Regulation of cytochrome P450 gene expression in the olfactory mucosa

Chemico-Biological Interactions

Volumn 147, Issue 3, 2004, Pages 247-258

  Ling, Guoyu ^a   Gu, Jun ^a   Genter, Mary Beth ^b   Zhuo, Xiaoliang ^a   Ding, Xinxin ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

2,6 dichlorobenzonitrile; 3 MC; 3 methylcholanthrene; AhR; aryl hydrocarbon receptor; BaP; benzo a pyrene; CYP; cytochrome P450; DCBN; LCR; locus control region; LSF; lung specific factor; mEH; microsomal epoxide hydrolase; NFI; nuclear factor 1; olfactory mucosa; OM

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 1A; CYTOCHROME P450 1A2; CYTOCHROME P450 2A; CYTOCHROME P450 2B; CYTOCHROME P450 2C; CYTOCHROME P450 2E1; CYTOCHROME P450 2G1; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; CHEMOSENSITIVITY; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME MECHANISM; GENE EXPRESSION REGULATION; HUMAN; MAMMAL; NONHUMAN; OLFACTORY EPITHELIUM; PREVALENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RISK ASSESSMENT; SEX DIFFERENCE; SHORT SURVEY; SMELLING DISORDER; SPECIES DIFFERENCE; STATISTICAL SIGNIFICANCE; TISSUE DISTRIBUTION; TOXICOKINETICS; XENOBIOTIC METABOLISM;

MAMMALIA;

EID: 2342512149     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2004.02.003     Document Type: Review

References (109)

1. X. Ding, A.R. Dahl, Olfactory mucosa: composition, enzymatic localization, and metabolism, in: R.L. Doty (Ed.), Handbook of Olfaction and Gustation, second ed., Marcel Dekker, New York, 2003, pp. 51-73.
2. H. Baker, M.B. Genter, The olfactory system and the nasal mucosa as portals of entry of viruses, drugs, and other exogenous agents into the brain, in: R.L. Doty (Ed.), Handbook of Olfaction and Gustation, second ed., Marcel Dekker, New York, 2003, pp. 549-573.
3. Ding X., Kaminsky L.S. Human extrahepatic cytochromes P450: function in xenobiotic metabolism and tissue-selective chemical toxicity in the respiratory and gastrointestinal tracts. Annu. Rev. Pharmacol. Toxicol. 43:2003;149-173
4. Ding X., Coon M.J. Immunochemical characterization of multiple forms of cytochrome P-450 in rabbit nasal microsomes and evidence for tissue-specific expression of P-450s NMa and NMb. Mol. Pharmacol. 37:1990;489-496
5. Genter M.B., Liang H.C., Gu J., Ding X., Negishi M., McKinnon R.A., Nebert D.W. Role of CYP2A5 and 2G1 in acetaminophen metabolism and toxicity in the olfactory mucosa of the Cyp1a2(-/-) mouse. Biochem. Pharmacol. 55:1998;1819-1826
6. Gu J., Zhang Q.-Y., Genter M.B., Lipinskas T.W., Negishi M., Nebert D.W., Ding X. Purification and characterization of heterologously expressed mouse CYP2A5 and CYP2G1: role in metabolic activation of acetaminophen and 2, 6-dichlorobenzonitrile in mouse olfactory mucosal microsomes. J. Pharmacol. Exp. Ther. 285:1998;1287-1295
7. Brandt I., Brittebo E.B., Feil V.J., Bakke J.E. Irreversible binding and toxicity of the herbicide dichlobenil (2, 6-dichlorobenzonitrile) in the olfactory mucosa of mice. Toxicol. Appl. Pharmacol. 103:1990;491-501
8. Deamer N.J., Genter M.B. Olfactory toxicity of diethyldithiocarbamate (DDTC) and disulfiram and the protective effect of DDTC against the olfactory toxicity of dichlobenil. Chem. Biol. Interact. 95:1995;215-226
