Cancer models, genomic instability and somatic cellular Darwinian evolution

Biology Direct

Volumn 5, Issue , 2010, Pages

  Little, Mark P ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; EVOLUTION; GENETICS; GENOMIC INSTABILITY; HUMAN; NEOPLASM; REVIEW;

ANIMALS; EVOLUTION; GENOMIC INSTABILITY; HUMANS; NEOPLASMS;

EID: 77950947945     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/1745-6150-5-19     Document Type: Review

References (166)

1. Armitage P, Doll R. The age distribution of cancer and a multi-stage theory of carcinogenesis. Br J Cancer 1954, 8:1-12. 2007940, 13172380.
2. Moolgavkar SH, Venzon DJ. Two-event models for carcinogenesis - incidence curves for childhood and adult tumors. Math Biosci 1979, 47:55-77.
3. Knudson AG. Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci USA 1971, 68:820-823. 10.1073/pnas.68.4.820, 389051, 5279523.
4. Little MP. Are two mutations sufficient to cause cancer? Some generalizations of the two-mutation model of carcinogenesis of Moolgavkar, Venzon, and Knudson, and of the multistage model of Armitage and Doll. Biometrics 1995, 51:1278-1291. 10.2307/2533259, 8589222.
5. Little MP, Wright EG. A stochastic carcinogenesis model incorporating genomic instability fitted to colon cancer data. Math Biosci 2003, 183:111-134. 10.1016/S0025-5564(03)00040-3, 12711407.
6. Little MP, Vineis P, Li G. A stochastic carcinogenesis model incorporating multiple types of genomic instability fitted to colon cancer data. J Theor Biol 2008, 254:229-238. 10.1016/j.jtbi.2008.05.027, 18640693.
7. Weinberg RA. The Biology of Cancer 2007, New York, NY: Garland Science.
8. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000, 100:57-70. 10.1016/S0092-8674(00)81683-9, 10647931.
9. Stanley WM. Virus-induced neoplasia - outlook for the future. Cancer Res 1960, 20:798-804.
10. Huebner RJ, Todaro GJ. Oncogenes of RNA tumor viruses as determinants of cancer. Proc Natl Acad Sci USA 1969, 64:1087-1094. 10.1073/pnas.64.3.1087, 223347, 5264139.
11. Kaplan HS. On the natural history of the murine leukemias: presidential address. Cancer Res 1967, 27:1325-1340.
12. Rowe WP. Genetic factors in the natural history of murine leukemia virus infection: G.H.A. Clowes Memorial Lecture. Cancer Res 1973, 33:3061-3068.
13. Duesberg PH. Retroviral transforming genes in normal cells?. Nature 1983, 304:219-226. 10.1038/304219a0, 6346107.
14. Duesberg PH. Activated proto-onc genes - sufficient or necessary for cancer?. Science 1985, 228:669-677. 10.1126/science.3992240, 3992240.
15. Stehelin D, Fujita DJ, Padgett T, Varmus HE, Bishop JM. Detection and enumeration of transformation-defective strains of avian sarcoma virus with molecular hybridization. Virology 1977, 76:675-684. 10.1016/0042-6822(77)90250-1, 190771.
16. Bishop JM. The molecular genetics of cancer. Science 1987, 235:305-311. 10.1126/science.3541204, 3541204.
17. Vogelstein B, Kinzler KW. The Genetic Basis of Human Cancer. 2002, New York, NY: McGraw-Hill Medical.
18. Boland CR, Goel A. Somatic evolution of cancer cells. Semin Cancer Biol 2005, 15:436-450. 10.1016/j.semcancer.2005.06.001, 16055343.
19. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990, 61:759-767. 10.1016/0092-8674(90)90186-I, 2188735.
20. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996, 87:159-170. 10.1016/S0092-8674(00)81333-1, 8861899.
21. Massagué J. G1 cell-cycle control and cancer. Nature 2004, 432:298-306. 10.1038/nature03094, 15549091.
22. Cordon-Cardo C. Mutations of cell cycle regulators. Biological and clinical implications for human neoplasia. Am J Pathol 1995, 147:545-560. 1870966, 7677168.
23. Kastan MB, Canman CE, Leonard CJ. P53, cell cycle control and apoptosis: Implications for cancer. Cancer Metastasis Rev 1995, 14:3-15. 10.1007/BF00690207, 7606818.
24. Hartwell LH, Weinert TA. Checkpoints: controls that ensure the order of cell-cycle events. Science 1989, 246:629-634. 10.1126/science.2683079, 2683079.
