Synergistic induction of DNA strand breakage by catechol-estrogen and nitric oxide: Implications for hormonal carcinogenesis

Free Radical Biology and Medicine

Volumn 24, Issue 2, 1998, Pages 341-348

  Yoshie, Yumiko ^a,b   Ohshima, Hiroshi ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b Y Yoshie Is Visiting Scientist I   (Japan)

Author keywords

Breast cancer; Catechol estrogens; Diethylstilbestrol; DNA strand breakage; Nitric oxide; Peroxynitrite; Quinone hydroquinone redox system

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; ASCORBIC ACID; CATECHOL; DIETHYLSTILBESTROL; ESTRADIOL; ESTROGEN; ESTRONE; NITRIC OXIDE;

ARTICLE; BREAST CANCER; CANCER RISK; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG MECHANISM; ESTROGEN METABOLISM; HORMONAL CARCINOGENESIS; HUMAN; HUMAN CELL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

ANTIOXIDANTS; BREAST NEOPLASMS; CARCINOGENS; CATALASE; DNA; DNA DAMAGE; DRUG SYNERGISM; ELECTROPHORESIS, AGAR GEL; ESTROGENS, CATECHOL; FREE RADICAL SCAVENGERS; HUMANS; HYDROXYL RADICAL; NITRIC OXIDE; PLASMIDS; SPECTROPHOTOMETRY, ULTRAVIOLET; SUPEROXIDE DISMUTASE;

LETHRINIDAE;

EID: 0031984349     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(97)00269-4     Document Type: Article

References (41)

