Characterization of negative feedback network motifs in the TGF-β signaling pathway

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Nicklas, Daniel ^a   Saiz, Leonor ^a  

^a University of California Davis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIGAND BINDING; MATHEMATICAL MODEL; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

ALGORITHMS; ANIMALS; BONE MORPHOGENETIC PROTEINS; CATTLE; CELL LINE; CLUSTER ANALYSIS; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; LIGANDS; MICE; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84893359901     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083531     Document Type: Article

References (54)

1. Derynck R, Miyazono K (2008) The TGF-β Family. Cold Spring. Harbor, N.Y: Cold Sprint Harbor Laboratory Press. xiv, 1114 p.
2. Massagué J (1998) TGF-β Signal Transduction. Annu Rev Biochem 67: 753-791.
3. Levy L, Hill CS (2006) Alterations in components of the TGF-β superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev 17: 41-58. (Pubitemid 43117515)
4. ten Dijke P, Arthur HM (2007) Extracellular control of TGFβ signalling in vascular development and disease. Nat Rev Mol Cell Biol 8: 857-869.
5. Shi Y, Massagué J (2003) Mechanisms of TGF-β Signaling from Cell Membrane to the Nucleus. Cell 113: 685-700. (Pubitemid 36724933)
6. Moustakas A, Heldin C-H (2009) The regulation of TGFβ signal transduction. Development 136: 3699-3714.
7. Hata A, Lagna G, Massagué J, Hemmati-Brivanlou A (1998) Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 12: 186-197. (Pubitemid 28060449)
8. Nakao A, Afrakhte M, Morén A, Nakayama T, Christian JL, et al. (1997) Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 389: 631-635. (Pubitemid 27446184)
9. Goto K, Kamiya Y, Imamura T, Miyazono K, Miyazawa K (2007) Selective Inhibitory Effects Of Smad6 On Bone Morphogenetic Protein Type I Receptors. J Biol Chem 282: 20603-20611. (Pubitemid 47100044)
10. Ebisawa T, Fukuchi M, Murakami G, Chiba T, Tanaka K, et al. (2001) Smurf1 Interacts with Transforming Growth Factor-β Type I Receptor through Smad7 and Induces Receptor Degradation. J Biol Chem 276: 12477-12480.
11. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, et al. (2000) Smad7 Binds to Smurf2 to Form an E3 Ubiquitin Ligase that Targets the TGFβ Receptor for Degradation. Mol Cell 6: 1365-1375. (Pubitemid 32045929)
12. Wegner K, Bachmann A, Schad J-U, Lucarelli P, Sahle S, et al. (2012) Dynamics and feedback loops in the transforming growth factor β signaling pathway. Biophys Chem 162: 22-34.
13. Chung S-W, Miles FL, Sikes RA, Cooper CR, Farach-Carson MC, et al. (2009) Quantitative Modeling and Analysis of the Transforming Growth Factor β Signaling Pathway. Biophys J 96: 1733-1750.
14. Clarke DC, Betterton MD, Liu X (2006) Systems theory of Smad signalling. IEE Proc-Syst Biol 153: 412-424. (Pubitemid 44712257)
15. Melke P, Jönsson H, Pardali E, ten Dijke P, Peterson C (2006) A Rate Equation Approach to Elucidate the Kinetics and Robustness of the TGF-β Pathway. Biophys J 91: 4368-4380. (Pubitemid 44904224)
16. Paulsen M, Legewie S, Eils R, Karaulanov E, Niehrs C (2011) Negative feedback in the bone morphogenetic protein 4 (BMP4) synexpression group governs its dynamic signaling range and canalizes development. Proc Natl Acad Sci U S A 108: 10202-10207.
17. Schmierer B, Tournier AL, Bates PA, Hill CS (2008) Mathematical modeling identifies Smad nucleocytoplasmic shuttling as a dynamic signal-interpreting system. Proc Natl Acad Sci U S A 105: 6608-6613. (Pubitemid 351754554)
18. Vilar JMG, Jansen R, Sander C (2006) Signal Processing in the TGF-β Superfamily Ligand-Receptor Network. PLoS Comput Biol 2: e3.
19. Vilar JMG, Saiz L (2011) Trafficking coordinate description of intracellular transport control of signaling networks. Biophys J 101: 2315-2323.
20. Celliere G, Fengos G, Herve M, Iber D (2011) Plasticity of TGF-beta signaling. BMC Syst Biol 5: 184.
21. Zi Z, Feng Z, Chapnick DA, Dahl M, Deng D, et al. (2011) Quantitative analysis of transient and sustained transforming growth factor-beta signaling dynamics. Mol Syst Biol 7: 492.
22. Zi Z, Klipp E (2007) Constraint-Based Modeling and Kinetic Analysis of the Smad Dependent TGF-β Signaling Pathway. PloS One 2: e936.
23. Zi Z, Chapnick DA, Liu X (2012) Dynamics of TGF-beta/Smad signaling. FEBS Lett 586: 1921-1928.
24. Ho J, Saiz L (2011) Computational Analysis of the TGF-Beta and BMP Signal Transduction Pathways. Biophys J 100: 164a.
25. Nicklas D, Saiz L (2013) Computational modeling of Smad-mediated negative feedback and crosstalk in the TGF-β superfamily network. J R Soc Interface 10: 20130363.
