Disturbance of hepatic and intestinal UDP-glucuronosyltransferase in rats with trinitrobenzene sulfonic acid-induced colitis

Drug Metabolism and Pharmacokinetics

Volumn 28, Issue 4, 2013, Pages 305-313

  Zhou, Xueyan ^a   Xie, Yang ^a   Qi, Qu ^a   Cheng, Xuefang ^a   Liu, Fang ^a   Liao, Ke ^a   Wang, Guangji ^a   Hao, Haiping ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

AhR; Cytokines; FXR; Inflammation; Membrane barriers; Nuclear receptors; Phase II drug metabolism; PPAR; PXR; UDP glucuronosyltransferases

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CONSTITUTIVE ANDROSTANE RECEPTOR; FARNESOID X RECEPTOR; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 1A1; GLUCURONOSYLTRANSFERASE 1A6; GLUCURONOSYLTRANSFERASE 1A7; GLUCURONOSYLTRANSFERASE 2B1; ISOPROTEIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PREGNANE X RECEPTOR; TRINITROBENZENESULFONIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; ENTEROPATHY; ENZYME ACTIVITY; ENZYME REGULATION; LIVER DISEASE; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

ANIMALS; COLITIS; GLUCURONOSYLTRANSFERASE; INTESTINE, SMALL; LIVER; MALE; RATS; RATS, WISTAR; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTION FACTORS; TRINITROBENZENESULFONIC ACID;

EID: 84883149747     PISSN: 13474367     EISSN: 18800920     Source Type: Journal    
DOI: 10.2133/dmpk.DMPK-12-RG-097     Document Type: Article

References (62)

