The torpedo effect in Bacillus subtilis: RNase J1 resolves stalled transcription complexes
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
LM2015055
Czech Research Infrastructure for Systems Biology C4SYS - International
LM2015062
Light Microscopy Core Facility, IMG ASCR, Prague, Czech Republic - International
CZ.2.16/3.1.00/21547
OPPK - International
LO1419
Ministry of Education, Youth, and Sports of the Czech Republic - International
LO1509
Ministry of Education, Youth, and Sports of the Czech Republic - International
P305/12/G034
Czech Science Foundation - International
19-12956S
Czech Science Foundation - International
Agence Nationale de la Recherche (ARNr-QC) and the Labex (Dynamo) program - International
PubMed
31840842
PubMed Central
PMC6996504
DOI
10.15252/embj.2019102500
Knihovny.cz E-zdroje
- Klíčová slova
- RNAP, RNase J1, stalling, torpedo, transcription-replication collision,
- MeSH
- Bacillus subtilis enzymologie genetika MeSH
- bakteriální proteiny metabolismus MeSH
- bakteriální RNA genetika metabolismus MeSH
- DNA řízené RNA-polymerasy metabolismus MeSH
- exoribonukleasy metabolismus MeSH
- genetická transkripce MeSH
- messenger RNA genetika metabolismus MeSH
- regulace genové exprese u bakterií MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriální proteiny MeSH
- bakteriální RNA MeSH
- DNA řízené RNA-polymerasy MeSH
- exoribonukleasy MeSH
- messenger RNA MeSH
RNase J1 is the major 5'-to-3' bacterial exoribonuclease. We demonstrate that in its absence, RNA polymerases (RNAPs) are redistributed on DNA, with increased RNAP occupancy on some genes without a parallel increase in transcriptional output. This suggests that some of these RNAPs represent stalled, non-transcribing complexes. We show that RNase J1 is able to resolve these stalled RNAP complexes by a "torpedo" mechanism, whereby RNase J1 degrades the nascent RNA and causes the transcription complex to disassemble upon collision with RNAP. A heterologous enzyme, yeast Xrn1 (5'-to-3' exonuclease), is less efficient than RNase J1 in resolving stalled Bacillus subtilis RNAP, suggesting that the effect is RNase-specific. Our results thus reveal a novel general principle, whereby an RNase can participate in genome-wide surveillance of stalled RNAP complexes, preventing potentially deleterious transcription-replication collisions.
Department of Cell Biology Faculty of Science Charles University Prague Czech Republic
Division of Biomolecular Physics Institute of Physics Charles University Prague 2 Czech Republic
Institute of Microbiology of the Czech Academy of Sciences Prague 4 Czech Republic
UMR8261 CNRS Université de Paris Institut de Biologie Physico Chimique Paris France
Zobrazit více v PubMed
Arraiano CM, Andrade JM, Domingues S, Guinote IB, Malecki M, Matos RG, Moreira RN, Pobre V, Reis FP, Saramago M et al (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 34: 883–923 PubMed
Baejen C, Andreani J, Torkler P, Battaglia S, Schwalb B, Lidschreiber M, Maier KC, Boltendahl A, Rus P, Esslinger S et al (2017) Genome‐wide analysis of RNA polymerase II termination at protein‐coding genes. Mol Cell 66: 38–49 e36 PubMed
Bar‐Nahum G, Epshtein V, Ruckenstein AE, Rafikov R, Mustaev A, Nudler E (2005) A ratchet mechanism of transcription elongation and its control. Cell 120: 183–193 PubMed
Bidnenko V, Nicolas P, Grylak‐Mielnicka A, Delumeau O, Auger S, Aucouturier A, Guerin C, Repoila F, Bardowski J, Aymerich S et al (2017) Termination factor Rho: from the control of pervasive transcription to cell fate determination in Bacillus subtilis . PLoS Genet 13: e1006909 PubMed PMC
