Influence of topoisomerase II inhibitors and ionizing radiation on growth arrest and cell death pathways in the breast tumor cell

Cell Biochemistry and Biophysics

Volumn 33, Issue 1, 2000, Pages 19-31

  Gewirtz, David A ^a   Sundaram, Sujatha ^b   Magnet, Karen J ^c  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c TRIPLER ARMY MEDICAL CENTER   (United States)

Author keywords

Adriamycin; Apoptoti cell death; Irradiation; MCF 7 cells; Vitamin D

Indexed keywords

ANTINEOPLASTIC AGENT; CALCITRIOL; COLECALCIFEROL; DNA TOPOISOMERASE (ATP HYDROLYSING); DRUG DERIVATIVE; ENZYME INHIBITOR; SEOCALCITOL;

APOPTOSIS; BREAST TUMOR; CELL CULTURE; CELL CYCLE; CELL DIVISION; DNA DAMAGE; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; HUMAN; IONIZING RADIATION; PATHOLOGY; RADIATION EXPOSURE; REVIEW;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CALCITRIOL; CELL CYCLE; CELL DIVISION; CHOLECALCIFEROL; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II; ENZYME INHIBITORS; FEMALE; HUMANS; RADIATION, IONIZING; TUMOR CELLS, CULTURED;

EID: 0034569758     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/CBB:33:1:19     Document Type: Article

References (106)

