From structure to dynamics: Frequency tuning in the p53-Mdm2 network. II. Differential and stochastic approaches.

Journal of Theoretical Biology

Volumn 264, Issue 4, 2010, Pages 1177-1189

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

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Bifurcation analysis; Feedback circuits; Mathematical modelling; P53 Mdm2 oscillations; Stochastic simulations

Indexed keywords

DNA; PROTEIN MDM2; PROTEIN P53;

MODELING; MOLECULAR ANALYSIS; NUMERICAL MODEL; PROTEIN; STOCHASTICITY;

ARTICLE; DNA DAMAGE; DOWN REGULATION; IRRADIATION; KINETICS; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; OSCILLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STRUCTURE; RADIATION DOSE; SIMULATION;

BIOLOGICAL CLOCKS; COMPUTER SIMULATION; DNA DAMAGE; HUMANS; KINETICS; PROTO-ONCOGENE PROTEINS C-MDM2; STOCHASTIC PROCESSES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77952955237     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2010.03.031     Document Type: Article

References (70)

1. Abou-Jaoudé W., Ouattara D.A., Kaufman M. From structure to dynamics: frequency tuning in the p53-mdm2 network I. Logical approach. J. Theor. Biol. 2009, 258(4):561-577.
2. Adimoolam S., Ford J.M. p53 and regulation of dna damage recognition during nucleotide excision repair. DNA Repair 2003, 2(9):947-954.
3. Andrecut M., Cloud D., Kauffman S.A. Monte carlo simulation of a simple gene network yields new evolutionary insights. J. Theor. Biol. 2008, 250(3):468-474.
4. Bakkenist C.J., Kastan M.B. Dna damage activates atm through intermolecular autophosphorylation and dimer dissociation. Nature 2003, 421(6922):499-506.
5. Bar-Or R.L., Maya R., Segel L.A., Alon U., Levine A.J., Oren M. Generation of oscillations by the p53-mdm2 feedback loop: a theoretical and experimental study. Proc. Natl. Acad. Sci. USA 2000, 97(21):11250-11255.
6. Barak Y., Juven T., Haffner R., Oren M. Mdm2 expression is induced by wild type p53 activity. EMBO J. 1993, 12(2):461-468.
7. Barik D., Paul M.R., Baumann W.T., Cao Y., Tyson J.J. Stochastic simulation of enzyme-catalyzed reactions with disparate timescales. Biophys. J. 2008, 95(8):3563-3574.
8. Batchelor E., Loewer A., Lahav G. The ups and downs of p53: understanding protein dynamics in single cells. Nat. Rev. Cancer 2009, 9(5):371-377.
9. Batchelor E., Mock C.S., Bhan I., Loewer A., Lahav G. Recurrent initiation: a mechanism for triggering p53 pulses in response to dna damage. Mol. Cell 2008, 30(3):277-289.
10. Bottani S., Grammaticos B. Analysis of a minimal model for p53 oscillations. J. Theor. Biol. 2007, 249(2):235-245.
11. Brooks C.L., Gu W. p53 ubiquitination: Mdm2 and beyond. Mol. Cell 2006, 21(3):307-315.
12. Cai X., Yuan Z.-M. Stochastic modeling and simulation of the p53-mdm2/mdmx loop. J. Comput. Biol. 2009, 16(7):917-933.
13. Chen J., Lin J., Levine A.J. Regulation of transcription functions of the p53 tumor suppressor by the mdm-2 oncogene. Mol. Med. 1995, 1(2):142-152.
14. Chène P. The role of tetramerization in p53 function. Oncogene 2001, 20(21):2611-2617.
15. Chickarmane, V., Nadim, A., Ray, A., Sauro, H.M., 2005. A p53 oscillator model of DNA break repair control. Online.
16. Ciliberto A., Capuani F., Tyson J.J. Modeling networks of coupled enzymatic reactions using the total quasi-steady state approximation. PLoS Comput. Biol. 2007, 3(3):e45.
17. Ciliberto A., Novak B., Tyson J.J. Steady states and oscillations in the p53/mdm2 network. Cell Cycle 2005, 4(3):488-493.
18. Dupont G., Abou-Lovergne A., Combettes L. Stochastic aspects of oscillatory ca2+ dynamics in hepatocytes. Biophys. J. 2008, 95(5):2193-2202.
19. Fang S., Jensen J.P., Ludwig R.L., Vousden K.H., Weissman A.M. Mdm2 is a ring finger-dependent ubiquitin protein ligase for itself and p53. J. Biol. Chem. 2000, 275(12):8945-8951.
20. Feng Z., Hu W., de Stanchina E., Teresky A.K., Jin S., Lowe S., Levine A.J. 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. 2007, 67(7):3043-3053.
