Roles of human UDP-glucuronosyltransferases in clearance and homeostasis of endogenous substrates, and functional implications

Biochemical Pharmacology

Volumn 96, Issue 2, 2015, Pages 77-82

  Bock, Karl Walter ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

20 HETE; Bilirubin; Serotonin; UDP glucuronosyltransferase; Vitamins A and D

Indexed keywords

20 HYDROXYICOSATETRAENOIC ACID; BILE ACID; BILIRUBIN; GLUCURONOSYLTRANSFERASE; ICOSANOID; LEVOTHYROXINE; LIGAND; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PREGNANE X RECEPTOR; RETINOL; SEROTONIN; STEROID HORMONE; THYROXINE; TRANSCRIPTION FACTOR NRF2; VITAMIN D; 20-HYDROXY-5,8,11,14-EICOSATETRAENOIC ACID; AROMATIC HYDROCARBON RECEPTOR; HYDROXYICOSATETRAENOIC ACID; LEUKOTRIENE B4;

ARTICLE; BILE ACID BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; CLEARANCE; CONJUGATION; DNA RESPONSIVE ELEMENT; ENTEROHEPATIC CIRCULATION; ENZYME SUBSTRATE; GLUCURONIDATION; HIGH THROUGHPUT SCREENING; HOMEOSTASIS; HORMONE BLOOD LEVEL; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SEROTONIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; ENZYME SPECIFICITY; FEEDBACK SYSTEM; METABOLISM;

BILIRUBIN; FEEDBACK, PHYSIOLOGICAL; GLUCURONOSYLTRANSFERASE; HOMEOSTASIS; HUMANS; HYDROXYEICOSATETRAENOIC ACIDS; LEUKOTRIENE B4; NF-E2-RELATED FACTOR 2; RECEPTORS, ARYL HYDROCARBON; SEROTONIN; SUBSTRATE SPECIFICITY; THYROXINE; VITAMIN A; VITAMIN D;

EID: 84930571686     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.04.020     Document Type: Note

References (77)

