Expression and inducibility of p450 enzymes during liver ontogeny

Microscopy Research and Technique

Volumn 39, Issue 5, 1997, Pages 424-435

  Rich, Kim J ^a,c   Boobis, Alan R ^b  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c Procter/Gamble Pharmaceuticals   (United Kingdom)

Author keywords

Development; Drug metabolism; Gene expression regulation; Hepatocytes; Human; Rodent

Indexed keywords

BIOCHEMISTRY; ENZYMES; MAMMALS; METABOLISM; MONOCLONAL ANTIBODIES; NUCLEIC ACIDS; SUBSTRATES;

CONSTITUTIVE EXPRESSIONS; CYTOCHROMES P450; DEVELOPMENT; DRUG METABOLISMS; ENHANCED SENSITIVITY; HEPATOCYTES; HUMAN; P450 ENZYMES; POLYCLONAL; RODENT;

GENE EXPRESSION;

CYTOCHROME P450; MESSENGER RNA;

ARTICLE; ENZYME ASSAY; ENZYME REGULATION; ENZYME SUBSTRATE; FETUS LIVER; HUMAN; IN SITU HYBRIDIZATION; LIVER DEVELOPMENT; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RODENT; SEX DIFFERENCE;

ANIMALIA; RODENTIA;

EID: 0030776172     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19971201)39:5<424::AID-JEMT5>3.0.CO;2-G     Document Type: Article

References (73)