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein‐dye binding. Anal Biochem 72: 248–254 PubMed
Buskirk AR, Green R (2017) Ribosome pausing, arrest and rescue in bacteria and eukaryotes. Philos Trans R Soc Lond B Biol Sci 372: 20160183 PubMed PMC
Cascante‐Estepa N, Gunka K, Stulke J (2016) Localization of components of the RNA‐degrading machine in Bacillus subtilis . Front Microbiol 7: 1492 PubMed PMC
Chang BY, Doi RH (1990) Overproduction, purification, and characterization of Bacillus subtilis RNA polymerase sigma A factor. J Bacteriol 172: 3257–3263 PubMed PMC
Condon C, Pellegrini O, Mathy N, Benard L, Redko Y, Oussenko IA, Deikus G, Bechhofer DH (2008) Assay of Bacillus subtilis ribonucleases in vitro . Methods Enzymol 447: 277–308 PubMed
Condon C (2010) What is the role of RNase J in mRNA turnover? RNA Biol 7: 316–321 PubMed
Condon C, Piton J, Braun F (2018) Distribution of the ribosome associated endonuclease Rae1 and the potential role of conserved amino acids in codon recognition. RNA Biol 15: 683–688 PubMed PMC
Costanzo G, Pino S, Timperio AM, Sponer JE, Sponer J, Novakova O, Sedo O, Zdrahal Z, Di Mauro E (2016) Non‐enzymatic oligomerization of 3′, 5′ cyclic AMP. PLoS One 11: e0165723 PubMed PMC
Cozy LM, Kearns DB (2010) Gene position in a long operon governs motility development in Bacillus subtilis . Mol Microbiol 76: 273–285 PubMed PMC
Dengl S, Cramer P (2009) Torpedo nuclease Rat1 is insufficient to terminate RNA polymerase II in vitro . J Biol Chem 284: 21270–21279 PubMed PMC
Doherty GP, Fogg MJ, Wilkinson AJ, Lewis PJ (2010) Small subunits of RNA polymerase: localization, levels and implications for core enzyme composition. Microbiology 156: 3532–3543 PubMed
Dorleans A, Li de la Sierra‐Gallay I, Piton J, Zig L, Gilet L, Putzer H, Condon C (2011) Molecular basis for the recognition and cleavage of RNA by the bifunctional 5′‐3′ exo/endoribonuclease RNase J. Structure 19: 1252–1261 PubMed
Durand S, Gilet L, Bessieres P, Nicolas P, Condon C (2012) Three essential ribonucleases‐RNase Y, J1, and III‐control the abundance of a majority of Bacillus subtilis mRNAs. PLoS Genet 8: e1002520 PubMed PMC
Eiamphungporn W, Helmann JD (2008) The Bacillus subtilis sigma(M) regulon and its contribution to cell envelope stress responses. Mol Microbiol 67: 830–848 PubMed PMC
Epshtein V, Nudler E (2003) Cooperation between RNA polymerase molecules in transcription elongation. Science 300: 801–805 PubMed
Epshtein V, Dutta D, Wade J, Nudler E (2010) An allosteric mechanism of Rho‐dependent transcription termination. Nature 463: 245–249 PubMed PMC
Epshtein V, Kamarthapu V, McGary K, Svetlov V, Ueberheide B, Proshkin S, Mironov A, Nudler E (2014) UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature 505: 372–377 PubMed PMC
Even S, Pellegrini O, Zig L, Labas V, Vinh J, Brechemmier‐Baey D, Putzer H (2005) Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 33: 2141–2152 PubMed PMC
Fan J, Leroux‐Coyau M, Savery NJ, Strick TR (2016) Reconstruction of bacterial transcription‐coupled repair at single‐molecule resolution. Nature 536: 234–237 PubMed
Figaro S, Durand S, Gilet L, Cayet N, Sachse M, Condon C (2013) Bacillus subtilis mutants with knockouts of the genes encoding ribonucleases RNase Y and RNase J1 are viable, with major defects in cell morphology, sporulation, and competence. J Bacteriol 195: 2340–2348 PubMed PMC
