Poly(ADP-ribosyl)ation of p53 during apoptosis in human osteosarcoma cells

Cancer Research

Volumn 59, Issue 9, 1999, Pages 2190-2194

  Simbulan Rosenthal, Cynthia M ^a   Rosenthal, Dean S ^a   Luo, RuiBai ^a   Smulson, Mark E ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DNA FRAGMENT; FAS ANTIGEN; GLYCOSIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN BAX; PROTEIN P53;

ADENOSINE DIPHOSPHATE RIBOSYLATION; APOPTOSIS; ARTICLE; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVATION; ENZYME DEGRADATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; OSTEOSARCOMA CELL; PRIORITY JOURNAL;

EID: 0033135756     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Kastan, M. B., Zhan, Q., El-Delry, W. S., Carrier, F., Jacks, T., Walsh, W. V., Plunkett, B. S., Vogelstein, B., and Fornace, A. J. J. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell, 71: 587-597, 1992.
2. 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.
3. Levine, A. p53, the cellular gatekeeper for growth and division. Cell, 88: 323-331, 1997.
4. Gradwohl, G., Menissier de-Murcia, J. M., Molinete, M., Simonin, F., Koken, M., Hoeijimakers, J. H., and de Murcia, G. The second zinc-finger domain of poly (ADP-ribose) polymerase determines specificity for single-stranded breaks in DNA. Proc. Natl. Acad. Sci. USA, 87: 2990-2994, 1990.
5. Malik, N., Miwa, M., Sugimura, T., Thraves, P., and Smulson, M. Immunoaffinity fractionation of the poly(ADP-ribosyl)ated domains of chromatin. Proc. Natl. Acad. Sci. USA, 80; 2554-2558, 1983.
6. Thraves, P. J., Kasid, U., and Smulson, M. E. Selective isolation of domains of chromatin proximal to both carcinogen-induced DNA damage and poly(ADP-ribosyl)ation. Cancer Res., 45: 386-391, 1985.
7. Satoh, M. S., and Lindahl, T. Role of poly(ADP-ribose) formation in DNA repair. Nature (Lond.), 356: 356-358, 1992.
8. +-dependent repair of damaged DNA by human cell extracts. J. Biol. Chem., 268: 5480-5487, 1993.
9. Smulson, M., Istock, N., Ding, R., and Chemey, B. Deletion mutants of poly(ADP-ribose) polymerase support a model of cyclic association and dissociation of enzyme from DNA ends during DNA repair. Biochemistry, 33: 6186-6191, 1994.
10. Smulson, M. E., Pang, D., Jung, M., Dimtchev, A., Chasovskikh, S., Spoonde, A., Simbulan-Rosenthal, C., Rosenthal, D., Yakovlev, A., and Dritschilo, A. Irreversible binding of poly(ADP-ribose) polymerase cleavage product to DNA ends revealed by atomic force microscopy: possible role in apoptosis. Cancer Res., 58: 3495-3498, 1998.
11. Kasid, U. N., Halligan, B., Liu, L. F., Dritschilo, A., and Smulson, M. Poly(ADP-ribose)-mediated post-translational modification of chromatin-associated human topoisomerase I. Inhibitory effects on catalytic activity. J. Biol. Chem., 264: 18687-18692, 1989.
12. Simbulan-Rosenthal, C. M. G., Rosenthal, D. S., Hilz, H., Mickey, R., Malkas, L., Applegren, N., Wu, Y., Bers, G., and Smulson, M. The expression of poly(ADP-ribose) polymerase during differentiation-linked DNA replication reveals that this enzyme is a component of the multiprotein DNA replication complex. Biochemistry, 35: 11622-11633, 1996.
13. Baksi, K., Alkhatib, H., and Smulson, M. E. In vivo characterization of the poly (ADP-ribosyl)ation of SV40 chromatin and large T antigen by immunofractionation. Exp. Cell Res., 172: 110-123, 1987.
14. Poirier, G. G., de Murcia, G., Jongstra-Bilen, J., Niedergang, C., and Mandel, P. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc. Natl. Acad. Sci. USA, 79: 3423-3427, 1982.
15. Butt, T. R., DeCoste, B., Jump, D., Nolan, N., and Smulson, M. E. Characterization of a putative poly adenosine diphosphate ribose chromatin complex. Biochemistry, 19: 5243-5249, 1980.
16. Ding, R., Pommier, Y., Kang, V. H., and Smulson, M. Depletion of poly(ADP-ribose) polymerase by antisense RNA expression results in a delay in DNA strand break rejoining. J. Biol. Chem., 267: 12804-12812, 1992.
