Model of the developing tumorigenic phenotype in mammalian cells and the roles of sustained stress and replicative senescence

Journal of Theoretical Biology

Volumn 227, Issue 2, 2004, Pages 253-264

  Karpinets, Tatiana V ^a   Foy, Brent D ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Cancer; Cellular senescence; Genomic instability; Stress response; Tumorigenesis

Indexed keywords

APOPTOSIS; CANCER;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL AGING; CELL CYCLE; CELL DEATH; CELL IMMORTALIZATION; CELL MUTANT; CELL PROLIFERATION; CELL SELECTION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; MAMMAL CELL; MOLECULAR BIOLOGY; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SENESCENCE; SIGNAL TRANSDUCTION; STRESS; TUMOR CELL;

ANIMALS; APOPTOSIS; CELL AGING; CELL DIVISION; CELLS; GENOMIC INSTABILITY; HUMANS; MODELS, BIOLOGICAL; MUTATION; NEOPLASMS; STRESS;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 1442335469     PISSN: 00225193     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jtbi.2003.11.005     Document Type: Article

References (84)

1. Abe R., Shimizu T., Ohkawara A., Nishihira J. Enhancement of macrophage migration inhibitory factor (MIF) expression in injured epidermis and cultured fibroblasts. Biochim. Biophys. Acta. 1500:2000;1-9.
2. Aikawa R., Komuro I., Yamazaki T., Zou Y., Kudoh S., Tanaka M., Shiojima I., Hiroi Y., Yazaki Y. Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J. Clin. Invest. 100:1997;1813-1821.
3. Alavi A., Hood J.D., Frausto R., Stupack D.G., Cheresh D.A. Role of Raf in vascular protection from distinct apoptotic stimuli. Science. 301:2003;94-96.
4. Alevizopoulos K., Vlach J., Hennecke S., Amati B. Cyclin E and c-Myc promote cell proliferation in the presence of p16INK4a and of hypophosphorylated retinoblastoma family proteins. EMBO J. 16:1997;5322-5333.
5. Ames B.N., Gold L.S. The causes and prevention of cancer. gaining perspective Environ. Health Perspect. 105:1997;865-873.
6. Andreassen P.R., Martineau S.N., Margolis R.L. Chemical induction of mitotic checkpoint override in mammalian cells results in aneuploidy following a transient tetraploid state. Mutat. Res. 372:1996;181-194.
7. Balashov S., Humayun M.Z. Mistranslation induced by streptomycin provokes a RecABC/RuvABC-dependent mutator phenotype in Escherichia coli cells. J. Mol. Biol. 315:2002;513-527.
8. Bazarov A.V., Adachi S., Li S.F., Mateyak M.K., Wei S., Sedivy J.M. A modest reduction in c-myc expression has minimal effects on cell growth and apoptosis but dramatically reduces susceptibility to Ras and Raf transformation. Cancer Res. 61:2001;1178-1186.
9. Bergmann A., Tugentman M., Shilo B.Z., Steller H. Regulation of cell number by MAPK-dependent control of apoptosis. a mechanism for trophic survival signaling Dev. Cell. 2:2002;159-170.
10. Bergoglio V., Bavoux C., Verbiest V., Hoffmann J.S., Cazaux C. Localisation of human DNA polymerase kappa to replication foci. J. Cell Sci. 115:2002;4413-4418.
11. Bianco P.R., Tracy R.B., Kowalczykowski S.C. DNA strand exchange proteins. a biochemical and physical comparison Front. Biosci. 3:1998;570-603.
12. Boman B.M., Melchert L., Fields J.Z. Hereditary cancer. Coleman W.B., Tsongalis G.J. The Molecular Basis of Human Cancer. 2002;81-111 Humana Press, Totowa, NJ.
13. Bonni A., Brunet A., West A.E., Datta S.R., Takasu M.A., Greenberg M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription- dependent and -independent mechanisms. Science. 286:1999;1358-1362.
14. Bridges B.A. Starvation-associated mutation in Escherichia coli. a spontaneous lesion hypothesis for "directed" mutation Mutat. Res. 307:1994;149-156.
15. Cairns J., Overbaugh J., Miller S. The origin of mutants. Nature. 335:1988;142-145.
