Mathematical modeling and sensitivity analysis of the integrated TNFα-mediated apoptotic pathway for identifying key regulators

Computers in Biology and Medicine

Volumn 41, Issue 7, 2011, Pages 512-528

  Koh, Geoffrey ^a   Lee, Dong Yup ^a,b  

^a AGENCY FOR SCIENCE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Mathematical modeling; Regulatory mechanisms; Sensitivity analysisApoptosis

Indexed keywords

APOPTOSIS PATHWAYS; APOPTOTIC; APOPTOTIC PATHWAYS; CELLULAR PROCESS; IN-DEPTH UNDERSTANDING; INTEGRATED MODELS; KEY REGULATORS; MASS ACTION KINETICS; MATHEMATICAL MODELING; REGULATORY MECHANISM; SENSITIVITY ANALYSISAPOPTOSIS; SIGNALING PATHWAYS;

CELL DEATH; COMPUTER SIMULATION; SIGNALING;

SENSITIVITY ANALYSIS;

INHIBITOR OF APOPTOSIS PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SIMULATION;

APOPTOSIS; CASPASE 3; COMPUTER SIMULATION; GENE KNOCKDOWN TECHNIQUES; MODELS, BIOLOGICAL; NF-KAPPA B; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79959193525     PISSN: 00104825     EISSN: 18790534     Source Type: Journal    
DOI: 10.1016/j.compbiomed.2011.04.017     Document Type: Article

References (69)

1. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35(4):495-516.
2. Feig C., Peter M.E. How apoptosis got the immune system in shape. Eur. J. Immunol. 2007, 37:S61-70.
3. Opferman J.T., Korsmeyer S.J. Apoptosis in the development and maintenance of the immune system. Nat. Immunol. 2003, 4(5):410-415.
4. Eguchi K. Apoptosis in autoimmune diseases. Intern. Med. 2001, 40(4):275-284.
5. Lowe S.W., Lin A.W. Apoptosis in cancer. Carcinogenesis 2000, 21(3):485-495.
6. Mastrangelo A.J., Hardwick J.M., Betenbaugh M.J. Bcl-2 inhibits apoptosis and extends recombinant protein production in cells infected with sindbis viral vectors. Cytotechnology 1996, 22(1-3):169-178.
7. Tey B.T., Singh R.P., Piredda L., Al-Rubeai M. Infl{ligature}uence of Bcl-2 on cell death during the cultivation of a chinese hamster ovary cell line expressing a chimeric antibody. Biotechnol. Bioeng. 2000, 68:31-43.
8. Dickson A.J. Apoptosis regulation and its applications to biotechnology. Trends Biotechnol. 1998, 16(8):339-342.
9. Gill C., Mestril R., Samali A. Losing heart: the role of apoptosis in heart disease-a novel therapeutic target?. FASEB J. 2002, 16(2):135-146.
10. Aldridge B.B., Burke J.M., Lauff{ligature}enburger D.A., Sorger P.K. Physicochemical modelling of cell signalling pathways. Nat. Cell Biol. 2006, 8(11):1195-1203.
11. Klipp E., Liebermeister W. Mathematical modeling of intracellular signaling pathways. BMC Neurosci. 2006, 7(Suppl. 1):S10.
12. Rajasethupathy P., Vayttaden S.J., Bhalla U.S. Systems modeling: a pathway to drug discovery. Curr. Opin. Chem. Biol. 2005, 9(4):400-406.
13. Bentele M., Lavrik I., Ulrich M., Stösser S., Heermann D.W., Kalthoff{ligature} H., Krammer P.H., Eils R. Mathematical modeling reveals threshold mechanism in CD95-induced apoptosis. J. Cell Biol. 2004, 166(6):839-851.
14. Fussenegger M., Bailey J.E., Varner J. A mathematical model of caspase function in apoptosis. Nat. Biotechnol. 2000, 18(7):768-774.
15. Bagci E.Z., Vodovotz Y., Billiar T.R., Ermentrout G.B., Bahar I. Bistability in apoptosis: roles of Bax, Bcl-2, and mitochondrial permeability transition pores. Biophys. J. 2006, 90(5):1546-1559.
16. Roy S., Nicholson D.W. Cross-talk in cell death signaling. Curr. Opin. Chem. Biol. 2000, 192(8):F21-F25.
17. Hu H., Jiang C., Li G., Lü J. PKB/AKT and ERK regulation of caspase-mediated apoptosis by methylseleninic acid in LNCaP prostate cancer cells. Carcinogenesis 2005, 26(8):1374-1381.
18. MacEwan D.J. TNF receptor subtype signaling: diff{ligature}erences and cellular consequences. Cell. Signal. 2002, 14(6):477-492.
19. Wolf B.B., Schuler M., Echeverri F., Green D.R. Caspase-3 is the primary activator of apoptotic DNA fragmentation via DNA fragmentation factor-45/inhibitor of caspase-activated DNase inactivation. J. Biol. Chem. 1999, 274(43):30651-30656.
20. Chen G., Goeddel D.V. TNF-R1 signaling: a beautiful pathway. Science 2002, 296(5573):1634-1635.
21. Eissner G., Kolch W., Scheurich P. Ligands working as receptors: reverse signaling by members of the TNF superfamily enhance the plasticity of the immune system. Cytokine Growth Factor Rev. 2004, 15(5):353-366.
22. Micheau O., Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003, 114(2):181-190.
23. Kaufmann S.H. The intrinsic pathway of apoptosis, Apoptosis, Senescence, and Cancer 2007, Humana Press, pp. 3-30.
24. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998, 94(4):481-490.
25. Eskes R., Desagher S., Antonsson B., Martinou J.C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell Biol. 2000, 20(3):929-935.
26. Rodriguez J., Lazebnik Y. Caspase-9 and APAF-1 form an active holoenzyme. Genes Dev. 1999, 13(24):3179-3184.
27. Denault J.B., Salvesen G.S. Caspases: keys in the ignition of cell death. Chem. Rev. 2002, 102(12):4489-4500.
28. Cowling V., Downward J. Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Diff{ligature}er. 2002, 9(10):1046-1056.
29. Legewie S., Blüthgen N., Herzel H. Mathematical modeling identifi{ligature}es inhibitors of apoptosis as mediators of positive feedback and stability. PLoS Comput. Biol. 2006, 2(9):e120.