25. Hartwell LH, Kastan MB. Cell-cycle control and cancer. Science 1994, 266:1821-1828. 10.1126/science.7997877, 7997877.
26. Norbury CJ, Zhivotovsky B. DNA damage-induced apoptosis. Oncogene 2004, 23:2797-2808. 10.1038/sj.onc.1207532, 15077143.
27. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature 1998, 396:643-649. 10.1038/25292, 9872311.
28. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B. Mutations of mitotic checkpoint genes in human cancers. Nature 1998, 392:300-303. 10.1038/32688, 9521327.
29. International Commission on Radiological Protection Low-dose extrapolation of radiation-related cancer risk. Ann ICRP 2005, 35(4):1-140. International Commission on Radiological Protection.
30. Chiou SS, Huang JL, Tsai YS, Chen TF, Lee KW, Juo SH, Jong YJ, Hung CH, Chang TT, Lin CS. Elevated mRNA transcripts of non-homologous end-joining genes in pediatric acute lymphoblastic leukemia. Leukemia 2007, 21:2061-2064. 10.1038/sj.leu.2404742, 17495966.
31. Aplan PD. Causes of oncogenic chromosomal translocation. Trends in Genetics 2006, 22:46-55. 10.1016/j.tig.2005.10.002, 1762911, 16257470.
32. Maseki N, Miyoshi H, Shimizu K, Homma C, Ohki M, Sakurai M, Kaneko Y. The 8;21 chromosome-translocation in acute myeloid leukemia is always detectable by molecular analysis using AML1. Blood 1993, 81:1573-1579.
33. McKeithan TW, Warshawsky L, Espinosa R, LeBeau MM. Molecular cloning of the breakpoints of a complex Philadelphia chromosome translocation: identification of a repeated region on chromosome 17. Proc Natl Acad Sci USA 1992, 89:4923-4927. 10.1073/pnas.89.11.4923, 49200, 1594595.
34. Loman N, Johannsson O, Kristoffersson U, Olsson H, Borg A. Family history of breast and ovarian cancers and BRCA1 and BRCA2 mutations in a population-based series of early-onset breast cancer. J Natl Cancer Inst 2001, 93:1215-1223. 10.1093/jnci/93.16.1215, 11504767.
35. Ramus SJ, Harrington PA, Pye C, DiCioccio RA, Cox MJ, Garlinghouse-Jones K, Oakley-Girvan I, Jacobs IJ, Hardy RM, Whittemore AS, Ponder BA, Piver MS, Pharoah PD, Gayther SA. Contribution of BRCA1 and BRCA2 mutations to inherited ovarian cancer. Hum Mutat 2007, 28:1207-1215. 10.1002/humu.20599, 17688236.
36. Boynton RF, Blount PL, Yin J, Brown VL, Huang Y, Tong Y, McDaniel T, Newkirk C, Resau JH, Raskind WH, Haggitt RC, Reid BJ, Meltzer SJ. Loss of heterozygosity involving the APC and MCC genetic loci occurs in the majority of human esophageal cancers. Proc Natl Acad Sci USA 1992, 89:3385-3388. 10.1073/pnas.89.8.3385, 48872, 1565631.
37. Mendes-da Silva P, Moreira A, Duro-da Costa J, Matias D, Monteiro C. Frequent loss of heterozygosity on chromosome 5 in non-small cell lung carcinoma. Mol Pathol 2000, 53:184-187. 10.1136/mp.53.4.184, 1186967, 11040940.
38. Vogel F. Genetics of retinoblastoma. Hum Genet 1979, 52:1-54. 10.1007/BF00295569, 393614.
39. Lee WH, Bookstein R, Hong F, Young LJ, Shew JY, Lee EY. Human retinoblastoma susceptibility gene: cloning, identification, and sequence. Science 1987, 235:1394-1399. 10.1126/science.3823889, 3823889.
40. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965, 37:614-636. 10.1016/0014-4827(65)90211-9, 14315085.
41. Hodes RJ. Telomere length, aging, and somatic cell turnover. J Exp Med 1999, 190:153-156. 10.1084/jem.190.2.153, 2195566, 10432278.
42. Day JP, Marder BA, Morgan WF. Telomeres and their possible role in chromosome stabilization. Environ Mol Mutagen 1993, 22:245-249. 10.1002/em.2850220411, 8223505.
43. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, Bacchetti S. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 1992, 11:1921-1929. 556651, 1582420.
