From structure to dynamics: Frequency tuning in the p53-Mdm2 network. I. Logical approach

Journal of Theoretical Biology

Volumn 258, Issue 4, 2009, Pages 561-577

  Abou Jaoudé, Wassim ^a   Ouattara, Djomangan A ^a   Kaufman, Marcelle ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

DNA damage response; Feedback loops; Mathematical modelling; Network dynamics; p53; Post translational modifications

Indexed keywords

PROTEIN MDM2; PROTEIN P53;

LOGISTICS; NUMERICAL MODEL; TUG;

ARTICLE; BINDING AFFINITY; BIOLOGICAL ACTIVITY; CELL STRESS; CELL TYPE; CONTROLLED STUDY; DNA BINDING; DNA REPAIR; FREQUENCY ANALYSIS; IRRADIATION; LOGIC; MOLECULAR DYNAMICS; MOLECULAR MODEL; OSCILLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN STRUCTURE; TRANSACTIVATION;

CELL NUCLEUS; CYTOPLASM; DNA DAMAGE; GENE FREQUENCY; GENE REGULATORY NETWORKS; HUMANS; LOGISTIC MODELS; MODELS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 67349272002     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2009.02.005     Document Type: Article

References (70)

1. Adimoolam S., and Ford J.M. p53 and regulation of DNA damage recognition during nucleotide excision repair. DNA Repair (Amst) 2 9 (2003) 947-954
2. Appella E., and Anderson C.W. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268 10 (2001) 2764-2772
3. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 6922 (2003) 499-506
4. Barak Y., Juven T., Haffner R., and Oren M. Mdm2 expression is induced by wild type p53 activity. EMBO J. 12 2 (1993) 461-468
5. Bar-Or R.L., Maya R., Segel L.A., Alon U., Levine A.J., and Oren M. Generation of oscillations by the p53-Mdm2 feedback loop: a theoretical and experimental study. Proc. Natl. Acad. Sci. USA 97 21 (2000) 11250-11255
6. Batchelor E., Mock C.S., Bhan I., Loewer A., and Lahav G. Recurrent initiation: a mechanism for triggering p53 pulses in response to DNA damage. Mol. Cell 30 3 (2008) 277-289
7. Bose I., and Ghosh B. The p53-Mdm2 network: from oscillations to apoptosis. J. Biosci. 32 5 (2007) 991-997
8. Bottani S., and Grammaticos B. Analysis of a minimal model for p53 oscillations. J. Theor. Biol. 249 2 (2007) 235-245
9. Brooks C.L., and Gu W. p53 ubiquitination: Mdm2 and beyond. Mol. Cell 21 3 (2006) 307-315
10. Brooks C.L., and Gu W. Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr. Opin. Cell. Biol. 15 2 (2003) 164-171
11. Chen J., Lin J., and Levine A.J. Regulation of transcription functions of the p53 tumor suppressor by the mdm-2 oncogene. Mol. Med. 1 2 (1995) 142-152
12. Chène P. The role of tetramerization in p53 function. Oncogene 20 21 (2001) 2611-2617
13. Chickarmane, V., Nadim, A., Ray, A., Sauro, H.M., 2005. A p53 oscillator model of DNA break repair control, arXiv:q-bio/0510002. Available at: 〈http://www.citebase.org/abstract?id=oai:arXiv.org:q-bio/0510002〉.
14. Ciliberto A., Novak B., and Tyson J.J. Steady states and oscillations in the p53/Mdm2 network. Cell Cycle 4 3 (2005) 488-493
15. Coutts A.S., Boulahbel H., Graham A., and Thangue N.B.L. Mdm2 targets the p53 transcription cofactor JMY for degradation. EMBO Rep. 8 1 (2007) 84-90
16. Fauré A., Naldi A., Chaouiya C., and Thieffry D. Dynamical analysis of a generic Boolean model for the control of the mammalian cell cycle. Bioinformatics 22 14 (2006) e124-e131
17. Feng Z., Hu W., Stanchina E.D., Teresky A.K., Jin S., Lowe S., et al. The regulation of AMPK beta1, TSC2, and PTEN expression by p53: stress, cell and tissue specificity, and the role of these gene products in modulating the IGF-1-AKT-mTOR pathways. Cancer Res. 67 7 (2007) 3043-3053
18. Freedman D.A., Wu L., and Levine A.J. Functions of the MDM2 oncoprotein. Cell Mol. Life Sci. 55 1 (1999) 96-107
19. Friedman P.N., Chen X., Bargonetti J., and Prives C. The p53 protein is an unusually shaped tetramer that binds directly to DNA. Proc. Natl. Acad. Sci. USA 90 8 (1993) 3319-3323
20. Gatz S.A., and Wiesmüller L. p53 in recombination and repair. Cell Death Differ. 13 6 (2006) 1003-1016
