Computational modeling of signaling pathways mediating cell cycle checkpoint control and apoptotic responses to ionizing radiation-induced DNA damage

Dose-Response

Volumn 10, Issue 2, 2012, Pages 251-273

  Zhao, Yuchao ^a,b   Lou, In Chio ^c   Conolly, Rory B ^a,d  

^a HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

^b BEIJING NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF MACAU   (Macao)

^d U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Apoptosis; Checkpoint arrest; Ionizing radiation; Mammalian cell cycle; Nonlinear dynamical system

Indexed keywords

ATM PROTEIN; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; HETERODIMER; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P27; PROTEIN P53; REACTIVE OXYGEN METABOLITE; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F;

APOPTOSIS; ARTICLE; BIOLISTIC TRANSFORMATION; CANCER GROWTH; CELL CYCLE CHECKPOINT; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL DEATH; CELL SURVIVAL; COMPUTER PROGRAM; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA REPAIR; DOSE RESPONSE; DOUBLE STRANDED DNA BREAK; IONIZING RADIATION; MATHEMATICAL MODEL; MOLECULAR INTERACTION; NONHUMAN; PLOTS AND CURVES; PREDICTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; QUALITATIVE ANALYSIS; RADIATION DOSE; SIGNAL TRANSDUCTION;

EID: 84863099234     PISSN: None     EISSN: 15593258     Source Type: Journal    
DOI: 10.2203/dose-response.11-021.Zhao     Document Type: Article

References (97)

