Modulation of hepatic cytochrome P450s by citrobacter rodentium infection in interleukin-6- and interferon-γ-null mice

Journal of Pharmacology and Experimental Therapeutics

Volumn 335, Issue 2, 2010, Pages 480-488

  Nyagode, Beatrice A ^a   Lee, Choon Myung ^a   Morgan, Edward T ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE PROTEIN; BACTERIUM LIPOPOLYSACCHARIDE; CYTOCHROME P450; CYTOCHROME P450 2B9; CYTOCHROME P450 2D22; CYTOCHROME P450 2D9; CYTOCHROME P450 2E1; CYTOCHROME P450 3A11; CYTOCHROME P450 3A13; CYTOCHROME P450 3A25; CYTOCHROME P450 4F18; GAMMA INTERFERON; INTERLEUKIN 6; MESSENGER RNA; MYELOPEROXIDASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD LEVEL; CITROBACTER RODENTIUM; CITROBACTER RODENTIUM INFECTION; COLON; CONTROLLED STUDY; DOWN REGULATION; ENTEROBACTERIACEAE INFECTION; ENZYME ACTIVITY; FEMALE; GENOTYPE; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELLS, CULTURED; CITROBACTER RODENTIUM; COLON; CYTOCHROME P-450 ENZYME SYSTEM; ENTEROBACTERIACEAE INFECTIONS; FEMALE; HEPATOCYTES; IMMUNOBLOTTING; INTERFERON-GAMMA; INTERLEUKIN-6; LIVER; MICE; MICE, KNOCKOUT; MICROSOMES, LIVER; PEROXIDASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78149251115     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.110.171488     Document Type: Article

References (37)

