Cooperativity and interaction energy threshold effects in recognition of the -10 promoter element by bacterial RNA polymerase

Nucleic Acids Research

Volumn 41, Issue 15, 2013, Pages 7276-7285

  Mekler, Vladimir ^a   Severinov, Konstantin ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; BACTERIAL ENZYME; DOUBLE STRANDED DNA; NUCLEOTIDE; RNA POLYMERASE; THYMINE;

AMINO TERMINAL SEQUENCE; ARTICLE; BASE PAIRING; COMPLEX FORMATION; ENERGY COST; ENZYME CONFORMATION; INHIBITION KINETICS; MOLECULAR BEACON; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; SUBSTITUTION REACTION; UPREGULATION;

BACTERIAL PROTEINS; BASE PAIRING; CONSENSUS SEQUENCE; DNA, BACTERIAL; DNA, INTERGENIC; DNA-DIRECTED RNA POLYMERASES; ENERGY TRANSFER; ESCHERICHIA COLI; HOLOENZYMES; MULTIPROTEIN COMPLEXES; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TRANSCRIPTION, GENETIC;

EID: 84883473606     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt541     Document Type: Article

References (44)

1. Murakami,K.S. and Darst,S.A. (2003) Bacterial RNA polymerases: the wholo story. Curr. Opin. Struct. Biol., 13, 31-39
2. Saecker,R.M., Record,M.T. Jr and Dehaseth,P.L. (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, 754-771
3. Marr,M.T. and Roberts,J.W. (1997) Promoter recognition as measured by binding of polymerase to nontemplate strand oligonucleotide. Science, 276, 1258-1260
4. Guo,J. and Gralla,J.D. (1998) Promoter opening via a DNA fork junction binding activity. Proc. Natl Acad. Sci. USA, 95, 11655-11660
5. Matlock,D.L. and Heyduk,T. (2000) Sequence determinants for the recognition of the fork junction DNA containing the -10 region of promoter DNA by E coli RNA polymerase. Biochemistry, 39, 12274-12283
6. Mekler,V., Pavlova,O. and Severinov,K. (2011) The interaction of Escherichia coli RNA polymerase s70 subunit with promoter elements in the context of free s70, RNA polymerase holoenzyme, and the b0-s70 complex. J. Biol. Chem., 286, 270-279
7. Young,B.A., Gruber,T.M. and Gross,C.A. (2004) Minimal machinery of RNA polymerase holoenzyme sufficient for promoter melting. Science, 303, 1382-1384
8. Hook-Barnard,I.G. and Hinton,D.M. (2007) Transcription initiation by mix and match elements: flexibility for polymerase binding to bacterial promoters. Gene Regul. Syst. Biol., 1, 275-293
9. Murakami,K.S., Masuda,S., Campbell,E.A., Muzzin,O. and Darst,S.A. (2002) Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science, 296, 1285-1290
10. Kirkegaard,K., Buc,H., Spassky,A. and Wang,J. (1983) Mapping of single-stranded regions in duplex DNA at the sequence level: single-strand-specific cytosine methylation in RNA polymerasepromoter complexes. Proc. Natl Acad. Sci. USA, 80, 2544-2548
11. Rogozina,A., Zaychikov,E., Buckle,M., Heumann,H. and Sclavi,B. (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, 5390-5404
12. Sclavi,B. ( 2009) Opening the DNA at the promoter; the energetic challange. In: Buc,H. and Strick,T. (eds), RNA Polymerases as Molecular Motors. RSC Publishing, Cambridge, UK, pp
13. Zaychikov,E., Denissova,L., Meier,T., Gotte,M. and Heumann,H. (1997) Influence of Mg2+and temperature on formation of the transcription bubble. J. Biol. Chem., 272, 2259-2267
14. Auner,H., Buckle,M., Deufel,A., Kutateladze,T., Lazarus,L., Mavathur,R., Muskhelishvili,G., Pemberton,I., Schneider,R. and Travers,A. (2003) Mechanism of transcriptional activation by FIS: role of core promoter structure and DNA topology. J. Mol. Biol., 331, 331-344
15. Severinov,K. and Darst,S.A. (1997) A mutant RNA polymerase that forms unusual open promoter complexes. Proc. Natl Acad. Sci. USA, 94, 13481-13486
16. Brodolin,K., Zenkin,N. and Severinov,K. (2005) Remodeling of the sigma70 subunit non-template DNA strand contacts during the final step of transcription initiation. J. Mol. Biol., 350, 930-937
17. Tomsic,M., Tsujikawa,L., Panaghie,G., Wang,Y., Azok,J. and deHaseth,P.L. (2001) Different roles for basic and aromatic amino acids in conserved region 2 of Escherichia coli sigma(70) in the nucleation and maintenance of the single-stranded DNA bubble in open RNA polymerase-promoter complexes. J. Biol. Chem., 276, 31891-31896
18. Feklistov,A. and Darst,S.A. (2011) Structural basis for promoter-10 element recognition by the bacterial RNA polymerase s subunit. Cell, 147, 1257-1269
19. Zhang,Y., Feng,Y., Chatterjee,S., Tuske,S., Ho,M.X., Arnold,E. and Ebright,R.H. (2012) Structural basis of transcription initiation. Science, 338, 1076-1080