9. Franzen A., Carlsson C., Brandt I., Brittebo E.B. Isomer-specific bioactivation and toxicity of dichlorophenyl methylsulphone in rat olfactory mucosa. Toxicol. Pathol. 31:2003;364-372
10. Gu J., Walker V.E., Lipinskas T.W., Walker D.M., Ding X. Intraperitoneal administration of coumarin causes tissue-selective depletion of cytochromes P450 and cytotoxicity in the olfactory mucosa. Toxicol. Appl. Pharmacol. 146:1997;134-143
11. Wong H.L., Murphy S.E., Hecht S.S. Preferential metabolic activation of N-nitrosopiperidine as compared to its structural homologue N-nitrosopyrrolidine by rat nasal mucosal microsomes. Chem. Res. Toxicol. 16:2003;1298-1305
12. Hong J.Y., Ding X., Smith T.J., Coon M.J., Yang C.S. Metabolism of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK), a tobacco-specific carcinogen, by rabbit nasal microsomes and cytochrome P450s NMa and NMb. Carcinogenesis. 13:1992;2141-2144
13. Gervasi P.G., Longo V., Naldi F., Panattoni G., Ursino F. Xenobiotic-metabolizing enzymes in human respiratory nasal mucosa. Biochem. Pharmacol. 41:1991;177-184
14. Liu C., Zhuo X., Gonzalez F.J., Ding X. Baculovirus-mediated expression and characterization of rat CYP2A3 and human CYP2A6: role in metabolic activation of nasal toxicants. Mol. Pharmacol. 50:1996;781-788
15. Thornton-Manning J.R., Nikula K.J., Hotchkiss J.A., Avila K.J., Rohrbacher K.D., Ding X., Dahl A.R. Nasal cytochrome P450 2A: identification, regional localization, and metabolic activity toward hexamethylphosphoramide, a known nasal carcinogen. Toxicol. Appl. Pharmacol. 142:1997;22-30
16. Su T., Bao Z., Zhang Q.-Y., Smith T.J., Hong J.Y., Ding X. Human cytochrome P450 CYP2A13: predominant expression in the respiratory tract and its high efficiency metabolic activation of a tobacco-specific carcinogen, 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Cancer Res. 60:2000;5074-5079
17. Schiffman S.S. Taste and smell in disease (first of two parts). N. Engl. J. Med. 308:1983;1275-1279
18. Spielman A.I. Chemosensory function and dysfunction. Crit. Rev. Oral Biol. Med. 9:1998;267-291
19. Calderongarciduenas L., Osnaya N., Rodriguezalcaraz A., Villarrealcalderon A. DNA damage in nasal respiratory epithelium from children exposed to urban pollution. Environ. Mol. Mutagen. 30:1997;11-20
20. Calderon-Garciduenas L., Valencia-Salazar G., Rodriguez-Alcaraz A., Gambling T.M., Garcia R., Osnaya N., Villarreal-Calderon A., Devlin R.B., Carson J.L. Ultrastructural nasal pathology in children chronically and sequentially exposed to air pollutants. Am. J. Resp. Cell. Mol. Biol. 24:2001;132-138
21. Ayiomamitis A., Parker L., Havas T. The epidemiology of malignant neoplasm of the nasal cavities, the paranasal sinuses and the middle ear in Canada. Arch. Otorhinolaryngol. 244:1988;367-371
22. Tisch M., Lohneier A., Schmezer P., Bartsch H., Maier H. Genotoxic effect of the insecticides pentachlorphenol and lindane on human nasal mucosal epithelium. Deutsche Medizinische Wochenschrift. 126:2001;1480-1486
23. Tisch M., Schmezer P., Faulde M., Groh A., Maier H. Genotoxicity studies on permethrin, DEET and diazinon in primary human nasal mucosal cells. Eur. Arch. Oto-Rhino-Laryngol. 259:2002;150-153
