2014).
18. Li, J., Mason, S. W., & Greenblatt, J. Elongation factor NusG interacts with termination factor rho to regulate termination and antitermination of transcription. Genes Dev. 7, 161-172 (1993).
19. Alifano, P., Rivellini, F., Limauro, D., Bruni, C. B., & Carlomagno, M. S. A consensus motif common to all Rho-dependent prokaryotic transcription terminators. Cell 64, 553-563 (1991).
20. Allison, T. J., et al. Crystal structure of the RNA-binding domain from transcription termination factor rho. Nat. Struct. Biol. 5, 352-356 (1998).
21. Bogden, C. E., Fass, D., Bergman, N., Nichols, M. D., & Berger, J. M. The structural basis for terminator recognition by the Rho transcription termination factor. Mol. Cell 3, 487-493 (1999).
22. Sevostyanova, A., & Groisman, E. A. An RNA motif advances transcription by preventing Rho-dependent termination. Proc. Natl Acad. Sci. USA 112, E6835-E6843 (2015).
23. Shimizu, Y., Kanamori, T., & Ueda, T. Protein synthesis by pure translation systems. Methods 36, 299-304 (2005).
24. Schyns, G., et al. Isolation and characterization of new thiamine-deregulated mutants of Bacillus subtilis. J. Bacteriol. 187, 8127-8136 (2005).
25. Perdrizet, 2nd G. A., Artsimovitch, I., Furman, R., Sosnick, T. R., & Pan, T. Transcriptional pausing coordinates folding of the aptamer domain and the expression platform of a riboswitch. Proc. Natl Acad. Sci. USA 109, 3323-3328 (2012).
26. Lussier, A., Bastet, L., Chauvier, A., & Lafontaine, D. A. A kissing loop is important for btub riboswitch ligand sensing and regulatory control. J. Biol. Chem. 290, 26739-26751 (2015).
27. Wickiser, J. K., Winkler, W. C., Breaker, R. R., & Crothers, D. M. The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol. Cell 18, 49-60 (2005).
28. Lemay, J. F., et al. Comparative study between transcriptionally-and translationally-Acting adenine riboswitches reveals key differences in riboswitch regulatory mechanisms. PLoS Genet. 7, e1001278 (2011).
29. Wong, T. N., Sosnick, T. R., & Pan, T. Folding of noncoding RNAs during transcription facilitated by pausing-induced nonnative structures. Proc. Natl Acad. Sci. USA 104, 17995-18000 (2007).
30. Morgan, W. D., Bear, D. G., & von Hippel, P. H. Rho-dependent termination of transcription. II. Kinetics of mRNA elongation during transcription from the bacteriophage lambda PR promoter. J. Biol. Chem. 258, 9565-9574 (1983).
31. Frieda, K. L., & Block, S. M. Direct observation of cotranscriptional folding in an adenine riboswitch. Science 338, 397-400 (2012).
32. Komissarova, N., & Kashlev, M. Functional topography of nascent RNA in elongation intermediates of RNA polymerase. Proc. Natl Acad. Sci. USA 95, 14699-14704 (1998).
33. Merino, E. J., Wilkinson, K. A., Coughlan, J. L., & Weeks, K. M. RNA structure analysis at single nucleotide resolution by selective 20-hydroxyl acylation and primer extension (SHAPE). J. Am. Chem. Soc. 127, 4223-4231 (2005).
34. Blouin, S., Chinnappan, R., & Lafontaine, D. A. Folding of the lysine riboswitch: importance of peripheral elements for transcriptional regulation. Nucleic Acids Res. 39, 3373-3387 (2010).
35. Heppell, B., et al. Molecular insights into the ligand-controlled organization of the SAM-I riboswitch. Nat. Chem. Biol. 7, 384-392 (2011).
36. Stoddard, C. D., Gilbert, S. D., & Batey, R. T. Ligand-dependent folding of the three-way junction in the purine riboswitch. RNA 14, 675-684 (2008).
37. Soulière, M. F., et al. Tuning a riboswitch response through structural extension of a pseudoknot. Proc. Natl Acad. Sci. USA 110, E3256-E3264 (2013).
38. Johnson, Jr J. E., Reyes, F. E., Polaski, J. T., & Batey, R. T. B12 cofactors directly stabilize an mRNA regulatory switch. Nature 492, 133-137 (2012).
