Model of specific complex between catabolite gene activator protein and B-DNA suggested by electrostatic complementarity (original) (raw)

Abstract

Calculation of the electrostatic potential energy surfaces of Escherichia coli catabolite gene activator protein (CAP) dimer suggests a model for the complex between CAP and a specific DNA sequence. The positive electrostatic charge density of CAP lies on the two COOH-terminal domains and about 20-30 A from the molecular 2-fold axis. Assuming that the 2-fold axes of the CAP dimer and the DNA to which it binds are coincident, the positions of the positive electrostatic potential surfaces strongly suggest the rotational orientation of the DNA relative to the protein. A specific complex between CAP and its DNA binding site in the lac operon has been built with the DNA in this orientation. The amino ends of the two protruding F alpha-helices interact in successive major grooves of the DNA. Four side chains emanating from each F helix can form hydrogen bonds with the exposed edges of four bases in the major groove. Electrostatic considerations as well as the necessity to make interactions between CAP and a DNA site as much as 20 base pairs long require us to bend or kink the DNA. In our model of CAP complexed with B-DNA, as with those proposed for Cro and lambda cI repressors, the protruding second helices of the two-helix motif from both subunits interact in successive major grooves of B-DNA. However, unlike Cro and similar to lambda cI, the protruding alpha-helices are nearly parallel to the bases rather than the groove.

