Cooperative and anticooperative effects in binding of the first and second plasmid O(sym) operators to a lad tetramer: Evidence for contributions of non-operator DNA binding by wrapping and looping

Journal of Molecular Biology

Volumn 260, Issue 5, 1996, Pages 697-717

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

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cooperativity; Lac operator; Lac repressor; Linkage; Protein DNA interactions

Indexed keywords

DIMER; PLASMID DNA; TETRAMER;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA BINDING; DNA CONFORMATION; EQUILIBRIUM CONSTANT; EXPERIMENTAL MODEL; GENETIC REGULATION; LACTOSE OPERON; OPERATOR; OSMOLARITY; PLASMID; POTASSIUM CELL LEVEL; PRIORITY JOURNAL; PROPRIOCEPTION; PROTEIN DNA INTERACTION; REPRESSOR GENE; STOICHIOMETRY;

EID: 0030564945     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0431     Document Type: Article

References (51)

1. Barkley, M. D. (1981). Salt dependence of the kinetics of the lac repressor-operator interaction: role of non operator deoxyribonucleic acid in the association reaction. Biochemistry, 20, 3833-3842.
2. Bellomy, G. R. & Record, M. T., Jr (1990). Stable DNA loops in vivo and in vitro: roles in gene regulation at a distance and in biophysical characterization of DNA. Prog. Nucl. Acid Res. Mol. Biol. 39, 81-128.
3. Brenowitz, M. & Jamison, E. (1993). Modulation of the stability of a lac repressor mediated looped complex by temperature and ions: allosteric regulation by chloride. Biochemistry, 32, 8693-8701.
4. Brenowitz, M., Pickar, A. & Jamison, E. (1991). Stability of lac repressor mediated "looped complex". Biochemistry, 30, 5986-5998.
5. Bujalowski, W. & Lohman, T. M. (1989). Negative cooperativity in E. coli single strand binding protein-oligonucleotide interactions. J. Mol. Biol. 207, 249-268.
6. Bujalowski, W. & Lohman, T. M. (1991). Monomers of the Escherichia coli SSB-1 mutant bind single-stranded DNA. J. Mol. Biol. 217, 63-74.
7. + concentrations lac repressor-lac operator binding: in vitro "thermodynamic analysis and in vivo relevance". J. Mol. Biol. 258, 25-36.
8. Cayley, S., Lewis, B. A., Guttman, H. J. & Record, M. T., Jr (1991). Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity: implications for protein-DNA interactions in vivo. J. Mol. Biol. 222, 281-300.
9. Chakerian, A. E. & Matthews, K. S. (1992). Effect of lac repressor oligomerization on regulatory outcome. Mol. Microbiol. 6, 963-968.
10. Eismann, E. R. & Müller-Hill, B. (1990). Lac repressor forms stable loops in vitro with supercoiled wildtype lac containing all three natural lac operators. J. Mol. Biol. 213, 763-775.
11. Fickert, R. & Müller-Hill, B. (1992). How lac repressor finds lac operator in vitro. J. Mol. Biol. 226, 59-68.
12. Frank, D. E. (1995). Thermodynamic origins of specificity in the lac repressor-lac operator interaction. PhD thesis, University of Wisconsin-Madison, WI.
13. Friedman, A. M., Fischmann, T. O. & Steitz, T. A. (1995). Crystal structure of lac repressor core tetramer and its implications for DNA looping. Science, 268, 1721-1727.
14. Ha, J.-H., Capp, M. W., Hohenwalter, M. D., Baskerville, M. & Record, M. T., Jr (1992). 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, 252-264.
15. Johnson, M. L. & Frasier, S. G. (1985). Nonlinear least-square analysis. Methods Enzymol. 117, 301-342.
16. Koblan, K. S. & Ackers, G. K. (1991). Energetics of subunit dimerization in bacteriophage λ, cl repressor: linkage to protons, temperature, and KCl. Biochemistry, 30, 7817-7821.
17. Laiken, S. L., Gross, C. A. & von Hippel, P. H. (1972). Equilibrium and kinetic studies of Escherichia coli lac repressor-inducer interactions. J. Mol. Biol. 66, 143-155.
18. Law, S. M., Bellomy, G. R., Schlax, P. J. & Record, M. T., Jr (1993). 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, 161-173.
19. Lehming, N., Sartorius, J., Niemoller, M., Genenger, G., von Wilcken-Bergmann, B. & Müller-Hill, B. (1987). The interaction of the recognition helix of lac repressor with lac operator. EMBO J. 6, 3145-3153.
20. Levandoski, M. M. (1995). A thermodynamic comparison of the DNA binding behaviors of wildtype (Tyr17) and the variant Phe17 lac repressors. PhD thesis, University of Wisconsin-Madison, WI.
21. Lewis, D. E. A. & Carey, J. (1993). Analysis of trp repressor-DNA interactions using gel electrophoresis. Electrophoresis, 14, 713-719.
22. Lewis, M., Chang, G., Horton, N. C., Kercher, M. A., Pace, H. C., Schumacher, M. A., Brennan, R. G. & Lu, P. (1996). Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science, 271, 1247-1254.
23. Liu, L.-C. & Matthews, K. S. (1993). Dependence of trp repressor-operator affinity, stoichiometry, and apparent cooperativity on DNA sequence and size. J. Biol. Chem. 268, 2239-2249.
24. 56 DNA binding modes. Biochemistry, 27, 2260-2265.
