Regulation of cytochrome P450 enzymes by aryl hydrocarbon receptor in human cells. CYP1A2 expression in the LS180 colon carcinoma cell line after treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin or 3-methylcholanthrene

Biochemical Pharmacology

Volumn 56, Issue 5, 1998, Pages 599-612

  Li, Wei ^a   Harper, Patricia A ^b   Tang, Bing Kou ^a   Okey, Allan B ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b Div Cardiovasc Surg Hosp S   (Canada)

Author keywords

2,3,7,8 tetrachlorodibenzo p dioxin; 3 Methylcholanthrene; AH receptor; CYP1A2; Cytochrome P450

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 3 METHYLCHOLANTHRENE; AROMATIC HYDROCARBON RECEPTOR; BENZ[A]ANTHRACENE; CYTOCHROME P450; MESSENGER RNA;

ARTICLE; CANCER; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG METABOLISM; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TECHNIQUE;

ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BENZ(A)ANTHRACENES; BLOTTING, NORTHERN; CATALYSIS; COLONIC NEOPLASMS; CYTOCHROME P-450 CYP1A2; DNA-BINDING PROTEINS; ENZYME INDUCTION; HUMANS; LOGISTIC MODELS; METHYLCHOLANTHRENE; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; TETRACHLORODIBENZODIOXIN; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 0032169826     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(98)00208-1     Document Type: Article

References (66)

