Initial Events in Bacterial Transcription Initiation

Biomolecules - Tập 5 Số 2 - Trang 1035-1062
Emily Ruff1, M. Thomas Record2, Irina Artsimovitch3
1Department of Biochemistry, University of Wisconsin-Madison, 1101 University Ave. Madison, Madison, WI 53706, USA. [email protected].
2Departments of Chemistry and Biochemistry, University of Wisconsin-Madison, 1101 University Ave. Madison, Madison, WI 53706, USA. [email protected].
3Department of Microbiology, The Ohio State University, 105 Biological Sciences, 484 W 12th Ave, Columbus, OH 43210, USA. [email protected].

Tóm tắt

Transcription initiation is a highly regulated step of gene expression. Here, we discuss the series of large conformational changes set in motion by initial specific binding of bacterial RNA polymerase (RNAP) to promoter DNA and their relevance for regulation. Bending and wrapping of the upstream duplex facilitates bending of the downstream duplex into the active site cleft, nucleating opening of 13 bp in the cleft. The rate-determining opening step, driven by binding free energy, forms an unstable open complex, probably with the template strand in the active site. At some promoters, this initial open complex is greatly stabilized by rearrangements of the discriminator region between the −10 element and +1 base of the nontemplate strand and of mobile in-cleft and downstream elements of RNAP. The rate of open complex formation is regulated by effects on the rapidly-reversible steps preceding DNA opening, while open complex lifetime is regulated by effects on the stabilization of the initial open complex. Intrinsic DNA opening-closing appears less regulated. This noncovalent mechanism and its regulation exhibit many analogies to mechanisms of enzyme catalysis.

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Tài liệu tham khảo

Decker, 2013, Transcription regulation at the core: Similarities among bacterial, archaeal, and eukaryotic RNA polymerases, Annu. Rev. Microbiol., 67, 113, 10.1146/annurev-micro-092412-155756

Ebright, 2000, RNA polymerase: Structural similarities between bacterial RNA polymerase and eukaryotic RNA polymerase II, J. Mol. Biol., 304, 687, 10.1006/jmbi.2000.4309

Saecker, 2011, Mechanism of bacterial transcription initiation: RNA polymerase—Promoter binding, isomerization to initiation-competent open complexes, and initiation of RNA synthesis, J. Mol. Biol., 412, 754, 10.1016/j.jmb.2011.01.018

Dorman, 2013, Co-operative roles for DNA supercoiling and nucleoid-associated proteins in the regulation of bacterial transcription, Biochem. Soc. Trans., 41, 542, 10.1042/BST20120222

Feklistov, 2014, Bacterial sigma factors: A historical, structural, and genomic perspective, Annu. Rev. Microbiol., 68, 357, 10.1146/annurev-micro-092412-155737

Haugen, 2008, Advances in bacterial promoter recognition and its control by factors that do not bind DNA, Nat. Rev. Microbiol., 6, 507, 10.1038/nrmicro1912

Lee, 2012, Activating transcription in bacteria, Annu. Rev. Microbiol., 66, 125, 10.1146/annurev-micro-092611-150012

Bae, 2013, Phage T7 Gp2 inhibition of Escherichia coli RNA polymerase involves misappropriation of σ70 domain 1.1, Proc. Natl. Acad. Sci. USA, 110, 19772, 10.1073/pnas.1314576110

Basu, 2014, Structural basis of transcription initiation by bacterial RNA polymerase holoenzyme, J. Biol. Chem., 289, 24549, 10.1074/jbc.M114.584037

Feklistov, 2011, Structural basis for promoter-10 element recognition by the bacterial RNA polymerase sigma subunit, Cell, 147, 1257, 10.1016/j.cell.2011.10.041

Lawson, 2004, Catabolite activator protein: DNA binding and transcription activation, Curr. Opin. Struct. Biol., 14, 10, 10.1016/j.sbi.2004.01.012

Murakami, 2013, X-ray crystal structure of Escherichia coli RNA polymerase σ70 holoenzyme, J. Biol. Chem., 288, 9126, 10.1074/jbc.M112.430900

Murakami, 2002, Structural basis of transcription initiation: An RNA polymerase holoenzyme-DNA complex, Science, 296, 1285, 10.1126/science.1069595

