ε, a new subunit of RNA polymerase found in gram-positive bacteria

Journal of Bacteriology

Volumn 196, Issue 20, 2014, Pages 3622-3632

  Keller, Andrew N ^a   Yang, Xiao ^a   Wiedermannova´, Jana ^b   Delumeau, Olivier ^c   Kra´sny´, Libor ^b   Lewis, Peter J ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^c UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE; RNA POLYMERASE EPSILON SUBUNIT; UNCLASSIFIED DRUG; DNA DIRECTED RNA POLYMERASE; PROTEIN SUBUNIT;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; COMPLEX FORMATION; CRYSTALLIZATION; DNA BINDING; ENTEROBACTERIA PHAGE T7; ENZYME STRUCTURE; GENE DELETION; NONHUMAN; OPERON; PHENOTYPE; PHYLUM; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; TRANSCRIPTION INITIATION; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ANIMALS; BACILLUS SUBTILIS; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN SUBUNITS;

EID: 84907088279     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02020-14     Document Type: Article

References (55)

1. Burgess RR. 1969. Separation and characterization of the subunits of ribonucleic acid polymerase. J. Biol. Chem. 244:6168-6176.
2. Wiedermannova J, Sudzinova P, Koval T, Rabatinova A, Sanderova H, Ramaniuk O, Rittich S, Dohnalek J, Fu Z, Lewis P, Halada P, Krasny L. 2014. Characterization of HelD, an interacting partner of RNA polymerase from Bacillus subtilis. Nucleic Acids Res. 42:5151-5163. http://dx.doi.org/10.1093/nar/gku113.
3. Juang YL, Helmann JD. 1994. The delta subunit of Bacillus subtilis RNA polymerase. An allosteric effector of the initiation and core-recycling phases of transcription. J. Mol. Biol. 239:1-14.
4. Rabatinova A, Sanderova H, Jirat Matejckova J, Korelusova J, Sojka L, Barvik I, Papouskova V, Sklenar V, Zidek L, Krasny L. 2013. The delta subunit of RNA polymerase is required for rapid changes in gene expression and competitive fitness of the cell. J. Bacteriol. 195:2603-2611. http://dx.doi.org/10.1128/JB.00188-13.
5. Lopez de Saro FJ, Woody AY, Helmann JD. 1995. Structural analysis of the Bacillus subtilis delta factor: a protein polyanion which displaces RNA from RNA polymerase. J. Mol. Biol. 252:189-202. http://dx.doi.org/10.1006/jmbi.1995.0487.
6. Delumeau O, Lecointe F, Muntel J, Guillot A, Guedon E, Monnet V, Hecker M, Becher D, Polard P, Noirot P. 2011. The dynamic protein partnership of RNA polymerase in Bacillus subtilis. Proteomics 11:2992-3001. http://dx.doi.org/10.1002/pmic.201000790.
7. Helmann JD. 2003. Purification of Bacillus subtilis RNA polymerase and associated factors. Methods Enzymol. 370:10-24. http://dx.doi.org/10.1016/S0076-6879(03)70002-0.
8. Yang X, Lewis PJ. 2008. Overproduction and purification of recombinant Bacillus subtilisRNApolymerase. Protein Expr. Purif. 59:86-93. http://dx.doi.org/10.1016/j.pep.2008.01.006.
9. Spiegelman GB, Hiatt WR, Whiteley HR. 1978. Role of the 21,000 molecular weight polypeptide of Bacillus subtilis RNA polymerase in RNA synthesis. J. Biol. Chem. 253:1756-1765.
10. Achberger EC, Tahara M, Whiteley HR. 1982. Interchangeability of delta subunits ofRNApolymerase from different species of the genus Bacillus. J. Bacteriol. 150:977-980.
11. Gentry DR, Burgess RR. 1986. The cloning and sequence of the gene encoding the omega subunit of Escherichia coli RNA polymerase. Gene 48:33-40. http://dx.doi.org/10.1016/0378-1119(86)90349-5.
12. 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. http://dx.doi.org/10.1128/JB.00164-13.
13. Kunst F, Rapoport G. 1995. Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J. Bacteriol. 177:2403-2407.
14. Guerout-Fleury AM, Frandsen N, Stragier P. 1996. Plasmids for ectopic integration in Bacillus subtilis. Gene 180:57-61. http://dx.doi.org/10.1016/S0378-1119(96)00404-0.
15. Nicolas P, Mader U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, Bidnenko E, Marchadier E, Hoebeke M, Aymerich S, Becher D, Bisicchia P, Botella E, Delumeau O, Doherty G, Denham EL, Fogg MJ, Fromion V, Goelzer A, Hansen A, Hartig E, Harwood CR, Homuth G, Jarmer H, Jules M, Klipp E, Le Chat L, Lecointe F, Lewis P, Liebermeister W, March A, Mars RA, Nannapaneni P, Noone D, Pohl S, Rinn B, Rugheimer F, Sappa PK, Samson F, Schaffer M, Schwikowski B, Steil L, Stulke J, Wiegert T, Devine KM, Wilkinson AJ, van Dijl JM, Hecker M, Volker U, Bessieres P, Noirot P. 2012. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335:1103-1106. http://dx.doi.org/10.1126/science.1206848.
