Dynamic network-based epistasis analysis: Boolean examples

Frontiers in Plant Science

Volumn 2, Issue DEC, 2011, Pages

  Azpeitia, Eugenio ^a,b   Benítez, Mariana ^b,c   Padilla Longoria, Pablo ^b   Espinosa Soto, Carlos ^b,d   Alvarez Buylla, Elena R ^a,b  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c MASARYK UNIVERSITY   (Czech Republic)

^d DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Boolean networks; Epistasis; Feed forward loops; Feedback loops; Gene interactions; Gene regulatory networks; Modeling; Temporal dynamics

Indexed keywords

EID: 84898834254     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2011.00092     Document Type: Article

References (92)

1. Alberch, P. (1989). The logic of monsters: evidence for internal constraint in development and evolution. Geobios Mem. Spec. 12, 21-57.
2. Albert, R., and Othmer, H. G. (2003). The topology of the regulatory interactions predicts the expression pattern of the segment polarity genes in Drosophila melanogaster. J. Theor. Biol. 223, 1-18.
3. Aldana, M., Balleza, E., Kauffman, S., and Resendiz, O. (2007). Robustness and evolvability in genetic regulatory networks. J. Theor. Biol. 245, 433-448.
4. Alvarez-Buylla, E. R., Balleza, E., Benítez, M., Espinosa-Soto, C., and Padilla-Longoria, P. (2008). "Gene regulatory network models: a dynamic and integrative approach to development,"in Practical Systems Biology, eds A. Hetherington and C. Grierson (New York, NY: Taylor and Francis).
5. Alvarez-Buylla, E. R., Benítez, M., Corvera-Poiré, A., Candor, A. C., de Folter, S., de Buen, A. G., Garay-Arroyo, A., García-Ponce, B., Jaimes-Miranda, F., Pérez-Ruiz, R. V., neiro Nelson, A. P., and Sánchez-Corrales, Y. E. (2010). Flower development. Arabidopsis Book 8, e0999.
6. Alvarez-Buylla, E. R., Benítez, M., Dávila, E. B., Chaos, A., Espinosa-Soto, C., and Padilla-Longoria, P. (2007). Gene regulatory network models for plant development. Curr. Opin. Plant Biol. 10, 83-91.
7. Alvarez-Buylla, E. R., Benítez, M., and Espinosa-Soto, C. (2011). Mutually reinforcing patterning mechanisms. Nat. Rev. Mol. Cell. Biol. 12, 533.
8. Avery, L., and Wasserman, S. (1992). Ordering gene function: the interpretation of epistasis in regulatory hierarchies. Trends Genet. 8, 312-316.
9. Aylor, D. L., and Zeng, Z. B. (2008). From classical genetics to quantitative genetics to systems biology: modeling epis-tasis. PLoS Genet. 4, e1000029. doi:10.1371/journal.pgen.1000029
10. Azpeitia, E., Benítez, M., Vega, I., Vil-larreal, C., and Alvarez-Buylla, E. R. (2010). Single-cell and coupled GRN models of cell patterning in the Arabidopsis thaliana root stem cell niche. BMC Syst. Biol. 4, 134. doi:10.1186/1752-0509-4-134
11. Balleza, E., Alvarez-Buylla, E. R., Chaos, A., Kauffman, S., Shmulevich, I., and Aldana, M. (2008). Critical dynamics in genetic regulatory networks: examples from four kingdoms. PLoS ONE 3, e2456. doi:10.1371/jour-nal.pone.0002456
12. Batten, D., Salthe, S., and Boschetti, F. (2008). Visions of evolution: self-organization proposes what natural selection disposes. Biol. Theory 3, 17-29.
13. Battle, A.L., Jonikas, M. C., Walter, P., Weissman, J. S., and Koller, D. (2010). Automated identification of pathways from quantitative genetic interaction data. Mol. Syst. Biol. 8, 379.
14. Benítez, M., Espinosa-Soto, C., Padilla-Longoria, P., and Alvarez-Buylla, E. R. (2008). Interlinked nonlinear subnetworks underlie the formation of robust cellular patterns in Ara-bidopsis epidermis: a dynamic spatial model. BMC Syst. Biol. 2, 98. doi:10.1186/1752-0509-2-98
15. Benítez, M., Monk, N. A., and Alvarez-Buylla, E. R. (2011). Epidermal patterning in Arabidopsis: models make a difference. J. Exp. Zool. B Mol. Dev. Evol. 316, 241-253.
16. Bornholdt, S. (2008). Boolean network models of cellular regulation: prospects and limitations. J. R. Soc. Interface 5(Suppl. 1), S85-S94.
17. Bowler, P. J. (1983). The Eclipse of Darwinism: Anti-Darwinian Evolution Theories in the Decades Around 1900. Baltimore: Johns Hopkins University Press.