44. Hayflick L. Mortality and immortality at the cellular level. A review. Biochemistry-Moscow 1997, 62:1180-1190.
45. Bryan TM, Cech TR. Telomerase and the maintenance of chromosome ends. Curr Opin Cell Biol 1999, 11:318-324. 10.1016/S0955-0674(99)80043-X, 10395557.
46. Shay JW, Wright WE. Hallmarks of telomeres in ageing research. J Pathol 2007, 211:114-123. 10.1002/path.2090, 17200948.
47. Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J 1995, 14:4240-4248. 394507, 7556065.
48. Dunham MA, Neumann AA, Fasching CL, Reddel RR. Telomere maintenance by recombination in human cells. Nature Genetics 2000, 26:447-450. 10.1038/82586, 11101843.
49. Papetti M, Herman IM. Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol - Cell Physiol 2002, 282:C947-C970.
50. Hlatky L, Hahnfeldt P, Folkman J. Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J Natl Cancer Inst 2002, 94:883-893.
51. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003, 3:401-410. 10.1038/nrc1093, 12778130.
52. Nowell PC. The clonal evolution of tumor cell populations. Science 1976, 194:23-28. 10.1126/science.959840, 959840.
53. Gatenby RA. Commentary: Carcinogenesis as Darwinian evolution? Do the math!. Int J Epidemiol 2006, 35:1165-1167. 10.1093/ije/dyl192, 16990285.
54. Vineis P, Berwick M. The population dynamics of cancer: a Darwinian perspective. Int J Epidemiol 2006, 35:1151-1159. 10.1093/ije/dyl185, 16987840.
55. Gatenby RA, Smallbone K, Maini PK, Rose F, Averill J, Nagle RB, Worrall L, Gillies RJ. Cellular adaptations to hypoxia and acidosis during somatic evolution of breast cancer. Br J Cancer 2007, 97:646-653. 10.1038/sj.bjc.6603922, 2360372, 17687336.
56. Smallbone K, Maini PK, Gatenby RA. Episodic, transient systemic acidosis delays evolution of the malignant phenotype: possible mechanism for cancer prevention by increased physical activity. Biology Direct 2010, 5:22. 10.1186/1745-6150-5-22, 20406440.
57. Harris H. A long view of fashions in cancer research. Bioessays 2005, 27:833-838. 10.1002/bies.20263, 16015588.
58. United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) Sources and Effects of Ionizing Radiation. UNSCEAR 1993 Report to the General Assembly, with Scientific Annexes. E.94.IX.2 1993, 1-922. New York: United Nations, United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR).
59. Sonnenschein C, Soto AM. The Society of Cells: Cancer and Control of Cell Proliferation. 1999, Oxford: Bios Scientific Publishers.
60. Barcellos-Hoff MH, Ravani SA. Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells. Cancer Res 2000, 60:1254-1260.
61. Barcellos-Hoff MH, Brooks AL. Extracellular signaling through the microenvironment: A hypothesis relating carcinogenesis, bystander effects, and genomic instability. Radiat Res 2001, 156:618-627. 10.1667/0033-7587(2001)156[0618:ESTTMA]2.0.CO;2, 11604083.
62. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer 2001, 1:46-54. 10.1038/35094059, 11900251.
63. Harris H. Is collagen XV a tumor suppressor?. DNA Cell Biol 2003, 22:225-226. 10.1089/104454903321908601, 12823898.
64. Kenny PA, Bissell MJ. Tumor reversion: correction of malignant behavior by microenvironmental cues. Int J Cancer 2003, 107:688-695. 10.1002/ijc.11491, 14566816.
65. Bissell MJ, LaBarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment?. Cancer Cell 2005, 7:17-23.
66. Rønnov-Jessen L, Bissell MJ. Breast cancer by proxy: can the microenvironment be both the cause and consequence?. Trends Mol Med 2009, 15:5-13. 10.1016/j.molmed.2008.11.001, 2746030, 19091631.
67. Harris H. Response to letters from Sonnenschein and Capp. Bioessays 2006, 28:103.
68. Morgan WF. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res 2003, 159:567-580. 10.1667/0033-7587(2003)159[0567:NADEOE]2.0.CO;2, 12710868.
69. Morgan WF. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiat Res 2003, 159:581-596. 10.1667/0033-7587(2003)159[0581:NADEOE]2.0.CO;2, 12710869.
70. Kinzler KW, Vogelstein B. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 1997, 386:761-763. 10.1038/386761a0, 9126728.