16. Doherty GP, Meredith DH, Lewis PJ. 2006. Subcellular partitioning of transcription factors in Bacillus subtilis. J. Bacteriol. 188:4101-4110. http://dx.doi.org/10.1128/JB.01934-05.
17. 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. http://dx.doi.org/10.1099/mic.0.041566-0.
18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404.
19. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059-3066. http://dx.doi.org/10.1093/nar/gkf436.
20. Ling MM, Robinson BH. 1997. Approaches to DNA mutagenesis: an overview. Anal. Biochem. 254:157-178. http://dx.doi.org/10.1006/abio.1997.2428.
21. Quin M, Newman J, Firbank S, Lewis RJ, Marles-Wright J. 2008. Crystallization and preliminary X-ray analysis of RsbS from Moorella thermoacetica at 2.5 A˚ resolution. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64:196-199. http://dx.doi.org/10.1107/S1744309108003849.
22. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM, Ellis PJ, Garman E, Gonzalez A, Sauter NK, Phizackerley RP, Soltis SM, Kuhn P. 2002. Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J. Synchrotron Radiat. 9:401-406. http://dx.doi.org/10.1107/S0909049502015170.
23. Evens G, Pettifer RF. 2001. CHOOCH: a program for deriving anomalous-scattering factors from X-ray fluorescence spectra. J. Appl. Crystallogr. 34:82-86. http://dx.doi.org/10.1107/S0021889800014655.
24. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. 2011. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67:271-281. http://dx.doi.org/10.1107/S0907444910048675.
25. Leslie AG. 2006. The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 62:48-57. http://dx.doi.org/10.1107/S0907444905039107.
26. CCP4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763. http://dx.doi.org/10.1107/S0907444994003112.
27. Ness SR, de Graaff RA, Abrahams JP, Pannu NS. 2004. CRANK: new methods for automated macromolecular crystal structure solution. Structure 12:1753-1761. http://dx.doi.org/10.1016/j.str.2004.07.018.
28. de Graaff RA, Hilge M, van der Plas JL, Abrahams JP. 2001. Matrix methods for solving protein substructures of chlorine and sulfur from anomalous data. Acta Crystallogr.DBiol. Crystallogr. 57:1857-1862. http://dx.doi.org/10.1107/S0907444901016535.
29. Abrahams JP, Leslie AG. 1996. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr.DBiol. Crystallogr. 52:30-42. http://dx.doi.org/10.1107/S0907444995008754.
30. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62:1002-1011. http://dx.doi.org/10.1107/S0907444906022116.
31. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501. http://dx.doi.org/10.1107/S0907444910007493.
32. Langer G, Cohen SX, Lamzin VS, Perrakis A. 2008. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3:1171-1179. http://dx.doi.org/10.1038/nprot.2008.91.
33. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Echols N, Headd JJ, Hung LW, Jain S, Kapral GJ, Grosse Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner RD, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2011. The Phenix software for automated determination of macromolecular structures. Methods 55:94-106. http://dx.doi.org/10.1016/j.ymeth.2011.07.005.
34. Yang X, Molimau S, Doherty GP, Johnston EB, Marles-Wright J, Rothnagel R, Hankamer B, Lewis RJ, Lewis PJ. 2009. The structure of bacterial RNA polymerase in complex with the essential transcription elongation factor NusA. EMBO Rep. 10:997-1002. http://dx.doi.org/10.1038/embor.2009.155.
35. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128:82-97. http://dx.doi.org/10.1006/jsbi.1999.4174.
36. Davies KM, Lewis PJ. 2003. Localization of rRNA synthesis in Bacillus subtilis: characterization of loci involved in transcription focus formation. J. Bacteriol. 185:2346-2353. http://dx.doi.org/10.1128/JB.185.7.2346-2353.2003.
37. Lewis PJ, Thaker SD, Errington J. 2000. Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J. 19:710-718. http://dx.doi.org/10.1093/emboj/19.4.710.