17. Rosenthal, D. S., Shima, T. B., Celli, G., De Luca, L. M., and Smulson, M. E. An engineered human skin model using poly(ADP-ribose) polymerase antisense expression shows a reduced response to DNA damage. J. Invest. Dermatol., 105: 38-44, 1995.
18. Stevnsner, T., Ding, R., Smulson, M., and Bohr, V. A. Inhibition of gene-specific repair of alkylation damage in cells depleted of poly(ADP-ribose) polymerase. Nucleic Acids Res., 22: 4620-4624, 1994.
19. Ding, R., and Smulson, M. Depletion of nuclear poly(ADP-ribose) polymerase by antisense RNA expression: influences on genomic stability, chromatin organization and carcinogen cytotoxicity. Cancer Res., 54: 4627-4634, 1994.
20. Smulson, M. E., Kang, V. H., Ntambi, J. M., Rosenthal, D. S., Ding, R., and Simbulan, C. M. G. Requirement for the expression of poly(ADP-ribose) polymerase during the early stages of differentiation of 3T3-L1 preadipocytes, as studied by antisense RNA induction. J. Biol. Chem., 270: 119-127, 1995.
21. Simbulan-Rosenthal, C. M., Rosenthal, D. S., Iyer, S., Boulares, A. H., and Smulson, M. E. Transient poly(ADP-ribosyl)ation of nuclear proteins and role for poly(ADP-ribose) polymerase in the early stages of apoptosis. J. Biol. Chem., 273: 13703-13712, 1998.
22. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., and Poirier, G. G. Specific proteolytic cleavage of poly(ADP-ribose)polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res., 53: 3976-3985, 1993.
23. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., Munday, N. A., Raju, S. M., Smulson, M. E., Yamin, T. T., Yu, V. L., and Miller, D. K. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (Lond.), 376: 37-43, 1995.
24. Rosenthal, D. S., Ding, R., Simbulan-Rosenthal, C. M. G., Vaillancourt, J. P., Nicholson, D. W., and Smulson, M. E. Intact cell evidence for the early synthesis, and subsequent late apopain-mediated suppression, of poly(ADP-ribose) during apoptosis. Exp. Cell Res., 232: 313-321, 1997.
25. Whitacre, C. M., Hashimoto, H., Tsai, M-L., Chatterjee, S., Berger, S. J., and Berger, N. A. Involvement of NAD-poly(ADP-ribose) metabolism in p53 regulation and its consequences. Cancer Res., 55: 3697-3701, 1995.
26. Tewari, M., Quan, L. T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S., and Dixit, V. M Yama/CPP32b, a mammalian homolog of CED-3, is a crmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell, 81: 801-809, 1995.
27. Fisher, D. Apoptosis in cancer therapy: crossing the threshold. Cell, 78: 539-542, 1994.
28. Yonish-Rouach, E., Resnitzky, D., Lotem, J., Sachs, L., Kimchi, A., and Oren, M. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature (Lond.), 352: 345-347, 1991.
29. Wesierska-Gadek, J., Schmid, G., and Cerni, C. ADP-ribosylation of wild-type p53 in vitro: binding of p53 protein to specific p53 consensus sequence prevents its modification. Biochem. Biophys. Res. Commun., 224: 96-102, 1996.
30. Kawamitsu, H., Hoshino, H., Okada, H., Miwa, M., Momoi, H., and Sugimura, T. Monoclonal antibodies to poly(adenosine diphosphate ribose) recognize different structures. Biochemistry, 23: 3771-3777, 1984.
31. Simbulan, C., Suzuki, M., Izuta, S., Sakurai, T., Savoysky, E., Kojima, K., Miyahara, K., Shizuta, Y., and Yoshida, S. Poly(ADP-ribose) polymerase stimulates DNA polymerase α. J. Biol. Chem., 268: 93-99, 1993.
32. Alkhatib, H. M., Chen, D. F., Cherney, B., Bhatia, K., Notario, V., Giri, C., Stein, G., Slattery, E., Roeder, R. G., and Smulson, M. E. Cloning and expression of cDNA for human poly(ADP-ribose) polymerase. Proc. Natl. Acad. Sci. USA, 84: 1224-1228, 1987.
33. Eldadah, B., Yakovlev, A., and Faden, A. A new approach for the electrophoretic detection of apoptosis. Nucleic Acids Res., 24: 4092-4093, 1996.
34. Simbulan-Rosenthal, C. M., Rosenthal, D. S., Iyer, S., Boulares, H., and Smulson, M. E. Involvement of PARP and poly(ADP-ribosyl)ation in the early stages of apoptosis and DNA replication. Mol. Cell. Biochem., in press, 1999.
