Linked expression of Ah receptor, ARNT, CYP1A1, and CYP1B1 in rat mammary epithelia, in Vitro, is each substantially elevated by specific extracellular matrix interactions that precede branching morphogenesis

Toxicological Sciences

Volumn 82, Issue 1, 2004, Pages 46-61

  Larsen, Michele Campaigne ^a   Brake, Paul B ^a   Pollenz, Richard S ^b   Jefcoate, Colin R ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Ahr; ARNT; Branching morphogenesis; CYP1A1; CYP1B1; ECM

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON; AROMATIC HYDROCARBON RECEPTOR; BETA CATENIN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; EPIDERMAL GROWTH FACTOR; GROWTH FACTOR; LAMININ; MATRIGEL; PLASTIC; REGULATOR PROTEIN; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; BREAST CANCER; BREAST EPITHELIUM; CARCINOGENESIS; CELL ADHESION; CELL CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CULTURE MEDIUM; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; IN VITRO STUDY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RAT STRAIN; STRAIN DIFFERENCE;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CELLS, CULTURED; COLLAGEN; CYTOCHROME P-450 CYP1A1; DNA-BINDING PROTEINS; DRUG COMBINATIONS; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; LAMININ; MAMMARY GLANDS, ANIMAL; MORPHOGENESIS; PROTEOGLYCANS; RATS; RATS, INBRED WF; RATS, INBRED WKY; RECEPTORS, ARYL HYDROCARBON; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 8444250980     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/kfh242     Document Type: Article

References (43)

