Function and regulation of the CYP2A5/CYP2A6 genes in response to toxic insults in the liver

Current Drug Metabolism

Volumn 14, Issue 1, 2013, Pages 137-150

  Abu Bakar, A'edah ^a   Hakkola, Jukka ^b   Juvonen, Risto ^c   Rahnasto Rilla, Minna ^c   Raunio, Hannu ^c   Lang, Matti A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF OULU   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

AhR; CYP2A5; CYP2A6; Gene regulation; Hepatotoxicity; HnRNP A1; Nrf2; Oxidative stress; PGC 1

Indexed keywords

1,3 BUTADIENE; AFLATOXIN B1; AROMATIC HYDROCARBON RECEPTOR; CHLOROFORM; COUMARIN; CYTOCHROME P450 2A5; CYTOCHROME P450 2A6; DICHLOBENIL; DIETHYLNITROSAMINE; EFAVIRENZ; ENZYME INDUCING AGENT; ENZYME INHIBITOR; GIMERACIL PLUS OTERACIL POTASSIUM PLUS TEGAFUR; HALOTHANE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENOUS RIBONUCLEOPROTEIN A1; INDOLE; LETROZOLE; LOSIGAMONE; MENTHOL; MESSENGER RNA; NICOTINE; PARAXANTHINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; QUINOLINE; TEGAFUR; TERT BUTYL METHYL ETHER; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; VALPROIC ACID; XENOBIOTIC AGENT;

ALCOHOL LIVER DISEASE; ARTICLE; BACTERIAL HEPATITIS; CATALYSIS; DRUG METABOLISM; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE CONTROL; GENE FUNCTION; GENETIC POLYMORPHISM; HEPATITIS; HUMAN; LIVER CELL CARCINOMA; LIVER INJURY; LIVER TOXICITY; MALARIA; MOLECULAR MODEL; NONHUMAN; OXIDATIVE STRESS; PARASITIC HEPATITIS; PRENEOPLASTIC LIVER LESION; SMOKING; TRANSCRIPTION REGULATION; VIRUS HEPATITIS;

EID: 84871281717     PISSN: 13892002     EISSN: 18755453     Source Type: Journal    
DOI: 10.2174/138920013804545223     Document Type: Article

References (179)

1. Kirischian, N.; McArthur, A. G.; Jesuthasan, C.; Krattenmacher, B.; Wilson, J. Y. Phylogenetic and functional analysis of the vertebrate cytochrome P450 2 family. J. Mol. Evol., 2011, 72, 561-571.
2. Raunio, H.; Hakkola, J.; Pelkonen, O. In: Cytochrome P450 - Role in Metabolism and Toxicity of Drugs and Other Xenobiotics, Ioannides C., Ed.; ACS Publishing: Cambridge, 2008; pp. 151-171.
3. Hoffman, S. M.; Nelson, D. R.; Keeney, D. S. Organization, structure and evolution of the CYP2 gene cluster on human chromosome 19. Pharmacogenetics, 2001, 11, 687-698.
4. Hoffman, S. M.; Fernandez-Salguero, P.; Gonzalez, F. J.; Mohrenweiser, H. W. Organization and evolution of the cytochrome P450 CYP2A-2B-2F subfamily gene cluster on human chromosome 19. J. Mol. Evol., 1995, 41, 894-900.
5. 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., 1995, 14, 130-139.
6. Su, T.; Sheng, J. J.; Lipinskas, T. W.; Ding, X. Expression of CYP2A genes in rodent and human nasal mucosa. Drug Metabol. Dispos., 1996, 24, 884-890.
7. Xie, F.; Zhou, X.; Genter, M. B.; Behr, M.; Gu, J.; Ding, X. The tissue-specific toxicity of methimazole in the mouse olfactory mucosa is partly mediated through target-tissue metabolic activation by CYP2A5. Drug Metab. Dispos., 2011, 39, 947-951.
8. Piras, E.; Franzén, A.; Fernández, E.; Bergström, U.; Raffalli-Mathieu, F.; Lang, M.; Brittebo, E. Cell-specific expression of CYP2A5 in the mouse respiratory tract: effects of olfactory toxicants. J. Histochem. Cytochem., 2003, 51, 1545-1555.
9. Honkakoski, P.; Kojo, A.; Raunio, H.; Pasanen, M.; Juvonen, R.; Lang, M. A. Hepatic mitochondrial coumarin 7-hydroxylase: Comparison with the microsomal enzyme. Arch. Biochem. Biophys., 1988, 267, 558-567.
10. Genter, M. B.; Clay, C. D.; Dalton, T. P.; Dong, H.; Nebert, D. W.; Shertzer, H. G. Comparison of mouse hepatic mitochondrial versus microsomal cytochrome P450 following TCDD treatment. Biochem. Biophys. Res. Commun., 2006, 342, 1375-1381.
11. Koskela, S.; Hakkola, J.; Hukkanen, J.; Pelkonen, O.; Sorri, M.; Saranen, A.; Anttila, S.; Fernandez-Salguero, P.; Gonzalez, F.; Raunio, H. Expression of CYP2A genes in human liver and extrahepatic tissue. Biochem. Pharmacol., 1999, 57, 1407-1413.
12. Saeki, M.; Saito, Y.; Nagano, M.; Teshima, R.; Ozawa, S.; Sawada, J. mRNA expression of multiple cytochrome P450 isozymes in four types of cultured skin cells. Int. Arch. Allergy Immunol., 2002, 127, 333-336.
13. Janmohamed, A.; Dolphin, C. T.; Phillips, I. R.; Shephard, E. A. Quantification and cellular localization of expression in human skin of genes encoding flavin-containing monooxygenases and cytochromes P450. Biochem. Pharmacol., 2001, 62, 777-786.
14. Yun, C. H.; Shimada, T.; Guengerich, F. P. Purification and characterization of human liver microsomal cytochrome P-450 2A6. Mol. Pharmacol., 1991, 40, 679-685.
15. Godoy, W.; Albano, R. M.; Moraes, E. G.; Pinho, P. R. A.; Nunes, R. A.; Saito, E. H.; Higa, C.; Filho, I. M.; Kruel, C. D. P.; Schrimer, C. C.; Gurski, R.; Lang, M. A.; Pinto, L. F. R. CYP2A6/CYP2A7 and CYP2E1 expression in human oesophageal mucosa: regional and inter-individual variation in expression and relevance to nitrosamine metabolism. Carcinogenesis, 2002, 23, 611-616.
