Investigating the role of RNA structures in transcriptional pausing using in vitro assays and in silico analyses

References

• Pan T, Sosnick T. RNA folding during transcription. Annu Rev Biophys Biomol Struct. 2006;35:161–175.
   PubMedGoogle Scholar
• Belogurov GA, Artsimovitch I. Regulation of transcript elongation. Annu Rev Microbiol. 2015;69:49–69.
   PubMed Web of Science ®Google Scholar
• Proshkin S, Rahmouni AR, Mironov A, et al. Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science. 2010;328:504–508.
   PubMed Web of Science ®Google Scholar
• Chauvier A, Nadon J-F, Grondin JP, et al. Role of a hairpin-stabilized pause in the Escherichia coli thiC riboswitch function. RNA Biol. 2019;16:1066–1073.
   PubMed Web of Science ®Google Scholar
• Richardson JP. Rho-dependent transcription termination. Biochim Biophys Acta. 1990;1048:127–138.
   PubMedGoogle Scholar
• Farnham PJ, Platt T. Rho-independent termination: dyad symmetry in DNA causes RNA polymerase to pause during transcription in vitro. Nucleic Acids Res. 1981;9:563–577.
   PubMed Web of Science ®Google Scholar
• Landick R. The regulatory roles and mechanism of transcriptional pausing. Biochem Soc Trans. 2006;34:1062–1066.
   PubMed Web of Science ®Google Scholar
• Kassavetis GA, Chamberlin MJ. Pausing and termination of transcription within the early region of bacteriophage T7 DNA in vitro. J Biol Chem. 1981;256:2777–2786.
   PubMed Web of Science ®Google Scholar
• Coppola JA, Field AS, Luse DS. Promoter-proximal pausing by RNA polymerase II in vitro: transcripts shorter than 20 nucleotides are not capped. Proc Natl Acad Sci USA. 1983;80:1251–1255.
   PubMed Web of Science ®Google Scholar
• Maderious A, Chen-Kiang S. Pausing and premature termination of human RNA polymerase II during transcription of adenovirus in vivo and in vitro. Proc Natl Acad Sci USA. 1984;81:5931–5935.
   PubMed Web of Science ®Google Scholar
• Kadesch TR, Chamberlin MJ. Studies of in vitro transcription by calf thymus RNA polymerase II using a novel duplex DNA template. J Biol Chem. 1982;257:5286–5295.
   PubMed Web of Science ®Google Scholar
• Kang JY, Mishanina TV, Landick R, et al. Mechanisms of transcriptional pausing in bacteria. J Mol Biol. 2019;431:4007–4029.
   PubMed Web of Science ®Google Scholar
• Landick R, Wang D, Chan CL. Quantitative analysis of transcriptional pausing by Escherichia coli RNA polymerase: his leader pause site as paradigm. Methods Enzym. 1996;274:334–353.
   PubMed Web of Science ®Google Scholar
• Nadon J-F, Epshtein V, Cameron E, et al. Site-specific photolabile roadblocks for the study of transcription elongation in biologically complex systems. Commun Biol. 2022;5:457.
   PubMed Web of Science ®Google Scholar
• Landick R. Transcriptional pausing as a mediator of bacterial gene regulation. Annu Rev Microbiol. 2021;75:291–314.
   PubMed Web of Science ®Google Scholar
• Zhang J, Landick R. A two-way street: regulatory interplay between RNA polymerase and nascent RNA structure. Trends Biochem Sci. 2016;41:293–310.
   PubMed Web of Science ®Google Scholar
• Kang JY, Mishanina TV, Bellecourt MJ, et al. RNA polymerase accommodates a pause RNA hairpin by global conformational rearrangements that prolong pausing. Mol Cell. 2018;69:802–815.e5.
   PubMed Web of Science ®Google Scholar
• Chan CL, Wang D, Landick R. Multiple interactions stabilize a single paused transcription intermediate in which hairpin to 3’ end spacing distinguishes pause and termination pathways. J Mol Biol. 1997;268:54–68.