1. Åström, A., Månër, S., and DePierre, J.W. (1986) Induction of cytochrome P-450 and related drug-metabolising activities in the livers of different rodent species by 2-acetylaminofluorene or by 3-methylcholanthrene. Biochem. Pharmacol., 35:2703-2713.
2. Atlas, S.A., Boobis, A.R., Felton, J.S., Thorgeirsson, S.S., and Nebert, D.W. (1977) Ontogenetic expression of polycyclic aromatic compound-inducible monooxygenase activities and forms of cytochrome P-450 in rabbit. J. Biol. Chem., 252:4712-4721.
3. Barnes, T.S., Shaw, P.M., Burke, M.D., and Melvin, W.T. (1987) Monoclonal antibodies against human cytochrome P-450 recognizing different pregnenolone 16α-carbonitrile-inducible rat cytochromes P-450. Biochem. J., 248:301-304.
4. Barnes, T.S., Burke, M.D., and Melvin, W.T. (1989) Differences in adult and foetal human cytochrome P-450 forms recognized by monoclonal antibodies with specificity for the P450III family. Biochem. J., 260:635-640.
5. Bonfils, C., Combalbert, J., Pineau, T., Angevin, J., Larroque, C., Derancourt, J., Capony, J-P., and Maurel, P. (1990) Ontogenesis of rabbit liver cytochrome P450. Mol. Pharmacol., 188:187-194.
6. Boobis, A.R., Davies, D.S., McQuade, J., and Sesardic, D. (1985a) Specificity of isozymes of cytochrome P-450 determined by inhibitory antibodies. Br. J. Pharmacol., 86:511P.
7. Boobis, A.R., McQuade, J., Sesardic, D., Robson, R.T., Hayward, C., Lock, E.A., Elcombe, C.R., Rose, M.S., and Davies, D.S. (1985b) A monoclonal antibody raised to rat liver cytochrome P-448 (form c) which recognizes an epitope common to many other forms of cytochrome P-450. Biochem. Pharmacol., 34:1671-1681.
8. Boobis, A.R., Edwards, R.J., Foster, J.R., and Rich, K.J. (1990) Ontogeny of expression, distribution and inducibility of cytochromes P450IA1 and IA2 in hepatic and extrahepatic tissues of the rat. Eur. J. Pharmacol., 183:1502.
9. Chen, D., Park, Y., and Kemper, B. (1994) Differential protein binding and transcriptional activities of HNF-4 elements in three closely related CYP2C genes. DNA Cell Biol., 13:771-779.
10. Christou, M., Wilson, N.M., and Jefcoate, C.R. (1987) Expression and function of three cytochrome P450 isozymes in rat extrahepatic tissues. Arch. Biochem. Biophys., 270:162-172.
11. Cresteil, T., Beaune, P., Kremers, P., Celier, C., Guengerich, F.P., and Leroux, J.P. (1985) Immunoquantification of epoxide hydrolase and cytochrome P-450 isozymes in fetal and adult human liver microsomes. Eur. J. Biochem., 151:345-350.
12. Cresteil, T., Beaune, P., Celier, C., Leroux, J.P., and Guengerich, F.P. (1986) Cytochrome P-450 isoenzyme content and monooxygenase activities in rat liver: Effect of ontogenesis and pretreatment by phenobarbital and 3-methylcholanthrene. J. Pharmacol. Exp Ther., 236:269-276.
13. Dey, A., Westphal, H., and Nebert, D.W. (1989) Cell-specific induction of mouse Cyp1a1 mRNA during development. Proc. Natl. Acad USA, 86:7446-7450.
14. Edwards, R.J., Singleton, A.M., Murray, B.P., Sesardic, D., Rich, K.J., Davies, D.S., and Boobis, A.R. (1990) An anti-peptide antibody targeted to a specific region of rat cytochrome P450IA2 inhibits enzyme activity. Biochem. J., 266:497-504.
15. Freidman, F.K., Park, S.S., Song, B.J., Cheng, K.C., Fujino, T., and Gelboin, H.V. (1986) Monoclonal antibody-directed analysis of cytochrome P-450. Adv. Exp. Med. Biol., 197:145-154.
16. Giachelli, C.M., and Omiecinski, C.J. (1987) Developmental regulation of cytochrome P-450 genes in the rat. Mol. Pharmacol., 31:477-484.
17. Gonzalez, F.J. (1988) The molecular biology of cytochrome P450s. Pharmacol. Rev., 40:244-288.
18. Gonzalez, F.J., Kimura, S., Song, B.-J., Pastewka, J., Gelboin, H.V., and Hardwick, J.P. (1986) Sequence of two related P-450 mRNAs transcriptionally increased during rat development. J. Biol. Chem., 261:10667-10672.
19. Gonzalez, F.J., Matsunaga, T., and Nagata, K. (1989) Structure and regulation of P-450s in the rat P450IIA gene subfamily. Drug Metab. Rev., 20:827-837.
