Methods for and results from the study of design principles in molecular systems

Mathematical Biosciences

Volumn 231, Issue 1, 2011, Pages 3-18

  Salvado, Baldiri ^a   Karathia, Hiren ^a   Chimenos, Anabel Usie ^a   Vilaprinyo, Ester ^b   Omholt, Stig ^c,d   Sorribas, Albert ^a   Alves, Rui ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

^b HOSPITAL DEL MAR   (Spain)

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

Biological networks; Design principles; Gene circuits; Metabolic circuits; Signal transduction

Indexed keywords

BIOCHEMICAL SYSTEMS THEORY; BIOLOGICAL DESIGN; BIOLOGICAL NETWORKS; COMPLEX NETWORKS; DESIGN FEATURES; DESIGN PRINCIPLES; GENE CIRCUITS; METABOLIC CIRCUITS; MOLECULAR LEVELS; MOLECULAR NETWORKS; MOLECULAR SYSTEMS; NATURAL EVOLUTION; QUANTITATIVE FEATURES; REGULATORY NETWORK;

BACTERIOPHAGES; BIOCHEMISTRY; BIOLOGICAL SYSTEMS; DESIGN; GENES; METABOLISM; MOLECULAR BIOLOGY; SIGNAL TRANSDUCTION;

NETWORKS (CIRCUITS);

GLUCOSE 6 PHOSPHATE DEHYDROGENASE; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR X; TRANSCRIPTION FACTOR Y; TRANSCRIPTION FACTOR Z; UNCLASSIFIED DRUG;

BIOLOGY; DESIGN; MOLECULAR ANALYSIS; REGULATORY FRAMEWORK;

ALGORITHM; ANALYTIC METHOD; ARTICLE; BINDING SITE; CALCULATION; CELL CYCLE; CELL DIVISION; CIRCADIAN RHYTHM; DEPHOSPHORYLATION; GENE EXPRESSION; GENE MUTATION; GENE REGULATORY NETWORK; INTERMETHOD COMPARISON; MATHEMATICAL MODEL; MOLECULAR SYSTEMATICS; NONHUMAN; PREDICTION; SIGNAL TRANSDUCTION;

BIOCHEMICAL PROCESSES; BIOLOGICAL EVOLUTION; SYSTEMS BIOLOGY; SYSTEMS THEORY;

EID: 79954608391     PISSN: 00255564     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mbs.2011.02.005     Document Type: Article

References (178)