   PubMed Web of Science ®Google Scholar
• Chan CL, Landick R. The Salmonella typhimurium his operon leader region contains an RNA hairpin-dependent transcription pause site Mechanistic implications of the effect on pausing of altered RNA hairpins. J Biol Chem. 1989;264:20796–20804.
   PubMed Web of Science ®Google Scholar
• Landick R, Yanofsky C. Stability of an RNA secondary structure affects in vitro transcription pausing in the trp operon leader region. J Biol Chem. 1984;259:11550–11555.
   PubMed Web of Science ®Google Scholar
• Fisher R, Yanofsky C. A complementary DNA oligomer releases a transcription pause complex. J Biol Chem. 1983;258:9208–9212.
   PubMed Web of Science ®Google Scholar
• Ingham CJ, Dennis J, Furneaux PA. Autogenous regulation of transcription termination factor Rho and the requirement for Nus factors in Bacillus subtilis, Mol. Microbiol. 1999;31:651–663.
   Web of Science ®Google Scholar
• Greenblatt J, McLimont M, Hanly S. Termination of transcription by nusA gene protein of Escherichia coli. Nature. 1981;292:215–220.
   PubMed Web of Science ®Google Scholar
• Burns CM, Richardson LV, Richardson JP. Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli. J Mol Biol. 1998;278:307–316.
   PubMed Web of Science ®Google Scholar
• Chan CL, Landick R. Dissection of the his leader pause site by base substitution reveals a multipartite signal that includes a pause RNA hairpin. J Mol Biol. 1993;233:25–42.
   PubMed Web of Science ®Google Scholar
• Johnston HM, Roth JR. DNA sequence changes of mutations altering attenuation control of the histidine operon of Salmonella typhimurium. J Mol Biol. 1981;145:735–756.
   PubMed Web of Science ®Google Scholar
• Barnes WM, Tuley E. DNA sequence changes of mutations in the histidine operon control region that decrease attenuation. J Mol Biol. 1983;165:443–459.
   PubMed Web of Science ®Google Scholar
• Landick R, Yanofsky C, Choo K, et al. Replacement of the Escherichia coli trp operon attenuation control codons alters operon expression. J Mol Biol. 1990;216:25–37.
   PubMed Web of Science ®Google Scholar
• Churchman LS, Weissman JS. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature. 2011;469:368–373.
   PubMed Web of Science ®Google Scholar
• Larson MH, Mooney RA, Peters JM, et al. A pause sequence enriched at translation start sites drives transcription dynamics in vivo. Science. 2014;344:1042–1047.
   PubMed Web of Science ®Google Scholar
• Imashimizu M, Takahashi H, Oshima T, et al. Visualizing translocation dynamics and nascent transcript errors in paused RNA polymerases in vivo. Genome Biol. 2015;16:98.
   PubMed Web of Science ®Google Scholar
• Vvedenskaya IO, Vahedian-Movahed H, Bird JG, et al. Interactions between RNA polymerase and the “core recognition element” counteract pausing. Science. 2014;344:1285–1289.
   PubMed Web of Science ®Google Scholar
• Saba J, Chua XY, Mishanina TV, et al. The elemental mechanism of transcriptional pausing. Elife. 2019;8. DOI:10.7554/eLife.40981
   PubMed Web of Science ®Google Scholar
• Artsimovitch I, Landick R. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc Natl Acad Sci USA. 2000;97:7090–7095.
   PubMed Web of Science ®Google Scholar
• Wong TN, Sosnick TR, Pan T. Folding of noncoding RNAs during transcription facilitated by pausing-induced nonnative structures. Proc Natl Acad Sci USA. 2007;104:17995–18000.
   PubMed Web of Science ®Google Scholar
• Lee Y, Ramamoorthy R, Park CU, et al. Sites of initiation and pausing in the Escherichia coli rnpB (M1 RNA) transcript. J Biol Chem. 1989;264:5098–5103.
   PubMed Web of Science ®Google Scholar
• Bartkus JM, Tyler B, Calvo JM. Transcription attenuation-mediated control of leu operon expression: influence of the number of Leu control codons. J Bacteriol. 1991;173:1634–1641.
