Emergence of switch-like behavior in a large family of simple biochemical networks

PLoS Computational Biology

Volumn 7, Issue 5, 2011, Pages

  Siegal Gaskins, Dan ^a   Mejia Guerra, Maria Katherine ^a   Smith, Gregory D ^b   Grotewold, Erich ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b The College of William and Mary   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL SYSTEMS; PROTEINS; RATE CONSTANTS; TRANSCRIPTION; YEAST;

BI-STABILITY; BIOCHEMICAL NETWORK; BIOLOGICAL FUNCTIONS; BISTABLES; CELLULAR CELL; CELLULAR DIFFERENTIATION; GENE REGULATORY NETWORKS; NETWORK TOPOLOGY; SIMPLE++; SUBNETWORKS;

NETWORK TOPOLOGY;

ARTICLE; BIOCHEMISTRY; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CHEMICAL REACTION; CONTROLLED STUDY; GENE EXPRESSION; GENE REGULATORY NETWORK; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; STOICHIOMETRY; BIOLOGICAL MODEL; CHEMICAL MODEL; COMPUTER SIMULATION; FUNGAL GENE; GENETICS; GENOMICS; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS;

SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE PROTEIN;

COMPUTER SIMULATION; GENE REGULATORY NETWORKS; GENES, FUNGAL; GENOMICS; MODELS, CHEMICAL; MODELS, GENETIC; PROTEIN INTERACTION MAPPING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 79958097395     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002039     Document Type: Article

References (82)

