High-resolution specificity from DNA sequencing highlights alternative modes of lac repressor binding

Genetics

Volumn 198, Issue 3, 2014, Pages 1329-1343

  Zuo, Zheng ^a   Stormo, Gary D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LAC REPRESSOR; MONOMER; ESCHERICHIA COLI PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; DNA SEQUENCE; LACTOSE OPERON; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERATOR GENE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; BIOLOGICAL MODEL; CONFORMATION; ESCHERICHIA COLI; GENE LIBRARY; GENETICS; METABOLISM; MOLECULAR GENETICS; THERMODYNAMICS;

BASE SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE LIBRARY; LAC REPRESSORS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OPERATOR REGIONS, GENETIC; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; THERMODYNAMICS;

EID: 84964312637     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.170100     Document Type: Article

References (74)

1. Badis, G., M. F. Berger, A. A. Philippakis, S. Talukder, A. R. Gehrke et al., 2009 Diversity and complexity in DNA recognition by transcription factors. Science 324: 1720-1723.
2. Bell, C. E., and M. Lewis, 2001 Crystallographic analysis of Lac repressor bound to natural operator O1. J. Mol. Biol. 312: 921-926.
3. Benos, P. V., M. L. Bulyk, and G. D. Stormo, 2002 Additivity in protein-DNA interactions: How good an approximation is it? Nucleic Acids Res. 30: 4442-4451.
4. Berger, M. F., A. A. Philippakis, A. M. Qureshi, F. S. He, P. W. Estep, 3rd et al., 2006 Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat. Biotechnol. 24: 1429-1435.
5. Betz, J. L., H. M. Sasmor, F. Buck, M. Y. Insley, and M. H. Caruthers, 1986 Base substitution mutants of the lac operator: in vivo and in vitro affinities for lac repressor. Gene 50: 123-132.
6. Boedicker, J. Q., H. G. Garcia, and R. Phillips, 2013 Theoretical and experimental dissection of DNA loop-mediated repression. Phys. Rev. Lett. 110: 018101.
7. Bulyk, M. L., P. L. Johnson, and G. M. Church, 2002 Nucleotides of transcription factor binding sites exert interdependent effects on the binding affinities of transcription factors. Nucleic Acids Res. 30: 1255-1261.
8. Christensen, R. G., A. Gupta, Z. Zuo, L. A. Schriefer, S. A. Wolfe et al., 2011 A modified bacterial one-hybrid system yields improved quantitative models of transcription factor specificity. Nucleic Acids Res. 39: e83.
9. Colasanti, A. V., M. A. Grosner, P. J. Perez, N. Clauvelin, X. J. Lu et al., 2013 Weak operator binding enhances simulated lac repressor-mediated DNA looping. Biopolymers 99: 1070-1081.
10. Daber, R., and M. Lewis, 2009 Towards evolving a better repressor. Protein Eng. Des. Sel. 22: 673-683.
11. Falcon, C. M., and K. S. Matthews, 2001 Engineered disulfide linking the hinge regions within lactose repressor dimer increases operator affinity, decreases sequence selectivity, and alters allostery. Biochemistry 40: 15650-15659.
12. Fields, D. S., and G. D. Stormo, 1994 Quantitative DNA sequencing to determine the relative protein-DNA binding constants to multiple DNA sequences. Anal. Biochem. 219: 230-239.
13. Fields, D. S., Y. He, A. Y. Al-Uzri, and G. D. Stormo, 1997 Quantitative specificity of the Mnt repressor. J. Mol. Biol. 271: 178-194.
14. Foat, B. C., A. V. Morozov, and H. J. Bussemaker, 2006 Statistical mechanical modeling of genome-wide transcription factor occupancy data by Matrix-REDUCE. Bioinformatics 22: e141-e149.
15. Frank, D. E., R. M. Saecker, J. P. Bond, M. W. Capp, O. V. Tsodikov et al., 1997 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: 1186-1206.
