Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Aug 1;92(16):7327–7331. doi: 10.1073/pnas.92.16.7327

Transcription regulation by inflexibility of promoter DNA in a looped complex.

H E Choy 1, S W Park 1, P Parrack 1, S Adhya 1
PMCID: PMC41332  PMID: 7638190

Abstract

The gal operon of Escherichia coli is negatively regulated by repressor binding to bipartite operators separated by 11 helical turns of DNA. Synergistic binding of repressor to separate sites on DNA results in looping, with the intervening DNA as a topologically closed domain containing the two promoters. A closed DNA loop of 11 helical turns, which is in-flexible to torsional changes, disables the promoters either by resisting DNA unwinding needed for open complex formation or by impeding the processive DNA contacts by an RNA polymerase in flux during transcription initiation. Interaction between two proteins bound to different sites on DNA modulating the activity of the intervening segment toward other proteins by allostery may be a common mechanism of regulation in DNA-multiprotein complexes.

Full text

PDF
7327

Images in this article

7328Fig. 2
on p.7328
7329Fig. 3
on p.7329
7330Fig. 4
on p.7330
7331Fig. 5
on p.7331

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adhya S., Gottesman M., Garges S., Oppenheim A. Promoter resurrection by activators--a minireview. Gene. 1993 Sep 30;132(1):1–6. doi: 10.1016/0378-1119(93)90507-y. [DOI] [PubMed] [Google Scholar]
  2. Adhya S. Multipartite genetic control elements: communication by DNA loop. Annu Rev Genet. 1989;23:227–250. doi: 10.1146/annurev.ge.23.120189.001303. [DOI] [PubMed] [Google Scholar]
  3. Alberti S., Oehler S., von Wilcken-Bergmann B., Krämer H., Müller-Hill B. Dimer-to-tetramer assembly of Lac repressor involves a leucine heptad repeat. New Biol. 1991 Jan;3(1):57–62. [PubMed] [Google Scholar]
  4. Bellomy G. R., Mossing M. C., Record M. T., Jr Physical properties of DNA in vivo as probed by the length dependence of the lac operator looping process. Biochemistry. 1988 May 31;27(11):3900–3906. doi: 10.1021/bi00411a002. [DOI] [PubMed] [Google Scholar]
  5. Borowiec J. A., Zhang L., Sasse-Dwight S., Gralla J. D. DNA supercoiling promotes formation of a bent repression loop in lac DNA. J Mol Biol. 1987 Jul 5;196(1):101–111. doi: 10.1016/0022-2836(87)90513-4. [DOI] [PubMed] [Google Scholar]
  6. Brenowitz M., Jamison E., Majumdar A., Adhya S. Interaction of the Escherichia coli Gal repressor protein with its DNA operators in vitro. Biochemistry. 1990 Apr 3;29(13):3374–3383. doi: 10.1021/bi00465a033. [DOI] [PubMed] [Google Scholar]
  7. Brenowitz M., Mandal N., Pickar A., Jamison E., Adhya S. DNA-binding properties of a lac repressor mutant incapable of forming tetramers. J Biol Chem. 1991 Jan 15;266(2):1281–1288. [PubMed] [Google Scholar]
  8. Buc H. Mechanism of activation of transcription by the complex formed between cyclic AMP and its receptor in Escherichia coli. Biochem Soc Trans. 1986 Apr;14(2):196–199. doi: 10.1042/bst0140196. [DOI] [PubMed] [Google Scholar]
  9. Chamberlin M. J. New models for the mechanism of transcription elongation and its regulation. Harvey Lect. 1992 1993;88:1–21. [PubMed] [Google Scholar]
  10. Chen J., Matthews K. S. Deletion of lactose repressor carboxyl-terminal domain affects tetramer formation. J Biol Chem. 1992 Jul 15;267(20):13843–13850. [PubMed] [Google Scholar]
  11. Choy H. E., Adhya S. Control of gal transcription through DNA looping: inhibition of the initial transcribing complex. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11264–11268. doi: 10.1073/pnas.89.23.11264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Choy H. E., Adhya S. RNA polymerase idling and clearance in gal promoters: use of supercoiled minicircle DNA template made in vivo. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):472–476. doi: 10.1073/pnas.90.2.472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dalma-Weiszhausz D. D., Brenowitz M. Interactions between DNA-bound transcriptional regulators of the Escherichia coli gal operon. Biochemistry. 1992 Aug 4;31(30):6980–6989. doi: 10.1021/bi00145a016. [DOI] [PubMed] [Google Scholar]
  14. Deuschle U., Gentz R., Bujard H. lac Repressor blocks transcribing RNA polymerase and terminates transcription. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4134–4137. doi: 10.1073/pnas.83.12.4134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Drew H. R., Travers A. A. DNA bending and its relation to nucleosome positioning. J Mol Biol. 1985 Dec 20;186(4):773–790. doi: 10.1016/0022-2836(85)90396-1. [DOI] [PubMed] [Google Scholar]
  16. Echols H. Multiple DNA-protein interactions governing high-precision DNA transactions. Science. 1986 Sep 5;233(4768):1050–1056. doi: 10.1126/science.2943018. [DOI] [PubMed] [Google Scholar]
  17. Gellert M., Nash H. Communication between segments of DNA during site-specific recombination. 1987 Jan 29-Feb 4Nature. 325(6103):401–404. doi: 10.1038/325401a0. [DOI] [PubMed] [Google Scholar]