1. Alon U. Biological networks: the tinkerer as an engineer. Science. 2003, 301:1866.
2. Turner J. The Tinkerer's Accomplice: How Design Emerges from Life Itself 2007, Harvard University Press.
3. Alon U. An Introduction to Systems Biology: Design Principles of Biological Circuits 2006, Chapman and Hall/CRC.
4. Banerjee R., Roy D. Codon usage and gene expression pattern of Stenotrophomonas maltophilia R551-3 for pathogenic mode of living. Biochem. Biophys. Res. Commun. 2009, 390:177.
5. Sharp P.M., Emery L.R., Zeng K. Forces that influence the evolution of codon bias. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365:1203.
6. Vilaprinyo E., Alves R., Sorribas A. Minimization of biosynthetic costs in adaptive gene expression responses of yeast to environmental changes. PLoS Comput. Biol. 2010, 6:e1000674.
7. Szilagyi A., Gyorffy D., Zavodszky P. The twilight zone between protein order and disorder. Biophys. J. 2008, 95:1612.
8. Minary P., Levitt M. Probing protein fold space with a simplified model. J. Mol. Biol. 2008, 375:920.
9. Melendez R., Melendez-Hevia E., Mas F., Mach J., Cascante M. Physical constraints in the synthesis of glycogen that influence its structural homogeneity: a two-dimensional approach. Biophys. J. 1998, 75:106.
10. Melendez R., Melendez-Hevia E., Cascante M. How did glycogen structure evolve to satisfy the requirement for rapid mobilization of glucose? A problem of physical constraints in structure building. J. Mol. Evol. 1997, 45:446.
11. Irvine D.H., Savageau M.A. Network regulation of the immune response: modulation of suppressor lymphocytes by alternative signals including contrasuppression. J. Immunol. 1985, 134:2117.
12. Irvine D.H., Savageau M.A. Network regulation of the immune response: alternative control points for suppressor modulation of effector lymphocytes. J. Immunol. 1985, 134:2100.
13. Savageau M.A. Concepts relating behavior of biochemical systems to their underlyin molecular properties. Arch. Biochem. Biophys. 1971, 145:612.
14. Savageau M.A. Genetic regulatory mechanisms and the ecological niche of Escherichia coli. Proc. Natl. Acad. Sci. USA 1974, 71:2453.
15. Savageau M.A. Optimal design of feedback-control by inhibition - steady-state considerations. J. Mol. Evol. 1974, 4:139.
16. Savageau M.A. Comparison of classical and autogenous systems of regulation in inducible operons. Nature 1974, 252:546.
17. Savageau M.A. Kinetic organization of biosynthetic regulatory systems in bacteria. Abstr. Papers Am. Chem. Soc. 1974, 26.
18. Savageau M.A. Selection of positive and negative mechanisms of genetic-control in enteric bacteria. Federation Proc. 1974, 33:1464.
19. Savageau M.A. Optimal design of feedback-control by inhibition - dynamic considerations. J. Mol. Evol. 1975, 5:199.
20. Savageau M.A. Biochemical systems analysis: a study of function and design in molecular biology 1976, Addison-Wesley.
21. Voit E.O. Canonical nonlinear modeling 1991, Springer.
22. Alves R., Savageau M.A. Extending the method of mathematically controlled comparison to include numerical comparisons. Bioinformatics 2000, 16:786.
23. Schwacke J.H., Voit E.O. Improved methods for the mathematically controlled comparison of biochemical systems. Theor Biol. Med. Model. 2004, 1:1.
24. Coelho P.M., Salvador A., Savageau M.A. Quantifying global tolerance of biochemical systems: design implications for moiety-transfer cycles. PLoS Comput. Biol. 2009, 5:e1000319.
25. Savageau M.A., Coelho P.M., Fasani R.A., Tolla D.A., Salvador A. Phenotypes and tolerances in the design space of biochemical systems. Proc. Natl. Acad. Sci. USA 2009, 106:6435.
26. Savageau M.A., Fasani R.A. Qualitatively distinct phenotypes in the design space of biochemical systems. FEBS Lett. 2009, 583:3914.