18. Brandman, O., and Meyer, T. (2008). Feedback loops shape cellular signals in space and time. Science 322, 390-395.
19. Callebaut, W., and Rasskin-Gutman, D. (2009). Modularity: Understanding the Development and Evolution of Natural Complex Systems. Cambridge: MIT Press.
20. Calzone, L., Fages, F., and Soliman, S. (2006). BIOCHAM: an environment for modeling biological systems and formalizing experimental knowledge. Bioinformatics 22, 1805-1807.
21. Chickarmane, V., and Peterson, C. (2008). A computational model for understanding stem cell, trophecto-derm and endoderm lineage determination. PLoS ONE 3, e3478. doi:10.1371/journal.pone.0003478
22. Davidich, M. I., and Bornholdt, S. (2008). Boolean network model predicts cell cycle sequence of fission yeast. PLoS ONE 3, e1672. doi:10.1371/journal.pone.0001672
23. Davidson, E. (2001). Genomic Regulatory Systems. Development and Evolution. New York: Academic Press.
24. Davidson, E. H., and Erwin, D. H. (2006). Gene regulatory networks and the evolution of animal body plans. Science 311, 796-800.
25. de Jong, H. (2002). Modeling and simulation of genetic regulatory systems: a literature review. J. Comput. Biol. 9, 67-103.
26. de Jong, H., Geiselmann, J., Hernán-dez, C., and Page, M. (2003). Genetic network analyzer: qualitative simulation of genetic regulatory networks. Bioinformatics 19, 336-344.
27. Di Cara, A., Garg, A., De Micheli, G., Xenarios, I., and Mendoza, L. (2007). Dynamic simulation of regulatory networks using SQUAD. BMC Bioinformatics 8, 462. doi:10.1186/1471-2105-8-462
28. Didier, G., Remy, E., and Chaouiya, C. (2011). Mapping multivalued onto Boolean dynamics. J. Theor. Biol. 270, 177-184.
29. Espinosa-Soto, C., Padilla-Longoria, P., and Alvarez-Buylla, E. R. (2004). A gene regulatory network model for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. Plant Cell 16, 2923-2939.
30. Fauré, A., Naldi, A., Chaouiya, C., and Thieffry, D. (2006). Dynamical analysis of a genetic Boolean model for the control of the mammalian cell cycle. Bioinformatics 22, e124-e131.
31. Fujita, H., Toyokura, K., Okada, K., and Kawaguchi, M. (2011). Reaction-diffusion pattern in shoot apical meristem of plants. PLoS ONE 6, e18243. doi:10.1371/jour-nal.pone.0018243
32. Giacomantonio, C. E., and Good-hill, G. J. (2010). A Boolean model of the gene regulatory network underlying Mammalian cortical area development. PLoS Comput. Biol. 6, e1000936. doi:10.1371/jour-nal.pcbi.1000936
33. Gierer, A., and Meinhardt, H. (1972). A theory of biological pattern formation. Kybernetik 12, 30-39.
34. Gómez-Mena, C., de Folter, S., Costa, M. M., Angenent, G. C., and Sablowski, R. (2005). Transcrip-tional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132, 429-438.
35. Goodwin, B. (2001). How the Leopard Changed Its Spots: The Evolution of Complexity. New Jersey: Princeton University Press.
36. Gordon, S. P., Chickarmane, V. S., Ohno, C., and Meyerowitz, E. M. (2009). Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. U.S.A. 106, 16529-16534.
37. Gould, S. J. (2002). The Structure of Evolutionary Theory. Cambridge: Belk-nap Press of Harvard University Press.
38. Greenspan, R. J. (2001). The flexible genome. Nat. Rev. Genet.2,383-387.
39. Griffiths, P. E., and Gray, R. D. (1994). Developmental systems and evolutionary explanation. J. Philos. XCI, 277-304.
40. Gustafson-Brown, C., Savidge, B., and Yanofsky, M. F. (1994). Regulation of the Arabidopsis floral homeotic gene AP1. Cell 76, 131-143.
41. Huang, L. S., and Sternberg, P. W. (2006). Genetic dissection of developmental pathways. Worm Book 14, 1-19.
42. Jablonka, E., and Lamb, M. J. (2005). Evolution in Four Dimensions. Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. Cambridge: MIT Press.
43. Jaeger, J., Irons, D., and Monk, N. (2008). Regulative feedback in pattern formation: towards a general relativistic theory of positional information. Development 135, 3175-3183.
44. Jiang, X., Neapolitan, R. E., Bar-mada, M. M., and Visweswaran, S. (2011). Learning genetic epistasis using Bayesian network scoring criteria. BMC Bioinformatics 12, 89. doi:10.1186/1471-2105-12-89
