Multiscale models of cell signaling

Annals of Biomedical Engineering

Volumn 40, Issue 11, 2012, Pages 2319-2327

  Bajikar, Sameer S ^a   Janes, Kevin A ^a  

^a University of Virginia   (United States)

Author keywords

Molecular biology; Multiscale modeling; Stochastic; Systems biology

Indexed keywords

CELL SIGNALING; COMPUTATIONAL APPROACH; COMPUTATIONAL MODEL; DATA SETS; MULTI-SCALE MODELING; MULTISCALE MODELS; SINGLE CELLS; STOCHASTIC; SYSTEMS BIOLOGY; WHOLE CELL;

MOLECULAR BIOLOGY; SIGNAL TRANSDUCTION;

COMPUTATIONAL METHODS;

ANIMAL; BIOLOGICAL MODEL; HUMAN; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 84868376130     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-012-0560-1     Document Type: Article

References (82)

1. Albeck, J.G., J.M.Burke, S. L. Spencer,D.A.Lauffenburger, and P. K. Sorger. Modeling a snap-action, variable-delay switch controlling extrinsic cell death. PLoS Biol. 6(12):2831-2852, 2008.
2. Albeck, J. G., G. MacBeath, F. M. White, P. K. Sorger, D. A. Lauffenburger, and S. Gaudet. Collecting and organizing systematic sets of protein data. Nat. Rev. Mol. Cell Biol. 7(11):803-812, 2006.
3. Aldridge, B. B., J. Saez-Rodriguez, J. L. Muhlich, P. K. Sorger, and D. A. Lauffenburger. Fuzzy logic analysis of kinase pathway crosstalk in TNF/EGF/insulin-induced signaling. PLoS Comput. Biol. 5(4):e1000340, 2009.
4. Alexander, J., D. Lim, B. A. Joughin, B. Hegemann, J. R. Hutchins, T. Ehrenberger, F. Ivins, F. Sessa, O. Hudecz, E. A. Nigg, A. M. Fry, A. Musacchio, P. T. Stukenberg, K. Mechtler, J. M. Peters, S. J. Smerdon, and M. B. Yaffe. Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for contextdependent mitotic signaling. Sci. Signal 4(179):ra42, 2011.
5. Alon, U., M. G. Surette, N. Barkai, and S. Leibler. Robustness in bacterial chemotaxis. Nature 397(6715):168- 171, 1999.
6. Altan-Bonnet, G., and R. N. Germain. Modeling T cell antigen discrimination based on feedback control of digital ERK responses. PLoS Biol. 3(11):e356, 2005.
7. Anderson, A. R., A. M. Weaver, P. T. Cummings, and V. Quaranta. Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell 127(5):905-915, 2006.
8. Basak, S., H. Kim, J. D. Kearns, V. Tergaonkar, E. O'Dea, S. L. Werner, C. A. Benedict, C. F. Ware, G. Ghosh, I. M. Verma, and A. Hoffmann. A fourth IkappaB protein within the NF-kappaB signaling module. Cell 128(2):369-381, 2007.
9. Bendall, S. C., E. F. Simonds, P. Qiu, A. D. Amir el, P. O. Krutzik, R. Finck, R. V. Bruggner, R. Melamed, A. Trejo, O. I. Ornatsky, R. S. Balderas, S. K. Plevritis, K. Sachs, D. Pe'er, S. D. Tanner, and G. P. Nolan. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332(6030):687-696, 2011.
10. Bentele, M., I. Lavrik, M. Ulrich, S. Stosser, D. W. Heermann, H. Kalthoff, P. H. Krammer, and R. Eils. Mathematical modeling reveals threshold mechanism in CD95-induced apoptosis. J. Cell Biol. 166(6):839-851, 2004.
11. Bhalla, U. S., and R. Iyengar. Emergent properties of networks of biological signaling pathways. Science 283(5400):381-387, 1999.
12. Blinov, M. L., J. R. Faeder, B. Goldstein, and W. S. Hlavacek. BioNetGen: software for rule-based modeling of signal transduction based on the interactions of molecular domains. Bioinformatics 20(17):3289-3291, 2004.
13. Blinov, M. L., J. R. Faeder, J. Yang, B. Goldstein, and W. S. Hlavacek. 'On-the-fly' or 'generate-first' modeling? Nat. Biotechnol. 23(11):1344-1345; author reply 1345, 2005.
14. Blume-Jensen, P., and T. Hunter. Oncogenic kinase signalling. Nature 411(6835):355-365, 2001.