27. Clutton-Brock T., Sheldon B.C. Individuals populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends Ecol. Evol. 2010, 25:562.
28. Vogel C., Teichmann S.A., Pereira-Leal J. The relationship between domain duplication and recombination. J. Mol. Biol. 2005, 346:355.
29. Price M.N., Dehal P.S., Arkin A.P. Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol. 2008, 9:R4.
30. Price M.N., Arkin A.P., Alm E.J. The life-cycle of operons. PLoS Genet. 2006, 2:e96.
31. Kashtan N., Parter M., Dekel E., Mayo A.E., Alon U. Extinctions in heterogeneous environments and the evolution of modularity. Evolution 2009, 63:1964.
32. Kashtan N., Mayo A.E., Kalisky T., Alon U. An analytically solvable model for rapid evolution of modular structure. PLoS Comput. Biol. 2009, 5:e1000355.
33. Parter M., Kashtan N., Alon U. Facilitated variation: how evolution learns from past environments to generalize to new environments. PLoS Comput. Biol. 2008, 4:e1000206.
34. Parter M., Kashtan N., Alon U. Environmental variability and modularity of bacterial metabolic networks. BMC Evol. Biol. 2007, 7:169.
35. Kashtan N., Alon U. Spontaneous evolution of modularity and network motifs. Proc. Natl. Acad. Sci. USA 2005, 102:13773.
36. Bayer T.S., Hoff K.G., Beisel C.L., Lee J.J., Smolke C.D. Synthetic control of a fitness tradeoff in yeast nitrogen metabolism. J. Biol. Eng. 2009, 3:1.
37. Cagatay T., Turcotte M., Elowitz M.B., Garcia-Ojalvo J., Suel G.M. Architecture-dependent noise discriminates functionally analogous differentiation circuits. Cell 2009, 139:512.
38. Igoshin O.A., Alves R., Savageau M.A. Hysteretic and graded responses in bacterial two-component signal transduction. Mol. Microbiol. 2008, 68:1196.
39. Coelho P.M., Salvador A., Savageau M.A. Relating mutant genotype to phenotype via quantitative behavior of the NADPH redox cycle in human erythrocytes. PLoS One 2010, 5.
40. Savageau M.A. Parameter sensitivity as a criterion for evaluating and comparing the performance of biochemical systems. Nature 1971, 229:542.
41. Kitano H. Towards a theory of biological robustness. Mol. Syst. Biol. 2007, 3:137.
42. Rao C.V., Arkin A.P. Control motifs for intracellular regulatory networks. Annu. Rev. Biomed. Eng. 2001, 3:391.
43. Salvador A., Savageau M.A. Evolution of enzymes in a series is driven by dissimilar functional demands. Proc. Natl. Acad. Sci. USA 2006, 103:2226.
44. Salvador A., Savageau M.A. Quantitative evolutionary design of glucose 6-phosphate dehydrogenase expression in human erythrocytes. Proc. Natl. Acad. Sci. USA 2003, 100:14463.
45. Craciun G., Feinberg M. Multiple equilibria in complex chemical reaction networks: I. The injectivity property. Siam J. Appl. Math. 2005, 65:1526.
46. Craciun G., Feinberg M. Multiple equilibria in complex chemical reaction networks: extensions to entrapped species models. IEE Proc. Syst. Biol. 2006, 153:179.
47. Craciun G., Feinberg M. Multiple equilibria in complex chemical reaction networks: II. The species-reaction graph. Siam J. Appl. Math. 2006, 66:1321.
48. Craciun G., Feinberg M. Multiple equilibria in complex chemical reaction networks: semiopen mass action systems. Siam J. Appl. Math. 2010, 70:1859.
49. Craciun G., Tang Y.Z., Feinberg M. Understanding bistability in complex enzyme-driven reaction networks. Proc. Natl. Acad. Sci. USA 2006, 103:8697.
50. Feinberg M. Reaction network structure and multiple steady-states in complex isothermal reactors. Abstr. Papers Am. Chem. Soc. 1985, 189:35.
51. Feinberg M. The existence and uniqueness of steady states for a class of chemical reaction networks. Arch. Rational Mech. Anal. 1995, 132:311.
52. Feinberg M. Multiple steady states for chemical reaction networks of deficiency one. Arch. Rational Mech. Anal. 1995, 132:371.