71. Loeb LA. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res 1991, 51:3075-3079.
72. Loeb LA. A mutator phenotype in cancer. Cancer Res 2001, 61:3230-3239.
73. Stoler DL, Chen N, Basik M, Kahlenberg MS, Rodriguez-Bigas MA, Petrelli NJ, Anderson GR. The onset and extent of genomic instability in sporadic colorectal tumor progression. Proc Natl Acad Sci USA 1999, 96:15121-15126. 10.1073/pnas.96.26.15121, 24783, 10611348.
74. Knuutila S, Aalto Y, Autio K, Bjorkqvist AM, El-Rifai W, Hemmer S, Huhta T, Kettunen E, Kiuru-Kuhlefelt S, Larramendy ML, Lushnikova T, Monni O, Pere H, Tapper J, Tarkkanen M, Varis A, Wasenius VM, Wolf M, Zhu Y. DNA copy number losses in human neoplasms. Am J Pathol 1999, 155:683-694. 1866903, 10487825.
75. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997, 386:623-627. 10.1038/386623a0, 9121588.
76. Ribic CM, Sargent DJ, Moore MJ, Thibodeau SN, French AJ, Goldberg RM, Hamilton SR, Laurent-Puig P, Gryfe R, Shepherd LE, Tu D, Redston M, Gallinger S. Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer. N Engl J Med 2003, 349:247-257. 10.1056/NEJMoa022289, 12867608.
77. Arzimanoglou II, Gilbert F, Barber HRK. Microsatellite instability in human solid tumors. Cancer 1998, 82:1808-1820. 10.1002/(SICI)1097-0142(19980515)82:10<1808::AID-CNCR2>3.0.CO;2-J, 9587112.
78. Fishel R, Lescoe MK, Rao MRS, Copeland NG, Jenkins NA, Garber J, Kane M, Kolodner R. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 1993, 75:1027-1038. 10.1016/0092-8674(93)90546-3, 8252616.
79. Leach FS, Nicolaides NC, Papadopoulos N, Liu B, Jen J, Parsons R, Peltomäki P, Sistonen P, Aaltonen LA, Nyström-Lahti M, et al. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 1993, 75:1215-1225. 10.1016/0092-8674(93)90330-S, 8261515.
80. Bronner CE, Baker SM, Morrison PT, Warren G, Smith LG, Lescoe MK, Kane M, Earabino C, Lipford J, Lindblom A, et al. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature 1994, 368:258-261. 10.1038/368258a0, 8145827.
81. Papadopoulos N, Nicolaides NC, Wei Y-F, Ruben SM, Carter KC, Rosen CA, Haseltine WA, Fleischmann RD, Fraser CM, Adams MD, et al. Mutation of a mutL homolog in hereditary colon cancer. Science 1994, 263:1625-1629. 10.1126/science.8128251, 8128251.
82. Breivik J. Don't stop for repairs in a war zone: Darwinian evolution unites genes and environment in cancer development. Proc Natl Acad Sci USA 2001, 98:5379-5381. 10.1073/pnas.101137698, 33219, 11344279.
83. Breivik J. The evolutionary origin of genetic instability in cancer development. Semin Cancer Biol 2005, 15:51-60. 10.1016/j.semcancer.2004.09.008, 15613288.
84. Bardelli A, Cahill DP, Lederer G, Speicher MR, Kinzler KW, Vogelstein B, Lengauer C. Carcinogen-specific induction of genetic instability. Proc Natl Acad Sci USA 2001, 98:5770-5775. 10.1073/pnas.081082898, 33288, 11296254.
85. Chow M, Rubin H. Clonal selection versus genetic instability as the driving force in neoplastic transformation. Cancer Res 2000, 60:6510-6518.
86. Tomlinson IPM, Novelli MR, Bodmer WF. The mutation rate and cancer. Proc Natl Acad Sci USA 1996, 93:14800-14803. 10.1073/pnas.93.25.14800, 26216, 8962135.
87. Tomlinson I, Bodmer W. Selection, the mutation rate and cancer: ensuring that the tail does not wag the dog. Nat Med 1999, 5:11-12. 10.1038/4687, 9883827.
88. Rubin H. Cell-cell contact interactions conditionally determine suppression and selection of the neoplastic phenotype. Proc Natl Acad Sci USA 2008, 105:6215-6221. 10.1073/pnas.0800747105, 2359782, 18434545.
89. Little MP, Li G. Stochastic modelling of colon cancer: is there a role for genomic instability?. Carcinogenesis 2007, 28:479-487. 10.1093/carcin/bgl173, 16973671.
90. Nowak MA, Komarova NL, Sengupta A, Jallepalli PV, Shih I-M, Vogelstein B, Lengauer C. The role of chromosomal instability in tumor initiation. Proc Natl Acad Sci USA 2002, 99:16226-16231. 10.1073/pnas.202617399, 138593, 12446840.