39. Steen, K.-A., Siegfried, N. A., & Weeks, K. M. Selective 20-hydroxyl acylation analyzed by protection from exoribonuclease (RNase-detected SHAPE) for direct analysis of covalent adducts and of nucleotide flexibility in RNA. Nat. Protoc. 6, 1683-1694 (2011).
40. Vicens, Q., Mondragón, E., & Batey, R. T. Molecular sensing by the aptamer domain of the FMN riboswitch: a general model for ligand binding by conformational selection. Nucleic Acids Res. 39, 8586-8598 (2011).
41. Steen, K. A., Malhotra, A., & Weeks, K. M. Selective 20-hydroxyl acylation analyzed by protection from exoribonuclease. J. Am. Chem. Soc. 132, 9940-9943 (2010).
42. Li, G. W., Burkhardt, D., Gross, C., & Weissman, J. S. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157, 624-635 (2014).
43. Blount, K. F., & Breaker, R. R. Riboswitches as antibacterial drug targets. Nat. Biotechnol. 24, 1558-1564 (2006).
44. Howe, J. A., et al. Selective small-molecule inhibition of an RNA structural element. Nature 526, 672-677 (2015).
45. Belogurov, G. A., & Artsimovitch, I. Regulation of transcript elongation. Annu. Rev. Microbiol. 69, 49-69 (2015).
46. Donahue, J. P., & Turnbough, C. L. Nucleotide-specific transcriptional pausing in the pyrBI leader region of Escherichia coli K-12. J. Biol. Chem. 269, 18185-18191 (1994).
47. Guedich, S., et al. Quantitative and predictive model of kinetic regulation by E. coli TPP riboswitches. RNA Biol. 13, 373-390 (2016).
48. Peters, J. M., Vangeloff, A. D., & Landick, R. Bacterial transcription terminators: The RNA 30-end chronicles. J. Mol. Biol. 412, 793-813 (2011).
49. de Crombrugghe, B., Adhya, S., Gottesman, M., & Pastan, I. Effect of Rho on transcription of bacterial operons. Nat. New Biol. 241, 260-264 (1973).
50. Burmann, B. M., et al. A NusE:NusG complex links transcription and translation. Science 328, 501-504 (2010).
51. Rabhi, M., et al. The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators. EMBO J. 30, 2805-2816 (2011).
52. Yu, D., et al. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl Acad. Sci. USA 97, 5978-5983 (2000).
53. Prevost, K., et al. The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol. Microbiol. 64, 1260-1273 (2007).
54. Lemay, J. F., Penedo, J. C., Tremblay, R., Lilley, D. M., & Lafontaine, D. A. Folding of the adenine riboswitch. Chem. Biol. 13, 857-868 (2006).
55. Will, S., Reiche, K., Hofacker, I. L., Stadler, P. F., & Backofen, R. Inferring noncoding RNA families and classes by means of genome-scale structure-based clustering. PLoS Comput. Biol. 3, 680-691 (2007).
56. Yao, Z., Weinberg, Z., & Ruzzo, W. L. CMfinder-A covariance model based RNA motif finding algorithm. Bioinformatics 22, 445-452 (2006).
57. Li, Y., Zhong, C., & Zhang, S. Finding consensus stable local optimal structures for aligned RNA sequences and its application to discovering riboswitch elements. Int. J. Bioinform. Res. Appl. 10, 498-518 (2014).
58. Nawrocki, E. P., & Eddy, S. R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933-2935 (2013).
59. El Korbi, A., Ouellet, J., Naghdi, M. R., & Perreault, J. Finding instances of riboswitches and ribozymes by homology search of structured RNA with Infernal. Methods Mol. Biol. 1103, 113-126 (2014).
60. Landick, R., Wang, D., & Chan, C. L. Quantitative analysis of transcriptional pausing by Escherichia coli RNA polymerase: his leader pause site as paradigm. Methods Enzym. 274, 334-353 (1996).
61. Nudler, E., Gusarov, I., & Bar-Nahum, G. Methods of walking with the RNA polymerase. Methods Enzymol. 371, 160-169 (2003).
62. Aiba, H., Adhya, S., & de Crombrugghe, B. Evidence for two functional gal promoters in intact Escherichia coli cells. J. Biol. Chem. 256, 11905-11910 (1981).