Accurate Genetic Switch in Escherichia coli: Novel Mechanism of Regulation by Co-repressor

Journal of Molecular Biology

Volumn 377, Issue 4, 2008, Pages 1002-1014

  Tabaka, Marcin ^a   Cybulski, Olgierd ^a   Hołyst, Robert ^a,b  

^a POLISH ACADEMY OF SCIENCES   (Poland)

^b CARDINAL STEFAN WYSZY SKI UNIVERSITY   (Poland)

Author keywords

genetic switch; repressor control; transcriptional regulation; trp operon

Indexed keywords

TRYPTOPHAN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE SWITCHING; GENETIC TRANSCRIPTION; NONHUMAN; OPERON; PRIORITY JOURNAL;

ESCHERICHIA COLI;

EID: 40849137415     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.01.060     Document Type: Article

References (73)

1. Khodursky A.B., Peter B.J., Cozzarelli N.R., Botstein D., Brown P.O., and Yanofsky C. DNA microarray analysis of gene expression in response to physiological and genetic changes that affect tryptophan metabolism in Escherichia coli. Proc. Natl Acad. Sci. USA 97 (2000) 12170-12175
2. Yanofsky C., and Horn V. Role of regulatory features of the trp operon of Escherichia coli in mediating a response to a nutritional shift. J. Bacteriol. 176 (1994) 6245-6254
3. Yanofsky C., and Crawford I.P. The tryptophan operon. In: Neidhart F.C. (Ed). Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology (1987), ASM Press, Washington, DC 1454-1472
4. Yanofsky C., Kelley R.L., and Horn V. Repression is relieved before attenuation in the trp operon of Escherichia coli as tryptophan starvation becomes increasingly severe. J. Bacteriol. 158 (1984) 1018-1024
5. Santillan M., and Mackey M.C. Dynamic regulation of the tryptophan operon: a modeling study and comparison with experimental data. Proc. Natl Acad. Sci. USA 98 (2001) 1364-1369
6. Santillan M., and Mackey M.C. Dynamic behavior in mathematical models of the tryptophan operon. Chaos 11 (2001) 261-268
7. Santillan M., and Zeron E.S. Dynamic influence of feedback enzyme inhibition and transcription attenuation on the tryptophan operon response to nutritional shifts. J. Theor. Biol. 231 (2004) 287-298
8. Bhartiya S., Rawool S., and Venkatesh K.V. Dynamic model of Escherichia coli tryptophan operon shows an optimal structural design. Eur. J. Biochem. 270 (2003) 2644-2651
9. Drozdov-Tikhomirov L.N., and Scoorida G.I. Mathematical model for the kinetic of tryptophan synthesis and excretion by the cell of E. coli. Mol. Biol. (Moscow) 11 (1977) 843-853
10. Bliss R.D., Painter P.R., and Marr A.G. Role of feedback inhibition in stabilizing the classical operon. J. Theor. Biol. 97 (1982) 177-193
11. Sinha S. Theoretical study of tryptophan operon: application in microbial technology. Biotechnol. Bioeng. 31 (1986) 117-124
12. Koh B.T., and Yap M.G. A simple genetically structured model of trp repressor-operator interactions. Biotechnol. Bioeng. 41 (1993) 707-714
13. Koh B.T., Tan R.B.H., and Yap M.G.S. Genetically structured mathematical modeling of trp attenuator mechanism. Biotechnol. Bioeng. 58 (1998) 502-509
14. Xiu Z.L., Zeng A.P., and Deckwer W.D. Model analysis concerning the effects of growth rate and intracellular tryptophan level on the stability and dynamics of tryptophan biosynthesis in bacteria. J. Biotechnol. 58 (1997) 125-140
15. Rose J.K., and Yanofsky C. Interaction of the operator of the tryptophan operon with repressor. Proc. Natl Acad. Sci. USA 71 (1974) 3134-3138
16. Sigler P.B. The molecular mechanism of trp repression. In: McKnight S.L., and Yamamoto K.R. (Eds). Transcriptional Regulation (1992), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 475-498
17. Jackson E.N., and Yanofsky C. The region between the operator and first structural gene of the tryptophan operon of Escherichia coli may have a regulatory function. J. Mol. Biol. 76 (1973) 89-101
18. Yanofsky C. Attenuation in the control of expression of bacterial operons. Nature 289 (1981) 751-758
19. Squires C.L., Lee F.D., and Yanofsky C. Interaction of the trp repressor and RNA polymerase with the trp operon. J. Mol. Biol. 92 (1975) 93-111
20. Gunsalus R.P., and Yanofsky C. Nucleotide sequence and expression of Escherichia coli trpR, the structural gene for the trp aporepressor. Proc. Natl Acad. Sci. USA 77 (1980) 7117-7121
21. Joachimiak A., Kelley R.L., Gunsalus R.P., Yanofsky C., and Sigler P.B. Purification and characterization of trp aporepressor. Proc. Natl Acad. Sci. USA 80 (1983) 668-672