20. Grana,D., Gardella,T. and Susskind,M.M. (1988) The effects of mutations in the ant promoter of phage P22 depend on context. Genetics, 120, 319-327
21. Mekler,V., Minakhin,L., Kuznedelov,K., Mukhamedyarov,D. and Severinov,K. (2012) RNA polymerase-promoter interactions determining different stability of the Escherichia coli and Thermus aquaticus transcription initiation complexes. Nucleic Acids Res., 40, 11352-11362
22. Del Peso-Santos,T., BernardoL,M.D., Skarfstad,E., Holmfeldt,L., Togneri,P. and Shingler,V. (2011) A hyper-mutant of the unusual s70-Pr promoter bypasses synergistic ppGpp/DksA co-stimulation. Nucleic Acids Res., 39, 5853-5865
23. Shultzaberger,R.K., Chen,Z., Lewis,K.A. and Schneider,T.D. (2007) Anatomy of Escherichia coli sigma70 promoters. Nucleic Acids Res., 35, 771-788
24. Moyle,H., Waldburger,C. and Susskind,M.M. (1991) Hierarchies of base pair preferences in the P22 ant promoter. J. Bacteriol., 173, 1944-1950
25. Roberts,C.W. and Roberts,J.W. (1996) Base-specific recognition of the nontemplate strand of promoter DNA by E coli RNA polymerase. Cell, 86, 495-501
26. Motulsky,H.J. and Mahan,L.C. (1984) The kinetics of competitive radioligand binding predicted by the law of mass action. Mol. Pharmacol., 25, 1-9
27. Haugen,S.P., Berkmen,M.B., Ross,W., Gaal,T., Ward,C. and Gourse,R.L. (2006) rRNA promoter regulation by nonoptimal binding of sigma region 1.2: an additional recognition element for RNA polymerase. Cell, 16, 1069-1082
28. Feklistov,V., Barinova,N., Sevostyanova,A., Heyduk,E., Bass,I., Vvedenskaya,I., Kuznedelov,K., Merkiene,E., Stavrovskaya,E., Klimasauskas,S. et al. (2006) A basal promoter element recognized by free RNA polymerase sigma subunit determines promoter recognition by RNA polymerase holoenzyme. Mol. Cell, 23, 97-107
29. Fenton,M.S. and Gralla,J.D. (2003) Effect of DNA bases and backbone on sigma70 holoenzyme binding and isomerization using fork junction probes. Nucleic Acids Res., 31, 2745-2750
30. Kool,E.T. (2001) Hydrogen bonding, base stacking, and steric effects in DNA replication. Annu. Rev. Biophys. Biomol. Struct., 30, 1-22
31. Del Peso-Santos,T., Landfors,M., Ska rfstad,E., Ryden,P. and Shingler,V. (2012) Pr is a member of a restricted class of s70-dependent promoters that lack a recognizable -10 element. Nucleic Acids Res., 40, 11308-11320
32. Fenton,M.S. and Gralla,J.D. (2001) Function of the bacterial TAT AAT -10 element as single-stranded DNA during RNA polymerase isomerization. Proc. Natl Acad. Sci. USA, 98, 9020-9025
33. Jose,D., Datta,K., Johnson,N.P. and von Hippel,P.H. (2009) Spectroscopic studies of position-specific DNA breathing fluctuations at replication forks and primer-template junctions. Proc. Natl Acad. Sci. USA, 106, 4231-4236
34. Estrem,S.T., Ross,W., Gaal,T., Chen,Z.W., Niu,W., Ebright,R.H. and Gourse,R.L. (1999) Bacterial promoter architecture: subsite structure of UP elements and interactions with the carboxyterminal domain of the RNA polymerase alpha subunit. Genes Dev., 13, 2134-2147
35. Crouch,T.H. and Klee,C.B. (1980) Positive cooperative binding of calcium to bovine brain calmodulin. Biochemistry, 19, 3692-3698
36. Geisel,N. and Gerland,U. (2011) Physical limits on cooperative protein-DNA binding and the kinetics of combinatorial transcription regulation. Biophys. J., 101, 1569-1579
37. Lim,H.M., Lee,H.J., Roy,S. and Adhya,S. (2001) A master in base unpairing during isomerization of a promoter upon RNA polymerase binding. Proc. Natl Acad. Sci. USA, 98, 14849-14852
38. Heyduk,E., Kuznedelov,K., Severinov,K. and Heyduk,T. (2006) A consensus adenine at position -11 of the nontemplate strand of bacterial promoter is important for nucleation of promoter melting. J. Biol. Chem., 281, 12362-12369
39. Chen,J., Darst,S.A. and Thirumalai,D. (2010) Promoter melting triggered by bacterial RNA polymerase occurs in three steps. Proc. Natl Acad. Sci. USA, 107, 12523-12528
40. SantaLucia,J. Jr and Hicks,D. (2004) The thermodynamics of DNA structural motifs. Annu. Rev. Biophys. Biomol. Struct., 33, 415-440
41. Krueger,A., Protozanova,E. and Frank-Kamenetskii,M.D. (2006) Sequence-dependent base pair opening in DNA double helix. Biophys. J., 90, 3091-3099
42. Stivers,J.T. (2008) Extrahelical damaged base recognition by DNA glycosylase enzymes. Chemistry, 14, 786-793
43. Choi,C.H., Kalosakas,G., Rasmussen,K.O., Hiromura,M., Bishop,A.R. and Usheva,A. (2004) DNA dynamically directs its own transcription initiation. Nucleic Acids Res., 32, 1584-1590
44. Altan-Bonnet,G., Libchaber,A. and Krichevsky,O. (2003) Bubble dynamics in double-stranded DNA. Phys. Rev. Lett., 90, 138101