1. Ishii, Y., Nurrochmad, A. and Yamada, H.: Modulation of UDPglucuronosyltransferase activity by endogenous compounds. Drug Metab. Pharmacokinet., 25: 134-148 (2010).
2. Richardson, T. A., Sherman, M., Kalman, D. and Morgan, E. T.: Expression of UDP-glucuronosyltransferase isoform mRNAs during inflammation and infection in mouse liver and kidney. Drug Metab. Dispos., 34: 351-353 (2006).
3. Wells, P. G., Mackenzie, P. I., Chowdhury, J. R., Guillemette, C., Gregory, P. A., Ishii, Y., Hansen, A. J., Kessler, F. K., Kim, P. M., Chowdhury, N. R. and Ritter, J. K.: Glucuronidation and the UDP-glucuronosyltransferases in health and disease. Drug Metab. Dispos., 32: 281-290 (2004).
4. Kaplan, M.: Genetic interactions in the pathogenesis of neonatal hyperbilirubinemia: Gilbert's Syndrome and glucose-6-phosphate dehydrogenase deficiency. J. Perinatol., 21 Suppl 1: S30-34; discussion S35-39 (2001).
5. Hu, Z. and Wells, P. G.: In vitro and in vivo biotransformation and covalent binding of benzo(a)pyrene in Gunn and RHA rats with a genetic deficiency in bilirubin uridine diphosphate-glucuronosyltransferase. J. Pharmacol. Exp. Ther., 263: 334-342 (1992).
6. Ciotti, M., Marrone, A., Potter, C. and Owens, I. S.: Genetic polymorphism in the human UGT1A6 (planar phenol) UDP-glucuronosyltransferase: pharmacological implications. Pharmacogenetics, 7: 485-495 (1997).
7. Wu, B., Kulkarni, K., Basu, S., Zhang, S. and Hu, M.: First-pass metabolism via UDP-glucuronosyltransferase: a barrier to oral bioavailability of phenolics. J. Pharm. Sci., 100: 3655-3681 (2011).
8. Strasser, S. I., Mashford, M. L. and Desmond, P. V.: Regulation of uridine diphosphate glucuronosyltransferase during the acute-phase response. J. Gastroenterol. Hepatol., 13: 88-94 (1998).
9. Congiu, M., Mashford, M. L., Slavin, J. L. and Desmond, P. V.: UDP glucuronosyltransferase mRNA levels in human liver disease. Drug Metab. Dispos., 30: 129-134 (2002).
10. Hao, H., Zhang, L., Jiang, S., Sun, S., Gong, P., Xie, Y., Zhou, X. and Wang, G.: Thioacetamide intoxication triggers transcriptional upregulation but enzyme inactivation of UDP-glucuronosyltransferases. Drug Metab. Dispos., 39: 1815-1822 (2011).
11. Rizzo, A., Pallone, F., Monteleone, G. and Fantini, M. C.: Intestinal inflammation and colorectal cancer: a double-edged sword? World J. Gastroenterol., 17: 3092-3100 (2011).
12. Degirolamo, C., Modica, S., Palasciano, G. and Moschetta, A.: Bile acids and colon cancer: Solving the puzzle with nuclear receptors. Trends Mol. Med., 17: 564-572 (2011).
13. Morris, G. P., Beck, P. L., Herridge, M. S., Depew, W. T., Szewczuk, M. R. and Wallace, J. L.: Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology, 96: 795-803 (1989).
14. Kretzmann, N. A., Fillmann, H., Mauriz, J. L., Marroni, C. A., Marroni, N., Gonzalez-Gallego, J. and Tunon, M. J.: Effects of glutamine on proinflammatory gene expression and activation of nuclear factor kappa B and signal transducers and activators of transcription in TNBS-induced colitis. Inflamm. Bowel Dis., 14: 1504-1513 (2008).
15. Masubuchi, Y., Enoki, K. and Horie, T.: Down-regulation of hepatic cytochrome P450 enzymes in rats with trinitrobenzene sulfonic acidinduced colitis. Drug Metab. Dispos., 36: 597-603 (2008).
16. Xia, Y. and Zweier, J. L.: Measurement of myeloperoxidase in leukocytecontaining tissues. Anal. Biochem., 245: 93-96 (1997).
17. Lee, J. H., Lee, B., Lee, H. S., Bae, E. A., Lee, H., Ahn, Y. T., Lim, K. S., Huh, C. S. and Kim, D. H.: Lactobacillus suntoryeus inhibits proinflammatory cytokine expression and TLR-4-linked NF-kappaB activation in experimental colitis. Int. J. Colorectal Dis., 24: 231-237 (2009).
18. Richardson, T. A. and Morgan, E. T.: Hepatic cytochrome P450 gene regulation during endotoxin-induced inflammation in nuclear receptor knockout mice. J. Pharmacol. Exp. Ther., 314: 703-709 (2005).
19. Wang, Q., Hao, H., Zhu, X., Yu, G., Lai, L., Liu, Y., Wang, Y., Jiang, S. and Wang, G.: Regioselective glucuronidation of tanshinone iia after quinone reduction: identification of human UDP-glucuronosyltransferases, species differences, and interaction potential. Drug Metab. Dispos., 38: 1132-1140 (2010).
20. Shiratani, H., Katoh, M., Nakajima, M. and Yokoi, T.: Species differences in UDP-glucuronosyltransferase activities in mice and rats. Drug Metab. Dispos., 36: 1745-1752 (2008).
21. Jiang, H., Wang, Y., Shet, M. S., Zhang, Y., Zenke, D. and Fast, D. M.: Development and validation of a sensitive LC/MS/MS method for the simultaneous determination of naloxone and its metabolites in mouse plasma. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 879: 2663-2668 (2011).