30. He K.L., Ting A.T. A20 inhibits tumor necrosis factor (TNF) alpha-induced apoptosis by disrupting recruitment of TRADD and RIP to the TNF receptor 1 complex in Jurkat T cells. Mol. Cell Biol. 2002, 22(17):6034-6045.
31. Lipniacki T., Paszek P., Brasier A.R., Luxon B., Kimmel M. Mathematical model of NF-regulatory module. J. Theor. Biol. 2004, 228(2):195-215.
32. Micheau O., Lens S., Gaide O., Alevizopoulos K., Tschopp J. NF-B signals induce the expression of c-FLIP. Mol. Cell Biol. 2001, 21(16):5299-5305.
33. Chao D.T., Korsmeyer S.J. BCL-2 family: regulators of cell death. Annu. Rev. Immunol. 1998, 16:395-419.
34. Kirsch D.G., Doseff{ligature} A., Chau B.N., Lim D.S., de Souza-Pinto N.C., Hansford R., Kastan M.B., Lazebnik Y.A., Hardwick J.M. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome c. J. Biol. Chem. 1999, 274(30):21155-21161.
35. Takahashi R., Deveraux Q., Tamm I., Welsh K., Assa-Munt N., Salvesen G.S., Reed J.C. A single BIR domain of XIAP suffi{ligature}cient for inhibiting caspases. J. Biol. Chem. 1998, 273(14):7787-7790.
36. Salvesen G.S., Duckett C.S. IAP proteins: blocking the road to death's door. Nat. Rev. Mol. Cell Biol. 2002, 3(6):401-410.
37. Huang Y., Rich R.L., Myszka D.G., Wu H. Requirement of both the second and third BIR domains for the relief of X-linked inhibitor of apoptosis protein (XIAP)-mediated caspase inhibition by Smac. J. Biol. Chem. 2003, 278(49):49517-49522.
38. Tafani M., Karpinch N.O., Serroni A., Russo M.A., Farber J.L. Re-evaluation of the distinction between Type I and Type II cells: the necessary role of the mitochondria in both the extrinsic and intrinsic signaling pathways upon Fas receptor activation. J. Cell. Physiol. 2006, 208:556-565.
39. Kuwana T., Smith J.J., Muzio M., Dixit V., Newmeyer D.D., Kornbluth S. Apoptosis induction by caspase-8 is amplifi{ligature}ed through the mitochondrial release of cytochrome c. J. Biol. Chem. 1998, 273(26):16589-16594.
40. Klipp E., Herwig R., Kowald A., Wierling C., Lehrach H. Systems Biology in Practice: Concepts, Implementation and Application 2005, John Wiley & Sons.
41. Funahashi A., Tanimura N., Morohashi M., Kitano H. CellDesigner: a process diagram editor for gene-regulatory and biochemical networks. BioSilico 2003, 1:159-162.
42. Cho K.H., Shin S.Y., Kolch W., Wolkenhauer O. Experimental design in systems biology, based on parameter sensitivity analysis using a Monte Carlo method: a case study for the TNFα mediated NF- signal transduction pathway. Simulation 2003, 79:726-739.
43. Werner S.L., Kearns J.D., Zadorozhnaya V., Lynch C., O'Dea E., Boldin M.P., Ma A., Baltimore D., Hoff{ligature}mann A. Encoding NF-B temporal control in response to TNF: distinct roles for the negative regulators IBα and A20. Genes Dev. 2008, 22(15):2093-2101.
44. Grell M., Wajant H., Zimmermann G., Scheurich P. The type 1 receptor (CD120a) is the high-affi{ligature}nity receptor for soluble tumor necrosis factor. Proc. Natl. Acad. Sci. USA 1998, 95(2):570-575.
45. Carlotti F., Chapman R., Dower S.K., Qwarnstrom E.E. Activation of nuclear factor B in single living cells. J. Biol. Chem. 1999, 274:37941-37949.
46. Chen K.C., Csikasz-Nagy A., Gyorff{ligature}y B., Val J., Novak B., Tyson J.J. Kinetic analysis of a molecular model of the budding yeast cell cycle. Mol. Biol. Cell 2000, 11(1):369-391.
47. Scaffi{ligature}di C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.M., Krammer P.H., Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 1998, 17(6):1675-1687.
48. Rangamani P., Sirovich L. Survival and apoptotic pathways initiated by TNFα: modeling and predictions. Biotechnol. Bioeng. 2007, 97(5):1216-1229.
49. Sahle S., Mendes P., Hoops S., Kummer U. A new strategy for assessing sensitivities in biochemical models. Philos. Trans. A Math. Phys. Eng. Sci. 2008, 366(1880):3619-3631.