26. Valdimarsdottir G, Goumans M-J, Itoh F, Itoh S, Heldin C-H, et al. (2006) Smad7 and protein phosphatase 1 α are critical determinants in the duration of TGF-β/ALK1 signaling in endothelial cells. BMC Cell Biol 7: 16.
27. Wrighton KH, Lin X, Yu PB, Feng X-H (2009) Transforming Growth Factor β Can Stimulate Smad1 Phosphorylation Independently of Bone Morphogenic Protein Receptors. J Biol Chem 284: 9755-9763.
28. Daly AC, Randall RA, Hill CS (2008) Transforming Growth Factor β-induced Smad1/5 Phosphorylation in Epithelial Cells is Mediated by Novel Receptor Complexes and Is Essential for Anchorage-Independent Growth. Mol Cell Biol 28: 6889-6902.
29. Edlund S, Lee SY, Grimsby S, Zhang S, Aspenström P, et al. (2005) Interaction between Smad7 and β-Catenin: Importance for Transforming Growth Factor β-Induced Apoptosis. Mol Cell Biol 25: 1475-1488. (Pubitemid 40204923)
30. Kitano H (2004) Biological robustness. Nat Rev Genet 5: 826-837.
31. Barkai N, Leibler S (1997) Robustness in simple biochemical networks. Nature 387: 913-917. (Pubitemid 27289593)
32. Blüthgen N, Herzel H (2003) How robust are switches in intracellular signaling cascades? J Theor Biol 225: 293-300. (Pubitemid 37355985)
33. Zi Z-K, Sun Z-R (2005) Robustness Analysis of the IFN-γ Induced JAK-STAT Signaling Pathway. J Comput Sci & Technol 20: 491-495. (Pubitemid 43257723)
34. Chen C, Cui J, Zhang W, Shen P (2007) Robustness analysis identifies the plausible model of the Bcl-2 apoptotic switch. FEBS Lett 581: 5143-5150. (Pubitemid 47576101)
35. Zou X, Liu M, Pan Z (2008) Robustness analysis of EGFR signaling network with a multi-objective evolutionary algorithm. Biosystems 91: 245-261. (Pubitemid 350297575)
36. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, et al. (2002) Network motifs: simple building blocks of complex networks. Science 298: 824-827. (Pubitemid 35231534)
37. Zi Z (2011) Sensitivity analysis approaches applied to systems biology models. IET Syst Biol 5: 336-346.
38. Hindmarsh AC, Brown PN, Grant KE, Lee SL, Serban R, et al. (2005) SUNDIALS: Suite of Nonlinear and Differential/Algebraic Equation Solvers. ACM Transactions on Mathematical Software 31: 363-396.
39. Chen YG, Hata A, Lo RS, Wotton D, Shi Y, et al. (1998) Determinants of specificity in TGF-beta signal transduction. Genes Dev 12: 2144-2152. (Pubitemid 28348038)
40. Funahashi A, Morohashi M, Kitano H (2003) CellDesigner: a process diagram editor for gene-regulatory and biochemical networks. BIOSILICO 1: 159-162.
41. Hucka M, Finney A, Sauro HM, Bolouri H, Doyle JC, et al. (2003) The systems biology markup language (SBML): a medium for representation and exchange of biochemical network models. Bioinformatics 19: 524-531. (Pubitemid 36336519)
42. Heinrich R, Neel BG, Rapoport TA (2002) Mathematical Models of Protein Kinase Signal Transduction. Mol Cell 9: 957-970. (Pubitemid 34626667)
43. Kucherenko S, Rodriguez-Fernandez M, Pantelides C, Shah N (2009) Monte Carlo evaluation of derivative-based global sensitivity measures. Reliab Eng Syst Saf 94: 1135-1148.
44. Varma A, Morbidelli M, Wu H (1999) Parametric sensitivity in chemical systems. Cambridge, U.K.; New YorkNY: Cambridge University Press. xvi, 342 p.
45. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (2007) Numerical recipes: the art of scientific computing. New York: Cambridge University Press. xxi, 1235 p.
46. Jones E, Oliphant T, Peterson P, others (2001 -) SciPy: Open source scientific tools for Python.
47. Inman GJ, Nicolás FJ, Hill CS (2002) Nucleocytoplasmic Shuttling of Smads 2, 3, and 4 Permits Sensing of TGF-β Receptor Activity. Mol Cell 10: 283-294. (Pubitemid 35007343)
48. Nicolas FJ, Hill CS (2003) Attenuation of the TGF-beta-Smad signaling pathway in pancreatic tumor cells confers resistance to TGF-beta-induced growth arrest. Oncogene 22: 3698-3711. (Pubitemid 36760732)
49. Alon U, Surette MG, Barkai N, Leibler S (1999) Robustness in bacterial chemotaxis. Nature 397: 168-171.
50. Kitano H (2007) Towards a theory of biological robustness. Mol Syst Biol 3: 137.
51. Csete ME, Doyle JC (2002) Reverse engineering of biological complexity. Science 295: 1664-1669. (Pubitemid 34202894)
52. Bode HW (1945) Network analysis and feedback amplifier design. New York: D. Van Nostrand company, inc. 2 p. l., iii-xii, 551 p. p.
53. Morén A, Itoh S, Moustakas A, Dijke P, Heldin CH (2000) Functional consequences of tumorigenic missense mutations in the amino-terminal domain of Smad4. Oncogene 19: 4396-4404.
54. Hata A, Lo RS, Wotton D, Lagna G, Massagué J (1997) Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 388: 82-87. (Pubitemid 27283893)