22. Shelby, M. K., Cherrington, N. J., Vansell, N. R. and Klaassen, C. D.: Tissue mRNA expression of the rat UDP-glucuronosyltransferase gene family. Drug Metab. Dispos., 31: 326-333 (2003).
23. Yu, C., Ritter, J. K., Krieg, R. J., Rege, B., Karnes, T. H. and Sarkar, M. A.: Effect of chronic renal insufficiency on hepatic and renal udpglucuronyltransferases in rats. Drug Metab. Dispos., 34: 621-627 (2006).
24. Miles, K. K., Kessler, F. K., Smith, P. C. and Ritter, J. K.: Characterization of rat intestinal microsomal UDP-glucuronosyltransferase activity toward mycophenolic acid. Drug Metab. Dispos., 34: 1632-1639 (2006).
25. King, C. D., Rios, G. R., Green, M. D., MacKenzie, P. I. and Tephly, T. R.: Comparison of stably expressed rat UGT1.1 and UGT2B1 in the glucuronidation of opioid compounds. Drug Metab. Dispos., 25: 251-255 (1997).
26. Chen, Y. L., Florentin, I., Batt, A. M., Ferrari, L., Giroud, J. P. and Chauvelot-Moachon, L.: Effects of interleukin-6 on cytochrome P450-dependent mixed-function oxidases in the rat. Biochem. Pharmacol., 44: 137-148 (1992).
27. Bánhegyi, G., Mucha, I., Garzo, T., Antoni, F. and Mandl, J.: Endotoxin inhibits glucuronidation in the liver. An effect mediated by intercellular communication. Biochem. Pharmacol., 49: 65-68 (1995).
28. Monshouwer, M., Witkamp, R. F., Nujmeijer, S. M., Van Amsterdam, J. G. and Van Miert, A. S.: Suppression of cytochrome P450-and UDP glucuronosyl transferase-dependent enzyme activities by proinflammatory cytokines and possible role of nitric oxide in primary cultures of pig hepatocytes. Toxicol. Appl. Pharmacol., 137: 237-244 (1996).
29. Mackenzie, P. I., Gregory, P. A., Gardner-Stephen, D. A., Lewinsky, R. H., Jorgensen, B. R., Nishiyama, T., Xie, W. and Radominska-Pandya, A.: Regulation of UDP glucuronosyltransferase genes. Curr. Drug Metab., 4: 249-257 (2003).
30. Weidenbach, H., Leiz, S., Nussler, A. K., Dikopoulos, N., Bachem, M., Buttenschoen, K., Reinshagen, M., Beger, H. G., Adler, G. and Schmid, R. M.: Disturbed bile secretion and cytochrome P450 function during the acute state of experimental colitis in rats. J. Hepatol., 32: 708-717 (2000).
31. Guidi, L., Costanzo, M., Ciarniello, M., De Vitis, I., Pioli, C., Gatta, L., Pace, L., Tricerri, A., Bartoloni, C., Coppola, L., Balistreri, P., Doria, G., Fedeli, G. and Gasbarrini, G. B.: Increased levels of NF-kappaB inhibitors (IkappaBalpha and IkappaBgamma) in the intestinal mucosa of Crohn's disease patients during infliximab treatment. Int. J. Immunopathol. Pharmacol., 18: 155-164 (2005).
32. Stio, M., Martinesi, M., Bruni, S., Treves, C., Mathieu, C., Verstuyf, A., d'Albasio, G., Bagnoli, S. and Bonanomi, A. G.: The Vitamin D analogue TX 527 blocks NF-kappaB activation in peripheral blood mononuclear cells of patients with Crohn's disease. J. Steroid Biochem. Mol. Biol., 103: 51-60 (2007).
33. Neurath, M. F., Pettersson, S., Meyer zum Buschenfelde, K. H. and Strober, W.: Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat. Med., 2: 998-1004 (1996).
34. Tochigi, Y., Yamashiki, N., Ohgiya, S., Ganaha, S. and Yokota, H.: Isoform-specific expression and induction of udp-glucuronosyltransferase in immunoactivated peritoneal macrophages of the rat. Drug Metab. Dispos., 33: 1391-1398 (2005).
35. Willey, J. C., Coy, E., Brolly, C., Utell, M. J., Frampton, M. W., Hammersley, J., Thilly, W. G., Olson, D. and Cairns, K.: Xenobiotic metabolism enzyme gene expression in human bronchial epithelial and alveolar macrophage cells. Am. J. Respir. Cell Mol. Biol., 14: 262-271 (1996).
36. Yamashiki, N., Yokota, H., Sakamoto, M. and Yuasa, A.: Presence of phenol UDP-glucuronosyltransferase in bovine alveolar macrophages and bronchial epithelial cells. Toxicology, 176: 221-227 (2002).
37. Oesch, F., Arand, M., Coughtrie, M. W., Burchell, B. and Steinberg, P.: The distribution of UDP-glucuronosyltransferases in rat liver parenchymal and nonparenchymal cells. Biochem. Pharmacol., 43: 731-737 (1992).
38. Ganousis, L. G., Goon, D., Zyglewska, T., Wu, K. K. and Ross, D.: Cellspecific metabolism in mouse bone marrow stroma: studies of activation and detoxification of benzene metabolites. Mol. Pharmacol., 42: 1118-1125 (1992).
39. Picard, N., Ratanasavanh, D., Premaud, A., Le Meur, Y. and Marquet, P.: Identification of the UDP-glucuronosyltransferase isoforms involved in mycophenolic acid phase II metabolism. Drug Metab. Dispos., 33: 139-146 (2005).