1. Nelson D.R., Koymans L., Kamataki T., Stegeman J.J., Feyereisen R., Waxman D.J., Waterman M.R., Gotoh O., Coon M.J., Estabrook R.W., Gunsalus I.C., Nebert D.W. P450 superfamily Update on new sequences, gene mapping, accession numbers and nomenclature . Pharmacogenetics. 6:1996;1-42.
2. Okey A.B. Enzyme induction in the cytochrome P-450 system. Pharmacol Ther. 45:1990;241-298.
3. Gonzalez F.J. Molecular genetics of the P-450 superfamily. Pharmacol Ther. 45:1990;1-38.
4. Nebert D.W., McKinnon R.A. Cytochrome P450 Evolution and functional diversity . Prog Liver Dis. 12:1994;63-97.
5. Otto S., Marcos C., Pidgeon C., Jefcoate C.R. A novel adrenocorticotropin-inducible cytochrome P450 from rat adrenal microsomes catalyzes polycyclic aromatic hydrocarbon metabolism. Endocrinology. 129:1991;970-982.
6. Otto S., Bhattacharyya K.K., Jefcoate C.R. Polycyclic aromatic hydrocarbon metabolism in rat adrenal, ovary, and testis microsomes is catalyzed by the same novel cytochrome P450 (P450RAP). Endocrinology. 131:1992;3067-3076.
7. Savas Ü., Bhattacharyya K.K., Christou M., Alexander D.L., Jefcoate C.R. Mouse cytochrome P-450EF, representative of a new 1B subfamily of cytochrome P-450s. Cloning, sequence determination, and tissue expression. J Biol Chem. 269:1994;14905-14911.
8. Bowes R., Parrish A., Steinberg M., Willett K., Zhao W., Savas U., Jefcoate C., Safe S., Ramos K. Atypical cytochrome P450 induction profiles in glomerular mesangial cells at the mRNA and enzyme level. Evidence for CYP1A1 and CYP1B1 expression and their involvement in benzo-[a]pyrene metabolism. Biochem Pharmacol. 52:1996;587-595.
9. Shimada T., Hayes C.L., Yamazaki H., Amin S., Hecht S.S., Guengerich F.P., Sutter T.R. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56:1996;2979-2984.
10. Whitlock J.P. Jr, Denison M.S. Induction of cytochrome P450 enzymes that metabolize xenobiotics. Ortiz de Montellano P.R. Cytochrome P450 Structure, Mechanism, and Biochemistry . 1995;367-391 Plenum Press, New York.
11. Harper P.A., Golas C.L., Okey A.B. Ah receptor in mice genetically "nonresponsive" for cytochrome P4501A1 induction Cytosolic Ah receptor, transformation to the nuclear binding state, and induction of aryl hydrocarbon hydroxylase by halogenated and nonhalogenated aromatic hydrocarbons in embryonic tissues and cells . Mol Pharmacol. 40:1991;818-826.
12. Christou M., Savas Ü., Spink D.C., Gierthy J.F., Jefcoate C.R. Co-expression of human CYP1A1 and a human analog of cytochrome P450-EF in response to 2,3,7,8-tetrachlorodibenzo-p-dioxin in the human mammary carcinoma-derived MCF-7 cells. Carcinogenesis. 15:1994;725-732.
13. Doehr O., Vogel C., Abel J. Different response of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-sensitive genes in human breast cancer MCF-7 and MDA-MB 231 cells. Arch Biochem Biophys. 321:1995;405-412.
14. Hayes C.L., Spink D.C., Spink B.C., Cao J.Q., Walker N.J. 17β-Estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc Natl Acad Sci USA. 93:1996;9776-9781.
15. Kress S., Greenlee W.F. Cell-specific regulation of human CYP1A1 and CYP1B1 genes. Cancer Res. 57:1997;1264-1269.
16. Fukuda Y., Ishida N., Noguchi T., Kappas A., Sassa S. Interleukin-6 down regulates the expression of transcripts encoding cytochrome P450 IA1, IA2 and IIIA3 in human hepatoma cells. Biochem Biophys Res Commun. 184:1992;960-965.
17. Chung I., Bresnick E. 3-Methylcholanthrene-mediated induction of cytochrome P4501A2 in human hepatoma HepG2 cells as quantified by the reverse transcription-polymerase chain reaction. Arch Biochem Biophys. 314:1994;75-81.
18. Roberts E.A., Furuya K.N., Tang B.K., Kalow W. Caffeine biotransformation in human hepatocyte lines derived from normal liver tissue. Biochem Biophys Res Commun. 201:1994;559-566.
19. Guengerich F.P., Turvy C.G. Comparison of levels of several human microsomal cytochrome P-450 enzymes and epoxide hydrolases in normal and disease states using immunochemical analysis of surgical liver samples. J Pharmacol Exp Ther. 256:1991;1189-1194.
20. Harper P.A., Prokipcak R.D., Bush L.E., Golas C.L., Okey A.B. Detection and characterization of the Ah receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin in the human colon adenocarcinoma cell line LS180. Arch Biochem Biophys. 290:1991;27-36.