35. Lowe, S. W., Ruley, H. E., Jacks, T., and Housman, D. E. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell, 74: 957-967, 1993.
36. Alnemri, E., Livingston, D., Nicholson, D., Salvesen, G., Thomberry, N., Wong, W., and Yuan, J. Human ICE/CED-3 protease nomenclature. Cell, 87: 171, 1996.
37. Adamietz, P. Poly(ADP-ribose) synthase is the major endogenous nonhistone acceptor for poly(ADP-ribose) in alkylated rat hepatoma cells. Eur. J. Biochem., 169: 365-372, 1987.
38. Wong, M., Miwa, M., Sugimura, T., and Smulson, M. Relationship between histone H1 poly(adenosine diphosphate ribosylation) and histone H1 phosphorylation using anti-poly(adenosine diphosphate ribose) antibody. Biochemistry, 22: 2384-2389, 1983.
39. Yoshihara, K., Itaya, A., Tanaka, Y., Ohashi, Y., Ito, K., Teraoka, H., Tsukada, K., Matsukage, A., and Kamiya, T. Inhibition of DNA polymerase α, DNA polymerase β, terminal nucleotidyltransferase and DNA ligase II by poly (ADP-ribosyl)ation reaction in vitro. Biochem. Biophys. Res. Commun., 128: 61-67, 1985.
40. Simbulan-Rosenthal, C. M., Rosenthal, D. S., Boulares, A. H., Mickey, R. J., Malkas, L. H., Coll, J. M., and Smulson, M. E. Regulation of the expression or recruitment of components of the DNA synthesome by poly( ADP-ribose) polymerase. Biochemistry, 37: 9363-9370, 1998.
41. Ferro, A. M., and Olivera, B. M. Poly (ADP-ribosylation) of DNA topoisomerase I from calf thymus. J. Biol. Chem., 259: 547-554, 1984.
42. Darby, M. K., Schmitt, B., Jongstra, B. J., and Vosberg, H. P. Inhibition of calf thymus type Il DNA topoisomerase by poly(ADP-ribosylation). EMBO J., 4: 2129-2134, 1985.
43. Chinnaiyan, A., Orth, K., O'Rourke, K., Duan, H., Poirier, G., and Dixit, V. Molecular ordering of the cell death palhway. Bcl-2 and Bcl-xL function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem., 271: 4573-4576, 1996.
44. Muller, M., Wilder, S., Bannasch, D., Israeli, D., Lelbach, K., Li-Weber, M., Friedman, S., Galle, P., Stremmel, W., Oren, M., and Krammer, P. p53 activates the CD9S (APO-1/Fas) gene in response to DNA damage by anticancer agents. J. Exp. Med., 188: 2033-2045, 1998.
45. Berger, N. A., and Petzold, S. J. Identification of the requirements of DNA for activation of poly (ADP-ribose) polymerase. Biochemistry, 24: 4352-4355, 1985.
46. Fritsche, M., Haessler, C., and Brandner, G. Induction of nuclear accumulation of the tumor suppressor protein by p53 by DNA damaging agents. Oncogene, 8: 307-318, 1993.
47. 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.
48. Vaziri, H., West, M., Allsop, R., Davison, T., Wu, Y., Arrowsmith, C., Poirier, G., and Benchimol, S. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the postranslational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J., 16: 6018-6033, 1997.
49. Wesierska-Gadek, J., Bugajska-Schretter, A., and Cemi, C. ADP-ribosylation of p53 tumor suppressor protein: mutant but not wild-type p53 is modified. J. Cell. Biochem., 62: 90-101, 1996.
50. Nelson, W. G., and Kaslan, M. B. DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol., 14: 1815-1823, 1994.
51. Agarwal, M., Agarwal, A., Taylor, W., Wang, Z. Q., and Wagner, E. Defective induction but normal activation and function of p53 in mouse cells lacking PARP. Oncogene, 15: 1035-1041, 1997.
52. Neamati, N., Fernandez, A., Wright, S., Kiefer, J., and McConkey, D. J. Degradation of lamin B1 precedes oligonucleosomal DNA fragmentation in apoptotic thymocytes and isolated thymocyte nuclei. J. Immunol., 154: 3788-3795, 1995.
53. Malanga, M., Pleschke, J., Kleczkowska, H., and Althaus, F. Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J. Biol. Chem., 273: 11839-11843, 1998.
54. Li, X., and Coffino, P. Identification of a region of p53 that confers lability. J. Biol. Chem., 271: 4447-4451, 1996.