Murakami, 2002, Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 Å resolution, Science, 296, 1280, 10.1126/science.1069594

Murakami, 2003, Crystallographic analysis of Thermus aquaticus RNA polymerase holoenzyme and a holoenzyme/promoter DNA complex, Methods Enzymol., 370, 42, 10.1016/S0076-6879(03)70004-4

Vassylyev, 2002, Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution, Nature, 417, 712, 10.1038/nature752

Zhang, 2012, Structural basis of transcription initiation, Science, 338, 1076, 10.1126/science.1227786

Ruff, E.F., Drennan, A., Capp, M.W., Poulos, M.A., Artsimovitch, I., and Record, M.T. (2015). Escherichia coli RNA polymerase determinants of open complex lifetime and structure. J. Mol. Biol., In press.

Rutherford, S.T. (2008). Insights into the Mechanism of DksA Action at Ribosomal RNA Promoters in Escherichia coli, University of Wisconsin.

Rammohan, 2015, CarD stabilizes mycobacterial open complexes via a two-tiered kinetic mechanism, Nucleic Acids Res., 43, 3272, 10.1093/nar/gkv078

Friedman, 2012, Mechanism of transcription initiation at an activator-dependent promoter defined by single-molecule observation, Cell, 148, 679, 10.1016/j.cell.2012.01.018

Heyduk, 2014, Next generation sequencing-based parallel analysis of melting kinetics of 4096 variants of a bacterial promoter, Biochemistry, 53, 282, 10.1021/bi401277w

Gries, 2010, One-step DNA melting in the RNA polymerase cleft opens the initiation bubble to form an unstable open complex, Proc. Natl. Acad. Sci. USA, 107, 10418, 10.1073/pnas.1000967107

Kontur, 2008, Late steps in the formation of E. coli RNA polymerase-λPR promoter open complexes: Characterization of conformational changes by rapid [perturbant] upshift experiments, J. Mol. Biol., 376, 1034, 10.1016/j.jmb.2007.11.064

Rogozina, 2009, DNA melting by RNA polymerase at the T7A1 promoter precedes the rate-limiting step at 37 degrees C and results in the accumulation of an off-pathway intermediate, Nucleic Acids Res., 37, 5390, 10.1093/nar/gkp560

Sclavi, 2005, Real-time characterization of intermediates in the pathway to open complex formation by Escherichia coli RNA polymerase at the T7A1 promoter, Proc. Natl. Acad. Sci. USA, 102, 4706, 10.1073/pnas.0408218102

Davis, 2007, Real-time footprinting of DNA in the first kinetically significant intermediate in open complex formation by Escherichia coli RNA polymerase, Proc. Natl. Acad. Sci. USA, 104, 7833, 10.1073/pnas.0609888104

Ko, 2014, Kinetics of promoter escape by bacterial RNA polymerase: Effects of promoter contacts and transcription bubble collapse, Biochem. J., 463, 135, 10.1042/BJ20140179

Mekler, 2014, Coupling of downstream RNA polymerase-promoter interactions with formation of catalytically competent transcription initiation complex, J. Mol. Biol., 426, 3973, 10.1016/j.jmb.2014.10.005

Mekler, 2011, A critical role of downstream RNA polymerase-promoter interactions in the formation of initiation complex, J. Biol. Chem., 286, 22600, 10.1074/jbc.M111.247080

Mekler, 2011, Interaction of Escherichia coli RNA polymerase σ70 subunit with promoter elements in the context of free σ70, RNA polymerase holoenzyme, and the β'-σ70 complex, J. Biol. Chem., 286, 270, 10.1074/jbc.M110.174102

Revyakin, 2004, Promoter unwinding and promoter clearance by RNA polymerase: Detection by single-molecule DNA nanomanipulation, Proc. Natl. Acad. Sci. USA, 101, 4776, 10.1073/pnas.0307241101

Revyakin, 2006, Abortive initiation and productive initiation by RNA polymerase involve DNA scrunching, Science, 314, 1139, 10.1126/science.1131398

Robb, 2013, The transcription bubble of the RNA polymerase-promoter open complex exhibits conformational heterogeneity and millisecond-scale dynamics: Implications for transcription start-site selection, J. Mol. Biol., 425, 875, 10.1016/j.jmb.2012.12.015

