Antioxidant butylated hydroxyanisole inhibits estrogen-induced breast carcinogenesis in female ACI rats

Journal of Biochemical and Molecular Toxicology

Volumn 23, Issue 3, 2009, Pages 202-211

  Singh, Bhupendra ^a   Mense, Sarah M ^a   Remotti, Fabrizio ^b   Liu, Xinhua ^a   Bhat, Hari K ^a  

^a Columbia University ^*  (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

17 estradiol; ACI rat; Animal model of breast cancer; Antioxidant; Breast cancer; Butylated hydroxyanisole; Estrogen; Oxidative stress

Indexed keywords

8 ISOPROSTANE; BUTYLATED HYDROXYANISOLE; CATALASE; CHOLESTEROL; ESTRADIOL; GLUTATHIONE PEROXIDASE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BREAST ADENOCARCINOMA; BREAST CANCER; BREAST CARCINOGENESIS; CONTROLLED STUDY; DRUG INHIBITION; ENZYME ACTIVITY; FEMALE; HISTOPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; RAT;

ANIMALS; ANTIOXIDANTS; BREAST NEOPLASMS; BUTYLATED HYDROXYANISOLE; DINOPROST; ESTRADIOL; ESTROGENS; FEMALE; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; OXIDATIVE STRESS; RATS; RATS, INBRED ACI;

ANIMALIA; RATTUS;

EID: 67649329396     PISSN: 10956670     EISSN: 10990461     Source Type: Journal    
DOI: 10.1002/jbt.20281     Document Type: Article

References (60)

