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

Journal of Molecular Biology

Volumn 267, Issue 5, 1997, Pages 1186-1206

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

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Consensus; lac repressor; Recognition; Specificity

Indexed keywords

DNA; DNA FRAGMENT; PROTEIN;

ARTICLE; BINDING AFFINITY; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA PROTEIN COMPLEX; DNA SEQUENCE; ENTHALPY; ENTROPY; LACTOSE OPERON; MOLECULAR STABILITY; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OPERATOR GENE; PRIORITY JOURNAL; PROTEIN DNA BINDING; REPRESSOR GENE; STRUCTURE ACTIVITY RELATION; TEMPERATURE SENSITIVITY; THERMODYNAMICS;

EID: 0031576995     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.0920     Document Type: Article

References (106)

1. Ackers G. K., Smith F. R. Effects of site-specific amino acid modification on protein interactions and biological function. Annu. Rev. Biochem. 54:1985;597-629.
2. Ades S. E., Sauer R. T. Specificity of minor-groove and major-groove interactions in a homeodomain-DNA complex. Biochemistry. 34:1995;14601-14608.
3. Alexander P., Fahnestock S., Lee T., Orban J., Bryan P. Thermodynamic analysis of the folding of the streptococcal protein G IgG-binding domains B2 and B2: why small proteins tend to have high denaturation temperatures. Biochemistry. 31:1992;3597-3603.
4. 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.
5. Bell A. C., Koudelka G. B. Operator sequence context influences amino acid-base-pair interactions in 434 repressor-operator complexes. J. Mol. Biol. 234:1993;542-553.
6. Berg O. G., von Hippel P. H. Selection of DNA binding sites by regulatory proteins. II. The binding specificity of cyclic AMP receptor protein to recognition sites. J. Mol. Biol. 200:1988a;709-723.
7. Berg O. G., von Hippel P. H. Selection of DNA binding sites by regulatory proteins. Trends Biochem. Sci. 13:1988b;207-211.
8. Brenowitz M., Jamison E., Majumdar A., Adhya S. Interaction of the Escherichia coli gal repressor protein with its DNA operators in vitro. Biochemistry. 29:1990;3374-3383.
9. Butler A. P., Revzin A., von Hippel P. H. Molecular parameters characterizing the interaction of Escherichia coli lac repressor with non-operator DNA and inducer. Biochemistry. 16:1977;4757-4768.
10. +concentrations on lac repressor- lac operator binding: in vitro thermodynamic analysis and in vivo relevance. J. Mol. Biol. 258:1996;25-36.
11. Chuprina V. P., Rullmann J. A. C., Lamerichs R. M. J. N., van Boom J. H., Boelens R., Kaptein R. Structure of the complex of lac repressor headpiece and an 11 base-pair half-operator determined by nuclear magnetic resonance spectroscopy and restrained molecular dynamics. J. Mol. Biol. 234:1993;446-462.
12. Connelly P., Ghosaini L., Hu C.-Q., Kitamura S., Tanaka A., Sturtevant J. M. A differential scanning calorimetric study of the thermal unfolding of seven mutant forms of phage T4 lysozyme. Biochemistry. 30:1991;1887-1891.
13. deHaseth P. L., Lohman T. M., Record M. T., Jr. Nonspecific interactions of lac repressor with DNA: an association reaction driven by counterion release. Biochemistry. 16:1977;4783-4790.
14. Ferrari M. E., Lohman T. Apparent heat capacity change accompanying a nonspecific protein-DNA interaction. Escherichia coli SSB tetramer binding to oligodeoxyadenylates. Biochemistry. 33:1994;12896-12910.
15. n. J. Mol. Biol. 122:1978;465-470.
16. Frank, D. E. 1995, Thermodynamic origins of specificity in the lac repressor- lac operator interactions. PhD thesis, University of Wisconsin-Madison, WI.
17. 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.
18. Gill S. J., Dec S. F., Olofsson F., Wadsö I. Anomalous heat capacity of hydrophobic solvation. J. Phys. Chem. 89:1985;3758-3791.
19. Guinto E. R., Di Cera E. Large heat capacity change in a protein-monovalent cation interaction. Biochemistry. 35:1996;8800-8804.
20. Ha J.-H., Spolar R. S., Record M. T., Jr. Role of the hydrophobic effect in stability of site-specific protein-DNA complexes. J. Mol. Biol. 209:1989;801-816.
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 non-specific 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. Harrison S. C., Aggarwal A. K. DNA recognition by proteins with the helix-turn-helix motif. Annu. Rev. Biochem. 59:1990;933-969.
