Pharmacological modulation of genome and proteome alterations in mice treated with the endocrine disruptor bisphenol A

Current Cancer Drug Targets

Volumn 10, Issue 2, 2010, Pages 147-154

  Izzotti, A ^a   Longobardi, M ^a   Cartiglia, C ^a   D'Agostini, F ^a   Kanitz, S ^a   De Flora, S ^a  

^a UNIVERSITY OF GENOA   (Italy)

Author keywords

Bisphenol A; Budesonide; DNA adducts; Liver; Mammary tissue; Mice; Phenethyl isothiocyanate; Proteome

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BUDESONIDE; CELL PROTEIN; DRINKING WATER; ESTROGEN RECEPTOR BETA; PHENETHYL ISOTHIOCYANATE; PHOSPHORUS 32; PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST CELL; CANCER PREVENTION; CHEMOPROPHYLAXIS; CLUSTER ANALYSIS; CONTROLLED STUDY; DNA ADDUCT; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG POTENCY; FEMALE; GENOME ANALYSIS; ISOTOPE LABELING; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PROTEIN DETERMINATION; UPREGULATION;

ANIMALS; ANTICARCINOGENIC AGENTS; DNA ADDUCTS; ENDOCRINE DISRUPTORS; ESTROGENS, NON-STEROIDAL; FEMALE; GENOME; ISOTHIOCYANATES; LIVER; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED ICR; PHENOLS; PROTEIN ARRAY ANALYSIS; PROTEOME;

EID: 77950686943     PISSN: 15680096     EISSN: None     Source Type: Journal    
DOI: 10.2174/156800910791054220     Document Type: Article

References (56)