1. Benton, M. E., Chen, K. S., Haag, J. D., Sattler, C. A., and Gould, M. N. (1999). Precocious differentiation of the virgin Wistar-Kyoto rat mammary gland. Endocrinology 140, 2659-2671.
2. Bhattacharyya, K. K., Brake, P. B., Eltom, S. E., Otto, S. A., and Jefcoate, C. R. (1995). Identification of a rat adrenal cytochrome P450 active in polycyclic hydrocarbon metabolism as rat CYP1B1-Demonstration of a unique tissue-specific pattern of hormonal and aryl hydrocarbon receptor-linked regulation. J. Biol. Chem. 270, 11595-11602.
3. Bissell, M. J., and Bilder, D. (2003). Polarity determination in breast tissue: Desmosomal adhesion, myoepithelial cells, and laminin 1. Breast Cancer Res. 5, 117-119.
4. Bissell, M. J., Rizki, A., and Mian, I. S. (2003). Tissue architecture: The ultimate regulator of breast epithelial function. Current Opinion Cell Biol. 15, 753-762.
5. Brown, N. M., Manzolillo, P. A., Zhang, J. X., Wang, J., and Lamartiniere, C. A. (1998). Prenatal TCDD and predisposition to mammary cancer in the rat. Carcinogenesis 19, 1623-1629.
6. Chesire, D. R., Dunn, T. A., Ewing, C. M., Luo, J., and Isaacs, W. B. (2004). Identification of aryl hydrocarbon receptor as a putative Wnt/β-catenin pathway target gene in prostate cancer cells. Cancer Res. 64, 2523-2533.
7. Christou, M., Savas, U., Schroeder, S., Shen, X., Thompson, T., Gould, M. N., and Jefcoate, C. R. (1995). Cytochromes CYP1A1 and CYP1B1 in the rat mammary gland: Cell-specific expression and regulation by polycyclic aromatic hydrocarbons and hormones. Mol. Cell. Endocrinol. 115, 41-50.
8. Cho, Y. C., Zheng, W., and Jefcoate, C. R. (2004). Disruption of cell-cell contact maximally but transiently activates AhR-mediated transcription in 10T1/2 fibroblasts. Toxicol. Appl. Pharmacol. October issue.
9. Chung, L. W., Gleave, M. E., Hsieh, J. T., Hong, S. J., and Zhau, H. E. (1991). Reciprocal mesenchymal-epithelial interaction affecting prostate tumour growth and hormonal responsiveness. Cancer Surveys 11, 91-121.
10. Denison, M. S., and Nagy, S. R. (2003). Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 43, 309-334.
11. Eltom, S. E., Larsen, M. C., and Jefcoate, C. R. (1998). Expression of CYP1B1 but not CYP1A1 by primary cultured human mammary stromal fibroblasts constitutively and in response to dioxin exposure: Role of the Ah receptor. Carcinogenesis 19, 1437-1444.
12. Eltom, S. E., Zhang, L., and Jefcoate, C. R. (1999). Regulation of cytochrome P-450 (CYP) 1B1 in mouse Hepa-1 variant cell lines: A possible role for aryl hydrocarbon receptor nuclear translocator (ARNT) as a suppressor of CYP1B1 gene expression. Mol. Pharmacol. 55, 594-604.
13. Fata, J. E., Werb, Z., and Bissell, M. J. (2004). Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res. 6, 1-11.
14. Fernandez-Salguero, P. M., Ward, J. M., Sundberg, J. P., and Gonzalez, F. J. (1997). Lesions of aryl-hydrocarbon receptor-deficient mice. Vet. Pathol. 34, 605-614.
15. Gammon, M. D., Santella, R. M., Neugut, A. I., Eng, S. M., Teitelbaum, S. L., Paykin, A., Levin, B., Terry, M. B., Young, T. L., Wang, L. W., Wang, Q., Britton, J. A., Wolff, M. S., Stellman, S. D., Hatch, M., Kabat, G. C., Senie, R., Garbowski, G., Maffeo, C., Montalvan, P., Berkowitz, G., Kemeny, M., Citron, M., Schnabel, F., Schuss, A., et al. (2002). Environmental toxins and breast cancer on Long Island. I. Polycyclic aromatic hydrocarbon DNA adducts. Cancer Epidemol. Biomarkers Prev. 11, 677-685.
16. Gu, Y. Z., Hogenesch, J. B., and Bradfield, C. A. (2000). The PAS superfamily: Sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40, 519-561.
17. Guengerich, F. P., and Shimada, T. (1998). Activation of procarcinogens by human cytochrome P450 enzymes. Mutation Res. 400, 201-213.
18. Gurrath, M., Muller, G., Kessler, H., Aumailley, M., and Timpl, R. (1992). Conformation/activity studies of rationally designed potent anti-adhesive RGD peptides. Eur. J. Biochem. 210, 911-921.
19. Hahm, H. A., Ip, M. M., Darcy, K., Black, J. D., Shea, W. K., Forczek, S., Yoshimura, M., and Oka, T. (1990). Primary culture of normal rat mammary epithelial cells within a basement membrane matrix. II. Functional differentiation under serum-free conditions. In Vitro Cell. Develop. Biol. 26, 803-814.
20. Haslam, S. Z., and Woodward, T. L. (2003). Epithelial-cell-stromal interactions and steroid hormone action in normal and cancerous mammary gland. Breast Cancer Res. 5, 208-215.
21. Hushka, L. J., Williams, J. S., and Greenlee, W. F. (1998). Characterization of 2,3,7,8-tetrachlorodibenzofuran-dependent suppression and AH receptor pathway gene expression in the developing mouse mammary gland. Toxicol. Appl. Pharmacol. 152, 200-210.