45. Kaplan, S., Bren, A., Dekel, E., and Alon, U. (2008). The incoherent feed-forward loop can generate non-monotonic input functions for genes. Mol. Syst. Biol. 4, 203.
46. Kauffman, S. (1969). Homeostasis and differentiation in random genetic control networks. Nature 224, 177-178.
47. Kondo, S., and Miura, T. (2010). Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616-1620.
48. Kwon, Y. K., and Cho, K. H. (2008). Coherent coupling of feedback loops: a design principle of cell signaling networks. Bioinformatics 24, 1926-1932.
49. Levesque, M. P., Vernoux, T., Busch, W., Cui, H., Wang, J. Y., Blilou, I., Hassan, H., Nakajima, K., Matsumoto, N., Lohmann, J. U., Scheres, B., and Benfey, P. N. (2006). Whole-genome analysis of theSHORT-ROOTdevel-opmental pathway in Arabidopsis. PLoS Biol. 4, e143. doi:10.1371/jour-nal.pbio.0040143
50. Lewontin, R. (2000). "Foreword," in The Ontogeny of Information: Developmental Systems and Evolution, ed. S. Oyama (Durham: Duke University Press), vii-xv.
51. Li, F., Long, T., Lu, Y., Ouyang, Q., and Tang, C. (2004). The yeast cell-cycle network is robustly designed. Proc. Natl. Acad. Sci. U.S.A. 101, 4781-4786.
52. Li, S., Assmann, S. M., and Albert, R. (2006). Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol. 4, e312. doi:10.1371/jour-nal.pbio.0040312
53. Longo, G., and Tendero, P.-E. (2007). The differential method and the causal incompleteness of Programming Theory in Molecular Biology. Found. Sci. 12, 337-366.
54. Lorenz, K. (1965). Evolution and Modification of Behaviour. Chicago: The University of Chicago Press.
55. Mangan, S., and Alon, U. (2003). Structure and function of the feed-forward loop network motif. Proc. Natl. Acad. Sci. U.S.A. 100, 11980-11985.
56. Mangan, S., Zaslaver, A., and Alon, U. (2003). The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J. Mol. Biol. 334, 197-204.
57. Mayr, E., and Provine, W. B. (1980). The Evolutionary Synthesis: Perspectives on the Unification of Biology. Cambridge: Harvard University Press.
58. Meinhardt, H., and Gierer, A. (2000). Pattern formation by local self-activation and lateral inhibition. Bioessays 22, 753-760.
59. Milo, R., Shen-Orr, S., Itzkovitz, S., Kashtan, N., Chklovskii, D., and Alon, U. (2002). Network motifs: simple building blocks of complex networks. Science 298, 824-827.
60. Mitrophanov, A. Y., and Groisman, E. A. (2008). Positive feedback in cellular control systems. Bioessays 30, 542-555.
61. Moore, J. H., and Williams, S. M. (2005). Traversing the conceptual divide between biological and statistical epistasis: systems biology and a more modern synthesis. Bioessays 27, 637-646.
62. Morata, G., and Lawrence, P. A. (1977). Homoeotic genes, compartments and cell determination in Drosophila. Nature 265, 211-216.
63. Müller, G. B. (2007). Evo-devo: extending the evolutionary synthesis. Nat. Rev. Genet. 8, 943-949.
64. Müssel, C., Hopfensitz, M., and Kestler, H. A. (2010). BoolNet - an R package for generation, reconstruction and analysis of Boolean networks. Bioinformatics 26, 1378-1380.
65. Newman, M., Barabasi, A.-L., and Watts, D. (2006). The Structure and Dynamics of Networks. New Jersey: Princeton Studies in complexity.
66. Nijouth, H. F. (1990). Metaphors and the role of genes in development. Bioessays 12, 441-446.
67. Nochomovitz, Y. D., and Li, H. (2006). Highly designable phenotypes and mutational buffers emerge from a systematic mapping between network topology and dynamic output. Proc. Natl. Acad. Sci. U.S.A. 103, 4180-4185.
68. Oyama, S. (1985). The Ontogeny of Information: Developmental Systems and Evolution. Cambridge: Cambridge University Press.
69. Phenix, H., Morin, K., Batenchuk, C., Parker, J., Abedi, V., Yang, L., Tepliakova, L., Perkins, T. J., and Kærn, M. (2011). Quantitative epis-tasis analysis and pathway inference from genetic interaction data. PLoS Comput. Biol. 7, e1002048. doi:10.1371/journal.pcbi.1002048