53. Schlosser P.M., Feinberg M. A theory of multiple steady-states in isothermal homogeneous cfstrs with many reactions. Chem. Eng. Sci. 1994, 49:1749.
54. Shinar G., Alon U., Feinberg M. Sensitivity and robustness in chemical reaction networks. Soc. Ind. Appl. Math. 2009, 69:977.
55. Shinar G., Feinberg M. Structural sources of robustness in biochemical reaction networks. Science 2010, 327:1389.
56. Melendez-Hevia E. The game of the pentose phosphate cycle: a mathematical approach to study the optimization in design of metabolic pathways during evolution. Biomed. Biochim. Acta 1990, 49:903.
57. Melendez-Hevia E., Isidoro A. The game of the pentose phosphate cycle. J. Theor. Biol. 1985, 117:251.
58. Melendez-Hevia E., Torres N.V. Economy of design in metabolic pathways: further remarks on the game of the pentose phosphate cycle. J. Theor. Biol. 1988, 132:97.
59. Sorribas A., Pozo C., Vilaprinyo E., Guillen-Gosalbez G., Jimenez L., Alves R. Optimization and evolution in metabolic pathways: global optimization techniques in Generalized Mass Action models. J. Biotechnol. 2010, 149:141.
60. Vilaprinyo E., Alves R., Sorribas A. Use of physiological constraints to identify quantitative design principles for gene expression in yeast adaptation to heat shock. BMC Bioinform. 2006, 7:184.
61. Voit E.O., Radivoyevitch T. Biochemical systems analysis of genome-wide expression data. Bioinformatics 2000, 16:1023.
62. Guillen-Gosalbez G., Sorribas A. Identifying quantitative operation principles in metabolic pathways: a systematic method for searching feasible enzyme activity patterns leading to cellular adaptive responses. BMC Bioinform. 2009, 10:386.
63. Igoshin O.A., Price C.W., Savageau M.A. Signalling network with a bistable hysteretic switch controls developmental activation of the sigma transcription factor in Bacillus subtilis. Mol. Microbiol. 2006, 61:165.
64. Hlavacek W.S., Savageau M.A. Rules for coupled expression of regulator and effector genes in inducible circuits. J. Mol. Biol. 1996, 255:121.
65. Hlavacek W.S., Savageau M.A. Completely uncoupled and perfectly coupled gene expression in repressible systems. J. Mol. Biol. 1997, 266:538.
66. Savageau M.A. Demand theory of gene regulation. I. Quantitative development of the theory. Genetics 1998, 149:1665.
67. Savageau M.A. Demand theory of gene regulation. II. Quantitative application to the lactose and maltose operons of Escherichia coli. Genetics 1998, 149:1677.
68. Bose I., Ghosh B., Karmakar R. Motifs in gene transcription regulatory networks. Physica A 2004, 346:49.
69. Novak B., Tyson J.J. Design principles of biochemical oscillators. Nat. Rev. Mol. Cell Biol. 2008, 9:981.
70. Alon U. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 2007, 8:450.
71. Cotterell J., Sharpe J. An atlas of gene regulatory networks reveals multiple three-gene mechanisms for interpreting morphogen gradients. Mol. Syst. Biol. 2010, 6.
72. Mangan S., Alon U. Structure and function of the feed-forward loop network motif. Proc. Natl. Acad. Sci. USA 2003, 100:11980.
73. Dekel E., Mangan S., Alon U. Environmental selection of the feed-forward loop circuit in gene-regulation networks. Phys. Biol. 2005, 2:81.
74. Wall M.E., Dunlop M.J., Hlavacek W.S. Multiple functions of a feed-forward-loop gene circuit. J. Mol. Biol. 2005, 349:501.
75. Savageau M.A. Regulation of differentiated cell-specific functions. Proc. Natl. Acad. Sci. USA 1983, 80:1411.
76. 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. 1995, 248:739.
77. Wall M.E., Hlavacek W.S., Savageau M.A. Design principles for regulator gene expression in a repressible gene circuit. J. Mol. Biol. 2003, 332:861.
78. Wall M.E., Hlavacek W.S., Savageau M.A. Design of gene circuits: lessons from bacteria. Nat. Rev. Genet. 2004, 5:34.