20. Guengerich, F.P., Dannan, G.A., Wright, S.T., Martin, M.V., and Kaminsky, L.S. (1982) Purification and characterization of liver microsomal cytochromes P-450: Electrophoretic, spectral, catalytic, and immunochemical properties, and inducibility of eight isozymes isolated from rats treated with phenobarbital or β-naphthoflavone. Biochemistry, 21:6019-6030.
21. Guenthner, T.M., and Nebert, D.W. (1978) Evidence in rat and mouse liver for temporal control of two forms of cytochrome P-450 inducible by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Eur. J. Biochem., 91:449-456.
22. Hakkola, J., Pasanen, M., Purkunen, R., Saarikoski, S., Pelkonen, O., Maenpaa, J., Rane, A., and Raunio, H. (1994) Expression of xenobiotic-metabolising cytochrome P450 forms in human adult and fetal liver. Biochem. Pharmacol., 48:59-64.
23. LAω). J. Biol. Chem., 262:801-810.
24. Henderson, C.J., Bammler, T., and Wolf, C.R. (1994) Deduced amino acid sequence of a murine cytochrome P-450 Cyp4a protein: Developmental and hormonal regulation in liver and kidney. Biochim. Biophys. Acta, 1200:182-190.
25. Hulla, J.E., and Juchau, M.R. (1989) Developmental aspects of P450IIIA: prenatal activity and inducibility. Drug Metab. Rev., 20:765-779.
26. Jaczq-Aigrain, E. (1989) Genetic polymorphisms of drug metabolism. Dev. Pharmacol. Ther., 13:78-84.
27. Johansson, I., Ekström, G., Scholte, B., Puzycki, D., Jörnvall, H., and Ingelman-Sundberg, M. (1988) Ethanol-, fasting-, and acetone-inducible cytochromes P-450 in rat liver: Regulation and characteristics of enzymes belonging to the IIB and IIE gene subfamilies. Biochemistry, 27:1925-1934.
28. Jones, S.M., Boobis, A.R., Moore, G.E., and Stanier, P.M. (1992) Expression of CYP2E1 during human fetal development: methylation of the CYP2E1 gene in human fetal and adult liver samples. Biochem. Pharmacol., 43:1876-1879.
29. Juchau, M.R., Giachelli, C.M., Fantel, A.G., Greenaway, J.C., Shepard, T.H., and Faustman-Watts, E.M. (1985) Effects of 3-methylcholanthrene and phenobarbital on the capacity of the embryo to bioactivate teratogens during organogenesis. Toxicol. Appl. Pharmacal., 80:137-146.
30. Juchau, M.R. (1990) Developmental drug metabolism. In: Compreheasive Medicinal Chemistry, Vol. 5. pp. 237-249.
31. 3450 genes: Differential transcriptional activation and mRNA stability in liver and extrahepatic tissue. Mol. Cell Biol., 6:1471-1477.
32. 1450 gene during differentiation without foreign chemical stimulation. J. Exp. Pathol., 3:61-74.
33. Kitada, M., Kamataki, T., Itahashi, K., Rikihisa, T, Kato, R, and Kanakubo, Y. (1985) Immunochemical examinations of cytochrome P-450 in various tissues of human fetuses using antibodies to human fetal cytochrome P-450, P-450HFLa. Biochem. Biophys. Res. Commun., 131:1154-1159.
34. Kitada, M., Ogoshi, N., Kamataki, T., Itahashi, K., Imaoka, S., Komori, M., Funae, Y., Rikihisa, T., and Kanakubo, Y. (1988) Immunochemical similarity of P-450 HFLa, a form of cytochrome P-450 in human fetal livers, to a form of rat liver cytochrome P-450 inducible by macrolide antibiotics. Arch. Biochem. Biophys., 264:61-66.
35. Kitada, M., Kato, T., Ohmori, S., Kamataki, T., Itahashi, K., Guengerich, F.P., Rikihisa, T., and Kanakubo, Y. (1992) Immunochemical characterization and toxicological significance of P-450HFLb purified from human fetal livers. Biochim. Biophys. Acta, 1117:301-305.
36. Komori, M., Nishio, K., Fujitani, T., Ohi, H., Kitada, M., Mima, S., Itahashi, K., and Kamataki, T. (1989) Isolation of a new human fetal liver cytochrome P450-cDNA clone: Evidence for expression of a limited number of forms of cytochrome P450 in human fetal liver. Arch. Biochem. Biophys., 272:219-225.
37. Koop, D.R., Morgan, E.T., Tarr, G.E., and Coon, M.J. (1982) Purification and characterization of a unique isozyme of cytochrome P-450 from liver microsomes of ethanol-treated rabbits. J. Biol. Chem., 257:8472-8480.
