BioJazz: In silico evolution of cellular networks with unbounded complexity using rule-based modeling

Nucleic Acids Research

Volumn 43, Issue 19, 2015, Pages e123-

  Feng, Song ^a   Ollivier, Julien F ^b   Swain, Peter S ^c   Soyer, Orkun S ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SCAFFOLD PROTEIN;

ALGORITHM; ALLOSTERISM; ARTICLE; ARTIFICIAL NEURAL NETWORK; BIOJAZZ; COMPUTER PROGRAM; COMPUTER SIMULATION; DYNAMICS; EVOLUTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; BIOCHEMISTRY; BIOLOGICAL MODEL; PROCEDURES; SIGNAL TRANSDUCTION; SOFTWARE; SYSTEMS BIOLOGY;

ALGORITHMS; BIOCHEMICAL PROCESSES; BIOLOGICAL EVOLUTION; COMPUTER SIMULATION; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SOFTWARE; SYSTEMS BIOLOGY;

EID: 84959318229     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv595     Document Type: Article

References (98)

1. Aldridge,B.B., Burke,J.M., Lauffenburger,D.A. and Sorger,P.K. (2006) Physicochemical modelling of cell signaling pathways. Nat. Cell Biol., 8, 1195-1203.
2. Lim,W.A. (2010) Designing customized cell signalling circuits. Nat. Rev. Mol. Cell Biol., 11, 393-403.
3. Elowitz,M. and Lim,W.A. (2010) Build life to understand it. Nature, 468, 889-890.
4. Ma,W., Trusina,A., El-Samad,H., Lim,W.A. and Tang,C. (2009) Defining network topologies that can achieve biochemical adaptation. Cell, 138, 760-773.
5. Milo,R., Itzkovitz,S., Kashtan,N., Levitt,R., Shen-Orr,S., Ayzenshtat,I., Sheffer,M. and Alon,U. (2004) Superfamilies of evolved and designed networks. Science, 303, 1538-1542.
6. Alon,U. (2007) Network motifs: theory and experimental approaches. Nat. Rev. Genet., 8, 450-461.
7. Steuer,R., Waldherr,S., Sourjik,V. and Kollmann,M. (2011) Robust signal processing in living cells. PLoS Comput. Biol., 7, e1002218.
8. Zhang,Q., Bhattacharya,S. and Andersen,M.E. (2013) Ultrasensitive response motifs: basic amplifiers in molecular signalling networks. Open Biol., 3, e130031.
9. Martins,B.M. and Swain,P.S. (2013) Ultrasensitivity in phosphorylation-dephosphorylation cycles with little substrate. PLoS Comput. Biol., 9, e1003175.
10. Levine,J.H., Fontes,M.E., Dworkin,J. and Elowitz,M.B. (2012) Pulsed feedback defers cellular differentiation. PLoS Biol., 10, e1001252.
11. Malleshaiah,M.K., Shahrezaei,V., Swain,P.S. and Michnick,S.W. (2010) The scaffold protein Ste5 directly controls a switch-like mating decision in yeast. Nature, 465, 101-105.
12. Huang,C.Y. and Ferrell,J.E. (1996) Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. U.S.A., 93, 10078-10083.
13. Bashor,C.J., Helman,N.C., Yan,S. and Lim,W.A. (2008) Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics. Science, 319, 1539-1543.
14. Lenz,P. and Swain,P.S. (2006) An entropic mechanism to generate highly cooperative and specific binding from protein phosphorylations. Curr. Biol., 16, 2150-2155.
15. Soyer,O.S. and O'Malley,M.A. (2013) Evolutionary systems biology: what it is and why it matters. Bioessays, 35, 696-705.
16. Francois,P. and Hakim,V. (2004) Design of genetic networks with specified functions by evolution in silico. Proc. Natl. Acad. Sci. U.S.A., 101, 580-585.
17. François,P. and Siggia,E.D. (2008) A case study of evolutionary computation of biochemical adaptation. Phys. Biol., 5, e026009.