1. Abdel-Razzak Z, Loyer P, Fautrel A, Gautier JC, Corcos L, Turlin B, Beaune P, and Guillouzo A (1993) Cytokines down-regulate expression of major cytochrome P-450 enzymes in adult human hepatocytes in primary culture. Mol Pharmacol 44:707-715.
2. Aitken AE and Morgan ET (2007) Gene-specific effects of inflammatory cytokines on cytochrome P450 2C, 2B6 and 3A4 mRNA levels in human hepatocytes. Drug Metab Dispos 35:1687-1693.
3. Ashino T, Oguro T, Shioda S, Horai R, Asano M, Sekikawa K, Iwakura Y, Numazawa S, and Yoshida T (2004) Involvement of interleukin-6 and tumor necrosis factor α in CYP3A11 and 2C29 down-regulation by Bacillus Calmette-Guerin and lipopolysaccharide in mouse liver. Drug Metab Dispos 32:707-714.
4. Castell JV, Gómez-Lechón MJ, David M, Andus T, Geiger T, Trullenque R, Fabra R, and Heinrich PC (1989) Interleukin-6 is the major regulator of acute phase protein synthesis in adult human hepatocytes. FEBS Lett 242:237-239.
5. Chaluvadi MR, Kinloch RD, Nyagode BA, Richardson TA, Raynor MJ, Sherman M, Antonovic L, Strobel HW, Dillehay DL, and Morgan ET (2009a) Regulation of hepatic cytochrome P450 expression in mice with intestinal or systemic infections of Citrobacter rodentium. Drug Metab Dispos 37:366-374.
6. Chaluvadi MR, Nyagode BA, Kinloch RD, and Morgan ET (2009b) TLR4-dependent and -independent regulation of hepatic cytochrome P450 in mice with chemically induced inflammatory bowel disease. Biochem Pharmacol 77:464-471.
7. Chen JQ, Ström A, Gustafsson JA, and Morgan ET (1995) Suppression of the constitutive expression of cytochrome P-450 2C11 by cytokines and interferons in primary cultures of rat hepatocytes: comparison with induction of acute-phase genes and demonstration that CYP2C11 promoter sequences are involved in the suppressive response to interleukins 1 and 6. Mol Pharmacol 47:940-947.
8. Craig PI, Mehta I, Murray M, McDonald D, Aström A, van der Meide PH, and Farrell GC (1990) Interferon down-regulates the male-specific cytochrome P450IIIA2 in rat liver. Mol Pharmacol 38:313-318.
9. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, and Stewart TA (1993) Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science 259:1739-1742.
10. Dann SM, Spehlmann ME, Hammond DC, Iimura M, Hase K, Choi LJ, Hanson E, and Eckmann L (2008) IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol 180:6816-6826.
11. Donato MT, Guillén MI, Jover R, Castell JV, and Gómez-Lechón MJ (1997) Nitric oxide-mediated inhibition of cytochrome P450 by interferon-γ in human hepatocytes. J Pharmacol Exp Ther 281:484-490.
12. Gonçalves NS, Ghaem-Maghami M, Monteleone G, Frankel G, Dougan G, Lewis DJ, Simmons CP, and MacDonald TT (2001) Critical role for tumor necrosis factor α in controlling the number of lumenal pathogenic bacteria and immunopathology in infectious colitis. Infect Immun 69:6651-6659.
13. Goralski KB, Abdulla D, Sinal CJ, Arsenault A, and Renton KW (2005) Toll-like receptor-4 regulation of hepatic Cyp3a11 metabolism in a mouse model of LPS-induced CNS inflammation. Am J Physiol Gastrointest Liver Physiol 289:G434-G443.
14. Higgins LM, Frankel G, Douce G, Dougan G, and MacDonald TT (1999) Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect Immun 67:3031-3039.
15. Huang S, Hendriks W, Althage A, Hemmi S, Bluethmann H, Kamijo R, Vilcek J, Zinkernagel RM, and Aguet M (1993) Immune response in mice that lack the interferon-γ receptor. Science 259:1742-1745.
16. Jover R, Bort R, Gómez-Lechón MJ, and Castell JV (2002) Down-regulation of human CYP3A4 by the inflammatory signal interleukin-6: molecular mechanism and transcription factors involved. Faseb J 16:1799-1801.
17. Kleine M, Schrem H, Borlak J, and Klempnauer J (2008) Clinical versatility of porcine hepatocytes in the light of interspecies differences in cytochrome P450 regulation and expression. Xenotransplantation 15:208-217.
18. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, Zinkernagel R, Bluethmann H, and Köhler G (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368:339-342. (Pubitemid 24104268)
19. Kourylko O, Fradette C, Arcand M, and du Souich P (2006) Modulation of CYP1A2 and CYP3A6 catalytic activities by serum from rabbits with a turpentine-induced inflammatory reaction and interleukin 6. Drug Metab Dispos 34:27-35.
20. Li-Masters T and Morgan ET (2001) Effects of bacterial lipopolysaccharide on phenobarbital-induced CYP2B expression in mice. Drug Metab Dispos 29:252-257.
21. Livak KJ and Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25:402-408.
22. Morgan ET (1997) Regulation of cytochromes P450 during inflammation and infection. Drug Metab Rev 29:1129-1188.
23. Morgan ET, Goralski KB, Piquette-Miller M, Renton KW, Robertson GR, Chaluvadi MR, Charles KA, Clarke SJ, Kacevska M, Liddle C, et al. (2008) Regulation of drug-metabolizing enzymes and transporters in infection, inflammation, and cancer. Drug Metab Dispos 36:205-216.
24. Morgan ET, Thomas KB, Swanson R, Vales T, Hwang J, and Wright K (1994) Selective suppression of cytochrome P-450 gene expression by interleukins 1 and 6 in rat liver. Biochim Biophys Acta 1219:475-483.
25. Muntané-Relat J, Ourlin JC, Domergue J, and Maurel P (1995) Differential effects of cytokines on the inducible expression of CYP1A1, CYP1A2, and CYP3A4 in human hepatocytes in primary culture. Hepatology 22:1143-1153.
26. Renton KW (2004) Cytochrome P450 regulation and drug biotransformation during inflammation and infection. Curr Drug Metab 5:235-243.
27. Richardson TA and Morgan ET (2005) Hepatic cytochrome P450 gene regulation during endotoxin-induced inflammation in nuclear receptor knockout mice. J Pharmacol Exp Ther 314:703-709.
28. Richardson TA, Sherman M, Antonovic L, Kardar SS, Strobel HW, Kalman D, and Morgan ET (2006) Hepatic and renal cytochrome p450 gene regulation during citrobacter rodentium infection in wild-type and toll-like receptor 4 mutant mice. Drug Metab Dispos 34:354-360.
29. Sewer MB and Morgan ET (1997) Nitric oxide-independent suppression of P450 2C11 expression by interleukin-1β and endotoxin in primary rat hepatocytes. Biochem Pharmacol 54:729-737.
30. Siewert E, Bort R, Kluge R, Heinrich PC, Castell J, and Jover R (2000) Hepatic cytochrome P450 down-regulation during aseptic inflammation in the mouse is interleukin 6 dependent. Hepatology 32:49-55.
31. Simmons CP, Goncalves NS, Ghaem-Maghami M, Bajaj-Elliott M, Clare S, Neves B, Frankel G, Dougan G, and MacDonald TT (2002) Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-γ. J Immunol 168:1804-1812.
32. Tapner M, Liddle C, Goodwin B, George J, and Farrell GC (1996) Interferon γ down-regulates cytochrome P450 3A genes in primary cultures of well-differentiated rat hepatocytes. Hepatology 24:367-373.
33. Trautwein C, Ramadori G, Gerken G, Meyer zum Büschenfelde KH, and Manns M (1992) Regulation of cytochrome P450 IID by acute phase mediators in C3H/HeJ mice. Biochem Biophys Res Commun 182:617-623.
34. Warren GW, Poloyac SM, Gary DS, Mattson MP, and Blouin RA (1999) Hepatic cytochrome P-450 expression in tumor necrosis factor-α receptor (p55/p75) knockout mice after endotoxin administration. J Pharmacol Exp Ther 288:945-950.
35. Warren GW, van Ess PJ, Watson AM, Mattson MP, and Blouin RA (2001) Cytochrome P450 and antioxidant activity in interleukin-6 knockout mice after induction of the acute-phase response. J Interferon Cytokine Res 21:821-826.
36. Williams JF, Bement WJ, Sinclair JF, and Sinclair PR (1991) Effect of interleukin 6 on phenobarbital induction of cytochrome P-450IIB in cultured rat hepatocytes. Biochem Biophys Res Commun 178:1049-1055.
37. Xu DX, Wang JP, Sun MF, Chen YH, and Wei W (2006) Lipopolysaccharide down-regulates the expressions of intestinal pregnane X receptor and cytochrome P450 3a11. Eur J Pharmacol 536:162-170.