16. Zhang, X.; D'Agostino, J.; Wu, H.; Zhang, Q. Y.; von Weymarn, L.; Murphy, S. E.; Ding, X. CYP2A13: variable expression and role in human lung microsomal metabolic activation of the tobaccospecific carcinogen 4-(methylnitrosamino)-1- (3-pyridyl)-1-butanone. J. Pharmacol. Exp. Ther., 2007, 323, 570-578.
17. Su, T.; Ding, X. Regulation of the cytochrome P450 2A genes. Toxicol. Appl. Pharmacol., 2004, 199, 285-294.
18. Hakkola, J.; Tanaka, E.; Pelkonen, O. Developmental expression of cytochrome P450 enzymes in human liver. Pharmacol. Toxicol., 1998, 82, 209-217.
19. Gonzalez, F. J.; Matsunaga, T.; Nagata, K. Structure and regulation of P-450s in the rat P450IIA gene subfamily. Drug Metab. Rev., 1989, 20, 827-837.
20. Imaoka, S.; Fujita, S.; Funae, Y. Age-dependent expression of cytochrome P-450s in rat liver. Biochim. Biophys. Acta, 1991, 1097, 187-192.
21. 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., 2000, 165, 158-162.
22. Chen, Y.; Liu, Y.; 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., 2003, 66, 1245-1251.
23. Hukkanen, J.; Jacob, Pr.; Benowitz, N. L. Metabolism and disposition kinetics of nicotine. Pharmacol. Rev., 2005, 57, 79-115.
24. Kirby, G. M.; Nichols, K. D.; Antenos, M. CYP2A5 induction and hepatocellular stress: An adaptive response to perturbations of heme homeostasis. Curr. Drug Metab., 2011, 12, 186-197.
25. Abu-Bakar, A.; Arthur, D. M.; Aganovic, S.; Ng, J. C.; Lang, M. A. Inducible bilirubin oxidase: A novel function for the mouse cytochrome P450 2A5. Toxicol. Appl. Pharmacol., 2011, 257, 14-22.
26. Abu-Bakar, A.; Arthur, D. M.; Wikman, A. S.; Rahnasto, M.; Juvonen, R. O.; Vepsalainen, J.; Raunio, H.; Ng, J. C.; Lang, M. A. Metabolism of bilirubin by human cytochrome P450 2A6. Toxicol. Appl. Pharmacol., 2012, 261, 50-58.
27. Otyepka, M.; Skopalík, J.; Anzenbacherová, E.; Anzenbacher, P. What common structural features and variations of mammalian P450s are known to date? Biochim. Biophys. Acta, 2007, 1770, 376-389.
28. Yano, J. K.; Hsu, M. H.; Griffin, K. J.; Stout, C. D.; Johnson, E. F. Structures of human microsomal cytochrome P450 2A6 complexed with coumarin and methoxsalen. Nat. Struct. Mol. Biol., 2005, 12, 822-823.
29. Yano, J. K.; Denton, T. T.; Cerny, M. A.; Zhang, X.; Johnson, E. F.; Cashman, J. R. Synthetic inhibitors of cytochrome P-450 2A6: inhibitory activity, difference spectra, mechanism of inhibition, and protein cocrystallization. J. Med. Chem., 2006, 19, 6987-7001.
30. Smith, B. D.; Sanders, J. L.; Porubsky, P. R.; Lushington, G. H.; Stout, C. D.; Scott, E. E. Structure of the human lung cytochrome P450 2A13. J. Biol. Chem., 2007, 282, 17306-17313.
31. He, X. Y.; Shen, J.; Hu, W. Y.; Ding, X.; Lu, A. Y.; Hong, J. Y. Identification of Val117 and Arg372 as critical amino acid residues for the activity difference between human CYP2A6 and CYP2A13 in coumarin 7-hydroxylation. Arch. Biochem. Biophys., 2004, 427, 143-153.
32. Kim, D.; Wu, Z. L.; Guengerich, F. P. Analysis of coumarin 7-hydroxylation activity of cytochrome P450 2A6 using random mutagenesis. J. Biol. Chem., 2005, 280, 40319-40327.
33. Negishi, M.; Iwasaki, M.; Juvonen, R. O.; Sueyosthi, T.; Darden, T. A.; Pedersen, L. G. Structural flexibility and functional versatility of cytochrome P450 and rapid evolution. Mut. Res., 1996, 350:43-50.
34. Lindberg, R. L.; Negishi, M. Alteration of mouse cytochrome P450coh substrate specificity by mutation of a single amino-acid residue. Nature, 1989, 339, 632-634.
35. Raunio, H.; Rautio, A.; Gullstén, H.; Pelkonen, O. Polymorphisms of CYP2A6 and its practical consequences. Br. J. Clin. Pharmacol., 2001, 52, 357-363.
36. Rendic, C. Summary of information on human CYP enzymes: human P450 metabolism data. Drug Metab. Rev., 2002, 34, 83-448.
37. *17) polymorphisms are independent predictors of efavirenz plasma concentrations in HIV-infected patients. Br. J. Clin. Pharmacol., 2009, 67, 427-436.
38. Blum, M.; Suzuki, A.; Ajani, J. A. A comprehensive review of S-1 in the treatment of advanced gastric adenocarcinoma. Future Oncol., 2011, 7, 715-726.
39. di Julio, J.; Fayet, A.; Arab-Alameddine, M.; Rotger, M.; Lubomirov, R.; Cavassini, M.; Furrer, H.; Günthard, H. F.; Colombo, S.; Csajka, C.; Eap, C. B.; Decosterd, L. A.; Telenti, A. Swiss HIV cohort study. In vivo analysis of efavirenz metabolism in individuals with impaired CYP2A6 function. Pharmacogenet. Genomics, 2009, 19, 300-309.
40. Miyazawa, M.; Marumoto, S.; Takahashi, T.; Nakahashi, H.; Haigou, R.; Nakanishi, K. Metabolism of (+) - and (-)-menthols by CYP2A6 in human liver microsomes. J. Oleo. Sci., 2011, 60, 127-132.
41. Miyazaki, M.; Yamazaki, H.; Takeuchi, H.; Saoo, K.; Yokohira, M.; Masumura, K.; Nohmi, T.; Funae, Y.; Imaida, K.; Kamataki, T. Mechanisms of chemopreventive effects of 8-methoxypsoralen against 4-(methylnitrosamino)-1 - (3-pyridyl)-1-butanone-induced mouse lung adenomas. Carcinogenesis, 2005, 26, 1947-1955.
