1887

Abstract

Regulatory interactions at the lac promoter.

Activation of the transcription of genes is central to many processes of adaptation and differentiation in bacteria. Here, I review the molecular mechanisms by which transcription factors can activate the initiation of specific transcripts at bacterial promoters. The story is presented in the context of Marjory Stephenson’s pioneering work on enzymatic adaptation in bacteria, and sets the different mechanisms in the greater context of how transcription regulatory mechanisms evolved.

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2019-02-18
2019-12-09
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References

  1. Woods DD. Marjory Stephenson, 1885-1948. Biochem J 1950;46:562–577[PubMed]
    [Google Scholar]
  2. Ullmann A. Origins of Molecular Biology: A Tribute to Jacques Monod Herndon, VA, USA: ASM Press; 2004
    [Google Scholar]
  3. Santos-Zavaleta A, Sánchez-Pérez M, Salgado H, Velázquez-Ramírez DA, Gama-Castro S et al. A unified resource for transcriptional regulation in Escherichia coli K-12 incorporating high-throughput-generated binding data into RegulonDB version 10.0. BMC Biol 2018;16:91 [CrossRef][PubMed]
    [Google Scholar]
  4. Muller-Hill B. The Lac Operon Berlin: Walter de Gruyter & Co; 1996
    [Google Scholar]
  5. Kolb A, Busby S, Buc H, Garges S, Adhya S. Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 1993;62:749–797 [CrossRef][PubMed]
    [Google Scholar]
  6. Feklístov A, Sharon BD, Darst SA, Gross CA. Bacterial sigma factors: a historical, structural, and genomic perspective. Annu Rev Microbiol 2014;68:357–376 [CrossRef][PubMed]
    [Google Scholar]
  7. Feklistov A, Darst SA. Structural basis for promoter-10 element recognition by the bacterial RNA polymerase σ subunit. Cell 2011;147:1257–1269 [CrossRef][PubMed]
    [Google Scholar]
  8. Zhang Y, Feng Y, Chatterjee S, Tuske S, Ho MX et al. Structural basis of transcription initiation. Science 2012;338:1076–1080 [CrossRef][PubMed]
    [Google Scholar]
  9. Zuo Y, Steitz TA. Crystal structures of the E. coli transcription initiation complexes with a complete bubble. Mol Cell 2015;58:534–540 [CrossRef][PubMed]
    [Google Scholar]
  10. Rhodius VA, Busby SJ. Positive activation of gene expression. Curr Opin Microbiol 1998;1:152–159 [CrossRef][PubMed]
    [Google Scholar]
  11. de Crombrugghe B, Busby S, Buc H. Cyclic AMP receptor protein: role in transcription activation. Science 1984;224:831–838 [CrossRef][PubMed]
    [Google Scholar]
  12. Schultz SC, Shields GC, Steitz TA. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science 1991;253:1001–1007 [CrossRef][PubMed]
    [Google Scholar]
  13. Busby S, Ebright RH. Transcription activation by catabolite activator protein (CAP). J Mol Biol 1999;293:199–213 [CrossRef][PubMed]
    [Google Scholar]
  14. Benoff B, Yang H, Lawson CL, Parkinson G, Liu J et al. Structural basis of transcription activation: the CAP-alpha CTD-DNA complex. Science 2002;297:1562–1566 [CrossRef][PubMed]
    [Google Scholar]
  15. Lawson CL, Swigon D, Murakami KS, Darst SA, Berman HM et al. Catabolite activator protein: DNA binding and transcription activation. Curr Opin Struct Biol 2004;14:10–20 [CrossRef][PubMed]
    [Google Scholar]
  16. Liu B, Hong C, Huang RK, Yu Z, Steitz TA. Structural basis of bacterial transcription activation. Science 2017;358:947–951 [CrossRef][PubMed]
    [Google Scholar]
  17. Hudson BP, Quispe J, Lara-González S, Kim Y, Berman HM et al. Three-dimensional EM structure of an intact activator-dependent transcription initiation complex. Proc Natl Acad Sci USA 2009;106:19830–19835 [CrossRef][PubMed]
    [Google Scholar]
  18. Feng Y, Zhang Y, Ebright RH. Structural basis of transcription activation. Science 2016;352:1330–1333 [CrossRef][PubMed]
    [Google Scholar]
  19. Lee DJ, Minchin SD, Busby SJ. Activating transcription in bacteria. Annu Rev Microbiol 2012;66:125–152 [CrossRef][PubMed]