Schroeder, 2009, Evidence for a tyrosine-adenine stacking interaction and for a short-lived open intermediate subsequent to initial binding of Escherichia coli RNA polymerase to promoter DNA, J. Mol. Biol., 385, 339, 10.1016/j.jmb.2008.10.023

Burgess, 1969, Separation and characterization of the subunits of ribonucleic acid polymerase, J. Biol. Chem., 244, 6168, 10.1016/S0021-9258(18)63521-5

Murakami, 2003, Bacterial RNA polymerases: The wholo story, Curr. Opin. Struct. Biol., 13, 31, 10.1016/S0959-440X(02)00005-2

Zhang, 1999, Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution, Cell, 98, 811, 10.1016/S0092-8674(00)81515-9

Cramer, 2001, Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution, Science, 292, 1863, 10.1126/science.1059493

Gnatt, 2001, Structural basis of transcription: An RNA polymerase II elongation complex at 3.3 Å resolution, Science, 292, 1876, 10.1126/science.1059495

Lane, 2010, Molecular evolution of multisubunit RNA polymerases: Sequence analysis, J. Mol. Biol., 395, 671, 10.1016/j.jmb.2009.10.062

Gruber, 2003, Multiple sigma subunits and the partitioning of bacterial transcription space, Annu. Rev. Microbiol., 57, 441, 10.1146/annurev.micro.57.030502.090913

Campbell, 2002, Structure of the bacterial RNA polymerase promoter specificity sigma subunit, Mol. Cell, 9, 527, 10.1016/S1097-2765(02)00470-7

Keilty, 1987, Constitutive function of a positively regulated promoter reveals new sequences essential for activity, J. Biol. Chem., 262, 6389, 10.1016/S0021-9258(18)45582-2

Schwartz, 2008, A full-length group 1 bacterial sigma factor adopts a compact structure incompatible with DNA binding, Chem. Biol., 15, 1091, 10.1016/j.chembiol.2008.09.008

Dombroski, 1993, Amino-terminal amino acids modulate sigma-factor DNA-binding activity, Genes Dev., 7, 2446, 10.1101/gad.7.12a.2446

Wilson, 1997, Region 1 of σ70 is required for efficient isomerization and initiation of transcription by Escherichia coli RNA polymerase, J. Mol. Biol., 267, 60, 10.1006/jmbi.1997.0875

Darst, 2001, Bacterial RNA polymerase, Curr. Opin. Struct. Biol., 11, 155, 10.1016/S0959-440X(00)00185-8

Chakraborty, 2012, Opening and closing of the bacterial RNA polymerase clamp, Science, 337, 591, 10.1126/science.1218716

Weixlbaumer, 2013, Structural basis of transcriptional pausing in bacteria, Cell, 152, 431, 10.1016/j.cell.2012.12.020

Tagami, 2010, Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein, Nature, 468, 978, 10.1038/nature09573

Ross, 2013, The magic spot: A ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation, Mol. Cell, 50, 420, 10.1016/j.molcel.2013.03.021

Zuo, 2013, The mechanism of E. coli RNA polymerase regulation by ppGpp is suggested by the structure of their complex, Mol. Cell, 50, 430, 10.1016/j.molcel.2013.03.020

Belogurov, 2009, Transcription inactivation through local refolding of the RNA polymerase structure, Nature, 457, 332, 10.1038/nature07510

Ho, 2009, Structures of RNA polymerase-antibiotic complexes, Curr. Opin. Struct. Biol., 19, 715, 10.1016/j.sbi.2009.10.010

Tupin, 2010, The transcription inhibitor lipiarmycin blocks DNA fitting into the RNA polymerase catalytic site, EMBO J., 29, 2527, 10.1038/emboj.2010.135

Chen, 2010, Promoter melting triggered by bacterial RNA polymerase occurs in three steps, Proc. Natl. Acad. Sci. USA, 107, 12523, 10.1073/pnas.1003533107

Cowing, 1989, Intermediates in the formation of the open complex by RNA polymerase holoenzyme containing the sigma factor σ32 at the groE promoter, J. Mol. Biol., 210, 521, 10.1016/0022-2836(89)90128-9

