Coupling of downstream RNA polymerase-promoter interactions with formation of catalytically competent transcription initiation complex

Journal of Molecular Biology

Volumn 426, Issue 24, 2014, Pages 3973-3984

  Mekler, Vladimir ^a   Minakhin, Leonid ^a   Borukhov, Sergei ^b   Mustaev, Arkady ^c   Severinov, Konstantin ^a,d,e  

^a RUTGERS UNIVERSITY   (United States)

^b UMDNJ School of Osteopathic Medicine   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d RUTGERS UNIVERSITY   (United States)

^e RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

Author keywords

DNA protein interactions; fluorescence spectroscopy; stringent response; transcription initiation; transcription regulation

Indexed keywords

BACTERIAL RNA; DNA FRAGMENT; DOUBLE STRANDED DNA; FLUORESCENT DYE; HOLOENZYME; RNA POLYMERASE; BACTERIAL DNA; DKSA PROTEIN, E COLI; DNA DIRECTED RNA POLYMERASE; ESCHERICHIA COLI PROTEIN; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; PROTEIN BINDING; RNA POLYMERASE SIGMA 70; SIGMA FACTOR;

ARTICLE; BACTERIOPHAGE T5; COMPLEX FORMATION; DNA BASE COMPOSITION; DNA DENATURATION; DNA PROBE; DNA TEMPLATE; ENZYME ACTIVITY; ENZYME BINDING; ESCHERICHIA COLI; GENE INTERACTION; NONHUMAN; PROMOTER REGION; PROTEIN DNA INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; BIOCATALYSIS; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE;

BIOCATALYSIS; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GUANOSINE TETRAPHOSPHATE; MODELS, GENETIC; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SIGMA FACTOR; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION INITIATION, GENETIC;

EID: 84914683079     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.10.005     Document Type: Article

References (52)