79. Shinar G., Dekel E., Tlusty T., Alon U. Rules for biological regulation based on error minimization. Proc. Natl. Acad. Sci. USA 2006, 103:3999.
80. Libby E., Perkins T.J., Swain P.S. Noisy information processing through transcriptional regulation. Proc. Natl. Acad. Sci. USA 2007, 104:7151.
81. Sprinzak D., Lakhanpal A., Lebon L., Santat L.A., Fontes M.E., Anderson G.A., Garcia-Ojalvo J., Elowitz M.B. Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 2010, 465:86.
82. Gerland U., Hwa T. Evolutionary selection between alternative modes of gene regulation. Proc. Natl. Acad. Sci. USA 2009, 106:8841.
83. Peter I.S., Davidson E.H. Modularity and design principles in the sea urchin embryo gene regulatory network. FEBS Lett. 2009, 583:3948.
84. Davidson E.H. Network design principles from the sea urchin embryo. Curr. Opin. Genet. Dev. 2009, 19:535.
85. Acar M., Pando B.F., Arnold F.H., Elowitz M.B., van Oudenaarden A. A general mechanism for network-dosage compensation in gene circuits. Science. 2010, 329:1656.
86. Zaslaver A., Mayo A.E., Rosenberg R., Bashkin P., Sberro H., Tsalyuk M., Surette M.G., Alon U. Just-in-time transcription program in metabolic pathways. Nat. Genet. 2004, 36:486.
87. von Heijne G., Savageau M.A. RNA splicing: advantages of parallel processing. J. Theor. Biol. 1982, 98:563.
88. Beisel C.L., Smolke C.D. Design principles for riboswitch function. PLoS Comput. Biol. 2009, 5:e1000363.
89. Win M.N., Liang J.C., Smolke C.D. Frameworks for programming biological function through RNA parts and devices. Chem. Biol. 2009, 16:298.
90. Win M.N., Smolke C.D. Higher-order cellular information processing with synthetic RNA devices. Science. 2008, 322:456.
91. Pfleger B.F., Pitera D.J., Smolke C.D., Keasling J.D. Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes. Nat. Biotechnol. 2006, 24:1027.
92. Levine E., Hwa T. Small RNAs establish gene expression thresholds. Curr. Opin. Microbiol. 2008, 11:574.
93. Levine E., Zhang Z., Kuhlman T., Hwa T. Quantitative characteristics of gene regulation by small RNA. PLoS Biol. 2007, 5:e229.
94. Flynt A.S., Lai E.C. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 2008, 9:831.
95. Savageau M.A. Feedforward inhibition in biosynthetic pathways: inhibition of the aminoacyl-tRNA synthetase by the penultimate product. J. Theor. Biol. 1979, 77:385.
96. Savageau M.A., Jacknow G. Feedfoward inhibition in biosynthetic pathways: inhibition of the aminoacyl-tRNA synthetase by intermediates of the pathway. J. Theor. Biol. 1979, 77:405.
97. Alves R., Savageau M.A. Effect of overall feedback inhibition in unbranched biosynthetic pathways. Biophys. J. 2000, 79:2290.
98. Alves R., Savageau M.A. Irreversibility in unbranched pathways: preferred positions based on regulatory considerations. Biophys. J. 2001, 80:1174.
99. Shinar G., Rabinowitz J.D., Alon U. Robustness in glyoxylate bypass regulation. PLoS Comput. Biol. 2009, 5:e1000297.
100. Salvador A. Evolution of enzymes in a series is driven by dissimilar functional demands. Proc. Natl. Acad. Sci. USA 2005.
101. Kwon Y.K., Cho K.H. Coherent coupling of feedback loops: a design principle of cell signaling networks. Bioinformatics 2008, 24:1926.
102. Heinrich R., Melendez-Hevia E., Montero F., Nuno J.C., Stephani A., Waddell T.G. The structural design of glycolysis: an evolutionary approach. Biochem. Soc. Trans. 1999, 27:294.
103. Melendez-Hevia E., Waddell T.G., Heinrich R., Montero F. Theoretical approaches to the evolutionary optimization of glycolysis-chemical analysis. Eur. J. Biochem. 1997, 244:527.
104. Heinrich R., Montero F., Klipp E., Waddell T.G., Melendez-Hevia E. Theoretical approaches to the evolutionary optimization of glycolysis: thermodynamic and kinetic constraints. Eur. J. Biochem. 1997, 243:191.