23. Hawley D. K., McClure W. R. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucl. Acids Res. 11:1983;2237-2255.
24. Hedge R. S., Grossman S. R., Laimins L. A., Sigler P. B. Crystal structure at 1.7 Å of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target. Nature. 359:1992;505-512.
25. Hinz H.-J., Cossmann M., Beyreuther K. lac -repressor headpiece constitutes a reversibly unfolding domain. FEBS Letters. 129:1981;246-248.
26. Jen-Jacobson L. Structural-perturbation approaches to thermodynamics of site-specific protein-DNA interactions. Methods Enzymol. 259:1995;305-344.
27. Jen-Jacobson L., Lesser D. R., Kurpiewski M. R. DNA sequence discrimination by EcoRI endonuclease. Nucleic Acids and Molecular Biology. 1991;Springer-Verlag, Berlin/New York.
28. Jin L., Yang J., Carey J. Thermodynamics of ligand binding to trp repressor. Biochemistry. 32:1993;7302-7309.
29. Johnson M. L., Frasier S. G. Nonlinear least-squares analysis. Methods Enzymol. 117:1985;301-342.
30. 31P NMR spectra of an oligodeoxyribonucleotide duplex lac operator-repressor headpiece complex. Biochemistry. 29:1990;6578-6584.
31. Kim J. L., Nikolov D. B., Burley S. K. Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature. 365:1993;520-527.
32. Kim Y., Geiger J. H., Hahn S., Sigler P. B. Crystal structure of a yeast TBP/TATA-box complex. Nature. 365:1993;512-519.
33. Klimasauskas S., Kumar S., Roberts R. J., Cheng X. HhaI methyltransferase flips its target base out of the DNA helix. Cell. 76:1994;357-369.
34. Ladbury J. E., Sturtevant J. M., Leontis N. V. The thermodynamics of formation of a three-strand, DNA three-way junction complex. Biochemistry. 33:1994a;6828-6833.
35. Ladbury J. E., Wright J. G., Sturtevant J. M., Sigler P. B. A thermodynamic study of the trp repressor-operator interaction. J. Mol. Biol. 238:1994b;669-681.
36. Laiken S. L., Gross C. A., von Hippel P. H. Equilibrium and kinetic studies of Escherichia colilac repressor-inducer interactions. J. Mol. Biol. 66:1972;143-155.
37. 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.
38. Law S. M., Eritja R., Goodman M. F., Breslauer K. J. Spectroscopic and calorimetric characterizations of DNA duplexes containing 2-aminopurine. Biochemistry. 35:1996;12329-12337.
39. Lehming N., Sartorius J., Niemöller M., Genenger G., v. Wilcken-Bergmann B., Müller-Hill B. The interaction of the recognition helix of lac repressor with lac operator. EMBO J. 6:1987;3145-3153.
40. Lehming N., Sartorius J., Kisters-Woike B., v. Wilcken-Bergmann B., Müller-Hill B. Mutant lac repressors with new specificities hint at rules for protein-DNA recognition. EMBO J. 9:1990;615-621.
41. Lesser D. R., Kurpiewski M. R., Jen-Jacobson L. The energetic basis of specificity in the Eco RI endonuclease-DNA interaction. Science. 250:1990;776-786.
42. 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.
43. symoperators to the two sites on LacI tetramer: contributions from wrapping and looping of non-operator DNA. J. Mol. Biol. 260:1996;697-717.
44. Lewis M., Chang G., Horton N. C., Kercher M. A., Pace H. C., Schumacher M., Brennan R. G., Lu P. Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science. 271:1996;1247-1254.
45. Lin S.-Y., Riggs A. D. lac repressor binding to non-operator DNA: detailed studies and a comparison of equilibrium and rate competition methods. J. Mol. Biol. 72:1972;671-690.
46. Lin S.-Y., Riggs A. D. The general affinity of lac repressor for E. coli DNA: implications for gene regulation in procaryotes and eucaryotes. Cell. 4:1975;107-111.
47. 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.
48. Lu M., Guo Q., Marky L. A., Seeman N. C., Kallenbach N. R. Thermodynamics of DNA branching. J. Mol. Biol. 223:1992;781-789.
49. Lundbäck T., Härd T. Sequence-specific DNA-binding dominated by dehydration. Proc. Natl Acad. Sci. USA. 93:1996;4754-4759.
50. Maquat L. E., Thornton K., Reznikoff W. S. Lac promoter mutations located downstream from the transcription start site. J. Mol. Biol. 138:1980;537-549.
51. Mascotti D. P., Lohman T. M. Thermodynamics of single-stranded RNA and DNA interactions with oligolysines containing tryptophan. Effects of base composition. Biochemistry. 32:1993;10568-10579.
52. Matthews K. S. The whole lactose repressor. Science. 271:1996;1245-1246.
