Role of mammary epithelial and stromal P450 enzymes in the clearance and metabolic activation of 7,12-dimethylbenz(a)anthracene in mice

Toxicology Letters

Volumn 212, Issue 2, 2012, Pages 97-105

  Lin, Yang ^a,b   Yao, Yunyi ^b   Liu, Senyan ^b   Wang, Lihua ^c   Moorthy, Bhagavatula ^c   Xiong, Dongsheng ^a   Cheng, Tao ^a   Ding, Xinxin ^b   Gu, Jun ^b  

^a INSTITUTE OF HEMATOLOGY AND BLOOD DISEASES HOSPITAL   (China)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

7,12 Dimethylbenz(a)anthracene; Cytochrome P450; Cytochrome P450 reductase; DNA adduct; Gene knockout; Mammary gland; Mice

Indexed keywords

7,12 DIMETHYLBENZ[A]ANTHRACENE; CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; CYTOCHROME P450 REDUCTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM; CARCINOGEN DNA INTERACTION; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; DNA DAMAGE; DRUG CLEARANCE; DRUG DISPOSITION; EMBRYO; ENZYME ACTIVITY; EXPERIMENTAL MODEL; FEMALE; GENE DELETION; HISTOPATHOLOGY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MAMMARY GLAND; METABOLIC ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STROMA CELL; WILD TYPE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BIOTRANSFORMATION; CARCINOGENS; CYTOCHROME P-450 CYP1A1; DNA ADDUCTS; EPITHELIUM; FEMALE; MAMMARY GLANDS, ANIMAL; METABOLIC CLEARANCE RATE; MICE;

MUS;

EID: 84861892525     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.05.005     Document Type: Article

References (39)