1. De Flora, S.; Ferguson, L. R. Overview of mechanisms of cancer chemopreventive agents. Mutat. Res. 2005, 591, 8-15.
2. De Flora, S.; Bennicelli, C.; Battistella, A; Bagnasco, M. In Chemoprevention of Cancer and DNA Damage by Dietary Factors: Mechanisms of chemoprevention, antimutagenesis and anticarcinogenesis: an overview; Knasmüller, S.; DeMarini, D. M.; Johnson, I. T.; Gerhäuser, C., Eds.; Wiley-VCH: Weinheim, Germany, 2009, pp. 57-72.
3. Vandenberg, L. N.; Maffini, M. V.; Sonnenschein, C.; Rubin, B. S.; Soto, A. M. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr. Rev. 2009, 30, 75-95.
4. Suzuki, T.; Nakagawa, Y.; Takano, I.; Yaguchi, K.; Yasuda, K. Environmental fate of bisphenol A and its biological metabolites in river water and their xeno-estrogenic activity. Environ. Sci. Technol. 2004, 38, 2389-2396.
5. Staples, C. A.; Dorn, P. B.; Klecka, G. M.; O'Block, S. T.; Harris, L. R. A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere 1998, 36, 2149-2173.
6. International Agency for Research on Cancer. Sex Hormones (II); IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans. Vol.21, IARC: Lyon, France, 1979.
7. Pike, M. C.; Spicer, D. V.; Dahmoush, L.; Press, M. F. Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk. Epidemiol. Rev. 1993, 15, 17-35.
8. Yang, M.; Ryu, J. H.; Jeon, R.; Kang, D.; Yoo, K.Y. Effects of bisphenol A on breast cancer and its risk factors. Arch. Toxicol. 2008, Oct 9 [Epub ahead of print].
9. Atkinson, A.; Roy, D. In vitro conversion of environmental estrogenic chemical bisphenol A to DNA binding metabolite(s). Biochem. Biophys. Res. Commun. 1995, 210, 424-433.
10. Edmonds, J. S.; Nomaki, M.; Terasaki, M.; Morita, M.; Skelton, B. W.; White, A. H. The reaction of bisphenol A 3,4-quinone with DNA. Biochem. Biophys. Res. Commun. 2004, 319, 556-561.
11. Tsutsui, T.; Tamura, Y.; Yagi, E.; Hasegawa, K.; Takahashi, M.; Maizumi, N.; Yamaguchi, F.; Barrett, J. C. Bisphenol-A induces cellular transformation, aneuploidy and DNA adduct formation in cultured Syrian hamster embryo cells. Int. J. Cancer 1998, 75, 290-294.
12. Atkinson, A.; Roy, D. In vivo DNA adduct formation by bisphenol A. Environ. Mol. Mutagen. 1995, 26, 60-66.
13. Izzotti, A.; Kanitz, S.; D'Agostini, F.; Camoiorano, A.; De Flora, S. Formation of DNA adducts by bisphenol A, an endocrine dysruptor, in vitro in DNA and in liver and mammary tissues of treated mice. Mutat. Res. 2009, 679, 28-32.
14. Yao, R.; Wang, Y.; Lemon, W. J.; Lubet, R. A.; You, M. Budesonide exerts its chemopreventive efficacy during mouse lung tumorigenesis by modulating gene expressions. Oncogene 2004, 23, 7746-7752.
15. Wattenberg, L. W.; Wiedmann, T. S.; Estensen, R. D.; Zimmerman, C. L.; Steele, V. E.; Kelloff, G. J. Chemoprevention of pulmonary carcinogenesis by aerosolized budesonide in female A/J mice. Cancer Res. 1997, 57, 5489-8492.
16. Estensen, R. D.; Jordan, M. M.; Wiedmann, T. S.; Galbraith, A. R.; Steele, V. E.; Wattenberg, L. W. Effect of chemopreventive agents on separate stages of progression of benzo[alpha]pyrene induced lung tumors in A/J mice. Carcinogenesis 2004, 25, 197-201.
17. Wang, Y.; Zhang, Z.; Kastens, E.; Lubet, R. A.; You, M. Mice with alterations in both p53 and Ink4a/Arf display a striking increase in lung tumor multiplicity and progression: differential chemopreventive effect of budesonide in wild-type and mutant A/J mice. Cancer Res. 2003, 63, 4389-4395.
18. Balansky, R.; D'Agostini, F.; Ganchev, G.; Izzotti, A.; Di Marco, B; Lubet, R. A.; Zanesi, N.; Croce, C. M.; De Flora, S. Influence of FHIT on benzo[a]pyrene-induced tumors and alopecia in mice: chemoprevention by budesonide and N-acetylcysteine. Proc. Natl. Acad. Sci. USA. 2006, 103, 7823-7828.
19. Pereira, M. A.; Li, Y.; Gunning, W. T.; Kramer, P. M.; Al-Yaqoub, F.; Lubet, R. A.; Steele, V. E.; Szabo, E.; Tao, L. Prevention of mouse lung tumors by budesonide and its modulation of biomarkers. Carcinogenesis 2002, 23, 1185-1189.