18. Evlampiev,K. and Isambert,H. (2007) Modeling protein network evolution under genome duplication and domain shuffling. BMC Syst. Biol., 1, e49.
19. Soyer,O.S., Pfeiffer,T. and Bonhoeffer,S. (2006) Simulating the evolution of signal transduction pathways. J. Theor. Biol., 241, 223-232.
20. Kashtan,N., Parter,M., Dekel,E., Mayo,A.E. and Alon,U. (2009) Extinctions in heterogeneous environments and the evolution of modularity. Evolution, 63, 1964-1975.
21. Cordero,O.X. and Hogeweg,P. (2006) Feed-forward loop circuits as a side effect of genome evolution. Mol. Biol. Evol., 23, 1931-1936.
22. Bogarad,L.D. and Deem,M.W. (1999) A hierarchical approach to protein molecular evolution. Proc. Natl. Acad. Sci. U.S.A., 96, 2591-2595.
23. Crombach,A. and Hogeweg,P. (2008) Evolution of evolvability in gene regulatory networks. PLoS Comput. Biol., 4, e1000112.
24. Stekel,D.J. and Jenkins,D.J. (2012) Evolution of resource and energy management in biologically realistic gene regulatory network models. Adv. Exp. Med. Biol., 751, 301-328.
25. Sun,J. and Deem,M.W. (2007) Spontaneous emergence of modularity in a model of evolving individuals. Phys. Rev. Lett., 99, e228107.
26. Kashtan,N. and Alon,U. (2005) Spontaneous evolution of modularity and network motifs. Proc. Natl. Acad. Sci. U.S.A., 102, 13773-13778.
27. Variano,E.A., McCoy,J.H. and Lipson,H. (2004) Networks, dynamics, and modularity. Phys. Rev. Lett., 92, e188701.
28. Lipson,H., Pollack,J.B. and Suh,N.P. (2002) On the origin of modular variation. Evolution, 56, 1549-1556.
29. Deckard,A. and Sauro,H.M. (2004) Preliminary studies on the in silico evolution of biochemical networks. ChemBioChem, 5, 1423-1431.
30. Jenkins,D.J. and Stekel,D.J. (2009) A new model for investigating the evolution of transcription control networks. Artif. Life, 15, 259-291.
31. Soyer,O.S. (2007) Emergence and maintenance of functional modules in signaling pathways. BMC Evol. Biol., 7, e205.
32. Paladugu,S.R., Chickarmane,V., Deckard,A., Frumkin,J.P., McCormack,M. and Sauro,H.M. (2006) In silico evolution of functional modules in biochemical networks. IEE Proc.-Syst. Biol., 153, 223-235.
33. Goldstein,R.A. and Soyer,O.S. (2008) Evolution of taxis responses in virtual bacteria: non-adaptive dynamics. PLoS Comput. Biol., 4, e1000084.
34. Salathé,M. and Soyer,O.S. (2008) Parasites lead to evolution of robustness against gene loss in host signaling networks. Mol. Syst. Biol., 4, e202.
35. François,P. and Siggia,E.D. (2010) Predicting embryonic patterning using mutual entropy fitness and in silico evolution. Development, 137, 2385-2395.
36. Bashor,C.J., Horwitz,A.A., Peisajovich,S.G. and Lim,W.A. (2010) Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. Annu. Rev. Biophys., 39, 515-537.
37. Peisajovich,S.G., Garbarino,J.E., Wei,P. and Lim,W.A. (2010) Rapid diversification of cell signaling phenotypes by modular domain recombination. Science, 328, 368-372.
38. Ollivier,J.F., Shahrezaei,V. and Swain,P.S. (2010) Scalable rule-based modelling of allosteric proteins and biochemical networks. PLoS Comput. Biol., 6, e1000975.