42. Yamazaki, H.; Inui, Y.; Yun, C. H.; Guengerich, F. P.; Shimada, T. Cytochrome P450 2E1 and 2A6 enzymes as major catalysts for metabolic activation of N-nitrosodialkylamines and tobacco-related nitrosamines in human liver microsomes. Carcinogenesis, 1992, 13, 1789-1794.
43. Kushida, H.; Fujita, K.; Suzuki, A.; Yamada, M.; Endo, T.; Nohmi, T.; Kamataki, T. Metabolic activation of N-alkylnitrosamines in genetically engineered Salmonella typhimurium expressing CYP2E1 or CYP2A6 together with human NADPH-cytochrome P450 reductase. Carcinogenesis, 2000, 21, 1227-1232.
44. Fujita, K.; Kamataki, T. Role of human cytochrome P450 (CYP) in the metabolic activation of N-alkylnitrosamines: application of genetically engineered Salmonella typhimurium YG7108 expressing each form of CYP together with human NADPH-cytochrome P450 reductase. Mutat. Res., 2001, 483, 35-41.
45. Hecht, S. S. Progress and challenges in selected areas of tobacco carcinogenesis. Chem. Res. Toxicol, 2008, 21, 160-171.
46. Wastl, U. M.; Rossmanith, W.; Lang, M. A.; Camus-Randon, A. M.; Grasl-Kraupp, B.; Bursch, W.; Schulte-Hermann, R. Expression of cytochrome P450 2A5 in preneoplastic and neoplastic mouse liver lesions. Mol. Carcinog., 1998, 22, 229-234.
47. Pelkonen, P.; Lang, M. A.; Negishi, M.; Wild, P. C.; Juvonen, R. O. Interaction of aflatoxin B1 with cytochrome P450 2A5 and its mutants: correlation with metabolic activation and toxicity. Chem. Res. Toxicol, 1997, 10, 85-90.
48. Pelkonen, P.; Lang, M. A.; Wild,. CP.; Negishi, M.; Juvonen, R. O. Activation of aflatoxin B1 by mouse CYP2A enzymes and cytotoxicity in recombinant yeast cells. Eur. J. Pharmacol, 1994, 292, 67-73.
49. Kirby, G. M.; Chemin, I.; Montesano, R.; Chisari, F. V.; Lang, M. A.; Wild, C. P. Induction of specific cytochrome P450 involved in aflatoxin B1 metabolism in hepatitis B virus transgenic mice. Mol. Carcinog., 1994, 11, 74-80.
50. Kirby, G. M.; Pelkonen, O.; Vatanasapt, V.; Camus, A. M.; Wild, C. P.; Lang, M. A. Association of liver fluke (Opisthorchis viverrini) infestation with increased expression of cytochrome P450 and carcinogen metabolism in male hamster liver. Mol. Carcinog., 1994, 11, 81-89.
51. Satarug, S.; Lang, M. A.; Yongvanit, P.; Sithithaworn, P.; Mairiang, E.; Mairiang, P.; Pelkonen, P.; Bartsch, H.; Haswell-Elkins, M. R. Induction of cytochrome P450 2A6 expression in humans by the carcinogenic parasite infection, Opisthorchiasis viverrini. Cancer Epidemiol. Biomarkers Prev., 1996, 5, 795-800.
52. Murphy, S. E.; Raulinaitis, V.; Brown, K. M. Nicotine 5'-oxidation and methyl oxidation by P450 2A enzymes. Drug Metab. Dispos., 2005, 33, 1166-1173.
53. Nakajima, M.; Itoh, M.; Yamanaka, H.; Fukami, T.; Tokudome, S.; Yamamoto, Y.; Yamamoto, H.; Yokoi, T. Isoflavones inhibit nicotine C-oxidation catalyzed by human CYP2A6. J. Clin. Pharmacol, 2006, 46, 337-344.
54. Rahnasto, M.; Wittekindt, C; Juvonen, R. O.; Turpeinen, M.; Petsalo, A.; Pelkonen, O.; Poso, A.; Stahl, G.; Höltje, H. D.; Raunio, H. Identification of inhibitors of the nicotine metabolising CYP2A6 enzyme: an in silico approach. Pharmacogenomics J., 2008, 8, 328-338.
55. Siu, E. C.; Tyndale, R. F. Selegiline is a mechanism-based inactivator of CYP2A6 inhibiting nicotine metabolism in humans and mice. J. Pharmacol. Exp. Ther., 2008, 324, 992-999.
56. Nakahashi, H.; Miyazawa, M. Biotransformation of (-)-camphor by Salmonella typhimurium OY1002/2A6 expressing human CYP2A6 and NADPH-P450 reductase. J. Oleo. Sci., 2011, 60, 545-548.
57. Ueng, Y. F.; Chen, C. C.; Chung, Y. T.; Liu, T. Y.; Chang, Y. P.; Lo, W. S.; Murayama, N.; Yamazaki, H.; Soucek, P.; Chau, G. Y.; Chi, C. W.; Chen, R. M.; Li, D. T. Mechanism-based inhibition of cytochrome P450 (CYP) 2A6 by chalepensin in recombinant systems, in human liver microsomes and in mice in vivo. Br. J. Pharmacol., 2011, 163, 1250-1262.
58. Denton, T. T.; Zhang, X.; Cashman, J. R. 5-substituted, 6-substituted, and unsubstituted 3-heteroaromatic pyridine analogues of nicotine as selective inhibitors of cytochrome P-450 2A6. J. Med. Chem., 2005, 48, 224-239.
59. Rahnasto, M.; Raunio, H.; Poso, A.; Juvonen, R. O. More potent inhibition of human CYP2A6 than mouse CYP2A5 enzyme activities by derivatives of phenylethylamine and benzaldehyde. Xenobiotica, 2003, 33, 529-539.
60. Rahnasto, M.; Raunio, H.; Poso, A.; Wittekindt, C.; Juvonen, R. O. Quantitative structure-activity relationship analysis of inhibitors of the nicotine metabolizing CYP2A6 enzyme. J. Med. Chem., 2005, 48, 440-449.
61. Siu, E. C.; Tyndale, R. F. Non-nicotinic therapies for smoking cessation. Annu. Rev. Pharmacol. Toxicol., 2007, 47, 541-564.
