The aryl hydrocarbon receptor activator benzo[a]pyrene enhances vitamin D3 catabolism in macrophages

Toxicological Sciences

Volumn 109, Issue 1, 2009, Pages 50-58

  Matsunawa, Manabu ^a   Amano, Yusuke ^a,b   Endo, Kaori ^a   Uno, Shigeyuki ^a   Sakaki, Toshiyuki ^c   Yamada, Sachiko ^a   Makishima, Makoto ^a  

^a NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c TOYAMA PREFECTURAL UNIVERSITY   (Japan)

Author keywords

Aryl hydrocarbon receptor; Benzo a pyrene; CYP24A1; Macrophages; Vitamin D; Vitamin D receptor

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ARACHIDONATE 5 LIPOXYGENASE; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CALCITRIOL; CATHELICIDIN; CD14 ANTIGEN; CYTOCHROME P450; CYTOCHROME P450 24A1; LITHOCHOLIC ACID; MESSENGER RNA; PROTEIN SYNTHESIS INHIBITOR; RETINOID X RECEPTOR; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR;

ARTICLE; CELL STRAIN MCF 7; CIGARETTE SMOKING; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE TARGETING; HUMAN; HUMAN CELL; HYDROXYLATION; MACROPHAGE; MODULATION; MONOCYTE; PROMOTER REGION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; VITAMIN D METABOLISM; VITAMIN METABOLISM;

ARYL HYDROCARBON HYDROXYLASES; BENZO(A)PYRENE; CELL LINE; CELL LINE, TUMOR; CHOLECALCIFEROL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GENE EXPRESSION; HUMANS; MACROPHAGES; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, CALCITRIOL; RETINOID X RECEPTOR ALPHA; SIGNAL TRANSDUCTION; STEROID HYDROXYLASES;

EID: 65549157442     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp044     Document Type: Article

References (39)