105. Mittenthal J.E., Clarke B., Waddell T.G., Fawcett G. A new method for assembling metabolic networks, with application to the Krebs citric acid cycle. J. Theor. Biol. 2001, 208:361.
106. Mittenthal J.E. An algorithm to assemble pathways from processes. Pac. Symp. Biocomput. 1997, 292.
107. Mittenthal J.E., Yuan A., Clarke B., Scheeline A. Designing metabolism: alternative connectivities for the pentose phosphate pathway. Bull. Math. Biol. 1998, 60:815.
108. Noor E., Eden E., Milo R., Alon U. Central carbon metabolism as a minimal biochemical walk between precursors for biomass and energy. Mol. Cell 2010, 39:809.
109. Kurland C.G., Dong H. Bacterial growth inhibition by overproduction of protein. Mol. Microbiol. 1996, 21:1.
110. Cascante M., Llorens M., Melendez-Hevia E., Puigjaner J., Montero F., Marti E. The metabolic productivity of the cell factory. J. Theor. Biol. 1996, 182:317.
111. Cascante M., Melendez-Hevia E., Kholodenko B., Sicilia J., Kacser H. Control analysis of transit time for free and enzyme-bound metabolites: physiological and evolutionary significance of metabolic response times. Biochem. J. 1995, 308(Pt 3):895.
112. Durek P., Walther D. The integrated analysis of metabolic and protein interaction networks reveals novel molecular organizing principles. BMC Syst. Biol. 2008, 2:100.
113. Ghosh A., Chance B. Oscillations of Glycolytic Intermediates in Yeast Cells. Biochem. Biophys. Res. Commun. 1964, 16:174.
114. Palmeirim I., Henrique D., IshHorowicz D., Pourquie O. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 1997, 91:639.
115. Leloup J.C., Goldbeter A. Chaos and birhythmicity in a model for circadian oscillations of the PER and TIM proteins in Drosophila. J. Theor. Biol. 1999, 198:445.
116. Csikasz-Nagy A., Novak B., Tyson J.J. Reverse engineering models of cell cycle regulation. Adv. Exp. Med. Biol. 2008, 641:88.
117. Csikasz-Nagy A., Kapuy O., Toth A., Pal C., Jensen L.J., Uhlmann F., Tyson J.J., Novak B. Cell cycle regulation by feed-forward loops coupling transcription and phosphorylation. Mol. Syst. Biol. 2009, 5:236.
118. Drapkin B.J., Lu Y., Procko A.L., Timney B.L., Cross F.R. Analysis of the mitotic exit control system using locked levels of stable mitotic cyclin. Mol. Syst. Biol. 2009, 5:328.
119. Tyson J.J., Novak B. Temporal organization of the cell cycle. Curr. Biol. 2008, 18:R759.
120. Kiang L., Heichinger C., Watt S., Bahler J., Nurse P. Cyclin-dependent kinase inhibits reinitiation of a normal S-phase program during G2 in fission yeast. Mol. Cell Biol. 2009, 29:4025.
121. Moseley J.B., Mayeux A., Paoletti A., Nurse P. A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 2009, 459:857.
122. Lu Y., Cross F.R. Periodic cyclin-Cdk activity entrains an autonomous Cdc14 release oscillator. Cell 2010, 141:268.
123. Charvin G., Oikonomou C., Siggia E.D., Cross F.R. Origin of irreversibility of cell cycle start in budding yeast. PLoS Biol. 2010, 8:e1000284.
124. Young M.W., Kay S.A. Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2001, 2:702.
125. Rand D.A., Shulgin B.V., Salazar D., Millar A.J. Design principles underlying circadian clocks. J. R. Soc. Interface 2004, 1:119.
126. Rand D.A., Shulgin B.V., Salazar J.D., Millar A.J. Uncovering the design principles of circadian clocks: mathematical analysis of flexibility and evolutionary goals. J. Theor. Biol. 2006, 238:616.
127. Dalchau N., Hubbard K.E., Robertson F.C., Hotta C.T., Briggs H.M., Stan G.B., Goncalves J.M., Webb A.A. Correct biological timing in Arabidopsis requires multiple light-signaling pathways. Proc. Natl. Acad. Sci. USA 2010, 107:13171.
128. Locke J.C., Westermark P.O., Kramer A., Herzel H. Global parameter search reveals design principles of the mammalian circadian clock. BMC Syst. Biol. 2008, 2:22.