1. Pisani P., Parkin D. M., Ferlay J. Estimates of the worldwide mortality from eighteen major cancers in 1985. Implications for prevention and projections of future burden. Int. J. Cancer. 55:1993;891-903.
2. Feigelson H. S., Henderson B. E. Estrogen and breast cancer. Carcinogenesis. 17:1996;2279-2284.
3. Barrett J. C., Tsutsui T. Mechanisms of estrogen-associated carcinogenesis. Huff J., Boyd J., Barrett J. C. Cellular and molecular mechanisms of hormonal carcinogenesis. Environmental influences. Progress in clinical and biological research. 394:1996;105-111 Wiley-Liss, New York.
4. Yager J. D., Liehr J. G. Molecular mechanisms of estrogen carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 36:1996;203-232.
5. Preston Martin S., Pike M. C., Ross R. K., Jones P. A., Henderson B. E. Increased cell division as a cause of human cancer. Cancer Res. 50:1990;7415-7421.
6. Nelson K. G., Sakai Y., Eitzman B., Steed T., McLachlan J. Exposure to diethylstilbestrol during a critical developmental period of the mouse reproductive tract leads to persistent induction of two estrogen-regulated genes. Cell Growth Differ. 5:1994;595-606.
7. Hou X., Li J. J., Chen W., Li S. A. Estrogen-induced proto-oncogene and suppressor gene expression in the hamster kidney: Significance for estrogen carcinogenesis. Cancer Res. 56:1996;2616-2620.
8. Liehr J. G. Genotoxic effects of estrogens. Mutat. Res. 238:1990;269-276.
9. Liehr J. G., Roy D. Free radical generation by redox cycling of estrogens. Free Radic. Biol. Med. 8:1990;415-423.
10. Kalyanaraman B., Felix C. C., Sealy R. C. Semiquinone anion radicals of catechol(amine)s, catechol estrogens, and their metal ion complexes. Environ. Health Perspect. 64:1985;185-198.
11. Nutter L. M., Ngo E. O., Abul Hajj Y. J. Characterization of DNA damage induced by 3,4-estrone-o-quinone in human cells. J. Biol. Chem. 266:1991;16380-16386.
12. Nutter L. M., Wu Y. Y., Ngo E. O., Sierra E. E., Gutierrez P. L., Abul Hajj Y. J. An o-quinone form of estrogen produces free radicals in human breast cancer cells: Correlation with DNA damage. Chem. Res. Toxicol. 7:1994;23-28.
13. Li Y., Trush M. A., Yager J. D. DNA damage caused by reactive oxygen species originating from a copper-dependent oxidation of the 2-hydroxy catechol of estradiol. Carcinogenesis. 15:1994;1421-1427.
14. Roy D., Floyd R. A., Liehr J. G. Elevated 8-hydroxydeoxyguanosine levels in DNA of diethylstilbestrol-treated Syrian hamsters: Covalent DNA damage by free radicals generated by redox cycling of diethylstilbestrol. Cancer Res. 51:1991;3882-3885.
15. Han X., Liehr J. G. Microsome-mediated 8-hydroxylation of guanine bases of DNA by steroid estrogens: Correlation of DNA damage by free radicals with metabolic activation to quinones. Carcinogenesis. 16:1995;2571-2574.
16. Dwivedy I., Devanesan P., Cremonesi P., Rogan E., Cavalieri E. Synthesis and characterization of estrogen 2,3- and 3,4-quinones. Comparison of DNA adducts formed by the quinones vs. horseradish peroxidase-activated catechol estrogens. Chem. Res. Toxicol. 5:1992;828-833.
17. Abul-Haji Y. J., Tabakovic K., Tabakovic I. An estrogen-nucleic acid adduct. Electroreductive intermolecular couplingof 3,4-estrone-o-quinone and adenine. J. Am. Chem. Soc. 117:1995;6144-6145.
18. Stack D. E., Byun J., Gross M. L., Rogan E. G., Cavalieri E. L. Molecular characteristics of catechol estrogen quinones in reactions with deoxyribonucleosides. Chem. Res. Toxicol. 9:1996;851-859.
19. Degen G. H. Role of prostaglandin-H synthase in mediating genotoxic and carcinogenic effects of estrogens. Environ. Health Perspect. 88:1990;217-223.
20. Liehr J. G., DaGue B. B., Ballatore A. M., Henkin J. Diethylstilbestrol (DES) quinone: A reactive intermediate in DES metabolism. Biochem. Pharmacol. 32:1983;3711-3718.
21. Liehr J. G., Ulubelen A. A., Strobel H. W. Cytochrome P-450-mediated redox cycling of estrogens. J. Biol. Chem. 261:1986;16865-16870.
22. Yoshie Y., Ohshima H. Nitric oxide synergistically enhances DNA strand breakage induced by polyhydroxyaromatic compounds, but inhibits that induced by the Fenton-reaction. Arch. Biochem. Biophys. 342:1997;13-21.
23. Tschugguel W., Knogler W., Czerwenka K., Mildner M., Weninger W., Zeillinger R., Huber J. C. Presence of endothelial calcium-dependent nitric oxide synthase in breast apocrine metaplasia. Br. J. Cancer. 74:1996;1423-1426.
24. Rosenfeld C. R., Cox B. E., Roy T., Magness R. Nitric oxide contributes to estrogen-induced vasodilation of the ovine uterine circulation. J. Clin. Invest. 98:1997;2158-2166.
25. Roussyn I., Briviba K., Masumoto H., Sies H. Selenium-containing compounds protect DNA from single-strand breaks caused by peroxynitrite. Arch. Biochem. Biophys. 330:1996;216-218.
26. Epe B., Hegler J. Oxidative DNA damage: Endonuclease fingerprinting. Methods Enzymol. 234:1994;122-131.
27. Epe B., Ballmaier D., Roussyn I., Briviba K., Sies H. DNA damage by peroxynitrite characterized with DNA repair enzymes. Nucleic Acids Res. 24:199;4105-4110.
28. Wang M. Y., Liehr J. G. Identification of fatty acid hydroperoxide cofactors in the cytochrome P450-mediated oxidation of estrogens to quinone metabolites. Role and balance of lipid peroxides during estrogen-induced carcinogenesis. J. Biol. Chem. 269:1994;284-291.
29. Beckman J. S., Chen J., Ischiropoulos H., Crow J. P. Oxidative chemistry of peroxynitrite. Methods Enzymol. 233:1994;229-240.
30. Pryor W. A., Squadrito G. L. The chemistry of peroxynitrite: A product from the reaction of nitric oxide with superoxide. Am. J. Physiol. 268:1995;L699-L722.
31. King P. A., Anderson V. E., Edwards J. O., Gustafson G., Plumb R. C., Suggs J. W. A stable solid that generates hydroxyl radical upon dissolution in aqueous solutions: Reactions with proteins and nucleic acid. J. Am. Chem. Soc. 114:1992;5430-5432.
32. Salgo M. G., Stone K., Squadrito G. L., Battista J. R., Pryor W. A. Peroxynitrite causes DNA nicks in plasmid pBR322. Biochem. Biophys. Res. Commun. 210:1995;1025-1030.
33. Rubio J., Yermilov V., Ohshima H. DNA damage induced by peroxynitrite: Formation of 8-nitroguanine and base propenals. Moncada S., Stamler J., Gross S., Higgs E. A. The biology of nitric oxide, part 5. 1996;34 Portland Press Proceedings, London.
34. Noronha Dutra A. A., Epperlein M. M., Woolf N. Reaction of nitric oxide with hydrogen peroxide to produce potentially cytotoxic singlet oxygen as a model for nitric oxide-mediated killing. FEBS Lett. 321:1993;59-62.
35. Park J. W., Kim H. K. Strand scission in DNA induced by S-nitrosothiol with hydrogen peroxide. Biochem. Biophys. Res. Commun. 200:1994;966-972.
36. Liehr J. G., Ricci M. J. 4-Hydroxylation of estrogens as marker of human mammary tumors. Proc. Natl. Acad. Sci. USA. 93:1996;3294-3296.
37. Liehr J. G., Ricci M. J., Jefcoate C. R., Hannigan E. V., Hokanson J. A., Zhu B. T. 4-Hydroxylation of estradiol by human uterine myometrium and myoma microsomes: Implications for the mechanism of uterine tumorigenesis. Proc. Natl. Acad. Sci. USA. 92:1995;9220-9224.
38. Nathan C., Xie Q. W. Nitric oxide synthases: Roles, tolls, and controls. Cell. 78:1994;915-918.
39. Moncada S., Higgs A. The L-arginine-nitric oxide pathway. N. Engl. J. Med. 329:1993;2002-2012.
40. Thomsen L. L., Miles D. W., Happerfield L., Bobrow L. G., Knowles R. G., Moncada S. Nitric oxide synthase activity in human breast cancer. Br. J. Cancer. 72:1995;41-44.
41. Zeillinger R., Tantscher E., Schneeberger C., Tschugguel W., Eder S., Sliutz G., Huber J. C. Simultaneous expression of nitric oxide synthase and estrogen receptor in human breast cancer cell lines. Breast Cancer Res. Treat. 40:1996;205-207.