91. Luebeck EG, Moolgavkar SH. Multistage carcinogenesis and the incidence of colorectal cancer. Proc Natl Acad Sci USA 2002, 99:15095-15100. 10.1073/pnas.222118199, 137549, 12415112.
92. Potten CS, Loeffler M. A comprehensive model of the crypts of the small intestine of the mouse provides insight into the mechanisms of cell migration and the proliferation hierarchy. J Theor Biol 1987, 127:381-391. 10.1016/S0022-5193(87)80136-4, 3328018.
93. Nowak MA, Michor F, Iwasa Y. The linear process of somatic evolution. Proc Natl Acad Sci USA 2003, 100:14966-14969. 10.1073/pnas.2535419100, 299861, 14657359.
94. Bach SP, Renehan AG, Potten CS. Stem cells: the intestinal stem cell as a paradigm. Carcinogenesis 2000, 21:469-476. 10.1093/carcin/21.3.469, 10688867.
95. Michor F, Iwasa Y, Rajagopalan H, Lengauer C, Nowak MA. Linear model of colon cancer initiation. Cell Cycle 2004, 3:358-362.
96. Guasch G, Schober M, Pasolli HA, Conn EB, Polak L, Fuchs E. Loss of TGFβ signaling destabilize homeostasis and promotes squalemous cell carcinomas in stratified epithelia. Cancer Cell 2007, 12:313-327. 10.1016/j.ccr.2007.08.020, 2424201, 17936557.
97. Omerovic J, Hammond DE, Clague MJ, Prior IA. Ras isoform abundance and signalling in human cancer cell lines. Oncogene 2008, 27:2754-2762. 10.1038/sj.onc.1210925, 2557550, 17998936.
98. Kuang C, Xiao Y, Liu X, Stringfield TM, Zhang S, Wang Z, Chen Y. In vivo disruption of TGF-β signaling by Smad7 leads to premalignant ductal lesions in the pancreas. Proc Natl Acad Sci USA 2006, 103:1858-1863. 10.1073/pnas.0508977103, 1413640, 16443684.
99. Little MP. Cancer models, ionizing radiation, and genomic instability: a review. Handbook of Cancer Models with Applications 2008, 109-148. New Jersey: World Scientific Publishing Company, Tan W-Y, Hanin L.
100. Nordling CO. A new theory on cancer-inducing mechanism. Br J Cancer 1953, 7:68-72. 2007872, 13051507.
101. Doll R. Age distribution of cancer: implications for models of carcinogenesis. J Roy Statist Soc Series A 1971, 134:133-166.
102. Moolgavkar SH. The multistage theory of carcinogenesis and the age distribution of cancer in man. J Natl Cancer Inst 1978, 61:49-52.
103. Moolgavkar SH, Luebeck EG. Multistage carcinogenesis: population-based model for colon cancer. J Natl Cancer Inst 1992, 84:610-618. 10.1093/jnci/84.8.610, 1313509.
104. Peto R. Epidemiology, multistage models, and short-term mutagenicity tests. Origins of Human Cancer 1977, 1403-1428. Cold Spring Harbor: Cold Spring Harbor Laborator, Hiatt HH, Winsten JA.
105. Armitage P, Doll R. A two-stage theory of carcinogenesis in relation to the age distribution of human cancer. Br J Cancer 1957, 11:161-169. 2073730, 13460138.
106. Tucker HG. A stochastic model for a two-stage theory of carcinogenesis. Fifth Berkeley Symposium on Mathematical Statistics and Probability 1967, 387-403. Berkeley, CA: University of California Press.
107. Moolgavkar SH, Knudson AG. Mutation and cancer: a model for human carcinogenesis. J Natl Cancer Inst 1981, 66:1037-1052.
108. Tan W-Y. Stochastic Models of Carcinogenesis. 1991, New York, NY: Marcel Dekker.
109. Moolgavkar SH, Dewanji A, Venzon DJ. A stochastic two-stage model for cancer risk assessment. I. The hazard function and the probability of tumor. Risk Anal 1988, 8:383-392. 10.1111/j.1539-6924.1988.tb00502.x, 3201016.
110. Little MP, Charles MW. Time variations in radiation-induced relative risk and implications for population cancer risks. J Radiol Prot 1991, 11:91-110.
111. Moolgavkar SH, Cross FT, Luebeck G, Dagle GE. A two-mutation model for radon-induced lung tumors in rats. Radiat Res 1990, 121:28-37. 10.2307/3577560, 2153988.
