Wild-type p53 can induce p21 and apoptosis in neuroblastoma cells but the DNA damage-induced G1 checkpoint function is attenuated

Clinical Cancer Research

Volumn 5, Issue 12, 1999, Pages 4199-4207

  McKenzie, Pamela P ^a   Guichard, Sylvie M ^a,b   Middlemas, David S ^a   Ashmun, Richard A ^a   Danks, Mary K ^a   Harris, Linda C ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b INSTITUT CLAUDIUS REGAUD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P21; PROTEIN P53;

APOPTOSIS; ARTICLE; CANCER SURVIVAL; CELL CYCLE G1 PHASE; CELL GROWTH; DNA DAMAGE; GENE INDUCTION; GENE MUTATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IONIZING RADIATION; NEURAL CREST; NEUROBLASTOMA CELL; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

ADENOVIRIDAE; APOPTOSIS; CELL NUCLEUS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA DAMAGE; FLUORESCENT ANTIBODY TECHNIQUE; G1 PHASE; HUMANS; NEUROBLASTOMA; TRANSCRIPTION, GENETIC; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033385058     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (46)

1. Lane, D. P. p53, guardian of the genome. Nature (Lond.), 358: 15-16, 1992.
2. Zambetti, G. P., and Levine, A. J. A comparison of the biological activities of wild-type and mutant p53. FASEB J., 7: 855-865, 1993.
3. El-Deiry, W. S., Harper, J. W., O'Conner, P. M., Velculescu, V. E., Canman, C. E., Jackman, J., Pietenpol, J. A., Burrell, M., Hill, D. E., Wang, Y., Wiman, K. G., Mercer, W. E., Kastan, M. B., Kohn, K. W., Elledge, S. J., Kinzler, K. W., and Vogelstein, B. WAF1/CIP1 is induced upon p53-mediated growth arrest and apoptosis. Cancer Res., 54: 1169-1174, 1994.
4. Lowe, S. W., Ruley, H. E., Jacks, T., and Houseman, D. E. p53-dependent apoptosis modulates the cytotoxicity of anticancer drugs. Cell, 74: 957-967, 1993.
5. Fan, S., El-Deiry, W. S., Bae, I., Freeman, J., Jondle, D., Bhatia, K., Fornace, A. J., Jr., Magrath, I., Kohn, K. W., and O'Connor, P. M. p53 gene mutations are associated with decreased sensitivity of human lymphoma cells to DNA damaging agents. Cancer Res., 54: 5824-5830, 1994.
6. Kohn, K. W., Jackman, J., and O'Connor, P. M. Cell cycle control and cancer chemotherapy. J. Cell. Biochem., 54: 440-452, 1994.
7. Levine, A. J., Momand, J., and Finlay, C. A. The p53 tumor suppressor gene. Nature (Lond.), 351: 453-455, 1991.
8. Jacks, T., Remington, L., Williams, B. O., Schmitt, E. M., Halachmi, S., Bronson, R. T., and Weinberg, R. A. Tumor spectrum analysis in p53-mutant mice. Curr. Biol., 4: 1-7, 1994.
9. Vogan, K., Bernstein, M., Leclerc, J. M., Brisson, L., Brodeur, G. M., Pelletier, J., and Gros, P. Absence of p53 mutations in primary neuroblastomas. Cancer Res., 53: 5269-5273, 1993.
10. Oliner, J. D., Kinzler, K. W., Meltzer, P. S., George, D. L., and Vogelstein, B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature (Lond.), 358: 80-83, 1992.
11. Momand, J., Zambetti, G. P., Olson, D. C., George, D., and Levine, A. J. The MDM2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell, 69: 1237-1245, 1992.
12. Knippschild, U., Oren, M., and Deppert, W. Abrogation of wildtype p53 mediated growth-inhibition by nuclear exclusion. Oncogene, 12: 1755-1765, 1996.