1. Lowe, S. W., Ruley, H. E., Jacks, T., and Housman, D. E. (1993) p53 dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74, 957-967.
2. Lowe, S. W., Bodis, S., Remington, L., Ruley, H. E., Fisher, D., Housman, D. E., and Jacks, T. (1994) p53 status and the efficacy of cancer therapy in vivo. Science 266, 807-810.
3. Magnet, K. J. and Gewirtz, D. A. Influence of ionizing radiation on elements of the G1 check-point and apoptotic pathways; relationship to growth arrest and cell death in breast tumor cells with wild-type p53 (In preparation).
4. Di, Y-M., Akalin A., Holt, S. E. and Gewirtz, D. A. Suppression of telomerase with induction of senescence in p53 wild-type MCF-7 breast tumor cells and delayed apoptosis in p53 mutated MDA-MB231 breast tumor cells after acute exposure to adriamycin. In preparation.
5. Jones. K. R. and Gewirtz, D. A. Non-apoptotic cell death and growth arrest in response to adriamycin in the p53 mutated T47D breast tumor cell line. In preparation.
6. Oberhammer, F., Wilson, J. W., Dive, C., Morris, I. D., Hickman, J. A., Wakeling, A. E., Walker, P. R., and Sikorska, M. (1993) Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J. 12, 3679-3684.
7. Fornari, F. A., Jarvis, W. D., Grant, S., Orr, M. S., Randolph, J. K., White, F. K. H., Mumaw, V. R., Lovings, E. T., Freeman, R. H., and Gewirtz, D. A. (1994) Induction of differentiation and growth arrest associated with nascent (nono-ligosomal) DNA fragmentation and reduced c-myc expression in MCF-7 human breast tumor cells after continuous exposure to a sublethal concentration of doxorubicin. Cell Growth Diff. 5, 723-733.
8. Wilson, J. W., Wakeling, A. E., Morris, I. D., Hickman, J. A., and Dive, C. (1995) MCF-7 human mammary adenocarcinoma cell death in vitro in response to hormonal withdrawal and DNA damage. Int. J. Cancer 51, 502-508.
9. Fan, S., Smith, M. L., Rivet, D. J., Duba, D., Zhan, Q., Kohn, K. W., Forance, A. J., and O'Connor, P. M. (1995) Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res. 55, 1649-1654.
10. Fornari, F. A., Jarvis, W. D., Orr, M. S., Randolph, J. K., Grant, S., and Gewirtz, D. A. (1996) Growth arrest and non-apoptotic cell death associated with the suppression of c-myc expression in MCF-7 breast tumor cells following acute exposure to doxorubicin. Biochem. Pharmacol. 51, 931-940.
11. Saunders, D. E., Lawrence, W. D., Christensen, C., Wappler, N. L., Ruan, H., and Deppe G. (1997) Paclitaxel-induced apoptosis in MCF-7 breast cancer cells. Int. J. Cancer 70, 214-220.
12. Watson, N. C., Di, Y-M., Orr, M. S., Fornari, F. A., Randolph, J. K., Magnet, K. J., Jain, P. T., and Gewirtz, D. A. (1997) The influence of ionizing radiation on proliferation, c-myc expression and the induction of apoptotic cell death in two breast tumor cell lines differing in p53 status. Int. J. Rad. Biol. 72, 547-559.
13. Whitacre, C. M. and Berger, N. A. (1997) Factors affecting topotecan induced programmed cell death: adhesion protects cells from apoptosis and impairs cleavage of poly(ADP-ribose) polymerase. Cancer Res. 57, 2157-2163.
14. Ling, Y-H., Priebe, W., and Perez-Solar, R. (1993) Apoptosis induced by anthracycline antibiotics in P388 parent and multidrug resistant cells. Cancer Res. 53, 1845-1852.
15. Skladanowski, A. and Konopa, J. (1993) Adriamycin and daunomycin induce programmed cell death (apoptosis) in tumour cells. Biochem. Pharmacol. 46, 375-382.
16. Zaleskis, G., Berleth, E., Verstovek, S., Ehrke, M. J., and Mihich, E. (1994) Doxorubicin-induced DNA degradation in murine thymocytes. Mol. Pharmacol. 46, 901-908.
17. Bose, R., Verheji, M., Haimovitz-Friedman, A., Scotto, K., Fuks, Z., and Kolesnick R. (1995) Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals. Cell 82, 405-414.