1. C.J. Omiecinski, J.P. Vanden Heuvel, G.H. Perdew, and J.M. Peters Xenobiotic metabolism, disposition, and regulation by receptors: From biochemical phenomenon to predictors of major toxicities Toxicol. Sci. 120 2011 S49 S75
2. A. Rowland, J.O. Miners, and P.I. Mackenzie The UDP-glucuronosyltransferases. Their role in drug metabolism and detoxification Int. J. Biochem. Cell Biol. 45 2013 1121 1132
3. C. Guillemette, E. Levesques, and M. Rouleau Pharmacogenomics of human uridine diphospho-glucuronosyltransferases (UGTs) and clinical implications Clin. Pharmacol. Ther. 96 2014 324 339
4. K.W. Bock Homeostatic control of xeno- and endobiotics in the drug-metabolizing enzyme system Biochem. Pharmacol. 90 2014 1 6
5. D.G. Hu, R. Meech, R.A. McKinnon, and P.I. Mackenzie Transcriptional regulation of human UDP-glucuronosyltransferase genes Drug Metab. Rev. 46 2014 421 458
6. A. Chawla, J.J. Repa, R.M. Evans, and D.J. Mangelsdorf Nuclear receptors and lipid physiology: opening the X-files Science 294 2001 1866 1870
7. Y.Z. Gu, J.B. Hogenesch, and C.A. Bradfield The PAS superfamily: sensors of environmental and developmental signals Ann. Rev. Pharmacol. Toxicol. 40 2000 519 561
8. J. Kapitulnik Bilirubin: an endogenous product of heme degradation with both cytotoxic and cytoprotective properties Mol. Pharmacol. 66 2004 773 779
9. M.W. Coughtrie, B. Burchell, J.E. Leakey, and R. Hume The inadequacy of perinatal glucuronidation: immunoblot analysis of the developmental expression of individual UDP-glucuronosyltransferase isoenzymes in rat and human liver microsomes Mol. Pharmacol. 34 1988 729 735
10. L. Novotny, and L. Vitek Inverse relationship between serum bilirubin and atherosclerosis in men: a meta-analysis of published studies Exp. Biol. Med. 228 2003 568 571
11. J.P. Lin, C.J. O'Donnell, J.P. Schwaiger, L.A. Cupples, A. Lingenhel, and S.C. Hunt Association between UDP1A1∗28 allele, bilirubin levels, and coronary heart disease in the Framingham Heart Study Circulation 114 2008 1476 1481
12. A.R. Kundur, I. Singh, and A.C. Bulmer Bilirubin, platelet activation and heart disease: a missing link to cardiovascular protection in Gilbert's syndrome Atherosclerosis 239 2014 73 84
13. D.E. Baranano, M. Rao, C.D. Ferris, and S.H. Snyder Biliverdin reductase: a major physiologic cytoprotectant Proc. Natl. Acad. Sci. U.S.A. 160 2002 93 98
14. A. Abu-Bakar, D.M. Arthur, A.S. Wikman, M. Rahnasto, R.O. Juvonen, and J. Vepsäläinen Metabolism of bilirubin by human cytochrome P450 2A6 Toxicol. Appl. Pharmacol. 15 2012 50 58
15. S.N. Muhsain, M.A. Lang, and A. Abu-Bakar Mitochondrial targeting of bilirubin regulatory enzymes: an adaptive response to oxidative stress Toxicol. Appl. Pharmacol. 282 2015 77 89
16. K. Sumida, M. Kawana, E. Kouno, T. Itoh, S. Takano, and T. Narawa Importance of UDP-glucuronosyltransferase 1A1 expression in skin and its induction by UVB in neonatal hyperbilirubinemia Mol. Pharmacol. 84 2013 679 686
17. E. Fritsche, C. Schäfer, C. Calles, T. Bernsmann, T. Bershausen, and M. Wurm Lightening up the UV response by identification of the aryl hydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation Proc. Natl. Acad. Sci. U.S.A. 104 2007 8851 8856
18. M.D. Gershon 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract Curr. Opin. Endocrinol. Diabetes Obes. 20 2013 14 21
19. S. Krishnaswamy, S.X. Duan, L.L. von Moltke, D.J. Greenblatt, and M.H. Court Validation of serotonin (5-hydroxytryptamine) as an in vitro substrate probe for human UDP-glucuronosyltransferase (UGT) 1A6 Drug Metab. Disp. 31 2003 133 139
20. S. Krishnaswamy, Q. Hao, A. Al-Rohaimi, L.M. Hesse, L.L. von Moltke, D.J. Greenblatt, and M.H. Court UDP glucuronosyltransferase (UGT) 1A6 pharmacogenetics: II. Functional impact of the three most common nonsynonymous UGT1A6 polymorphisms (S7A, T181A, and R184S) J. Pharmacol. Exp. Ther. 313 2005 1340 1346