21. Furrer B., Candrian U., Wieland P., Luthy J. Improving PCR efficiency. Nature. 346:1990;324.
22. Li W., Donat S., Doehr O., Unfried K., Abel J. Ah receptor in different tissues of C57BL/6J and DBA/2J mice Use of competitive polymerase chain reaction to measure Ah-receptor mRNA expression . Arch Biochem Biophys. 315:1994;279-284.
23. Dolwick K.M., Schmidt J.V., Carver L.A., Swanson H.I., Bradfield C.A. Cloning and expression of a human Ah receptor cDNA. Mol Pharmacol. 44:1993;911-917.
24. Hoffman E.C., Reyes H., Chu F.-F., Sander F., Conley L.H., Brooks B.A., Hankinson O. Cloning of a factor required for activity of the Ah (dioxin) receptor. Science. 252:1991;954-958.
25. 1-450 Complementary DNA and amino acid sequence . Science. 228:1985;80-83.
26. 3450 cDNA and complete amino acid sequence . Nucleic Acids Res. 14:1986;6773-6774.
27. Sutter T.R., Tang Y.M., Hayes C.L., Wo Y.-Y.P., Jabs E.W., Li X., Yin H., Cody C.W., Greenlee W.F. Complete cDNA sequence of a human dioxin-inducible mRNA identifies a new gene subfamily of cytochrome P450 that maps to chromosome 2. J Biol Chem. 269:1994;13092-13099.
28. Ponte P., Ng S.-Y., Engel J., Gunning P., Kedes L. Evolutionary conservation in the untranslated regions of actin mRNAs DNA sequence of a human beta-actin cDNA . Nucleic Acids Res. 12:1984;1687-1696.
29. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:1976;248-254.
30. Edwards R.J., Murray B.P., Murray S., Schulz T., Neubert D., Gant T.W., Thorgeirsson S.S., Boobis A.R., Davies D.S. Contribution of CYP1A1 and CYP1A2 to the activation of heterocyclic amines in monkeys and human. Carcinogenesis. 15:1994;829-836.
31. Giannone J.V., Okey A.B., Harper P.A. Characterization of polyclonal antibodies to the aromatic hydrocarbon receptor. Can J Physiol Pharmacol. 73:1995;7-17.
32. Gu L, Caffeine Metabolism as Index of Cytochrome P4501A2 Activity. M.S. Thesis, University of Toronto, 1992.
33. Riddick D.S., Huang Y., Harper P.A., Okey A.B. 2,3,7,8-Tetrachlorodibenzo-p-dioxin versus 3-methylcholanthrene Comparative studies of Ah receptor binding, transformation, and induction of CYP1A1 . J Biol Chem. 269:1994;12118-12128.
34. Muntane-Relat J., Ourlin J.-C., Domergue J., Maurel P. Differential effects of cytokines on the inducible expression of CYP1A1, CYP1A2, and CYP3A4 in human hepatocytes in primary culture. Hepatology. 22:1995;1143-1153.
35. Reyes H., Reisz-Porszasz S., Hankinson O. Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science. 256:1992;1193-1195.
36. Ikeya K., Jaiswal A.K., Owens R.A., Jones J.E., Nebert D.W., Kimura S. Human CYP1A2 Sequence, gene structure, comparison with the mouse and rat orthologous gene, and differences in liver 1A2 mRNA expression . Mol Endocrinol. 3:1989;1399-1408.
37. Giannone J.V., Li W., Probst M., Okey A.B. Prolonged depletion of AH receptor without alteration of receptor mRNA levels after treatment of cells in culture with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem Pharmacol. 55:1998;489-497.
38. Sesardic D., Edwards R.J., Davies D.S., Thomas P.E., Levin W., Boobis A.R. High affinity phenacetin O-deethylase is catalyzed specifically by cytochrome P450d (P4501A2) in the liver of the rat. Biochem Pharmacol. 39:1990;489-498.
39. Brøsen K. Drug interaction and the cytochrome P450 system. The role of cytochrome P450 1A2. Clin Pharmacokinet. 29:1995;20-25.
40. Tassaneeyakul W., Birkett D.J., Veronese M.E., McManus M.E., Tukey R.H., Quattrochi L.C., Gelboin H.V., Miners J.O. Specificity of substrate and inhibitor probes for human cytochromes P450 1A1 and 1A2. J Pharmacol Exp Ther. 265:1993;401-407.
41. Brøsen K., Skjelbo E., Rasmussen B.B., Poulsen H.E., Loft S. Fluvoxamine is a potent inhibitor of cytochrome P4501A2. Biochem Pharmacol. 45:1993;1211-1214.
42. Schweikl H., Taylor J.A., Kitareewan S., Linko P., Nagorney D., Goldstein J.A. Expression of CYP1A1 and CYP1A2 genes in human liver. Pharmacogenetics. 3:1993;239-249.
43. Bock K.W. Aryl hydrocarbon or dioxin receptor Biology and toxic responses . Rev Physiol Biochem Pharmacol. 125:1993;1-42.