1. Adams M and Carpenter PB. 2006. Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div 1: 1-19.
2. Aderem A and Smith KD. 2004. A systems approach to dissecting immunity and inflammation. Semin Immunol 16: 55-67.
3. Agarwal ML, Taylor WR, Chernov MV, Chernova OB, Stark GR. 1998. The p53 network. J Biol Chem 27: 1-4.
4. Akli S, Zheng PJ, Multani AS, Wingate HF, Pathak S, Zhang N, et al. 2004. Tumor-specific low molecular weight forms of cyclin E induce genomic instability and resistance to p21, p27, and antiestrogens in breast cancer. Cancer Res 64: 3198-3208.
5. Albeck JB, Burke JM, Aldridge BB, Zhang M, Lauffenburger DA, Sorger PK. 2008. Quantitiative analysis of pathways controlling extrinsic apoptosis in single cells. Mol Cell 30(1): 11-25.
6. Albert R and Othmer HG. 2003. The topology of the regulatory interactions predicts the expression pattern of the segment polarity genes in Drosophila melanogaster. J Theor Biol 223: 1-18.
7. Angeli D, Ferrell JE, Sontag ED. 2004. Detection of multistability, bifurcations, and hysteresis in a large class of biological positive-feedback systems. Proc Natl Acad Sci USA 101(7): 1822-1827.
8. Arroyo M and Raychaudhuri P. 1992. Retinoblastoma-repression of E2F-dependent transcription depends on the ability of the retinoblastoma protein to interact with E2F and is abrogated by the adenovirus E1A oncoprotein. Nucleic Acids Res 20: 5947-5954.
9. Azzam EI, de Toledo SM, Waker AJ and Little JB. 2000. High and low fluences of alpha-particles induce a G1 checkpoint in human diploid fibroblasts. Cancer Res 60: 2623-2631.
10. Bahassi el M, Hennigan RF, Myer DL, Stambrook PJ. 2004. Cdc25C phosphorylation on serine 191 by Plk3 promotes its nuclear translocation. Oncogene 23: 2658-2663.
11. Bakkenist CJ and Kastan MB. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 421: 499-506.
12. Bartek J and Lukas J. 2001. Pathways governing G1/S transition and their response to DNA damage. FEBS Lett 490: 117-122.
13. BEIR. 2006. Health risks from exposure to low levels of ionizing radiation: BEIR VII. Phase 2. Committee to Assess Health Risks from Exposure to Low Levels of Ionzing Radiation. Board of Radiation Effects. Research Division of Earth and Life Studeis. National Research Council of the National Academies. National Academy of Sciences (Washiongton, DC: National Academies Press).
14. Bhalla US, Ram PT, and Iyengar R. 2002. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297: 1018-1023.
15. Boreham D, Dolling J, Somers C, Quinn J, and Mitchel REJ. 2006. The adaptive response and protection against heritable mutation and fetal malformations. Dose Response 4(4): 317-326.
16. Brenner DJ, Little JB, and Sachs RK. 2001. The bystander effect in radiation oncogenesis: II. A quantitative model. Radiat Res 155: 402-408.
17. Calabrese EJ and Ricci PF. 2010. Hormesis in Environmental Health. In: Encyclopedia of Environmental Health. Elsevier Publishers (In press).
18. Chen C, Cui J, Lu R, Wang S, and Zhang, S. 2007. Modeling of the role of a Bax-activation switch in the mitochondrial apoptosis decision. Biophys J 92: 4303-4315.
19. Chao DT, Linette GP, Boise LH, White LS, Thompson CB, and Korsmeyer SJ. 1995. Bcl-XL and Bcl-2 repress a common pathway of cell death. J Exp Med 182: 821-828.
20. Cohen BL. 1995. Test of the linear-no threshold theory of radiation carcinogenesis for inhaled radon decay products. Health Phys 68(2): 157-174.
21. Conolly RB and Lutz WK. 2004. Nonmonotonic dose-response relationships: mechanistic basis, kinetic modeling, and implications for risk assessment. Toxicol Sci 77: 151-157.
22. Criswell T, Leskov K, Miyamoto S, Luo G, and Boothman DA. 2003. Transcription factors activated in mammalian cells after clinically relevant doses of ionizing radiation. Oncogene 22: 5813-5827.