16. Castagnetta L.A., Miceli M.D., Sorci C.M., Pfeffer U., Farruggio R., Oliveri G., Calabro M., Carruba G. Growth of LNCaP human prostate cancer cells is stimulated by estradiol via its own receptor. Endocrinology. 136:1995;2309-2319.
17. Chang S., Khoo C.M., Naylor M.L., Maser R.S., DePinho R.A. Telomere-based crisis. functional differences between telomerase activation and alt in tumor progression Genes Dev. 17:2003;88-100.
18. Concin N., Stimpfl M., Zeillinger C., Wolff U., Hefler L., Sedlak J., Leodolter S., Zeillinger R. Role of p53 in G2/M cell cycle arrest and apoptosis in response to gamma-irradiation in ovarian carcinoma cell lines. Int. J. Oncol. 22:2003;51-57.
19. Counter C.M., Avilion A.A., LeFeuvre C.E., Stewart N.G., Greider C.W., Harley C.B., Bacchetti S. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11:1992;1921-1929.
20. de Lange T. Telomere dynamics and genomic instability in human cancer. Blackburn E.H., Greider C.W. Telomeres. 1995;265-293 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Donnellan R., Chetty R. Cyclin E in human cancers. FASEB J. 13:1999;773-780.
22. Dunham M.J., Badrane H., Ferea T., Adams J., Brown P.O., Rosenzweig F., Botstein D. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA. 99:2002;16144-16149.
23. Dykhuizen D.E. Chemostats used for studying natural selection and adaptive evolution. Methods Enzymol. 224:1993;613-631.
24. Evan G.I., Vousden K.H. Proliferation, cell cycle and apoptosis in cancer. Nature. 411:2001;342-348.
25. Fijalkowska I.J., Dunn R.L., Schaaper R.M. Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity. J. Bacteriol. 179:1997;7435-7445.
26. Friedberg E.C., Fischhaber P.L., Kisker C. Error-prone DNA polymerases. novel structures and the benefits of infidelity Cell. 107:2001;9-12.
27. Goodman M.F. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem. 71:2002;17-50.
28. Grandori C., Cowley S.M., James L.P., Eisenman R.N. The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16:2000;653-699.
29. Hahn W.C., Counter C.M., Lundberg A.S., Beijersbergen R.L., Brooks M.W., Weinberg R.A. Creation of human tumour cells with defined genetic elements. Nature. 400:1999;464-468.
30. Hall B.G. Adaptive mutations in Escherichia coli as a model for the multiple mutational origins of tumors. Proc. Natl Acad. Sci. USA. 92:1995;5669-5673.
31. Hall P.A., Coates P.J., Ansari B., Hopwood D. Regulation of cell number in the mammalian gastrointestinal tract. the importance of apoptosis J. Cell Sci. 107:1994;3569-3577.
32. Hellin A.C., Bentires-Alj M., Verlaet M., Benoit V., Gielen J., Bours V., Merville M.P. Roles of nuclear factor-kappaB, p53, and p21/WAF1 in daunomycin-induced cell cycle arrest and apoptosis. J. Pharmacol. Exp. Ther. 295:2000;870-878.
33. Hendrickson H., Slechta E.S., Bergthorsson U., Andersson D.I., Roth J.R. Amplification-mutagenesis. evidence that "directed" adaptive mutation and general hypermutability result from growth with a selected gene amplification Proc. Natl Acad. Sci. USA. 99:2002;2164-2169.
34. Humayun M.Z. SOS and Mayday. multiple inducible mutagenic pathways in Escherichia coli Mol. Microbiol. 30:1998;905-910.
35. Jahr S., Hentze H., Englisch S., Hardt D., Fackelmayer F.O., Hesch R.D., Knippers R. DNA fragments in the blood plasma of cancer patients. quantitations and evidence for their origin from apoptotic and necrotic cells Cancer Res. 61:2001;1659-1665.
36. Kandel E.S., Skeen J., Majewski N., Di Cristofano A., Pandolfi P.P., Feliciano C.S., Gartel A., Hay N. Activation of Akt/protein kinase B overcomes a G(2)/m cell cycle checkpoint induced by DNA damage. Mol. Cell. Biol. 22:2002;7831-7841.
37. Kannouche P., Broughton B.C., Volker M., Hanaoka F., Mullenders L.H.F., Lehmann A.R. Domain structure, localization, and function of DNA polymerase η, defective in xeroderma pigmentosum variant cells. Genes Dev. 15:2001;158-172.