24. Chen Y., Liu Y.Q., Su T., Ren X., Shi L., Liu D., Gu J., Zhang Q.-Y., Ding X. Immunoblot analysis and immunohistochemical characterization of CYP2A expression in human olfactory mucosa. Biochem. Pharmacol. 66:2003;1245-1251
25. Harkema J.R. Comparative aspects of nasal airway anatomy: relevance to inhalation toxicology. Toxicol. Pathol. 19:1991;321-336
26. Leopold D.A., Hummel T., Schwob J.E., Hong S.C., Knecht M., Kobal G. Anterior distribution of human olfactory epithelium. Laryngoscope. 110:2000;417-421
27. Paik S.I., Lehman M.N., Seiden A.M., Duncan H.J., Smith D.V. Human olfactory biopsy. The influence of age and receptor distribution. Arch. Otolaryngol. Head Neck Surg. 118:1992;731-738
28. Zhuo X., Gu J., Behr M.J., Swiatek P.J., Cui H., Zhang Q.-Y., Xie Y., Collins D.N., Ding X. Targeted disruption of the olfactory mucosa-specific Cyp2g1 gene: impact on acetaminophen toxicity in the lateral nasal gland, and tissue-selective effects on Cyp2a5 expression. J. Pharmacol. Exp. Ther. 308:2004;719-728
29. Persson E., Larsson P., Tjalve H. Cellular activation and neuronal transport of intranasally instilled benzo(a)pyrene in the olfactory system of rats. Toxicol. Lett. 133:2002;211-219
30. Ghantous H., Dencker L., Gabrielsson J., Danielsson B.R.G., Bergrnan K. Accumulation and turnover of metabolites of toluene and xylene in nasal mucosa and olfactory bulb in the mouse. Pharmacol. Toxicol. 66:1990;87-92
31. Genter M.B., Owens D.M., Deamer N.J. Distribution of microsomal epoxide hydrolase and glutathione S-transferase in the rat olfactory mucosa: relevance to distribution of lesions caused by systemically-administered olfactory toxicants. Chem. Sens. 20:1995;385-392
32. Genter M.B., Burman D.M., Dingeldein M.W., Clough I., Bolon B. Evolution of alachlor-induced nasal neoplasms in the Long-Evans rat. Toxicol. Pathol. 28:2000;770-781
33. Chen Y., Getchell M.L., Ding X., Getchell T.V. Immunolocalization of two cytochrome P450 isozymes in rat nasal chemosensory tissue. NeuroReport. 3:1992;749-752
34. Gu J., Dudley C., Su T., Spink D.C., Zhang Q.-Y., Moss R.L., Ding X. Cytochrome P450 and steroid hydroxylase activity in mouse olfactory and vomeronasal mucosa. Biochem. Biophys. Res. Commun. 266:1999;262-267
35. Sheng J., Guo J., Hua Z., Caggana M., Ding X. Characterization of human CYP2G genes: widespread loss-of-function mutations and genetic polymorphism. Pharmacogenetics. 10:2000;667-678
36. Su T., Sheng J.J., Lipinskas T.W., Ding X. Expression of CYP2A genes in rodent and human nasal mucosa. Drug Metab. Dispos. 24:1996;884-890
37. Su T., Zhang Q.-Y., Zhang J., Swiatek P., Ding X. Expression of the rat CYP2A3 gene in transgenic mice. Drug Metab. Dispos. 30:2002;548-552
38. Cruzan G., Carlson G.P., Johnson K.A., Andrews L.S., Banton M.I., Bevan C., Cushman J.R. Styrene respiratory tract toxicity and mouse lung tumors are mediated by CYP2F-generated metabolites. Regul. Toxicol. Pharmacol. 35:2002;308-319
39. National Toxicology Program, Toxicology and carcinogenesis studies of naphthalene (CAS No. 91-20-3) in B6C3F1 mice (inhalation studies), TR-410 (1992).
40. National Toxicology Program, Toxicology and carcinogenesis studies of naphthalene (CAS No. 91-20-3) in F344/N rats (inhalation studies), TR-500 (2000).