25. Lohman, T. M. & Bujalowski, W. (1991). Thermodynamic methods for the model-independent determination of equilibrium binding isotherms for protein-DNA interactions, using spectroscopic approaches to monitor binding. Methods Enzymol. 208, 1258-1290.
26. Lohman, T. M. & Bujalowski, W. (1994). Effects of base composition on the negative cooperativity and binding mode transitions of E. coli SSB-single-stranded DNA complexes. Biochemistry, 33, 6167-6176.
27. O'Gorman, R. B., Dunaway, M. & Matthews, K. S. (1980). DNA binding characteristics of lactose repressor and the trypsin-resistant core repressor. J. Biol Chem. 255, 10100-10106.
28. Oehler, S., Eismann, E. R., Krämer, H. & Müller-Hill, B. (1990). The three operators of the lac operon cooperate in repression. EMBO J. 9, 973-979.
29. Record, M. T., Jr, Anderson, C. F. & Lohman, T. M. (1978). Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening, and ion effects on water activity. Quart. Rev. Biophys, 2, 103-178.
30. Record, M. T., Jr, Ha, J.-H. & Fisher, M. A. (1991). Use of equilibrium and kinetic measurements to determine the thermodynamic origins of stability and specificity and mechanism of formation of site-specific complexes between proteins and helical DNA. Methods Enzymol. 208, 291-343.
31. Record, M. T., Jr & Spolar, R. S. (1990). Some thermodynamic principles of nonspecific and site-specific protein-DNA interactions. In The Biology of Nonspecific DNA-Protein Interactions (Revzin, A., ed.), pp. 33-69, CRC Press, Boston.
32. Riggs, A. D., Suzuki, H. & Bourgeois, S. (1970a). Lac repressor-operator interaction. I. Equilibrium studies. J. Mol. Biol. 48, 67-83.
33. Riggs, A. D., Bourgeois, S. & Cohn, M. (1970b). Lac repressor-operator interaction. III. Kinetic studies. J. Mol. Biol. 53, 401-417.
34. Rosenberg, J. M., Khallai, O. B., Kopka, M. L., Dickerson, R. E. & Riggs, A. D. (1977). Lac repressor purification without inactivation of DNA binding activity. Nucl. Acids Res. 4, 567-572.
35. 32P on the physical and biological properties of DNA. J. Mol. Biol. 54, 441-463.
36. Royer, C. A., Chakerian, A. E. & Matthews, K. S. (1990). Macromolecular binding equilibria in the lac repressor system: studies using high-pressure fluorescence spectroscopy. Biochemistry, 29, 4959-4966.
37. Royer, C. A., Weber, G., Daly, T. J. & Matthews, K. S. (1986). Dissociation of the lactose repressor protein tetramer using high hydrostatic pressure. Biochemistry, 25, 8308-8315.
38. Sambrook, J., Fritsch, E. F. & Maniatis, T., Editors (1989). Molecular Cloning, 2nd edit., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Senear, D. F. & Batey, R. (1991). Comparison of operator-specific and nonspecific DNA binding of the λ, cl repressor: [KCl] and pH effects. Biochemistry, 30, 6677-6688.
40. Simons, A., Tils, D., von Wilcken-Bergmann, B. & Müller-Hill, B. (1984). Possible ideal lac repressor: Escherichia coli lac operator-like sequences from eukaryotic genomes lack the central GC pair. Proc. Natl Acad. Sci. USA, 81, 1624-1628.
41. Smolarsky, M. & Tal, M. (1970). Novel method for measuring polyuridylic acid binding to ribosomes. Biochim. Biophys. Acta, 199, 447-452.
42. Stickle, D. F., Liu, G. & Fried, M. G. (1994). Analysis of the thermodynamic linkage of DNA binding and ion binding for dimeric and tetrameric forms of the lac repressor. Eur. J. Biochem. 226, 869-876.
43. von Hippel, P. H. & Berg, O. G. (1989). Facilitated target location in biological systems. J. Biol. Chem. 264, 675-678.
44. Vossen, K. M., Stickle, D. F. & Fried, M. G. (1996). The mechanism of CAP-lac repressor binding cooperativity at the E. coli lactose promoter. J. Mol. Biol. 255, 44-54.
45. Whitson, P. A. & Matthews, K. S. (1986). Dissociation of the lactose repressor-operator DNA complex: effects of size and sequence context of operator-containing DNA. Biochemistry, 25, 3845-3852.
46. Whitson, P. A., Olson, J. S. & Matthews, K. S. (1986). Thermodynamic analysis of the lactose repressor-operator DNA interaction. Biochemistry, 25, 3852-3858.
47. Winter, R. B., Berg, O. G. & von Hippel, P. H. (1981). Diffusion-driven mechanism of protein translocation on nucleic acids. 3. The Escherichia coli lac repressor-operator interaction: kinetic measurements and conclusions. Biochemistry, 20, 6961-6977.
48. Winter, R. B. & von Hippel, P. H. (1981). Diffusion-driven mechanisms of protein translocation on nucleic acids. 2. The Escherichia coli lac repressor-operator interaction: equilibrium measurements. Biochemistry, 20, 6948-6960.
49. Wong, I., Chao, K. L., Bujalowski, W. & Lohman, T. M. (1992). DNA-induced dimerization of the Escherichia coli rep helicase. Allosteric effects of single-stranded and duplex DNA. J. Biol. Chem. 267, 7596-7610.
50. Wong, I. & Lohman, T. M. (1995). Linkage of protein assembly and protein-DNA binding. Methods Enzymol. 259, 95-126.
51. Zhang, X. & Gottlieb, P. A. (1995). Modified nucleotides reveal the indirect role of the central base pair in stabilizing the lac repressor-operator complex. Nucl. Acids Res. 23, 1502-1511.