39. Danos,V., Feret,J., Fontana,W., Harmer,R. and Krivine,J. (2007) Rule-based modelling of cellular signalling. In:Caires,L. and Vasconcelos,VT (eds). CONCUR 2007, Lect. Notes Comput. Sc., Springer, Berlin Heidelberg, 4703, pp. 17-41.
40. Hlavacek,W.S., Faeder,J.R., Blinov,M.L.M.L., Posner,R.G., Hucka,M.M. and Fontana,W. (2006) Rules for modeling signal-transduction systems. Sci. STKE, 344,re6.
41. Chylek,L.A., Harris,L.A., Tung,C.S., Faeder,J.R., Lopez,C.F. and Hlavacek,W.S. (2013) Rule-based modeling: a computational approach for studying biomolecular site dynamics in cell signaling systems. WIREs Syst. Biol. Med., 6, 13-36.
42. Blinov,M.L., Feader,J.R., Goldstein,B. and Hlavacek,W.S. (2004) BioNetGen: software for rule-based modeling of signal transduction based on the interaction of molecular domains. Bioinformatics, 10, 22-41.
43. Yang,J., Meng,X. and Hlavacek,W.S. (2010) Rule-based modelling and simulation of biochemical systems with molecular finite automata. IET Syst. Biol., 4, 1-23.
44. Sneddon,M.W., Faeder,J.R. and Emonet,T. (2010) Efficient modeling, simulation and coarse-graining of biological complexity with NFsim. Nat. Methods, 8, 177-183.
45. Monod,J., Wyman,J. and Changeux,J.-P. (1965) On the nature of allosteric transitions: a plausible model. J. Mol. Biol., 12, 88-118.
46. Bhattacharyya,R.P., Reményi,A., Yeh,B.J. and Lim,W.A. (2006) Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu. Rev. Biochem., 75, 655-680.
47. Jin,J., Xie,X., Chen,C., Park,J.G., Stark,C., James,D.A., Olhovsky,M., Linding,R., Mao,Y. and Pawson,T. (2009) Eukaryotic protein domains as functional units of cellular evolution. Sci. Signal., 2, ra76.
48. Halabi,N., Rivoire,O., Leibler,S. and Ranganathan,R. (2009) Protein sectors: evolutionary units of three-dimensional structure. Cell, 138, 774-786.
49. Yeh,B.J., Rutigliano,R.J., Deb,A., Bar-Sagi,D. and Lim,W.A. (2007) Rewiring cellular morphology pathways with synthetic guanine nucleotide exchange factors. Nature, 447, 596-600.
50. Dueber,J.E., Yeh,B.J., Bhattacharyya,R.P. and Lim,W.A. (2004) Rewiring cell signaling: the logic and plasticity of eukaryotic protein circuitry. Curr. Opin. Struct. Biol., 14, 690-699.
51. Park,S., Zarrinpar,A. and Lim,W.A. (2003) Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms. Science, 299, 1061-1064.
52. Dueber,J.E., Yeh,B.J., Chak,K. and Lim,W.A. (2003) Reprogramming control of an allosteric signaling switch through modular recombination. Science, 301, 1904-1908.
53. Bruschweiler,R., Liao,X. and Wright,P.E. (1995) Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling. Science, 268, 886-889.
54. Soyer,O.S. and Creevey,C.J. (2010) Duplicate retention in signalling proteins and constraints from network dynamics. J. Evol. Biol., 23, 2410-2421.
55. Zhang,J. (2003) Evolution by gene duplication: an update. Trends Ecol. Evol., 18, 292-298.
56. Björklund,A.K., Ekman,D. and Elofsson,A. (2006) Expansion of protein domain repeats. PLoS Comput. Biol., 2, e114.
57. Orr,H.A. (2009) Fitness and its role in evolutionary genetics. Nat. Rev. Genet., 10, 531-539.
58. Soyer,O.S., Salathé,M. and Bonhoeffer,S. (2006) Signal transduction networks: topology, response and biochemical processes. J. Theor. Biol., 238, 416-425.