62. Raunio, H.; Pokela, N.; Puhakainen, K.; Rahnasto, M.; Mauriala, T.; Auriola, S.; Juvonen, R. O. Nicotine metabolism and urinary elimination in mouse: in vitro and in vivo. Xenobiotica, 2008, 38, 34-47.
63. Zhou, X.; Zhuo, X.; Xie, F.; Kluetzman, K.; Shu, Y. Z.; Humphreys, W. G.; Ding, X. Role of CYP2A5 in the clearance of nicotine and cotinine: insights from studies on a Cyp2a5-null mouse model. J. Pharmacol. Exp. Ther., 2010, 332, 578-587.
64. Poso, A.; Gynther, J.; Juvonen, R. A comparative molecular field analysis of cytochrome P450 2A5/2A6 inhibitors. J. Computer-Aided Mol. Design, 2001, 15, 195-202.
65. Lewis, D. F.; Lake, B. G. Molecular modelling of members of the P4502A subfamily: application to studies of enzyme specificity. Xenobiotica, 1995, 25, 585-598.
66. Lewis, D. F.; Ito, Y.; Lake, B. G. Metabolism of coumarin by human P450s: a molecular modelling study. Toxciol. In Vitro, 2006, 20, 256-264.
67. Lewis, D. F.; Lake, B. G.; Dickins, M.; Goldfarb, P. S. Homology modelling of CYP2A6 based on the CYP2C5 crystallographic template: enzyme-substrate interactions and QSARs for binding affinity and inhibition. Toxicol. In Vitro, 2003, 17, 179-190.
68. Jalas, J. R.; Seetharaman, M.; Hecht, S. S.; Murphy, S. E. Molecular modelling of CYP2A enzymes: application to metabolism of the tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl) - 1-butanone (NNK). Xenobiotica, 2004, 34, 515-533.
69. Asikainen, A.; Tarhanen, J.; Poso, A.; Pasanen, M.; Alhava, E.; Juvonen, R. O. Predictive value of comparative molecular field analysis modelling of naphthalene inhibition of human CYP2A6 and mouse CYP2A5 enzymes. Toxicol. In Vitro, 2003, 17, 449-455.
70. Rahnasto, M. K.; Raunio, H. A.; Wittekindt, C.; Salminen, K. A.; Leppänen, J.; Juvonen, R. O.; Poso, A.; Lahtela-Kakkonen, M. K. Identification of novel CYP2A6 inhibitors by virtual screening. Bioorg. Med. Chem., 2011, 19, 7186-7193.
71. Di, Y. M.; Chow, V. D-W.; Yang, L-P.; Zhou, S-F. Structure, function, regulation and polymorphism of human cytochrome P450 2A6. Curr. Drug. Metab., 2009, 10, 754-780.
72. Dempsey, D.; Tutka, P.; Jacob, Pr.; Allen, F.; Schoedel, K.; Tyndale, R. F.; Benowitz, N. L. Nicotine metabolite ratio as an index of cytochrome P450 2A6 metabolic activity. Clin. Pharmacol. Ther., 2004, 76, 64-72.
73. Schoedel, K. A.; Hoffman, E. B.; Rao, Y.; Sellers, E. M.; Tyndale, R. F. Ethnic variation in CYP2A6 and association of genetically slow nicotine metabolism and smoking in adult Caucasians. Pharmacogenetics, 2004, 14, 615-626.
74. Rossini, A.; Simao, T. A.; Albano, R. M.; Pinto, L. F. R. CYP2A6 polymorphisms and risk for tobacco-related cancers. Pharmacogenomics, 2008, 9, 1737-1752.
75. Nakajima, M. Smoking behavior and related cancers: the role of CYP2A6 polymorphisms. Curr. Opin. Mol. Ther., 2007, 9, 538-544.
76. Kamataki, T.; Fujieda, M.; Kiyotani, K.; Iwano, S.; Kunitoh, H. Genetic polymorphism of CYP2A6 as one of the potential determinants of tobacco-related cancer risk. Biochem. Biophys. Res. Commun., 2005, 338, 306-310.
77. Rodriguez-Antona, C.; Gomez, A.; Karlgren, M.; Sim, S. C.; Ingelman-Sundberg, M. Molecular genetics and epigenetics of the cytochrome P450 gene family and its relevance for cancer risk and treatment. Human Genet., 2010, 127, 1-17.
78. Thorgeirsson, T. E.; Gudbjartsson, D. F.; Surakka, I.; Vink, J. M.; Amin, N.; Geller, F.; Sulem, P.; Rafnar, T.; Esko, T., Walter, S.; Gieger, C.; et al. Sequence variants at CHRNB3-CHRNA6 and CYP2A6 affect smoking behavior. Nat. Genet., 2010, 42, 448-453.
79. Wassenaar, C. A.; Dong, Q.; Wei, Q.; Amos, C. I.; Spitz, M. R.; Tyndale, R. F. Relationship between CYP2A6 and CHRNA5-CHRNA3-CHRNB4 variation and smoking behaviors and lung cancer risk. J. Natl. Cancer Inst., 2011, 103, 1342-1346.
80. Zhang, X.; Amemo, K.; Ameno, S.; Iwahashi, K.; Kinoshita, H.; Kubota, T.; Mostofa, J.; Ijiri, I. Lack of association between smoking and CYP2A6 gene polymorphisms in a Japanese population. Nihon Arukoru Yakubutsu Igakkai Zasshi, 2001, 36, 486-490.
81. Loriot, M. A.; Rebuissou, S.; Oscarson, M.; Cenée, S.; Miyamoto, M.; Ariyoshi, N.; Kamataki, T.; Hémon, D.; Beaune, P.; Stücker, I. Genetic polymorphisms of cytochrome P450 2A6 in a case-control study on lung cancer in a French population. Pharmacogenetics, 2001, 11, 39-44.
82. Ando, M.; Hamajima, N.; Ariyoshi, N.; Kamataki, T.; Matsuo, K.; Ohno, Y. Association of CYP2A6 gene deletion with cigarette smoking status in Japanese adults. J. Epidemiol., 2003, 13, 176-181.
83. Khokhar, J. Y.; Ferguson, C. S.; Zhu, A. Z.; Tyndale, R. F. Pharmacogenetics of drug dependence: role of gene variations in susceptibility and treatment. Annu. Rev. Pharmacol. Toxicol., 2010, 50, 39-61.