18. Jaffrezou, J-P., Levade, T., Bettaieb, A., Andrieu, N., Bezombes, C., Maestre, N., Vermeersch, S., Rousse, A., and Laurent, G. (1996) Daunorubicin-induced apoptosis: triggering of ceramide generation through sphingomyelin hydrolysis. EMBOJ. 15, 2417-2424.
19. Herr, I., Wilhelm, D., Bohler, T., Angel, P., and Debatin, K. M. (1997) Activation of CD95 (APO-1/FAS) signaling by ceramide mediates cancer therapy-induced apoptosis. EMBO J. 16, 6200-6208.
20. Gamen, S., Anel, A., Lasierra, P., Alava, M. A., martinez-Lorenzo, M. J., Piniero, A., and Naval, J. (1997) Doxorubicin-induced apoptosis in human T-cell leukemia is mediated by caspase-3 activation in a Fas-independent way. FEBS Lett. 417, 360-354.
21. Jeremias, I., Kupatt, C., Baumann, B., Herr, I., Wirth, T., and Debatin, K. M. (1998) Inhibition of nuclear factor kappaB activation attenuates apoptosis resistance in lymphoid cells. Blood 91, 4624-4631.
22. Gewirtz, D. A., Randolph, J. K., Chalwa, J., Orr, M. S., and Fornari, F. A. (1998) Induction of DNA damage, inhibition of DNA synthesis and suppression of c-myc expression by the anthra-cycline analog, idarubicin. Cancer Chemother Pharmacol. 41, 361-369.
23. Yonish-Rouach, E., Reznitsky, D., Lotem, J., Sachs, L., Kimchi, A., and Oren, M., (1991) Wildtype p53 induces apoptosis of myeloid leukemic cells that is inhibited by interleukin-2. Nature 352, 345-347.
24. Ramqvist, T., Magnusson, K. P., Wang, Y., Szekely, L., Klein, G., and Wiman, K. G. (1993) Wild-type p53 induces apoptosis in a Burkitt Lymphoma (BL) line that carries mutant p53. Oncogene 8, 1495-1500.
25. Radford, I. J., Murphy, T. K., Radlev, J. M., and Ellis, S. L. (1994) Radiation response of mouse lymphoma and melanoma cells Part II. Apoptotic death is shown in all cell lines examined. Int. J. Rad. Biol. 65, 217-227.
26. Bracey, T. S., Miller, J. C., and Paraskeva, C. (1995) Radiation induced apoptosis in human colorectal adenoma and carcinoma cell lines can occur in the absence of wild type p53. Oncogene 10, 2391-2396.
27. Maity, A., McKenna, W. G., and Muschel, R. J. (1994) The molecular basis for cell cycle delays following ionizing radiation: a review. Radiother Oncol. 31, 1-13.
28. Cameron, D. A., Ritchie, A. A., Langdon, S., Anderson, T. J., and Miller, W. R. (1997) Tamoxifen induced apoptosis in ZR-75 breast cancer xenografts antedates tumor regression. Breast Cancer Res. Treat. 45, 99-107.
29. Toma, S, Isnardi, L., Raffo, P., Dastoli, G., De Francisci, E., Riccardi, L., Palumbo, R., and Bollag, W. (1997) Effects of all-trans-retinoic acid and 13-cis-retinoic acid on breast cancer cell lines: growth inhibition and apoptosis induction. Int. J. Cancer 70, 619-627.
30. Eck, K. M., Yuan, L., Duffy, L., Ram, P. T., Ayettey, S., Chen, I., Cohn, C. S., Reed, J. C., and Hill, S. M. (1998) A sequential treatment regimen with melatonin and all-trans retinoic acid induces apoptosis in MCF-7 tumour cells. Br. J. Cancer 77, 2129-2137.
31. Schaerli, P. and Jaggi, R. (1998) EGF-induced programmed cell death of human mammary carcinoma MDA-MB468 cells is preceded by activation of AP-1. Cell Mol. Life Sci. 54, 129-138.
32. cdc2 kinase activation and apoptosis inhibited by 12-O-Tetradecanoyl phorbol-13-acetate in human breast MCF-7 adenocarcinoma cells. Cell Growth Diff. 9, 25-29.
33. Uckun, F. M., Narla, R. K., Jun, X., Zeren, T., Yen katachalam, T., Waddick, K. G., Rostostev, A., and Myers, D. E. (1998) Cytotoxic activity of epidermal growth factor-genistein against breast cancer cells. Clin. Cancer Res. 4, 901-912.
34. Kastan, M. B., Onyekwere, O., Sidransky, D., Vogelstein, B., and Craig, R. W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51, 6304-6311.
35. waf1/cip1 expression in human breast epithelial cells. Oncogene 11, 253-261.
36. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. (1993) The p21 cdk-interacting protein cip 1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75, 805-816.