1. T.M. Gruber, and C.A. Gross Multiple sigma subunits and the partitioning of bacterial transcription space Annu Rev Microbiol 57 2003 441 466
2. R.M. Saecker, M.T. Record, and P.L. Dehaseth Mechanism of bacterial transcription initiation: RNA polymerase-promoter binding, isomerization to initiation-competent open complexes, and initiation of RNA synthesis J Mol Biol 412 2011 754 771
3. M.T. Marr, and J.W. Roberts Promoter recognition as measured by binding of polymerase to nontemplate strand oligonucleotide Science 276 1997 1258 1260
4. S.P. Haugen, M.B. Berkmen, W. Ross, T. Gaal, C. Ward, and R.L. Gourse rRNA promoter regulation by nonoptimal binding of sigma region 1.2: an additional recognition element for RNA polymerase Cell 16 2006 1069 1082
5. 70 complex J Biol Chem 286 2011 270 279
6. J. Guo, and J.D. Gralla Promoter opening via a DNA fork junction binding activity Proc Natl Acad Sci USA 95 1998 11655 11660
7. V. Mekler, and K. Severinov Cooperativity and interaction energy threshold effects in recognition of the - 10 promoter element by bacterial RNA polymerase Nucleic Acids Res 41 2013 7276 7285
8. R.M. Saecker, O.V. Tsodikov, K.L. McQuade, P.E. Schlax, M.W. Capp, and M.T. Record Kinetic studies and structural models of the association of E. coli σ70 RNA polymerase with the lambdaP(R) promoter: large scale conformational changes in forming the kinetically significant intermediates J Mol Biol 319 2002 649 671
9. V. Mekler, L. Minakhin, and K. Severinov A critical role of downstream RNA polymerase-promoter interactions in the formation of initiation complex J Biol Chem 286 2011 22600 22608
10. E. Nudler, E. Avetissova, V. Markovtsov, and A. Goldfarb Transcription processivity: protein-DNA interactions holding together the elongation complex Science 273 1996 211 217
11. J. Ederth, I. Artsimovitch, L.A. Isaksson, and R. Landick The downstream DNA jaw of bacterial RNA polymerase facilitates both transcriptional initiation and pausing J Biol Chem 277 2002 37456 37463
12. V. Mekler, L. Minakhin, C. Sheppard, S. Wigneshweraraj, and K. Severinov Molecular mechanism of transcription inhibition by phage T7 gp2 protein J Mol Biol 413 2011 1016 1027
13. B. Camara, M. Liu, J. Reynolds, A. Shadrin, B. Liu, and K. Kwok 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 USA 107 2010 2247 2252
14. J. Mukhopadhyay, K. Das, S. Ismail, D. Koppstein, M. Jang, and B. Hudson The RNA polymerase "switch region" is a target for inhibitors Cell 135 2008 295 307
15. M.M. Babu, and S.A. Teichmann Functional determinants of transcription factors in Escherichia coli: protein families and binding sites Trends Genet 19 2003 75 79
16. S.T. Rutherford, C.L. Villers, J.H. Lee, W. Ross, and R.L. Gourse Allosteric control of Escherichia coli rRNA promoter complexes by DksA Genes Dev 23 2009 236 248
17. A.L. Gnatt, P. Cramer, J. Fu, D.A. Bushnell, and R.D. Kornberg Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 Å resolution Science 292 2001 1876 1882
18. D.G. Vassylyev, M.N. Vassylyeva, A. Perederina, T.H. Tahirov, and I. Artsimovitch Structural basis for transcription elongation by bacterial RNA polymerase Nature 448 2007 157 162
19. Y. Zhang, Y. Feng, S. Chatterjee, S. Tuske, M.X. Ho, and E. Arnold Structural basis of transcription initiation Science 338 2012 1076 1080
20. S.A. Darst, N. Opalka, P. Chacon, A. Polyakov, C. Richter, and G. Zhang Conformational flexibility of bacterial RNA polymerase Proc Natl Acad Sci USA 99 2002 4296 4301
21. R. Landick RNA polymerase clamps down Cell 105 2001 567 570
22. P. Cramer, D.A. Bushnell, and R.D. Kornberg Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution Science 292 2001 1863 1876
23. S. Tagami, S. Sekine, T. Kumarevel, N. Hino, Y. Murayama, and S. Kamegamori Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein Nature 468 2010 978 982
24. A. Chakraborty, D. Wang, Y.W. Ebright, Y. Korlann, E. Kortkhonjia, and T. Kim Opening and closing of the bacterial RNA polymerase clamp Science 337 2012 591 595
25. A. Weixlbaumer, K. Leon, R. Landick, and S.A. Darst Structural basis of transcriptional pausing in bacteria Cell 152 2013 431 441
26. V. Mekler, L. Minakhin, K. Kuznedelov, D. Mukhamedyarov, and K. Severinov RNA polymerase-promoter interactions determining different stability of the Escherichia coli and Thermus aquaticus transcription initiation complexes Nucleic Acids Res 40 2012 11352 11362
27. V. Mekler, E. Kortkhonjia, J. Mukhopadhyay, J. Knight, A. Revyakin, and A.N. Kapanidis Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex Cell 108 2002 599 614