84. Malaiyandi, V.; Lerman, C.; Benowitz, N. L.; Jepson, C.; Patterson, F.; Tyndale, R. F. Impact of CYP2A6 genotype on pretreatment smoking behaviour and nicotine levels from and usage of nicotine replacement therapy. Mol. Psychiatry., 2006, 11, 400-409.
85. Strasser, A. A.; Malaiyandi, V.; Hoffman, E.; Tyndale, R. F.; Lerman, C. An association of CYP2A6 genotype and smoking topography. Nictoine Tob. Res., 2007, 9, 511-518.
86. Tyndale, R. F.; Sellers, E. M. Variable CYP2A6-mediated nicotine metabolism alters smoking behavior and risk. Drug Metab. Dispos., 2001, 29, 548-552.
87. Camus-Randon, A. M.; Raffalli, F.; Bereziat, J. C.; McGregor, D.; Konstandi, M.; Lang, M. A. Liver injury and expression of cytochromes P450: evidence that regulation of CYP2A5 is different from that of other major xenobiotic metabolizing CYP enzymes. Toxicol. Appl. Pharmacol., 1996, 138. 140-148.
88. Abu-Bakar, A.; Satarug, S.; Marks, G. C.; Lang, M. A.; Moore, M. R. Acute cadmium chloride administration induces hepatic and renal CYP2A5 mRNA, protein and activity in the mouse: involvement of transcription factor NRF2. Toxicol. Lett., 2004, 148, 199-210.
89. Juvonen, R.; Autio, S.; Lang, M. A. Pyrazole as a modifier of liver microsomal monooxygenase in DBA/2N and AKR/J mice. Biochem. Pharmacol., 1987, 36, 3993-3997.
90. Donato, M. T.; Viitala, P.; Rodriguez-Antona, C.; Lindfors, A.; Castell, J. V.; Raunio, H.; Gomez-Lechon, M. J.; Pelkonen, O. Cyp2a5/2a6 expression in mouse and human hepatocytes treated with various in vivo inducers. Drug Metab. Dispos., 2000, 28, 1321-1326.
91. Salonpaa, P.; Iscan, M.; Pasanen, M.; Arvela, P.; Pelkonen, O.; Raunio, H. Cerium-induced strain-dependent increase in Cyp2a-4/5 (cytochrome P4502a-4/5) expression in the liver and kidneys of inbred mice. Biochem. Pharmacol., 1992, 44, 1269-1274.
92. Seubert, J. M.; Webb, C. D.; Bend, J. R. Acute sodium arsenite treatment induces Cyp2a5 but not cyp1a1 in the C57Bl/6 mouse in a tissue (kidney) selective manner. J. Biochem. Mol. Toxicol., 2002, 16, 96-106.
93. Chemin, I.; Takahashi, S.; Belloc, C.; Lang, M. A.; Ando, K.; Guidotti, L. G.; Chisari, F. V.; Wild, C. P. Differential induction of carcinogen metabolizing enzymes in a transgenic mouse model of fulminant hepatitis. Hepatology, 1996, 24, 649-656.
94. Chomarat, P.; Sipowicz, M. A.; Diwan, B. A.; Fornwald, L. W.; Awasthi, Y. C.; Anver, M. R.; Rice, J. M.; Anderson, L. M.; Wild, C. P. Distinct time courses of increase in cytochrome P450 1A2, 2A5 and glutathione S-transferases during the progressive hepatitis associated with Helicobacter hepaticus. Carcinogenesis, 1997, 18, 2179-2190.
95. Sipowicz, M. A.; Chomarat, P.; Diwan, B. A.; Anver, M. R.; Awasthi, Y. C.; Ward, J. M.; Rice, J. M.; Kasprzak, K. S.; Wild, C. P.; Anderson, L. M. Increased oxidative DNA damage and hepatocytes overexpression of specific cytochrome P450 isoforms in hepatitis of mice infected with Helicobacter hepaticus. Am. J. Pathol., 1997, 151, 933-941.
96. Kobliakov, V.; Kulikova, L.; Samoilov, D.; Lang, M. A. High expression of cytochrome P450 2a-5 (coumarin 7-hydroxylase) in mouse hepatomas. Mol. Carcinog., 1993, 7, 276-280.
97. Jounaidi, Y.; Bonfils, C.; Perin, F.; Negishi, M.; Lange, R. Overexpression of a cytochrome P-450 of the 2a family (Cyp2a-5) in chemically induced hepatomas from male mice. Eur. J. Biochem., 1994, 219, 791-798.
98. Montero, R.; Gentile, G. J.; Frederick, L.; McMannis, J.; Murphy, T.; Silva, G.; Blankespoor, H.; Gentile, J. M. Induced expression of CYP2A5 in inflamed trematode-infested mouse liver. Mutagenesis, 1999, 14, 217-220.
99. Thai, S. F.; Allen, J. W.; DeAngelo, A. B.; George, M. H.; Fuscoe, J. C. Altered gene expression in mouse liver after trichloroacetic acid exposure. Mutat. Res., 2003, 543, 167-180.
100. Kirby, G. M.; Batist, G.; Alpert, L.; Lamoureux, E.; Cameron, R. G.; Alaoui-Jamali, M. A. Overexpression of cytochrome P-450 isoforms involved in aflatoxin B1 activation in human liver with cirrhosis and hepatitis. Toxicol. Pathol., 1996, 24, 458-467.
101. Raunio, H.; Juvenon, R.; Pasanen, M.; Pelkonen, O.; Paakko, P.; Soini, Y. Cytochrome P4502A6 (CYP2A6) expression in human hepatocellular carcinoma. Hepatology, 1998, 27, 427-432.
102. Niemela, O.; Parkkila, S.; Juvenon, R. O.; Viitala, K.; Gelbion, H. V.; Pasanen, M. Cytochromes P450 2A6, 2E1, and 3A and production of protein-aldehyde adducts in the liver of patients with alcoholic and non-alcoholic liver diseases. J. Hepatol., 2000, 33, 893-901.
103. Abu-Bakar, A.; Lämsä, V.; Arpiainen, S.; Moore, M. R.; Lang, M. A.; Hakkola, J. Regulation of CYP2A5 gene by the transcription factor nuclear factor (erythroid-derived 2)-like 2. Drug Metab. Dispos., 2007, 35, 787-794.
104. Alam, J.; Shibahara, S.; Smith, A. Transcriptional activation of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. J. Biol. Chem., 1989, 264, 6371-6375.