41. West J.A., Pakehham G., Morin D., Fleschner C.A., Buckpitt A.R., Plopper C.G. Inhaled naphthalene causes dose dependent Clara cell cytotoxicity in mice but not in rats. Toxicol. Appl. Pharmacol. 173:2001;114-119
42. Nef P., Larabee T.M., Kagimoto K., Meyer U.A. Olfactory-specific cytochrome P-450 (P-450olf1; IIG1) gene structure and developmental regulation. J. Biol. Chem. 265:1990;2903-2907
43. Lavery D.J., Lopez-Molina L., Margueron R., Fleury-Olela F., Conquet F., Schibler U., Bonfils C. Circadian expression of the steroid 15 alpha-hydroxylase (Cyp2a4) and coumarin 7-hydroxylase (Cyp2a5) genes in mouse liver is regulated by the PAR leucine zipper transcription factor DBP. Mol. Cell. Biol. 19:1999;6488-6499
44. Viitala P., Posti K., Lindfors A., Pelkonen O., Raunio H. cAMP mediated upregulation of CYP2A5 in mouse hepatocytes. Biochem. Biophys. Res. Commun. 280:2001;761-767
45. Ding X., Peng H.M., Coon M.J. Cytochromes P450 NMa, NMb (2G1), and LM4 (1A2) are differentially expressed during development in rabbit olfactory mucosa and liver. Mol. Pharmacol. 42:1992;1027-1032
46. Gu J., Su T., Chen Y., Zhang Q.-Y., Ding X. Expression of biotransformation enzymes in human fetal olfactory mucosa: potential roles in developmental toxicity. Toxicol. Appl. Pharmacol. 165:2000;158-162
47. Margalit T., Lancet D. Expression of olfactory receptor and transduction genes during rat development. Dev. Brain Res. 73:1993;7-16
48. Zhuo X., Schwob J.E., Swiatek P.J., Ding X. Mouse cyp2g1 gene: promoter structure and tissue-specific expression of a cyp2g1-lacZ fusion gene in transgenic mice. Arch. Biochem. Biophys. 391:2001;127-136
49. Getchell M.L., Chen Y., Ding X., Sparks D.L., Getchell T.V. Immunohistochemical localization of a cytochrome P-450 isozyme in human nasal mucosa: age-related trends. Ann. Otol. Rhinol. Laryngol. 102:1993;368-374
50. Genter M.B., Ali S.F. Age-related susceptibility to 3, 3′-iminodipropionitrile-induced olfactory mucosal damage. Neurobiol. Aging. 19:1998;569-574
51. T. Su, X. Ding, Regulation of the cytochrome P450 2A genes, Toxicol. Appl. Pharmacol., 2004, in press.
52. Genter M.B., Burman D.M., Vijayakumar S., Ebert C.L., Aronow B.J. Genomic analysis of alachlor-induced oncogenesis in rat olfactory mucosa. Physiol. Genomics. 12:2002;35-45
53. Weech M., Quash M., Walters E. Characterization of the mouse olfactory glutathione S-transferases during the acute phase response. J. Neurosci. Res. 73:2003;679-685
54. Schwob J.E., Youngentob S.L., Mezza R.C. Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. Comp. Neurol. 359:1995;15-37
55. Walters E., Buchheit K., Maruniak J.A. Receptor neuron losses result in decreased cytochrome P-450 immunoreactivity in associated non-neuronal cells of mouse olfactory mucosa. J. Neurosci. Res. 33:1992;103-111
56. Walters E., Buchheit K., Maruniak J.A. Olfactory cytochrome P-450 immunoreactivity in mice is altered by dichlobenil but preserved by metyrapone. Toxicology. 81:1993;113-122
57. Ding X., Koop D.R., Crump B.L., Coon M.J. Immunochemical identification of cytochrome P-450 isozyme 3a (P-450alc) in rabbit nasal and kidney microsomes and evidence for differential induction by alcohol. Mol. Pharmacol. 30:1986;370-378
58. Zhang J., Zhang Q.-Y., Guo J., Zhou Y., Ding X. Identification and functional characterization of a conserved, nuclear factor 1-like element in the proximal promoter region of CYP1A2 gene specifically expressed in the liver and olfactory mucosa. J. Biol. Chem. 275:2000;8895-8902