21. A. Helander, O. Beck, and L. Boysen 5-Hydroxytryptophol conjugation in man: Influence of alcohol consumption and altered serotonin turnover Life Sci. 56 1995 1529 1534
22. C. Köhle, O.A. Badary, K. Nill, B.S. Bock-Hennig, and K.W. Bock Serotonin glucuronidation by Ah receptor- and oxidative stress-inducible human UDP-glucuronosyltransferase (UGT) 1A6 in Caco-2 cells Biochem. Pharmacol. 69 2005 1397 1402
23. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Ann. Rev. Pharmacol. Toxicol. 47 2007 89 116
24. M. Ouzzine, S. Gulberti, N. Ramalanjaona, J. Magdalou, and S. Fournel-Gigleux The UDP-glucuronosyltransferases of the blood-brain barrier: Their role in drug metabolism and detoxication Frontiers Cell Neurosci. 8 2014 1 12
25. J.W. Lampe, J. Bigler, N.K. Horner, J.D. Potter. UDP-glucuronosyltransferase (UGT1A1∗28 and UGT1A6∗2) polymorphisms in Caucasians and Asians: Relationship to serum bilirubin concentrations. Pharmacogenetics 199 (9) 341-349.
26. C. Köhle, B. Möhrle, P.A. Münzel, M. Schwab, D. Wernet, and O.A. Badary Frequent co-occurrence of the TATA box mutation associated with Gilbert's syndrome (UGT1A1∗28) with other polymorphisms of the UDP-glucuronosyltransferase-1 locus (UGT1A6∗2 and UGT1A7∗3) in Caucasians and Egyptians Biochem. Pharmacol. 65 2003 1521 1527
27. P. Lee, G. Jones, and M.J. Seibel Dual polymorphisms in UDP-glucuronosyltransferases 1A1 and 1A6: A novel mechanism for hyperserotoninemia in Gilbert's syndrome mimicking carcinoid syndrome Eur. J. Gastroenterol. Hepatol. 19 2007 337 340
28. A. Maladaki, M.P. Yavropoulou, K. Kotsa, T. Tranga, S. Ventis, and J.G. Yovos Non tumoral hyperserotoninaemia responsive to octreotide due to dual polymorphism in UGT1A1 and UGT1A6 Hormones 11 2012 104 108
29. D.W. Nebert, and C.L. Karp Endogenous functions of the aryl hydrocarbon receptor (AHR): Intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology J. Biol. Chem. 283 2008 36061 36065
30. D. Turgeon, S. Chouinard, P. Belanger, S. Picard, J.F. Labbe, and P. Borgeat Glucuronidation of arachidonic and linoleic acid metabolites by UDP-glucuronosyltransferases J. Lipid Res. 44 2003 1182 1191
31. J.M. Little, M. Kurkela, J. Sonka, S. Jäntti, R. Ketola, and S. Bratton Glucuronidation of oxidized fatty acids and prostaglandins B1 and E2 by human hepatic and recombinant UDP-glucuronosyltransferases J. Lipid Res. 45 2004 1694 1703
32. K.M. Knights, A. Rowland, and J.O. Miners Renal drug metabolism in humans: The potential for drug-endobiotic interactions involving cytochrome P450 (CYP) and UDP-glucuronosyltransferase (UGT) Br. J. Clin. Pharmacol. 76 2013 587 602
33. S. Chouinard, G. Pelletier, A. Belanger, and O. Barbier Isoform-specific regulation of uridine diphosphate-glucuronosyltransferase 2B enzymes in the human prostate: differential consequences for androgen and bioactive lipid inactivation Endocrinology 147 2006 5431 5442
34. Y.B. Jarrar, E.Y. Cha, K.A. Seo, J.L. Ghim, H.J. Kim, and D.H. Kim Determination of major UDP-glucuronosyltransferase enzymes and their genotypes responsible for 20-HETE glucuronidation J. Lipid Res. 55 2014 2334 2342
35. D. Sacerdoti, M. Balazy, P. Angeli, A. Gatta, and J.C. McGiff Eisosanoid excretion in hepatic cirrhosis. Predominance of 20-HETE J. Clin. Invest. 100 1997 1264 1270
36. C.C. Wu, and L. Schwartzman The role of 20-HETE in androgen-mediated hypertension Prostaglandins Other Lipid Mediat. 96 2011 45 53
37. K.A. Zemski Berry, P. Borgeat, J. Gosselin, L. Flamand, and R.C. Murphy Urinary metabolites of leukotriene B4 in the human subject J. Biol. Chem. 278 2003 24449 24460
38. S. Chouinard, M.F. Yueh, R.H. Tukey, F. Giton, J. Fiet, and G. Pelletier Inactivation by UDP-glucuronosyltransferase enzymes: the end of androgen signaling J. Steroid Biochem. Mol. Biol. 109 2008 247 253
