Design principles for regulator gene expression in a repressible gene circuit

Journal of Molecular Biology

Volumn 332, Issue 4, 2003, Pages 861-876

  Wall, Michael E ^a   Hlavacek, William S ^b   Savageau, Michael A ^c,d  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d University of California   (United States)

Author keywords

Autoregulation; Design principles; Gene regulation; Mathematical model; Repression

Indexed keywords

REGULATOR PROTEIN;

ARTICLE; AUTOREGULATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE REPRESSION; GENETIC ENGINEERING; GENETIC LINKAGE; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THEORETICAL MODEL;

EID: 0041825399     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00948-3     Document Type: Article

References (79)

1. Somerville R. The Trp repressor, a ligand-activated regulatory protein. Prog. Nucl. Acid Res. Mol. Biol. 42:1992;1-38.
2. Yanofsky C., Crawford I.P. The tryptophan operon. Neidhardt F.C. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. 1st edit. 1987;1453 American Society for Microbiology, Washington, DC.
3. Jacob F., Monod J. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3:1961;318-356.
4. Goldberger R.F. Autogenous regulation of gene expression. Science. 183:1974;810-816.
5. Maloy S., Stewart V. Autogenous regulation of gene expression. J. Bacteriol. 175:1993;307-316.
6. Hlavacek W.S., Savageau M.A. Rules for coupled expression of regulator and effector genes in inducible circuits. J. Mol. Biol. 255:1996;121-139.
7. Klig L.S., Carey J., Yanofsky C. trp repressor interactions with the trp aroH and trpR operators. Comparison of repressor binding in vitro and repression in vivo. J. Mol. Biol. 202:1988;769-777.
8. Kölling R., Lother H. AsnC: an autogenously regulated activator of asparagine synthetase A transcription in Escherichia coli. J. Bacteriol. 164:1985;310-315.
9. de Wind N., de Jong M., Meijer M., Stuitje A.R. Site-directed mutagenesis of the Escherichia coli chromosome near oriC: identification and characterization of asnC, a regulatory element in E. coli asparagine metabolism. Nucl. Acids Res. 13:1985;8797-8811.
10. Savageau M.A. Are there rules governing patterns of gene regulation? Goodwin B.C., Saunders P.T. Theoretical Biology: Epigenetic and Evolutionary Order from Complex Systems. 1989;42-66 Edinburgh University Press, Edinburgh.
11. Neidhardt F.C., Savageau M.A. Regulation beyond the operon. Neidhardt F.C. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd edit. 1996;1310-1324 American Society for Microbiology, Washington, DC.
12. Reitzer L.J. Ammonia assimilation and the biosynthesis of glutamine, glutamate, aspartate, asparagine, L-alanine, and D-alanine. Neidhardt F.C. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd edit. 1996;391-407 American Society for Microbiology, Washington, DC.
13. Savageau M.A. Significance of autogenously regulated and constitutive synthesis of regulatory proteins in repressible biosynthetic systems. Nature. 258:1975;208-214.
14. Savageau M.A. Biochemical Systems Analysis: A Study of Function and Design in Molecular Biology. 1976;Addison-Wesley, Reading, MA.
15. Savageau M.A. Autogenous and classical regulation of gene expression: a general theory and experimental evidence. Goldberger R.F. Biological Regulation and Development. vol. 1:1979;57-108 Plenum, New York.
16. Hlavacek W.S., Savageau M.A. Completely uncoupled and perfectly coupled gene expression in repressible systems. J. Mol. Biol. 266:1997;538-558.
17. Hlavacek W.S., Savageau M.A. Method for determining natural design principles of biological control circuits. J. Intell. Fuzzy Syst. 6:1998;147-160.
18. Savageau M.A. A theory of alternative designs for biochemical control systems. Biomed. Biochim. Acta. 44:1985;875-880.
19. Savageau M.A. Design principles for elementary gene circuits: elements, methods and examples. Chaos. 11:2001;142-159.
20. Jacob F. Evolution and tinkering. Science. 196:1977;1161-1166.
21. Jacob F. The Possible and the Actual. 1982;University of Washington Press, Seattle, WA.
22. Savageau M.A. Demand theory of gene regulation. I. Quantitative development of the theory. Genetics. 149:1998;1665-1676.
23. Hlavacek W.S., Savageau M.A. Subunit structure of regulator proteins influences the design of gene circuitry: analysis of perfectly coupled and completely uncoupled circuits. J. Mol. Biol. 248:1995;739-755.
24. Savageau M.A. Biochemical systems analysis. II. The steady-state solutions for an n-pool system using a power-law approximation. J. Theor. Biol. 25:1969;370-379.