1. Galati G, O'Brien PJ. Potential toxicity of flavonoids and other dietary phenolics: Significance for their chemopreventive and anticancer properties. Free Radic Biol Med 2004;37(3):287-303. (Pubitemid 38833996)
2. Henderson BE, Feigelson HS. Hormonal carcinogenesis. Carcinogenesis 2000;21(3):427-433. (Pubitemid 30137927)
3. Ju YH, Allred KF, Allred CD, Helferich WG. Genistein stimulates growth of human breast cancer cells in a novel, postmenopausal animal model, with low plasma estradiol concentrations. Carcinogenesis 2006;27(6):1292-1299. (Pubitemid 43994865)
4. Bhat HK, Calaf G, Hei TK, Loya T, Vadgama JV. Critical role of oxidative stress in estrogen-induced carcinogenesis. Proc Natl Acad Sci USA 2003;100(7):3913-3918. (Pubitemid 36418131)
5. Cavalieri E, Chakravarti D, Guttenplan J, Hart E, Ingle J, Jankowiak R, Muti P, Rogan E, Russo J, Santen R, et al. Catechol estrogen quinones as initiators of breast and other human cancers: Implications for biomarkers of susceptibility and cancer prevention. Biochim Biophys Acta 2006;1766(1):63-78. (Pubitemid 44175632)
6. International Agency for Research on Cancer (IARC). Monographs on the evaluation of carcinogenic risks to humans: Overall evaluations of carcinogenicity, an updating of IARC monographs volumes 1 to 42. Supplement 7. Lyon, France: International Agency for Research on Cancer; 1987.
7. International Agency for Research on Cancer (IARC). Monographs on the evaluation of carcinogenic risks to humans: Hormonal contraception and postmenopausal hormone therapy, 72. Lyon, France: International Agency for Research on Cancer; 1999. pp. 474-530.
8. NTP. Report on Carcinogens. National Toxicology Program, Research Triangle Park, NC; 2002.
9. Key T, Appleby P, Barnes I, Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: Reanalysis of nine prospective studies. J Natl Cancer Inst 2002;94(8):606-616. (Pubitemid 34498648)
10. McPherson K, Steel CM, Dixon JM. ABC of breast diseases. Breast cancer-epidemiology, risk factors, and genetics. BMJ 2000;321(7261):624-628.
11. Clemons M, Goss P. Estrogen and the risk of breast cancer. N Engl J Med 2001;344(4):276-285.
12. 32P-postlabelling in studies of hormonal carcinogenesis. IARC Sci Publ 1993;124:149-155.
13. Patel MM, Bhat HK. Differential oxidant potential of carcinogenic and weakly carcinogenic estrogens: Involvement of metabolic activation and cytochrome P450. J Biochem Mol Toxicol 2004;18(1):37-42. (Pubitemid 38312721)
14. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med 2006;354(3):270-282. (Pubitemid 43113032)
15. Cavalieri EL, Rogan EG.Aunifyingmechanism in the initiation of cancer and other diseases by catechol quinones. Ann NY Acad Sci 2004;1028:247-257. (Pubitemid 40361826)
16. Cavalieri EL, Stack DE, Devanesan PD, Todorovic R, Dwivedy I, Higginbotham S, Johansson SL, Patil KD, Gross ML, Gooden JK, et al. Molecular origin of cancer: Catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc Natl Acad Sci USA 1997;94(20):10937-10942. (Pubitemid 27430839)
17. Cao K, Stack DE, Ramanathan R, Gross ML, Rogan EG, Cavalieri EL. Synthesis and structure elucidation of estrogen quinones conjugated with cysteine, N-acetylcysteine, and glutathione. Chem Res Toxicol 1998;11(8):909-916.
18. Singh KP, Roy D. Somatic mutations in stilbene estrogen-induced Syrian hamster kidney tumors identified by DNA fingerprinting. J Carcinog 2004;3(1):4. (Pubitemid 38751388)
19. Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D. Estrogens as endogenous genotoxic agents - DNA adducts and mutations. J Natl Cancer Inst Monogr 2000;2000(27):75-93.
20. Liehr JG, Fang WF, Sirbasku DA, Ari-Ulubelen A. Carcinogenicity of catechol estrogens in Syrian hamsters. J Steroid Biochem 1986;24(1):353-356.
21. Roy D, Liehr JG. Estrogen, DNA damage and mutations. Mutat Res 1999;424(1-2):107-115.