21. Freedman D.A., Wu L., Levine A.J. Functions of the mdm2 oncoprotein. Cell Mol. Life Sci. 1999, 55(1):96-107.
22. Gatz S.A., Wiesmüller L. p53 in recombination and repair. Cell Death Differ. 2006, 13(6):1003-1016.
23. Geva-Zatorsky N., Rosenfeld N., Itzkovitz S., Milo R., Sigal A., Dekel E., Yarnitzky T., Liron Y., Polak P., Lahav G., Alon U. Oscillations and variability in the p53 system. Mol. Syst. Biol. 2006, 2. (2006-0033).
24. Gibson M.A., Bruck J. Approximate accelerated stochastic simulation on chemically reacting systems. J. Chem. Phys. 2001, 115(4):1716-1733.
25. Gillespie D.T. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 1977, 81(25):2340-2361.
26. Goldbeter A., Koshland D.E. An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. USA 1981, 78(11):6840-6844.
27. Gonze D., Halloy J., Golberter A. Deterministic versus stochastic models for circadian rhythms. J. Biol. Phys. 2002, 28:637-653.
28. Gonze D., Halloy J., Goldbeter A. Robustness of circadian rhythms with respect to molecular noise. Proc. Natl. Acad. Sci. USA 2002, 99(2):673-678.
29. Gottlieb T.M., Leal J.F.M., Seger R., Taya Y., Oren M. Cross-talk between akt, p53 and mdm2: possible implications for the regulation of apoptosis. Oncogene 2002, 21(8):1299-1303.
30. Goutsias J. Quasiequilibrium approximation of fast reaction kinetics in stochastic biochemical systems. J. Chem. Phys. 2005, 122(18):184102.
31. Håkansson P., Hofer A., Thelander L. Regulation of mammalian ribonucleotide reduction and dntp pools after dna damage and in resting cells. J. Biol. Chem. 2006, 281(12):7834-7841.
32. Hamstra D.A., Bhojani M.S., Griffin L.B., Laxman B., Ross B.D., Rehemtulla A. Real-time evaluation of p53 oscillatory behavior in vivo using bioluminescent imaging. Cancer Res. 2006, 66(15):7482-7489.
33. Hsu Y.-L., Kuo P.-L., Chiang L.-C., Lin C.-C. Involvement of p53, nuclear factor kappab and fas/fas ligand in induction of apoptosis and cell cycle arrest by saikosaponin d in human hepatoma cell lines. Cancer Lett. 2004, 213(2):213-221.
34. Hu W., Feng Z., Ma L., Wagner J., Rice J.J., Stolovitzky G., Levine A.J. A single nucleotide polymorphism in the mdm2 gene disrupts the oscillation of p53 and mdm2 levels in cells. Cancer Res. 2007, 67(6):2757-2765.
35. Inoue T., Geyer R.K., Howard D., Yu Z.K., Maki C.G. Mdm2 can promote the ubiquitination, nuclear export, and degradation of p53 in the absence of direct binding. J. Biol. Chem. 2001, 276(48):45255-45260.
36. Kruse J.-P., Gu W. Modes of p53 regulation. Cell 2009, 137(4):609-622.
37. Kummer U., Krajnc B., Pahle J., Green A.K., Dixon C.J., Marhl M. Transition from stochastic to deterministic behavior in calcium oscillations. Biophys. J. 2005, 89(3):1603-1611.
38. Lahav G. Oscillations by the p53-mdm2 feedback loop. Adv. Exp. Med. Biol. 2008, 641:28-38.
39. Lahav G., Rosenfeld N., Sigal A., Geva-Zatorsky N., Levine A.J., Elowitz M.B., Alon U. Dynamics of the p53-mdm2 feedback loop in individual cells. Nat. Genet. 2004, 36(2):147-150.
40. Lipniacki T., Paszek P., Brasier A.R., Luxon B., Kimmel M. Mathematical model of nf-kappab regulatory module. J. Theor. Biol. 2004, 228(2):195-215.
41. Lozano G., Elledge S.J. p53 sends nucleotides to repair DNA. Nature 2000, 404(6773):24-25.
42. Ma L., Wagner J., Rice J.J., Hu W., Levine A.J., Stolovitzky G.A. A plausible model for the digital response of p53 to DNA damage. Proc. Natl. Acad. Sci. USA 2005, 102(40):14266-14271.
43. Macnamara S., Bersani A.M., Burrage K., Sidje R.B. Stochastic chemical kinetics and the total quasi-steady-state assumption: application to the stochastic simulation algorithm and chemical master equation. J. Chem. Phys. 2008, 129(9):095105.
44. Mayo L.D., Donner D.B. A phosphatidylinositol 3-kinase/akt pathway promotes translocation of mdm2 from the cytoplasm to the nucleus. Proc. Natl. Acad. Sci. USA 2001, 98(20):11598-11603.