1. Pomerening JR, (2008) Uncovering mechanisms of bistability in biological systems. Curr Opin Biotechnol 19: 381-8.
2. Lai K, Robertson MJ, Schaffer DV, (2004) The sonic hedgehog signaling system as a bistable genetic switch. Biophys J 86: 2748-57.
3. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, et al. (2006) Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126: 755-66.
4. Huang S, Guo YP, May G, Enver T, (2007) Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev Biol 305: 695-713.
5. Cross FR, Archambault V, Miller M, Klovstad M, (2002) Testing a mathematical model of the yeast cell cycle. Mol Biol Cell 13: 52-70.
6. Bagci EZ, Vodovotz Y, Billiar TR, Ermentrout GB, Bahar I, (2006) Bistability in apoptosis: roles of Bax, Bcl-2, and mitochondrial permeability transition pores. Biophys J 90: 1546-59.
7. Eissing T, Conzelmann H, Gilles ED, Allgöwer F, Bullinger E, et al. (2004) Bistability analyses of a caspase activation model for receptor-induced apoptosis. J Biol Chem 279: 36892-7.
8. Legewie S, Blüthgen N, Herzel H, (2006) Mathematical modeling identifies inhibitors of apoptosis as mediators of positive feedback and bistability. PLoS Comput Biol 2: e120.
9. Avery SV, (2005) Cell individuality: the bistability of competence development. Trends Microbiol 13: 459-62.
10. Ninfa AJ, Mayo AE, (2004) Hysteresis vs. graded responses: the connections make all the difference. Sci STKE 2004.
11. Guidi G, Goldbeter A, (1997) Bistability without hysteresis in chemical reaction systems: a theoretical analysis of irreversible transitions between multiple steady states. J Phys Chem A 101: 9367-9376.
12. Pomerening JR, Sontag ED, Ferrell JE, (2003) Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2. Nat Cell Biol 5: 346-51.
13. ShaW, Moore J, Chen K, Lassaletta AD, Yi CS, et al. (2003) Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc Natl Acad Sci USA 100: 975-80.
14. Ozbudak EM, Thattai M, Lim HN, Shraiman BI, van Oudenaarden A, (2004) Multistability in the lactose utilization network of Escherichia coli. Nature 427: 737-40.
15. Tyson JJ, Chen KC, Novák B, (2001) Network dynamics and cell physiology. Nat Rev Mol Cell Biol 2: 908-16.
16. Feinberg M, (1987) Chemical reaction network structure and the stability of complex isothermal reactors-I. The Deficiency Zero and Deficiency One Theorems. Chem Eng Sci 42: 2229-2268.
17. Feinberg M, (1988) Chemical reaction network structure and the stability of complex isothermal reactors. II: Multiple steady states for networks of deficiency one. Chem Eng Sci 43: 1-25.
18. Ellison P, Feinberg M, (2000) How catalytic mechanisms reveal themselves in multiple steady-state data: I. Basic principles. J Mol Catal A-Chem 154: 155-167.
19. Kaltenbach HM, Dimopoulos S, Stelling J, (2009) Systems analysis of cellular networks under uncertainty. FEBS Lett 583: 3923-30.
20. Conradi C, Saez-Rodriguez J, Gilles ED, Raisch J, (2005) Using chemical reaction network theory to discard a kinetic mechanism hypothesis. Syst Biol 152: 243-8.
21. Otero-Muras I, Banga JR, Alonso AA, (2009) Exploring multiplicity conditions in enzymatic reaction networks. Biotechnol Prog 25: 619-31.
22. Craciun G, Tang Y, Feinberg M, (2006) Understanding bistability in complex enzyme-driven reaction networks. Proc Natl Acad Sci USA 103: 8697-702.
23. Siegal-Gaskins D, Grotewold E, Smith GD, (2009) The capacity for multistability in small gene regulatory networks. BMC Syst Biol 3: 96.
24. Ellison P, (1998) The advanced deficiency algorithm and its applications to mechanism discrimination [PhD thesis]. Rochester (New York) Department of Chemical Engineering, University of Rochester.
25. Conradi C, Flockerzi D, Raisch J, Stelling J, (2007) Subnetwork analysis reveals dynamic features of complex (bio)chemical networks. Proc Natl Acad Sci USA 104: 19175-80.
26. Flockerzi D, Conradi C, (2008) Subnetwork analysis for multistationarity in mass action kinetics. J Phys: Conf Ser 138: 012006.
27. Miller CA, Beard DA, (2008) The effects of reversibility and noise on stochastic phosphorylation cycles and cascades. Biophys J 95: 2183-92.
28. Saez-Rodriguez J, Hammerle-Fickinger A, Dalal O, Klamt S, Gilles ED, et al. (2008) Multistability of signal transduction motifs. IET Syst Biol 2: 80-93.
29. Keller AD, (1995) Model genetic circuits encoding autoregulatory transcription factors. J Theor Biol 172: 169-85.
30. Hasty J, Isaacs F, Dolnik M, McMillen D, Collins JJ, (2001) Designer gene networks: Towards fundamental cellular control. Chaos 11: 207-220.
31. Isaacs FJ, Hasty J, Cantor CR, Collins JJ, (2003) Prediction and measurement of an autoregulatory genetic module. Proc Natl Acad Sci USA 100: 7714-9.
32. Becskei A, Séraphin B, Serrano L, (2001) Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion. EMBO J 20: 2528-35.
33. Cinquin O, Demongeot J, (2002) Positive and negative feedback: striking a balance between necessary antagonists. J Theor Biol 216: 229-41.
34. Cherry JL, Adler FR, (2000) How to make a biological switch. J Theor Biol 203: 117-33.
35. Gardner TS, Cantor CR, Collins JJ, (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339-42.
36. François P, Hakim V, (2004) Design of genetic networks with specified functions by evolution in silico. Proc Natl Acad Sci USA 101: 580-5.
37. Lipshtat A, Loinger A, Balaban NQ, Biham O, (2006) Genetic toggle switch without cooperative binding. Phys Rev Lett 96: 188101.
38. Buchler NE, Louis M, (2008) Molecular titration and ultrasensitivity in regulatory networks. J Mol Biol 384: 1106-19.
39. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, et al. (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA 92: 7834-8.
40. Basak S, Shih VFS, Hoffmann A, (2008) Generation and activation of multiple dimeric transcription factors within the NF-κB signaling system. Mol Cell Biol 28: 3139-50.