59. Gronostajski R.M. Roles of the NFI/CTF gene family in transcription and development. Gene. 249:2000;31-45
60. Pickwell G.V., Shih H., Quattrochi L.C. Interaction of upstream stimulatory factor proteins with an E-box located within the human CYP1A2 5′-flanking gene contributes to basal transcriptional gene activation. Biochem. Pharmacol. 65:2003;1087-1096
61. Nef P., Heldmann J., Lazard D., Margalit T., Jaye M., Hanukoglu I., Lancet D. O1factory-specific cytochrome P-450: cDNA cloning of a novel neuroepithelial enzyme possibly involved in chemoreception. J. Biol. Chem. 264:1989;6780-6785
62. Hua Z., Zhang Q.-Y., Su T., Lipinskas T.W., Ding X. cDNA cloning, heterologous expression, and characterization of mouse CYP2G1, an olfactory-specific steroid hydroxylase. Arch. Biochem. Biophys. 340:1997;208-214
63. Zhang J., Ding X. Identification and characterization of a novel tissue-specific transcriptional activating element in the 5′-flanking region of the CYP2A3 gene predominantly expressed in rat olfactory mucosa. J. Biol. Chem. 273:1998;23454-23462
64. Baumeister H., Gronostajski R.M., Lyons G.E., Margolis F.L. Identification of NFI-binding sites and cloning of NFI-cDNAs suggest a regulatory role for NFI transcription factors in olfactory neuron gene expression. Mol. Brain Res. 72:1999;65-79
65. Xie Y., Madelian V., Zhang J., Ling G., Ding X. Activation of the NPTA element of the CYP2A3 gene by NFI-A2, a nasal mucosa-selective nuclear factor 1 isoform. Biochem. Biophys. Res. Commun. 289:2001;1225-1228
66. Carr B.A., Wan J., Hines R.N., Yost G.S. Characterization of the human lung CYP2F1 gene and identification of a novel lung-specific binding motif. J. Biol. Chem. 278:2003;15473-15483
67. Bonifer C. Long-distance chromatin mechanisms controlling tissue-specific gene locus activation. Gene. 238:1999;277-289
68. Futscher B.W., Oshiro M.M., Wozniak R.J., Holtan N., Hanigan C.L., Duan H., Domann F.E. Role for DNA methylation in the control of cell type specific maspin expression. Nat. Genet. 31:2002;175-179
69. Hashimshony T., Zhang J., Keshet I., Bustin M., Cedar H. The role of DNA methylation in setting up chromatin structure during development. Nat. Genet. 34:2003;187-192
70. Vieira I., Sonnier M., Cresteil T. Developmental expression of CYP2E1 in the human liver, hypermethylation control of gene expression during the neonatal period. Eur. J. Biochem. 238:1996;476-483
71. Nakajima M., Iwanari M., Yokoi T. Effects of histone deacetylation and DNA methylation on the constitutive and TCDD-inducible expressions of the human CYP1 family in MCF-7 and HeLa cells. Toxicol. Lett. 144:2003;247-256
72. Fraser P., Grosveld F. Locus control regions, chromatin activation and transcription. Curr. Opin. Cell Biol. 10:1998;361-365
73. Hoffman S.M., Nelson D.R., Keeney D.S. Organization, structure and evolution of the CYP2 gene cluster on human chromosome 19. Pharmacogenetics. 11:2001;687-698
74. Wang H., Donley K.M., Keeney D.S., Hoffman S.M.G. Organization and evolution of the Cyp2 gene cluster on mouse chromosome 7, and comparison with the syntenic human cluster. Environ. Health Perspect. 111:2003;1835-1842
75. Hadley W.M., Dahl A.R., Benson J.M., Hahn F.F., McClellan R.O. Cytochrome P450 dependent monooxygenases in nasal epithelial membranes: effect of phenobarbital and benzo(A)pyrene. Proc. Western Pharmacol. Soc. 25:1982;197-199