53. McClarin J. A., Frederick C. A., Wang B.-C., Greene P., Boyer H. W., Grable J., Rosenberg J. M. Structure of the DNA- Eco RI endonuclease recognition complex at 3 Å resolution. Science. 234:1986;1526-1541.
54. Merabet E., Ackers G. K. Calorimetric analysis of λ cI repressor binding to DNA operator sites. Biochemistry. 34:1995;8554-8563.
55. Mossing M. C., Record M. T., Jr. Thermodynamic origins of specificity in the lac repressor-operator interactions. J. Mol. Biol. 186:1985;295-305.
56. 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.
57. Mulligan M. E., McClure W. R. Analysis of the occurrence of promoter-sites in DNA. Nucl. Acids Res. 14:1986;109-126.
58. Mulligan M. E., Hawley D. K., Entriken E., McClure W. R. Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity. Nucl. Acids Res. 12:1984;789-800.
59. Murphy K. P., Gill S. J., Privalov P. L. Common features of protein unfolding and dissolution of hydrophobic compounds. Science. 247:1990;559-561.
60. Nagadoi A., Morikawa S., Nakamura H., Enari M., Kobayashi K., Yamamoto H., Sampei G., Mizobuchi K., Schumacher M. A., Brennan R. G. Structural comparison of the free and DNA-bound forms of the purine repressor DNA-binding domain. Structure. 3:1995;1217-1224.
61. Newman M., Strzelecka T., Dorner L. F., Schildkraut I., Aggarwal A. K. Structure of Bam HI endonuclease bound to DNA: partial folding and unfolding on DNA binding. Science. 269:1995;656-663.
62. Nussinov R. Some guidelines for identification of recognition sequences: regulatory sequences frequently contain (T)GTG/CAC(A), TGA/TCA and (T)CTC/GAG. Biochim. Biophys. Acta. 866:1986;93-108.
63. 8+) to the center of DNA oligomers. Biophys. J. 68:1995;634-647.
64. Otting G., Qian Y. Q., Billeter M., Müller M., Affolter M., Gehring W. J., Wüthrich K. Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution. EMBO J. 9:1990;3085-3092.
65. Petersen J. M., Skalicky J. J., Donaldson L. W., McIntosh L. P., Alber T., Graves B. J. Modulation of transcription factor Ets-1 DNA binding: DNA-induced unfolding of an alpha helix. Science. 269:1995;1866-1869.
66. Petri V., Hsieh M., Brenowitz M. Thermodynamic and kinetic characterization of the binding of the TATA binding protein to the adenovirus E4 promoter. Biochemistry. 35:1995;9977-9984.
67. Privalov P. L., Gill S. J. Stability of protein structure and hydrophobic interaction. Advan. Protein Chem. 39:1988;191-234.
68. Record M. T., Jr, Spolar R. S. Some thermodynamic principles of nonspecific and site-specific protein-DNA interactions. Revzin Arnold. Nonspecific DNA-Protein Interactions. 1990;CRC Press, Boca Raton.
69. Record M. T., Jr, Lohman T. M., deHaseth P. L. Ion effects on ligand-nucleic acid interactions. J. Mol. Biol. 107:1976;145-158.
70. Record M. T., Jr, deHaseth P. L., Lohman T. M. Interpretation of monovalent and divalent cation effects on the lac repressor-operator interaction. Biochemistry. 16:1977;4791-4796.
71. Record M. T., Jr, Mazur S. J., Melancon P., Roe J.-H., Shaner S. L., Unger L. Double helical DNA: conformations, physical properties, and interactions with ligands. Annu. Rev. Biochem. 50:1981;997-1024.
72. Record M. T., Jr, Ha J.-H., Fisher M. A. Analysis 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. 208:1991;290-343.
73. Revzin A., von Hippel P. H. Direct measurement of association constants for the binding of Escherichia colilac repressor to non-operator DNA. Biochemistry. 16:1977;4769-4776.
74. Riggs A. D., Bourgeois S., Newby R. F., Cohn M. DNA binding of the lac repressor. J. Mol. Biol. 34:1968;365-368.
75. Riggs A. D., Suzuki H., Bourgeois S. lac repressor-operator interaction. I. Equilibrium studies. J. Mol. Biol. 48:1970;67-83.
76. Rpromoter interaction: assignment of the kinetic steps corresponding to protein conformation change and DNA opening. J. Mol. Biol. 184:1985;441-453.
77. Sadler J. R., Sasmor H., Betz J. L. A perfectly symmetric lac operator binds the lac repressor very tightly. Proc. Natl Acad. Sci. USA. 80:1983;6785-6789.
78. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd Edit. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
79. Sarai A., Takeda Y. λ Repressor recognizes the approximately 2-fold symmetric half-operator sequences asymmetrically. Proc. Natl Acad. Sci. USA. 86:1989;6513-6517.
80. Sasmor H. M., Betz J. L. Symmetric lac operator derivatives: effects of half-operator sequence and spacing on repressor affinity. Gene. 89:1990;1-6.