70. Phillips, P. C. (2008). Epistasis - the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 9, 855-867.
71. Pigliucci, M. (2007). Do we need an extended evolutionary synthesis? Evolution 61, 2743-2749.
72. Pigliucci, M. (2009). An extended synthesis for evolutionary biology. Ann. N. Y. Acad. Sci. 1168, 218-228.
73. Pigliucci, M., and Müller, G. B. (2010). Evolution - the Extended Synthesis. Cambridge: The MIT Press.
74. Robert, J. S. (2004). Embryology, Epi-genesis and Evolution: Taking Development Seriously. Cambridge: Cambridge University Press.
75. Roeder, A. H., Tarr, P. T., Tobin, C., Zhang, X., Chickarmane, V., Cunha, A., and Meyerowitz, E. M. (2011a). Computational morphody-namics of plants: integrating development over space and time. Nat. Rev. Mol. Cell Biol. 12, 265-273.
76. Roeder, A. H., Tarr, P. T., Tobin, C., Zhang, X., Chickarmane, V., Cunha, A., and Meyerowitz, E. M. (2011b). Mutually reinforcing patterning mechanisms: authors' reply. Nat. Rev. Mol. Cell Biol. 12, 533.
77. Roth, F. P., Lipshitz, H. D., and Andrews, B. J. (2009). Q&A: epistasis. J. Biol. 8, 35.
78. Salazar-Ciudad, I. (2006). Developmental constraints vs. variational properties: how pattern formation can help to understand evolution and development. J. Exp. Zool. B Mol. Dev. Evol. 306, 107-125.
79. Savage, N. S., Walker, T., Wieck-owski, Y., Schiefelbein, J., Dolan, L., and Monk, N. A. (2008). A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biol. 6, e235. doi:10.1371/jour-nal.pbio.0060235
80. Schoof, H., Lenhard, M., Haecker, A., Mayer, K. F., Jürgens, G., and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between CLAVATA and WUSCHEL genes. Cell 100, 635-644.
81. Shen-Orr, S. S., Milo, R., Mangan, S., and Alon, U. (2002). Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31, 64-68.
82. Shmulevich, I., and Kauffman, S. A. (2004). Activities and sensitivities in boolean network models. Phys. Rev. Lett. 93, 048701.
83. St Onge, R. P., Mani, R., Oh, J., Proctor, M., Fung, E., Davis, R. W., Nis-low, C., Roth, F. P., and Giaever, G. (2007). Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat. Genet. 39, 199-206.
84. Tong, A. H., Lesage, G., Bader, G. D., Ding, H., Xu, H., Xin, X., Young, J., Berriz, G. F., Brost, R. L., Chang, M., Chen, Y., Cheng, X., Chua, G., Friesen, H., Goldberg, D. S., Haynes, J., Humphries, C., He, G., Hussein, S., Ke, L., Krogan, N., Li, Z., Levinson, J. N., Lu, H., Ménard, P., Munyana, C., Parsons, A. B., Ryan, O., Tonikian, R., Roberts, T., Sdicu, A. M., Shapiro, J., Sheikh, B., Suter, B., Wong, S. L., Zhang, L. V., Zhu, H., Burd, C. G., Munro, S., Sander, C., Rine, J., Greenblatt, J., Peter, M., Bretscher, A., Bell, G., Roth, F. P., Brown, G. W., Andrews, B., Bussey, H., and Boone, C. (2004). Global mapping of the yeast genetic interaction network. Science 303, 808-813.
85. Tyler, A. L., Asselbergs, F. W., Williams, S. M., and Moore, J. H. (2009). Shadows of complexity: what biological networks reveal about epis-tasis and pleiotropy. Bioessays 31, 220-227.
86. von Dassow, G., Meir, E., Munro, E. M., and Odell, G. M. (2000). The segment polarity network is a robust developmental module. Nature 406, 188-192.
87. Wagner, A. (1999). Causality in complex systems. Biol. Philos. 14, 83-101.
88. Wagner, A. (2009). Evolutionary constraints permeate large metabolic networks. BMC Evol. Biol. 9, 231. doi:10.1186/1471-2148-9-231
89. Wagner, G. P., Pavlicev, M., and Cheverud, J. M. (2007). The road to modularity. Nat. Rev. Genet. 8, 921-931.
90. Watson, J. D., and Crick, F. H. (1953). Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171, 737-738.
91. Wittmann, D. M., Krumsiek, J., Saez-Rodriguez, J., Lauffenburger, D. A., Klamt, S., and Theis, F. J. (2009). Transforming Boolean models to continuous models: methodology and application to T-cell receptor signaling. BMC Syst. Biol. 3, 98. doi:10.1186/1752-0509-3-98
92. Zheng, J., Zhang, D., Przytycki, P. F., Zielinski, R., Capala, J., and Przytycka, T. M. (2010). Sim-BoolNet - a Cytoscape plugin for dynamic simulation of signaling networks. Bioinformatics 26, 141-142.