23. Csikasz-Nagy A, Kapuy O, Toth A, Pal C, Jensen LJ, Uhlmann F, Tyson JJ and Novak B. 2009. Cell cycle regulation by feed-forward loops coupling transcription and phosphorylation. Mol Syst Biol 5:236.
24. Cui J, Chen H, Lu H, Sun T, and Shen P. 2008. Two independent positive feedbacks and bistability in the bcl-2 apoptotic switch. PloS ONE 3:e1469.
25. Day T, Zeng G, Hooker A, Bhat M, Scott BR, Turner DR, and Sykes PJ. 2007. Adaptive response for chromosomal inversions in pKZ1 mouse prostate induced by low doses of X radiation delivered after a high dose. Radiat Res 167: 682-692.
26. DeGregori J. 2004. The Rb network. J Cell Sci 117: 3411-3413.
27. Elledge SJ. 1996. Cell cycle checkpoints: preventing an identity crisis. Science 274: 1664-1672.
28. Eissing T, Conzelmann H, Gilles ED, Allgower F, Bullinger E, Scheurich P. 2004. Bistability analyses of a caspase activation model for receptor-induced apoptosis. 279(35): 36892-36897.
29. Fei P and El-Deiry WS. 2003. P53 and radiation responses. Oncogene 22: 5774-5783.
30. Feinendegen LE, Bond VP, Sondhaus CA, Altman KI, 1999. Cellular signal adaptation with damage control at low doses versus the predominance of DNA damage at high doses. C. R. Acad. Sci. III. 322, 245-251.
31. Feinendegen LE. 2002. Reactive oxygen species in cell responses to toxic agents. Hum Exp Toxicol 21: 85-90.
32. Fernet M, Angele S, Dork T, and Hall J. 2003. Variation in radiation-induced apoptosis in ataxia telangiectasia lymphoblastoid cell lines. Int J Radiat Biol 79: 193-202.
33. Fournier C, Wiese C, and Taucher-Scholz G. 2004. Accumulation of the cell cycle regulators TP53 and CDKN1A (p21) in human fibroblasts after exposure to low-and high-LET radiation. Radiat Res 161: 675-684.
34. Furukawa Y. 2002. Cell cycle control genes and hematopoietic cell differentiation. Leuk Lymphoma 43: 225-231.
35. Fussenegger M, Bailey JE, and Varner J. 2000. A mathematical model of caspase function in apoptosis. Nat Biotechnol 18: 768-774.
36. Gala S, Marreiros A, Stewart GJ, and Williamson P. 2001. Overexpression of E2F-1 leads to cytokineindependent proliferation and survival in the hematopoietic cell line BaF-B03. Blood 97: 227-234.
37. Gardner RD and Burke DJ. 2000. The spindle checkpoint: two transitions, two pathways. Trends Cell Biol. 10: 154-158.
38. Gupta N, Vij R, Haas-Kogan DA, Israel MA, Deen DF, and Morgan WF. 1996. Cytogenetic damage and the radiation-induced G1-phase checkpoint. Radiat Res. 145: 289-298.
39. Halaban R. 1999. Melanoma cell autonomous growth: the Rb/E2F pathway. Cancer Metastasis Rev 18: 333-343.
40. Han Z, Yang L, MacLellan WR, Weiss JN, and Qu Z. 2005. Hysteresis and cell cycle transition: How crutial is it? Biophys J 88:1626-1634.
41. Iliakis G, Wang Y, Guan J, Wang H, 2003. DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene 22, 5834-5847.
42. Kapuy O, He E, Lopez-Aviles S, Uhlmann F, Tyson JJ, and Novak B. 2009. System-level feedbacks control cell cycle progression. FEBS Lett. 22, Epub ahead of print.
43. Kaufmann WK. 1998. Human topoisomerase II function, tyrosine phosphorylation and cell cycle checkpoints. Proc Soc Exp Biol Med 217: 327-334.
44. Kitano H. 2004. Biological robustness. Nature Reviews Genetics 5: 826-837.
45. Koepp DM, Schaefer LK, Ye X, Keyomarsi K, Chu C, and Harper JW, et al., 2001. Phosphorylationdependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294: 173-177.
46. Laiho M and Latonen L. 2003. Cell cycle control, DNA damage checkpoints and cancer. Ann Med 35: 391-397.
47. Lane HA, Motoyama AB, Beuvink I and Hynes NE. 2001. Modulation of p27/Cdk2 complex formation through 4D5-mediated inhibition of HER2 receptor signaling. Ann Oncol 12 Suppl 1, S21-22.
48. Leng X, Connell-Crowley L, Goodrich D and Harper JW. 1997. S-Phase entry upon ectopic expression of G1 cyclin-dependent kinases in the absence of retinoblastoma protein phosphorylation. Curr Biol 7: 709-712.