16. Gilbert, W., J. Gralla, J. Majors, and A. Maxam, 1975 Lactose operator sequences and the action of lac repressors, pp. 193-210 in Protein-Ligand Interactions, edited by B. Sund. De Gruyter, Berlin/ New York.
17. Glasfeld, A., A. N. Koehler, M. A. Schumacher, and R. G. Brennan, 1999 The role of lysine 55 in determining the specificity of the purine repressor for its operators through minor groove interactions. J. Mol. Biol. 291: 347-361.
18. Goeddel, D. V., D. G. Yansura, and M. H. Caruthers, 1978 How lac repressor recognizes lac operator. Proc. Natl. Acad. Sci. USA 75: 3578-3582.
19. Gordan, R., N. Shen, I. Dror, T. Zhou, J. Horton et al., 2013 Genomic regions flanking E-box binding sites influence DNA binding specificity of bHLH transcription factors through DNA shape. Cell Rep. 3: 1093-1104.
20. Gupta, A., R. G. Christensen, H. A. Bell, M. Goodwin, R. Y. Patel et al., 2014 An improved predictive recognition model for Cys (2)-His(2) zinc finger proteins. Nucleic Acids Res. 42: 4800-4812.
21. Hammar, P., P. Leroy, A. Mahmutovic, E. G. Marklund, O. G. Berg et al., 2012 The lac repressor displays facilitated diffusion in living cells. Science 336: 1595-1598.
22. Hammar, P., M. Wallden, D. Fange, F. Persson, O. Baltekin et al., 2014 Direct measurement of transcription factor dissociation excludes a simple operator occupancy model for gene regulation. Nat. Genet. 46: 405-408.
23. Jacob, F., and J. Monod, 1961 Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3: 318-356.
24. Jolma, A., T. Kivioja, J. Toivonen, L. Cheng, G. Wei et al., 2010 Multiplexed massively parallel SELEX for characterization of human transcription factor binding specificities. Genome Res. 20: 861-873.
25. Jolma, A., J. Yan, T. Whitington, J. Toivonen, K. R. Nitta et al., 2013 DNA-binding specificities of human transcription factors. Cell 152: 327-339.
26. Kalodimos, C. G., A. M. Bonvin, R. K. Salinas, R. Wechselberger, R. Boelens et al., 2002 Plasticity in protein-DNA recognition: lac repressor interacts with its natural operator 01 through alternative conformations of its DNA-binding domain. EMBO J. 21: 2866-2876.
27. Kalodimos, C. G., N. Biris, A. M. Bonvin, M. M. Levandoski, M. Guennuegues et al., 2004a Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes. Science 305: 386-389.
28. Kalodimos, C. G., R. Boelens, and R. Kaptein, 2004b Toward an integrated model of protein-DNA recognition as inferred from NMR studies on the Lac repressor system. Chem. Rev. 104: 3567-3586.
29. Kim, J. B., G. D. Spotts, Y. D. Halvorsen, H. M. Shih, T. Ellenberger et al., 1995 Dual DNA binding specificity of ADD1/SREBP1 controlled by a single amino acid in the basic helix-loop-helix domain. Mol. Cell. Biol. 15: 2582-2588.
30. Lehming, N., J. Sartorius, B. Kisters-Woike, B. von Wilcken-Bergmann, and B. Muller-Hill, 1990 Mutant lac repressors with new specificities hint at rules for protein-DNA recognition. EMBO J. 9: 615-621.
31. Lewis, M., 2005 The lac repressor. C. R. Biol. 328: 521-548.
32. Liu, J., and G. D. Stormo, 2005a Combining SELEX with quantitative assays to rapidly obtain accurate models of protein-DNA interactions. Nucleic Acids Res. 33: e141.
33. Liu, J., and G. D. Stormo, 2005b Quantitative analysis of EGR proteins binding to DNA: assessing additivity in both the binding site and the protein. BMC Bioinformatics 6: 176.
34. Maerkl, S. J., and S. R. Quake, 2007 A systems approach to measuring the binding energy landscapes of transcription factors. Science 315: 233-237.
