Activated oncogenes promote and cooperate with chromosomal instability for neoplastic transformation

Genes and Development

Volumn 18, Issue 11, 2004, Pages 1317-1330

  Woo, Richard A ^a   Poon, Randy Y C ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Chromosomal instability; Oncogenic Ras; p53; Transformation

Indexed keywords

BETA GALACTOSIDASE; COMPLEMENTARY DNA; PROTEIN P53; RAS PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CHROMOSOME; CHROMOSOME REARRANGEMENT; EMBRYO; ENZYME ACTIVITY; ENZYME ASSAY; GENE TRANSFER; KARYOTYPE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE H RAS; PRIORITY JOURNAL; RETROVIRUS; TUMOR SUPPRESSOR GENE;

ACETYLCYSTEINE; ADENOVIRUS E1A PROTEINS; ANIMALS; APOPTOSIS; CELL AGING; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CHROMOSOMAL INSTABILITY; CULTURE MEDIA, SERUM-FREE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; EMBRYO; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, RAS; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; REACTIVE OXYGEN SPECIES; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; MUS MUSCULUS; UNIDENTIFIED RETROVIRUS;

EID: 2642527955     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1165204     Document Type: Article

References (65)

1. INK4a in replicative senescence of normal human fibroblasts. Proc. Natl. Acad. Sci. 93: 13742-13747.
2. Artandi, S.E., Chang, S., Lee, S.L., Alson, S., Gottlieb, G.J., Chin, L., and DePinho, R.A. 2000. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406: 641-645.
3. Aruoma, O.I., Halliwell, B., Hoey, B.M., and Butler, J. 1989. The antioxidant action of N-acetylcysteine: Its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic. Biol. Med. 6: 593-597.
4. Barnes, D. and Sato, G. 1980. Methods for growth of cultured cells in serum-free medium. Anal. Biochem. 102: 255-270.
5. Blasco, M.A., Lee, H.W., Hande, M.P., Samper, E., Lansdorp, P.M., DePinho, R.A., and Greider, C.W. 1997. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25-34.
6. Bodnar, A.G., Ouellette, M., Frolkis, M., Holt, S.E., Chiu, C.P., Morin, G.B., Harley, C.B., Shay, J.W., Lichtsteiner, S., and Wright, W.E. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349-352.
7. Bos, J.L. 1989. ras oncogenes in human cancer: A review. Cancer Res. 49: 4682-4689.
8. Burgunder, J.M., Varriale, A., and Lauterburg, B.H. 1989. Effect of N-acetylcysteine on plasma cysteine and glutathione following paracetamol administration. Eur. J. Clin. Pharmacol. 36: 127-131.
9. Cone, R.D., Grodzicker, T., and Jaramillo, M. 1988. A retrovirus expressing the 12S adenoviral E1A gene product can immortalize epithelial cells from a broad range of rat tissues. Mol. Cell. Biol. 8: 1036-1044.
10. Debbas, M. and White, E. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes & Dev. 7: 546-554.
11. Denko, N.C., Giaccia, A.J., Stringer, J.R., and Stambrook, P.J. 1994. The human Ha-ras oncogene induces genomic instability in murine fibroblasts within one cell cycle. Proc. Natl. Acad. Sci. 91: 5124-5128.
12. Dimri, G.P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E.E., Linskens, M., Rubelj, I., Pereira-Smith, O., et al. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. 92: 9363-9367.
13. Donehower, L.A., Harvey, M., Slagle, B.L., McArthur, M.J., Montgomery Jr., C.A., Butel, J.S., and Bradley, A. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
14. Elenbaas, B., Spirio, L., Koerner, F., Fleming, M.D., Zimonjic, D.B., Donaher, J.L., Popescu, N.C., Hahn, W.C., and Weinberg, R.A. 2001. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes & Dev. 15: 50-65.
15. Felsher, D.W., Zetterberg, A., Zhu, J., Tlsty, T., and Bishop, J.M. 2000. Overexpression of MYC causes p53-dependent G2 arrest of normal fibroblasts. Proc. Natl. Acad. Sci. 97: 10544-10548.
16. Hahn, W.C. and Weinberg, R.A. 2002. Rules for making human tumor cells. N. Engl. J. Med. 347: 1593-1603.
17. Hahn, W.C., Counter, C.M., Lundberg, A.S., Beijersbergen, R.L., Brooks, M.W., and Weinberg, R.A. 1999. Creation of human tumour cells with defined genetic elements. Nature 400: 464-468.