49. Levine AJ. 1997. p53, the cellular gatekeeper for growth and division. Cell 88: 323-331.
50. Levrero M, De Laurenzi V, Costanzo A, Gong J, Wang JY, and Melino G. 2000. The p53/p63/p73 family of transcription factors: overlapping and distinct functions. J Cell Sci 113 (Pt 10): 1661-1670.
51. Li P, Li C, Zhao X, Zhang X, Nicosia SV, and Bai W. 2004. p27(Kip1) stabilization and G(1) arrest by 1,25-dihydroxyvitamin D(3) in ovarian cancer cells mediated through down-regulation of cyclin E/cyclin-dependent kinase 2 and Skp1-Cullin-F-box protein/Skp2 ubiquitin ligase. J Biol Chem 279: 25260-25267.
52. Li S, Brazhnik P, Sobral B, and Tyson JJ. 2009. Temporal controls of the asymmetric cell division cycle in Caulobacter crescentus. PLoS Comput Biol. 5(8): e1000463.
53. Little MP. 2003. Risks associated with ionizing radiation. Br Med Bull 68: 259-275.
54. Little MP, Filipe JA, Prise KM, Folkard M, and Belyakov OV. 2005. A model for radiation-induced bystander effects, with allowance for spatial position and the effects of cell turnover. J Theor Biol 232: 329-338.
55. Matsumoto H, Takahashi A, and Ohnishi T. 2004. Radiation-induced adaptive responses and bystander effects. Biol Sci Space. 18: 247-254.
56. Mikkelsen RB, and Wardman P. 2003. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 22: 5734-5754.
57. Mitchel REJ. 2007a. Cancer and low dose responses in vivo: implications for radiation protection. Dose-Response 5: 284-291
58. Mitchel REJ (2007b). Low doses of radiation reduce risk in vivo. Dose-Response 5: 1-10
59. Moberg KH, Bell DW, Wahrer DC, Haber DA, and Hariharan IK. 2001. Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 413: 311-316.
60. Moolgavkar SH, Dewanji A, and Venzon DJ, 1988. A stochastic two-stage model for cancer risk assessment. I. The hazard function and the probability of tumor. Risk Anal 8: 383-392.
61. Moolgavkar SH, and Knudson AG, Jr. 1981. Mutation and cancer: a model for human carcinogenesis. J Natl Cancer Inst 66: 1037-1052.
62. Morris EJ, and Dyson NJ. 2001. Retinoblastoma protein partners. Adv Cancer Res. 82: 1-54.
63. Nikjoo H, and Khvostunov IK, 2003. Biophysical model of the radiation-induced bystander effect. Int J Radiat Biol 79: 43-52.
64. Novak B, Pataki Z, Ciliberto A, and Tyson JJ. 2001. Mathematical model of the cell division cycle of fission yeast. Chaos. 11: 277-286.
65. Novak B, Tyson JJ, Gyorffy B, and Csikasz-Nagy A. 2007. Irreversible cell-cycle transitons are due to systmes-level feedback. Nat Cell Biol 9: 724-728.
66. Ohtani K, 1999. Implication of transcription factor E2F in regulation of DNA replication. Front Biosci 4: D793-804.
67. Pietenpol JA, and Stewart ZA. 2002. Cell cycle checkpoint signaling: cell cycle arrest versus apoptosis. Toxicology. 181-182: 475-481.
68. Qin XQ, Chittenden T, Livingston DM, and Kaelin WG, Jr. 1992. Identification of a growth suppression domain within the retinoblastoma gene product. Genes. Dev. 6: 953-964.
69. Qu Z, MacLellan WR, and Weiss JN, 2003a. Dynamics of the cell cycle: checkpoints, sizers, and timers. Biophys J 85: 3600-3611.
70. Qu Z, Weiss JN, and MacLellan WR, 2003b. Regulation of the mammalian cell cycle: a model of the G1-to-S transition. Am J Physiol Cell Physiol. 284: C349-364.
71. Qu Z, Weiss JN, and MacLellan WR. 2004. Coordination of cell growth and cell division: a mathematical study. J Cell Sci 117: 4199-4207.
72. Redpath J, Liang D, Taylor T, James C, Christie E, and Elmore E. 2001. The shape of dose-response curve for radiation-induced neoplastic transformation in vitro: evidence for an adaptive response against neoplastic transformation at low doses of low-LET radiation. Radiat Res 156:700-707.
73. Reynolds R, Witherspoon S, and Fox T, 2004. The infant mouse as a in vivo model for the detection and study of DNA damage-induced changes in the liver. Mol Carcinog 40: 62-72.