59. Hafner,M., Koeppl,H. and Wagner,A. (2009) Evolution of feedback loops in oscillatory systems. In: Third International Conference on Foundations of Systems Biology in Engineering, pp. 157-160. http://arxiv.org/abs/1003.1231.
60. Siso-Nadal,F., Ollivier,J.F. and Swain,P.S. (2007) Facile: a command-line network compiler for systems biology. BMC Syst. Biol., 1, e36.
61. Kauffman,S. and Levin,S. (1987v) Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol., 128, 11-45.
62. Perelson,A.S. and Macken,C.A. (1995) Protein evolution on partially correlated landscapes. Proc. Natl. Acad. Sci. U.S.A., 92, 9657-9661.
63. Kauffman,S.A. and Macready,W.G. (1995) Search strategies for applied molecular evolution. J. Theor. Biol., 173, 427-440.
64. Kimura,M. (1962) On the probability of fixation of mutant genes in a population. Genetics, 47, 713-719.
65. Kimura,M. (1957) Some problems of stochastic processes in genetics. Ann. Math. Stat., 28, 882-901.
66. Desai,M.M. and Nelson,D.R. (2005) A quasispecies on a moving oasis. Theor. Popul. Biol., 67, 33-45.
67. Bull,J.J., Meyers,L.A. and Lachmann,M. (2005) Quasispecies made simple. PLoS Comput. Biol., 1, e61.
68. Hofbauer,J. and Sigmund,K. (1998) Evolutionary Games and Population Dynamics. Cambridge University Press, Cambridge.
69. Pollock,D.D., Thiltgen,G. and Goldstein,R.A. (2012) Amino acid coevolution induces an evolutionary Stokes shift. Proc. Natl. Acad. Sci. U.S.A., 109, E1352-E1359.
70. Goldstein,R.A. (2011) The evolution and evolutionary consequences of marginal thermostability in proteins. Proteins, 79, 1396-1407.
71. Lynch,M. and Conery,J.S. (2003) The origins of genome complexity. Science, 302, 1401-1404.
72. Crow,J.F. and Kimura,M. (1970) An Introduction to Population Genetics Theory. The Blackburn Press, Caldwell.
73. François,P. (2014) Evolving phenotypic networks in silico. Semin. Cell Dev. Biol., 35, 90-97.
74. Soyer,O.S. and Bonhoeffer,S. (2006) Evolution of complexity in signaling pathways. Proc. Natl. Acad. Sci. U.S.A., 103, 16337-16342.
75. Goldbeter,A. and Koshland,D.E. (1982) Sensitivity amplification in biochemical systems. Quart. Rev. Biophys., 15, 555-591.
76. Rabitz,H., Kramer,M. and Dacol,D. (1983n) Sensitivity analysis in chemical kinetics. Annu. Rev. Phys. Chem., 34, 419-461.
77. Goldbeter,A. and Koshland,D.E. (1981) An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. U.S.A., 78, 6840-6844.
78. Macnab,R.M. and Koshland,D.E. Jr (1972) The gradient-sensing mechanism in bacterial chemotaxis. Proc. Natl. Acad. Sci. U.S.A., 69, 2509-2512.
79. Barkai,N. and Leibler,S. (1997) Robustness in simple biochemical networks. Nature, 387, 913-917.
80. Alon,U., Surette,M.G., Barkai,N. and Leibler,S. (1999) Robustness in bacterial chemotaxis. Nature, 397, 168-171.
81. Klipp,E., Nordlander,B., Krüger,R., Gennemark,P. and Hohmann,S. (2005) Integrative model of the response of yeast to osmotic shock. Nat. Biotechnol., 23, 975-982.
82. Muzzey,D., Gómez-Uribe,C.A., Mettetal,J.T. and van Oudenaarden,A. (2009) A systems-level analysis of perfect adaptation in yeast osmoregulation. Cell, 138, 160-171.