Frindert J, Zhang Y, Nubel G, Kahloon M, Kolmar L, Hotz‐Wagenblatt A, Burhenne J, Haefeli WE, Jaschke A (2018) Identification, biosynthesis, and decapping of NAD‐capped RNAs in B. subtilis . Cell Rep 24: 1890–1901 e1898 PubMed
Fukushima T, Afkham A, Kurosawa S, Tanabe T, Yamamoto H, Sekiguchi J (2006) A new D, L‐endopeptidase gene product, YojL (renamed CwlS), plays a role in cell separation with LytE and LytF in Bacillus subtilis . J Bacteriol 188: 5541–5550 PubMed PMC
Gilet L, DiChiara JM, Figaro S, Bechhofer DH, Condon C (2015) Small stable RNA maturation and turnover in Bacillus subtilis . Mol Microbiol 95: 270–282 PubMed PMC
Gimpel M, Brantl S (2017) Dual‐function small regulatory RNAs in bacteria. Mol Microbiol 103: 387–397 PubMed
Goodsell DS (2001) The molecular perspective: ultraviolet light and pyrimidine dimers. Oncologist 6: 298–299 PubMed
Guo X, Myasnikov AG, Chen J, Crucifix C, Papai G, Takacs M, Schultz P, Weixlbaumer A (2018) Structural basis for NusA stabilized transcriptional pausing. Mol Cell 69: 816–827 e814 PubMed PMC
Hamperl S, Cimprich KA (2016) Conflict resolution in the genome: how transcription and replication make it work. Cell 167: 1455–1467 PubMed PMC
He B, Zalkin H (1992) Repression of Escherichia coli purB is by a transcriptional roadblock mechanism. J Bacteriol 174: 7121–7127 PubMed PMC
Helmann JD, Masiarz FR, Chamberlin MJ (1988) Isolation and characterization of the Bacillus subtilis sigma 28 factor. J Bacteriol 170: 1560–1567 PubMed PMC
Hsieh PK, Richards J, Liu Q, Belasco JG (2013) Specificity of RppH‐dependent RNA degradation in Bacillus subtilis . Proc Natl Acad Sci USA 110: 8864–8869 PubMed PMC
Hunt A, Rawlins JP, Thomaides HB, Errington J (2006) Functional analysis of 11 putative essential genes in Bacillus subtilis . Microbiology 152: 2895–2907 PubMed
Janniere L, Canceill D, Suski C, Kanga S, Dalmais B, Lestini R, Monnier AF, Chapuis J, Bolotin A, Titok M et al (2007) Genetic evidence for a link between glycolysis and DNA replication. PLoS One 2: e447 PubMed PMC
Jervis AJ, Thackray PD, Houston CW, Horsburgh MJ, Moir A (2007) SigM‐responsive genes of Bacillus subtilis and their promoters. J Bacteriol 189: 4534–4538 PubMed PMC
Jimenez RM, Polanco JA, Luptak A (2015) Chemistry and biology of self‐cleaving ribozymes. Trends Biochem Sci 40: 648–661 PubMed PMC
Juang YL, Helmann JD (1994) A promoter melting region in the primary sigma factor of Bacillus subtilis. Identification of functionally important aromatic amino acids. J Mol Biol 235: 1470–1488 PubMed
Kang JY, Mishanina TV, Landick R, Darst SA (2019) Mechanisms of transcriptional pausing in bacteria. J Mol Biol 431: 4007–4029 PubMed PMC
Kawai Y, Asai K, Errington J (2009) Partial functional redundancy of MreB isoforms, MreB, Mbl and MreBH, in cell morphogenesis of Bacillus subtilis . Mol Microbiol 73: 719–731 PubMed
Keller AN, Yang X, Wiedermannova J, Delumeau O, Krasny L, Lewis PJ (2014) epsilon, a new subunit of RNA polymerase found in gram‐positive bacteria. J Bacteriol 196: 3622–3632 PubMed PMC
Kim M, Krogan NJ, Vasiljeva L, Rando OJ, Nedea E, Greenblatt JF, Buratowski S (2004) The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature 432: 517–522 PubMed
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12: 357–360 PubMed PMC
Kireeva ML, Kashlev M (2009) Mechanism of sequence‐specific pausing of bacterial RNA polymerase. Proc Natl Acad Sci USA 106: 8900–8905 PubMed PMC
Kohler R, Mooney RA, Mills DJ, Landick R, Cramer P (2017) Architecture of a transcribing‐translating expressome. Science 356: 194–197 PubMed PMC