21. Geva-Zatorsky N., Rosenfeld N., Itzkovitz S., Milo R., Sigal A., Dekel E., et al. Oscillations and variability in the p53 system. Mol. Syst. Biol. 2 (2006) 2006.0033
22. Glass L., and Kauffman S.A. The logical analysis of continuous, nonlinear biochemical control networks. J. Theor. Biol. 39 (1973) 103-129
23. Gonzalez A.G., Naldi A., Sánchez L., Thieffry D., and Chaouiya C. GINsim: a software suite for the qualitative modelling, simulation and analysis of regulatory networks. Biosystems 84 2 (2006) 91-100
24. Gottlieb T.M., Martinez J.F., Seger R., Taya Y., and Oren M. Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. Oncogene 21 8 (2002) 1299-1303
25. Hamstra D.A., Bhojani M.S., Griffin L.B., Laxman B., Ross B.D., and Rehemtulla A. Real-time evaluation of p53 oscillatory behavior in vivo using bioluminescent imaging. Cancer Res. 66 15 (2006) 7482-7489
26. Haupt Y., Maya R., Kazaz A., and Oren M. Mdm2 promotes the rapid degradation of p53. Nature 387 6630 (1997) 296-299
27. Honda R., and Yasuda H. Activity of MDM2, a ubiquitin ligase, toward p53 or itself is dependent on the RING finger domain of the ligase. Oncogene 19 11 (2000) 1473-1476
28. Hu W., Feng Z., Ma L., Wagner J., Rice J.J., Stolovitzky G., and Levine A.J. A single nucleotide polymorphism in the MDM2 gene disrupts the oscillation of p53 and MDM2 levels in cells. Cancer Res. 67 6 (2007) 2757-2765
29. Kaufman M., Urbain J., and Thomas R. Towards a logical analysis of the immune response. J. Theor. Biol. 114 (1985) 527-561
30. Lahav G., Rosenfeld N., Sigal A., Geva-Zatorsky N., Levine A.J., Elowitz M.B., et al. Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat. Genet. 36 2 (2004) 147-150
31. Lozano G., and Elledge S.J. p53 sends nucleotides to repair DNA. Nature 404 6773 (2000) 24-25
32. Ma L., Wagner J., Rice J.J., Hu W., Levine A.J., and Stolovitzky G.A. A plausible model for the digital response of p53 to DNA damage. Proc. Natl. Acad. Sci. USA 102 40 (2005) 14266-14271
33. Mayo L.D., and Donner D.B. The PTEN, Mdm2, p53 tumor suppressor-oncoprotein network. Trends Biochem. Sci. 27 9 (2002) 462-467
34. Mayo L.D., Seo Y.R., Jackson M.W., Smith M.L., Guzman J.R., Korgaonkar C.K., et al. Phosphorylation of human p53 at serine 46 determines promoter selection and whether apoptosis is attenuated or amplified. J. Biol. Chem. 280 28 (2005) 25953-25959
35. McLure K.G., and Lee P.W. How p53 binds DNA as a tetramer. EMBO J. 17 12 (1998) 3342-3350
36. Meek D.W. Multisite phosphorylation and the integration of stress signals at p53. Cell Signal 10 3 (1998) 159-166
37. Momand J., Zambetti G.P., Olson D.C., George D., and Levine A.J. The Mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69 7 (1992) 1237-1245
38. Monk N.A. Oscillatory expression of Hes1, p53, and NF-kappa B driven by transcriptional time delays. Curr. Biol. 13 (2003) 1409-1413
39. Naldi, A., Thieffry, D., Chaouiya, C., 2007. Decision diagrams for the representation of logical models of regulatory networks. In: CMSB'07, Lecture Notes in Bioinformatics (LNBI), vol. 4695. pp. 233-247.
40. Offer H., Wolkowicz R., Matas D., Blumenstein S., Livneh Z., and Rotter V. Direct involvement of p53 in the base excision repair pathway of the DNA repair machinery. FEBS Lett. 450 3 (1999) 197-204
41. Ogunnaike B.A. Elucidating the digital control mechanism for DNA damage repair with the p53-Mdm2 system: single cell data analysis and ensemble modelling. J. R. Soc. Interface 3 6 (2006) 175-184
42. Oliner J.D., Pietenpol J.A., Thiagalingam S., Gyuris J., Kinzler K.W., and Vogelstein B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 362 6423 (1993) 857-860
43. Oren M. Decision making by p53: life, death and cancer. Cell Death Differ. 10 4 (2003) 431-442
44. Oren M., Damalas A., Gottlieb T., Michael D., Taplick J., Leal J.F.M., Maya R., Moas M., Seger R., Taya Y., and Ben-Ze'ev A. Regulation of p53: intricate loops and delicate balances. Biochem. Pharmacol. 64 5-6 (2002) 865-871
45. Puszyński K., Hat B., and Lipniacki T. Oscillations and bistability in the stochastic model of p53 regulation. J. Theor. Biol. 254 2 (2008) 452-465