1. Arif J.M., Smith W.A., Gupta R.C. Tissue distribution of DNA adducts in rats treated by intramammillary injection with dibenzo[a,l]pyrene, 7,12-dimethylbenz(a)anthracene and benzo[a]pyrene. Mutation Research 1997, 378:31-39.
2. Black S.D., Coon M.J. P-450 cytochromes: structure and function. Advances in Enzymology and Related Areas of Molecular Biology 1987, 60:35-87.
3. Christou M., Savas U., Schroeder S., Shen X., Thompson T., Gould M.N., Jefcoate C.R. Cytochromes CYP1A1 and CYP1B1 in the rat mammary gland: cell-specific expression and regulation by polycyclic aromatic hydrocarbons and hormones. Molecular and Cellular Endocrinology 1995, 115:41-50.
4. Conroy J.L., Fang C., Gu J., Zeitlin S.O., Yang W., Yang J., VanAlstine M.A., Nalwalk J.W., Albrecht P.J., Mazurkiewicz J.E., Snyder-Keller A., Shan Z., Zhang S.Z., Wentland M.P., Behr M., Knapp B.I., Bidlack J.M., Zuiderveld O.P., Leurs R., Ding X., Hough L.B. Opioids activate brain analgesic circuits through cytochrome P450/epoxygenase signaling. Nature Neuroscience 2010, 13:284-286.
5. Cui Y., Miyoshi K., Claudio E., Siebenlist U.K., Gonzalez F.J., Flaws J., Wagner K.U., Hennighausen L. Loss of the peroxisome proliferation-activated receptor gamma (PPARgamma) does not affect mammary development and propensity for tumor formation but leads to reduced fertility. Journal of Biological Chemistry 2002, 277:17830-17835.
6. Fang C., Gu J., Xie F., Behr M., Yang W., Abel E.D., Ding X. Deletion of the NADPH-cytochrome P450 reductase gene in cardiomyocytes does not protect mice against doxorubicin-mediated acute cardiac toxicity. Drug Metabolism and Disposition: The Biological Fate of Chemicals 2008, 36:1722-1728.
7. Fang C., Behr M., Xie F., Lu S., Doret M., Luo H., Yang W., Aldous K., Ding X., Gu J. Mechanism of chloroform-induced renal toxicity: non-involvement of hepatic cytochrome P450-dependent metabolism. Toxicology and Applied Pharmacology 2008, 227:48-55.
8. Feng Y., Manka D., Wagner K.U., Khan S.A. Estrogen receptor-alpha expression in the mammary epithelium is required for ductal and alveolar morphogenesis in mice. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:14718-14723.
9. Galvan N., Teske D.E., Zhou G., Moorthy B., MacWilliams P.S., Czuprynski C.J., Jefcoate C.R. Induction of CYP1A1 and CYP1B1 in liver and lung by benzo(a)pyrene and 7,12-d imethylbenz(a)anthracene do not affect distribution of polycyclic hydrocarbons to target tissue: role of AhR and CYP1B1 in bone marrow cytotoxicity. Toxicology and Applied Pharmacology 2005, 202:244-257.
10. Gu J., Chen C.S., Wei Y., Fang C., Xie F., Kannan K., Yang W., Waxman D.J., Ding X. A mouse model with liver-specific deletion and global suppression of the NADPH-cytochrome P450 reductase gene: characterization and utility for in vivo studies of cyclophosphamide disposition. Journal of Pharmacology and Experimental Therapeutics 2007, 321:9-17.
11. Gu J., Weng Y., Zhang Q.Y., Cui H., Behr M., Wu L., Yang W., Zhang L., Ding X. Liver-specific deletion of the NADPH-cytochrome P450 reductase gene: impact on plasma cholesterol homeostasis and the function and regulation of microsomal cytochrome P450 and heme oxygenase. Journal of Biological Chemistry 2003, 278:25895-25901.
12. Guengerich F.P. Roles of cytochrome P-450 enzymes in chemical carcinogenesis and cancer chemotherapy. Cancer Research 1988, 48:2946-2954.
13. Gupta R.C. Nonrandom binding of the carcinogen N-hydroxy-2-acetylaminofluorene to repetitive sequences of rat liver DNA in vivo. Proceedings of the National Academy of Sciences of the United States of America 1984, 81:6943-6947.
14. Hellmold H., Lamb J.G., Wyss A., Gustafsson J.A., Warner M. Developmental and endocrine regulation of P450 isoforms in rat breast. Molecular Pharmacology 1995, 48:630-638.
15. Hellmold H., Magnusson M., Pelto-Huikko M., Rylander T., Gustafsson J., Warner M. Identification of CYP2A3 as a major cytochrome P450 enzyme in the female peripubertal rat breast. Molecular Pharmacology 1998, 53:475-482.
16. Izzotti A., Camoirano A., Cartiglia C., Grubbs C.J., Lubet R.A., Kelloff G.J., De Flora S. Patterns of DNA adduct formation in liver and mammary epithelial cells of rats treated with 7,12-dimethylbenz(a)anthracene, and selective effects of chemopreventive agents. Cancer Research 1999, 59:4285-4290.
17. Kleiner H.E., Vulimiri S.V., Hatten W.B., Reed M.J., Nebert D.W., Jefcoate C.R., DiGiovanni J. Role of cytochrome P4501 family members in the metabolic activation of polycyclic aromatic hydrocarbons in mouse epidermis. Chemical Research in Toxicology 2004, 17:1667-1674.