41. Monod J, Jacob F, (1961) Teleonomic mechanisms in cellular metabolism, growth, and differentiation. Cold Spring Harb Symp Quant Biol 26: 389-401.
42. Ramakrishnan N, Bhalla US, (2008) Memory switches in chemical reaction space. PLoS Comput Biol 4: e1000122.
43. Ma W, Trusina A, El-Samad H, Lim WA, Tang C, (2009) Defining network topologies that can achieve biochemical adaptation. Cell 138: 760-73.
44. Sabouri-Ghomi M, Ciliberto A, Kar S, Novák B, Tyson JJ, (2008) Antagonism and bistability in protein interaction networks. J Theor Biol 250: 209-18.
45. Bundschuh R, Hayot F, Jayaprakash C, (2003) Fluctuations and slow variables in genetic networks. Biophys J 84: 1606-15.
46. Stamatakis M, Mantzaris NV, (2009) Comparison of deterministic and stochastic models of the lac operon genetic network. Biophys J 96: 887-906.
47. Kepler TB, Elston TC, (2001) Stochasticity in transcriptional regulation: origins, consequences, and mathematical representations. Biophys J 81: 3116-36.
48. Blake WJ, Kaern M, Cantor CR, Collins JJ, (2003) Noise in eukaryotic gene expression. Nature 422: 633-7.
49. Samoilov M, Plyasunov S, Arkin AP, (2005) Stochastic amplification and signaling in enzymatic futile cycles through noise-induced bistability with oscillations. Proc Natl Acad Sci USA 102: 2310-5.
50. Arkin AP, Ross J, McAdams HH, (1998) Stochastic kinetic analysis of developmental pathway bifurcation in phage lambda-infected Escherichia coli cells. Genetics 149: 1633-48.
51. Gillespie DT, (2007) Stochastic simulation of chemical kinetics. Annu Rev Phys Chem 58: 35-55.
52. Jenal U, Hengge-Aronis R, (2003) Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 6: 163-72.
53. Johnson PR, Swanson R, Rakhilina L, Hochstrasser M, (1998) Degradation signal masking by heterodimerization of MATα2 and MATa1 blocks their mutual destruction by the ubiquitinproteasome pathway. Cell 94: 217-27.
54. Kelemen JZ, Ratna P, Scherrer S, Becskei A, (2010) Spatial epigenetic control of mono- and bistable gene expression. PLoS Biol 8: e1000332.
55. Soranzo N, Altafini C, (2009) ERNEST: a toolbox for chemical reaction network theory. Bioinformatics 25: 2853-4.
56. Chothia C, Gough J, Vogel C, Teichmann SA, (2003) Evolution of the protein repertoire. Science 300: 1701-3.
57. Force A, Cresko WA, Pickett FB, Proulx SR, Amemiya C, et al. (2005) The origin of subfunctions and modular gene regulation. Genetics 170: 433-46.
58. Lynch M, Conery JS, (2003) The origins of genome complexity. Science 302: 1401-4.
59. Buljan M, Frankish A, Bateman A, (2010) Quantifying the mechanisms of domain gain in animal proteins. Genome Biol 11: R74.
60. Babushok DV, Ostertag EM, Kazazian HH, (2007) Current topics in genome evolution: molecular mechanisms of new gene formation. Cell Mol Life Sci 64: 542-54.
61. Koonin EV, Aravind L, Kondrashov AS, (2000) The impact of comparative genomics on our understanding of evolution. Cell 101: 573-6.
62. Veening JW, Smits WK, Kuipers OP, (2008) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62: 193-210.
63. Jablonka E, Lamb M, (1998) Epigenetic inheritance in evolution. J Evol Biol 11: 159-183.
64. Bishop AL, Rab FA, Sumner ER, Avery SV, (2007) Phenotypic heterogeneity can enhance rare-cell survival in 'stress-sensitive' yeast populations. Mol Microbiol 63: 507-20.
65. Kussell E, Leibler S, (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-8.
66. Dubnau D, Losick R, (2006) Bistability in bacteria. Mol Microbiol 61: 564-72.
67. Hollenhorst PC, Pietz G, Fox CA, (2001) Mechanisms controlling differential promoter-occupancy by the yeast forkhead proteins Fkh1p and Fkh2p: implications for regulating the cell cycle and differentiation. Genes Dev 15: 2445-56.
68. Zhu G, Spellman PT, Volpe T, Brown PO, Botstein D, et al. (2000) Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 406: 90-4.
69. Hannenhalli S, Kaestner KH, (2009) The evolution of Fox genes and their role in development and disease. Nat Rev Genet 10: 233-40.
70. Lamb TM, Mitchell AP, (2003) The transcription factor Rim101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae. Mol Cell Biol 23: 677-86.
71. Bensen ES, Martin SJ, Li M, Berman J, Davis DA, (2004) Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol Microbiol 54: 1335-51.
72. Kumamoto CA, Vinces MD, (2005) Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol 7: 1546-54.
73. Baumgartner U, Hamilton B, Piskacek M, Ruis H, Rottensteiner H, (1999) Functional analysis of the zn(2)cys(6) transcription factors oaf1p and pip2p. different roles in fatty acid induction of beta-oxidation in saccharomyces cerevisiae. J Biol Chem 274: 22208-16.
74. Smith JJ, Ramsey SA, Marelli M, Marzolf B, Hwang D, et al. (2007) Transcriptional responses to fatty acid are coordinated by combinatorial control. Mol Syst Biol 3: 115.
75. Andrianantoandro E, Basu S, Karig DK, Weiss R, (2006) Synthetic biology: new engineering rules for an emerging discipline. Mol Syst Biol 2: 2006.0028.
76. Ellis T, Wang X, Collins JJ, (2009) Diversity-based, model-guided construction of synthetic gene networks with predicted functions. Nat Biotechnol 27: 465-71.
77. Shinar G, Feinberg M, (2010) Structural sources of robustness in biochemical reaction networks. Science 327: 1389-91.
78. Bailey JE, (2001) Complex biology with no parameters. Nat Biotechnol 19: 503-4.
79. Harbison C, Gordon D, Lee T, Rinaldi N, Macisaac K, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
80. Drobna E, Bialkova A, Subik J, (2008) Transcriptional regulators of seven yeast species: Comparative genome analysis- review. Folia Microbiol 53: 275-287.
81. Breitkreutz BJ, Stark C, Reguly T, Boucher L, Breitkreutz A, et al. (2008) The BioGRID interaction database: 2008 update. Nucleic Acids Res 36: D637-D640.
82. Teixeira MC, Monteiro P, Jain P, Tenreiro S, Fernandes AR, et al. (2006) The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 34: D446-D451.