37. Chellappan, S. P., Hiebert, S., Mudryj, M., Horowitz, J. M., and Nevins, J. R. (1991) The E2F transcription factor is a cellular target for the Rb protein. Cell 65, 1053-1061.
38. Wang, J. Y. J., Knudsen, E. S., and Welch, P. J. (1994) The retinoblastoma tumor suppressor protein. Adv. Cancer Res. 64, 25-85.
39. Weinberg, RA. (1995) The retinoblastoma protein and cell cycle control. Cell 81, 323-330 (1995).
40. Beijersbergen, R. L. and Bernards, R. (1996) Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins. Biochim Biophys Acta 1287, 103-120.
41. Helin, K., Wu, C. L., Fattaey, A. R., Lees, J. A., Dynlacht, B. D., Ngwu, C., and Harlow, E. (1993) Heterodimerization of the transcription factor E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7, 1850-1861.
42. Tao, Y., Kassatly, R. F., Cress, W. D., and Horowitz, J. M. (1997) Subunit composition determines E2F DNA-binding site specificity. Mol. Cell. Biol. 17, 6994-7007.
43. Weintraub, S. J., Prater, C. A., and Dean, D. C. (1992) Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358, 259-261.
44. Farnham, P. J., Slansky, J. E., and Kollmer, R. (1993) The role of E2F in the mammalian cell cycle. Biochim Biophys Acta. 1155, 125-131.
45. Sala, A., Nicolaides, N. C., Engelhard, A., Bellon, T., Lawe, D. C., Arnold, A, Grana, X., Giordano, A., and Calabretta, B. (1994) Correlation between E2F-1 requirement in the S phase and E2F-1 transactivation of cell cycle related genes in human cells. Cancer Res. 54, 1402-1406.
46. Weintraub, S. J., Chow, K. N., Luo, R. X., Zhang, S. H., He, S., and Dean, D. C. (1995) Mechanism of active transcriptional repression by the retinoblastoma protein. Nature 375, 812-815.
47. Huang, Y., Ishiko, T., Nakada, S., Utsugisawa, T., Kato, T., and Yuan, Z-M. (1997) Role for E2F in DNA damage induced entry of cells into S phase. Cancer Res. 57, 3640-3643.
48. Flores-Rozas, H., Kelman, Z., Dean, F. B., Pan, Z. Q., Harper, J. W., Elledge, S. J., O'Donnell, M., and Hurwitz, J. (1994) CDK interacting protein 1 binds directly with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by the DNA polymerase delta holoenzyme. Proc. Natl. Acad. Sci. USA 91, 8655-8659.
49. Waga, S., Hannon, J. G., Beach, D., and Stillman, B. (1994) The p21 inhibitor of cyclin dependent kinase controls DNA replication by interaction with PCNA. Nature 369, 574-578.
50. Evan, G. I., Wyllie, A. H., Gilbert, C. S., Littlewood, T. D., Land, H., Brooks, M., Walters, C. M., Penn, L. Z., and Hancock, D. C. (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell 69, 119-128.
51. Lowe, S. W., Schmitt, E. M., Smith, S. W., Osborn, B. A., and Jacks, T. (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362, 847-849.
52. Wu, X. and Levine, A. J. (1994) p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91, 3602-3606.
53. Hermeking, H. and Eick, D. (1994) Mediation of c-Myc induced apoptosis by p53. Science 265, 2091-2093.
54. DeGregori, J., Leone, G., Miron, A., Jakoi, L., and Nevins, J. R. (1997) Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. 94, 7245-7250.
55. Rupnow, B. A., Alarcon, R. M., Giaccia, A. J., and Knox, S. J. (1998) p53 mediates apoptosis induced by c-Myc activation in hypoxic or gamma irradiated fibroblasts. Cell Death Diff. 5, 141-147.
56. Oltvai, Z. N., Milliman, C. L., and Korsmeyer, S. J. (1993) Bcl-2 heterodimerizes in vivo with a homologue Bax that accelerates programmed cell death. Cell 74, 609-619.
57. Boise, L. H., Gonzales-Garcia, M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X., Nunez, G., and Thompson C. (1993) bcl-x, a bcl-2 related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597-608.
58. Schott, A. F., Apel, I. J., Nunez, G., and Clarke, M. F. (1995) Bcl-x, protects cancer cells from p53-mediated apoptosis. Oncogene 11, 1389-1394.
59. L and Bcl-2 displaces Bax and promotes cell death. Cell 80, 285-291.