18. Kleiner H.E., Vulimiri S.V., Miller L., Johnson W.H., Whitman C.P., DiGiovanni J. Oral administration of naturally occurring coumarins leads to altered phases I and II enzyme activities and reduced DNA adduct formation by polycyclic aromatic hydrocarbons in various tissues of SENCAR mice. Carcinogenesis 2001, 22:73-82.
19. Li D., Wang M., Dhingra K., Hittelman W.N. Aromatic DNA adducts in adjacent tissues of breast cancer patients: clues to breast cancer etiology. Cancer Research 1996, 56:287-293.
20. Li D., Wang M., Firozi P.F., Chang P., Zhang W., Baer-Dubowska W., Moorthy B., Vulimiri S.V., Goth-Goldstein R., Weyand E.H., DiGiovanni J. Characterization of a major aromatic DNA adduct detected in human breast tissues. Environmental and Molecular Mutagenesis 2002, 39:193-200.
21. Loladze A.V., Stull M.A., Rowzee A.M., Demarco J., Lantry J.H., Rosen C.J., Leroith D., Wagner K.U., Hennighausen L., Wood T.L. Epithelial-specific and stage-specific functions of insulin-like growth factor-I during postnatal mammary development. Endocrinology 2006, 147:5412-5423.
22. Median D. Mammary tumors. The Mouse in Biomedical Research 1982, Vol. IV:373-391. Academic Press, New York.
23. Parkinson A., Ogilvie B.W. Biotransformation of xenobiotics. Casarett and Doull's Toxicology: The Basic Science of Poisons 2008, 161-304. McGraw-Hill, New York. C.D. Klaassen (Ed.).
24. Pass G.J., Carrie D., Boylan M., Lorimore S., Wright E., Houston B., Henderson C.J., Wolf C.R. Role of hepatic cytochrome p450s in the pharmacokinetics and toxicity of cyclophosphamide: studies with the hepatic cytochrome p450 reductase null mouse. Cancer Research 2005, 65:4211-4217.
25. Perera F.P., Estabrook A., Hewer A., Channing K., Rundle A., Mooney L.A., Whyatt R., Phillips D.H. Carcinogen-DNA adducts in human breast tissue. Cancer Epidemiology, Biomarkers and Prevention 1995, 4:233-238.
26. Reddy M.V., Randerath K. Nuclease P1-mediated enhancement of sensitivity of 32P-postlabeling test for structurally diverse DNA adducts. Carcinogenesis 1986, 7:1543-1551.
27. Russo J., Russo I.H. Experimentally induced mammary tumors in rats. Breast Cancer Research and Treatment 1996, 39:7-20.
28. Sharma D., Smits B.M., Eichelberg M.R., Meilahn A.L., Muelbl M.J., Haag J.D., Gould M.N. Quantification of epithelial cell differentiation in mammary glands and carcinomas from DMBA- and MNU-exposed rats. PLoS One 2011, 6:e26145.
29. Shen A.L., O'Leary K.A., Kasper C.B. Association of multiple developmental defects and embryonic lethality with loss of microsomal NADPH-cytochrome p450 oxidoreductase. Journal of Biological Chemistry 2002, 277:6536-6541.
30. Todorovic R., Ariese F., Devanesan P., Jankowiak R., Small G.J., Rogan E., Cavalieri E. Determination of benzo[a]pyrene- and 7,12-dimethylbenz(a)anthracene-DNA adducts formed in rat mammary glands. Chemical Research in Toxicology 1997, 10:941-947.
31. Wagner K.U., Krempler A., Qi Y., Park K., Henry M.D., Triplett A.A., Riedlinger G., Rucker E.B., Hennighausen L. Tsg101 is essential for cell growth, proliferation, and cell survival of embryonic and adult tissues. Molecular and Cellular Biology 2003, 23:150-162.
32. Wagner K.U., McAllister K., Ward T., Davis B., Wiseman R., Hennighausen L. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Research 2001, 10:545-553.
33. Weng Y., Fang C., Turesky R.J., Behr M., Kaminsky L.S., Ding X. Determination of the role of target tissue metabolism in lung carcinogenesis using conditional cytochrome p450 reductase-null mice. Cancer Research 2007, 67:7825-7832.
34. Williams J.A., Phillips D.H. Mammary expression of xenobiotic metabolizing enzymes and their potential role in breast cancer. Cancer Research 2000, 60:4667-4677.
35. Wiseman B.S., Werb Z. Stromal effects on mammary gland development and breast cancer. Science 2002, 296:1046-1049.
36. Wu L., Gu J., Weng Y., Kluetzman K., Swiatek P., Behr M., Zhang Q.Y., Zhuo X., Xie Q., Ding X. Conditional knockout of the mouse NADPH-cytochrome p450 reductase gene. Genesis 2003, 36:177-181.
37. Xiao Y., Ge M., Xue X., Wang C., Wang H., Wu X., Li L., Liu L., Qi X., Zhang Y., Li Y., Luo H., Xie T., Gu J., Ren J. Hepatic cytochrome P450s metabolize aristolochic acid and reduce its kidney toxicity. Kidney International 2008, 73:1231-1239.
38. Zhang Q.Y., Fang C., Zhang J., Dunbar D., Kaminsky L., Ding X. An intestinal epithelium-specific cytochrome P450 (P450) reductase-knockout mouse model: direct evidence for a role of intestinal p450s in first-pass clearance of oral nifedipine. Drug Metabolism and Disposition: The Biological Fate of Chemicals 2009, 37:651-657.
39. Zhang Q.Y., Kaminsky L.S., Dunbar D., Zhang J., Ding X. Role of small intestinal cytochromes p450 in the bioavailability of oral nifedipine. Drug Metabolism and Disposition: The Biological Fate of Chemicals 2007, 35:1617-1623.