22. Somerville R. The Trp repressor, a ligand-activated regulatory protein. Prog. Nucleic Acid Res. Mol. Biol. 42 (1992) 1-38
23. Arvidson D.N., Bruce C., and Gunsalus R.P. Interaction of the Escherichia coli trp aporepressor with its ligand, l-tryptophan. J. Biol. Chem. 261 (1986) 238-243
24. Lane A.N. The interaction of the trp repressor from Escherichia coli with l-tryptophan and indole propanoic acid. Eur. J. Biochem. 157 (1986) 405-413
25. Marmorstein R.Q., Joachimiak A., Sprinzl M., and Sigler P.B. The structural basis for the interaction between l-tryptophan and the Escherichia coli trp aporepressor. J. Biol. Chem. 262 (1987) 4922-4927
26. Jin L., Yang J., and Carey J. Thermodynamics of ligand binding to trp repressor. Biochemistry 32 (1993) 7302-7309
27. Schevitz R.W., Otwinowski Z., Joachimiak A., Lawson C.L., and Sigler P.B. The three-dimensional structure of trp repressor. Nature 317 (1985) 782-786
28. Zhang R.G., Joachimiak A., Lawson C.L., Schevitz R.W., Otwinowski Z., and Sigler P.B. The crystal structure of trp aporepressor at 1.8 Å shows how binding tryptophan enhances DNA affinity. Nature 327 (1987) 591-597
29. Lawson C.L., Zhang R.G., Schevitz R.W., Otwinowski Z., Joachimiak A., and Sigler P.B. Flexibility of the DNA-binding domains of trp repressor. Proteins 3 (1988) 18-31
30. Arrowsmith C., Pachter R., Altman R., and Jardetzky O. The solution structures of Escherichia coli trp repressor and trp aporepressor at an intermediate resolution. Eur. J. Biochem. 202 (1991) 53-66
31. Zhao D., Arrowsmith C.H., Jia X., and Jardetzky O. Refined solution structures of the Escherichia coli trp holo- and aporepressor. J. Mol. Biol. 229 (1993) 735-746
32. 15N-labelled protein. Eur. J. Biochem. 225 (1994) 601-608
33. Otwinowski Z., Schevitz R.W., Zhang R.G., Lawson C.L., Joachimiak A., Marmorstein R.Q., et al. Crystal structure of trp repressor/operator complex at atomic resolution. Nature 335 (1988) 321-329
34. Zhang H., Zhao D., Revington M., Lee W., Jia X., Arrowsmith C., and Jardetzky O. The solution structures of the trp repressor-operator DNA complex. J. Mol. Biol. 238 (1994) 592-614
35. Lawson C.L., and Carey J. Tandem binding in crystals of a trp repressor/operator half-site complex. Nature 366 (1993) 178-182
36. Kumamoto A.A., Miller W.G., and Gunsalus R.P. Escherichia coli tryptophan repressor binds multiple sites within the aroH and trp operators. Genes Dev. 1 (1987) 556-564
37. Liu Y.C., and Matthews K.S. Dependence of trp repressor-operator affinity, stoichiometry, and apparent cooperativity on DNA sequence and size. J. Biol. Chem. 268 (1993) 23239-23249
38. Yang J., Gunasekera A., Lavoie T.A., Jin L.H., Lewis D.E.A., and Carey J. In vivo and in vitro studies of TrpR-DNA interactions. J. Mol. Biol. 258 (1996) 37-52
39. Joachimiak A., Haran T.E., and Sigler P.B. Mutagenesis supports water mediated recognition in the trp repressor-operator system. EMBO J. 13 (1994) 367-372
40. Brown M.P., Grillo A.O., Boyer M., and Royer C.A. Probing the role of water in the tryptophan repressor-operator complex. Protein Sci. 8 (1999) 1276-1285
41. Bareket-Samish A., Cohen I., and Haran T.E. Repressor assembly at trp binding sites is dependent on the identity of the intervening dinucleotide between the binding half sites. J. Mol. Biol. 267 (1997) 103-117
42. Bareket-Samish A., Cohen I., and Haran T.E. Direct versus indirect readout in the interaction of the trp repressor with non-canonical binding sites. J. Mol. Biol. 277 (1998) 1071-1080
43. Haran T.E., Joachimiak A., and Sigler P.B. The DNA target of the trp repressor. EMBO J. 11 (1992) 3021-3030
44. Liu Y.C., and Matthews K.S. Trp repressor mutations alter DNA complex stoichiometry. J. Biol. Chem. 269 (1994) 1692-1698
45. Jeeves M., Evans P.D., Parslow R.A., Jaseja M., and Hyde E.I. Studies of the Escherichia coli Trp repressor binding to its five operators and to variant operator sequences. Eur. J. Biochem. 265 (1999) 919-928
46. Grillo A.O., Brown M.P., and Royer C.A. Probing the physical basis for trp repressor-operator recognition. J. Mol. Biol. 287 (1999) 539-554
47. Hurlburt B.K., and Yanofsky C. Enhanced operator binding by trp superrepressors of Escherichia coli. J. Biol. Chem. 265 (1990) 7853-7858