Komissarova N, Kireeva ML, Becker J, Sidorenkov I, Kashlev M (2003) Engineering of elongation complexes of bacterial and yeast RNA polymerases. Methods Enzymol 371: 233–251 PubMed
Krajewski WW, Fu X, Wilkinson M, Cronin NB, Dillingham MS, Wigley DB (2014) Structural basis for translocation by AddAB helicase‐nuclease and its arrest at chi sites. Nature 508: 416–419 PubMed PMC
Krasny L, Vacik T, Fucik V, Jonak J (2000) Cloning and characterization of the str operon and elongation factor Tu expression in Bacillus stearothermophilus. J Bacteriol 182: 6114–6122 PubMed PMC
Kusuya Y, Kurokawa K, Ishikawa S, Ogasawara N, Oshima T (2011) Transcription factor GreA contributes to resolving promoter‐proximal pausing of RNA polymerase in Bacillus subtilis cells. J Bacteriol 193: 3090–3099 PubMed PMC
Larson MH, Greenleaf WJ, Landick R, Block SM (2008) Applied force reveals mechanistic and energetic details of transcription termination. Cell 132: 971–982 PubMed PMC
Le TT, Yang Y, Tan C, Suhanovsky MM, Fulbright RM Jr, Inman JT, Li M, Lee J, Perelman S, Roberts JW et al (2018) Mfd dynamically regulates transcription via a release and catch‐up mechanism. Cell 172: 344–357 e315 PubMed PMC
LeBlanc SJ, Gauer JW, Hao P, Case BC, Hingorani MM, Weninger KR, Erie DA (2018) Coordinated protein and DNA conformational changes govern mismatch repair initiation by MutS. Nucleic Acids Res 46: 10782–10795 PubMed PMC
Lehnik‐Habrink M, Lewis RJ, Mader U, Stulke J (2012) RNA degradation in Bacillus subtilis: an interplay of essential endo‐ and exoribonucleases. Mol Microbiol 84: 1005–1017 PubMed
Lei Y, Oshima T, Ogasawara N, Ishikawa S (2013) Functional analysis of the protein Veg, which stimulates biofilm formation in Bacillus subtilis . J Bacteriol 195: 1697–1705 PubMed PMC
Lenhart JS, Schroeder JW, Walsh BW, Simmons LA (2012) DNA repair and genome maintenance in Bacillus subtilis . Microbiol Mol Biol Rev 76: 530–564 PubMed PMC
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R Genome Project Data Processing (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078–2079 PubMed PMC
Liu J, Hanne J, Britton BM, Bennett J, Kim D, Lee JB, Fishel R (2016) Cascading MutS and MutL sliding clamps control DNA diffusion to activate mismatch repair. Nature 539: 583–587 PubMed PMC
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biol 15: 550 PubMed PMC
Luo W, Bentley D (2004) A ribonucleolytic rat torpedoes RNA polymerase II. Cell 119: 911–914 PubMed
Ma C, Mobli M, Yang X, Keller AN, King GF, Lewis PJ (2015) RNA polymerase‐induced remodelling of NusA produces a pause enhancement complex. Nucleic Acids Res 43: 2829–2840 PubMed PMC
Mathy N, Benard L, Pellegrini O, Daou R, Wen T, Condon C (2007) 5′‐to‐3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129: 681–692 PubMed
Mathy N, Hebert A, Mervelet P, Benard L, Dorleans A, Li de la Sierra‐Gallay I, Noirot P, Putzer H, Condon C (2010) Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75: 489–498 PubMed
Mirel DB, Lustre VM, Chamberlin MJ (1992) An operon of Bacillus subtilis motility genes transcribed by the sigma D form of RNA polymerase. J Bacteriol 174: 4197–4204 PubMed PMC
Molle V, Fujita M, Jensen ST, Eichenberger P, Gonzalez‐Pastor JE, Liu JS, Losick R (2003) The Spo0A regulon of Bacillus subtilis . Mol Microbiol 50: 1683–1701 PubMed
Mori F, Tanji K, Miki Y, Toyoshima Y, Sasaki H, Yoshida M, Kakita A, Takahashi H, Wakabayashi K (2018) Immunohistochemical localization of exoribonucleases (DIS3L2 and XRN1) in intranuclear inclusion body disease. Neurosci Lett 662: 389–394 PubMed