35. Man, T. K., and G. D. Stormo, 2001 Non-independence of Mnt repressor-operator interaction determined by a new quantitative multiple fluorescence relative affinity (QuMFRA) assay. Nucleic Acids Res. 29: 2471-2478.
36. Man, T. K., J. S. Yang, and G. D. Stormo, 2004 Quantitative modeling of DNA-protein interactions: effects of amino acid substitutions on binding specificity of the Mnt repressor. Nucleic Acids Res. 32: 4026-4032.
37. Markiewicz, P., L. G. Kleina, C. Cruz, S. Ehret, and J. H. Miller, 1994 Genetic studies of the lac repressor. XIV. Analysis of 4000 altered Escherichia coli lac repressors reveals essential and non-essential residues, as well as “spacers” which do not require a specific sequence. J. Mol. Biol. 240: 421-433.
38. Mathelier, A., and W. W. Wasserman, 2013 The next generation of transcription factor binding site prediction. PLoS Comput. Biol. 9: e1003214.
39. Mathelier, A., X. Zhao, A. W. Zhang, F. Parcy, R. Worsley-Hunt et al., 2014 JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 42: D142-D147.
40. Meng, X., M. H. Brodsky, and S. A. Wolfe, 2005 A bacterial onehybrid system for determining the DNA-binding specificity of transcription factors. Nat. Biotechnol. 23: 988-994.
41. Milk, L., R. Daber, and M. Lewis, 2010 Functional rules for lac repressor-operator associations and implications for proteinDNA interactions. Protein Sci. 19: 1162-1172.
42. Mossing, M. C., and M. T. Record, Jr.., 1985 Thermodynamic origins of specificity in the lac repressor-operator interaction. Adaptability in the recognition of mutant operator sites. J. Mol. Biol. 186: 295-305.
43. Motlhabi, L. M., and G. D. Stormo, 2011 Assessing the effects of symmetry on motif discovery and modeling. PLoS ONE 6: e24908.
44. Ng, C. K., N. X. Li, S. Chee, S. Prabhakar, P. R. Kolatkar et al., 2012 Deciphering the Sox-Oct partner code by quantitative cooperativity measurements. Nucleic Acids Res. 40: 4933-4941.
45. Novichkov, P. S., A. E. Kazakov, D. A. Ravcheev, S. A. Leyn, G. Y. Kovaleva et al., 2013 RegPrecise 3.0-a resource for genomescale exploration of transcriptional regulation in bacteria. BMC Genomics 14: 745.
46. Noyes, M. B., R. G. Christensen, A. Wakabayashi, G. D. Stormo, M. H. Brodsky et al., 2008 Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133: 1277-1289.
47. Nutiu, R., R. C. Friedman, S. Luo, I. Khrebtukova, D. Silva et al., 2011 Direct measurement of DNA affinity landscapes on a high-throughput sequencing instrument. Nat. Biotechnol. 29: 659-664.
48. Orenstein, Y., and R. Shamir, 2014 A comparative analysis of transcription factor binding models learned from PBM, HT-SELEX and ChIP data. Nucleic Acids Res. 42: e63.
49. Parraga, A., L. Bellsolell, A. R. Ferre-D’Amare, and S. K. Burley, 1998 Co-crystal structure of sterol regulatory element binding protein 1a at 2.3 A resolution. Structure 6: 661-672.
50. Royer, C. A., A. E. Chakerian, and K. S. Matthews, 1990 Macromolecular binding equilibria in the lac repressor system: studies using high-pressure fluorescence spectroscopy. Biochemistry 29: 4959-4966.
51. Sadler, J. R., H. Sasmor, and J. L. Betz, 1983 A perfectly symmetric lac operator binds the lac repressor very tightly. Proc. Natl. Acad. Sci. USA 80: 6785-6789.
52. Sarai, A., and Y. Takeda, 1989 Lambda repressor recognizes the approximately 2-fold symmetric half-operator sequences asymmetrically. Proc. Natl. Acad. Sci. USA 86: 6513-6517.
53. Sartorius, J., N. Lehming, B. Kisters, B. von Wilcken-Bergmann, and B. Muller-Hill, 1989 Lac repressor mutants with double or triple exchanges in the recognition helix bind specifically to lac operator variants with multiple exchanges. EMBO J. 8: 1265-1270.