45. Mayo L.D., Seo Y.R., Jackson M.W., Smith M.L., Guzman J.R., Korgaonkar C.K., Donner D.B. Phosphorylation of human p53 at serine 46 determines promoter selection and whether apoptosis is attenuated or amplified. J. Biol. Chem. 2005, 280(28):25953-25959.
46. McLure K.G., Lee P.W. How p53 binds dna as a tetramer. EMBO J. 1998, 17(12):3342-3350.
47. Offer H., Wolkowicz R., Matas D., Blumenstein S., Livneh Z., Rotter V. Direct involvement of p53 in the base excision repair pathway of the dna repair machinery. FEBS Lett. 1999, 450(3):197-204.
48. Oliner J.D., Pietenpol J.A., Thiagalingam S., Gyuris J., Kinzler K.W., Vogelstein B. Oncoprotein mdm2 conceals the activation domain of tumour suppressor p53. Nature 1993, 362(6423):857-860.
49. Oren M. Decision making by p53: life, death and cancer. Cell Death Differ. 2003, 10(4):431-442.
50. Oren M., Maltzman W., Levine A.J. Post-translational regulation of the 54k cellular tumor antigen in normal and transformed cells. Mol. Cell Biol. 1981, 1(2):101-110.
51. Pahl H.L., Baeuerle P.A. Control of gene expression by proteolysis. Curr. Opinion Cell Biol. 1996, 8:340-347.
52. Proctor C.J., Gray D.A. Explaining oscillations and variability in the p53-mdm2 system. BMC Syst. Biol. 2008, 2:75.
53. Puszynỳski K., Hat B., Lipniacki T. Oscillations and bistability in the stochastic model of p53 regulation. J. Theor. Biol. 2008, 254(2):452-465.
54. Ramalingam S., Honkanen P., Young L., Shimura T., Austin J., Steeg P.S., Nishizuka S. Quantitative assessment of the p53-mdm2 feedback loop using protein lysate microarrays. Cancer Res. 2007, 67(13):6247-6252.
55. Rao C.V., Arkin A.P. Stochastic chemical kinetics and the quasi-steady-state assumption: application to the Gillespie algorithm. J. Chem. Phys. 2003, 118(11):4999-5010.
56. Reich N.C., Oren M., Levine A.J. Two distinct mechanisms regulate the levels of a cellular tumor antigen, p53. Mol. Cell Biol. 1983, 3(12):2143-2150.
57. Singh B., Reddy P.G., Goberdhan A., Walsh C., Dao S., Ngai I., Chou T.C., Charoenrat O.-P., Levine A.J., Rao P.H., Stoffel A. p53 regulates cell survival by inhibiting pik3ca in squamous cell carcinomas. Genes Dev. 2002, 16(8):984-993.
58. Stambolic V., MacPherson D., Sas D., Lin Y., Snow B., Jang Y., Benchimol S., Mak T.W. Regulation of pten transcription by p53. Mol. Cell. 2001, 8(2):317-325.
59. Stommel J.M., Wahl G.M. A new twist in the feedback loop: stress-activated mdm2 destabilization is required for p53 activation. Cell Cycle 2005, 4(3):411-417.
60. Toettcher J.E., Loewer A., Ostheimer G.J., Yaffe M.B., Tidor B., Lahav G. Distinct mechanisms act in concert to mediate cell cycle arrest. Proc. Natl. Acad. Sci. USA 2009, 106(3):785-790.
61. Tyson J.J. Another turn for p53. Mol. Syst. Biol. 2006, 2. (2006.0032).
62. Ventura A., Kirsch D.G., McLaughlin M.E., Tuveson D.A., Grimm J., Lintault L., Newman J., Reczek E.E., Weissleder R., Jacks T. Restoration of p53 function leads to tumour regression in vivo. Nature 2007, 445(7128):661-665.
63. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408(6810):307-310.
64. Vousden K.H., Lane D.P. p53 in health and disease. Nat. Rev. Mol. Cell Biol. 2007, 8(4):275-283.
65. Wagner J., Ma L., Rice J.J., Hu W., Levine A.J., 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) 2005, 152(3):109-118.
66. Wee K.B., Surana U., Aguda B.D. Oscillations of the p53-akt network: implications on cell survival and death. PLoS ONE 2009, 4(2):e4407.
67. Weinberg R.L., Freund S.M.V., Veprintsev D.B., Bycroft M., Fersht A.R. Regulation of DNA binding of p53 by its c-terminal domain. J. Mol. Biol. 2004, 342(3):801-811.
68. Zhang T., Brazhnik P., Tyson J.J. Exploring mechanisms of the DNA-damage response: p53 pulses and their possible relevance to apoptosis. Cell Cycle 2007, 6(1):85-94.
69. Zhang X.-P., Liu F., Cheng Z., Wang W. Cell fate decision mediated by p53 pulses. Proc. Natl. Acad. Sci. USA 2009, 106(30):12245-12250.
70. Zhou B.P., Liao Y., Xia W., Zou Y., Spohn B., Hung M.C. Her-2/neu induces p53 ubiquitination via akt-mediated mdm2 phosphorylation. Nat. Cell Biol. 2001, 3(11):973-982.