20. Izzotti, A.; Balansky, R. M.; D'Agostini, F.; Bennicelli, C.; Myers, S. R.; Grubbs, C. J.; Lubet, R. A.; Kelloff, G. J.; De Flora, S. Modulation of biomarkers by chemopreventive agents in smoke-exposed rats. Cancer Res. 2001, 61, 2472-2479.
21. Izzotti, A.; Bagnasco, M.; Cartiglia, C.; Longobardi, M.; Camoirano, A.; Tampa, E.; Lubet, R. A.; De Flora, S. Modulation of multigene expression and proteome profiles by chemopreventive agents. Mutat. Res. 2005, 591, 212-223.
22. Hecht, S. S. Chemoprevention of cancer by isothiocyanates, modifiers of carcinogen metabolism. J. Nutr. 1999, 129, 768S-774S.
23. Stoner, G. D.; Morse, M. A. Isothiocyanates and plant polyphenols as inhibitors of lung and esophageal cancer. Cancer Lett. 1997, 114, 113-119.
24. Ye, B.; Zhang, Y. X.; Yang, F.; Chen, H. L.; Xia, D.; Liu, M. Q.; Lai, B. T. Induction of lung lesions in Wistar rats by 4-(methylnitrosamino)-1-(3- pyridyl)-1-butanone and its inhibition by aspirin and phenethyl isothiocyanate. BMC Cancer 2007, 7, 90.
25. Micale, R. T.; D'Agostini, F.; Steele, V. E.; La Maestra, S.; De Flora, S. Budesonide and phenethyl isothiocyanate attenuate DNA damage in bronchoalveolar lavage cells of mice exposed to environmental cigarette smoke. Curr. Cancer Drug Targets 2008, 8, 703-708.
26. D'Agostini, F.; Mastracci, L.; Izzotti, A.; Balansky, R.; Pennisi, T. M.; Steele, V. E.; De Flora, S. Modulation by phenethyl isothiocyanate and budesonide of molecular and histopathological alterations induced by environmental cigarette smoke in mice. Cancer Prev. Res. 2009, 2, 546-556.
27. Balansky, R.; Ganchev, G.; Iltcheva, M.; Steele, V. E.; De Flora, S. Prevention of cigarette smoke-induced lung cancer in mice by budesonide, phenethyl isothiocyanate, and N-acetylcysteine. Int. J. Cancer 2009, 126, 1047-1054.
28. Izzotti, A.; Balansky, R. M.; Blagoeva, P. M.; Mircheva, Z. I.; Tulimiero, L.; Cartiglia, C.; De Flora, S. DNA alterations in rat organs after chronic exposure to cigarette smoke and/or ethanol ingestion. FASEB J. 1998, 12, 753-758.
29. Moon, R. C.; Janns, D. H. ; Young, S. Preparation of fat cell "free" rat mammary gland. J. Histochem. Cytochem. 1969, 17, 182-186.
30. Izzotti, A.; Bagnasco, M.; D'Agostini, F.; Cartiglia, C.; Lubet, R. A.; Kelloff, G. J.; De Flora, S. Formation and persistence of nucleotide alterations in rats exposed whole-body to environmental cigarette smoke. Carcinogenesis 1999, 20, 1499-1505.
31. Randerath, K.; Liehr, J. G.; Gladek, A.; Randerath, E. Age-dependent covalent DNA alterations (I-compounds) in rodent tissues: species, tissue and sex specificities. Mutat. Res. 1989, 219, 121-133.
32. De Flora, S.; Izzotti, A.; Randerath, K.; Randerath, E.; Bartsch, H.; Nair, J.; Balansky, R.; van Schooten, F.; Degan, P.; Fronza, G.; Walsh, D.; Lewtas, J. DNA adducts and chronic degenerative disease. Pathogenetic relevance and implications in preventive medicine. Mutat. Res. 1996, 366, 197-238.
33. Izzotti, A.; Scatolini, L.; Lewtas, J.; Walsh, D.; De Flora, S. Enhanced levels of DNA adducts in the liver of woodchucks infected with hepatitis virus. Chem. Biol. Interact. 1995, 97, 273-285.
34. Yoo, S. D.; Shin, B. S.; Lee, B. M.; Lee, K. C.; Han, S. Y.; Kim, H. S. Bioavailability and mammary excretion of bisphenol A in Sprague-Dawley rats. J. Toxicol. Environ. Health 2001, A 64, 417-426.
35. Hu, R.; Xu, C.; Shen, G.; Jain, M. R.; Khor, T. O.; Gopalkrishnan, A.; Lin, W.; Reddy, B.; Chan, J. Y.; Kong, A. N. Identification of Nrf2-regulated genes induced by chemopreventive isothiocyanate PEITC by oligonucleotide microarray. Life Sci. 2006, 79, 1944-1955.
36. Moral, R.; Wang, R.; Russo, I. H.; Lamartiniere, C. A.; Pereira, J.; Russo, J. Effect of prenatal exposure to the endocrine disruptor bisphenol A on mammary gland morphology and gene expression signature. J. Endocrinol. 2008, 196, 101-112.