   PubMed Web of Science ®Google Scholar
• Keller EB, Calvo JM. Alternative secondary structures of leader RNAs and the regulation of the trp, phe, his, thr, and leu operons. Proc Natl Acad Sci USA. 1979;76:6186–6190.
   PubMed Web of Science ®Google Scholar
• Zurawski G, Brown K, Killingly D, et al. Nucleotide sequence of the leader region of the phenylalanine operon of Escherichia coli. Proc Natl Acad Sci USA. 1978;75:4271–4275.
   PubMed Web of Science ®Google Scholar
• Yang MT, Gardner JF. Isolation and footprint analysis of the Escherichia coli thr leader paused transcription complex. Nucleic Acids Res. 1991;19:1671–1680.
   PubMed Web of Science ®Google Scholar
• Donahue JP, Turnbough CL. Nucleotide-specific transcriptional pausing in the pyrBI leader region of Escherichia coli K-12. J Biol Chem. 1994;269:18185–18191.
   PubMed Web of Science ®Google Scholar
• Gardner JF. Initiation, pausing, and termination of transcription in the threonine operon regulatory region of Escherichia coli. J Biol Chem. 1982;257:3896–3904.
   PubMed Web of Science ®Google Scholar
• Winkler ME, Yanofsky C. Pausing of RNA polymerase during in vitro transcription of the tryptophan operon leader region. Biochemistry. 1981;20(13):3738–3744.
   PubMed Web of Science ®Google Scholar
• Landick R, Yanofsky C. Isolation and structural analysis of the Escherichia coli trp leader paused transcription complex. J Mol Biol. 1987;196:363–377.
   PubMed Web of Science ®Google Scholar
• Kyzer S, Ha KS, Landick R, et al. Direct versus limited-step reconstitution reveals key features of an RNA hairpin-stabilized paused transcription complex. J Biol Chem. 2007;282:19020–19028.
   PubMed Web of Science ®Google Scholar
• Farnham PJ, Greenblatt J, Platt T. Effects of NusA protein on transcription termination in the tryptophan operon of Escherichia coli. Cell. 1982;29:945–951.
   PubMed Web of Science ®Google Scholar
• Chen JW, Harms E, Umbarger HE. Mutations replacing the leucine codons or altering the length of the amino acid-coding portion of the ilvGMEDA leader region of Escherichia coli. J Bacteriol. 1991;173:2341–2353.
   PubMed Web of Science ®Google Scholar
• Lynn SP, Gardner JF, Reznikoff WS. Attenuation regulation in the thr operon of Escherichia coli K-12: molecular cloning and transcription of the controlling region. J Bacteriol. 1982;152:363–371.
   PubMed Web of Science ®Google Scholar
• Levin HL, Schachman HK. Regulation of aspartate transcarbamoylase synthesis in Escherichia coli: analysis of deletion mutations in the promoter region of the pyrBI operon. Proc Natl Acad Sci USA. 1985;82:4643–4647.
   PubMed Web of Science ®Google Scholar
• Springer M, Trudel M, Graffe M, et al. Escherichia coli phenylalanyl-tRNA synthetase operon is controlled by attenuation in vivo. J Mol Biol. 1983;171:263–279.
   PubMed Web of Science ®Google Scholar
• Lorenz R, Bernhart SH, Höner Zu Siederdissen C, et al. ViennaRNA package 20, algorithms. Mol Biol. 2011;6:26.
   Web of Science ®Google Scholar
• Weinberg Z, Breaker RR. R2R–software to speed the depiction of aesthetic consensus RNA secondary structures. BMC Bioinf. 2011;12:3.
   PubMed Web of Science ®Google Scholar
• Baty F, Ritz C, Charles S, et al. A toolbox for nonlinear regression in R: the package nlstools. J Stat Softw. 2015;66(5):1–21.
   Web of Science ®Google Scholar
• Welch BL. The generalisation of student’s problems when several different population variances are involved. Biometrika. 1947;34:28–35.
   PubMed Web of Science ®Google Scholar
• Hulsen T, de Vlieg J, Alkema W. BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics. 2008;9:488.
   PubMed Web of Science ®Google Scholar