39. C. Guillemette, A. Belanger, and J. Lepine Metabolic inactivation of estrogens in breast tissue by UDP-glucuronosyltransferase enzymes: an overview Breast Cancer Res. 6 2004 246 254
40. E. Audet-Walsh, J. Lepine, J. Gregoire, M. Plante, P. Caron, and B. Tetu Profiling of endogenous estrogens, their precursors, and metabolites in endometrial cancer patients: association with risk and relationship to clinical characteristics J. Clin. Endocrinol. Metab. 96 2011 E330 E339
41. A. Rane, and L. Ekström Androgens and doping tests: genetic variation and pitfalls Br. J. Clin. Pharmacol. 74 2012 3 15
42. N. Isoherranen, and K.E. Thummel Drug metabolism and transport during pregnancy: How does drug disposition change during pregnancy and what are the mechanisms that cause such changes Drug Metab. Disp. 41 2013 256 262
43. S. Chen, D. Beaton, N. Nguyen, K. Seneko-Effenberger, E. Brace-Sinokrak, and U. Argikar Tissue-specific, inducible, and hormonal control of the human UDP-glucuronosyltransfrase-1 (UGT1) locus J. Biol. Chem. 280 2005 37547 37557
44. J.H. Jeong, S. Choi, J.W. Song, H. Chen, and J.H. Fischer Regulation of UDP-glucuronosyltransferase (UGT) 1A1 by progesterone and its impact on labetalol elimination Xenobiotica 38 2008 62 75
45. H. Chen, K. Yang, S. Choi, J.H. Fischer, and H. Jeong Up-regulation of UDP-glucuronosyltransferase (UGT) 1A4 by 17ß-estradiol: A potential mechanism of increased lamotrigine elimination in pregnancy Drug Metab. Disp. 37 2009 1841 1847
46. J. Lepine, O. Bernard, M. Plante, B. Tetu, G. Pelletier, and F. Labrie Specificity and regioselectivity of the conjugation of estradiol, estrone, and their catecholestrogen and methoxyestrogen metabolites by human uridine diphospho-glucuronosyltransferases expressed in endometrium J. Clin. Endocrinol. Metab. 89 2004 5222 5232
47. E. Levesque, D. Turgeon, J.S. Carrier, V. Montminy, M. Beaulieu, and A. Belanger Isolation and characterization of the UGT2B28 cDNA encoding a novel human steroid conjugating UDP-glucuronosyltransferase Biochemistry 40 2001 3869 3881
48. A. Stiel, R. Raedsch, G. Rudolph, U. Gundert-Remy, and M. Senn Biliary and urinary excretion of sulfated, glucuronidated, and tetrahydroxylated bile acids in cirrhotic patients Hepatol 5 1985 492 495
49. O. Barbier, J. Trottier, J. Kaeding, P. Caron, and M. Verreault Lipid-activated transcription factors control bile acid glucuronidation Mol. Cell Biochem. 326 2009 3 8
50. M.H. Court, X. Zhang, X. Ding, K.K. Yee, L.M. Hesse, and M. Finel Quantitative distribution of mRNAs encoding 19 human UDP-glucuronosyltransferase enzymes in 26 adult and 3 fetal tissues Xenobiotica 42 2012 266 277
51. J. Shoda, R. Mahara, T. Osuga, M. Tohma, S. Ohnishi, and H. Miazaki Similarity of unusual bile acids in human umbilical cord blood and amniotic fluid from newborns and in the sera from adult patients with cholestatic liver diseases J. Lipid Res. 29 1988 847 858
52. A.F. McDonagh, L.A. Palma, and R. Schmid Reduction of biliverdin and placental transfer of bilirubin and biliverdin in the pregnant guinea pig Biochem. J. 194 1981 273 282
53. A.L. Yoder Graber, J. Ramirez, F. Innocenti, and M.J. Ratain UGT1A1∗28 genotype affects the in-vitro glucuronidation in human livers Pharmacogenet. Genom. 17 2007 619 627
54. V.M. Richardson, S.S. Ferguson, Y.M. Sey, and M.J. DeVito In vitro metabolism of thyroxine by rat and human hepatocytes Xenobiotica 44 2014 391 403
55. Y. Kato, S.I. Ikushiro, Y. Emi, S. Tamaki, H. Suzuki, and T. Sakaki Hepatic UDP-glucuronosyltransferases responsible for glucuronidation of thyroxine in humans Drug Metab. Disp. 36 2008 51 55
56. X.H. Tang, and L.J. Gudas Retinoids, retinoic acid receptors, and cancer Ann. Rev. Pathol. Mech. Dis. 6 2011 345 364
57. S.M. O'Byrne, and W.S. Blaner Retinol and retinyl esters: biochemistry and physiology J. Lipid Res. 54 2013 1731 1743