37. Wadia, P. R.; Vandenberg, L. N.; Schaeberle, C. M.; Rubin, B. S.; Sonnenschein, C.; Soto, A. M. Perinatal bisphenol A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environ. Health Perspect. 2007, 115, 592-598.
38. Youn, J. Y.; Park, H. Y.; Lee, J. W.; Jung, I. O.; Choi, K. H.; Kim, K.; Cho, K. H. Evaluation of the immune response following exposure of mice to bisphenol A: induction of Th1 cytokine and prolactin by BPA exposure in the mouse spleen cells. Arch. Pharm. Res. 2002, 5, 946-953.
39. Yamashita, U.; Kuroda, E.; Yoshida, Y.; Sugiura, T. Effect of endocrine disrupters on immune responses in vivo. J. UOEH 2003, 25, 365-374.
40. Vandenberg, L. N.; Maffini, M. V.; Schaeberle, C. M.; Ucci, A. A.; Sonnenschein, C.; Rubin, B. S.; Soto, A. M. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reprod. Toxicol. 2008, 26, 210-219.
41. Dandekar, A. M.; Robinson, E. A.; Appella, E.; Qasba, P. K. Complete sequence analysis of cDNA clones encoding rat whey phosphoprotein: homology to a protease inhibitor. Proc. Natl. Acad. Sci USA 1982, 79, 3987-3991.
42. Pereira, M. A.; Li, Y.; Gunning, W. T.; Kramer, P. M.; Al-Yaqoub, F.; Lubet, R. A.; Steele, V. E.; Szabo, E.; Tao, L. Prevention of mouse lung tumors by budesonide and its modulation of biomarkers. Carcinogenesis 2002, 23, 1185-1192.
43. Mager, D. E.; Moledina, N.; Jusko, W. J. Relative immunosuppressive potency of therapeutic corticosteroids measured by whole blood lymphocyte proliferation. J. Pharm. Sci. 2003, 92, 1521-1525.
44. Namkung-Matthäi, H.; Seale, J. P.; Brown, K.; Mason, R. S. Comparative effects of anti-inflammatory corticosteroids in human bone-derived osteoblast-like cells. Eur. Respir. J. 1998, 12, 1327-1333.
45. Jung, S.; Fehr, S.; Harder-d'Heureuse, J.; Wiedenmann, B.; Dignass, A. U. Corticosteroids impair intestinal epithelial wound repair mechanisms in vitro. Scand. J. Gastroenterol. 2001, 36, 963-970.
46. Banciu, M.; Metselaar, J. M.; Schiffelers, R. M.; Storm, G. Liposomal glucocorticoids as tumor-targeted anti-angiogenic nanomedicine in B16 melanoma-bearing mice. J. Steroid. Biochem. Mol. Biol. 2008, 111, 101-110.
47. Seandel, M.; Noack-Kunnmann, K.; Zhu, D.; Aimes, R. T.; Quigley, J. P. Growth factor-induced angiogenesis in vivo requires specific cleavage of fibrillar type I collagen. Blood 2001, 97, 2323-2332.
48. Kang, L.; Ding, L.; Wang, Z. Y. Isothiocyanates repress estrogen receptor alpha expression in breast cancer cells. Oncol. Rep. 2009, 21, 185-192.
49. Prawan, A.; Saw, C. L.; Khor, T.O.; Keum, Y. S.; Yu, S.; Hu, L.; Kong, A. N. Anti-NF-kappaB and anti-inflammatory activities of synthetic isothiocyanates: effect of chemical structures and cellular signaling. Chem. Biol. Interact. 2009, 179, 202-211.
50. Ferguson, L. R.; Philpott, M. Cancer prevention by dietary bioactive components that target the immune response. Curr. Cancer Drug Targets 2007, 7, 459-464.
51. Mi, L.; Xiao, Z.; Hood, B. L.; Dakshanamurthy, S.; Wang, X.; Govind, S.; Conrads, T. P.; Veenstra, T. D.; Chung, F. L. Covalent binding to tubulin by isothiocyanates. A mechanism of cell growth arrest and apoptosis. J. Biol. Chem. 2008, 283, 22136-22146.
52. D'Agostini, F.; Izzotti, A.; Balansky, R. M.; Bennicelli, C.; De Flora, S. Modulation of apoptosis by chemopreventive agents. Mutat. Res. 2005, 591, 173-186.
53. Woolner, S.; O'Brien, L. L.; Wiese, C.; Bement, W. M. Myosin-10 and actin filaments are essential for mitotic spindle function. J. Cell. Biol. 2008, 182, 77-88.
54. Suh, S. J.; Moon, S. K.; Kim, C. H. Raphanus sativus and its isothiocyanates inhibit vascular smooth muscle cells proliferation and induce G(1) cell cycle arrest. Int. Immunopharmacol. 2006, 6, 854-861.
55. Xiao, D.; Singh, S. V. Phenethyl isothiocyanate inhibits angiogenesis in vitro and ex vivo. Cancer Res. 2007, 67, 2239-2246.
56. Dabbs, D. J.; Gown, A. M. Distribution of calponin and smooth muscle myosin heavy chain in fine-needle aspiration biopsies of the breast. Diagn. Cytopathol. 1999, 20, 203-207.