1. Adachi, R., Shulman, A. I., Yamamoto, K., Shimomura, I., Yamada, S., Mangelsdorf, D. J., and Makishima, M. (2004). Structural determinants for vitamin D receptor response to endocrine and xenobiotic signals. Mol. Endocrinol. 18, 43-52.
2. Andersson, P., McGuire, J., Rubio, C., Gradin, K., Whitelaw, M. L., Pettersson, S., Hanberg, A., and Poellinger, L. (2002). A constitutively active dioxin/aryl hydrocarbon receptor induces stomach tumors. Proc. Natl. Acad. Sci. U. S. A. 99, 9990-9995.
3. Anthonisen, N. R., Skeans, M. A., Wise, R. A., Manfreda, J., Kanner, R. E., and Connett, J. E. (2005). The effects of a smoking cessation intervention on 14.5-year mortality: A randomized clinical trial. Ann. Intern. Med. 142, 233-239.
4. Black, P. N., and Scragg, R. (2005). Relationship between serum 25-hydroxyvitamin D and pulmonary function in the third national health and nutrition examination survey. Chest 128, 3792-3798.
5. Bock, K. W., and Kohle, C. (2006). Ah receptor: Dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem. Pharmacol. 72, 393-404.
6. Chen, K. S., and DeLuca, H. F. (1995). Cloning of the human 1α,25-dihydroxyvitamin D-3 24-hydroxylase gene promoter and identification of two vitamin D-responsive elements. Biochim. Biophys. Acta. 1263, 1-9.
7. Drane, P., Compe, E., Catez, P., Chymkowitch, P., and Egly, J. M. (2004). Selective regulation of vitamin D receptor-responsive genes by TFIIH. Mol. Cell. 16, 187-197.
8. Endo, K., Uno, S., Seki, T., Ariga, T., Kusumi, Y., Mitsumata, M., Yamada, S., and Makishima, M. (2008). Inhibition of aryl hydrocarbon receptor transactivation and DNA adduct formation by CYP1 isoform-selective metabolic deactivation of benzo[a]pyrene. Toxi col. Appl. Pharmacol. 230, 135-143.
9. Gasiewicz, T. A., and Rucci, G. (1991). α-Naphthoflavone acts as an antagonist of 2,3,7, 8-tetrachlorodibenzo-p-dioxin by forming an inactive complex with the Ah receptor. Mol. Pharmacol. 40, 607-612.
10. Giovannucci, E., Liu, Y., Rimm, E. B., Hollis, B. W., Fuchs, C. S., Stampfer, M. J., and Willett, W. C. (2006). Prospective study of predictors of vitamin D status and cancer incidence and mortality in men. J. Natl. Cancer Inst. 98, 451-459.
11. Hamamoto, H., Kusudo, T., Urushino, N., Masuno, H., Yamamoto, K., Yamada, S., Kamakura, M., Ohta, M., Inouye, K., and Sakaki, T. (2006). Structure-function analysis of vitamin D 24-hydroxylase (CYP24A1) by site-directed mutagenesis: Amino acid residues responsible for species-based difference of CYP24A1 between humans and rats. Mol. Pharmacol. 70, 120-128.
12. 3 derivatives with adamantane or lactone ring side chains are cell type-selective vitamin D receptor modulators. Mol. Pharmacol. 71, 1298-1311.
13. Irigaray, P., Newby, J. A., Clapp, R., Hardell, L., Howard, V., Montagnier, L., Epstein, S., and Belpomme, D. (2007). Lifestyle-related factors and environmental agents causing cancer: An overview. Biomed. Pharmacother. 61, 640-658.
14. Ishizawa, M., Matsunawa, M., Adachi, R., Uno, S., Ikeda, K., Masuno, H., Shimizu, M., Iwasaki, K., Yamada, S., and Makishima, M. (2008). Lithocholic acid derivatives act as selective vitamin D receptor modulators without inducing hypercalcemia. J. Lipid Res. 49, 763-772.
15. Joiakim, A., Mathieu, P. A., Elliott, A. A., and Reiners, J. J., Jr. (2004). Superinduction of CYP1A1 in MCF10A cultures by cycloheximide, anisomycin, and puromycin: A process independent of effects on protein translation and unrelated to suppression of aryl hydrocarbon receptor proteolysis by the proteasome. Mol. Pharmacol. 66, 936-947.
16. 3 stimulates cyclic vitamin D receptor/retinoid X receptor DNA-binding, coactivator recruitment, and histone acetylation in intact osteoblasts. J. Bone Miner. Res. 20, 305-317.
17. 3 by CYP24: Species-based difference between humans and rats. Biochem. Biophys. Res. Commun. 309, 885-892.
18. Liu, P. T., Stenger, S., Li, H., Wenzel, L., Tan, B. H., Krutzik, S. R., Ochoa, M. T., Schauber, J., Wu, K., Meinken, C., et al. (2006). Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311, 1770-1773.
19. Makishima, M., Lu, T. T., Xie, W., Whitfield, G. K., Domoto, H., Evans, R. M., Haussler, M. R., and Mangelsdorf, D. J. (2002). Vitamin D receptor as an intestinal bile acid sensor. Science 296, 1313-1316.
20. Makishima, M., and Yamada, S. (2005). Targeting the vitamin D receptor: Advances in drug discovery. Expert Opin. Ther. Pat. 15, 1133-1145.
21. Miller, K. P., and Ramos, K. S. (2001). Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab. Rev. 33 1-35.
22. Nebert, D. W., Roe, A. L., Dieter, M. Z., Solis, W. A., Yang, Y., and Dalton, T. P. (2000). Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 59, 65-85.
23. Ohtake, F., Baba, A., Takada, I., Okada, M., Iwasaki, K., Miki, H., Takahashi, S., Kouzmenko, A., Nohara, K., Chiba, T., et al. (2007). Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446, 562-566.
24. Ohtake, F., Takeyama, K., Matsumoto, T., Kitagawa, H., Yamamoto, Y., Nohara, K., Tohyama, C., Krust, A., Mimura, J., Chambon, P., et al. (2003). Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 423, 545-550.
25. 3 by CYP24: Species-based difference between humans and rats. Biochem. Pharmacol. 65, 1957-1965.
26. 3 with C24-C25 bond cleavage catalyzed by human CYP24A1. Biochemistry 43, 4530-4537.
27. Seuter, S., Vaisanen, S., Radmark, O., Carlberg, C., and Steinhilber, D. (2007). Functional characterization of vitamin D responding regions in the human 5-Lipoxygenase gene. Biochim. Biophys. Acta. 1771, 864-872.
28. Shang, Y., Hu, X., DiRenzo, J., Lazar, M. A., and Brown, M. (2000). Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103, 843-852.
29. Sharma, O. P. (1996). Vitamin D, calcium, and sarcoidosis. Chest 109, 535-539.
30. Shimada, T. (2006). Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab. Pharmacokinet. 21, 257-276.
31. Tavangar, K., Hoffman, A. R., and Kraemer, F. B. (1990). A micromethod for the isolation of total RNA from adipose tissue. Anal. Biochem. 186, 60-63.
32. 3. Mol. Pharmacol. 60, 1399-1406.
33. Thun, M. J., Henley, S. J., and Calle, E. E. (2002). Tobacco use and cancer: An epidemiologic perspective for geneticists. Oncogene 21, 7307-7325.
34. Uno, S., Dalton, T. P., Derkenne, S., Curran, C. P., Miller, M. L., Shertzer, H. G., and Nebert, D. W. (2004). Oral exposure to benzo[a ]pyrene in the mouse: Detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol. Pharmacol. 65 1225-1237.
35. Uno, S., Dalton, T. P., Dragin, N., Curran, C. P., Derkenne, S., Miller, M. L., Shertzer, H. G., Gonzalez, F. J., and Nebert, D. W. (2006). Oral benzo[a]pyrene in Cyp1 knockout mouse lines: CYP1A1 important in de toxication, CYP1B1 metabolism required for immune damage independent of total-body burden and clearance rate. Mol. Pharmacol. 69, 1103-1114.
36. van Schoor, N. M., Visser, M., Pluijm, S. M. F., Kuchuk, N., Smit, J. H., and Lips, P. (2008). Vitamin D deficiency as a risk factor for osteoporotic fractures. Bone 42, 260-266.
37. Wang, T. J., Pencina, M. J., Booth, S. L., Jacques, P. F., Ingelsson, E., Lanier, K., Benjamin, E. J., D'Agostino, R. B., Wolf, M., and Vasan, R. S. (2008). Vitamin D deficiency and risk of cardiovascular disease. Circulation 117, 503-511.
38. Waugh, E. J., Lam, M. A., Hawker, G. A., McGowan, J., Papaioannou, A., Cheung, A. M., Hodsman, A. B., Leslie, W. D., Siminoski, K., and Jamal, S. A. (2009). Risk factors for low bone mass in healthy 40-60 year old women: A systematic review of the literature. Osteoporos. Int. 20, 1-21.
39. 3: Implications for drug-induced osteomalacia. Mol. Pharmacol. 69, 56-65.