40. Morgan, E. T.: Regulation of cytochromes P450 during inflammation and infection. Drug Metab. Rev., 29: 1129-1188 (1997).
41. Morgan, E. T.: Regulation of cytochrome p450 by inflammatory mediators: why and how? Drug Metab. Dispos., 29: 207-212 (2001).
42. Cheng, P. Y., Wang, M. and Morgan, E. T.: Rapid transcriptional suppression of rat cytochrome P450 genes by endotoxin treatment and its inhibition by curcumin. J. Pharmacol. Exp. Ther., 307: 1205-1212 (2003).
43. Aitken, A. E., Richardson, T. A. and Morgan, E. T.: Regulation of drugmetabolizing enzymes and transporters in inflammation. Annu. Rev. Pharmacol. Toxicol., 46: 123-149 (2006).
44. Bock, K. W.: Functions and transcriptional regulation of adult human hepatic UDP-glucuronosyl-transferases (UGTs): mechanisms responsible for interindividual variation of UGT levels. Biochem. Pharmacol., 80: 771-777 (2010).
45. Ke, S., Rabson, A. B., Germino, J. F., Gallo, M. A. and Tian, Y.: Mechanism of suppression of cytochrome P-450 1A1 expression by tumor necrosis factor-alpha and lipopolysaccharide. J. Biol. Chem., 276: 39638-39644 (2001).
46. Zhou, C., Tabb, M. M., Nelson, E. L., Grun, F., Verma, S., Sadatrafiei, A., Lin, M., Mallick, S., Forman, B. M., Thummel, K. E. and Blumberg, B.: Mutual repression between steroid and xenobiotic receptor and NFkappaB signaling pathways links xenobiotic metabolism and inflammation. J. Clin. Invest., 116: 2280-2289 (2006).
47. Langmann, T., Moehle, C., Mauerer, R., Scharl, M., Liebisch, G., Zahn, A., Stremmel, W. and Schmitz, G.: Loss of detoxification in inflammatory bowel disease: dysregulation of pregnane X receptor target genes. Gastroenterology, 127: 26-40 (2004).
48. Leite, R. S., Brown, A. G. and Strauss, J. F., 3rd: Tumor necrosis factoralpha suppresses the expression of steroid receptor coactivator-1 and-2: a possible mechanism contributing to changes in steroid hormone responsiveness. FASEB J., 18: 1418-1420 (2004).
49. Beigneux, A. P., Moser, A. H., Shigenaga, J. K., Grunfeld, C. and Feingold, K. R.: Reduction in cytochrome P-450 enzyme expression is associated with repression of CAR (constitutive androstane receptor) and PXR (pregnane X receptor) in mouse liver during the acute phase response. Biochem. Biophys. Res. Commun., 293: 145-149 (2002).
50. Kakizaki, S., Yamazaki, Y., Takizawa, D. and Negishi, M.: New insights on the xenobiotic-sensing nuclear receptors in liver diseases-CAR and PXR. Curr. Drug Metab., 9: 614-621 (2008).
51. Ghose, R., Guo, T. and Haque, N.: Regulation of gene expression of hepatic drug metabolizing enzymes and transporters by the Toll-like receptor 2 ligand, lipoteichoic acid. Arch. Biochem. Biophys., 481: 123-130 (2009).
52. Ihunnah, C. A., Jiang, M. and Xie, W.: Nuclear receptor PXR, transcriptional circuits and metabolic relevance. Biochim. Biophys. Acta, 1812: 956-963 (2011).
53. Kiss, E. A., Vonarbourg, C., Kopfmann, S., Hobeika, E., Finke, D., Esser, C. and Diefenbach, A.: Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science, 334: 1561-1565 (2011).
54. Pot, C.: Aryl hydrocarbon receptor controls regulatory CD4+ T cell function. Swiss Med. Wkly., 142: w13592 (2012).
55. Stockinger, B., Hirota, K., Duarte, J. and Veldhoen, M.: External influences on the immune system via activation of the aryl hydrocarbon receptor. Semin. Immunol., 23: 99-105 (2011).
56. Kimura, A., Naka, T., Nohara, K., Fujii-Kuriyama, Y. and Kishimoto, T.: Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl. Acad. Sci. USA, 105: 9721-9726 (2008).
57. Quintana, F. J., Basso, A. S., Iglesias, A. H., Korn, T., Farez, M. F., Bettelli, E., Caccamo, M., Oukka, M. and Weiner, H. L.: Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature, 453: 65-71 (2008).
58. Kimura, A., Naka, T., Nakahama, T., Chinen, I., Masuda, K., Nohara, K., Fujii-Kuriyama, Y. and Kishimoto, T.: Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. J. Exp. Med., 206: 2027-2035 (2009).
59. Tukey, R. H. and Strassburg, C. P.: Human UDP-glucuronosyltransferases: metabolism, expression, and disease. Annu. Rev. Pharmacol. Toxicol., 40: 581-616 (2000).
60. Rhodes, J. M., Gallimore, R., Elias, E., Allan, R. N. and Kennedy, J. F.: Faecal mucus degrading glycosidases in ulcerative colitis and Crohn's disease. Gut, 26: 761-765 (1985).
61. Joh, E. H., Lee, I. A., Han, S. J., Chae, S. and Kim, D. H.: Lancemaside A ameliorates colitis by inhibiting NF-kappaB activation in TNBS-induced colitis mice. Int. J. Colorectal Dis., 25: 545-551 (2010).
62. Ullman, T. A. and Itzkowitz, S. H.: Intestinal inflammation and cancer. Gastroenterology, 140: 1807-1816 (2011).