28. I.G. Hook-Barnard, and D.M. Hinton The promoter spacer influences transcription initiation via sigma70 region 1.1 of Escherichia coli RNA polymerase Proc Natl Acad Sci USA 106 2009 737 742
29. S. Vuthoori, C.W. Bowers, A. McCracken, A.J. Dombroski, and D.M. Hinton Domain 1.1 of the sigma(70) subunit of Escherichia coli RNA polymerase modulates the formation of stable polymerase/promoter complexes J Mol Biol 309 2001 561 572
30. E. James, M. Liu, C. Sheppard, V. Mekler, B. Camara, and B. Liu Structural and mechanistic basis for the inhibition of Escherichia coli RNA polymerase by T7 Gp2 Mol Cell 47 2012 755 766
31. B. Bae, E. Davis, D. Brown, E. Campbell, S. Wigneshweraraj, and S. Darst Phage T7 Gp2 inhibition of Escherichia coli RNA polymerase involves misappropriation of sigma70 domain 1.1 Proc Natl Acad Sci USA 110 2013 19772 19777
32. S. Borukhov, and E. Nudler RNA polymerase: the vehicle of transcription Trends Microbiol 16 2008 126 134
33. A. Mustaev, E. Zaychikov, K. Severinov, M. Kashlev, A. Polyakov, and V. Nikiforov Topology of the RNA polymerase active center probed by chimeric rifampicin-nucleotide compounds Proc Natl Acad Sci USA 91 1994 12036 12040
34. I.K. Pemberton, G. Muskhelishvili, A.A. Travers, and M. Buckle The G + C-rich discriminator of the tyrT promoter antagonises the formation of stable preinitiation complexes J Mol Biol 299 2000 859 864
35. S.P. Haugen, W. Ross, and R.L. Gourse Advances in bacterial promoter recognition and its control by factors that do not bind DNA Nat Rev Microbiol 6 2008 507 519
36. A. Perederina, V. Svetlov, M.N. Vassylyeva, T.H. Tahirov, S. Yokoyama, and I. Artsimovitch Regulation through the secondary channel - structural framework for ppGpp-DksA synergism during transcription Cell 118 2004 297 309
37. Y. Zuo, Y. Wang, and T.A. Steitz The mechanism of E. coli RNA polymerase regulation by ppGpp is suggested by the structure of their complex Mol Cell 50 2013 430 436
38. W. Ross, C.E. Vrentas, P. Sanchez-Vazquez, T. Gaal, and R.L. Gourse The magic spot: a ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation Mol Cell 50 2013 420 429
39. C.W. Lennon, W. Ross, S. Martin-Tumasz, I. Toulokhonov, C.E. Vrentas, and S.T. Rutherford Direct interactions between the coiled-coil tip of DksA and the trigger loop of RNA polymerase mediate transcriptional regulation Genes Dev 26 2012 2634 2646
40. B.J. Paul, M.M. Barker, W. Ross, D.A. Schneider, C. Webb, and J.W. Foster DksA: A critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP Cell 118 2004 311 322
41. J. Lee, C. Lennon, W. Ross, and R. Gourse Role of the coiled-coil tip of Escherichia coli DksA in promoter control J Mol Biol 416 2012 503 517
42. K. Brodolin Antibiotics trapping transcription initiation intermediates: to melt or to bend, what's first? Transcription 2 2011 60 65
43. K.S. Murakami The X-ray crystal structure of Escherichia coli RNA polymerase s70 holoenzyme J Biol Chem 288 2013 9126 9134
44. D. Pupov, N. Miropolskaya, A. Sevostyanova, I. Bass, I. Artsimovitch, and A. Kulbachinskiy Multiple roles of the RNA polymerase b′ SW2 region in transcription initiation, promoter escape, and RNA elongation Nucleic Acids Res 38 2010 5784 5796
45. S.C. Wiesler, P.C. Burrows, and M. Buck A dual switch controls bacterial enhancer-dependent transcription Nucleic Acids Res 40 2012 10878 10892
46. Q. Wang, T.D. Tullius, and J.R. Levin Effects of discontinuities in the DNA template on abortive initiation and promoter escape by Escherichia coli RNA polymerase J Biol Chem 282 2007 26917 26927
47. O. Schroder, E.P. Geiduschek, and G.A. Kassavetis A single-stranded promoter for RNA polymerase III Proc Natl Acad Sci USA 100 2003 934 939
48. R. Furman, O.V. Tsodikov, Y.I. Wolf, and I. Artsimovitch An insertion in the catalytic trigger loop gates the secondary channel of RNA polymerase J Mol Biol 425 2013 82 93
49. I. Artsimovitch, V. Svetlov, K.S. Murakami, and R. Landick Co-overexpression of Escherichia coli RNA polymerase subunits allows isolation and analysis of mutant enzymes lacking lineage-specific sequence insertions J Biol Chem 278 2003 12344 12355
50. A. Drennan, M. Kraemer, M. Capp, T. Gries, E. Ruff, and C. Sheppard Key roles of the downstream mobile jaw of Escherichia coli RNA polymerase in transcription initiation Biochemistry 51 2012 9447 9459
51. M. Kashlev, E. Nudler, K. Severinov, S. Borukhov, N. Komissarova, and A. Goldfarb Histidine-tagged RNA polymerase of Escherichia coli and transcription in solid phase Methods Enzymol 274 1996 326 334
52. J. Mukhopadhyay, V. Mekler, E. Kortkhonjia, A.N. Kapanidis, Y.W. Ebright, and R.H. Ebright Fluorescence resonance energy transfer (FRET) in analysis of transcription-complex structure and function Methods Enzymol 371 2003 144 159