105. Beyersmann, D.; Hechtenberg, S. Cadmium, gene regulation, and cellular signalling in mammalian cells. Toxicol. Appl. Pharmacol., 1997, 144, 247-261.
106. Gottschling, B. C.; Maronpot, R. R.; Hailey, J. R.; Peddada, S.; Moomaw, C. R.; Klaunig, J. E.; Nyska, A. The role of oxidative stress in indium phosphide-induced lung carcinogenesis in rats. Toxicol. Sci., 2001, 64, 28-40.
107. Valko, M.; Morris, H.; Cronin, M. T. Metals, toxicity and oxidative stress. Curr. Med. Chem., 2005, 12, 1161-1208.
108. Beddowes, E..; Faux, S. P.; Chipman, J. K. Chloroform, carbon tetrachloride and glutathione depletion induce secondary genotoxicity in liver cells via oxidative stress. Toxicology, 2003, 187, 101-115.
109. Devi, B. G.; Chan, A. W. Cocaine-induced peroxidative stress in rat liver: antioxidant enzymes and mitochondria. J. Pharmacol. Exp. Ther., 1996, 279, 359-366.
110. Salonpaa, P.; Krause, K.; Pelkonen, O.; Raunio, H. Up-regulation of CYP2A5 expression by porphyrinogenic agents in mouse liver. Naunyn-Schmiedebergs Arch. Exper. Path. Pharmakol., 1995, 351, 446-452.
111. Abu-Bakar, A.; Moore, M. R.; Lang, M. A. Evidence for induced microsomal bilirubin degradation by cytochrome P450 2A5. Biochem. Pharmacol., 2005, 70, 1527-1535.
112. Gilmore, W. J.; Kirby, G. M. Endoplasmic reticulum stress due to altered cellular redox status positively regulates murine hepatic CYP2A5 expression. Pharmacol. Exp. Ther., 2004, 308, 600-608.
113. Baird, L.; Dinkova-Kostova, A. T. The cytoprotective role of the Keap1-Nrf2 pathway. Arch. Toxicol., 2011, 84, 241-272.
114. Lämsä, V.; Levonen, A. L.; Leinonen, H.; Yla-Herttuala, S.; Yamamoto, M.; Hakkola, J. Cytochrome P450 2A5 constitutive expression and induction by heavy metals is dependent on redoxsensitive transcription factor Nrf2 in liver. Chem. Res. Toxicol., 2010, 23, 977-985.
115. Hayes, J. D.; McMahon, M.; Chowdhry, S.; Dinkova-Kostova, A. T. Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid. Redox Signal, 2010, 13, 1713-1748.
116. Ogawa, K.; Sun, J.; Taketani, S.; Nakajima, O.; Nishitani, C.; Sassa, S.; Hayashi, N.; Yamamoto, M.; Shibahara, S.; Fujita, H.; Igarashi, K. Heme mediates depression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J., 2001, 20, 2835-2843.
117. Zenke-Kawasaki, Y.; Dohi, Y.; Katoh, Y.; Ikura, T.; Ikura, M.; Asahara, T.; Tokunaga, F.; Iwai, K.; Igarashi, K. Heme induces ubiquitination and degradation of the transcription factor Bach1. Mol. Cell Biol., 2007, 27, 6962-6971.
118. Suzuki, H.; Tashiro, S.; Sun, J.; Doi, H.; Satomi, S.; Igarashi, K. Cadmium induces nuclear export Bach1, a transcriptional repressor of heme oxygenase-1 gene. J. Biol. Chem., 2003, 278, 49246-49253.
119. Kaspar, J. W.; Jaiswal, A. K. Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. J. Biol. Chem., 2010, 285, 153-162.
120. Yokota, S.; Higashi, E.; Fukami, T.; Yokoi, T.; Nakajima, M. Human CYP2A6 is regulated by nuclear factor-erythroid 2 related factor 2. Biochem. Pharmacol, 2011, 81, 289-294.
121. Abel, J.; Haarmann-Stemmann, T. An introduction to the molecular basics of aryl hydrocarbon receptor biology. Biol. Chem., 2010, 391, 1235-1248.
122. Arpiainen, S.; Raffalli-Mathieu, F.; Lang, M. A.; Pelkonen, O.; Hakkola, J. Regulation of the Cyp2a5 gene involves an aryl hydrocarbon-dependent pathway. Mol. Pharmacol, 2005, 67, 1325-1333.
123. Lu, H.; Cui, W.; Klaassen, CD. Nrf2 protects against 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD)-induced oxidative injury and steatohepatitis. Toxicol. Appl. Pharmacol, 2011, 256, 122-135.
124. Hayes, J. D.; Dinkova-Kostova, A. T.; McMahon, M. Cross-talk between transcription factors AhR and Nrf2: lessons for cancer chemoprevention from dioxin. Toxicol. Sci., 2009, 111, 199-201.
125. Arpiainen, S.; Lämsä, V.; Pelkonen, O.; Yim, S. H.; Gonzalez, F. J.; Hakkola, J. Aryl hydrocarbon receptor nuclear translocator and upstream stimulatory factor regulate cytochrome P450 2a5 transcription through a common E-box site. J. Mol. Biol, 2007, 369, 640-652.
126. Corre, S.; Primot, A.; Baron, Y.; Le Seyec, J.; Goding, C; Galibert, M. D. Target gene specificity of USF-1 is directed via p38-mediated phosphorylation-dependent acetylation. J. Biol. Chem., 2009, 284, 18851-18862.
127. Handschin, C. The biology of PGC-1a and its therapeutic potential. Trends Pharmacol. Sci., 2009, 30, 322-329.
128. Arpiainen, S.; Järvenpää, S. M.; Manninen, A.; Viitala, P.; Lang, M. A.; Pelkonen, O.; Hakkola, J. Coactivator PGC-1alpha regulates the fasting inducible xenobiotic-metabolizing enzyme CYP2A5 in mouse primary hepatocytes. Toxicol. Appl. Pharmacol, 2008, 232, 135-141.
129. St-Pierre, J.; Drori, S.; Uldry, M.; Silvaggi, J. M.; Rhee, J.; Jäger, S.; Handschin, C; Zheng, K.; Lin, J.; Yang, W.; Simon, D. K.; Bachoo, R.; Spiegelman, B. A. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell, 2006, 127, 397-408.