Craig, 1998, DNA footprints of the two kinetically significant intermediates in formation of an RNA polymerase-promoter open complex: Evidence that interactions with start site and downstream DNA induce sequential conformational changes in polymerase and DNA, J. Mol. Biol., 283, 741, 10.1006/jmbi.1998.2129

Saecker, 2002, Kinetic studies and structural models of the association of E. coli σ70 RNA polymerase with the λPR promoter: Large scale conformational changes in forming the kinetically significant intermediates, J. Mol. Biol., 319, 649, 10.1016/S0022-2836(02)00293-0

McClure, 1985, Mechanism and control of transcription initiation in prokaryotes, Annu. Rev. Biochem., 54, 171, 10.1146/annurev.bi.54.070185.001131

Neidhardt, F.C. (1996). Escherichia coli and Salmonella Cellular and Molecular Biology, ASM Press.

Kontur, 2010, Probing DNA binding, DNA opening, and assembly of a downstream clamp/jaw in Escherichia coli RNA polymerase-λPR promoter complexes using salt and the physiological anion glutamate, Biochemistry, 49, 4361, 10.1021/bi100092a

Kontur, 2006, Solute probes of conformational changes in open complex (RPo) formation by Escherichia coli RNA polymerase at the λPR promoter: Evidence for unmasking of the active site in the isomerization step and for large-scale coupled folding in the subsequent conversion to RPo, Biochemistry, 45, 2161, 10.1021/bi051835v

Roe, 1984, Kinetics and mechanism of the interaction of Escherichia coli RNA polymerase with the λPR promoter, J. Mol. Biol., 176, 495, 10.1016/0022-2836(84)90174-8

Roe, 1985, Temperature dependence of the rate constants of the Escherichia coli RNA polymerase-λPR promoter interaction. Assignment of the kinetic steps corresponding to protein conformational change and DNA opening, J. Mol. Biol., 184, 441, 10.1016/0022-2836(85)90293-1

Losick, R., and Chamberlin, M.J. (1976). RNA Polymerase, Cold Spring Harbor Laboratory.

Gourse, 2000, UPs and downs in bacterial transcription initiation: The role of the alpha subunit of RNA polymerase in promoter recognition, Mol. Microbiol., 37, 687, 10.1046/j.1365-2958.2000.01972.x

Ross, 1993, A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase, Science, 262, 1407, 10.1126/science.8248780

Estrem, 1998, Identification of an UP element consensus sequence for bacterial promoters, Proc. Natl. Acad. Sci. USA, 95, 9761, 10.1073/pnas.95.17.9761

Rao, 1994, Factor independent activation of rrnB P1. An “extended” promoter with an upstream element that dramatically increases promoter strength, J. Mol. Biol., 235, 1421, 10.1006/jmbi.1994.1098

Estrem, 1999, Bacterial promoter architecture: Subsite structure of UP elements and interactions with the carboxy-terminal domain of the RNA polymerase alpha subunit, Genes Dev., 13, 2134, 10.1101/gad.13.16.2134

Gaal, 1994, Localization of the intrinsically bent DNA region upstream of the E.coli rrnB P1 promoter, Nucleic Acids Res., 22, 2344, 10.1093/nar/22.12.2344

Koo, 1986, DNA bending at adenine · thymine tracts, Nature, 320, 501, 10.1038/320501a0

Davis, 2005, The effects of upstream DNA on open complex formation by Escherichia coli RNA polymerase, Proc. Natl. Acad. Sci. USA, 102, 285, 10.1073/pnas.0405779102

Mangiarotti, 2009, Sequence-dependent upstream DNA-RNA polymerase interactions in the open complex with λPR and λPRM promoters and implications for the mechanism of promoter interference, J. Mol. Biol., 385, 748, 10.1016/j.jmb.2008.11.019

Zuo, 2015, Crystal structures of the E. coli transcription initiation complexes with a complete bubble, Mol. Cell, 58, 534, 10.1016/j.molcel.2015.03.010

Ross, 2005, Sequence-independent upstream DNA-alphaCTD interactions strongly stimulate Escherichia coli RNA polymerase-lacUV5 promoter association, Proc. Natl. Acad. Sci. USA, 102, 291, 10.1073/pnas.0405814102