    [Google Scholar]
  20. Browning D, Lee D, Green J, Busby S. Secrets of bacterial transcription initiation taught by the Escherichia coli FNR protein. Signals, Switches, Regulons & Cascades: Control of Bacterial Gene Expressionvol. 61 SGM Symposium; 2002; pp.127–142
    [Google Scholar]
  21. Barnard A, Wolfe A, Busby S. Regulation at complex bacterial promoters: how bacteria use different promoter organizations to produce different regulatory outcomes. Curr Opin Microbiol 2004;7:102–108 [CrossRef][PubMed]
    [Google Scholar]
  22. H-C W, Tyson K, Cole J, Busby S. Regulation of the E. coli nir operon by two transcription factors: a new mechanism to account for co-dependence on two activators. Mol Microbiol 1998;27:493–505
    [Google Scholar]
  23. Browning DF, Cole JA, Busby SJ. Suppression of FNR-dependent transcription activation at the Escherichia coli nir promoter by Fis, IHF and H-NS: modulation of transcription initiation by a complex nucleo-protein assembly. Mol Microbiol 2000;37:1258–1269 [CrossRef][PubMed]
    [Google Scholar]
  24. Browning DF, Grainger DC, Busby SJ. Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 2010;13:773–780 [CrossRef][PubMed]
    [Google Scholar]
  25. Dillon SC, Dorman CJ. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 2010;8:185–195 [CrossRef][PubMed]
    [Google Scholar]
  26. Browning DF, Cole JA, Busby SJ. Transcription activation by remodelling of a nucleoprotein assembly: the role of NarL at the FNR-dependent Escherichia coli nir promoter. Mol Microbiol 2004;53:203–215 [CrossRef][PubMed]
    [Google Scholar]
  27. Browning DF, Cole JA, Busby SJ. Regulation by nucleoid-associated proteins at the Escherichia coli nir operon promoter. J Bacteriol 2008;190:7258–7267 [CrossRef][PubMed]
    [Google Scholar]
  28. Browning DF, Busby SJ. Local and global regulation of transcription initiation in bacteria. Nat Rev Microbiol 2016;14:638–650 [CrossRef][PubMed]
    [Google Scholar]
  29. Buck M, Gallegos MT, Studholme DJ, Guo Y, Gralla JD. The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor. J Bacteriol 2000;182:4129–4136 [CrossRef][PubMed]
    [Google Scholar]
  30. Yang Y, Darbari VC, Zhang N, Lu D, Glyde R et al. Transcription. Structures of the RNA polymerase-σ54 reveal new and conserved regulatory strategies. Science 2015;349:882–885 [CrossRef][PubMed]
    [Google Scholar]
  31. Campbell EA, Kamath S, Rajashankar KR, Wu M, Darst SA. Crystal structure of Aquifex aeolicus σ(N) bound to promoter DNA and the structure of σ(N)-holoenzyme. Proc Natl Acad Sci USA 2017;114:1805–1814
    [Google Scholar]
  32. Glyde R, Ye F, Darbari VC, Zhang N, Buck M et al. Structures of RNA polymerase closed and intermediate complexes reveal mechanisms of DNA opening and transcription initiation. Mol Cell 2017;67:106–116 [CrossRef][PubMed]
    [Google Scholar]
  33. Glyde R, Ye F, Jovanovic M, Kotta-Loizou I, Buck M et al. Structures of bacterial RNA polymerase complexes reveal the mechanism of DNA loading and transcription initiation. Mol Cell 2018;70:1111–1120 [CrossRef][PubMed]
    [Google Scholar]
  34. Visweswariah SS, Busby SJ. Evolution of bacterial transcription factors: how proteins take on new tasks, but do not always stop doing the old ones. Trends Microbiol 2015;23:463–467 [CrossRef][PubMed]
    [Google Scholar]
  35. Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJ. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 2005;102:17693–17698 [CrossRef][PubMed]
    [Google Scholar]
  36. Shimada T, Ishihama A, Busby SJ, Grainger DC. The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res 2008;36:3950–3955 [CrossRef][PubMed]
    [Google Scholar]
  37. Fouqueau T, Blombach F, Werner F. Evolutionary origins of two-barrel RNA polymerases and site-specific transcription initiation. Annu Rev Microbiol 2017;71:331–348 [CrossRef][PubMed]
    [Google Scholar]
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