Induction of p53 by the concerted actions of aziridine and quinone moieties of diaziquone

Chemical Research in Toxicology

Volumn 11, Issue 4, 1998, Pages 360-368

  Ngo, Emily O ^a,c   Nutter, Louise M ^a   Sura, Tushar ^b   Gutierrez, Peter L ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 BENZOQUINONE; ANTINEOPLASTIC AGENT; AZIRIDINE; DIAZIQUONE; DIAZIQUONE DERIVATIVE; MENADIONE; PROTEIN P53; REACTIVE OXYGEN METABOLITE; THIOTEPA;

APOPTOSIS; ARTICLE; BREAST ADENOCARCINOMA; CANCER CELL; CELL STRAIN MCF 7; DNA DAMAGE; GENOTOXICITY; HUMAN; HUMAN CELL; OXIDATION REDUCTION REACTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

ADENOCARCINOMA; ANTINEOPLASTIC AGENTS; AZIRIDINES; BENZOQUINONES; BREAST NEOPLASMS; HUMANS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0031901502     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx9701945     Document Type: Article

References (74)

1. Hollstein, M., Sidransky, D., Vogelstein, B., and Harris, C. C. (1991) p53 mutations in human cancers. Science 253, 49-53.
2. Davidoff, A. M., Humprey, P. A., Iglehart, J. D., and Marks, J. R. (1991) Genetic basis for p53 overexpression in human breast cancer. Proc. Natl. Acad. Sci. U.S.A. 88, 5006-5010.
3. Newcomb, E. W. (1995) p53 gene mutations in lymphoid diseases and their possible relevance to drug resistance. Leukemia Lymphoma 17, 211-221.
4. Pietenpol, J. A., Tokino, T., Thiagalingam, S., El-Deiry, W., Kinzler, K. W., and Vogelstein, B. (1994) Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl. Acad. Sci. U.S.A. 91, 1998-2002.
5. Pietenpol, J. A., and Vogelstein, B. (1993) No room at the p53 inn. Nature 365, 17-18.
6. Hainaut, P. (1995) The tumor suppressor protein p53: a receptor to genotoxic stress that controls cell growth and survival. Curr. Opin. Oncol. 7, 76-82.
7. 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.
8. Pritsche, M., Haessler, C., and Brandner, G. (1993) Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene 8, 307-318.
9. Tishler, R. B., Calderwood, S. K., Coleman, C. N., and Price, B. D. (1993) Increases in sequence specific DNA binding by p53 following treatment with chemotherapeutic and DNA-damaging agents. Cancer Res. 53, 2212-2216.
10. Kuerbirtz, S. J., Plunkett, B. S., Walsh, W. V., and Kastan, M. B. (1992) Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl. Acad. Sci. U.S.A. 89, 7491-7495.
11. Yang, C., Cirielli, C., Capogrossi, M. C., and Passaniti, A. (1995) Adenovirus-mediated wild-type p53 expression induces apoptosis and suppresses tumorigenesis of prostatic tumor cells. Cancer Res. 55, 4210-4213.
12. Mohammad, R. M., Duvakaran, H., Maki, A., Emara, M. A., Pettit, G. R., Redman, B., and al-Katib, A. (1995) Bryostatin 1 induces apoptosis and augments inhibitory effects of vincristine in human diffuse large cell lymphoma. Leukemia Res. 19, 667-673.
13. Perego, P., Giaroia, M., Righetti, S. C., Supino, R., Caserini, C., Delia, D., Pierotti, M. A., Miyashita, T., Reed, J. C., and Zunino, F. (1996) Association between cisplatin resistance and mutation of p53 gene and reduced bax expression in ovarian carcinoma cell systems. Cancer Res. 56, 556-562.
14. Canman, C. E., and Kastan, M. B. (1995) Induction of apoptosis by tumor suppressor genes and oncogenes. Sem. Cancer Biol. 6, 17-25.
15. Miyashita, T., and Reed, J. C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299.
16. Planchon, S. M., Wuerzberger, S., Frydman, B., Witiak, D. T., Hutson, P., Church, D. R., Wilding, G., and Boothman, D. A. (1995) Beta-lapachone-mediated apoptosis in human promyelocytic leukemia (HL-60) and human prostate cancer cells: a p53- independent response. Cancer Res. 55, 3706-3711.
17. Li, C. J., Wang, C., and Pardee, A. B. (1995) Induction of apoptosis by Beta-lapachone in human prostate cancer cells. Cancer Res. 55, 3712-3715.