112. Heidenreich WF, Jacob P, Paretzke HG, Cross FT, Dagle GE. Two-step model for the risk of fatal and incidental lung tumors in rats exposed to radon. Radiat Res 1999, 151:209-217. 10.2307/3579772, 9952306.
113. Heidenreich WF, Brugmans MJ, Little MP, Leenhouts HP, Paretzke HG, Morin M, Lafuma J. Analysis of lung tumour risk in radon-exposed rats: an intercomparison of multi-step modelling. Radiat Environ Biophys 2000, 39:253-264. 10.1007/s004110000075, 11200969.
114. Moolgavkar SH, Luebeck EG, Krewski D, Zielinski JM. Radon, cigarette smoke, and lung cancer: a re-analysis of the Colorado Plateau uranium miners' data. Epidemiology 1993, 4:204-217. 10.1097/00001648-199305000-00004, 8512985.
115. Luebeck EG, Heidenreich WF, Hazelton WD, Paretzke HG, Moolgavkar SH. Biologically based analysis of the data for the Colorado uranium miners cohort: age, dose and dose-rate effects. Radiat Res 1999, 152:339-351. 10.2307/3580219, 10477911.
116. Hazelton WD, Luebeck EG, Heidenreich WF, Moolgavkar SH. Analysis of a historical cohort of Chinese tin miners with arsenic, radon, cigarette smoke, and pipe smoke exposures using the biologically based two-stage clonal expansion model. Radiat Res 2001, 156:78-94. 10.1667/0033-7587(2001)156[0078:AOAHCO]2.0.CO;2, 11418076.
117. Little MP, Haylock RGE, Muirhead CR. Modelling lung tumour risk in radon-exposed uranium miners using generalizations of the two-mutation model of Moolgavkar, Venzon and Knudson. Int J Radiat Biol 2002, 78:49-68. 10.1080/09553000110085797, 11747553.
118. Heidenreich WF, Luebeck EG, Moolgavkar SH. Effects of exposure uncertainties in the TSCE model and application to the Colorado miners data. Radiat Res 2004, 161:72-81. 10.1667/RR3089, 14680394.
119. Kai M, Luebeck EG, Moolgavkar SH. Analysis of the incidence of solid cancer among atomic bomb survivors using a two-stage model of carcinogenesis. Radiat Res 1997, 148:348-358. 10.2307/3579520, 9339951.
120. Heidenreich WF, Nyberg U, Hall P. A biologically based model for liver cancer risk in the Swedish Thorotrast patients. Radiat Res 2003, 159:656-662. 10.1667/0033-7587(2003)159[0656:ABBMFL]2.0.CO;2, 12710877.
121. Den Otter W, Koten JW, Vegt BJH, Beemer FA, Boxma OJ, Derkinderen DJ, de Graaf PW, Huber J, Lips CJM, Roholl PJM, et al. Oncogenesis by mutations in anti-oncogenes: a view. Anticancer Res 1990, 10:475-487.
122. Derkinderen DJ, Boxma OJ, Koten JW, Den Otter W. Stochastic theory of oncogenesis. Anticancer Res 1990, 10:497-504.
123. Little MP. Generalisations of the two-mutation and classical multi-stage models of carcinogenesis fitted to the Japanese atomic bomb survivor data. J Radiol Prot 1996, 16:7-24.
124. Tan WY. A stochastic Gompertz birth-death process. Statistics & Probability Letters 1986, 4:25-28.
125. Bartoszyński R, Edler L, Hanin L, Kopp-Schneider A, Pavlova L, Tsodikov A, Zorin A, Yakovlev AY. Modeling cancer detection: tumor size as a source of information on unobservable stages of carcinogenesis. Math Biosci 2001, 171:113-142. 10.1016/S0025-5564(01)00058-X, 11395047.
126. Little MP. Are two mutations sufficient to cause cancer? Modelling radiation-induced cancer in the Japanese atomic bomb survivors using generalizations of the two-mutation model of Moolgavkar, Venzon and Knudson and of the multistage model of Armitage and Doll. Health Effects of Low Dose Radiation. Challenges of the 21st Century. Proceedings of the Conference Organized by the British Nuclear Energy Society and held in Stratford-upon-Avon, UK, on 11-14 May 1997 1997, 169-174. London: British Nuclear Energy Society.
127. Little MP, Muirhead CR, Stiller CA. Modelling lymphocytic leukaemia incidence in England and Wales using generalizations of the two-mutation model of carcinogenesis of Moolgavkar, Venzon and Knudson. Stat Med 1996, 15:1003-1022. 10.1002/(SICI)1097-0258(19960530)15:10<1003::AID-SIM214>3.0.CO;2-3, 8783438.