76. Bond J.A. Some biotransformation enzymes responsible for polycyclic aromatic hydrocarbon metabolism in rat nasal turbinates: effects on enzyme activities of in vitro modifiers and intraperitoneal and inhalation exposure of rats to inducing agents. Cancer Res. 43:1983;4805-4811
77. Longo V., Citti L., Gervasi P.G. Biotransformation enzymes in nasal mucosa and liver of Sprague-Dawley rats. Toxicol. Lett. 44:1988;289-297
78. Ding X., Coon M.J. Induction of cytochrome P-450 isozyme 3a (P-450IIE1) in rabbit olfactory mucosa by ethanol and acetone. Drug Metab. Dispos. 18:1990;742-745
79. Longo V., Ingelman-Sundberg M. Acetone-dependent regulation of cytochromes P4502E1 and P4502B1 in rat nasal mucosa. Biochem. Pharmacol. 46:1993;1945-1951
80. Genter M.B., Deamer N.J., Cao Y., Levi P.E. Effects of P450 inhibition and induction on the olfactory toxicity of beta, beta′- iminodipropionitrile (IDPN) in the rat. J. Biochem. Toxicol. 9:1994;31-39
81. Hong J.Y., Pan J.M., Gonzalez F.J., Gelboin H.V., Yang C.S. The induction of a specific form of cytochrome P-450 (P-450j) by fasting. Biochem. Biophys. Res. Commun. 142:1987;1077-1083
82. Longo V., Ingelman-Sundberg M., Amato G., Salvetti A., Gervasi P.G. Effect of starvation and chlormethiazole on cytochrome P450s of rat nasal mucosa. Biochem. Pharmacol. 59:2000;1425-1432
83. Gillner M., Brittebo E.B., Brandt I., Soderkvist P., Appelgren L.E., Gustafsson J.A. Uptake and specific binding of 2, 3, 7, 8-tetrachlorodibenzo-p- dioxin in the olfactory mucosa of mice and rats. Cancer Res. 47:1987;4150-4159
84. Voigt J.M., Guengerich F.P., Baron J. Localization and induction of cytochrome P450 1A1 and aryl hydrocarbon hydroxylase activity in rat nasal mucosa. J. Histochem. Cytochem. 41:1993;877-885
85. Wardlaw S.A., Nikula K.J., Kracko D.A., Finch G.L., Thornton-Manning J.R., Dahl A.R. Effect of cigarette smoke on CYP1A1, CYP1A2 and CYP2B1/2 of nasal mucosae in F344 rats. Carcinogenesis. 19:1998;655-662
86. Smolowitz R.M., Schultz M.E., Stegeman J.J. Cytochrome P4501A induction in tissues, including olfactory epithelium, of topminnows (Poeciliopsis spp.) by waterborne benzo[a]pyrene. Carcinogenesis. 13:1992;2395-2402
87. Zhang Q.-Y., Ding X., Dunbar D., Cao L., Kaminsky L.S. Induction of rat small intestinal cytochrome P-450 2J4. Drug Metab. Dispos. 27:1999;1123-1127
88. Xie Q., Zhang Q.-Y., Zhang Y., Su T., Gu J., Kaminsky L.S., Ding X. Induction of mouse CYP2J by pyrazole in the eye, kidney, liver, lung, olfactory mucosa, and small intestine, but not in the heart. Drug Metab. Dispos. 28:2000;1311-1316
89. Genter M.B., Apparaju S., Desai P.B. Induction of olfactory mucosal and liver metabolism of lidocaine by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. J. Biochem. Mol. Toxicol. 16:2002;128-134
90. Imaoka S., Terano Y., Funae Y. Changes in the amount of cytochrome P450s in rat hepatic microsomes with starvation. Arch. Biochem. Biophys. 278:1990;168-178
91. Ronis M.J., Huang J., Longo V., Tindberg N., Ingelman-Sundberg M., Badger T.M. Expression and distribution of cytochrome P450 enzymes in male rat kidney: effects of ethanol. Biochem. Pharmacol. 55:1998;123-129
92. Koop D.R., Tierney D.J. Multiple mechanisms in the regulation of ethanol-inducible cytochrome P450IIE1. Bioessays. 12:1990;429-435
93. Song B.J., Veech R.L., Park S.S., Gelboin H.V., Gonzalez F.J. Induction of rat hepatic N-nitrosodimethylamine demethylase by acetone is due to protein stabilization. J. Biol. Chem. 264:1989;3568-3572