81. Schnarr M., Maurizot J.-C. Unfolding of lac repressor and its proteolytic fragments by urea: headpieces stabilize the core within lac repressor. Biochemistry. 20:1981;6164-6169.
82. Schnarr M., Maurizot J.-C. Stability of the lac repressor headpiece against thermal denaturation and tryptic hydrolysis. Biochim. Biophys. Acta. 702:1982;155-162.
83. Schneider T. D., Stormo G. D., Gold L., Ehrenfeucht A. Information content of binding sites on nucleotide sequences. J. Mol. Biol. 188:1986;415-431.
84. Schultz S. C., Shields G. C., Steitz T. A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90° Science. 253:1991;1001-1007.
85. Schumacher M. A., Choi K. Y., Zalkin H., Brennan R. G. Crystal structure of LacI member, PurR, bound to DNA: minor groove binding by a helices. Science. 266:1994;763-770.
86. Silvaraja M., Botfield M. C., Mueller M., Jancso A., Weiss M. A. Solution structure of a POU-specific homeodomain: 3D-NMR studies of human B-cell transcription factor Oct-2. Biochemistry. 33:1994;9845-9855.
87. Simons A., Tils D., von Wilcken-Bergmann B., Müller-Hill B. Possible ideal lac operator: Escherichia colilac operator-like sequences from eukaryotic genomes lack the central G·C pair. Proc. Natl Acad. Sci. USA. 81:1984;1624-1628.
88. 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 and 3D NOE data: change of tertiary structure upon binding to the lac operator. J. Mol. Biol. 259:1996;761-773.
89. Smolarsky M., Tal M. Novel method for measuring polyuridylic acid binding to ribosomes. Biochim. Biophys. Acta. 199:1970;447-452.
90. Spolar R. S., Record M. T., Jr. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:1994;777-784.
91. Spolar R. S., Ha J.-H., Record M. T., Jr. Role of the hydrophobic effect in stability of site-specific protein-DNA complexes. Proc. Natl Acad. Sci. USA. 86:1989;8382-8385.
92. Spolar R. S., Livingstone J. R., Record M. T., Jr. Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water. Biochemistry. 31:1992;3947-3955.
93. Spronk C. A. E. M., 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;916-919.
94. Sturtevant J. M. Heat capacity and entropy changes in processes involving proteins. Proc. Natl Acad. Sci. USA. 74:1977;2236-2240.
95. Takeda Y., Sarai A., Rivera V. M. Analysis of the sequence-specific interactions between cro repressor and operator DNA by systematic base substitution experiments. Proc. Natl Acad. Sci. USA. 86:1989;439-443.
96. Takeda Y., Ross P. D., Mudd C. P. Thermodynamics of Cro protein-DNA interactions. Proc. Natl Acad. Sci. USA. 89:1992;8180-8184.
97. Tsao D. H. H., Gruschus J. M., Wang L.-H., Nirenberg M., Ferretti J. A. Elongation of helix III of the NK-2 homeodomain upon binding to DNA: a secondary structure study by NMR. Biochemistry. 33:1994;15053-15060.
98. van Tilborg M. A., Bonvin A. M., Hard K., Davis A. L., Maler B., Boelens R., Yamamoto K. R., Kaptein R. Structure refinement of the glucocorticoid receptor-DNA binding domain from NMR data by relaxation matrix calculations. J. Mol. Biol. 247:1995;689-700.
99. Wade-Jardetzky N., Bray R. P., Conover W. W., Jardetzky O., Geisler N., Weber K. Differential mobility of the N-terminal headpiece in the lac -repressor protein. J. Mol. Biol. 128:1979;259-264.
100. Wemmer D., Ribeiro A. A., Bray R. P., Wade-Jardetzky N. G., Jardetzky O. High resolution nuclear magnetic resonance studies of the lac repressor. 3. Unfolding of the lac repressor headpiece. Biochemistry. 20:1981;829-833.
101. Werner M. H., Huth J. R., Gronenborn A. M., Clore G. M. Molecular basis of human 46X,Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex. Cell. 81:1995;705-714.
102. 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;3845-3858.
103. 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.
104. Yang W., Steitz T. A. Crystal structure of the site-specific recombinase γδ resolvase complexed with a 34 bp cleavage site. Cell. 82:1995;193-207.
105. Zhang X., Gottlieb P. A. Thermodynamic and alkylation interference analysis of the lac repressor-operator substituted with the analogue 7-deazaguanine. Biochemistry. 32:1993;11374-11384.
106. Zhang W., Bond J. P., Anderson C. F., Lohman T. M., Record M. T., Jr. Large electrostatic differences in the binding energetics of a cationic peptide to oligomeric and polymeric DNA. Proc. Natl Acad. Sci. USA. 93:1996;2511-2516.