Hawley, 1983, Compilation and analysis of Escherichia coli promoter DNA sequences, Nucleic Acids Res., 11, 2237, 10.1093/nar/11.8.2237

Lisser, 1993, Compilation of E. coli mRNA promoter sequences, Nucleic Acids Res., 21, 1507, 10.1093/nar/21.7.1507

Ross, 2003, An intersubunit contact stimulating transcription initiation by E coli RNA polymerase: Interaction of the alpha C-terminal domain and sigma region 4, Genes Dev., 17, 1293, 10.1101/gad.1079403

Dove, 2000, Mechanism for a transcriptional activator that works at the isomerization step, Proc. Natl. Acad. Sci. USA, 97, 13215, 10.1073/pnas.97.24.13215

Chen, 2003, Functional interaction between RNA polymerase alpha subunit C-terminal domain and σ70 in UP-element- and activator-dependent transcription, Mol. Cell, 11, 1621, 10.1016/S1097-2765(03)00201-6

Dove, 2003, Region 4 of sigma as a target for transcription regulation, Mol. Microbiol., 48, 863, 10.1046/j.1365-2958.2003.03467.x

Niu, 1996, Transcription activation at class II CAP-dependent promoters: Two interactions between CAP and RNA polymerase, Cell, 87, 1123, 10.1016/S0092-8674(00)81806-1

Nickels, 2006, RNA-mediated destabilization of the σ70 region 4/β flap interaction facilitates engagement of RNA polymerase by the Q antiterminator, Mol. Cell, 24, 457, 10.1016/j.molcel.2006.09.014

Mitchell, 2003, Identification and analysis of ‘extended-10’ promoters in Escherichia coli, Nucleic Acids Res., 31, 4689, 10.1093/nar/gkg694

Shimada, 2014, The whole set of constitutive promoters recognized by RNA polymerase RpoD holoenzyme of Escherichia coli, PLoS ONE, 9, e90447, 10.1371/journal.pone.0090447

Aoyama, 1983, Essential structure of E. coli promoter: Effect of spacer length between the two consensus sequences on promoter function, Nucleic Acids Res., 11, 5855, 10.1093/nar/11.17.5855

Mulligan, 1985, Characterization in vitro of the effect of spacer length on the activity of Escherichia coli RNA polymerase at the TAC promoter, J. Biol. Chem., 260, 3529, 10.1016/S0021-9258(19)83654-2

Stefano, 1982, Spacer mutations in the lac ps promoter, Proc. Natl. Acad. Sci. USA, 79, 1069, 10.1073/pnas.79.4.1069

Hinton, 2009, The promoter spacer influences transcription initiation via σ70 region 1.1 of Escherichia coli RNA polymerase, Proc. Natl. Acad. Sci. USA, 106, 737, 10.1073/pnas.0808133106

Yuzenkova, 2011, A new basal promoter element recognized by RNA polymerase core enzyme, EMBO J., 30, 3766, 10.1038/emboj.2011.252

Barne, 1997, Region 2.5 of the Escherichia coli RNA polymerase σ70 subunit is responsible for the recognition of the ‘extended-10’ motif at promoters, EMBO J., 16, 4034, 10.1093/emboj/16.13.4034

Haugen, 2006, rRNA promoter regulation by nonoptimal binding of sigma region 1.2: An additional recognition element for RNA polymerase, Cell, 125, 1069, 10.1016/j.cell.2006.04.034

Guo, 2000, Promoter opening by σ54 and σ70 RNA polymerases: σ factor-directed alterations in the mechanism and tightness of control, Genes Dev., 14, 2242, 10.1101/gad.794800

Waldburger, 1990, Changes in conserved region 2 of Escherichia coli σ70 affecting promoter recognition, J. Mol. Biol., 215, 267, 10.1016/S0022-2836(05)80345-6

Marr, 1997, Promoter recognition as measured by binding of polymerase to nontemplate strand oligonucleotide, Science, 276, 1258, 10.1126/science.276.5316.1258

Roberts, 1996, Base-specific recognition of the nontemplate strand of promoter DNA by E. coli RNA polymerase, Cell, 86, 495, 10.1016/S0092-8674(00)80122-1