15. Borisov, N., E. Aksamitiene, A. Kiyatkin, S. Legewie, J. Berkhout, T. Maiwald, N. P. Kaimachnikov, J. Timmer, J. B. Hoek, and B. N. Kholodenko. Systems-level interactions between insulin-EGF networks amplify mitogenic signaling. Mol. Syst. Biol. 5:256, 2009.
16. Chatterjee, M. S., J. E. Purvis, L. F. Brass, and S. L. Diamond. Pairwise agonist scanning predicts cellular signaling responses to combinatorial stimuli. Nat. Biotechnol. 28(7):727-732, 2010.
17. Chen, W. W., B. Schoeberl, P. J. Jasper, M. Niepel, U. B. Nielsen, D. A. Lauffenburger, and P. K. Sorger. Inputoutput behavior of ErbB signaling pathways as revealed by a mass action model trained against dynamic data. Mol. Syst. Biol. 5:239, 2009.
18. Clancy, C. E., and Y. Rudy. Linking a genetic defect to its cellular phenotype in a cardiac arrhythmia. Nature 400(6744):566-569, 1999.
19. Cohen, P., and M. Tcherpakov. Will the ubiquitin system furnish as many drug targets as protein kinases? Cell 143(5):686-693, 2010.
20. Cohen-Saidon, C., A. A. Cohen, A. Sigal, Y. Liron, and U. Alon. Dynamics and variability of ERK2 response to EGFin individual living cells. Mol. Cell 36(5):885-893, 2009.
21. Cosgrove, B. D., L. G. Alexopoulos, T. C. Hang, B. S. Hendriks, P. K. Sorger, L. G. Griffith, and D. A. Lauffenburger. Cytokine-associated drug toxicity in human hepatocytes is associated with signaling network dysregulation. Mol. BioSyst. 6(7):1195-1206, 2010.
22. Downward, J. The ins and outs of signalling. Nature 411(6839):759-762, 2001.
23. Emanuele, M. J., A. E. Elia, Q. Xu, C. R. Thoma, L. Izhar, Y. Leng, A. Guo, Y. N. Chen, J. Rush, P. W. Hsu, H. C. Yen, and S. J. Elledge. Global identification of modular cullin-RING ligase substrates. Cell 147(2):459-474, 2011.
24. Faeder, J. R., M. L. Blinov, B. Goldstein, and W. S. Hlavacek. Combinatorial complexity and dynamical restriction of network flows in signal transduction. Syst. Biol. (Stevenage) 2(1):5-15, 2005.
25. Ferrell, J. E., Jr., and E. M. Machleder. The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science 280(5365):895-898, 1998.
26. Friedman, N., M. Linial, I. Nachman, and D. Pe'er. Using Bayesian networks to analyze expression data. J. Comput. Biol. 7(3-4):601-620, 2000.
27. Furdui, C. M., E. D. Lew, J. Schlessinger, and K. S. Anderson. Autophosphorylation of FGFR1 kinase is mediated by a sequential and precisely ordered reaction. Mol. Cell 21(5):711-717, 2006.
28. Garmaroudi, F. S., D. Marchant, X. Si, A. Khalili, A. Bashashati, B. W. Wong, A. Tabet, R. T. Ng, K. Murphy, H. Luo, K. A. Janes, and B. M. McManus. Pairwise network mechanisms in the host signaling response to coxsackievirus B3 infection. Proc. Natl Acad. Sci. USA 107(39):17053-17058, 2010.
29. Gaudet, S., K. A. Janes, J. G. Albeck, E. A. Pace, D. A. Lauffenburger, and P. K. Sorger. A compendium of signals and responses triggered by prodeath and prosurvival cytokines. Mol. Cell. Proteomics 4(10):1569-1590, 2005.
30. Geva-Zatorsky, N., E. Dekel, A. A. Cohen, T. Danon, L. Cohen, and U. Alon. Protein dynamics in drug combinations: a linear superposition of individual-drug responses. Cell 140(5):643-651, 2010.