Nadkarni A, Burns JA, Gandolfi A, Chowdhury MA, Cartularo L, Berens C, Geacintov NE, Scicchitano DA (2016) Nucleotide excision repair and transcription‐coupled DNA repair Abrogate the impact of DNA damage on transcription. J Biol Chem 291: 848–861 PubMed PMC
Nicolas P, Mader U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, Bidnenko E, Marchadier E, Hoebeke M, Aymerich S et al (2012) Condition‐dependent transcriptome reveals high‐level regulatory architecture in Bacillus subtilis . Science 335: 1103–1106 PubMed
Nudler E (2012) RNA polymerase backtracking in gene regulation and genome instability. Cell 149: 1438–1445 PubMed PMC
Panova N, Zborníková E, Šimák O, Pohl R, Kolář M, Bogdanová K, Večeřová R, Seydlová G, Fišer R, Hadravová R et al (2015) Insights into the mechanism of action of bactericidal lipophosphonoxins. PLoS One 10: e0145918 PubMed PMC
Park J, Kang M, Kim M (2015) Unraveling the mechanistic features of RNA polymerase II termination by the 5′‐3′ exoribonuclease Rat1. Nucleic Acids Res 43: 2625–2637 PubMed PMC
Pearson EL, Moore CL (2013) Dismantling promoter‐driven RNA polymerase II transcription complexes in vitro by the termination factor Rat1. J Biol Chem 288: 19750–19759 PubMed PMC
Peters JM, Mooney RA, Kuan PF, Rowland JL, Keles S, Landick R (2009) Rho directs widespread termination of intragenic and stable RNA transcription. Proc Natl Acad Sci USA 106: 15406–15411 PubMed PMC
Phung DK, Rinaldi D, Langendijk‐Genevaux PS, Quentin Y, Carpousis AJ, Clouet‐d'Orval B (2013) Archaeal beta‐CASP ribonucleases of the aCPSF1 family are orthologs of the eukaryal CPSF‐73 factor. Nucleic Acids Res 41: 1091–1103 PubMed PMC
Qi Y, Hulett FM (1998) PhoP‐P and RNA polymerase sigmaA holoenzyme are sufficient for transcription of Pho regulon promoters in Bacillus subtilis: PhoP‐P activator sites within the coding region stimulate transcription in vitro . Mol Microbiol 28: 1187–1197 PubMed
Radhakrishnan A, Green R (2016) Connections underlying translation and mRNA stability. J Mol Biol 428: 3558–3564 PubMed
Ramaniuk O, Cerny M, Krasny L, Vohradsky J (2017) Kinetic modelling and meta‐analysis of the B. subtilis SigA regulatory network during spore germination and outgrowth. Biochim Biophys Acta Gene Regul Mech 1860: 894–904 PubMed
Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, Heyne S, Dundar F, Manke T (2016) deepTools2: a next generation web server for deep‐sequencing data analysis. Nucleic Acids Res 44: W160–W165 PubMed PMC
Randall JR, Hirst WG, Simmons LA (2017) Substrate specificity for bacterial RNase HII and HIII is influenced by metal availability. J Bacteriol 200: e00401‐17 PubMed PMC
Ruff EF, Record MT Jr, Artsimovitch I (2015) Initial events in bacterial transcription initiation. Biomolecules 5: 1035–1062 PubMed PMC
Sanders K, Lin CL, Smith AJ, Cronin N, Fisher G, Eftychidis V, McGlynn P, Savery NJ, Wigley DB, Dillingham MS (2017) The structure and function of an RNA polymerase interaction domain in the PcrA/UvrD helicase. Nucleic Acids Res 45: 3875–3887 PubMed PMC
Schroeder JW, Randall JR, Hirst WG, O'Donnell ME, Simmons LA (2017) Mutagenic cost of ribonucleotides in bacterial DNA. Proc Natl Acad Sci USA 114: 11733–11738 PubMed PMC
Serizawa M, Yamamoto H, Yamaguchi H, Fujita Y, Kobayashi K, Ogasawara N, Sekiguchi J (2004) Systematic analysis of SigD‐regulated genes in Bacillus subtilis by DNA microarray and Northern blotting analyses. Gene 329: 125–136 PubMed