Cook, 2007, Strand opening-deficient Escherichia coli RNA polymerase facilitates investigation of closed complexes with promoter DNA: Effects of DNA sequence and temperature, J. Biol. Chem., 282, 21319, 10.1074/jbc.M702232200

Shultzaberger, 2007, Anatomy of Escherichia coli σ70 promoters, Nucleic Acids Res., 35, 771, 10.1093/nar/gkl956

Campagne, 2014, Structural basis for –10 promoter element melting by environmentally induced sigma factors, Nat. Struct. Mol. Biol., 21, 269, 10.1038/nsmb.2777

Haugen, 2008, Fine structure of the promoter-sigma region 1.2 interaction, Proc. Natl. Acad. Sci. USA, 105, 3292, 10.1073/pnas.0709513105

Jeong, 1994, Start site selection at lacUV5 promoter affected by the sequence context around the initiation sites, Nucleic Acids Res., 22, 4667, 10.1093/nar/22.22.4667

Lewis, 2004, Axiom of determining transcription start points by RNA polymerase in Escherichia coli, Mol. Microbiol., 54, 692, 10.1111/j.1365-2958.2004.04318.x

Liu, 1994, Effects of transcriptional start site sequence and position on nucleotide-sensitive selection of alternative start sites at the pyrC promoter in Escherichia coli, J. Bacteriol., 176, 2938, 10.1128/jb.176.10.2938-2945.1994

1989, Escherichia coli promoters. I. Consensus as it relates to spacing class, specificity, repeat substructure, and three-dimensional organization, J. Biol. Chem., 264, 5522

Thomason, 2015, Global transcriptional start site mapping using differential RNA sequencing reveals novel antisense RNAs in Escherichia coli, J. Bacteriol., 197, 18, 10.1128/JB.02096-14

Feklistov, 2006, A basal promoter element recognized by free RNA polymerase sigma subunit determines promoter recognition by RNA polymerase holoenzyme, Mol. Cell, 23, 97, 10.1016/j.molcel.2006.06.010

Travers, 1980, Promoter sequence for stringent control of bacterial ribonucleic acid synthesis, J. Bacteriol., 141, 973, 10.1128/jb.141.2.973-976.1980

Guerin, 1996, High resolution mapping of E.coli transcription elongation complex in situ reveals protein interactions with the non-transcribed strand, EMBO J., 15, 5397, 10.1002/j.1460-2075.1996.tb00923.x

Vvedenskaya, 2014, Transcription. Interactions between RNA polymerase and the “core recognition element” counteract pausing, Science, 344, 1285, 10.1126/science.1253458

Gaal, 1997, Transcription regulation by initiating NTP concentration: RRNA synthesis in bacteria, Science, 278, 2092, 10.1126/science.278.5346.2092

Guthold, 1999, Direct observation of one-dimensional diffusion and transcription by Escherichia coli RNA polymerase, Biophys. J., 77, 2284, 10.1016/S0006-3495(99)77067-0

Harada, 1999, Single-molecule imaging of RNA polymerase-DNA interactions in real time, Biophys. J., 76, 709, 10.1016/S0006-3495(99)77237-1

Kabata, 1993, Visualization of single molecules of RNA polymerase sliding along DNA, Science, 262, 1561, 10.1126/science.8248804

Ricchetti, 1988, One-dimensional diffusion of Escherichia coli DNA-dependent RNA polymerase: A mechanism to facilitate promoter location, Proc. Natl. Acad. Sci. USA, 85, 4610, 10.1073/pnas.85.13.4610

Singer, 1987, Promoter search by Escherichia coli RNA polymerase on a circular DNA template, J. Biol. Chem., 262, 14178, 10.1016/S0021-9258(18)47921-5

Friedman, 2013, RNA polymerase approaches its promoter without long-range sliding along DNA, Proc. Natl. Acad. Sci. USA, 110, 9740, 10.1073/pnas.1300221110

Wang, 2013, The promoter-search mechanism of Escherichia coli RNA polymerase is dominated by three-dimensional diffusion, Nat. Struct. Mol. Biol., 20, 174, 10.1038/nsmb.2472