44. Quattrochi L.C., Vu T., Tukey R.H. The human CYP1A2 gene and induction by 3-methylcholanthrene. A region of DNA that supports Ah-receptor binding and promoter-specific induction. J Biol Chem. 269:1994;6949-6954.
45. Chung I., Bresnick E. Identification of positive and negative regulatory elements of the human cytochrome P4501A2 (CYP1A2) gene. Arch Biochem Biophys. 338:1997;220-226.
46. McDonnell W.M., Scheiman J.M., Traber P.G. Induction of cytochrome P450IA genes (CYP1A) by omeprazole in the human alimentary tract. Gastroenterology. 103:1992;1509-1516.
47. Daujat M., Charrasse S., Fabre I., Lesca P., Jounaïdi Y., Larroque C., Poellinger L., Maurel P. Induction of CYP1A1 gene by benzimidazole derivatives during Caco-2 cell differentiation. Evidence for an aryl-hydrocarbon receptor-mediated mechanism. Eur J Biochem. 237:1996;642-652.
48. Eaton D., Gallagher E.P., Bammler T.K., Kunze K.L. Role of cytochrome P4501A2 in chemical carcinogenesis Implications for human variability in expression and enzyme activity . Pharmacogenetics. 5:1995;259-274.
49. Guengerich F.P. Human cytochrome P450 enzymes. Ortiz de Montellano P.R. Cytochrome P450, Structure, Mechanism, and Biochemistry. 1995;473-536 Plenum Press, New York.
50. Gonzalez F.J., Gelboin H.V. Role of human cytochrome P-450s in risk assessment and susceptibility to environmentally based disease. J Toxicol Environ Health. 40:1993;289-308.
51. Hakkola J., Pasanen M., Pelkonen O., Hukkanen J., Evisalmi S., Anttila S., Rane A., Mäntylä M., Purkunen R., Saarikoski S., Tooming M., Raunio H. Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis. 18:1997;391-397.
52. Marie S., Anderson A., Cresteil T. Transplacental induction of cytochromes P-450IA1 and P-450IA2 by polycyclic aromatic carcinogens TCDD-binding protein level as the rate-limiting step . Carcinogenesis. 9:1988;2059-2063.
53. Tritscher A.M., Goldstein J.A., Portier C.J., McCoy Z., Clark G.C., Lucier G.W. Dose-response relationships for chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin in a rat tumor promotion model Quantification and immunolocalization of CYP1A1 and CYP1A2 in the liver . Cancer Res. 52:1992;3436-3442.
54. 3-450 mRNA levels by 3-methylcholanthrene. Mol Pharmacol. 26:1984;117-121.
55. Goasduff T., Menez J.F., Dreano Y., Berthou F. CYP1A2 and 2E1 expression in rat liver treated with combined inducers (3-methylcholanthrene and ethanol). Biochem Biophys Res Commun. 211:1995;497-503.
56. Carver L.A., Hogenesch J.B., Bradfield C.A. Tissue specific expression of the rat Ah-receptor and ARNT mRNAs. Nucleic Acids Res. 22:1994;3038-3044.
57. Hankinson O. The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol. 35:1995;307-340.
58. Ema M., Taya S., Yokotani N., Sogawa K., Matsuda Y., Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA. 94:1997;4273-4278.
59. Hogenesch J.B., Chan W.K., Jackiw V.H., Brown R.C., Gu Y.-Z., Pray-Grant M., Perdew G.H., Bradfield C.A. Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J Biol Chem. 272:1997;8581-8593.
60. Kallio P.J., Pongratz I., Gradin K., McGuire J., Poellinger L. Activation of hypoxia-inducible factor 1α Posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor . Proc Natl Acad Sci USA. 94:1997;5667-5672.
61. Ma Q., Whitlock J.P. Jr. A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Chem. 272:1997;8878-8884.
62. 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 . Mol Cell Endocrinol. 115:1995;41-50.
63. Sutter T.R., Greenlee W.F. Classification of members of the Ah gene battery. Chemosphere. 25:1992;223-226.
64. Abel J., Li W., Doehr O., Vogel C. Concentration-response relationship of cytochrome P4501b1 mRNA induction by 2,3,7,8-tetrachlorodibenzo-p-dioxin in livers of C57BL/6J and DBA/2J mice. Arch Toxicol. 70:1996;510-513.
65. Prokipcak R.D., Okey A.B. Downregulation of the Ah receptor in mouse hepatoma cells treated in culture with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Can J Physiol Pharmacol. 69:1991;1204-1210.
66. Pollenz R.S. The aryl-hydrocarbon receptor, but not the aryl-hydrocarbon receptor nuclear translocator protein, is rapidly depleted in hepatic and nonhepatic cultured cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol Pharmacol. 49:1996;391-398.