94. Winters D.K., Cederbaum A.I. Time course characterization of the induction of cytochrome P-450 2E1 by pyrazole and 4-methylpyrazole. Biochim. Biophys. Acta. 1117:1992;15-24
95. Su T., He W., Gu J., Lipinskas T.W., Ding X. Differential xenobiotic induction of CYP2A5 in mouse liver, kidney, lung, and olfactory mucosa. Drug Metab. Dispos. 26:1998;822-824
96. Maglich J.M., Stoltz C.M., Goodwin B., Hawkins-Brown D., Moore J.T., Kliewer S.A. Nuclear pregnane × receptor and constitutive androstane receptor regulate overlapping but distinct sets of genes involved in xenobiotic detoxification. Mol. Pharmacol. 62:2002;638-646
97. Aida K., Negishi M. Posttranscriptional regulation of coumarin 7-hydroxylase induction by xenobiotics in mouse liver: mRNA stabilization by pyrazole. Biochemistry. 30:1991;8041-8045
98. Hahnemann B., Salonpaa P., Pasanen M., Maenpaa J., Honkakoski P., Juvonen R., Lang M.A., Pelkonen O., Raunio H. Effect of pyrazole, cobalt and phenobarbital on mouse liver cytochrome P-450 2a-4/5 (Cyp2a-4/5) expression. Biochem. J. 286:1992;289-294
99. Geneste O., Raffalli F., Lang M.A. Identification and characterization of a 44 kDa protein that binds specifically to the 3′-untranslated region of CYP2a5 mRNA: inducibility. Biochem. J. 313:1996;1029-1037
100. Thulke-Gross M., Hergenhahn M., Tilloy-Ellul A., Lang M.A., Bartsch H. Pyrazole-inducible proteins in DBA/2 mouse liver bind with high affinity to the 3′-untranslated regions of the mRNAs of coumarin hydroxylase (CYP2A5) and c-jun. Biochem. J. 331:1998;473-481
101. Raffalli-Mathieu F., Glisovic T., Ben-David Y., Lang M.A. Heterogeneous nuclear ribonucleoprotein A1 and regulation of the xenobiotic-inducible gene Cyp2a5. Mol. Pharmacol. 61:2002;795-799
102. Tilloy-Ellul A., Raffalli-Mathieu F., Lang M.A. Analysis of RNA-protein interactions of mouse liver cytochrome P4502A5 mRNA. Biochem. J. 339:1999;695-703
103. Kimura S., Kozak C.A., Gonzalez F.J. Identification of a novel P450 expressed in rat lung: cDNA cloning and sequence, chromosome mapping, and induction by 3-methylcholanthrene. Biochemistry. 28:1989;3798-3803
104. Robottom-Ferreira A.B., Aquino S.R., Queiroga R., Albano R.M., Pinto L.F.R. Expression of CYP2A3 mRNA and its regulation by 3-methylcholanthrene, pyrazole, and beta-ionone in rat tissues. Braz. J. Med. Biol. Res. 36:2003;839-844
105. Bereziat J.C., Raffalli F., Schmezer P., Frei E., Geneste O., Lang M.A. Cytochrome P450 2A of nasal epithelium: regulation and role in carcinogen metabolism. Mol. Carcinog. 14:1995;130-139
106. Blanchard K.T., Morris J.B. Effects of m-xylene on rat nasal cytochrome P450 mixed function oxidase activities. Toxicol. Lett. 70:1994;253-259
107. Zhuo X.L., Gu J., Zhang Q.-Y., Spink D.C., Kaminsky L.S., Ding X. Biotransformation of coumarin by rodent and human cytochromes P-450: metabolic basis of tissue-selective toxicity in olfactory mucosa of rats and mice. J. Pharmacol. Exp. Ther. 288:1999;463-471
108. Wang H., Tan W., Hao B., Miao X., Zhou G., He F., Lin D. Substantial reduction in risk of lung adenocarcinoma associated with genetic polymorphism in CYP2A13, the most active cytochrome P450 for the metabolic activation of tobacco-specific carcinogen NNK. Cancer Res. 63:2003;8057-8061
109. Gresham L.S., Molgaard C.A., Smith R.A. Induction of cytochrome P-450 enzymes via tobacco smoke: a potential mechanism for developing resistance to environmental toxins as related to parkinsonism and other neurologic diseases. Neuroepidemiology. 12:1993;114-116