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Selected References

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  1. Aiba H. Autoregulation of the Escherichia coli crp gene: CRP is a transcriptional repressor for its own gene. Cell. 1983 Jan;32(1):141–149. doi: 10.1016/0092-8674(83)90504-4. [DOI] [PubMed] [Google Scholar]
  2. Anderson W. F., Ohlendorf D. H., Takeda Y., Matthews B. W. Structure of the cro repressor from bacteriophage lambda and its interaction with DNA. Nature. 1981 Apr 30;290(5809):754–758. doi: 10.1038/290754a0. [DOI] [PubMed] [Google Scholar]
  3. Anderson W. F. Proposed alpha-helical super-secondary structure associated with protein-dna recognition. J Mol Biol. 1982 Aug 25;159(4):745–751. doi: 10.1016/0022-2836(82)90111-5. [DOI] [PubMed] [Google Scholar]
  4. Arnott S., Hukins D. W. Optimised parameters for A-DNA and B-DNA. Biochem Biophys Res Commun. 1972 Jun 28;47(6):1504–1509. doi: 10.1016/0006-291x(72)90243-4. [DOI] [PubMed] [Google Scholar]
  5. Dickson R. C., Abelson J., Johnson P. Nucleotide sequence changes produced by mutations in the lac promoter of Escherichia coli. J Mol Biol. 1977 Mar 25;111(1):65–75. doi: 10.1016/s0022-2836(77)80132-0. [DOI] [PubMed] [Google Scholar]
  6. Epstein W., Rothman-Denes L. B., Hesse J. Adenosine 3':5'-cyclic monophosphate as mediator of catabolite repression in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2300–2304. doi: 10.1073/pnas.72.6.2300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Garner M. M., Revzin A. Stoichiometry of catabolite activator protein/adenosine cyclic 3',5'-monophosphate interactions at the lac promoter of Escherichia coli. Biochemistry. 1982 Nov 23;21(24):6032–6036. doi: 10.1021/bi00267a001. [DOI] [PubMed] [Google Scholar]
  8. Hecht M. H., Nelson H. C., Sauer R. T. Mutations in lambda repressor's amino-terminal domain: implications for protein stability and DNA binding. Proc Natl Acad Sci U S A. 1983 May;80(9):2676–2680. doi: 10.1073/pnas.80.9.2676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hochschild A., Irwin N., Ptashne M. Repressor structure and the mechanism of positive control. Cell. 1983 Feb;32(2):319–325. doi: 10.1016/0092-8674(83)90451-8. [DOI] [PubMed] [Google Scholar]
  10. Kolb A., Buc H. Is DNA unwound by the cyclic AMP receptor protein? Nucleic Acids Res. 1982 Jan 22;10(2):473–485. doi: 10.1093/nar/10.2.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kolb A., Spassky A., Chapon C., Blazy B., Buc H. On the different binding affinities of CRP at the lac, gal and malT promoter regions. Nucleic Acids Res. 1983 Nov 25;11(22):7833–7852. doi: 10.1093/nar/11.22.7833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lewis M., Jeffrey A., Wang J., Ladner R., Ptashne M., Pabo C. O. Structure of the operator-binding domain of bacteriophage lambda repressor: implications for DNA recognition and gene regulation. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 1):435–440. doi: 10.1101/sqb.1983.047.01.051. [DOI] [PubMed] [Google Scholar]
  13. Matthew J. B., Hanania G. I., Gurd F. R. Electrostatic effects in hemoglobin: hydrogen ion equilibria in human deoxy- and oxyhemoglobin A. Biochemistry. 1979 May 15;18(10):1919–1928. doi: 10.1021/bi00577a011. [DOI] [PubMed] [Google Scholar]
  14. Matthew J. B., Richards F. M. Anion binding and pH-dependent electrostatic effects in ribonuclease. Biochemistry. 1982 Sep 28;21(20):4989–4999. doi: 10.1021/bi00263a024. [DOI] [PubMed] [Google Scholar]
  15. Matthew J. B., Weber P. C., Salemme F. R., Richards F. M. Electrostatic orientation during electron transfer between flavodoxin and cytochrome c. Nature. 1983 Jan 13;301(5896):169–171. doi: 10.1038/301169a0. [DOI] [PubMed] [Google Scholar]
  16. McKay D. B., Steitz T. A. Structure of catabolite gene activator protein at 2.9 A resolution suggests binding to left-handed B-DNA. Nature. 1981 Apr 30;290(5809):744–749. doi: 10.1038/290744a0. [DOI] [PubMed] [Google Scholar]
  17. McKay D. B., Weber I. T., Steitz T. A. Structure of catabolite gene activator protein at 2.9-A resolution. Incorporation of amino acid sequence and interactions with cyclic AMP. J Biol Chem. 1982 Aug 25;257(16):9518–9524. [PubMed] [Google Scholar]
  18. Movva R. N., Green P., Nakamura K., Inouye M. Interaction of cAMP receptor protein with the ompA gene, a gene for a major outer membrane protein of Escherichia coli. FEBS Lett. 1981 Jun 15;128(2):186–190. doi: 10.1016/0014-5793(81)80077-4. [DOI] [PubMed] [Google Scholar]
  19. Ohlendorf D. H., Anderson W. F., Fisher R. G., Takeda Y., Matthews B. W. The molecular basis of DNA-protein recognition inferred from the structure of cro repressor. Nature. 1982 Aug 19;298(5876):718–723. doi: 10.1038/298718a0. [DOI] [PubMed] [Google Scholar]
  20. Ohlendorf D. H., Anderson W. F., Lewis M., Pabo C. O., Matthews B. W. Comparison of the structures of cro and lambda repressor proteins from bacteriophage lambda. J Mol Biol. 1983 Sep 25;169(3):757–769. doi: 10.1016/s0022-2836(83)80169-7. [DOI] [PubMed] [Google Scholar]
  21. Ohlendorf D. H., Anderson W. F., Takeda Y., Matthews B. W. High resolution structural studies of Cro repressor protein and implications for DNA recognition. J Biomol Struct Dyn. 1983 Oct;1(2):553–563. doi: 10.1080/07391102.1983.10507461. [DOI] [PubMed] [Google Scholar]
  22. Pabo C. O., Krovatin W., Jeffrey A., Sauer R. T. The N-terminal arms of lambda repressor wrap around the operator DNA. Nature. 1982 Jul 29;298(5873):441–443. doi: 10.1038/298441a0. [DOI] [PubMed] [Google Scholar]
  23. Pabo C. O., Lewis M. The operator-binding domain of lambda repressor: structure and DNA recognition. Nature. 1982 Jul 29;298(5873):443–447. doi: 10.1038/298443a0. [DOI] [PubMed] [Google Scholar]
  24. Sauer R. T., Yocum R. R., Doolittle R. F., Lewis M., Pabo C. O. Homology among DNA-binding proteins suggests use of a conserved super-secondary structure. Nature. 1982 Jul 29;298(5873):447–451. doi: 10.1038/298447a0. [DOI] [PubMed] [Google Scholar]
  25. Shire S. J., Hanania G. I., Gurd F. R. Electrostatic effects in myoglobin. Hydrogen ion equilibria in sperm whale ferrimyoglobin. Biochemistry. 1974 Jul 2;13(14):2967–2974. doi: 10.1021/bi00711a028. [DOI] [PubMed] [Google Scholar]
  26. Simpson R. B. Interaction of the cAMP receptor protein with the lac promoter. Nucleic Acids Res. 1980 Feb 25;8(4):759–766. [PMC free article] [PubMed] [Google Scholar]
  27. Steitz T. A., Ohlendorf D. H., McKay D. B., Anderson W. F., Matthews B. W. Structural similarity in the DNA-binding domains of catabolite gene activator and cro repressor proteins. Proc Natl Acad Sci U S A. 1982 May;79(10):3097–3100. doi: 10.1073/pnas.79.10.3097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Steitz T. A., Weber I. T., Matthew J. B. Catabolite gene activator protein: structure, homology with other proteins, and cyclic AMP and DNA binding. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 1):419–426. doi: 10.1101/sqb.1983.047.01.049. [DOI] [PubMed] [Google Scholar]
  29. Steitz T. A., Weber I. T., Ollis D., Brick P. Crystallographic studies of protein-nucleic acid interaction: catabolite gene activator protein and the large fragment of DNA polymerase I. J Biomol Struct Dyn. 1983 Dec;1(4):1023–1037. doi: 10.1080/07391102.1983.10507500. [DOI] [PubMed] [Google Scholar]
  30. Takahashi M., Blazy B., Baudras A. An equilibrium study of the cooperative binding of adenosine cyclic 3',5'-monophosphate and guanosine cyclic 3',5'-monophosphate to the adenosine cyclic 3',5'-monophosphate receptor protein from Escherichia coli. Biochemistry. 1980 Oct 28;19(22):5124–5130. doi: 10.1021/bi00563a029. [DOI] [PubMed] [Google Scholar]
  31. Weber I. T., McKay D. B., Steitz T. A. Two helix DNA binding motif of CAP found in lac repressor and gal repressor. Nucleic Acids Res. 1982 Aug 25;10(16):5085–5102. doi: 10.1093/nar/10.16.5085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wu H. M., Crothers D. M. The locus of sequence-directed and protein-induced DNA bending. Nature. 1984 Apr 5;308(5959):509–513. doi: 10.1038/308509a0. [DOI] [PubMed] [Google Scholar]
  33. Zubay G., Schwartz D., Beckwith J. Mechanism of activation of catabolite-sensitive genes: a positive control system. Proc Natl Acad Sci U S A. 1970 May;66(1):104–110. doi: 10.1073/pnas.66.1.104. [DOI] [PMC free article] [PubMed] [Google Scholar]