18. Hayflick, L. 1965. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37: 614-636.
19. Hendzel, M.J., Nishioka, W.K., Raymond, Y., Allis, C.D., Bazett-Jones, D.P., and Th'ng, J.P. 1998. Chromatin condensation is not associated with apoptosis. J. Biol. Chem. 273: 24470-24478.
20. Hermeking, H. and Eick, D. 1994. Mediation of c-Myc-induced apoptosis by p53. Science 265: 2091-2093.
21. Hollstein, M., Shomer, B., Greenblatt, M., Soussi, T., Hovig, E., Montesano, R., and Harris, C.D. 1996. Somatic point mutations in the p53 gene of human tumors and cell lines: Updated compilation. Nucleic Acids Res. 24: 141-146.
22. Irani, K., Xia, Y., Zweier, J.L., Sollott, S.J., Der, C.J., Fearon, E.R., Sundaresan, M., Finkel, T., and Goldschmidt-Clermont, P.J. 1997. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652.
23. Jiang, X.R., Jimenez, G., Chang, E., Frolkis, M., Kusler, B., Sage, M., Beeche, M., Bodnar, A.G., Wahl, G.M., Tlsty, T.D., et al. 1999. Telomerase expression in human somatic cells does not induce changes associated with a transformed phenotype. Nat. Genet. 21: 111-114.
24. Johnson, L., Mercer, K., Greenbaum, D., Bronson, R.T., Crowley, D., Tuveson, D.A., and Jacks, T. 2001. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410: 1111-1116.
25. Karanjawala, Z.E., Murphy, N., Hinton, D.R., Hsieh, C.L., and Lieber, M.R. 2002. Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Curr. Biol. 12: 397-402.
26. Karlsson, A., Deb-Basu, D., Cherry, A., Turner, S., Ford, J., and Felsher, D.W. 2003. Defective double-strand DNA break repair and chromosomal translocations by MYC overexpression. Proc. Natl. Acad. Sci. 100: 9974-9979.
27. Land, H., Parada, L.F., and Weinberg, R.A. 1983. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304: 596-602.
28. Lee, A.C., Fenster, B.E., Ito, H., Takeda, K., Bae, N.S., Hirai, T., Yu, Z.X., Ferrans, V.J., Howard, B.H., and Finkel, T. 1999. Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J. Biol. Chem. 274: 7936-7940.
29. Li, T.K., Chen. A.Y., Yu, C., Mao, Y., Wang, H., and Liu, L.F. 1999. Activation of topoisomerase II-mediated excision of chromosomal DNA loops during oxidative stress. Genes & Dev. 13: 1553-1560.
30. Li, R., Sonik, A., Stindl, R., Rasnick, D., and Duesberg, P. 2000. Aneuploidy vs. gene mutation hypothesis of cancer: Recent study claims mutation but is found to support aneuploidy. Proc. Natl. Acad. Sci. 97: 3236-3241.
31. Lin, A.W., Barradas, M., Stone, J.C., van Aelst, L., Serrano, M., and Lowe, S.W. 1998. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes & Dev. 12: 3008-3019.
32. Loo, D.T., Fuquay, J.I., Rawson, C.L., and Bames, D.W. 1987. Extended culture of mouse embryo cells without senescence: Inhibition by serum. Science 236: 200-202.
33. Lowe, S.W. and Ruley, H.E. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes & Dev. 7: 535-545.
34. Lowe, S.W., Ruley, H.E., Jacks, T., and Housman, D.E. 1993. p53-dependent apoptosis modulates the cytotoxicity of anti-cancer agents. Cell 74: 957-967.
35. Lowe, S.W., Jacks, T., Housman, D.E., and Ruley, H.E. 1994. Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc. Natl. Acad. Sci. 91: 2026-2030.
36. MacKenzie, K.L., Franco, S., Naiyer, A.J., May, C., Sadelain, M., Rafii, S., and Moore, M.A. 2002. Multiple stages of malignant transformation of human endothelial cells modelled by co-expression of telomerase reverse transcriptase, SV40 T antigen and oncogenic N-ras. Oncogene 21: 4200-4211.
37. Marx, J. 2002. Debate surges over the origins of genomic defects in cancer. Science 297: 544-546.
38. Masutomi, K., Yu, E.Y., Khurts, S., Ben-Porath, I., Currier, J.L., Metz, G.B., Brooks, M.W., Kaneko, S., Murakami, S., DeCaprio, J.A., et al. 2003. Telomerase maintains telomere structure in normal human cells. Cell 114: 241-253.
39. Morales, C.P., Holt, S.E., Ouellette, M., Kaur, K.J., Yan, Y., Wilson, K.S., White, M.A., Wright, W.E., and Shay, J.W. 1999. Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat. Genet. 21: 115-118.