54. Sasmor, H. M., and J. L. Betz, 1990 Symmetric lac operator derivatives: effects of half-operator sequence and spacing on repressor affinity. Gene 89: 1-6.
55. Slattery, M., T. Riley, P. Liu, N. Abe, P. Gomez-Alcala et al., 2011 Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147: 1270-1282.
56. Spronk, C. A., G. E. Folkers, A. M. Noordman, R. Wechselberger, N. van den Brink et al., 1999 Hinge-helix formation and DNA bending in various lac repressor-operator complexes. EMBO J. 18: 6472-6480.
57. Stormo, G. D., 2000 DNA binding sites: representation and discovery. Bioinformatics 16: 16-23.
58. Stormo, G. D., 2013 Modeling the specificity of protein-DNA interactions. Quant. Biol. 1: 115-130.
59. Stormo, G. D., and D. S. Fields, 1998 Specificity, free energy and information content in protein-DNA interactions. Trends Biochem. Sci. 23: 109-113.
60. Stormo, G. D., and M. Yoshioka, 1991 Specificity of the Mnt protein determined by binding to randomized operators. Proc. Natl. Acad. Sci. USA 88: 5699-5703.
61. Stormo, G. D., and Y. Zhao, 2007 Putting numbers on the network connections. BioEssays 29: 717-721.
62. Stormo, G. D., and Y. Zhao, 2010 Determining the specificity of protein-DNA interactions. Nat. Rev. Genet. 11: 751-760.
63. Stormo, G. D., T. D. Schneider, and L. Gold, 1986 Quantitative analysis of the relationship between nucleotide sequence and functional activity. Nucleic Acids Res. 14: 6661-6679.
64. Stormo, G. D., S. Strobl, M. Yoshioka, and J. S. Lee, 1993 Specificity of the Mnt protein. Independent effects of mutations at different positions in the operator. J. Mol. Biol. 229: 821-826.
65. Takeda, Y., A. Sarai, and V. M. Rivera, 1989 Analysis of the sequence-specific interactions between Cro repressor and operator DNA by systematic base substitution experiments. Proc. Natl. Acad. Sci. USA 86: 439-443.
66. Von Hippel, P. H., 1979 On the molecular bases of the specificity of interaction of transcriptional proteins with genome DNA, pp. 279-347 in Biological Regulation and Development, edited by R. F. Goldberger. Plenum, New York.
67. von Hippel, P. H., and O. G. Berg, 1986 On the specificity of DNA-protein interactions. Proc. Natl. Acad. Sci. USA 83: 1608-1612.
68. Warren, C. L., N. C. Kratochvil, K. E. Hauschild, S. Foister, M. L. Brezinski et al., 2006 Defining the sequence-recognition profile of DNA-binding molecules. Proc. Natl. Acad. Sci. USA 103: 867-872.
69. Weirauch, M. T., A. Cote, R. Norel, M. Annala, Y. Zhao et al., 2013 Evaluation of methods for modeling transcription factor sequence specificity. Nat. Biotechnol. 31: 126-134.
70. Wong, D., A. Teixeira, S. Oikonomopoulos, P. Humburg, I. N. Lone et al., 2011 Extensive characterization of NF-kappaB binding uncovers non-canonical motifs and advances the interpretation of genetic functional traits. Genome Biol. 12: R70.
71. Zhao, Y., and G. D. Stormo, 2011 Quantitative analysis demonstrates most transcription factors require only simple models of specificity. Nat. Biotechnol. 29: 480-483.
72. Zhao, Y., D. Granas, and G. D. Stormo, 2009 Inferring binding energies from selected binding sites. PLoS Comput. Biol. 5: e1000590.
73. Zhao, Y., S. Ruan, M. Pandey, and G. D. Stormo, 2012 Improved models for transcription factor binding site identification using nonindependent interactions. Genetics 191: 781-790.
74. Zykovich, A., I. Korf, and D. J. Segal, 2009 Bind-n-Seq: highthroughput analysis of in vitro protein-DNA interactions using massively parallel sequencing. Nucleic Acids Res. 37: e151.