31. Gilman, A. G., M. I. Simon, H. R. Bourne, B. A. Harris, R. Long, E. M. Ross, J. T. Stull, R. Taussig, A. P. Arkin, M. H. Cobb, J. G. Cyster, P. N. Devreotes, J. E. Ferrell, D. Fruman, M. Gold, A. Weiss, M. J. Berridge, L. C. Cantley, W. A. Catterall, S. R. Coughlin, E. N. Olson, T. F. Smith, J. S. Brugge, D. Botstein, J. E. Dixon, T. Hunter, R. J. Lefkowitz, A. J. Pawson, P. W. Sternberg, H. Varmus, S. Subramaniam, R. S. Sinkovits, J. Li, D. Mock, Y. Ning, B. Saunders, P. C. Sternweis, D. Hilgemann, R. H. Scheuermann, D. DeCamp, R. Hsueh, K. M. Lin, Y. Ni, W. E. Seaman, P. C. Simpson, T. D. O'Connell, T. Roach, S. Choi, P. Eversole-Cire, I. Fraser, M. C. Mumby, Y. Zhao, D. Brekken, H. Shu, T. Meyer, G. Chandy, W. D. Heo, J. Liou, N. O'Rourke, M. Verghese, S. M. Mumby, H. Han, H. A. Brown, J. S. Forrester, P. Ivanova, S. B. Milne, P. J. Casey, T. K. Harden, J. Doyle, M. L. Gray, S. Michnick, M. A. Schmidt, M. Toner, R. Y. Tsien, M. Natarajan, R. Ranganathan, and G. R. Sambrano. Overview of the alliance for cellular signaling. Nature 420(6916):703-706, 2002.
32. Goentoro, L., O. Shoval, M. W. Kirschner, and U. Alon. The incoherent feedforward loop can provide fold-change detection in gene regulation. Mol. Cell 36(5):894-899, 2009.
33. Gordus, A., J. A. Krall, E. M. Beyer, A. Kaushansky, A. Wolf-Yadlin, M. Sevecka, B. H. Chang, J. Rush, and G. MacBeath. Linear combinations of docking affinities explain quantitative differences in RTK signaling. Mol. Syst. Biol. 5:235, 2009.
34. Hatzivassiliou, G., K. Song, I. Yen, B. J. Brandhuber, D. J. Anderson, R. Alvarado, M. J. Ludlam, D. Stokoe, S. L. Gloor, G. Vigers, T. Morales, I. Aliagas, B. Liu, S. Sideris, K. P. Hoeflich, B. S. Jaiswal, S. Seshagiri, H. Koeppen, M. Belvin, L. S. Friedman, and S. Malek. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 464(7287):431-435, 2010.
35. Hayenga, H. N., B. C. Thorne, S. M. Peirce, and J. D. Humphrey. Ensuring congruency in multiscale modeling: towards linking agent based and continuum biomechanical models of arterial adaptation. Ann. Biomed. Eng. 39(11):2669-2682, 2011.
36. Hlavacek, W. S., and J. R. Faeder. The complexity of cell signaling and the need for a new mechanics. Sci. Signal. 2(81):pe46, 2009.
37. Hoffmann, A., A. Levchenko, M. L. Scott, and D. Baltimore. The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation. Science 298(5596):1241-1245, 2002.
38. Hsueh, R. C., M. Natarajan, I. Fraser, B. Pond, J. Liu, S. Mumby, H. Han, L. I. Jiang, M. I. Simon, R. Taussig, and P. C. Sternweis. Deciphering signaling outcomes from a system of complex networks. Sci. Signal. 2(71):ra22, 2009.
39. Huang, P. H., and F. M. White. Phosphoproteomics: unraveling the signaling web. Mol. Cell 31(6):777-781, 2008.
40. Hutti, J. E., E. T. Jarrell, J. D. Chang, D. W. Abbott, P. Storz, A. Toker, L. C. Cantley, and B. E. Turk. A rapid method for determining protein kinase phosphorylation specificity. Nat. Methods 1(1):27-29, 2004.
41. Ideker, T., T. Galitski, and L. Hood. A new approach to decoding life: systems biology. Annu. Rev. Genomics Hum. Genet. 2:343-372, 2001.
42. Jain, A., R. Liu, B. Ramani, E. Arauz, Y. Ishitsuka, K. Ragunathan, J. Park, J. Chen, Y. K. Xiang, and T. Ha. Probing cellular protein complexes using single-molecule pull-down. Nature 473(7348):484-488, 2011.
43. Janes, K. A. Paring down signaling complexity. Nat. Biotechnol. 28(7):681-682, 2010.
44. Janes, K. A., J. G. Albeck, S. Gaudet, P. K. Sorger, D. A. Lauffenburger, and M. B. Yaffe. A systems model of signaling identifies a molecular basis set for cytokine-induced apoptosis. Science 310(5754):1646-1653, 2005.
45. Janes, K. A., S. Gaudet, J. G. Albeck, U. B. Nielsen, D. A. Lauffenburger, and P. K. Sorger. The response of human epithelial cells to TNF involves an inducible autocrine cascade. Cell 124(6):1225-1239, 2006.
46. Janes, K. A., and D. A. Lauffenburger. A biological approach to computational models of proteomic networks. Curr. Opin. Chem. Biol. 10(1):73-80, 2006.