129. Indic P., Schwartz W.J., Paydarfar D. Design principles for phase-splitting behaviour of coupled cellular oscillators: clues from hamsters with 'split' circadian rhythms. J. R. Soc. Interface 2008, 5:873.
130. Pando B.F., van Oudenaarden A. Coupling cellular oscillators-circadian and cell division cycles in cyanobacteria. Curr. Opin. Genet. Dev. 2010.
131. Mori T., Binder B., Johnson C.H. Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. Proc. Natl. Acad. Sci. USA 1996, 93:10183.
132. Yang Q., Pando B.F., Dong G., Golden S.S., van Oudenaarden A. Circadian gating of the cell cycle revealed in single cyanobacterial cells. Science 2010, 327:1522.
133. Matsuo T., Yamaguchi S., Mitsui S., Emi A., Shimoda F., Okamura H. Control mechanism of the circadian clock for timing of cell division in vivo. Science 2003, 302:255.
134. Nagoshi E., Saini C., Bauer C., Laroche T., Naef F., Schibler U. Circadian gene expression in individual fibroblasts: cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 2004, 119:693.
135. Parkinson J.S., Appleby Jeryl L., Bourret Robert B. Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 1996, 86:845.
136. Hoch J.A. Two-component and phosphorelay signal transduction. Curr. Opin. Microbiol. 2000, 3:165.
137. D'Agostino I.B., Kieber J.J. Phosphorelay signal transduction: the emerging family of plant response regulators. Trends Biochem. Sci. 1999, 24:452.
138. Loomis W.F., Kuspa A., Shaulsky G. Two-component signal transduction systems in eukaryotic microorganisms. Curr. Opin. Microbiol. 1998, 1:643.
139. Shinar G., Milo R., Martinez M.R., Alon U. Input output robustness in simple bacterial signaling systems. Proc. Natl. Acad. Sci. USA 2007, 104:19931.
140. Alves R., Savageau M.A. Comparative analysis of prototype two-component systems with either bifunctional or monofunctional sensors: differences in molecular structure and physiological function. Mol. Microbiol. 2003, 48:25.
141. Mehta P., Goyal S., Long T., Bassler B.L., Wingreen N.S. Information processing and signal integration in bacterial quorum sensing. Mol. Syst. Biol. 2009, 5:325.
142. Ray J.C., Igoshin O.A. Adaptable functionality of transcriptional feedback in bacterial two-component systems. PLoS Comput. Biol. 2010, 6:e1000676.
143. Plahte E., Mestl T., Omholt S.W. A methodological basis for description and analysis of systems with complex switch-like interactions. J. Math. Biol. 1998, 36:321.
144. Tiwari [144]A., Balázsi G., Gennaro M.L., Igoshin O.A. Interplay of multiple feedbacks with post-translational kinetics results in bistability of mycobacterial stress-response. Phys. Biol. 2010, 23:036005.
145. Csikasz-Nagy A., Cardelli L., Soyer O.S. Response dynamics of phosphorelays suggest their potential utility in cell signalling. J. R. Soc. Interface 2010.
146. Goldbeter A., Koshland D.E. An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. USA 1981, 78:6840.
147. Goldbeter A., Koshland D.E. Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero-order and multistep effects. J. Biol. Chem. 1984, 259:14441.
148. Goldbeter A., Koshland D.E. Energy expenditure in the control of biochemical systems by covalent modification. J. Biol. Chem. 1987, 262:4460.
149. Huang C.Y., Ferrell J.E. Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 1996, 93:10078.
150. Schwacke J.H., Voit E.O. Computation and analysis of time-dependent sensitivities in Generalized Mass Action systems. J. Theor. Biol. 2005, 236:21.
151. Schwacke J.H., Voit E.O. Concentration-dependent effects on the rapid and efficient activation of the MAP kinase signaling cascade. Proteomics 2007, 7:890.
152. Schwacke J.H., Voit E.O. The potential for signal integration and processing in interacting MAP kinase cascades. J. Theor. Biol. 2007, 246:604.