Shepanek NA, Smith RF, Tyer ZE, Royall GD, Allen KS (1989) Behavioral and neuroanatomical sequelae of prenatal naloxone administration in the rat. Neurotoxicol Teratol 11: 441–446 PubMed
Sikova M, Janouskova M, Ramaniuk O, Palenikova P, Pospisil J, Bartl P, Suder A, Pajer P, Kubickova P, Pavlis O et al (2018) Ms1 RNA increases the amount of RNA polymerase in Mycobacterium smegmatis . Mol Microbiol 111: 354–372 PubMed
Sun M, Schwalb B, Pirkl N, Maier KC, Schenk A, Failmezger H, Tresch A, Cramer P (2013) Global analysis of eukaryotic mRNA degradation reveals Xrn1‐dependent buffering of transcript levels. Mol Cell 52: 52–62 PubMed
Tagami S, Sekine S, Minakhin L, Esyunina D, Akasaka R, Shirouzu M, Kulbachinskiy A, Severinov K, Yokoyama S (2014) Structural basis for promoter specificity switching of RNA polymerase by a phage factor. Genes Dev 28: 521–531 PubMed PMC
Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high‐performance genomics data visualization and exploration. Brief Bioinform 14: 178–192 PubMed PMC
Tornaletti S, Hanawalt PC (1999) Effect of DNA lesions on transcription elongation. Biochimie 81: 139–146 PubMed
Toulme F, Mosrin‐Huaman C, Sparkowski J, Das A, Leng M, Rahmouni AR (2000) GreA and GreB proteins revive backtracked RNA polymerase in vivo by promoting transcript trimming. EMBO J 19: 6853–6859 PubMed PMC
Turner MS, Helmann JD (2000) Mutations in multidrug efflux homologs, sugar isomerases, and antimicrobial biosynthesis genes differentially elevate activity of the sigma(X) and sigma(W) factors in Bacillus subtilis . J Bacteriol 182: 5202–5210 PubMed PMC
Twist KA, Campbell EA, Deighan P, Nechaev S, Jain V, Geiduschek EP, Hochschild A, Darst SA (2011) Crystal structure of the bacteriophage T4 late‐transcription coactivator gp33 with the beta‐subunit flap domain of Escherichia coli RNA polymerase. Proc Natl Acad Sci USA 108: 19961–19966 PubMed PMC
Weiss A, Shaw LN (2015) Small things considered: the small accessory subunits of RNA polymerase in Gram‐positive bacteria. FEMS Microbiol Rev 39: 541–554 PubMed PMC
Wiedermannova J, Sudzinova P, Koval T, Rabatinova A, Sanderova H, Ramaniuk O, Rittich S, Dohnalek J, Fu Z, Halada P et al (2014) Characterization of HelD, an interacting partner of RNA polymerase from Bacillus subtilis . Nucleic Acids Res 42: 5151–5163 PubMed PMC
Yakhnin AV, Murakami KS, Babitzke P (2016) NusG is a sequence‐specific RNA polymerase pause factor that binds to the non‐template DNA within the paused transcription bubble. J Biol Chem 291: 5299–5308 PubMed PMC
Yang XC, Sullivan KD, Marzluff WF, Dominski Z (2009) Studies of the 5′ exonuclease and endonuclease activities of CPSF‐73 in histone pre‐mRNA processing. Mol Cell Biol 29: 31–42 PubMed PMC
Zhang Y, Mooney RA, Grass JA, Sivaramakrishnan P, Herman C, Landick R, Wang JD (2014) DksA guards elongating RNA polymerase against ribosome‐stalling‐induced arrest. Mol Cell 53: 766–778 PubMed PMC
Zhu B, Stulke J (2018) SubtiWiki in 2018: from genes and proteins to functional network annotation of the model organism Bacillus subtilis. Nucleic Acids Res 46: D743–D748 PubMed PMC
Zweers JC, Nicolas P, Wiegert T, van Dijl JM, Denham EL (2012) Definition of the sigma(W) regulon of Bacillus subtilis in the absence of stress. PLoS One 7: e48471 PubMed PMC
The alternative sigma factor SigN of Bacillus subtilis is intrinsically toxic
LEGO-Lipophosphonoxins: A Novel Approach in Designing Membrane Targeting Antimicrobials
β-CASP proteins removing RNA polymerase from DNA: when a torpedo is needed to shoot a sitting duck
Mycobacterial HelD is a nucleic acids-clearing factor for RNA polymerase