47. Janes, K. A., H. C. Reinhardt, and M. B. Yaffe. Cytokineinduced signaling networks prioritize dynamic range over signal strength. Cell 135(2):343-354, 2008.
48. Janes, K. A., C. C. Wang, K. J. Holmberg, K. Cabral, and J. S. Brugge. Identifying single-cell molecular programs by stochastic profiling. Nat. Methods 7(4):311-317, 2010.
49. Janes, K. A., and M. B. Yaffe. Data-driven modelling of signal-transduction networks. Nat. Rev. Mol. Cell Biol. 7(11):820-828, 2006.
50. Kemp, M. L., L. Wille, C. L. Lewis, L. B. Nicholson, and D. A. Lauffenburger. Quantitative network signal combinations downstream of TCR activation can predict IL-2 production response. J. Immunol. 178(8):4984-4992, 2007.
51. Kholodenko, B. N., O. V. Demin, G. Moehren, and J. B. Hoek. Quantification of short term signaling by the epidermal growth factor receptor. J. Biol. Chem. 274(42): 30169-30181, 1999.
52. Kim, W., E. J. Bennett, E. L. Huttlin, A. Guo, J. Li, A. Possemato, M. E. Sowa, R. Rad, J. Rush, M. J. Comb, J. W. Harper, and S. P. Gygi. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44(2):325-340, 2011.
53. Kumar, D., R. Srikanth, H. Ahlfors, R. Lahesmaa, and K. V. S. Rao. Capturing cell-fate decisions from the molecular signatures of a receptor-dependent signaling response. Mol. Syst. Biol. 3:150, 2007.
54. Kumar, N., A. Wolf-Yadlin, F. M. White, and D. A. Lauffenburger. Modeling HER2 effects on cell behavior from mass spectrometry phosphotyrosine data. PLoS Comput. Biol. 3(1):e4, 2007.
55. Lander, A. D., Q. Nie, and F. Y. M. Wan. Do morphogen gradients arise by diffusion? Dev. Cell 2(6):785-796, 2002.
56. Lee, E., A. Salic, R. Kruger, R. Heinrich, and M. W. Kirschner. The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol. 1(1):E10, 2003.
57. Levsky, J. M., and R. H. Singer. Gene expression and the myth of the average cell. Trends Cell Biol. 13(1):4-6, 2003.
58. Linding, R., L. J. Jensen, G. J. Ostheimer, M. A. van Vugt, C. Jorgensen, I. M. Miron, F. Diella, K. Colwill, L. Taylor, K. Elder, P. Metalnikov, V. Nguyen, A. Pasculescu, J. Jin, J. G. Park, L. D. Samson, J. R. Woodgett, R. B. Russell, P. Bork,M.B. Yaffe, and T. Pawson. Systematic discovery of in vivo phosphorylation networks. Cell 129(7):1415-1426, 2007.
59. Lok, L., and R. Brent. Automatic generation of cellular reaction networks with Moleculizer 1.0. Nat. Biotechnol. 23(1):131-136, 2005.
60. Miller-Jensen, K., K. A. Janes, J. S. Brugge, and D. A. Lauffenburger. Common effector processing mediates cellspecific responses to stimuli. Nature 448(7153):604-608, 2007.
61. Miller-Jensen, K., K. A. Janes, Y. L. Wong, L. G. Griffith, and D. A. Lauffenburger. Adenoviral vector saturates Akt pro-survival signaling and blocks insulin-mediated rescue of tumor-necrosis-factor-induced apoptosis. J. Cell Sci. 119(Pt 18):3788-3798, 2006.
62. Nakakuki, T., M. R. Birtwistle, Y. Saeki, N. Yumoto, K. Ide, T. Nagashima, L. Brusch, B. A. Ogunnaike, M. Okada-Hatakeyama, and B. N. Kholodenko. Ligandspecific c-Fos expression emerges from the spatiotemporal control of ErbB network dynamics. Cell 141(5):884-896, 2010.
63. Natarajan, M., K. M. Lin, R. C. Hsueh, P. C. Sternweis, and R. Ranganathan. A global analysis of cross-talk in a mammalian cellular signalling network. Nat. Cell Biol. 8(6):571-580, 2006.
64. Obenauer, J. C., L. C. Cantley, and M. B. Yaffe. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31(13):3635-3641, 2003.