38. Ladona, M.G., Park, S.S., Gelboin, H.V., Hammar, L., and Rane, A. (1988) Monoclonal antibody directed detection of cytochrome P-450 (PCN) in human fetal livers. Biochem. Pharmacol., 37:4735-4741.
39. Leakey, J.E.A. (1983) Ontogenesis. In: Biological Basis of Detoxification. J. Caldwell and W.B. Jacoby, eds. Academic Press, New York, pp. 77-104.
40. Liem, H.H., Muller-Eberhard, U., and Johnson, E.F. (1980) Differential induction by 2,3,7,8-tetrachloro-dibenzo-ρ-dioxin of multiple forms of rabbit microsomal cytochrome P-450: Evidence for tissue specificity. Mol. Pharmacol., 18:565-570.
41. Marie, S., and Cresteil, T. (1989) Phenobarbital-inducible gene expression in developing rat liver: Relationship to hepatocyte function. Biochim. Biophys. Acta, 1009:221-228.
42. Marie, S., Roussel, F., and Cresteil, T. (1993) Age- and tissue-dependent expression of CYP2C23 in the rat. Biochim. Biophys. Acta, 1172:124-130.
43. Murray, G.I., Barnes, T.S., Sewell, H.F., Ewen, S.W.B., Melvin, W.T., Shaw, P.M., Fowler, J., and Burke, M.D. (1987) Cytochrome P-450 localization in normal human adult and foetal liver by immunocytochemistry using a monoclonal antibody against human cytochrome P-450. Histochem. J., 19:537-545.
44. Nebert, D.W. (1991) Proposed role of drug-metabolising enzymes: Regulation of steady state levels of the ligands that effect growth, homeostasis, differentiation, and neuroendocrine functions. Mol. Endocrinol., 5:1203-1314.
45. Negishi, M., and Nebert, D.W. (1979) Structural gene products of the Ah locus. Genetic and immunochemical evidence for two forms of mouse liver cytochrome P-450 induced by 3-methylcholanthrene. J. Biol. Chem., 254:11015-11023.
46. Nelson, D.R., Kamataki, T., Waxman, D.J., Guengerich, F.P., Estabrook, R.W., Feyereisen, R., Gonzalez, F.J., Coon, M.J., Gunsalus, I.C., Gotoh, O., Okuda, K., and Nebert, D.W. (1993) The P450 Superfamily: Update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol., 12:1-51.
47. Omiecinski, C.J., Hassett, C., and Costa, P. (1990) Developmental expression and in situ localization of the phenobarbital-inducible rat hepatic mRNAs for cytochromes CYP2B1, CYP2B2, CYP2C6, and CYP3A1. Mol. Pharmacol., 38:462-470.
48. Pacifici, G.M., Park, S.S., Gelboin, H.W., and Rane, A. (1988) Ontogenic development of 7-ethyoxycoumarin and 7-ethoxyresorufin O-deethylase in the rat and effect of monoclonal antibodies. Pharmacol. Toxicol., 62:101-103.
49. Parandoosh, Z., Fujita, V.S., Coon, M.J., and Philpot, R.M. (1987) Cytochrome P-450 isozymes 2 and 5 in rabbit lung and liver: comparisons of structure and inducibility. Drug Metab. Dispos., 15:59-67.
50. Pineau, T., Daujat, M., Pichard, L., Girard, F., Angevain, J., Bonfils, C., and Maurel, P. (1991) Developmental expression of rabbit cytochrome P450 CYP1A1, CYP1A2 and CYP3A6 genes. Eur. J. Biochem., 197:145-153.
51. Ratanasavanh, D., Beaune, P., Morel, F., Flinois, J.-P., Guengerich, F.P., and Guillouzo, A. (1991) Intralobular distribution and quantitation of cytochrome P-450 enzymes in human liver as a function of age. Hepatology, 13:1142-1151.
52. Raucy, J.L., Lasker, J.M., Lieber, C.S., and Black, M. (1989) Acetaminophen activation by human liver cytochromes P450IIE1 and P450IA2. Arch. Biochem. Biophys., 271:270-283.
53. Reik, L.M., Levin, W., Ryan, D.E., and Thomas, P.E. (1982) Immunochemical relatedness of rat hepatic microsomal cytochromes P-450c and P-450d. J. Biol. Chem., 257:3950-3957.
54. Reik, L.M., Levin, W., Ryan, D.E., Maines, S.L., and Thomas, P.E. (1985) Monoclonal antibodies distinguish among isozymes of the cytochrome P-450b subfamily. Arch. Biochem. Biophys., 242:365-382.
55. Rich, K.J., Sesardic, D., Foster, J.R., Davies, D.S., and Boobis, A.R. (1989) Immunohistochemical localization of cytochrome P450b/e in hepatic and extrahepatic tissues of the rat. Biochem. Pharmacol., 38:3305-3322.
56. Rich, K.J., Foster, J.R., Edwards, R.J., Davies, D.S., and Boobis, A.R. (1993) Ontogenetic development of the distribution of constitutive and 3-methylcholanthrene-induced CYP1A1 and CYP1A2 in rabbit liver. J. Histochem. Cytochem., 41:915-925.
