Regulation of hepatic drug-metabolizing enzymes in germ-free mice by conventionalization and probiotics

Drug Metabolism and Disposition

Volumn 44, Issue 2, 2016, Pages 262-274

  Selwyn, Felcy Pavithra ^a   Cheng, Sunny Lihua ^a   Klaassen, Curtis D ^a   Cui, Julia Yue ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ALCOHOL DEHYDROGENASE 1; CARBOXYESTERASE 2A; CARBOXYLESTERASE; CYTOCHROME P450 3A; CYTOCHROME P450 4A; GLUCURONOSYLTRANSFERAS 2A3; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 1A9; GLUTATHIONE TRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PREGNANE X RECEPTOR; PROBIOTIC AGENT; UNCLASSIFIED DRUG; VSL3; CYTOCHROME P450; MESSENGER RNA; STEROID RECEPTOR; UDP-GLUCURONOSYLTRANSFERASE 1A9;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM INFANTIS; BIFIDOBACTERIUM LONGUM; CONTROLLED STUDY; CYP3A GENE; CYP4A GENE; DNA BINDING; DOWN REGULATION; DRUG METABOLISM; ENZYME ACTIVITY; GENE CLUSTER; GENE EXPRESSION; GENETIC CORRELATION; GERMFREE MOUSE; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS DELBRUECKII SUBSP. BULGARICUS; LACTOBACILLUS PARACASEI; LACTOBACILLUS PLANTARUM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH JUICE; STREPTOCOCCUS THERMOPHILUS; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; LIVER; METABOLISM; PHYSIOLOGY;

ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; DOWN-REGULATION; GLUCURONOSYLTRANSFERASE; GLUTATHIONE TRANSFERASE; LIVER; MALE; MICE; MICE, INBRED C57BL; PPAR ALPHA; PROBIOTICS; RECEPTORS, STEROID; RNA, MESSENGER; UP-REGULATION;

EID: 84958151759     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.115.067504     Document Type: Article

References (39)