18. Gartenhaus, R. B., Wang, P., and Hoffman, P. (1996) Induction of the WAF1/CIP1 protein and apoptosis in human T-leukemia virus type 1-transformed lymphocytes after treatment with adriamycin by using a p53-independent pathway. Proc. Natl. Acad. Sci. U.S.A. 93, 265-268.
19. Seki, H., Kanegane, H., Iwai, K., Konno, A., Ohta, K., Yachie, A., Taniguchi, N., and Miyawaki, T. (1994) Ionizing radiation induces apoptotic cell death in human TcR-gamma/delta+ T and natural killer cells without detectable p53 protein. Eur. J. Immunol. 24, 2914-2917.
20. Merlo, G. R., Basolo, F., Fiore, L., Duboc, L., and Hynes, N. E. (1995) p53-dependent and p53-independent activation of apoptosis in mammary epithelial cells reveals a survival function of EGF and insulin. J. Cell Biol. 128, 1185-1196.
21. Xu, R., Meikrantz, W., Schlegel, R., and Sager, R. (1995) The human papilloma virus 16E6 gene sensitizes human mammary epithelial cells to apoptosis induced by DNA damage. Proc. Natl. Acad. Sci. U.S.A. 92, 7829-7833.
22. Selter, H., and Montenarh, M. (1994) The emerging picture of p53. Int. J. Biochem. 26, 145-154.
23. Hassan, H. M., and Fridovich, I. (1979) Intracellular production of Superoxide radical and of hydrogen peroxide by redox active compounds. Arch. Biochem. Biophys. 196, 385-395.
24. Lin, A. J., Cosby, L. A., Shansky, C. W., and Sartorelli, A. C. (1972) Potential bioreductive alkylating agents. 1. Benzoquinone derivatives. J. Med. Chem. 15, 1247-1252.
25. Kohn, K. W. (1981) Molecular mechanisms of DNA cross-linking by alkylating agents and platinum complexes. In Molecular Actions and Targets for Cancer Chemotherapeutic Agents (Sartorelli, A. C., Ed.) pp 3-115, Academic Press, New York.
26. Sato, S., Iwaizumi, M., Handa, K., and Tamura, Y. (1977) Electron spin resonance study on the mode of generation of free radicals of daunomycin, adriamycin and carboquone in NAD(P)H-microsome system. GANN 68, 603-608.
27. Bachur, N. R., Gordon, S. L., Gee, M. V., and Konh, H. (1979) NADPH cytochrome P-450 reductase activation of quinone anticancer agents to free radicals. Proc. Natl. Acad. Sci. U.S.A., 76, 954-957.
28. Gutierrez, P. L., Gee, M. V., and Bachur, N. R. (1983) Kinetics of anthracycline antibiotic free radical formation and reductive glycoside activity. Arch. Biochem. Biophys. 223, 68-75.
29. Hildenbrand, K., and Schulte-Frohlinde, D. (1989) ESR studies on the mechanism of ·OH-induced strand breakage of poly U. Free Radical Res. Commun. 6, 137-138.
30. Brunmark, A., and Cadenas, E. (1989) Redox and addition chemistry of quinoid compounds and its biological implications. Free Radical Biol. Med. 7, 435-477.
31. Tannock, I. F. (1987) Biological properties of anticancer drugs. In The Basic Science of Oncology (Tannock, I. F., and Hill, R. P., Eds.) pp 278-291, Pergamon Press, New York.
32. Swallow, A. J. (1960) In Radiation Chemistry of Organic Compounds (Swallow, A. J., Ed.) pp 211-224, Pergamon Press, New York.
33. Gutierrez, P. L., Biswal, S., Nardino, R., and Biswal, N. (1986) Reductive activation of diaziquone and possible involvement of free radicals and the hydroquinone dianion. Cancer Res. 46, 5779-5785.
34. Gutierrez, P. L., Egorin, M. J., Fox, B. M., Friedman, R., and Bachur, N. R. (1985) Cellular activation of diaziquone [2,5- diaziridinyl-3,6-bis(carboethoxyamino)-1,4-benzoquinone] to its free radical species. Biochem. Pharmacol. 34, 1449-1455.
35. Nguyen, B., Biswal, S., and Gutierrez, P. L. (1988) The influence of diaziquone free radicals on the in vitro activity of diaziquone. Xenobiotica 18, 593-602.
36. Gutierrez, P. L., Freidman, R. D., and Bachur, N. R. (1982) Biochemical activation of AZQ[3,6-diaziridinyl-2,5-bis(carboethoxyamino)-1,4-benzoquinone] to its free radical species. Cancer Treat. Rep. 66, 339-342.