57. Ryan, D.E., Ramanathan, L., Iida, S., Thomas, P.E., Hanui, M., Shively, J.E., Lieber, C.S., and Levin, W. (1985) Characterization of a major form of rat hepatic microsomal cytochrome P-450 induced by isoniazid. J. Biol. Chem., 260:6385-6393.
58. Schuetz, E.G., Wrighton, S.A., Barwick, J.L., and Guzelain, P.S. (1984) Induction of cytochrome P-450 by glucocorticoids in rat liver. 1. Evidence that glucocorticoids and pregnenolone 16α-carbonitrile regulate de novo synthesis of a common form of cytochrome P-450 in cultures of adult rat hepatocytes and in the liver in vivo. J. Biol. Chem., 259:1999-2006.
59. Schwab, G.E., and Johnson, E.F. (1987) Enzymology of rabbit cytochromes P-450. In: Mammalian Cytochromes P-450 1. F.P. Guengerich, ed. CRC Press, Boca Raton, Florida, pp. 56-105.
60. Sesardic, D., Boobis, A.R., McQuade, J., Baker, S., Lock, E.A., Elcombe, C.R., Robson, R.T., Hayward, C., and Davies, D.S. (1986) Inter-relatedness of some isoenzymes of cytochrome P450 from rat, rabbit and human, determined with monoclonal antibodies. Biochem. J., 236:569-577.
61. Shimada, T., Yamazaki, H., Mimura, M., Inui, Y., and Guengerich, F.P. (1994) Interindividual variations in human liver cytochrome P-450 enzymes involved in the oxidation of drugs, carcinogens and toxic chemicals: studies with liver microsomes of 30 Japanese and 30 Caucasians. J. Pharmacol. Exp. Ther., 270:414-423.
62. Simmons, D.L., and Kasper, C.B. (1989) Quantitation of mRNAs specific for the mixed-function oxidase system in rat liver and extrahepatic tissues during development. Arch. Biochem. Biophys., 271:10-20.
63. Thomas, P.E., Reik, L.M., Ryan, D.E., and Levin, W. (1983) Induction of two immunochemically related rat liver cytochrome P-450 isozymes, cytochromes P-450c and P-450d, by structurally diverse xenobiotics. J. Biol. Chem., 258:4590-4598.
64. Thomas, P.E., Reik, L.M., Ryan, D.E., and Levin, W. (1984a) Characterization of nine monoclonal antibodies against rat hepatic cytochrome P-450c. J. Biol. Chem., 259:3890-3899.
65. Thomas, P.E., Reidy, J., Reik, L.M., Ryan, D.E., Koop, D.R., and Levin, W. (1984b) Use of monoclonal antibody probes against rat hepatic cytochromes P-450c and P-450d to detect immunochemically related isozymes in liver microsomes from different species. Arch. Biochem. Biophys., 235:239-253.
66. Thomas, P.E., Bandiera, S., Reik, L.M., Maines, S.L., Ryan, D.E., and Levin, W. (1987) Polyclonal and monoclonal antibodies as probes of rat hepatic cytochrome P-450 isozymes. Fed. Proc., 46:2563-2566.
67. 3-450 genes. Dev. Biol., 112:177-184.
68. Waxman, D.J., Dannan, G.A., and Guengerich, F.P. (1985) Regulation of rat hepatic cytochrome P-450: Age-dependent expression, hormonal imprinting, and xenobiotic inducibility of sex-specific isoenzymes. Biochemistry 24:4409-4417.
69. Wrighton, S.A., and Vandenbranden, M. (1989) Isolation and characterization of human fetal liver cytochrome P450Lp2: A third member of the P450III gene family. Arch. Biochem. Biophys., 268:144-151.
70. Wrighton, S.A., Maurel, P., Schuetz, E.G., Watkins, P.B.P., Young, B., and Guzelian, P.S. (1985) Identification of the cytochrome P-450 induced by macrolide antibiotics in rat liver as the glucocorticoid responsive cytochrome P-450p. Biochemistry, 24:2171-2178.
71. Wrighton, S.A., Molowa, D.T., and Guzelian, P.S. (1988) Identification of a cytochrome P-450 in human fetal liver related to glucocorticoid-inducible cytochrome P-450HLp in the adult. Biochem. Pharmacol., 37:3053-3055.
72. Yang, H.-Y.L., Namkung, M.J., and Juchau, M.R. (1988) Cytochrome P-450-dependent biotransformation of a series of phenoxazone ethers in the rat conceptus during early organogenesis: Evidence for multiple P-450 isoenzymes. Mol. Pharmacol., 34:67-73.
73. Yang, H.-Y.L., Zelus, B.D., and Juchau, M.R. (1991) Organogenesisstage cytochrome P450 isoforms: Utilization of PCR for detection of CYP1A1 mRNA in rat conceptual tissues. Biochem. Biophys. Res. Commun., 178:236-241.