1. Aleksunes LM and Klaassen CD (2012) Coordinated regulation of hepatic phase I and II drugmetabolizing genes and transporters using AhR-, CAR-, PXR-, PPARa-, and Nrf2-null mice. Drug Metab Dispos 40:1366-1379.
2. Alnouti Y and Klaassen CD (2008) Regulation of sulfotransferase enzymes by prototypical microsomal enzyme inducers in mice. J Pharmacol Exp Ther 324:612-621.
3. Barrera LO and Ren B (2006) The transcriptional regulatory code of eukaryotic cells-insights from genome-wide analysis of chromatin organization and transcription factor binding. Curr Opin Cell Biol 18:291-298.
4. Bibiloni R, Fedorak RN, Tannock G.W., Madsen KL, Gionchetti P, Campieri M, De Simone C, and Sartor RB (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100:1539-1546.
5. Boyle RJ, Robins-Browne RM, and Tang ML (2006) Probiotic use in clinical practice: what are the risks? Am J Clin Nutr 83:1256-1264; quiz 1446-1257.
6. Buckley DB and Klaassen CD (2009) Induction of mouse UDP-glucuronosyltransferase mRNA expression in liver and intestine by activators of aryl-hydrocarbon receptor, constitutive androstane receptor, pregnane X receptor, peroxisome proliferator-activated receptor alpha, and nuclear factor erythroid 2-related factor 2. Drug Metab Dispos 37:847-856.
7. Carvalho BM, Guadagnini D, Tsukumo D.M., Schenka AA, Latuf-Filho P, Vassallo J, Dias J.C., Kubota LT, Carvalheira JB, and Saad MJ (2012) Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia 55:2823-2834.
8. Claus SP, Ellero SL, Berger B, Krause L., Bruttin A, Molina J, Paris A., Want EJ, de Waziers I, and Cloarec O, et al. (2011) Colonization-induced host-gut microbial metabolic interaction. MBio 2:e00271-e10.
9. Collado MC, Rautava S, Isolauri E., and Salminen S (2015) Gut microbiota: a source of novel tools to reduce the risk of human disease? Pediatr Res 77:182-188.
10. Cui JY, Gunewardena SS, Rockwell C.E., and Klaassen CD (2010) ChIPing the cistrome of PXR in mouse liver. Nucleic Acids Res 38:7943-7963.
11. Dhar M, Sepkovic DW, Hirani V, Magnusson R.P., and Lasker JM (2008) Omega oxidation of 3-hydroxy fatty acids by the human CYP4F gene subfamily enzyme CYP4F11. J Lipid Res 49: 612-624.
12. Furet JP, Quénée P, and Tailliez P (2004) Molecular quantification of lactic acid bacteria in fermented milk products using real-time quantitative PCR. Int J Food Microbiol 97:197-207.
13. Hardwick JP (2008) Cytochrome P450 omega hydroxylase (CYP4) function in fatty acid metabolism and metabolic diseases. Biochem Pharmacol 75:2263-2275.
14. Jancova P, Anzenbacher P, and Anzenbacherova E (2010) Phase II drug metabolizing enzymes. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 154:103-116.
15. Kim DH (2015) Gut Microbiota-Mediated Drug-Antibiotic Interactions. Drug Metab Dispos 43: 1581-1589.
16. Knight TR, Choudhuri S, and Klaassen CD (2008) Induction of hepatic glutathione S-transferases in male mice by prototypes of various classes of microsomal enzyme inducers. Toxicol Sci 106: 329-338.
17. Kroetz DL, Yook P, Costet P., Bianchi P, and Pineau T (1998) Peroxisome proliferator-activated receptor alpha controls the hepatic CYP4A induction adaptive response to starvation and diabetes. J Biol Chem 273:31581-31589.
18. Lee JH, Moon G, Kwon H.J., Jung WJ, Seo PJ, Baec TY, Lee J.H., and Kim HS (2012) [Effect of a probiotic preparation (VSL#3) in patients with mild to moderate ulcerative colitis]. Korean J Gastroenterol 60:94-101.
19. Lee JM, Wagner M, Xiao R., Kim KH, Feng D, Lazar MA, and Moore DD (2014) Nutrientsensing nuclear receptors coordinate autophagy. Nature 516:112-115.
20. Mar JS, Nagalingam NA, Song Y, Onizawa M., Lee JW, and Lynch SV (2014) Amelioration of DSS-induced murine colitis by VSL#3 supplementation is primarily associated with changes in ileal microbiota composition. Gut Microbes 5:494-503.
21. Mardini HE and Grigorian AY (2014) Probiotic mix VSL#3 is effective adjunctive therapy for mild to moderately active ulcerative colitis: a meta-analysis. Inflamm Bowel Dis 20:1562-1567.
22. Oishi K, Shirai H, and Ishida N (2005) CLOCK is involved in the circadian transactivation of peroxisome-proliferator-activated receptor alpha (PPARalpha) in mice. Biochem J 386: 575-581.
23. Penner RM and Fedorak RN (2005) Probiotics in the management of inflammatory bowel disease. MedGenMed 7:19.
24. Pratt-Hyatt M., Lickteig AJ, and Klaassen CD (2013) Tissue distribution, ontogeny, and chemical induction of aldo-keto reductases in mice. Drug Metab Dispos 41:1480-1487.
25. Robinson JT, Thorvaldsdottir H, Winckler W., Guttman M, Lander ES, Getz G, and Mesirov JP (2011) Integrated genomics viewer. Nat Biotechnol 29:24-6.
26. Sanders ME (2008) Probiotics: definition, sources, selection, and uses. Clin Infect Dis 46 Suppl 2:S58-61; discussion S144-151.
27. Selwyn FP, Cheng SL, Bammler T.K., Prasad B., Vrana M, Klaassen C, and Cui JY (2015a) Developmental regulation of drug-processing genes in livers of germ-free mice. Toxicol Sci 147:84-103.
28. Selwyn FP, Cui JY, and Klaassen CD (2015b) RNA-Seq quantification of hepatic drug processing genes in germ-free mice. Drug Metab Dispos 43:1572-1580.
29. Staudinger JL, Goodwin B, Jones S.A., Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y., Klaassen CD, Brown KK, and Reinhard J, et al. (2001) The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci USA 98: 3369-3374.
30. Toda T, Saito N, Ikarashi N., Ito K, Yamamoto M, Ishige A., Watanabe K, and Sugiyama K (2009) Intestinal flora induces the expression of Cyp3a in the mouse liver. Xenobiotica 39: 323-334.
31. Vandenplas Y, Huys G, and Daube G (2015) Probiotics: an update. J Pediatr (Rio J) 91: 6-21.
32. Venkatesh M, Mukherjee S, Wang H., Li H, Sun K, Benechet A.P., Qiu Z., Maher L, Redinbo MR, and Phillips RS, et al. (2014) Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity 41:296-310.
33. Vitali B, Candela M, Matteuzzi D., and Brigidi P (2003) Quantitative detection of probiotic Bifidobacterium strains in bacterial mixtures by using real-time PCR. Syst Appl Microbiol 26: 269-276.
34. Wang MZ, Saulter JY, Usuki E, Cheung Y.L., Hall M., Bridges AS, Loewen G, Parkinson OT, Stephens C.E., and Allen JL, et al. (2006) CYP4F enzymes are the major enzymes in human liver microsomes that catalyze the O-demethylation of the antiparasitic prodrug DB289 [2,5-bis (4-amidinophenyl)furan-bis-O-methylamidoxime]. 2,5-bis 4-amidinophenyl furan-bis-Omethylamidoxime Drug Metab Dispos 34:1985-1994.
35. Wang Z, Schones DE, and Zhao K (2009) Characterization of human epigenomes. Curr Opin Genet Dev 19:127-134.
36. Wilkinson GR (1996) Cytochrome P4503A (CYP3A) metabolism: prediction of in vivo activity in humans. J Pharmacokinet Biopharm 24:475-490.
37. Xu C, Li CY, and Kong AN (2005) Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28:249-268.
38. Yamamoto M, Yamaguchi R, Munakata K., Takashima K, Nishiyama M, Hioki K., Ohnishi Y, Nagasaki M, Imoto S., and Miyano S, et al. (2012) A microarray analysis of gnotobiotic mice indicating that microbial exposure during the neonatal period plays an essential role in immune system development. BMC Genomics 13:335.
39. Zhang Y, Limaye PB, Lehman-McKeeman LD, and Klaassen CD (2012) Dysfunction of organic anion transporting polypeptide 1a1 alters intestinal bacteria and bile acid metabolism in mice. PLoS One 7:e34522.