13. Moll, U. M., Ostermeyer, A. G., Haladay, R., Winkfield, B., Frazier, M., and Zambetti, G. P. Cytoplasmic sequestration of wild-type p53 protein impairs the G1 checkpoint after DNA damage. Mol. Cell. Biol., 16: 1126-1137, 1996.
14. Matthay, K. K. Neuroblastoma. A clinical challenge and biological puzzle. CA Cancer J. Clin., 45: 179-192, 1995.
15. Crist, W. M., and Kun, L. E. Common solid tumors of childhood. N. Engl. J. Med., 324: 461-471, 1991.
16. Goldman, S. C., Chen, C-Y., Lansing, T. J., Gilmer, T. M., and Kastan, M. B. The p53 signal transduction pathway is intact in human neuroblastoma despite cytoplasmic localization. Am. J. Pathol., 148: 1381-1385, 1996.
17. Thompson, J., Zamboni, W. C., Cheshire, P. J., Lutz, L., Luo, X., Li, Y., Houghton, J. A., and Houghton, P. J. Efficacy of systemic administration of irinotecan against neuroblastoma xenografts. Clin. Cancer Res., 3: 423-431, 1997.
18. Danks, M. K., Garrett, K. E., Marion, R. C., and Whipple, D. O. Subcellular redistribution of DNA topoisomerase I in anaplastic astrocytoma cells treated with topotecan. Cancer Res., 56: 1664-1673, 1996.
19. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254, 1976.
20. McPake, C. R., Tillman, D. M., Poquette, C. A., George, E. O., Houghton, J. A., and Harris, L. C. Bax is an important determinant of chemosensitivity in pediatric tumor cell lines independent of Bcl-2 expression and p53 status. Oncol. Res., 10: 235-244, 1998.
21. Davidoff, A. M., Pence, J. C., Shorter, N. A., Inglehart, J. D., and Marks, J. R. Expression of p53 in human neuroblastoma- and neuroepithelioma-derived cell lines. Oncogene, 7: 127-133, 1992.
22. Thottassery, J., Zambetti, G., Arimori, K., and Schuetz, J. p53 regulates expression of the endogenous mdr gene. Proc. Am. Assoc. Cancer Res., 38: 251, 1997.
23. Kastan, M. B., Onyekwere, O., Sidransky, D., Vogelstein, B., and Craig, R. W. Participation of p53 protein in the cellular response to DNA damage. Cancer Res., 51: 6304-6311, 1991.
24. Isaacs, J. S., Hardman, R., Carman, T. A., Barrett, J. C., and Weissman, B. E. Differential subcellular p53 localization and function in N- and S-type neuroblastoma cell lines. Cell Growth Differ., 9: 545-555, 1998.
25. Danks, M. K., Whipple, D. O., McPake, C. R., Lu, D., and Harris, L. C. Differences in epitope accessibility of p53 monoclonal antibodies suggest at least three conformations or states of protein binding of p53 protein in human tumor cell lines. Cell Death Differ., 5: 678-686, 1998.
26. Stewart, N., Hicks, G. G., Paraskevas, F., and Mowat, M. Evidence for a second cell cycle block at G2/M by p53. Oncogene, 10: 109-115, 1995.
27. Agarwal, M. L., Agarwal, A., Taylor, W. R., and Stark, G. R. p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc. Natl. Acad. Sci. USA., 92: 8493-8497, 1995.
28. Hwang, A., and Muschel, R. J. Radiation and the G2 phase of the cell cycle. Radiat. Res., 150: S52-S59, 1998.
29. Watanabe, T., Kuszynski, C., Ino, K., Heimann, D. G., Shepard, H. M., Yasui, Y., Maneval, D. C., and Talmadge, J. E. Gene transfer into human bone marrow hematopoietic cells mediated by adenoviral vectors. Blood, 87: 5032-5039, 1996.
30. Oliner, J. D., Pietenpol, J. A., Thiagalingam, S., Gyuris, J., Kinzler, K. W., and Vogelstein, B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature (Lond.), 362: 857-860, 1993.