Bakshi, 2013, Partitioning of RNA polymerase activity in live Escherichia coli from analysis of single-molecule diffusive trajectories, Biophys. J., 105, 2676, 10.1016/j.bpj.2013.10.024

deHaseth, 1978, Nonspecific interactions of Escherichia coli RNA polymerase with native and denatured DNA: Differences in the binding behavior of core and holoenzyme, Biochemistry, 17, 1612, 10.1021/bi00602a006

Hofer, 1985, The pathway of E. coli RNA polymerase-promoter complex formation as visualized by footprinting, Nucleic Acids Res., 13, 5995, 10.1093/nar/13.16.5995

Kovacic, 1987, The 0 degree C closed complexes between Escherichia coli RNA polymerase and two promoters, T7-A3 and lacUV5, J. Biol. Chem., 262, 13654, 10.1016/S0021-9258(19)76477-1

Mecsas, 1991, Development of RNA polymerase-promoter contacts during open complex formation, J. Mol. Biol., 220, 585, 10.1016/0022-2836(91)90102-C

Schickor, 1990, Topography of intermediates in transcription initiation of E. coli, EMBO J., 9, 2215, 10.1002/j.1460-2075.1990.tb07391.x

Spassky, 1985, Changes in the DNA structure of the lac UV5 promoter during formation of an open complex with Escherichia coli RNA polymerase, Biochemistry, 24, 2723, 10.1021/bi00332a019

Ruff, E.F., Zorn, K., Capp, M.W., Artsimovitch, I., and Record, M.T. (2015). Effects of upstream Escherichia coli RNA polymerase-DNA interactions on open complex formation, Unpublished work.

Naryshkin, 2000, Structural organization of the RNA polymerase-promoter open complex, Cell, 101, 601, 10.1016/S0092-8674(00)80872-7

Bartlett, 1998, RNA polymerase mutants that destabilize RNA polymerase-promoter complexes alter NTP-sensing by rrn P1 promoters, J. Mol. Biol., 279, 331, 10.1006/jmbi.1998.1779

Rutherford, 2009, Allosteric control of Escherichia coli rRNA promoter complexes by DksA, Genes Dev., 23, 236, 10.1101/gad.1745409

Li, 1998, Characterization of the closed complex intermediate formed during transcription initiation by Escherichia coli RNA polymerase, J. Biol. Chem., 273, 23549, 10.1074/jbc.273.36.23549

Browning, 2004, The regulation of bacterial transcription initiation, Nat. Rev. Microbiol., 2, 57, 10.1038/nrmicro787

Drennan, 2012, Key roles of the downstream mobile jaw of Escherichia coli RNA polymerase in transcription initiation, Biochemistry, 51, 9447, 10.1021/bi301260u

Mekler, 2011, Molecular mechanism of transcription inhibition by phage T7 Gp2 protein, J. Mol. Biol., 413, 1016, 10.1016/j.jmb.2011.09.029

Artsimovitch, 2003, Co-overexpression of Escherichia coli RNA polymerase subunits allows isolation and analysis of mutant enzymes lacking lineage-specific sequence insertions, J. Biol. Chem., 278, 12344, 10.1074/jbc.M211214200

Hawley, D.K., Malan, T.P., Mulligan, M.E., and McClure, W.R. (1982). Promoters: Structure and Function, Praeger.

McClure, 1980, Rate-limiting steps in RNA chain initiation, Proc. Natl. Acad. Sci. USA, 77, 5634, 10.1073/pnas.77.10.5634

Tsodikov, 1999, General method of analysis of kinetic equations for multistep reversible mechanisms in the single-exponential regime: Application to kinetics of open complex formation between Eσ70 RNA polymerase and λPR promoter DNA, Biophys. J., 76, 1320, 10.1016/S0006-3495(99)77294-2

Drennan, A.C. (2012). Key conformational changes of Escherichia coli RNA polymerase and promoter DNA in transcription initiation. [Ph.D. Thesis, University of Wisconsin].

Heitkamp, S.E. (2012). Real-Time characterization of transcription initiation intermediates for E. coli RNA polymerase using fast footprinting and equilibrium and stopped-flow fluorescence. [Ph.D. Thesis, University of Wisconsin].

Hinton, 2007, Transcription initiation by mix and match elements: Flexibility for polymerase binding to bacterial promoters, Gene Regul. Syst. Biol., 1, 275