  18. Goodrich J. A., McClure W. R. Regulation of open complex formation at the Escherichia coli galactose operon promoters. Simultaneous interaction of RNA polymerase, gal repressor and CAP/cAMP. J Mol Biol. 1992 Mar 5;224(1):15–29. doi: 10.1016/0022-2836(92)90573-3. [DOI] [PubMed] [Google Scholar]
  19. Haber R., Adhya S. Interaction of spatially separated protein-DNA complexes for control of gene expression: operator conversions. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9683–9687. doi: 10.1073/pnas.85.24.9683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hochschild A., Ptashne M. Cooperative binding of lambda repressors to sites separated by integral turns of the DNA helix. Cell. 1986 Mar 14;44(5):681–687. doi: 10.1016/0092-8674(86)90833-0. [DOI] [PubMed] [Google Scholar]
  21. Horowitz D. S., Wang J. C. Torsional rigidity of DNA and length dependence of the free energy of DNA supercoiling. J Mol Biol. 1984 Feb 15;173(1):75–91. doi: 10.1016/0022-2836(84)90404-2. [DOI] [PubMed] [Google Scholar]
  22. Irani M. H., Orosz L., Adhya S. A control element within a structural gene: the gal operon of Escherichia coli. Cell. 1983 Mar;32(3):783–788. doi: 10.1016/0092-8674(83)90064-8. [DOI] [PubMed] [Google Scholar]
  23. Krämer H., Amouyal M., Nordheim A., Müller-Hill B. DNA supercoiling changes the spacing requirement of two lac operators for DNA loop formation with lac repressor. EMBO J. 1988 Feb;7(2):547–556. doi: 10.1002/j.1460-2075.1988.tb02844.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kuhnke G., Theres C., Fritz H. J., Ehring R. RNA polymerase and gal repressor bind simultaneously and with DNA bending to the control region of the Escherichia coli galactose operon. EMBO J. 1989 Apr;8(4):1247–1255. doi: 10.1002/j.1460-2075.1989.tb03498.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Le Bret M. Catastrophic variation of twist and writhing of circular DNAs with constraint? Biopolymers. 1979 Jul;18(7):1709–1725. doi: 10.1002/bip.1979.360180710. [DOI] [PubMed] [Google Scholar]
  26. Lehming N., Sartorius J., Oehler S., von Wilcken-Bergmann B., Müller-Hill B. Recognition helices of lac and lambda repressor are oriented in opposite directions and recognize similar DNA sequences. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7947–7951. doi: 10.1073/pnas.85.21.7947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Majumdar A., Adhya S. Effect of ethylation of operator-phosphates on Gal repressor binding. DNA contortion by repressor. J Mol Biol. 1989 Jul 20;208(2):217–223. doi: 10.1016/0022-2836(89)90383-5. [DOI] [PubMed] [Google Scholar]
  28. Majumdar A., Rudikoff S., Adhya S. Purification and properties of Gal repressor:pL-galR fusion in pKC31 plasmid vector. J Biol Chem. 1987 Feb 15;262(5):2326–2331. [PubMed] [Google Scholar]
  29. Mandal N., Su W., Haber R., Adhya S., Echols H. DNA looping in cellular repression of transcription of the galactose operon. Genes Dev. 1990 Mar;4(3):410–418. doi: 10.1101/gad.4.3.410. [DOI] [PubMed] [Google Scholar]
  30. Mossing M. C., Record M. T., Jr Upstream operators enhance repression of the lac promoter. Science. 1986 Aug 22;233(4766):889–892. doi: 10.1126/science.3090685. [DOI] [PubMed] [Google Scholar]
  31. Musso R. E., Di Lauro R., Adhya S., de Crombrugghe B. Dual control for transcription of the galactose operon by cyclic AMP and its receptor protein at two interspersed promoters. Cell. 1977 Nov;12(3):847–854. doi: 10.1016/0092-8674(77)90283-5. [DOI] [PubMed] [Google Scholar]
  32. Ptashne M. Gene regulation by proteins acting nearby and at a distance. Nature. 1986 Aug 21;322(6081):697–701. doi: 10.1038/322697a0. [DOI] [PubMed] [Google Scholar]
  33. Ptashne M. How eukaryotic transcriptional activators work. Nature. 1988 Oct 20;335(6192):683–689. doi: 10.1038/335683a0. [DOI] [PubMed] [Google Scholar]
  34. Pérez-Martín J., Espinosa M. Correlation between DNA bending and transcriptional activation at a plasmid promoter. J Mol Biol. 1994 Aug 5;241(1):7–17. doi: 10.1006/jmbi.1994.1468. [DOI] [PubMed] [Google Scholar]
  35. Schleif R. DNA looping. Annu Rev Biochem. 1992;61:199–223. doi: 10.1146/annurev.bi.61.070192.001215. [DOI] [PubMed] [Google Scholar]
  36. Sellitti M. A., Pavco P. A., Steege D. A. lac repressor blocks in vivo transcription of lac control region DNA. Proc Natl Acad Sci U S A. 1987 May;84(10):3199–3203. doi: 10.1073/pnas.84.10.3199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shore D., Baldwin R. L. Energetics of DNA twisting. I. Relation between twist and cyclization probability. J Mol Biol. 1983 Nov 15;170(4):957–981. doi: 10.1016/s0022-2836(83)80198-3. [DOI] [PubMed] [Google Scholar]
  38. Wu H. Y., Liu L. F. DNA looping alters local DNA conformation during transcription. J Mol Biol. 1991 Jun 20;219(4):615–622. doi: 10.1016/0022-2836(91)90658-s. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES