Wrapping of flanking non-operator DNA in lac repressor-operator complexes: Implications for DNA looping

Journal of Molecular Biology

Volumn 294, Issue 3, 1999, Pages 639-655

  Tsodikov, Oleg V ^b   Saecker, Ruth M ^b   Melcher, Sonya E ^a   Levandoski, Mark M ^a   Frank, Diane E ^a   Capp, Michael W ^b   Record Jr , M Thomas ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NONE

Author keywords

Cooperativity; lac repressor; Looping; Salt effects; Wrapping

Indexed keywords

DNA BINDING PROTEIN; PHOSPHATE; PLASMID DNA; POLYELECTROLYTE; TETRAMER;

ARTICLE; BINDING AFFINITY; DNA BINDING; DNA FLANKING REGION; DNA SEQUENCE; DNA STRUCTURE; LACTOSE OPERON; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; REPRESSOR GENE; THERMODYNAMICS;

EID: 0033521211     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3283     Document Type: Article

References (73)

1. Amouyal M., Buc H. Topological unwinding of strong and weak promoters by RNA polymerase: a comparison between the lac wild-type and the UV5 sites of Escherichia coli. J. Mol. Biol. 195:1987;795-808.
2. Antson A. A., Dodson E. J., Dodson G. G., Greaves R. B., Chen X.-P., Gollnick P. Structure of the Trp RNA-binding attenuation protein, trap, bound to RNA. Nature. 401:1999;235-242.
3. Barkley M. D. Salt dependence of the kinetics of the lac repressor-operator interaction: role of nonoperator deoxyribonucleic acid in the association reaction. Biochemistry. 20:1981;3833-3842.
4. Barry J. K., Matthews K. S. Thermodynamic analysis of unfolding and dissociation in lactose repressor protein. Biochemistry. 38:1999;6520-6528.
5. 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. 27:1988;3900-3906.
6. 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. 196:1987;101-111.
7. Brenowitz M., Pickar A., Jamison E. Stability of lac repressor mediated "looped complex" Biochemistry. 30:1991;5986-5998.
8. +concentrations on Lac repressor- lac operator binding: in vitro thermodynamic analysis and in vivo relevance. J. Mol. Biol. 258:1996;25-36.
9. Coulombe B., Burton Z. F. DNA bending and wrapping around RNA polymerase: A "revolutionary" model describing transcriptional mechanisms. Microbiol. Mol. Biol. Rev. 63:1999;457-478.
10. 2+ binding and its structural consequences at the transcription start site. Biochemistry. 34:1995;15624-15632.
11. deHaseth P. L., Lohman T., Record M. T. Non-specific interactions of lac repressor with DNA: an association reaction driven by counterion release. Biochemistry. 22:1977;4783-4790.
12. Du H., Tarpey R., Babitzke P. The trp RNA-binding attenuation protein regulates TrpG synthesis by binding to the trpG ribosome binding site of Bacillus subtilis. J. Bacteriol. 179:1997;2582-2586.
13. Ebright R. H. RNA polymerase-DNA interaction: structures of intermediate, open, and elongation complexes. Cold Spring Harbor Symp. Quant. Biol. 63:1998;11-20.
14. Echols H. Multiple DNA-protein interactions govern high-precision DNA transactions. Science. 233:1986;1050-1056.
15. Echols H. Nucleoprotein structures initiating DNA replication, transcription, and site-specific recombination. J. Biol. Chem. 265:1990;14697-14700.
16. Eismann E. R., Müller-Hill B. lac Repressor forms stable loops in vitro with supercoiled wild-type lac DNA containing all three natural lac operators. J. Mol. Biol. 213:1990;763-775.
17. Finkel S. E., Johnson R. C. The Fis protein: it's not just for DNA inversion anymore. Mol. Microbiol. 6:1992;3257-3265.
18. Frank D. E., Saecker R. M., Bond J. P., Capp M. W., Tsodikov O. V., Melcher S. E., Levandoski M. M., Record M. T. Jr. Thermodynamics of the interactions of lac repressor with variants of the symmetric lac operator: effects of converting a consensus site to a non-specific site. J. Mol. Biol. 267:1997;1186-1206.
19. Friedman A. M., Fischmann T. O., Steitz T. A. Crystal structure of Lac repressor core tetramer and its implications for DNA looping. Science. 268:1995;1721-1727.
20. Goosen N., van Ulsen P., Zulianello L., van de Putte P. Transcription activation by histone-like protein integration host factor. Methods Enzymol. 274:1996;32-43.
21. Ha J.-H., Capp M. W., Hohenwalter M. D., Baskerville M., Record M. T. Jr. Thermodynamic stoichiometries of participation of water, cations and anions in specific and nonspecific binding of lac repressor to DNA: possible thermodynamic origins of the "glutamate effect" on protein-DNA interactions. J. Mol. Biol. 228:1992;252-264.
22. adi, and the native dimeric gal repressor. J. Biol. Chem. 272:1997;22092-22096.
23. Hsieh W.-T., Whitson P. A., Matthews K. S., Wells R. D. Influence of sequence and distance between two operators on interaction with the lac repressor. J. Biol. Chem. 262:1987;14583-14591.
24. Johnson M. L., Frasier S. G. Nonlinear least-squares analysis. Methods Enzymol. 117:1985;301-342.
25. Kirkegaard K., Wang J. C. Mapping the topography of DNA wrapped around gyrase by nucleolytic and chemical probing of complexes of unique DNA sequences. Cell. 23:1981;721-729.
26. Krämer H., Niemoller M., Amouyal M., Revet B., von Wilcken-Bergmann B., Müller-Hill B. Lac repressor forms loops with linear DNA carrying two suitably spaced lac operators. EMBO J. 6:1987;1481-1491.
27. 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. 7:1988;547-556.
28. Law S. M., Bellomy G. R., Schlax P. J., Record M. T. Jr. In vivo thermodynamic analysis of repression with and without looping in lac constructs: estimates of free and local lac repressor concentrations and of physical properties of a region of supercoiled plasmid DNA in vivo. J. Mol. Biol. 230:1993;161-173.
29. sym operators to a LacI tetramer: evidence for contribution of non-operator DNA binding by wrapping and looping. J. Mol. Biol. 260:1996;697-717.
30. Lewis M., Chang G., Horton N. C., Kercher M. A., Pace H. C., Schumacher M. A., Brennan R. G., Lu P. Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science. 271:1996;1247-1254.
31. Lohman T. M., deHaseth P. L., Record M. T. Jr. Pentalysine-deoxyribonucleic acid interactions: a model for the general effects of ion concentrations on the interactions of proteins with nucleic acids. Biochemistry. 19:1980;3522-3530.
32. Luger K., Mader A. W., Richmond R. K., Sargent D. F., Richmond T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 389:1997;251-260.
33. Mossing M. C., Record M. T. Jr. Thermodynamic origins of specificity in the lac repressor-operator interaction: adaptability in the recognition of mutant operator sites. J. Mol. Biol. 186:1985;295-305.
34. Müller J., Oehler S., Müller-Hill B. Repression of lac promoter as a function of distance, phase and quality of an auxiliary lac operator. J. Mol. Biol. 257:1996;21-29.
35. Mukhodpadyay G., Chattoraj D. K. Conformation of the origin of P1 plasmid replication. Initiator protein induced wrapping and intrinsic unstacking. J. Mol. Biol. 231:1993;19-28.
36. Oehler S., Eismann E. R., Krämer H., Müller-Hill B. The three operators of the lac operon cooperate in repression. EMBO J. 9:1990;973-979.
37. Pace H. C., Kercher M. A., Lu P., Markiewicz P., Miller J. H., Chang G., Lewis M. Lac repressor genetic map in real space. Trends Biochem. Sci. 22:1997;334-339.
38. Pan C. Q., Finkel S. E., Cramton S. E., Feng J. A., Sigman D. S., Johnson R. C. Variable structures of Fis-DNA complexes determined by flanking DNA -protein contacts. J. Mol. Biol. 264:1996;675-695.
39. Perros M., Steitz T. DNA looping and lac repressor-CAP interaction. Science. 274:1996;1929-1930.
40. Pettijohn D. E. The nucleoid. Neidhardt F. C. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. 1996;58-166 ASM Press, Washington.
41. Polyakov A., Severinova E., Darst S. A. Three-dimensional structure of E. coli core RNA polymerase: promoter binding and elongation conformations of the enzyme. Cell. 83:1995;365-373.
42. Record M. T. Jr, Lohman T. M., deHaseth. P. Ion effects on ligand-nucleic acid interactions. J. Mol. Biol. 107:1976;145-158.
43. Record M. T. Jr, Courtenay E. S., Cayley D. S., Guttman H. J. Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23:1998;143-148.
44. Reece R. J., Maxwell A. The C-terminal domain of the Escherichia coli DNA gyrase A subunit is a DNA-binding protein. Nucl. Acids Res. 19:1991;1399-1405.
45. Rice P. A., Yang S.-W., Mizuuchi K., Nash H. A. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell. 87:1996;1295-1306.
46. Riggs A. D., Suzuki H., Bourgeois S. Lac repressor-operator interaction I. Equilibrium studies. J. Mol. Biol. 48:1970;67-83.
47. Rivetti C., Guthold M., Bustamante C. Wrapping of DNA around the E. coli RNA polymerase open promoter complex. EMBO J. 18:1999;4464-4475.
48. Robert F., Douziech M., Forget D., Egly J. M., Greenblatt J., Burton Z. F., Coulombe B. Wrapping of promoter DNA around the RNA polymerase II initiation complex induced by TFIIF. Mol. Cell. 2:1998;341-351.
49. Rybenkov V. V., Vologodskii A. V., Cozzarelli N. R. The effect of ionic conditions on the conformations of supercoiled DNA. II. Equilibrium catenation. J. Mol. Biol. 267:1997;312-323.
50. Sambrook J., Fritsch E. F., Maniatis T. Editors of Molecular Cloning. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
51. Schlax P. E. Jr, Capp M. W., Record M. T. Jr. Preparative-scale purification of DNA restriction fragments by continuous-flow gel electrophoresis. BioTechniques. 18:1995;94-99.
52. Schumacher M. A., Choi K. Y., Zalkin H., Brennan R. G. Crystal structure of LacI member, PurR, bound to DNA: minor groove binding by α helices. Science. 266:1994;763-770.
53. Simons A., Tils D., von Wilcken-Bergmann B., Müller-Hill B. Possible ideal Lac operator: Escherichia coli Lac operator-like sequences from eukaryotic genomes lack the central GC pair. Proc. Natl Acad. Sci. USA. 81:1984;1624-1628.
54. Slijper M., Bonvin A. M. J. J., Boelens R., Kaptein R. Refined structure of lac repressor headpiece (1-56) determined by relaxation matrix calculations from 2D NOE data: change of tertiary structure upon binding to the lac operator. J. Mol. Biol. 259:1996;761-773.
55. Slijper M., Boelens R., Davis A. L., Konings R. N. H., van der arel G. A., van Boom J. H., Kaptein R. Backbone and side chain dynamics of lac repressor headpiece (1-56) and its complex with DNA. Biochemistry. 36:1997;249-254.
56. Spolar R. S., Record M. T. Jr. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:1994;777-784.
57. Spronk C. A., Slijper M., van Boom J. H., Kaptein R., Boelens R. Formation of the hinge helix in the lac repressor is induced upon binding to the lac operator. Nature Struct. Biol. 3:1996;447-452.
58. Travers A. A. DNA conformation and protein binding. Advan. Protein Chem. 58:1989;427-452.
59. Ueguchi C., Seto C., Suzuki T., Mizuno T. Clarification of the dimerization domain and its functional significance for the Escherichia coli nucleoid protein H-NS. J. Mol. Biol. 274:1997;145-151.
60. Wang J. C. DNA topoisomerases. Annu. Rev. Biochem. 65:1996;635-692.
61. Wang J. C., Barkley M. D., Bourgeois S. Measurements of unwinding of lac operator by repressor. Nature. 251:1974;247-249.
62. Whitson P. A., Matthews K. S. Dissociation of the lactose repressor-operator DNA complex: effects of size and sequence context of operator-containing DNA. Biochemistry. 25:1986;3845-3852.
63. Whitson P. A., Olson J. S., Matthews K. S. Thermodynamic analysis of the lactose repressor-operator DNA interaction. Biochemistry. 25:1986;3852-3858.
64. Whitson P. A., Hsieh W.-T., Wells R., Matthews K. S. Supercoiling facilitates lac operator-repressor-pseudooperator interactions. J. Biol. Chem. 262:1987;4943-4946.
65. Winter R. B., von Hippel P. H. Diffusion-driven mechanisms of protein translocation on nucleic acids. 2. The Escherichia coli repressor-operator interaction: equilibrium measurements. Biochemistry. 20:1981;6948-6960.
66. Winter R. B., Berg O. G., von Hippel P. H. Diffusion-driven mechanisms of protein translocation on nucleic acids. 3. The Escherichia coli repressor-operator interaction: kinetic measurements and conclusions. Biochemistry. 20:1981;6961-6977.
67. Wong I., Lohman T. M. Linkage of protein assembly and protein-DNA binding. Methods Enzymol. 259:1995;95-126.
68. Wong I., Chao K. L., Bujalowski W., Lohman T. M. DNA-induced dimerization of the Escherichia coli Rep helicase. Allosteric effects of single-stranded and duplex DNA. J. Biol. Chem. 267:1992;7596-7610.
69. Yang C.-C., Nash H. A. The interaction of E. coli IHF protein with its specific binding sites. Cell. 57:1989;869-880.
70. Yang M., Chen X. P., Militello K., Hoffman R., Fernandez B., Baumann C., Gollnick P. Alanine-scanning mutagenesis of Bacillus subtilis trp RNA-binding attenuation protein (TRAP) reveals residues involved in tryptophan binding and RNA binding. J. Mol. Biol. 270:1997;696-710.
71. Zhang W., Bond J. P., Anderson C. F., Lohman T. M., Record M. T. Jr. Large electrostatic differences in the binding thermodynamics of a cationic peptide to oligomeric and polymeric DNA. Proc. Natl Acad. Sci. USA. 93:1996;2511-2516.
72. Zhang W., Ni H., Capp M. W., Anderson C. F., Lohman T. M., Record M. T. Jr. The importance of coulombic end effects: experimental characterization of the effects of oligonucleotide flanking charges on the strength and salt dependence of oligocation (L8+) binding to single-stranded DNA oligomers. Biophys. J. 76:1999;1008-1017.
73. Zwieb C., Kim J., Adhya S. DNA bending by negative regulatory proteins: Gal and Lac repressors. Genes Dev. 3:1989;606-611.