50. Yue H., Brown M., He F., Jia J., Kell D.B. Sensitivity analysis and robust experimental design of a signal transduction pathway system. Int. J. Chem. Kin. 2008, 40(11):730-741.
51. Yue H., Brown M., Knowles J., Wang H., Broomhead D.S., Kell D.B. Insights into the behavior of systems biology models from dynamic sensitivity and identifi{ligature}ability analysis: a case study of an NFB signaling pathway. Mol. BioSyst. 2006, 2:640-649.
52. Mahdavi A., Davey R.E., Bhola P., Yin T., Zandstra P.W. Sensitivity analysis of intracellular signaling pathway kinetics predicts targets for stem cell fate control. PLoS Comput. Biol. 2007, 3(7):e130.
53. Hoops S., Sahle S., Gauges R., Lee C., Pahle J., Simus N., Singhal M., Xu L., Mendes P., Kummer U. COPASI-a COmplex PAthway SImulator. Bioinformatics 2006, 22(24):3067-3074.
54. Sass G., Shembade N.D., Haimerl F., Lamoureux N., Hashemolhosseini S., Tannapfel A., Tiegs G. TNF pretreatment interferes with mitochondrial apoptosis in the mouse liver by A20-mediated down-regulation of Bax. J. Immunol. 2007, 179(10):7042-7049.
55. Hornberger G., Spear R. An approach to the preliminary analysis of environmental systems. J. Environ. Manage. 1981, 12:7-18.
56. Zi Z., Cho K.H., Sung M.H., Xia X.F., Zheng J.S., Sun Z.R. In silico identifi{ligature}cation of the key components and steps in IFN-γ induced JAK-STAT signaling pathway. FEBS Lett. 2005, 579:1101-1108.
57. Liu B., Zhang J., Tan P.Y., Hsu D., Blom A.M., Leong B., Sethi S., Ho B., Ding J.L., Thiagarajan P.S. A computational and experimental study of the regulatory mechanisms of the complement system. PLoS Comput. Biol. 2011, 7(1):e1001059.
58. Helton J.C., Davis F.J., Johnson J.D. A comparison of uncertainty and sensitivity analysis results obtained with random and latin hypercube sampling. Reliab. Eng. Syst. Saf. 2005, 89:305-330.
59. Zi Z., Zheng Y., Rundell A.E., Klipp E. SBML-SAT: a systems biology markup language (SBML) based sensitivity analysis tool. BMC Bioinformat. 2008, 9:342.
60. Furusu A., Nakayama K., Xu Q., Konta T., Kitamura M. MAP kinase-dependent, NF-B-independent regulation of inhibitor of apoptosis protein genes by TNF-α. J. Cell Physiol. 2007, 210(3):703-710.
61. Eissing T., Conzelmann H., Gilles E.D., Allgöwer F., Bullinger E., Scheurich P. Bistability analyses of a caspase activation model for receptor-induced apoptosis. J Biol. Chem. 2004, 279(35):36892-36897.
62. Rehm M., Huber H.J., Dussman H., Prehn J.H.M. Systems analysis of eff{ligature}ector caspase activation and its control by X-linked inhibitor of apoptosis protein. EMBO J. 2006, 25(18):4338-4349.
63. Zhou Z., Gengaro P., Wang W., Wang X.Q., Li C., Faubel S., Rivard C., Schrier R.W. Role of NF-B and PI3-kinase/Akt in TNF-α-induced cytotoxicity in microvascular endothelial cells. Am. J. Physiol. Renal Physiol. 2008, 295(4):F932-F941.
64. Curtin J.F., Cotter T.G. Live and let die: regulatory mechanisms in Fas-mediated apoptosis. Cell Signal 2003, 15(11):983-992.
65. Slee E.A., Adrain C., Martin S.J. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J. Biol. Chem. 2001, 276(10):7320-7326.
66. Park Y.C., Ye H., Hsia C., Segal D., Rich R.L., Liou H.C., Myszka D.G., Wu H. A novel mechanism of TRAF signaling revealed by structural and functional analyses of the TRADD-TRAF2 interaction. Cell 2000, 101(7):777-787.
67. B. Schoeberl, Mathematical Modeling of Signal Transduction Pathways in Mammalian Cells at the Example of the EGF Induced Map Kinase Cascade and TNF Receptor Crosstalk, Ph.D. Thesis, University of Stuttgart, Stuttgart, Germany, 2003.
68. Jeong M.S., Jang S.B. Full-length Fas-associated death domain protein interacts with short form of cellular FLICE inhibitory protein. Bull. Korean Chem. Soc. 2006, 27(1):87-92.
69. Vucic D., Franklin M.C., Wallweber H.J.A., Das K., Eckelman B.P., Shin H., Elliott L.O., Kadkhodayan S., Deshayes K., Salvesen G.S., Fairbrother W.J. Engineering ML-IAP to produce an extraordinarily potent caspase 9 inhibitor: implications for smac-dependent antiapoptotic activity of ML-IAP. Biochem. J. 2005, 385(1):11-20.