74. Russo AA, Jeffrey PD, Patten AK, Massague J, and Pavletich NP. 1996. Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382: 325-331.
75. Sakai L., Nomura T, and Ina Y. 2006. Enhancement of bio-protective functions by low dose/dose-rate radiation. Dose-Response 4:327-332.
76. Sekiguchi T., and Hunter T., 1998. Induction of growth arrest and cell death by overexpression of the cyclin-Cdk inhibitor p21 in hamster BHK21 cells. Oncogene. 16: 369-380.
77. Sherr CJ. 2000. The Pezcoller lecture: cancer cell cycles revisited. Cancer Res 60: 3689-3695.
78. Sherr CJ., and Roberts JM., 2004. Living with or without cyclins and cyclin-dependent kinases. Genes Dev. 18(22): 2699-2711.
79. Slupphaug G, Kavli B, and Krokan HE. 2003. The interacting pathways for prevention and repair of oxidative DNA damage. Mutat Res 531: 231-251.
80. Sun F, Anantharam V, Latchoumycandane C, Kanthasamy A, and Kanthasamy AG. 2005. Dieldrin Induces Ubiquitin-Proteasome Dysfunction in {alpha}-Synuclein Overexpressing Dopaminergic Neuronal Cells and Enhances Susceptibility to Apoptotic Cell Death. J Pharmacol Exp Ther 315: 69-79.
81. Tan YM, Butterworth BE, Gargas ML, and Conolly RB, 2003. Biologically motivated computational modeling of chloroform cytolethality and regenerative cellular proliferation. Toxicol Sci 75: 192-200.
82. Taylor WR, and Stark GR. 2001. Regulation of the G2/M transition by p53. Oncogene. 20: 1803-1815.
83. Thomas A, Giesler T, and White E, 2000. p53 mediates bcl-2 phosphorylation and apoptosis via activation of the Cdc42/JNK1 pathway. Oncogene. 19: 5259-5269.
84. Tubiana M, Aurengo A, Averbeck D, and Masse R. 2006. Recent reports on the effect of low doses of ionizing radiation and its dose-effect relationship. Radiat Environ Biophys 44: 245-251.
85. Tubiana M, Feinendegen LE, Yang C, and Kaminski JM. 2009. The linear no-threshold relationship is inconsistent with radiation biologic and experimental data. Radiology 251: 13-22
86. Tyson JJ, Chen K, and Novak B. 2001. Network dynamics and cell physiology. Nat Rev Mol Cell Biol. 2: 908-916.
87. Tyson JJ, and Novak B. 2001. Regulation of the eukaryotic cell cycle: molecular antagonism, hysteresis, and irreversible transitions. J Theor Biol 210: 249-263.
88. Tyson JJ, Csikasz-Nagy A, and Novak B. 2002. The dynamics of cell cycle regulation. Bioessays, 24: 1095-1109.
89. Upton AC. 2002. Carcinogenic effects of low-level ionizing radiation: problems and prospects. In. Vivo. 16: 527-533.
90. Wang B, Ohyama H, Shang Y, Fujita K, Tanaka K, and Nakajima T, et al., 2004. Adaptive response in embryogenesis: IV. Protective and detrimental bystander effects induced by X radiation in cultured limb bud cells of fetal mice. Radiat Res 161: 9-16.
91. Weintraub SJ, Prater CA, and Dean DC. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature. 358: 259-261.
92. Wells J, Yan PS, Cechvala M, Huang T, and Farnham PJ. 2003. Identification of novel pRb binding sites using CpG microarrays suggests that E2F recruits pRb to specific genomic sites during S phase. Oncogene. 22: 1445-1460.
93. Yamasaki L, 2003. Role of the RB tumor suppressor in cancer. Cancer Treat Res 115: 209-239.
94. Yang J, Xu ZP, Huang Y, and Hamrick HE. Duerksen-Hughes P.J., Yu Y.N., 2004. ATM and ATR: sensing DNA damage. World J Gastroenterol 10: 155-160.
95. Zamborszky J, Hong CI, and Csikasz NA. 2007. Computational analysis of mammalian cell division gated by a circadian clock: quantized cell cycle and cell size control. J Biol Rhythms 22(6): 542-553.
96. Zhang T, Brazhnik P, Tyson JJ. 2009. Computational Analysis of Dynamical Responses to the Intrinsic Pathway of Programmed Cell Death. Biophys J 97: 415-434.
97. Zhao Y and Ricci PF. 2010. Modeling dose-response at low dose: a systems biology approach for ionizing radiation. Dose Response 8(4): 456-477.