58. Y. Li, and W.S. Wongsiriroj Blaner The multifaceted nature of retinoid transport and metabolism Hepatobiliary Surg. Nutr. 3 2014 126 139
59. A.R. Topletz, S. Tripathy, R.S. Foti, J.A. Shimshoni, W.L. Nelson, and N. Isoherranen Induction of CYP26A1 by metabolites of retinoic acid: evidence that CYP26A1 is an important enzyme in the elimination of active retinoids Mol. Pharmacol. 87 2015 430 441
60. V.M. Samokyszyn, W.E. Gall, G. Zawada, M.A. Freyaldenhoven, G. Chen, and P.I. Mackenzie 4-Hydroxyretinoic acid, a novel substrate for human liver microsomal UDP-glucuronosyltransferase(s) and recombinant UGT2B7 J. Biol. Chem. 275 2000 6908 6914
61. Y. Lu, S. Bratton, J.M. Heydel, and A. Radomiska-Pandya Effect of retinoids on UDP-glucuronosyltransferase mRNA expression in Caco-2 cells Drug Metab. Pharmacokinet. 23 2008 364 372
62. H.F. DeLuca Evolution of our understanding of vitamin D Nutr. Rev. 66 2008 S73 S87
63. T. Hashizume, Y. Xu, J. Mohutzky Alberts, C. Hadden, and T.F. Kalhorn Identification of human UDP-glucuronosyltransferases catalyzing hepatic 1α, 25-dihydroxyvitamin D3 conjugation Biochem. Pharmacol. 75 2008 1240 1250
64. Z. Wang, T. Wong, T. Hashizume, L.Z. Dickmann, M. Scian, and N.J. Koszewski Human UGT1A4 and UGT1A3 conjugate 25-hydroxyvitamin D3: metabolite structure, kinetics, inducibility, and interindividual variability Endocrinology 155 2014 2052 2063
65. P. Fernandez-Salguero, T. Pineau, D.M. Hilbert, T. McPhail, S.S.T. Lee, and S. Kimura Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor Science 268 1995 722 726
66. L.P. Nguyen, and C.A. Bradfield The search for endogenous activators of the aryl hydrocarbon receptor Chem. Res. Toxicol. 21 2008 102 116
67. B. Stockinger, P. Di Meglio, M. Gialitakis, and J.H. Duarte The aryl hydrocarbon receptor: multitasking in the immune system Ann. Rev. Pharmacol. Toxicol. 32 2014 403 432
68. R.L. Yeager, S.A. Reisman, L.M. Aleksunes, and C.D. Klaassen Introducing the 'TCDD-inducible AhR-Nrf2 gene battery' Toxicol. Sci. 111 2009 238 246
69. P.A. Münzel, S. Schmohl, F. Buckler, J. Jaehrling, F.T. Raschko, C. Köhle, and K.W. Bock Contribution of the Ah receptor to the phenolic antioxidant-mediated expression of human and rat UDP-glucuronosyltransferase UGT1A6 in Caco-2 and rat hepatoma 5L cells Biochem. Pharmacol. 66 2003 841 847
70. P.A. Münzel, S. Schmohl, H. Heel, K. Kälberer, B.S. Bock-Hennig, and K.W. Bock Induction of human UDP-glucuronosyltransferases (UGT1A6, UGT1A9, and UGT2B7) by t-butylhydroquinone and 2,3,7,8-tetrachlorodibenzo-p-dioxin in Caco-2 cells Drug Metab. Disp. 27 1999 569 573
71. J. Sugatani Function, genetic polymorphism, and transcriptional regulation of human UDP-glucuronosyltransferase (UGT) 1A1 Drug Metab. Pharmacokin. 28 2013 83 92
72. W. Huang, J. Zhang, S.S. Chua, M. Qatanani, Y. Han, and R. Ganata Induction of bilirubin clearance by the constitutive androstane receptor (CAR) Proc. Natl. Acad. Sci. U.S.A. 100 2003 4156 4161
73. Y.E. Timsit, and M. Negishi CAR and PXR. The xenobiotic-sensing receptors Steroids 72 2007 231 246
74. M.W. Buczynski, D.S. Dumlao, and E.A. Dennis An integrated omics analysis of eicosanoid biology J. Lipid Res. 50 2009 1015 1038
75. V.R. Narala, R.K. Adapala, M.V. Suresh, T.G. Brock, M. Peters-Golden, and R. Reddy Leucotriene B4 is a physiologically relevant endogenous peroxysome proliferator-activated receptor-α agonist J. Biol. Chem. 285 2010 22067 22074
76. K.W. Bock Human UDP-glucuronosyltransferases. Feedback loops between substrates and ligands of their transcription factors Biochem. Pharmacol. 84 2012 1000 1006
77. C.S. Caspersen, B. Reznik, P.L. Weldy, K.M. Abildskov, R.I. Stark, and M. Garland Molecular cloning of the baboon UDP-glucuronosyltransferase 1A gene family. Evolution of the primate UGT1 locus and relevance for models of human drug metabolism Pharmacogenet. Genom. 17 2007 11 24