130. Lu, Z.; Xu, X.; Hu, X.; Fassett, J.; Zhu, G.; Tao, Y.; Li, J.; Huang, Y.; Zhang, P.; Zhao, B.; Chen, Y. PGC-1 alpha regulates expression of myocardial mitochondrial antioxidants and myocardial oxidative stress after chronic systolic overload. Antioxid. Redox Signal, 2010, 13, 1011-1022.
131. Krecic, A. M.; Swanson, M. S. hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol, 1999, 11, 363-371.
132. Lau, J. S.; Baumeister, P.; Kim, E.; Roy, B.; Hsieh, T. Y.; Lai, M.; Lee, A. S. Heterogeneous nuclear ribonucleoproteins as regulators of gene expression through interactions with human thymidine kinase promoter. J. Cell Biochem., 2000, 79, 395-406.
133. Glisovic, T.; Soderberg, M.; Christian, K.; Lang, M. A.; Raffalli-Mathieu, F. Interplay between transcriptional and posttranscriptional regulation of Cyp2a5 expression. Biochem. Pharmacol, 2003, 65, 1653-1661.
134. van der Houven van Oordt, W.; Diaz-Meco, M. T.; Lozano, J.; Krainer, A. R.; Moscat, J.; Cáceres, J. F. The MKK (3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J. Cell Biol, 2000, 149, 307-316.
135. Aida, K.; Negishi, M. Posttranscriptional regulation of coumarin 7-hydroxylase induction by xenobiotics in mouse liver: mRNA stabilisation by pyrazole. Biochemistry, 1991, 30, 8041-8045.
136. 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, subcellular distribution and possible role in mRNA stabilization. Biochem. J., 1996, 313, 1029-1037.
137. Tilloy-Ellul, A.; Raffalli-Mathieu, F.; Lang, M. A. Analysis of RNA-protein interactions of mouse liver cytochrome P4502A5 mRNA. Biochem. J., 1999, 339, 695-703.
138. 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., 2002, 61, 795-799.
139. Glisovic, T.; Ben-David, Y.; Lang, M. A.; Raffalli-Mathieu, F. Interplay between hnRNP A1 and a cis-acting element in the 3'UTR of CYP2A5 mRNA is central for high expression of the gene. FEBS Lett., 2003, 535, 147-152.
140. Christian, K.; Lang, M.; Maurel, P.; Raffalli-Mathieu, F. Interaction of heterogenous nuclear ribonucleoprotein A1 with cytochrome P450 2A6 mRNA: Implications for post-transcriptional regulation of the CYP2A6 gene. Mol. Pharmacol., 2004, 65, 1405-1414.
141. Damgaard, C. K.; Tange, T. O.; Kjems, J. hnRNP A1 controls HIV-1 mRNA splicing through cooperative binding to intron and exon splicing silencers in the context of a conserved secondary structure. RNA, 2002, 8, 1401-1415.
142. Guil, S.; Gattoni, R.; Carrascal, M.; Abián, J.; Stévenin, J.; Bach-Elias, M. Roles of hnRNP A1, SR proteins, and p68 helicase in c-H-ras alternative splicing regulation. Mol. Cell Biol., 2003, 23, 2927-2941.
143. Juvonen, R.; Kaipainen, P.; Lang, M. A. Selective induction of coumarin 7-hydroxylase by pyrazole in D2 mice. Eur. J. Biochem., 1985, 152, 3-8.
144. Lake, B. G. Coumarin metabolism, toxicity and carcinogenicity: Relevance for human risk assessment. Food Chem. Toxicol., 1999, 37, 423-453.
145. Dore, S.; Takahashi, M.; Ferris, C. D.; Hester, L. D.; Guastella, D.; Snyder, S. H. Bilirubin, formed by activaton of haem oxygenase-2, protects neurons against oxidative stress injury. PNAS., 1999, 96, 2445-2450.
146. Jansen, T.; Hortmann, M.; Oelze, M.; Opitz, B.; Steven, S.; Schell, R.; Knorr, M.; Karbach, S.; Schuhmacher, S.; Wenzel, P.; Münzel, T.; Daiber, A. Conversion of biliverdin to bilirubin by biliverdin reductase contributes to endothelial cell protection by heme oxygenase-1-evidence for direct and indirect antioxidant actions of bilirubin. J. Mol. Cell Cardiol., 2010, 49, 186-195.
147. Stocker, R.; Ames, B. N. Potential role of conjugated bilirubinand copper in the metabolism of lipid peroxides in the bile. PNAS., 1987, 84, 8130-8134.
148. Baranano, D. E.; Rao, M.; Ferris, C. D.; Snyder, S. H. Biliverdin reductase: a major physiologic cytoprotectant. PNAS., 2002, 99, 16093-16098.
149. Sedlak, T. W.; Snyder, S. H. Bilirubin benefits: Cellular protection by a biliverdin reductase antioxidant cycle. Pediatrics, 2004, 113, 1776-1782.
150. De Matteis, F.; Dawson, S. J.; Gibbs, A. H. Two pathways of ironcatalyzed oxidation of bilitubin: Effect of desferrioxamine and trolox, and comparison with microsomal oxidation. Free Radic. Biol. Med., 1993, 15, 301-309.
151. Minetti, M.; Mallozzi, C.; Di Stasi, A. M.; Pietraforte, D. Bilirubin is an effective antioxidant of peroxynitrite-mediated protein oxidation in human blood plasma. Arch. Biochem. Biophys., 1998, 352, 165-174.
152. Maghzal, G. J.; Leck, M. C.; Collinson, E.; Li, C.; Stocker, R. Limited role for the bilirubin-biliverdin redox amplification cycle in the cellular antioxidant protection by biliverdin reductase. J. Biol. Chem., 2009, 284, 29251-29259.
153. McDonagh, A. F. The biliverdin-bilirubin antioxidant cycle of cellular protection: Missing a wheel? Free Radic. Biol. Med., 2010, 49, 814-820.
154. Pae, H.; Chung, H. Heme oxygenase-1: its therapeutic roles in inflammatory diseases. Immune. Netw., 2009, 9, 12-19.
155. Gozzelino, R.; Jeney, V.; Soares, M. P. Mechanisms of cell protection by heme oxygenase-1. Annu. Rev. Pharmacol. Toxicol., 2010, 50, 323-354.
156. Okuhara, K.; Kisaka, T.; Ozono, R.; Kurisu, S.; Inoue, I.; Soga, J.; Yano, Y.; Oshima, T.; Kihara, Y.; Yoshizumi, M. Change in bilirubin level following acute myocardial infarction is an index for heme oxygenase activation. South Med. J., 2010, 103, 876-881.