38. Khong H.T., Restifo N.P. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 3:2002;999-1005.
39. Khosravi-Far R., Campbell S., Rossman K.L., Der C.J. Increasing complexity of Ras signal transduction. involvement of Rho family proteins Adv. Cancer Res. 72:1998;57-107.
40. Kunkel T.A., Pavlov Y.I., Bebenek K. Functions of human DNA polymerases eta, kappa and iota suggested by their properties, including fidelity with undamaged DNA templates. DNA Repair (Amsterdam). 2:2003;135-149.
41. Lamar C.A., Dorgan J.F., Longcope C., Stanczyk F.Z., Falk R.T., Stephenson H.E. Jr. Serum sex hormones and breast cancer risk factors in postmenopausal women. Cancer Epidemiol. Biomarkers Prev. 12:2003;380-383.
42. Land H., Chen A.C., Morgestain J.P., Parada L.F., Weinberg R.A. Behavior of myc and ras oncogenes in transformation of rat embryo fibroblasts. Mol. Cell. Biol. 6:1986;1917-1925.
43. Laskin J.D., Heck D.E., Laskin D.L. The ribotoxic stress response as a potential mechanism for MAP kinase activation in xenobiotic toxicity. Toxicol. Sci. 69:2002;289-291.
44. Lawrence C.W., Maher V.M. Eukaryotic mutagenesis and translesion replication dependent on DNA polymerase zeta and Rev1 protein. Biochem. Soc. Trans. 29:2001;187-191.
45. LeCouter J., Moritz D.R., Li B., Phillips G.L., Liang X.H., Gerber H.P., Hillan K.J., Ferrara N. Angiogenesis-independent endothelial protection of liver. role of VEGFR-1 Science. 299:2003;890-893.
46. Limoli C.L., Giedzinski E., Morgan W.F., Cleaver J.E. Inaugural article. polymerase eta deficiency in the xeroderma pigmentosum variant uncovers an overlap between the S phase checkpoint and double-strand break repair Proc. Natl Acad. Sci. USA. 97:2000;7939-7946.
47. Linet M.S., Wacholder S., Zahm S.H. Interpreting epidemiologic research. lessons from studies of childhood cancer Pediatrics. 112:2003;218-232.
48. Lukas J., Herzinger T., Hansen K., Moroni M.C., Resnitzky D., Helin K., Reed S.I., Bartek J. Cyclin E-induced S phase without activation of the pRb/E2F pathway. Genes Dev. 11:1997;1479-1492.
49. Lundin C., Erixon K., Arnaudeau C., Schultz N., Jenssen D., Meuth M., Helleday T. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 22:2002;5869-5878.
50. Lutz, M., Knaus, P., 2002. Integration of TGF-beta pathway into the cellular signalling network. Cell Signal. 14, 977-988.
51. Matsuda T., Bebenek K., Masutani C., Hanaoka F., Kunkel T.A. Low fidelity DNA synthesis by human DNA polymerase-eta. Nature. 404:2000;1011-1013.
52. McCance, D.J., 1999. Oncogenic viruses. In: Nature Encyclopedia of Life Sciences. Nature Publishing Group, London, http://www.els.net/, doi:10.1038/npg.els.0000421.
53. McKenzie G.J., Rosenberg S.M. Adaptive mutations, mutator DNA polymerases and genetic change strategies of pathogens. Curr. Opin. Microbiol. 4:2001;586-594.
54. Meier P., Finch A., Evan G. Apoptosis in development. Nature. 407:2000;796-801.
55. Murphy L.O., Smith S., Chen R.H., Fingar D.C., Blenis J. Molecular interpretation of ERK signal duration by immediate early gene products. Nat. Cell Biol. 4:2002;556-564.
56. Nilsen T.I., Vatten L.J. Prospective study of colorectal cancer risk and physical activity, diabetes, blood glucose and BMI. exploring the hyperinsulinaemia hypothesis Br. J. Cancer. 84:2001;417-422.
57. Nossal G.J. The double helix and immunology. Nature. 421:2003;440-444.
58. O'Hagan R., Chang S., Maser R., Mohan R., Artandi S., Chin L., DePinho R. Telomere dysfunction provokes regional amplification and deletion in cancer genomes. Cancer Cell. 2:2002;149-155.
59. Ohri S., Sharma D., Dixit A. Modulation of c-myc and c-fos gene expression in regenerating rat liver by 2-mercaptopropionylglycine. Cell Biol. Int. 26:2002;187-192.
60. Opferman J.T., Korsmeyer S.J. Apoptosis in the development and maintenance of the immune system. Nat. Immunol. 4:2003;410-415.