22. Lan, H., Kendziorski, C. M., Haag, J. D., Shepel, L. A., Newton, M. A., and Gould, M. N. (2001). Genetic loci controlling breast cancer susceptibility in the Wistar-Kyoto rat. Genetics 157, 331-339.
23. Larsen, M. C., Angus, W. G. R., Brake, P. B., Eltom, S. E., Sukow, K. A., and Jefcoate, C. R. (1998). Characterization of CYP1B1 and CYP1A1 expression in human mammary epithelial cells: Role of the aryl hydrocarbon receptor in polycyclic aromatic hydrocarbon metabolism. Cancer Res. 58, 2366-2374.
24. Lin, T. M., Ko, K., Moore, R. W., Simanainen, U., Oberley, T. D., and Peterson, R. E. (2002). Effects of aryl hydrocarbon receptor null mutation and in utero and lactational 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on prostate and seminal vesicle development in C57BL/6 mice. Toxicol. Sci. 68, 479-487.
25. Murray, G. I., Melvin, W. T., Greenlee, W. F., and Burke, M. D. (2001). Regulation, function, and tissue-specific expression of cytochrome P450 CYP1B1. Annu. Rev. Pharmacol. Toxicol. 41, 297-316.
26. Muskhelishvili, L., Thompson, P. A., Kussewitt, D. F., Wang, C., and Kadlubar, F. F. (2001). In situ hybridization and immunohistochemical analysis of cytochrome P450 1B1 expression in human normal tissues. J. Histochem. Cytochem. 49, 229-236.
27. Novato, V., Roskelley, C. D., and Bissell, M. J. (2003). Collagen-IV and laminin-1 regulate estrogen receptor a expression and function in mouse mammary epithelial cells. J. Cell Sci. 116, 2975-2986.
28. Rundle, A., Tang, D. L., Hibshoosh, H., Estabrook, A., Schnabel, F., Cao, W. F., Grumet, S., and Perera, F. P. (2000). The relationship between genetic damage from polycyclic aromatic hydrocarbons in breast tissue and breast cancer. Carcinogenesis 21, 1281-1289.
29. Ruoslahti, E. (1996). RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12, 697-715.
30. Russo, J., Hu, Y., Yang, X., and Russo, I. (2000). Developmental, cellular, and molecular basis of human breast cancer. J. Natl. Cancer Inst. Monogr. 27, 17-37.
31. Russo, J., Hu, Y.F., Silva, I. D. C. G., and Russo, I. H. (2001). Cancer risk related to mammary gland structure and development. Microscopy Res. Tech. 52, 204-223.
32. Sadek, C. M., and Allen-Hoffmann, B. L. (1994). Suspension-mediated induction of Hepa 1c1c7 Cyp1a-1 expression is dependent on the Ah receptor signal transduction pathway. J. Biol. Chem. 269, 31505-31509.
33. Savas, Ü., Bhattacharyya, K. K., Christou, M., Alexander, D. L., and Jefcoate, C. R. (1994). Mouse cytochrome P-450EF, representative of a new 1B subfamily of cytochrome P-450s-cloning, sequence determination and tissue expression. J. Biol. Chem. 269, 14905-14911.
34. Savas, Ü., Carstens, C-P., and Jefcoate, C. R. (1997). Biological oxidations and P450 reactions. Recombinant mouse CYP1B1 expressed in Escherichia coli exhibits selective binding by polycyclic aromatic hydrocarbons and metabolism, which parallels C3H10T1/2 cell microsomes, but differs from human recombinant CYP1B1. Arch. Biochem. Biophys. 347, 181-192.
35. Schmidt, J. V., and Bradfield, C. A. (1996). Ah receptor signaling pathways. Annu. Rev. Cell Dev. Biol. 12, 55-89.
36. Silberstein, G. B. (2001a). Postnatal mammary gland morphogenesis. Microsc. Res. Tech. 52, 155-162.
37. Silberstein, G. B. (2001b). Tumour-stromal interactions. Role of the stroma in mammary development. Breast Cancer Res. 3, 218-223.
38. Simian, M., Hirai, Y., Navre, M., Werb, Z., Lochter, A., and Bissell, M. J. (2001). The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128, 3117-3131.
39. Spink, D. C., Spink, B. C., Cao, J. Q., DePasquale, J. A., Pentecost, B. T., Fasco, M. J., Li, Y., and Sutter, T. R. (1998). Differential expression of CYP1A1 and CYP1B1 in human breast epithelial cells and breast tumor cells. Carcinogenesis 19, 291-298.
40. Trombino, A. F., Near, R. I., Matulka, R. A., Yang, S., Hafer, L. J., Toselli, P. A., Kim, D. W., Rogers, A. E., Sonenshein, G. E., and Sherr, D. H. (2000). Expression of the aryl hydrocarbon receptor/transcription factor (AhR) and AhR-regulated CYP1 gene transcripts in a rat model of mammary tumorigenesis. Breast Cancer Res. Treatment 63, 117-131.
41. Wegner, C. C., and Carson, D. D. (1992). Mouse uterine stromal cells secrete a 30-kilodalton protein in response to coculture with uterine epithelial cells. Endocrinology 131, 2565-2572.
42. Wiseman, B. S., and Werb, Z. (2002). Stromal effects on mammary gland development and breast cancer. Science 296, 1046-1049.
43. Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J., and Keely, P. J. (2003). ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 163, 583-595.