46. Ramalingam S., Honkanen P., Young L., Shimura T., Austin J., Steeg P.S., and Nishizuka S. Quantitative assessment of the p53-Mdm2 feedback loop using protein lysate microarrays. Cancer Res. 67 13 (2007) 6247-6252
47. Remy E., Ruet P., and Thieffry D. Graphic requirements for multistability and attractive cycles in a Boolean dynamical framework. Adv. Appl. Math. 41 (2008) 335-350
48. Richard A., and Comet J.-P. Necessary conditions for multistationarity in discrete dynamical systems. Discrete Appl. Math. 155 18 (2007) 2403-2413
49. Siebert, H., Bockmayr, A., 2007. Context sensitivity in logical modelling with time delays. In: Computational Methods in Systems Biology, CMSB 2007. Lecture Notes in Bioinformatics (LNBI), vol. 4695. Springer, Berlin, pp. 64-79.
50. Siebert H., and Bockmayr A. Temporal constraints in the logical analysis of regulatory networks. Theor. Comput. Sci. 391 (2008) 258-275
51. Singh B., Reddy P.G., Goberdhan A., Walsh C., Dao S., Ngai I., et al. p53 regulates cell survival by inhibiting PIK3CA in squamous cell carcinomas. Genes Dev. 16 8 (2002) 984-993
52. Snoussi E.H. Qualitative dynamics of piecewise-linear differential equations: a discrete mapping approach. Dyn. Stability Systems 4 (1989) 189-207
53. Snoussi E.H., and Thomas R. Logical identification of all steady states: the concept of feedback loop characteristic states. Bull. Math. Biol. 55 (1993) 973-991
54. Stambolic V., MacPherson D., Sas D., Lin Y., Snow B., Jang Y., et al. Regulation of PTEN transcription by p53. Mol. Cell 8 (2001) 317-325
55. Stommel J.M., and Wahl G.M. Accelerated MDM2 auto-degradation induced by DNA-damage kinases is required for p53 activation. EMBO J. 23 (2004) 1547-1556
56. Stommel J.M., and Wahl G.M. A new twist in the feedback loop: stress-activated MDM2 destabilization is required for p53 activation. Cell Cycle 4 3 (2005) 411-417
57. Thomas R. Boolean formalization of genetic control circuits. J. Theor. Biol. 42 (1973) 563-585
58. Thomas R. Logical analysis of systems comprising feedback loops. J. Theor. Biol. 73 (1978) 631-656
59. Thomas, R., 1979. Some biological examples. In: Lecture Notes in Biomathematics, vol. 29. pp. 354-401.
60. Thomas R. Regulatory networks seen as asynchronous automata: a logical description. J. Theor. Biol. 153 (1991) 1-23
61. Thomas R., and D'Ari R. Biological Feedback (1990), CRC Press, Boca Raton, FL 316pp
62. Thomas R., and Kaufman M. Multistationarity, the basis of cell differentiation and memory II. Logical analysis of regulatory networks in terms of feedback circuits. Chaos 11 (2001) 180-195
63. Thomas R., and Kaufman M. Multistationarity, the basis of cell differentiation and memory I. Structural conditions of multistationarity and other nontrivial behavior. Chaos 11 (2001) 170-179
64. Thomas R., Thieffry D., and Kaufman M. Dynamical behaviour of biological regulatory networks-I. Biological role of feedback loops and practical use of the concept of the loop-characteristic state. Bull. Math. Biol. 5 2 (1995) 247-276
65. Tiana G., Jensen M., and Sneppen K. Time delay as a key to apoptosis induction in the p53 network. Eur. Phys. J. B 29 (2002) 135-140
66. Vogelstein B., Lane D., and Levine A.J. Surfing the p53 network. Nature 408 6810 (2000) 307-310
67. Wagner J., Ma L., Rice J.J., Hu W., Levine A.J., and Stolovitzky G.A. p53-Mdm2 loop controlled by a balance of its feedback strength and effective dampening using ATM and delayed feedback. Syst. Biol. (Stevenage) 152 3 (2005) 109-118
68. Weinberg R.L., Veprintsev D.B., and Fersht A.R. Cooperative binding of tetrameric p53 to DNA. J. Mol. Biol. 341 3 (2004) 1145-1159
69. Xirodimas D.P., Saville M.K., Bourdon J.-C., Hay R.T., and Lane D.P. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 118 1 (2004) 83-97
70. Zhang T., Brazhnik P., and Tyson J.J. Exploring mechanisms of the DNA-damage response: p53 pulses and their possible relevance to apoptosis. Cell Cycle 6 1 (2007) 85-94