38. Britton RA, Wen T, Schaefer L, Pellegrini O, Uicker WC, Mathy N, Tobin C, Daou R, Szyk J, Condon C. 2007. Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol. Microbiol. 63:127-138. http://dx.doi.org/10.1111/j.1365-2958.2006.05499.x.
39. Hunt A, Rawlins JP, Thomaides HB, Errington J. 2006. Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152:2895-2907. http://dx.doi.org/10.1099/mic.0.29152-0.
40. Gabdulkhakov A, Nikonov S, Garber M. 2013. Revisiting the Haloarcula marismortui 50S ribosomal subunit model. Acta Crystallogr.DBiol. Crystallogr. 69:997-1004. http://dx.doi.org/10.1107/S0907444913004745.
41. Serrano-Heras G, Salas M, Bravo A. 2006. A uracil-DNA glycosylase inhibitor encoded by a non-uracil containing viral DNA. J. Biol. Chem. 281:7068-7074. http://dx.doi.org/10.1074/jbc.M511152200.
42. Serrano-Heras G, Ruiz-Maso JA, del Solar G, Espinosa M, Bravo A, Salas M. 2007. Protein p56 from the Bacillus subtilis phage phi29 inhibits DNA-binding ability of uracil-DNA glycosylase. Nucleic Acids Res. 35:5393-5401. http://dx.doi.org/10.1093/nar/gkm584.
43. Hesselbach BA, Nakada D. 1977. I protein: bacteriophage T7-coded inhibitor of Escherichia coli RNA polymerase. J. Virol. 24:746-760.
44. Nechaev S, Severinov K. 1999. Inhibition of Escherichia coli RNA polymerase by bacteriophage T7 gene 2 protein. J. Mol. Biol. 289:815-826. http://dx.doi.org/10.1006/jmbi.1999.2782.
45. Bae B, Davis E, Brown D, Campbell EA, Wigneshweraraj S, Darst SA. 2013. Phage T7 Gp2 inhibition of Escherichia coli RNA polymerase involves misappropriation of sigma70 domain 1.1. Proc. Natl. Acad. Sci. U. S. A. 110:19772-19777. http://dx.doi.org/10.1073/pnas.1314576110.
46. James E, Liu M, Sheppard C, Mekler V, Camara B, Liu B, Simpson P, Cota E, Severinov K, Matthews S, Wigneshweraraj S. 2012. Structural and mechanistic basis for the inhibition of Escherichia coli RNA polymerase by T7 Gp2. Mol. Cell 47:755-766. http://dx.doi.org/10.1016/j.molcel.2012.06.013.
47. Sheppard C, Camara B, Shadrin A, Akulenko N, Liu M, Baldwin G, Severinov K, Cota E, Matthews S, Wigneshweraraj SR. 2011. Inhibition of Escherichia coli RNAp by T7 Gp2 protein: role of negatively charged strip of amino acid residues in Gp2. J. Mol. Biol. 407:623-632. http://dx.doi.org/10.1016/j.jmb.2011.02.013.
48. Camara B, Liu M, Reynolds J, Shadrin A, Liu B, Kwok K, Simpson P, Weinzierl R, Severinov K, Cota E, Matthews S, Wigneshweraraj SR. 2010. T7 phage protein Gp2 inhibits the Escherichia coli RNA polymerase by antagonizing stable DNA strand separation near the transcription start site. Proc. Natl. Acad. Sci. U. S. A. 107:2247-2252. http://dx.doi.org/10.1073/pnas.0907908107.
49. Vrentas CE, Gaal T, Ross W, Ebright RH, Gourse RL. 2005. Response of RNA polymerase to ppGpp: requirement for the omega subunit and relief of this requirement by DksA. Genes Dev. 19:2378-2387. http://dx.doi.org/10.1101/gad.1340305.
50. Perederina A, Svetlov V, Vassylyeva MN, Tahirov TH, Yokoyama S, Artsimovitch I, Vassylyev DG. 2004. Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription. Cell 118:297-309. http://dx.doi.org/10.1016/j.cell.2004.06.030.
51. Vassylyeva MN, Svetlov V, Dearborn AD, Klyuyev S, Artsimovitch I, Vassylyev DG. 2007. The carboxy-terminal coiled-coil of the RNA polymerase ß'-subunit is the main binding site for Gre factors. EMBO Rep. 8:1038-1043. http://dx.doi.org/10.1038/sj.embor.7401079.
52. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. 2004. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32:W665-W667. http://dx.doi.org/10.1093/nar/gkh381.
53. Studier FW, Moffatt BA. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130. http://dx.doi.org/10.1016/0022-2836(86)90385-2.
54. Neylon C, Brown SE, Kralicek AV, Miles CS, Love CA, Dixon NE. 2000. Interaction of the Escherichia coli replication terminator protein (Tus) with DNA: a model derived from DNA-binding studies of mutant proteins by surface plasmon resonance. Biochemistry 39:11989-11999. http://dx.doi.org/10.1021/bi001174w.
55. Lewis PJ, Marston AL. 1999. GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227:101-110. http://dx.doi.org/10.1016/S0378-1119(98)00580-0.