60. Bargou, R. C., Daniel, P. T., Mapara, M. Y., Bommert, K., Wagener, C., Kallinich, B., Royer, H. D., and Dorken, B. (1995) Expression of the bcl-2 gene family in normal and malignant breast tissue: low bax expression in tumor cells correlates with resistance towards apoptosis. Intl. J. Cancer 60, 845-859.
61. Kluck, R. M., Bossy-Wetzel, E., Green, D. R., and Newmeyer, D. D. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
62. Kroemer, G. (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med. 3, 614-620.
63. L regulates the membrane potential and volume homeostasis of mitochondria. Cell 91, 627-637.
64. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Grifin, P. R., Labelle, M., Lazebnik, Y A. et al. (1995) Identification and inhibition of the ICE/CED3 protease necessary for mammalian apoptosis. Nature 376, 37-43.
65. White E. (1996) Life, death and the pursuit of apoptosis. Genes Dev. 10, 1-15.
66. Cheng, E. H-Y., Kirsch, D. G., Clem, R. J., Ravi, R., Kastan, M. B., Bedi, A., Ueno, K., and Hardwick, J. M. (1997) Conversion of Bcl-2 to a Bax like death effector by caspases. Science 278, 1966-1968.
67. Zou, H., Henzel, W. J., Liu, X., Lutscheg, A., and Wang, X. (1997) Apaf, a human protein analog to C elegans CED-4, participates in cytochrome c dependent activation of caspase 3. Cell 90, 405-413.
68. Schmitt, E., Sane, A. T., Steyaert, A., Cimoli, G., and Bertrand R. (1997) The Bcl-xl and Bax-alpha control points: modulation of apoptosis induced by cancer chemotherapy and relation to TPCK-sensitive protease and caspase activa-tion. Biochem. Cell Biol. 75, 301-314.
69. Cohen, GM. (1997) Caspases: the executioners of apoptosis. Biochem J. 326, 1-16.
70. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., and Poirer, G. G. (1993) Specific proteolytic cleavage of poly (ADP-ribose) polymerase: an early marker of chemotherapy induced apoptosis. Cancer Res. 53, 3976-3985.
71. Jarvis, W. D., Kolesnick, R. N., Fornari, F. A., Traylor, R. A., Gewirtz, D. A., and Grant, S. (1994) Induction of apoptotic DNA damage and cell death by activation of the sphingomyelin pathway. Proc. Natl. Acad. Sci. 91, 73-77.
72. Wang, S., Guo, Y., Castillo, T., Dent, P., and Grant, S. (1998) Potentiation of taxol-induced apoptosis and antiproliferative effects in human myeloid leukemic cells (U937) by bryostatin-1. Biochem. Pharmacol. 56, 635-644.
73. Attardi L. D., Lowe S. W., Brugarolas, J., and Jacks, T. (1996) Transcriptional activation by p53 but not induction of the p21 gene, is essential for oncogene mediated apoptosis. EMBO J. 15, 3693-3701.
74. Polyak, K., Waldman, T., He, T-. C, Kinzler, K. W., and Vogelstein, B. (1996) Genetic determinants of p53-induced apoptosis and growth arrest. Genes Devel. 10, 1945-1952.
75. Rowan, S., Ludwig, R. L., Haupt, Y., Bates, S., Lu, X., Oren, M., and Vousden, K. H. (1996) Specific loss of apoptotic but not cell cycle arrest function in a human tumor derived p53 mutant. EMBO J. 15, 827-838.
76. waf1/Cip1 protects againts p53-mediated apoptosis of human melanoma cells. Oncogene 14, 929-935.
77. waf1/cip1-mediated G1 arrest and induces apoptosis in human cancer cells. Oncogene 15, 1903-1909.
78. Sherr, J. C. and Weber, J. D. (2000) The ARF/p53 Pathway. Curr Opin Genet Dev. 10: 94-99.
79. Haldar, S., Jena, N., and Croce, C. (1995) Inactivation of Bcl-2 by phosphorylation. Proc. Natl. Acad. Sci. USA 92, 4507-4511.
80. Blagosklonny, M. V., Giannakakou, P., El-Deiry, W. S., Kingston, D. G. I., Higgs, P. I., Neckers, L., and Fojo, T. (1997) Raf/bcl-2 phosphorylation: a step from microtubule damage to cell death. Cancer Res. 57, 130-135.
81. Srivastava, R. K., Srivastava, A. R., Korsmeyer, S. J., Nesterova, M., Cho-Chung, Y. S., and Longo, D. L. (1998) Involvement of microtubules in the regulation of BC1-2 phosphorylation and apoptosis through cyclic AMP dependent protein kinase. mol. Cell Biol. 18, 3509-3517.
82. L depends on normal p53 function. Oncogene 13, 2287-2293.