65. O'Neill, R. A., A. Bhamidipati, X. Bi, D. Deb-Basu, L. Cahill, J. Ferrante, E. Gentalen, M. Glazer, J. Gossett, K. Hacker, C. Kirby, J. Knittle, R. Loder, C. Mastroieni, M. Maclaren, T. Mills, U. Nguyen, N. Parker, A. Rice, D. Roach, D. Suich, D. Voehringer, K. Voss, J. Yang, T. Yang, and P. B. Vander Horn. Isoelectric focusing technology quantifies protein signaling in 25 cells. Proc. Natl Acad. Sci. USA 103(44):16153-16158, 2006.
66. Oda, K., Y. Matsuoka, A. Funahashi, and H. Kitano. A comprehensive pathway map of epidermal growth factor receptor signaling. Mol. Syst. Biol., 2005. doi:10.1038/msb4100014.
67. Park, C. S., I. C. Schneider, and J. M. Haugh. Kinetic analysis of platelet-derived growth factor receptor/phosphoinositide 3-kinase/Akt signaling in fibroblasts. J. Biol. Chem. 278(39):37064-37072, 2003.
68. Peirce, S. M., E. J. Van Gieson, and T. C. Skalak. Multicellular simulation predicts microvascular patterning and in silico tissue assembly. FASEB J. 18(6):731-733, 2004.
69. Plikus, M. V., R. E. Baker, C. C. Chen, C. Fare, D. de la Cruz, T. Andl, P. K. Maini, S. E. Millar, R. Widelitz, and C. M. Chuong. Self-organizing and stochastic behaviors during the regeneration of hair stem cells. Science 332(6029):586-589, 2011.
70. Poulikakos, P. I., C. Zhang, G. Bollag, K. M. Shokat, and N. Rosen. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 464(7287):427-430, 2010.
71. Qutub, A. A., and A. S. Popel. Elongation, proliferation & migration differentiate endothelial cell phenotypes and determine capillary sprouting. BMC Syst. Biol. 3:13, 2009.
72. Sachs, K., O. Perez, D. Pe'er, D. A. Lauffenburger, and G. P. Nolan. Causal protein-signaling networks derived from multiparameter single-cell data. Science 308(5721): 523-529, 2005.
73. Rodriguez, J., L. G. Alexopoulos, J. Epperlein, R. Samaga, D. A. Lauffenburger, S. Klamt, and P. K. Sorger. Discrete logic modelling as a means to link protein signalling networks with functional analysis of mammalian signal transduction. Mol. Syst. Biol. 5:331, 2009.
74. Salic, A., E. Lee, L. Mayer, and M. W. Kirschner. Control of beta-catenin stability: reconstitution of the cytoplasmic steps of the Wnt pathway in Xenopus egg extracts. Mol. Cell 5(3):523-532, 2000.
75. Sample, C., and S. Y. Shvartsman. Multiscale modeling of diffusion in the early Drosophila embryo. Proc Natl Acad Sci USA 107(22):10092-10096, 2010.
76. Saucerman, J. J., L. L. Brunton, A. P. Michailova, and A. D. McCulloch. Modeling beta-adrenergic control of cardiac myocyte contractility in silico. J. Biol. Chem. 278(48):47997-48003, 2003.
77. Soltis, A. R., and J. J. Saucerman. Robustness portraits of diverse biological networks conserved despite order-ofmagnitude parameter uncertainty. Bioinformatics 27(20): 2888-2894, 2011.
78. Songyang, Z., S. Blechner, N. Hoagland, M. F. Hoekstra, H. Piwnica-Worms, and L. C. Cantley. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4(11):973-982, 1994.
79. Thomson, M., and J. Gunawardena. Unlimited multistability in multisite phosphorylation systems. Nature 460(7252):274-277, 2009.
80. von Mering, C., L. J. Jensen, B. Snel, S. D. Hooper, M. Krupp, M. Foglierini, N. Jouffre, M. A. Huynen, and P. Bork. STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res. 33(Database issue):D433-D437, 2005.
81. Wang, C. C., L. Jamal, and K. A. Janes. Normal morphogenesis of epithelial tissues and progression of epithelial tumors. Wiley Interdiscip. Rev. Syst. Biol. Med. 4(1):51-78, 2012.
82. Werner, S. L., D. Barken, and A. Hoffmann. Stimulus specificity of gene expression programs determined by temporal control of IKK activity. Science 309(5742):1857-1861, 2005.