25. Savageau M.A. Concepts relating the behavior of biochemical systems to their underlying molecular properties. Arch. Biochem. Biophys. 145:1971;612-621.
26. Gantmacher F.R. Applications of the Theory of Matrices. 1959;Interscience Publishers, New York.
27. Lyapunov A.M. The General Problem of the Stability of Motion. 1992;Taylor & Francis, London.
28. Liénard A., Chipart M.H. Sur le signe de la partie réelle des racines d'une équation algébrique. J. Math. Pures Appl. 10:1914;291-346.
29. Hurwitz A. Über die Bedingungen, unter welchen eine Gleichung nur Wurzeln mit negativen reellen Thielen besitzt. Math. Ann. 46:1895;273-284.
30. Savageau M.A. Coupled circuits of gene regulation. Calendar R., Gold L. Sequence Specificity in Transcription and Translation. 1985;633-642 Alan R. Liss, New York.
31. Little J.W., Shepley D.P., Wert D.W. Robustness of a gene regulatory circuit. EMBO J. 18:1999;4299-4307.
32. Shiraishi F., Savageau M.A. The tricarboxylic acid cycle in Dictyostelium discoideum. II. Evaluation of model consistency and robustness. J. Biol. Chem. 267:1992;22919-22925.
33. Savageau M.A., Sorribas A. Constraints among molecular and systemic properties: implications for physiological genetics. J. Theor. Biol. 141:1989;93-115.
34. Hindmarsh A.C. ODEPACK: A systematized collection of ODE solvers. Stepleman R.S. Scientific Computing. 1983;55-64 North-Holland, Amsterdam.
35. Thieffry D., Huerta A.M., Pérez-Rueda E., Collado-Vides J. From specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli. Bioessays. 20:1998;433-440.
36. Becskei A., Serrano L. Engineering stability in gene networks by autoregulation. Nature. 405:2000;590-593.
37. Rosenfeld N., Elowitz M.B., Alon U. Negative autoregulation speeds the response times of transcription networks. J. Mol. Biol. 323:2002;785-793.
38. Salgado H., Santos-Zavaleta A., Gama-Castro S., Millán-Zá rate D., Díaz-Peredo E., Sánchez-Solano F., et al. RegulonDB (version 3.2): transcriptional regulation and operon organization in Escherichia coli K-12. Nucl. Acids Res. 29:2001;72-74.
39. Shen-Orr S.S., Milo R., Mangan S., Alon U. Network motifs in the transcriptional regulation network of Escherichia coli. Nature Genet. 31:2002;64-68.
40. Hryniewicz M.M., Kredich N.M. The cysP promoter of Salmonella typhimurium: characterization of two binding sites for CysB protein, studies of in vivo transcription initiation, and demonstration of the anti-inducer effects of thiosulfate. J. Bacteriol. 173:1991;5876-5886.
41. Ostrowski J., Kredich N.M. Negative autoregulation of cysB in Salmonella typhimurium: in vitro interactions of CysB protein with the cysB promoter. J. Bacteriol. 173:1991;2212-2218.
42. Henry M.F., Cronan J.E. Jr. A new mechanism of transcriptional regulation: release of an activator triggered by small molecule binding. Cell. 70:1992;671-679.
43. Cronan J.E. Jr, Rock C.O. Biosynthesis of membrane lipids. Neidhardt F.C. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd edit. 1996;612-636 ASM Press, Washington, DC.
44. Rock C.O., Cronan J.E. Escherichia coli as a model for the regulation of dissociable (type II) fatty acid biosynthesis. Biochim. Biophys. Acta. 1302:1996;1-16.
45. Chin A.M., Feldheim D.A., Saier M.H. Jr. Altered transcriptional patterns affecting several metabolic pathways in strains of Salmonella typhimurium which overexpress the fructose regulon. J. Bacteriol. 171:1989;2424-2434.
46. Ramseier T.M., Negre D., Cortay J.C., Scarabel M., Cozzone A.J., Saier M.H. Jr. In vitro binding of the pleiotropic transcriptional regulatory protein, FruR, to the fru, pps, ace, pts and icd operons of Escherichia coli and Salmonella typhimurium. J. Mol. Biol. 234:1993;28-44.
47. Ramseier T.M., Bledig S., Michotey V., Feghali R., Saier M.H. Jr. The global regulatory protein FruR modulates the direction of carbon flow in Escherichia coli. Mol. Microbiol. 16:1995;1157-1169.
48. Saier M.H. Jr, Ramseier T.M. The catabolite repressor/activator (Cra) protein of enteric bacteria. J. Bacteriol. 178:1996;3411-3417.
49. Saier M.H. Jr, Ramseier T.M., Reizer J. Regulation of carbon utilization. Neidhardt F.C. Escherichia coli and Salmonella: Cellular and Molecular Biology. 1996;1325-1343 American Society for Microbiology, Washington, DC.
50. Poggio S., Domeinzain C., Osorio A., Camarena L. The nitrogen assimilation control (Nac) protein represses asnC and asnA transcription in Escherichia coli. FEMS Microbiol. Lett. 206:2002;151-156.
51. Khodursky A.B., Peter B.J., Cozzarelli N.R., Botstein D., Brown P.O., 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.