153. Shankaran H., Resat H., Wiley H.S. Cell surface receptors for signal transduction and ligand transport: a design principles study. PLoS Comput. Biol. 2007, 3:e101.
154. Shankaran H., Wiley H.S., Resat H. Receptor downregulation and desensitization enhance the information processing ability of signalling receptors. BMC Syst. Biol. 2007, 1:48.
155. Lestas I., Vinnicombe G., Paulsson J. Fundamental limits on the suppression of molecular fluctuations. Nature 2010, 467:174.
156. Ben-Zvi D., Barkai N. Scaling of morphogen gradients by an expansion-repression integral feedback control. Proc. Natl. Acad. Sci. USA 2010, 107:6924.
157. Ben-Zvi D., Fainsod A., Shilo B., Barkai N. Scaling of the Bmp morphogen gradient in Xenopus embryos. Dev. Biol. 2009, 331:425.
158. Barkai N., Shilo B.Z. Robust generation and decoding of morphogen gradients. Cold Spring Harb. Perspect. Biol. 2009, 1.
159. Kampf M.M., Weber W. Synthetic biology in the analysis and engineering of signaling processes. Integr. Biol. (Camb) 2010, 2:12.
160. Khalil A.S., Collins J.J. Synthetic biology: applications come of age. Nat. Rev. Genet. 2010, 11:367.
161. Rothschild L.J. A powerful toolkit for synthetic biology: Over 3.8 billion years of evolution. Bioessays 2010, 32:304.
162. Aubel D., Fussenegger M. Mammalian synthetic biology-from tools to therapies. Bioessays 2010, 32:332.
163. Bashor C.J., Horwitz A.A., Peisajovich S.G., Lim W.A. Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. Annu. Rev. Biophys. 2010, 39:515.
164. Young E., Alper H. Synthetic biology: tools to design, build, and optimize cellular processes. J. Biomed. Biotechnol. 2010, 2010:130781.
165. Alterovitz G., Muso T., Ramoni M.F. The challenges of informatics in synthetic biology: from biomolecular networks to artificial organisms. Brief Bioinform. 2010, 11:80.
166. Mukherji S., van Oudenaarden A. Synthetic biology: understanding biological design from synthetic circuits. Nat. Rev. Genet. 2009, 10:859.
167. Marner W.D. Practical application of synthetic biology principles. Biotechnol. J. 2009, 4:1406.
168. Agapakis C.M., Silver P.A. Synthetic biology: exploring and exploiting genetic modularity through the design of novel biological networks. Mol. Biosyst. 2009, 5:704.
169. Purnick P.E., Weiss R. The second wave of synthetic biology: from modules to systems. Nat. Rev. Mol. Cell Biol. 2009, 10:410.
170. Endler L., Rodriguez N., Juty N., Chelliah V., Laibe C., Li C., Le Novere N. Designing and encoding models for synthetic biology. J. R. Soc. Interface 2009, 6(Suppl. 4):S405.
171. Martin C.H., Nielsen D.R., Solomon K.V., Prather K.L. Synthetic metabolism: engineering biology at the protein and pathway scales. Chem. Biol. 2009, 16:277.
172. Lee S.K., Chou H., Ham T.S., Lee T.S., Keasling J.D. Metabolic engineering of microorganisms for biofuels production: from bugs to synthetic biology to fuels. Curr. Opin. Biotechnol. 2008, 19:556.
173. Saito H., Inoue T. Synthetic biology with RNA motifs. Int. J. Biochem. Cell Biol. 2009, 41:398.
174. Brenner K., You L., Arnold F.H. Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol. 2008, 26:483.
175. Channon K., Bromley E.H., Woolfson D.N. Synthetic biology through biomolecular design and engineering. Curr. Opin. Struct. Biol. 2008, 18:491.
176. Becskei A., Serrano L. Engineering stability in gene networks by autoregulation. Nature 2000, 405:590.
177. Skerker J.M., Lucks J.B., Arkin A.P. Evolution, ecology and the engineered organism: lessons for synthetic biology. Genome Biol. 2009, 10:114.
178. Atkinson M.R., Savageau M.A., Myers J.T., Ninfa A.J. Development of genetic circuitry exhibiting toggle switch or oscillatory behavior in Escherichia coli. Cell 2003, 113:597.