22. 0-arrested estrogen-dependent breast cancer cells is regulated by mitochondrial oxidant signaling. Oncogene 2005;24(31):4883-4893.
23. Felty Q, Xiong WC, Sun D, Sarkar S, Singh KP, Parkash J, Roy D. Estrogen-induced mitochondrial reactive oxygen species as signal-transducing messengers. Biochemistry 2005;44(18):6900-6909. (Pubitemid 40632408)
24. Roy D, Cai Q, Felty Q, Narayan S. Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers. J Toxicol Environ Health B: Crit Rev 2007;10(4):235-257. (Pubitemid 47057178)
25. Liehr JG, Avitts TA, Randerath E, Randerath K. Estrogen-induced endogenous DNA adduction: Possible mechanism of hormonal cancer. Proc Natl Acad Sci USA 1986;83(14):5301-5305. (Pubitemid 16051363)
26. Yager JD. Endogenous estrogens as carcinogens through metabolic activation. J Natl Cancer Inst Monogr 2000;2000(27):67-73.
27. Turan VK, Sanchez RI, Li JJ, Li SA, Reuhl KR, Thomas PE, Conney AH, Gallo MA, Kauffman FC, Mesia-Vela S. The effects of steroidal estrogens in ACI rat mammary carcinogenesis: 17β-estradiol, 2-hydroxyestradiol, 4-hydroxyestradiol, 16α-hydroxyestradiol, and 4-hydroxyestrone. J Endocrinol 2004;183(1):91-99. (Pubitemid 40124646)
28. Arnerlov C, Emdin SO, Cajander S, Bengtsson NO, Tavelin B, Roos G. Intratumoral variations in DNA ploidy and s-phase fraction in human breast cancer. Anal Cell Pathol 2001;23(1):21-28. (Pubitemid 34014657)
29. Li JJ, Papa D, Davis MF, Weroha SJ, Aldaz CM, El-Bayoumy K, Ballenger J, Tawfik O, Li SA. Ploidy differences between hormone- and chemical carcinogen-induced rat mammary neoplasms: Comparison to invasive human ductal breast cancer. Mol Carcinog 2002;33(1):56-65. (Pubitemid 34052307)
30. Li JJ, Weroha SJ, Lingle WL, Papa D, Salisbury JL, Li SA. Estrogen mediates aurora-A overexpression, centrosome amplification, chromosomal instability, and breast cancer in female ACI rats. Proc Natl Acad Sci USA 2004;101(52):18123-18128. (Pubitemid 40054084)
31. Li SA, Weroha SJ, Tawfik O, Li JJ. Prevention of solely estrogen-induced mammary tumors in female ACI rats by tamoxifen: Evidence for estrogen receptor mediation. J Endocrinol 2002;175(2):297-305. (Pubitemid 35422606)
32. Makris A, Allred DC, Powles TJ, Dowsett M, Fernando IN, Trott PA, Ashley SE, Ormerod MG, Titley JC, Osborne CK. Cytological evaluation of biological prognostic markers from primary breast carcinomas. Breast Cancer Res Treat 1997;44(1):65-74. (Pubitemid 27179770)
33. Shull JD, Spady TJ, Snyder MC, Johansson SL, Pennington KL. Ovary-intact, but not ovariectomized female ACI rats treated with 17β-estradiol rapidly develop mammary carcinoma. Carcinogenesis 1997;18(8):1595-1601. (Pubitemid 28134784)
34. Weroha SJ, Li SA, Tawfik O, Li JJ. Overexpression of cyclins D1 and D3 during estrogen-induced breast oncogenesis in female ACI rats. Carcinogenesis 2006;27(3):491-498. (Pubitemid 43372878)
35. Han X, Liehr JG. DNA single-strand breaks in kidneys of Syrian hamsters treated with steroidal estrogens: Hormone-induced free radical damage preceding renal malignancy. Carcinogenesis 1994;15(5):997-1000. (Pubitemid 24156901)
36. Wang MY, Liehr JG. Induction by estrogens of lipid peroxidation and lipid peroxide-derived malonaldehyde-DNA adducts in male Syrian hamsters: Role of lipid peroxidation in estrogen-induced kidney carcinogenesis. Carcinogenesis 1995;16(8):1941-1945.
37. Mense SM, Remotti F, Bhan A, Singh B, El-Tamer M, Hei TK, Bhat HK. Estrogen-induced breast cancer: Alterations in breast morphology and oxidative stress as a function of estrogen exposure. Toxicol Appl Pharmacol 2008;232(1):78-85.
38. Milne GL, Yin H, Brooks JD, Sanchez S, Jackson Roberts L, II, Morrow JD. Quantification of F2-isoprostanes in biological fluids and tissues as a measure of oxidant stress. Methods Enzymol 2007;433:113-126.