52. Putney S.D., Schimmel P. An aminoacyl tRNA synthetase binds to a specific DNA sequence and regulates its gene transcription. Nature. 291:1981;632-635.
53. Urbanowski M.L., Stauffer G.V. Autoregulation by tandem promoters of the Salmonella typhimurium LT2 metJ gene. J. Bacteriol. 165:1986;740-745.
54. Bagg A., Neilands J.B. Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry. 26:1987;5471-5477.
55. de Lorenzo V., Herrero M., Giovannini F., Neilands J.B. Fur (ferric uptake regulation) protein and CAP (catabolite-activator protein) modulate transcription of fur gene in Escherichia coli. Eur. J. Biochem. 173:1988;537-546.
56. Escolar L., Pérez-Martín J., de Lorenzo V. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:1999;6223-6229.
57. Meng L.M., Kilstrup M., Nygaard P. Autoregulation of PurR repressor synthesis and involvement of purR in the regulation of purB, purC, purL, purMN and guaBA expression in Escherichia coli. Eur. J. Biochem. 187:1990;373-379.
58. Xu H., Moraitis M., Reedstrom R.J., Matthews K.S. Kinetic and thermodynamic studies of purine repressor binding to corepressor and operator DNA. J. Biol. Chem. 273:1998;8958-8964.
59. Tian G., Lim D., Oppenheim J.D., Maas W.K. Explanation for different types of regulation of arginine biosynthesis in Escherichia coli B and Escherichia coli K12 caused by a difference between their arginine repressors. J. Mol. Biol. 235:1994;221-230.
60. Lu Y., Turner R.J., Switzer R.L. Roles of the three transcriptional attenuators of the Bacillus subtilis pyrimidine biosynthetic operon in the regulation of its expression. J. Bacteriol. 177:1995;1315-1325.
61. Switzer R.L., Turner R.J., Lu Y. Regulation of the Bacillus subtilis pyrimidine biosynthetic operon by transcriptional attenuation: control of gene expression by an mRNA-binding protein. Prog. Nucl. Acid Res. Mol. Biol. 62:1999;329-367.
62. Ghim S.Y., Kim C.C., Bonner E.R., D'Elia J.N., Grabner G.K., Switzer R.L. The Enterococcus faecalis pyr operon is regulated by autogenous transcriptional attenuation at a single site in the 5′ leader. J. Bacteriol. 181:1999;1324-1329.
63. Camakaris H., Pittard J. Autoregulation of the tyrR gene. J. Bacteriol. 150:1982;70-75.
64. Pittard A.J. Biosynthesis of the aromatic amino acids. Neidhardt F.C. Escherichia coli and Salmonella: Cellular and Molecular Biology. 2nd edit. 1996;458-484 American Society for Microbiology, Washington, DC.
65. Foster J.W., Holley-Guthrie E.A., Warren F. Regulation of NAD metabolism in Salmonella typhimurium: genetic analysis and cloning of the nadR repressor locus. Mol. Gen. Genet. 208:1987;279-287.
66. Alves R., Savageau M.A. Comparing systemic properties of ensembles of biological networks by graphical and statistical methods. Bioinformatics. 16:2000;527-533.
67. Umbarger H.E. Evidence for a negative-feedback mechanism in the biosynthesis of isoleucine. Science. 123:1956;848.
68. Yates R.A., Pardee A.B. Control of pyrimidine biosynthesis in E. coli by a feedback mechanism. J. Biol. Chem. 221:1956;757-770.
69. Alves R., Savageau M.A. Effect of overall feedback inhibition in unbranched biosynthetic pathways. Biophys. J. 79:2000;2290-2304.
70. Bliss R.D., Painter P.R., Marr A.G. Role of feedback inhibition in stabilizing the classical operon. J. Theor. Biol. 97:1982;177-193.
71. Yanofsky C., 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.
72. Baker T.I., Crawford I.P. Anthranilate synthetase. Partial purification and some kinetic studies on the enzyme from Escherichia coli. J. Biol. Chem. 241:1966;5577-5584.
73. Kennell D.E. The instability of messenger RNA in bacteria. Reznikoff W., Gold L. Maximizing Gene Expression. 1986;101-142 Butterworth Publishers, Stoneham, MA.
74. Goldberg A.L., St John A.C. Intracellular protein degradation in mammalian and bacterial cells: Part 2. Annu. Rev. Biochem. 45:1976;747-803.
75. Yanofsky C., Horn V., Gollnick P. Physiological studies of tryptophan transport and tryptophanase operon induction in Escherichia coli. J. Bacteriol. 173:1991;6009-6017.
76. Joseph D.R., Muench K.H. Tryptophanyl transfer ribonucleic acid synthetase of Escherichia coli. I. Purification of the enzyme and of tryptrophan transfer ribonucleic acid. J. Biol. Chem. 246:1971;7602-7609.
77. Maaløe O. Regulation of the protein-synthesizing machinery: ribosomes, tRNA, factors and so on. Goldberger R.F. Biological Regulation and Development. vol. 1:1979;487-542 Plenum, New York.
78. Ingraham J.L., Maaløe O., Neidhardt F.C. Growth of the Bacterial Cell. 1983;Sinauer Associates, Sunderland, MA.
79. Blundell M., Craig E., Kennell D. Decay rates of different mRNA in E. coli and models of decay. Nature New Biol. 238:1972;46-49.