48. Finucane M.D., and Jardetzky O. Surface plasmon resonance studies of wild-type and AV77 tryptophan repressor resolve ambiguities in superrepressor activity. Protein Sci. 12 (2003) 1613-1620
49. Chou W.Y., Bieber C., and Matthews K.S. Tryptophan and 8-anilino-1-naphthalenesulfonate compete for binding to trp repressor. J. Biol. Chem. 264 (1989) 18309-18313
50. Hurlburt B.K., and Yanofsky C. trp repressor/trp operator interaction. Equilibrium and kinetic analysis of complex formation and stability. J. Biol. Chem. 267 (1992) 16783-16789
51. 15N]-l-tryptophan. J. Biomol. NMR 5 (1995) 367-375
52. Gillespie D.T. A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J. Comput. Phys. 22 (1976) 403-434
53. van Kampen N.G. Stochastic processes in physics and chemistry (1997), Elsevier, Amsterdam
54. Gillespie D.T. A rigorous derivation of the chemical master equation. Phys. A 188 (1992) 404-425
55. Hurlburt B.K., and Yanofsky C. Analysis of heterodimer formation by the Escherichia coli trp repressor. J. Biol. Chem. 268 (1993) 14794-14798
56. Reedstrom R.J., Brown M.P., Grillo A., Roen D., and Royer C.A. Affinity and specificity of trp repressor-DNA interactions studied with fluorescent oligonucleotides. J. Mol. Biol. 273 (1997) 572-585
57. Carey J. Gel retardation at low pH resolves trp repressor-DNA complexes for quantitative study. Proc. Natl Acad. Sci. USA 85 (1988) 975-979
58. Czernik P.J., Shin D.S., and Hurlburt B.K. Functional selection and characterization of DNA binding sites for trp repressor of Escherichia coli. J. Biol. Chem. 269 (1994) 27869-27875
59. Klig L.S., Crawford I.P., and Yanofsky C. Analysis of trp repressor-operator interaction by filter binding. Nucleic Acids Res. 15 (1987) 5339-5351
60. Gunsalus R.P., Miguel A.G., and Gunsalus G.L. Intracellular Trp repressor levels in Escherichia coli. J. Bacteriol. 167 (1986) 272-278
61. Gibson M.A., and Bruck J. Efficient exact stochastic simulation of chemical systems with many species and many channels. J. Phys. Chem. A 104 (2000) 1876-1889
62. Chatterjee S., Zhou Y.N., Roy S., and Adhya S. Interaction of Gal repressor with inducer and operator: induction of gal transcription from repressor-bound DNA. Proc. Natl Acad. Sci. USA 94 (1997) 2957-2962
63. Swint-Kruse L., Zhan H., and Matthews K.S. Integrated insights from simulation, experiment, and mutational analysis yield new details of LacI function. Biochemistry 44 (2005) 11201-11213
64. van Zon J.S., Morelli M.J., Tǎnase-Nicola S., and ten Wolde P.R. Diffusion of transcription factors can drastically enhance the noise in gene expression. Biophys. J. 91 (2006) 4350-4367
65. Schmitt T.H., Zheng Z., and Jardetzky O. Dynamics of tryptophan binding to Escherichia coli Trp repressor wild type and AV77 mutant: an NMR study. Biochemistry 34 (1995) 13183-13189
66. Jardetzky O., and Finucane M.D. Tandem interactions in the trp repressor system may regulate binding to operator DNA. In: Puglisi J.D. (Ed). Structure and Biophysics-New Technologies for Current Challenges in Biology and Beyond (2007), Springer Netherlands, Dordrecht, the Netherlands 49-64
67. Sclavi B., Zaychikov E., Rogozina A., Walther F., Buckle M., and Heumann H. Real-time characterization of intermediates in the pathway to open complex formation by Escherichia coli RNA polymerase at the T7A1 promoter. Proc. Natl Acad. Sci. USA 102 (2005) 4706-4711
68. Baker R., and Yanofsky C. Transcription initiation frequency and translational yield for the tryptophan operon of Escherichia coli. J. Mol. Biol. 69 (1972) 89-102
69. McClure W.R. Mechanism and control of transcription initiation in prokaryotes. Annu. Rev. Biochem. 54 (1985) 171-204
70. 70), promoters, and the kinetics of the steps of transcription initiation. In: Neidhart F.C. (Ed). Escherichia coli and Salmonella thyphymurium: Cellular and Molecular Biology (1996), ASM Press, Washington, DC 792-821
71. Mulligan M.E., Hawley D.K., Entriken R., and McClure W.R. Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity. Nucleic Acids Res. 12 (1984) 789-800
72. Bliss R.D. A specific method for determination of free tryptophan and endogenous tryptophan in Escherichia coli. Anal. Biochem. 93 (1979) 390-398
73. Bremer H., Dennis P., and Ehrenberg M. Free RNA polymerase and modeling global transcription in Escherichia coli. Biochimie 85 (2003) 597-609