128. Little MP, Muirhead CR, Boice JD, Kleinerman RA. Using multistage models to describe radiation-induced leukaemia. J Radiol Prot 1995, 15:315-334.
129. Tan WY, Chen CW, Zhang LJ. Cancer biology, cancer models and some new approaches to carcinogenesis. Handbook of Cancer Models with Applications 2008, 45-89. New Jersey: World Scientific Publishing Company, Tan W-Y, Hanin L.
130. Mao JH, Lindsay KA, Balmain A, Wheldon TE. Stochastic modelling of tumorigenesis in p53 deficient mice. Br J Cancer 1998, 77:243-252. 2151221, 9460995.
131. Ohtaki M, Niwa O. A mathematical model of radiation carcinogenesis with induction of genomic instability and cell death. Radiat Res 2001, 156:672-677. 10.1667/0033-7587(2001)156[0672:AMMORC]2.0.CO;2, 11604091.
132. Tan WY, Tan XW. A new stochastic and state space model of human colon cancer incorporating multiple pathways. Biology Direct 2010, 5:26. 10.1186/1745-6150-5-26, 20406446.
133. Hanin LG, Yakovlev AY. A nonidentifiability aspect of the two-stage model of carcinogenesis. Risk Anal 1996, 16:711-715. 10.1111/j.1539-6924.1996.tb00819.x, 8962520.
134. Heidenreich WF. On the parameters of the clonal expansion model. Radiat Environ Biophys 1996, 35:127-129. 10.1007/BF02434036, 8792461.
135. Hanin LG. Identification problem for stochastic models with application to carcinogenesis, cancer detection and radiation biology. Discrete Dynamics in Nature and Society 2002, 7:177-189.
136. Heidenreich WF, Luebeck EG, Moolgavkar SH. Some properties of the hazard function of the two-mutation clonal expansion model. Risk Anal 1997, 17:391-399. 10.1111/j.1539-6924.1997.tb00878.x, 9232020.
137. Rothenberg TJ. Identification in parametric models. Econometrica 1971, 39:577-591.
138. Jacquez JA, Perry T. Parameter estimation: local identifiability of parameters. Am J Physiol 1990, 258:E727-E736.
139. Catchpole EA, Morgan BJT. Detecting parameter redundancy. Biometrika 1997, 84:187-196.
140. Little MP, Heidenreich WF, Li G. Parameter identifiability and redundancy: theoretical considerations. PLoS ONE 2010, 5(1):e8915.
141. Little MP, Heidenreich WF, Li G. Parameter identifiability and redundancy in a general class of stochastic carcinogenesis models. PLoS ONE 2009, 4(12):e8520. 10.1371/journal.pone.0008520, 2797326, 20046831.
142. Basanta D, Simon M, Hatzikirou H, Deutsch A. Evolutionary game theory elucidates the role of glycolysis in glioma progression and invasion. Cell Prolif 2008, 41:980-987. 10.1111/j.1365-2184.2008.00563.x, 19040573.
143. Komarova NL, Sadovsky AV, Wan FY. Selective pressures for and against genetic instability in cancer: a time-dependent problem. J R Soc Interface 2008, 5:105-121. 10.1098/rsif.2007.1054, 2605501, 17580291.
144. d'Onofrio A, Gandolfi A. A family of models of angiogenesis and anti-angiogenesis anti-cancer therapy. Math Med Biol 2009, 26:63-95. 10.1093/imammb/dqn024, 19033598.
145. Ledzewicz U, Schattler H. Optimal and suboptimal protocols for a class of mathematical models of tumor anti-angiogenesis. J Theor Biol 2008, 252:295-312. 10.1016/j.jtbi.2008.02.014, 18371982.
146. Enderling H, Hlatky L, Hahnfeldt P. Migration rules: tumours are conglomerates of self-metastases. Br J Cancer 2009, 100:1917-1925. 10.1038/sj.bjc.6605071, 19455139.
147. Wcisło R, Dzwinel W, Yuen DA, Dudek AZ. A 3-D model of tumor progression based on complex automata driven by particle dynamics. J Mol Model 2009, 15:1517-1539. 10.1007/s00894-009-0511-4, 19466466.
148. Macklin P, McDougall S, Anderson ARA, Chaplain MAJ, Cristini V, Lowengrub J. Multiscale modelling and nonlinear simulation of vascular tumour growth. J Math Biol 2009, 58:765-798. 10.1007/s00285-008-0216-9, 18781303.