83. cdc2/cyclin B activity induced by doxorubicin in synchronized P388 cells. Mol. Pharmacol. 49, 832-841.
84. Rao, A. P. and Rao, P. N. (1976) The cause of G2 arrest in Chinese hamster ovary cells treated with anticancer drugs. J. Natl. Cancer Inst. 57, 1139-1143.
85. Konopa, J. (1988) G2 block induced by DNA crosslinking agents and its consequences. Biochem Pharmacol. 37, 2303-2309.
86. INK4 participates in a G1 arrest checkpoint in response to DNA damage. Mol. Cell Biol. 18, 378-387.
87. waf1/cip1 and promote Rb dephosphorylation but fail to suppress E2F activity in MCF-7 breast tumor cells. mol. Pharmacol. 52, 373-379.
88. Jain, P. T. and Gewirtz, D. A. Enhancement of p53 gene delivery to human breast tumor cells promotes apoptotic cell death (Submitted.)
89. Sundaram, S. and Gewirtz, D. A. (1999) The Vitamin D3 analog EB1089 enhances the response to radiation in human breast tumor cells. Rad Res 152: 479-486.
90. Sundaram, S. Chaudhry M. Reardon D. Gupta M. and Gewirtz, D. A. (2000) EB1089 enhances the antiproliferative and apoptotic effects of adriamycin in MCF-7 breast tumor cells. Breast Cancer Research and Treatment 1847: 1-10.
91. Colston, K. W., Mackay, A. G., James, S. Y., Binderup, L., Chandler, S, and Coombes, R. C. (1992) EB 1089, a new vitamin D analog that inhibits the growth of breast cancer cells in vivo and in vitro. Biochem. Pharmacol. 44, 2273-2280.
92. Colston, K. W., Chander, S. K., Mackay, A. G., and Coombes, R. C. (1992) Effects of synthetic Vitamin D analogs on breast cancer cell proliferation in vivo and in vitro. Biochem. Pharmacol. 44, 693-702.
93. 3 resistant MCF-7 cell line. Endocrinology 137, 400-409.
94. 3 on proliferation of cancer cells in vitro. Cancer Lett. 120, 65-69.
95. 3 resistant variant. Endocrinology 138, 4690-4698.
96. Rozen, F., Feng-Yang, X., Huynh, H., and Pollak, M. (1997) Antiproliferative action of Vitamin D related compounds and insulin-like growth factor-binding protein 5 accumulation. J. Natl. Cancer Inst. 89, 652-656.
97. James, S. Y., Mackay, A. G., and Colston K. W. (1995) Vitamin D derivatives in combination with cis-retinoic acid promote active cell death in breast cancer cells. J. Mol. Endocrinol. 14, 391-395.
98. 3 and EB 1089 on cell cycle kinetics and apoptosis in MCF-7 breast cancer cells. Breast Cancer Res. Treat. 42, 31-41.
99. L expression in human fibroblasts and acts in synergy with ionizing radiation to induce apoptosis. Rad. Res. 149, 187-194.
100. Chang, W. P. and Little, J. B. (1991) Delayed reproductive cell death in x-irradiated Chinese hamster ovary cells. Intl. J. Radiat. Biol. 60, 483-496.
101. Szumiel, I. (1994) Review: Ionizing radiation-induced cell death. Intl. J. Radiat. Biol. 66, 329-341.
102. Lock, R. B. and Stribinskiene, L. (1996) Dual modes of death induced by etoposide in human epithelial tumor cells allow Bcl-2 to inhibit apoptosis without affecting clonogenic survival. Cancer Res. 56, 4006-4012.
103. Han, J. W., Dionne, C. A., Kedersha, N. L., and Goldmacher, V. S. (1997) p53 status affects the rate of onset but not the overall extent of doxorubicin-induced cell death in rat-1 fibroblasts constitutively expressing c-myc. Cancer Res. 57, 176-182.
104. Olivier, M., Bautista, S., Vallies, H., and Theillet, C. (1998) Relaxed cell cycle arrests and propagation of unrepaired chromosomal damage in cancer cell lines with wild type p53. Mol Carcinogen. 23, 1-12.
105. Schmidt-Ulrich, R. K., Contessa, J. N., Dent P., Mikkelsen, R. B., Valerie, K., Reardon, C. B., Bowers, G. and Lin P-S. (1999) Molecular mechanisms of radiation-induced accelerated repopulation. Radiat Oncol Invest. 7: 321-330.
106. Gewirtz, D. A. (2000) Growth arrest and cell death in the breast tumor cell in response to ionizing radiation and chemotherapeutic agents which induce DNA damage. Breast Cancer Research and Treatment 1621: 1-13.