83. Zi,Z., Liebermeister,W. and Klipp,E. (2010) A quantitative study of the Hog1 MAPK response to fluctuating osmotic stress in Saccharomyces cerevisiae. PLoS One, 5, e9522.
84. Behar,M., Hao,N., Dohlman,H.G. and Elston,T.C. (2007) Mathematical and computational analysis of adaptation via feedback inhibition in signal transduction pathways. Biophys. J., 93, 806-821.
85. François,P., Hakim,V. and Siggia,E.D. (2007) Deriving structure from evolution: metazoan segmentation. Mol. Syst. Biol., 3, e154.
86. Ten Tusscher,K.H. and Hogeweg,P. (2011) Evolution of networks for body plan patterning; interplay of modularity, robustness and evolvability. PLoS Comput. Biol., 7, e1002208.
87. Pfeiffer,T., Soyer,O.S. and Bonhoeffer,S. (2005) The evolution of connectivity in metabolic networks. PLoS Biol., 3, e228.
88. Lalanne,J.B. and François,P. (2013) Principles of adaptive sorting revealed by in silico evolution. Phys. Rev. Lett., 110, e218102.
89. Danos,V., Feret,J., Fontana,W. and Krivine,J. (2007) Scalable simulation of cellular signaling networks. In:Shao,Z. (ed). Programming Languages and Systems. Springer, Berlin Heidelberg, pp. 139-157.
90. Yang,J., Monine,M.I.M.I., Faeder,J.R. and Hlavacek,W.S. (2008) Kinetic Monte Carlo method for rule-based modeling of biochemical networks. Phy. Rev. E, 78, e31910.
91. Flamm,C., Ullrich,A., Ekker,H., Mann,M., Högerl,D., Rohrschneider,M., Sauer,S., Scheuermann,G., Klemm,K. and Hofacker,I.L. (2010) Evolution of metabolic networks: a computational framework. J. Syst. Chem., 1,e4.
92. Thomson,T.M., Benjamin,K.R., Bush,A., Love,T., Pincus,D., Resnekov,O., Richard,C.Y., Gordon,A., Colman-Lerner,A., Endy,D. et al. (2011) Scaffold number in yeast signaling system sets tradeoff between system output and dynamic range. Proc. Natl. Acad. Sci. U.S.A., 108, 20265-20270.
93. Fujioka,A., Terai,K., Itoh,R.E., Aoki,K., Nakamura,T., Kuroda,S., Nishida,E. and Matsuda,M. (2006) Dynamics of the Ras/ERK MAPK cascade as monitored by fluorescent probes. J. Biol. Chem., 281, 8917-8926.
94. Ghaemmaghami,S., Huh,W.K., Bower,K., Howson,R.W., Belle,A., Dephoure,N., O'Shea,E.K. and Weissman,J.S. (2003) Global analysis of protein expression in yeast. Nature, 425, 737-741.
95. Schoeberl,B., Eichler-Jonsson,C., Gilles,E.D. and Muller,G. (2002) Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat. Biotechnol., 20, 370-375.
96. Slaughter,B.D., Schwartz,J.W. and Li,R. (2007) Mapping dynamic protein interactions in MAP kinase signaling using live-cell fluorescence fluctuation spectroscopy and imaging. Proc. Natl. Acad. Sci. U.S.A., 104, 20320-20325.
97. Maeder,C.I., Hink,M.A., Kinkhabwala,A., Mayr,R., Bastiaens,P.I.H. and Knop,M. (2007) Spatial regulation of Fus3 MAP kinase activity through a reaction-diffusion mechanism in yeast pheromone signalling. Nat. Cell. Biol., 9, 1319-1326.
98. Hatakeyama,M., Kimura,S., Naka,T., Kawasaki,T., Yumoto,N., Ichikawa,M., Kim,J.H., Saito,K., Saeki,M., Shirouzu,M. et al. (2003) A computational model on the modulation of mitogen-activated protein kinase (MAPK) and Akt pathways in heregulin-induced ErbB signalling. Biochem. J., 373, 451-463.