149. Anderson ARA. A hybrid multiscale model of solid tumour growth and invasion: evolution and the microenvironment. Single-Cell-Cased Models in Biology and Medicine 2007, 3-28. Basel: Birkhäuser, Anderson ARA, Chaplain MAJ, Rejniak KA.
150. Adam JA, Bellomo N. A survey of models for tumor-immune system dynamics. 1997, Boston: Birkhäuser.
151. Terasima T, Tolmach LJ. X-ray sensitivity and DNA synthesis in synchronous populations of HeLa cells. Science 1963, 140:490-492. 10.1126/science.140.3566.490, 13980636.
152. Sinclair WK. Cyclic x-ray responses in mammalian cells in vitro. Radiat Res 1968, 33:620-643. 10.2307/3572419, 4867897.
153. Wilson GD. Cell kinetics. Clin Oncol (R Coll Radiol) 2007, 19:370-384.
154. Alarcón T, Byrne HM, Maini PK. A mathematical model of the effects of hypoxia on the cell-cycle of normal and cancer cells. J Theor Biol 2004, 229:395-411. 10.1016/j.jtbi.2004.04.016, 15234206.
155. Hazelton WD. Modeling the effects of radiation on cell cycle regulation and carcinogenesis. Handbook of Cancer Models with Applications 2008, 91-108. New Jersey: World Scientific Publishing Company, Tan W-Y, Hanin L.
156. Ribba B, Colin T, Schnell S. A multiscale mathematical model of cancer, and its use in analyzing irradiation therapies. Theor Biol Med Model 2006, 3:7. 10.1186/1742-4682-3-7, 1388194, 16472396.
157. Fodde R, Kuipers J, Rosenberg C, Smits R, Kielman M, Gaspar C, van Es JH, Breukel C, Wiegant J, Giles RH, Clevers H. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nature Cell Biol 2001, 3:433-438. 10.1038/35070129, 11283620.
158. Paoloni-Giacobino A, Rey-Berthod C, Couturier A, Antonarakis SE, Hutter P. Differential rates of frameshift alterations in four repeat sequences of hereditary nonpolyposis colorectal cancer tumors. Hum Genetics 2002, 111:284-289.
159. Kim I-J, Kang HC, Park J-H, Shin Y, Ku J-L, Lim S-B, Park SY, Jung S-Y, Kim HK, Park JG. Development and applications of a β-catenin oligonucleotide microarray: β-catenin mutations are dominantly found in the proximal colon cancers with microsatellite instability. Clin Cancer Res 2003, 9:2920-2925.
160. Samowitz WS, Holden JA, Curtin K, Edwards SL, Walker AR, Lin HA, Robertson MA, Nichols MF, Gruenthal KM, Lynch BJ, Leppert MF, Slattery ML. Inverse relationship between microsatellite instability and K-ras and p53 gene alterations in colon cancer. Am J Pathol 2001, 158:1517-1524. 1891913, 11290569.
161. Hornsby C, Page KM, Tomlinson IPM. What can we learn from the population incidence of cancer? Armitage and Doll revisited. Lancet Oncol 2007, 8:1030-1038. 10.1016/S1470-2045(07)70343-1, 17976613.
162. Frank SA. Age-specific incidence of inherited versus sporadic cancers: A test of the multistage theory of carcinogenesis. Proc Natl Acad Sci USA 2005, 102:1071-1075. 10.1073/pnas.0407299102, 545832, 15657129.
163. Voskuil DW, Vasen HFA, Kampman E, van't Veer P. Colorectal cancer risk in HNPCC families: development during lifetime and in successive generations. National Collaborative Group on HNPCC. Int J Cancer 1997, 72:205-209. 10.1002/(SICI)1097-0215(19970717)72:2<205::AID-IJC1>3.0.CO;2-V, 9219821.
164. Surveillance Epidemiology and End Results (SEER) Program http://www.seer.cancer.gov Registry Data, 1973-1999. Surveillance, Epidemiology, and End Results (SEER) Program, National Cancer Institute, Division of Cancer Control and Population Sciences, Surveillance Research Program, Cancer Statistics Branch. 2000, Surveillance Epidemiology and End Results (SEER) Program.
165. McCullagh P, Nelder JA. Generalized Linear Models. 1989, Boca Raton, FA: Chapman and Hall/CRC, 2.
166. Potten CS, Booth C, Hargreaves D. The small intestine as a model for evaluating adult tissue stem cell drug targets. Cell Prolif 2003, 36:115-129. 10.1046/j.1365-2184.2003.00264.x, 12814429.