37. Gutierrez, P. L. (1989) Mechanisms of bioreductive activation. The example of diaziquone (AZQ). Free Radical Biol. Med. 6, 405- 445.
38. Butler, J., Hoey, B. M., and Lea, J. S. (1987) The reduction of antitumor diaziridinyl benzoquinones. Biochim. Biophys. Acta 925, 144-149.
39. Powis, G. (1987) Metabolism and reactions of quinoid anticancer agents. Pharm. Ther. 35, 57-162.
40. Mossoba, M. M., Alizadeh, M., and Gutierrez, P. L. (1985) Mechanism for the reductive activation of diaziquone. J. Pharm. Sci. 74, 1249-1254.
41. Ross, D., Beall, H., Traver, R. D., Siegel, D., Phillips, R. M., and Gibson, N. W. (1994) Bioactivation of quinones by DT-diaphorase, molecular, biochemical and chemical studies. Oncol. Res. 6, 493- 500.
42. Siegel, D., Gibson, N. W., Preusch, P. C., and Ross, D. (1990) Metabolism of diaziquone by NAD(P)H:(quinone acceptor) oxidoreductase (DT-diaphorase): Role of diaziquone-induced DNA damage and cytotoxicity in human colon carcinoma cells. Cancer Res. 50, 7293-7300.
43. Fisher, G. R., and Gutierrez, P. L. (1991) The reductive metabolism of diaziquone (AZQ) in the S9 fraction of MCF-7 cells: Free radical formation and NAD(P)H:quinone-acceptor oxidoreductase (DT diaphorase) activity. Free Radical Biol. Med. 10, 359-370.
44. Fisher, G. R., Donis, J., and Gutierrez, P. L. (1992) Reductive metabolism of diaziquone (AZQ) in the S9 fraction of MCF-7cells. II. Enhancement of the alkylating activity of AZQ by NAD(P)H: quinone-acceptor oxidoreductase (DT diaphorase). Biochem. Pharmacol. 44, 1625-1635.
45. De Mol, N. J., Lusthof, K. J., and Decuyper, J. (1988) DNA modifications by potential antitumor bisaziridinylquinones. Biochem. Pharmacol. 37, 1837-1838.
46. Szmigiero, L., Erickson, L. C., Ewig, R. A., and Kohn, K. W. (1984) DNA strand scission and cross-linking by diaziridinyl benzoquinone (Diaziquone) in human cells and relation to cell killing. Cancer Res. 44, 4447-4452.
47. King, C. L., Hittleman, W. N., and Loo, T. L. (1984) Induction of DNA strand breaks and cross-links by 2,5-diaziridinyl-2,5-bis(carboethoxyamino)-1,4-benzoquinone in Chinese hamster ovary cells. Cancer Res. 44, 5634-5637.
48. Berardini, M. D., Souhami, R. L., Lee, C.-S., Gibson, N. W., Butler, J., and Hartley, J. A. (1993) Two structurally related diaziridinylbenzoquinones preferentially cross-link DNA at different sites upon reduction with DT-diaphorase. Biochemistry 32, 3306-3312.
49. Gibson, N. W., Hartley, J. A., Butler, J., Siegel, D., and Ross, D. (1992) Relationship between DT-diaphorase-mediated metabolism of a series of aziridinylbenzoquinones and DNA damage and cytotoxicity. Mol. Pharmacol. 42, 531-536.
50. Lee, C.-S., Hartley, J. A., Berardini, M. D., Butler, J., Siegel, D., Ross, D., and Gibson, N. W. (1992) Alteration in DNA cross- linking and sequence selectivity of a series of aziridinylbenzoquinones after enzymatic reduction by DT-diaphorase. Biochemistry 31, 3019-3025.
51. Petersen, S., Gauss, W., and Urbschat, E. (1955) Synthese einfacher Chinon-Derivative mit fungiziden, bakteriostatischen oder cytostatischen Eigenschaften. Angew. Chem. 8, 217-240.
52. Funk, W. D., Pak, D. T., Karas, R. H., Wright, W. E., and Shay, J. W. (1992) A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 12, 2866-2871.
53. Price, B. D., and Calderwood, S. K. (1993) Increased sequence- specific p53-DNA binding activity after DNA damage is attenuated by phorbol esters. Oncogens 8, 3055-3062.
54. dePierre, J., and Dallner, G. (1976) Isolation, subfractionation and characterization of the endoplasmic reticulum. In Biochemical Analysis of Membranes (Maddy, A. H., Ed.) pp 79-131, Wiley, New York.
55. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram qualities of protein utilizing the principal of protein-dye binding. Anal. Biochem. 72, 248-254.
56. Jiang, Z. Y., Wollard, A. C. S., and Wolff, S. P. (1990) Hydrogen peroxide production during experimental protein glycation. FEBS Lett. 268, 69-71.
57. Subramanian, T., Tarodi, B., and Chinnadurai, G. (1995) p53- independent apoptotic and necrotic cell deaths induced by adenovirus infection: suppression by E1B 19k and Bcl-2 proteins. Cell Growth Diff. 6, 131-137.
58. Runnebaum, I. B., Nagarajan, M., Bowman, M., Soto, D., and Sukumar, S. (1991) Mutations in p53 as potential molecular markers for human breast cancer. Proc. Natl. Acad. Sci. U.S.A. 88, 10657-10661.
59. Fan, S., Smith, M. L., Rivet, D. J., 2nd, Duba, D., Zhan, Q., Kohn, K. W., Fornace, A. J., Jr., 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.
60. Yewdell, J. W., Gannon, J. V., and Lane, D. P. (1986) Monoclonal antibody analysis of p53 expression in normal and transformed cells. J. Virol. 59, 444-452.
61. Nutter, L. M., Ngo, E. O., Fisher, G. R., and Gutierrez, P. L. (1992) DNA strand scission and free radical production in menadione- treated cells: Correlation with cytotoxicity and role of NAD- (P)H: quinone acceptor oxidoreductase. J. Biol. Chem. 267, 2474- 2479.
62. Henry, T. R., and Wallace, K. B. (1995) Differential mechanisms of induction of the mitochondrial permeability transition by quinones of varying chemical reactivities. Toxicol. Appl. Pharmacol. 134, 195-203.
63. Vojtesek, B., and Lane, D. P. (1993) Regulation of p53 protein expression in human breast cancer cell lines. J. Cell Sci. 105, 607-612.
64. Nelson, W. G., and Kastan, M. B. (1994) DNA strand breaks: The DNA template alterations that triggers p53-dependent DNA damage response pathways. Mot. Cell. Biol., 14, 1815-1823.
65. Wosikowski, K., Regis, J. T., Robey, R. W., Alvarez, M., Buters, J. T. M., Gudas, J. M., and Bates, S. E. (1995) Normal p53 status and function despite the development of drug resistance in human breast cancer cells. Cell Growth Diff. 6, 1395-1403.
66. Zhan, Q., Fan, S., Bae, I., Guillouf, C., Liebermann, D. A., O'Connor, P. M., and Fornace, A. J., Jr. (1994) Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene 9, 3743-3751.
67. Takahashi, K., Sumimoto, H., Suzuki, K., and Ono, T. (1993) Protein synthesis-dependent cytoplasmic translocation of p53 protein after serum stimulation of growth-arrested MCF-7 cells. Mol. Carcinogen. 8, 58-66.
68. Petkau, A., Kelly, K., Chelack, W., and Barefoot, C. (1976) Protective effect of Superoxide dismutase on erythrocytes of X irradiated mice. Biochem. Biophys. Res. Commun. 70, 452-458.
69. Doroshow, J. H. (1986) Role of hydrogen peroxide and hydroxyl radical formation in the killing of Ehrlich tumor cells by anticancer quinones. Proc. Natl. Acad. Sci. U.S.A. 83, 4514-4518.
70. Ngo, E. O., Sun, T. P., Chang, J. Y., Wang, C. C., Chi, K. W., Cheng, A. L., and Nutter, L. M. (1991) Menadione-induced DNA damage in a human tumor cell line. Biochem. Pharmacol. 42, 1961-1968.
71. Egorin, M. E., Fox, B. M., Spiegel, J. F., Gutierrez, P. L., Friedman, R. D., and Bachur, N. R. (1985) Cellular pharmacology in murine and human leukemic cell lines of diaziquone (NSC 182986). Cancer Res. 45, 992-999.
72. 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.
73. 2+- dependent endonuclease activation is an early event in VP-16- induced apoptosis of human breast cancer MCF-7 cells in vitro. Biochim. Biophys. Acta 1266, 135-142.
74. Sreerama, L., and Sladek, N. E. (1994) Identification of a methylcholanthrene-induced aldehyde dehydrogenase in a human breast adenocarcinoma cell line exhibiting xazaphosphorine- specific acquired resistance. Cancer Res. 54, 2176-2185.