61. Oulton R., Harrington L. Telomeres, telomerase, and cancer. life on the edge of genomic stability Curr. Opin. Oncol. 12:2000;74-81.
62. Pietenpol J.A., Stewart Z.A. Cell cycle checkpoint signaling. cell cycle arrest versus apoptosis Toxicology. 181-182:2002;475-481.
63. Radfar A., Unnikrishnan I., Lee H.W., DePinho R.A., Rosenberg N. P19(Arf) induces p53-dependent apoptosis during Abelson virus-mediated pre-B cell transformation. Proc. Natl Acad. Sci. USA. 95:1998;13194-13199.
64. Raff M.C. Cell suicide for beginners. Nature. 396:1998;119-122.
65. Ries S., Biederer C., Woods D., Shifman O., Shirasawa S., Sasazuki T., McMahon M., Oren M., McCormick F. Opposing effects of Ras on p53. transcriptional activation of mdm2 and induction of p19ARF Cell. 103:2000;321-330.
66. Rodin S.N., Rodin A.S. Human lung cancer and p53. the interplay between mutagenesis and selection Proc. Natl Acad. Sci. USA. 97:2000;12244-12249.
67. Ruf I.K., Rhyne P.W., Yang H., Borza C.M., Hutt-Fletcher L.M., Cleveland J.L., Sample J.T. Epstein-Barr virus regulates c-MYC, apoptosis, and tumorigenicity in Burkitt lymphoma. Mol. Cell. Biol. 19:1999;1651-1660.
68. Santana C., Ortega E., Garcia-Carranca A. Oncogenic H-ras induces cyclin B1 expression in a p53-independent manner. Mutat. Res. 508:2002;49-58.
69. Santoni-Rugiu E., Falck J., Mailand N., Bartek J., Lukas J. Involvement of Myc activity in a G(1)/S-promoting mechanism parallel to the pRb/E2F pathway. Mol. Cell. Biol. 20:2000;3497-3509.
70. Schwartz R.C., Stanton L.W., Riley S.C., Marcu K.B., Witte O.N. Synergism of v-myc and v-ras in the in vitro neoplastic progression of murine lymphoid cells. Mol. Cell. Biol. 6:1986;3221-3231.
71. Seitz E.M., Kowalczykowski S.C. The DNA binding and pairing preferences of the archaeal RadA protein demonstrate a universal characteristic of DNA strand exchange proteins. Mol. Microbiol. 37:2000;555-560.
72. Shay J.W., Wright W.E. Telomeres and telomerase. implications for cancer and aging Radiat. Res. 155:2001;188-193.
73. Sheen J.H., Woo J.K., Dickson R.B. C-Myc alters the DNA damage-induced G2/M arrest in human mammary epithelial cells. Br. J. Cancer. 89:2003;1479-1485.
74. Shields J.M., Pruitt K., McFall A., Shaub A., Der C.J. Understanding Ras. 'it ain't over 'til it's over' Trends Cell. Biol. 10:2000;147-154.
75. Sommer L., Rao M. Neural stem cells and regulation of cell number. Prog. Neurobiol. 66:2002;1-18.
76. Starr T.K., Jameson S.C., Hogquist K.A. Positive and negative selection of T cells. Annu. Rev. Immunol. 21:2003;139-176.
77. Trumpp A., Refaeli Y., Oskarsson T., Gasser S., Murphy M., Martin G.R., Bishop J.M. C-Myc regulates mammalian body size by controlling cell number but not cell size. Nature. 414:2001;768-773.
78. Unnikrishnan I., Radfar A., Jenab-Wolcott J., Rosenberg N. P53 mediates apoptotic crisis in primary Abelson virus-transformed pre-B cells. Mol. Cell. Biol. 19:1999;4825-4831.
79. Wang Z. DNA damage-induced mutagenesis. a novel target for cancer prevention Mol. Interv. 1:2001;269-281.
80. Watnick R.S., Cheng Y.N., Rangarajan A., Ince T.A., Weinberg R.A. Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell. 3:2003;219-231.
81. Woodgate R. A plethora of lesion-replicating DNA polymerases. Genes Dev. 13:1999;2191-2195.
82. Yamada N.A., Farber R.A. Induction of a low level of microsatellite instability by overexpression of DNA polymerase Beta. Cancer Res. 62:2002;6061-6064.
83. Zhang Y., Wu X., Guo D., Rechkoblit O., Geacintov N.E., Wang Z. Two-step error-prone bypass of the (+)- and (-)-trans-anti-BPDE-N(2)-dG adducts by human DNA polymerases eta and kappa. Mutat. Res. 510:2002;23-35.
84. Zimmerman K.C., Bonzon C., Green D.R. The machinery of programmed cell death. Pharmacol. Ther. 92:2002;57-70.