31. El Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. P., Parsons, R., Trent, J. M., Liu, D., Merrer, W. E., Kinzler, K. W., and Vogelstein, B. WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993.
32. Dulic, V., Kaufmann, W. K., Wilson, S. J., Tlsty, T. D., Lees, E., Harper, J. W., Elledge, S. J., and Reed, S. I. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell, 76: 1013-1023, 1994.
33. Beijersbergen, R. L., and Bernards, R. Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins. Biochim. Biophys. Acta, 1287: 103-120, 1996.
34. Bhatia, K., Fan, S., Spangler, G., Weintraub, M., O'Connor, P. M., Judde, J. G., and Magrath, I. A mutant p21 cyclin-dependent kinase inhibitor isolated from a Burkitt's lymphoma. Cancer Res., 55: 1431-1435, 1995.
35. Gao, X., Chen, Y. Q., Wu, N., Grignon, D. J., Sakr, W., Porter, A. T., and Honn, K. V. Somatic mutations of the WAF1/CIP1 gene in primary prostate cancer. Oncogene, 11: 1395-1398, 1995.
36. Balbin, M., Hannon, G. J., Pendas, A. M., Ferrando, A. A., Vizoso, F., Fueyo, A., and Lopez-Otin, C. Functional analysis of a p21WAF1, CIP1, SDI1 mutant (Arg94→Trp) identified in a human breast carcinoma. Evidence that the mutation impairs the ability of p21 to inhibit cyclin-dependent kinases. J. Biol. Chem., 271: 15782-15786, 1996.
37. Welcker, M., Lukas, J., Strauss, M., and Bartek, J. p21WAF1/CIP1 mutants deficient in inhibiting cyclin-dependent kinases (CDKs) can promote assembly of active cyclin D/CDK4(6) complexes in human tumor cells. Cancer Res., 58: 5053-5056, 1998.
38. Easton, J., Wei, T., Lahti, J. M., and Kidd, V. J. Disruption of the cyclin D/cyclin dependent kinase/INK4/retinoblastoma protein regulatory pathway in human neuroblastomas. Cancer Res., 58: 2624-2632, 1998.
39. O'Connor, P. M., Jackman, J., Jondle, D., Bhatia, K., Magrath, I., and Kohn, K. W. Role of the p53 tumor suppressor gene in cell cycle arrest and radiosensitivity of Burkitt's lymphoma cell lines. Cancer Res., 53: 4776-4780, 1993.
40. Clarke, A. R., Purdie, C. A., Harrison, D. J., Morris, R. G., Bird, C. C., Hooper, M. L., and Wyllie, A. H. Thymocyte apoptosis induced by p53-dependent and independent pathways [see comments]. Nature (Lond.), 362: 849-852, 1993.
41. Guillouf, C., Rosselli, F., Krishnaraju, K., Moustacchi, E., Hoffman, B., and Liebermann, D. A. p53 involvement in control of G2 exit of the cell cycle: role in DNA damage-induced apoptosis. Oncogene, 10: 2263-2270, 1995.
42. Lee, J. M., and Bernstein, A. p53 mutations increase resistance to ionizing radiation. Proc. Natl. Acad. Sci. USA, 90: 5742-5746, 1993.
43. Waldman, T., Lengauer, C., Kinzler, K. W., and Vogelstein, B. Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature (Lond.), 381: 713-716, 1996.
44. WAF1/CIP1/MDA6 increases the susceptibility of human leukemia cells (U937) to 1-β-D-arabinofuranosylcytosine-mediated mitochondrial dysfunction and apoptosis. Cancer Res., 59: 1259-1267. 1999.
45. CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell, 82: 675-684, 1995.
46. Kasten, M. M., and Giordano, A. pRB and the cdks in apoptosis and the cell cycle. Cell Death Differ., 5: 132-140, 1998.