157. Menken, M.; Waggoner, J. G.; Berlin, N. I. The influence of bilirubin in oxidative phosphorylation and related reactions in brain and liver mitochondria: effects of protein-binding. J. Neurochem., 1966, 13, 1241-1248.
158. Noir, B. A.; Boveris, A.; Garaza Pereira, A. M.; Stopanni, A. O. M. Bilirubin: A multi-site inhibitor of mitochondrial respiration. FEBS Lett., 1972, 27, 270-274.
159. Cashore, W. J. The neurotoxicity of bilirubin. Clin. Perinatol., 1990, 17, 437-447.
160. Keshavan, P.; Schwemberger, S. J.; Smith, D. L. H.; Babcock, G. F.; Zucker, S. D. Unconjugated bilirubin induces apoptosis in colon cancer cells by triggering mitochondrial depolarization. Int. J. Cancer, 2004, 112, 433-445.
161. Pellinen, P.; Stenback, F.; Rautio, A.; Pelkonen, O.; Lang, M.; Pasanen, M. Response of mouse liver coumarin 7-hydroxylase activity to hepatotoxins: dependence on strain and agent and comparison to other monooxygenases. Naunyn Schmiedebergs Arch. Pharmacol., 1993, 348, 435-443.
162. Pellinen, P.; Stenback, F.; Raunio, H.; Pelkonen, O.; Pasanen, M. Modification of hepatic cytochrome P450 profile by cocaine induced hepatotoxicity in DBA/2 mouse. Eur. J. Pharmacol., 1994, 292, 57-65.
163. Lu, Y.; Zhuge, J.; Wu, D.; Cederbaum, A. I. Ethanol induction by CYP2A5: permissible role for CYP2E1. Drug Metab. Dipos., 2011, 39, 330-336.
164. Onica, T.; Nichols, K.; Larin, M.; Ng, L.; Maslen, A.; Dvorak, Z.; Pascussi, J. M.; Vilarem, M. J.; Maurel, P.; Kirby, G. M. Dexamethasone-mediated up-regulation of human CYP2A6 involves the glucocorticoid receptor and increased binding of hepatic nuclear factor 4-alpha to the proximal promoter. Mol. Pharmacol., 2008, 73, 451-460.
165. Cai, Y.; Konishi, T.; Han, G.; Campwala, K. H.; French, S. W.; Wan, Y. J. The role of hepatocyte RXR alpha in xenobiotic-sensing nuclear receptor-mediated pathways. Eur. J. Pharm. Sci., 2002, 15, 89-96.
166. Wood, A. W.; Conney, A. H. Genetic variation in coumarin hydroxylase activity in the mouse (Mus musculus). Science, 1974, 185, 612-614.
167. Raunio, H.; Kojo, A.; Juvonen, R.; Honkakoski, P.; Järvinen, P.; Lang, M. A.; Vähäkangas, K.; Gelbion, H. V.; Park, S.; Pelkonen, O. Mouse hepatic cytochrome p-450 isozyme induction by 1, 4-bis [2-(3, 5-dichloropyridyloxy)] benzene, pyrazole, and phenobarbital. Biochem. Pharmacol., 1988, 37, 4141-4147.
168. Gokhale, M. S.; Bunton, T. E.; Zurlo, J.; Yager, J. D. Cytochrome P450 isoenzyme activities in cultured rat and mouse liver slices. Xenobiotica, 1997, 27, 341-355.
169. Salonpaa, P.; Krause, K.; Pelkonen, O.; Raunio, H. Up-regulation of CYP2A5 expression by porphyrinogenic agents in mouse liver. Naunyn Schmiedebergs Arch. Pharmacol., 1995, 351, 446-452.
170. Arvela, P.; Kraul, H.; Stenback, F.; Pelkonen, O. The cerium induced liver injury and oxidative drug metabolism in DBA/2 and C57BL/6 mice. Toxicology, 1991, 69, 1-9.
171. Legrum, W.; Netter, K. J. Characteristics of coumarin metabolism by liver microsomes from cobalt-pretreated mice. Xenobiotica, 1980, 10, 271-279.
172. Mangoura, S. A.; Strack, A.; Legrum, W.; Netter, K. J. Indium selectively increases the cytochrome P-450 dependent o-dealkylation of coumarin derivatives in male mice. Naunyn Schmiedebergs Arch. Pharmacol., 1989, 339, 596-602.
173. Emde, B.; Tegtmeier, M.; Hahnemann, B.; Legrum, W. Inorganic tin - a new selective inducer of the murine coumarin 7-hydroxylase (CYP2A5). Toxicology, 1996, 108, 73-78.
174. Viitala, P.; Posti, K.; Lindfors, A.; Pelkonen, O.; Raunio, H. cAMP mediated upregulation of CYP2A5 in mouse hepatocytes. Biochem. Biophys. Res. Commun., 2001, 280, 761-767.
175. Chisari, F. V.; Klopchin, K.; Moriyama, T.; Pasquinelli, C.; Dunsford, H. A.; Sell, S.; Pinkert, C. A.; Brinster, R. L.; Palmiter, R. D. Molecular pathogenesis of hepatocellular carcinoma in hepatitis B virus transgenic mice. Cell, 1989, 59, 1145-1156.
176. Richardson, T. A.; Sherman, M.; Antonovic, L.; Kardar, S. S.; Strobel, H. W.; Kalman, D.; Morgan, E. T. Hepatic and renal cytochrome P450 gene regulation during Citrobacter Rodentium infection in wild-type and toll-like receptor 4 mutant mice. Drug Metab. Dispos., 2006, 34, 354-360.
177. De-Oliveira, A. C.; Da-Matta, A. C.; Paumgartten, F. J. Plasmodium berghei (ANKA): infection induces CYP2A5 and 2E1 while depressing other CYP isoforms in the mouse liver. Exp. Parasitol., 2006, 113, 256-261.
178. Lange, R.; Perin, F.; Larroque, C.; Zajdela, F. Isolation and partial characterisation of a cytochrome P-450 isoenzyme (cytochrome P-450tu) from mouse liver tumors. Biochim. Biophys. Acta, 1990, 1038, 130-135.
179. Kobliakov, V.; Kulikova, L.; Samoilov, D.; Lang, M. A. High expression of cytochrome P450 2a-5 (coumarin 7-hydroxylase) in mouse hepatomas. Mol. Carcinog., 1993, 7, 276-280.