39. Montuschi P, Barnes PJ, Roberts LJ, II. Isoprostanes: Markers and mediators of oxidative stress. FASEB J 2004;18(15):1791-1800.
40. Morrow JD, Hill KE, Burk RF, Nammour TM, Badr KF, Roberts LJ, II. A series of prostaglandin F2-like compounds are produced in vivo in humans by a noncyclooxygenase, free radical-catalyzed mechanism. Proc Natl Acad Sci USA 1990;87(23):9383-9387.
41. Pratico D, Lawson JA, FitzGerald GA. Cyclooxygenase-dependent formation of the isoprostane, 8-epi prostaglandin F2 alpha. J Biol Chem 1995;270(17):9800-9808.
42. Henderson BE, Ross RK, Pike MC, Casagrande JT. Endogenous hormones as a major factor in human cancer. Cancer Res 1982;42(8):3232-3239. (Pubitemid 12041084)
43. Lupulescu A. Estrogen use and cancer incidence: A review. Cancer Invest 1995;13(3):287-295.
44. Cavalieri E, Rogan E. Catechol quinones of estrogens in the initiation of breast, prostate, and other human cancers: Keynote lecture. Ann NY Acad Sci 2006;1089:286-301. (Pubitemid 47092096)
45. Cavalieri EL, Rogan EG, Chakravarti D. Initiation of cancer and other diseases by catechol ortho-quinones: A unifying mechanism. Cell Mol Life Sci 2002;59(4):665-681. (Pubitemid 34460682)
46. Jefcoate CR, Liehr JG, Santen RJ, Sutter TR, Yager JD, Yue W, Santner SJ, Tekmal R, Demers L, Pauley R, et al. Tissue-specific synthesis and oxidative metabolism of estrogens. J Natl Cancer Inst Monogr 2000: 2000(27):95-112.
47. Liehr JG. Is estradiol a genotoxic mutagenic carcinogen? Endocr Rev 2000;21(1):40-54.
48. Liehr JG, Roy D. Free radical generation by redox cycling of estrogens. Free Radic Biol Med 1990;8(4):415-423. (Pubitemid 20186989)
49. Liehr JG HX, Bhat HK. In: Phillips DH, Castegnaro M, Bartsch H, editors. Postlabelling methods for detection of DNA adducts; Lyon, France: IARC Scientific Publications; 1993. pp 149-155.
50. Weisz J, Bui QD, Roy D, Liehr JG. Elevated 4-hydroxylation of estradiol by hamster kidney microsomes: A potential pathway of metabolic activation of estrogens. Endocrinology 1992;131(2):655-661.
51. McCormick DL, Major N, Moon RC. Inhibition of 7,12-dimethylbenz(a) anthracene-induced rat mammary carcinogenesis by concomitant or postcarcinogen antioxidant exposure. Cancer Res 1984;44(7):2858-2863. (Pubitemid 14083249)
52. Cha YN, Heine HS. Comparative effects of dietary administration of 2(3)-tert-butyl-4-hydroxyanisole and 3,5-di-tert-butyl-4-hydroxytoluene on several hepatic enzyme activities in mice and rats. Cancer Res 1982;42(7):2609-2615.
53. Iverson F. In vivo studies on butylated hydroxyanisole. Food Chem Toxicol 1999;37(9-10):993-997.
54. Lam LK, Wattenberg LW. Effects of butylated hydroxyanisole on the metabolism of benzo[a]pyrene by mouse liver microsomes. J Natl Cancer Inst 1977;58(2):413-417. (Pubitemid 8042535)
55. Sydor W, Jr, Chou MW, Yang SK, Yang CS. Regioselective inhibition of benzo[a]pyrene metabolism by butylated hydroxyanisole. Carcinogenesis 1983;4(2):131-136.
56. Dock L, Cha YN, Jernstrom B, Moldeus P. Differential effects of dietary BHA on hepatic enzyme activities and benzo[a]pyrene metabolism in male and female NMRI mice. Carcinogenesis 1982;3(1):15-19.
57. Marnett LJ, Reed GA, Johnson JT. Prostaglandin synthetase dependent benzo(a)pyrene oxidation: Products of the oxidation and inhibition of their formation by antioxidants. Biochem Biophys Res Commun 1977;79(2):569-576. (Pubitemid 8239150)
58. Roy D, Liehr JG. Inhibition of estrogen-induced kidney carcinogenesis in Syrian hamsters by modulators of estrogen metabolism. Carcinogenesis 1990;11(4):567-570. (Pubitemid 20137404)
59. Cadet J, Delatour T, Douki T, Gasparutto D, Pouget JP, Ravanat JL, Sauvaigo S. Hydroxyl radicals and DNA base damage. Mutat Res 1999;424(1-2):9-21. (Pubitemid 29101604)
60. Wang Y. Bulky DNA lesions induced by reactive oxygen species. Chem Res Toxicol 2008;21(2):276-281.