40. Nigro, J.M., Baker, S.J., Preisinger, A.C., Jessup, J.M., Hostetter, R., Cleary, K., Bigner, S.H., Davidson, N., Baylin, S., Devilee, P., et al. 1989. Mutations in the p53 gene occur in diverse human tumour types. Nature 342: 705-708.
41. O'Brien, W., Stenman, G., and Sager, R. 1986. Suppression of tumor growth by senescence in virally transformed human fibroblasts. Proc. Natl. Acad. Sci. 83: 8659-8663.
42. Parrinello, S., Samper, E., Krtolica, A., Goldstein, J., Melov, S., and Campisi, J. 2003. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5: 741-747.
43. Pihan, G. and Doxsey, S.J. 2003. Mutations and aneuploidy: Co-conspirators in cancer? Cancer Cell 4: 89-94.
44. Poon, R.Y.C., Toyoshima, H., and Hunter, T. 1995. Redistribution of the CDK inhibitor p27 between different cyclin CDK complexes in the mouse fibroblast cell cycle and in cells arrested with lovastatin or ultraviolet irradiation. Mol. Biol. Cell 6: 1197-1213.
45. Purdie, C.A., Harrison, D.J., Peter, A., Dobbie, L., White, S., Howie, S.E., Salter, D.M., Bird, C.C., Wyllie, A.H., Hooper, M.L., et al. 1994. Tumour incidence, spectrum and ploidy in mice with a large deletion in the p53 gene. Oncogene 9: 603-609.
46. Qin, X.Q., Livingston, D.M., Kaelin Jr., W.G., and Adams, P.D. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. 91: 10918-10922.
47. Ramirez, R.D., Morales, C.P., Herbert, B.S., Rohde, J.M., Passons, C., Shay, J.W., and Wright, W.E. 2001. Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes & Dev. 15: 398-403.
48. Rawson, C., Shirahata, S., Collodi, P., Natsuno, T., and Bames, D. 1991. Oncogene transformation frequency of nonsenescent SFME cells is increased by c-myc. Oncogene 6: 487-489.
49. Rich, J.N., Guo, C., McLendon, R.E., Bigner, D.D., Wang, X.F., and Counter, C.M. 2001. A genetically tractable model of human glioma formation. Cancer Res. 61: 3556-3560.
50. Ruley, H.E. 1983. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature 304: 602-606.
51. Seger, Y.R., Garcia-Cao, M., Piccinin, S., Cunsolo, C.L., Doglioni, C., Blasco, M.A., Hannon, G.J., and Maestro, R. 2002. Transformation of normal human cells in the absence of telomerase activation. Cancer Cell 2: 401-413.
52. INK4a. Cell 88: 593-602.
53. Sherr, C.J. and DePinho, R.A. 2000. Cellular senescence: Mitotic clock or culture shock? Cell 102: 407-410.
54. Shieh, S.Y., Ikeda, M., Taya, Y., and Prives, C. 1997. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334.
55. Shih, I.M., Zhou, W., Goodman, S.N., Lengauer, C., Kinzler, K.W., and Vogelstein, B. 2001. Evidence that genetic instability occurs at an early stage of colorectal tumorigenesis. Cancer Res. 61: 818-822.
56. Siliciano, J.D., Canman, C.E., Taya, Y., Sakaguchi, K., Appella, E., and Kastan, M.B. 1997. DNA damage induces phosphorylation of the amino terminus of p53. Genes & Dev. 11: 3471-3481.
57. Soucek, L. and Evan, G. 2002. Myc-Is this the oncogene from Hell? Cancer Cell 1: 406-408.
58. Stevenson, M. and Volsky, D.J. 1986. Activated v-myc and v-ras oncogenes do not transform normal human lymphocytes. Mol. Cell. Biol. 6: 3410-3417.
59. Todaro, G.J. and Green, H. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17: 299-313.
60. Vara, O., Wade, M., Kern, S., Beeche, M., Pandita, T.K., Hampton, G.M., and Wahl, G.M. 2002. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: A mechanism for oncogene-induced genetic instability. Mol. Cell 9: 1031-1044.
61. Vaziri, H. and Benchimol, S. 1998. Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr. Biol. 8: 279-282.
62. Wang, T.L., Rago, C., Silliman, N., Ptak, J., Markowitz, S., Willson, J.K., Parmigiani, G., Kinzler, K.W., Vogelstein, B., and Velculescu, V.E. 2002. Prevalence of somatic alterations in the colorectal cancer cell genome. Proc. Natl. Acad. Sci. 99: 3076-3080.
63. Wu, X. and Levine, A.J. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. 91: 3602-3606.
64. ARF, is a candidate for the plasmacytoma susceptibility locus, Pctrl. Proc. Natl. Acad. Sci. 95: 2429-2434.
65. Zimonjic, D., Brooks, M.W., Popescu, N., Weinberg, R.A., and Hahn, W.C. 2001. Derivation of human tumor cells in vitro without widespread genomic instability. Cancer Res. 61: 8838-8844.