Isothiocyanates induce UGT1A1 in humanized UGT1 mice in a CAR dependent fashion that is highly dependent upon oxidative stress

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Yoda, Emiko ^a,b   Paszek, Miles ^a   Konopnicki, Camille ^a   Fujiwara, Ryoichi ^c   Chen, Shujuan ^a   Tukey, Robert H ^a  

^a San Diego   (United States)

^b SHOWA UNIVERSITY   (Japan)

^c KITASATO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; CELL RECEPTOR; CONSTITUTIVE ANDROSTANE RECEPTOR; GLUCURONOSYLTRANSFERASE; ISOTHIOCYANIC ACID DERIVATIVE; NFE2L2 PROTEIN, MOUSE; PHENETHYL ISOTHIOCYANATE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; UGT1A1 ENZYME;

ANIMAL; BIOSYNTHESIS; BLOOD; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIVER; METABOLISM; MOUSE; OXIDATIVE STRESS; TRANSGENIC MOUSE;

ANIMALS; BILIRUBIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONOSYLTRANSFERASE; HUMANS; ISOTHIOCYANATES; LIVER; MICE; MICE, TRANSGENIC; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 85017659539     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep46489     Document Type: Article

References (50)

1. Keck, A. S., Finley, J. W. Cruciferous vegetables: Cancer protective mechanisms of glucosinolate hydrolysis products and selenium. Integr Cancer Ther 3, 5-12 (2004).
2. Talalay, P., Fahey, J. W. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. JNutr 131, 3027S-3033S (2001).
3. Murillo, G., Mehta, R. G. Cruciferous vegetables and cancer prevention. Nutr Cancer 41, 17-28 (2001).
4. Shapiro, T. A., et al. Safety, tolerance, metabolism of broccoli sprout glucosinolates and isothiocyanates: A clinical phase I study. Nutr Cancer 55, 53-62 (2006).
5. Shapiro, T. A., Fahey, J. W., Wade, K. L., Stephenson, K. K., Talalay, P. Chemoprotective glucosinolates and isothiocyanates ofbroccoli sprouts: Metabolism and excretion in humans. Cancer Epidemiol Biomarkers Prev 10, 501-508 (2001).
6. Li, W., Kong, A. N. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol Carcinog 48, 91-104 (2009).
7. Favreau, L. V., Pickett, C. B. Transcriptional regulation of the rat NAD(P)H:quinone reductase gene Identification of regulatoryelements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J. Biol. Chem 266, 4556-4561 (1991).
8. Rushmore, T. H., Morton, M. R., Pickett, C. B. The antioxidant responsive element Activation by oxidative stress and identificationof the DNA consensus sequence required for functional activity. J. Biol. Chem 266, 11632-11639 (1991).
9. Shen, G., Kong, A. N. Nrf2 plays an important role in coordinated regulation of Phase II drug metabolism enzymes and Phase IIIdrug transporters. Biopharm. Drug Dispos 30, 345-355 (2009).
10. Dutton, G. J. Glucuronidation of drugs and other compounds (CRC Press, Inc., Boca Raton, 1980).
11. Tukey, R. H., Strassburg, C. P. Human UDP-Glucuronosyltransferases: Metabolism, Expression, Disease. Annu Rev PharmacolToxicol 40, 581-616 (2000).
12. Keppler, D., Leier, I., Jedlitschky, G., Konig, J. ATP-dependent transport of glutathione S-conjugates by the multidrug resistanceprotein MRP1 and its apical isoform MRP2. Chem. Biol. Interact 111-112, 153-161 (1998).
13. Kamisako, T., et al. Transport of monoglucuronosyl and bisglucuronosyl bilirubin by recombinant human and rat multidrugresistance protein 2. Hepatology 30, 485-490 (1999).
14. Keppler, D., Konig, J. Hepatic secretion of conjugated drugs and endogenous substances. Semin. Liver Dis 20, 265-272 (2000).
15. Mackenzie, P. I., et al. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet. Genomics 15, 677-685 (2005).
16. Strassburg, C. P., Manns, M. P., Tukey, R. H. Differential down regulation of the UDP-glucuronosyltransferase 1A locus is an earlyevent in human liver and biliary cancer. Cancer Res 57, 2979-2985 (1997).
17. Strassburg, C. P., Oldhafer, K., Manns, M. P., Tukey, R. H. Differential expression of the UGT1A locus in human liver, biliary, gastric tissue: Identification of UGT1A7 and UGT1A10 transcripts in extrahepatic tissue. Mol. Pharmacol 52, 212-220 (1997).
18. Strassburg, C. P., Nguyen, N., Manns, M. P., Tukey, R. H. Polymorphic expression of the UDP-glucuronosyltransferase UGT1Agene locus in human gastric epithelium. Molecular Pharmacology 54, 647-654 (1998).
19. Strassburg, C. P., Manns, M. P., Tukey, R. H. Expression of the UDP-glucuronosyltransferase 1A locus in human colon. Identificationand characterization of the novel extrahepatic UGT1A8. J. Biol. Chem 273, 8719-8726 (1998).
20. Fujiwara, R., Nguyen, N., Chen, S., Tukey, R. H. Developmental hyperbilirubinemia and CNS toxicity in mice humanized with theUDP glucuronosyltransferase 1 (UGT1) locus. Proc. Natl. Acad. Sci. USA 107, 5024-5029 (2010).
21. Chen, S., et al. Tissue-specific, inducible, hormonal control of the human UDP-glucuronosyltransferase-1 (UGT1) locus. J. Biol. Chem 280, 37547-37557 (2005).
22. Leakey, J. E., Hume, R., Burchell, B. Development of multiple activities of UDP-glucuronyltransferase in human liver. Biochem J243, 859-861 (1987).
23. Fujiwara, R., Chen, S., Karin, M., Tukey, R. H. Reduced expression of UGT1A1 in intestines of humanized UGT1 mice viainactivation of NF-kappaB leads to hyperbilirubinemia. Gastroenterology 142, 109-118 (2012).
24. Bosma, P. J., et al. Bilirubin UDP-glucuronosyltransferase 1 is the only relevant bilirubin glucuronidating isoform in man. J. Biol. Chem 269, 17960-17964 (1994).
25. Xie, W., et al. Control of steroid, heme, carcinogen metabolism by nuclear pregnane X receptor and constitutive androstanereceptor. Proc Natl Acad Sci USA 100, 4150-4155 (2003).
26. Sugatani, J., et al. Transcriptional regulation of human UGT1A1 gene expression: Activated glucocorticoid receptor enhancesconstitutive androstane receptor/pregnane X receptor-mediated UDP-glucuronosyltransferase 1A1 regulation with glucocorticoidreceptor-interacting protein 1. Mol. Pharmacol 67, 845-855 (2005).
27. Senekeo-Effenberger, K., et al. Expression of the Human UGT1 Locus in Transgenic Mice by 4-Chloro-6-(2, 3-xylidino)-2-pyrimidinylthioacetic Acid (WY-14643) and Implications on Drug Metabolism through Peroxisome Proliferator-ActivatedReceptor a Activation. Drug Metabolism and Disposition 35, 419-427 (2007).
28. Yueh, M. F., et al. Involvement of the xenobiotic response element (XRE) in ah receptor-mediated induction of human UDPglucuronosyltransferase1A1. Journal of Biological Chemistry 278, 15001-15006 (2003).
29. Yueh, M. F., Bonzo, J. A., Tukey, R. H. The role of Ah receptor in induction of human UDP-glucuronosyltransferase 1A1. MethodsEnzymol 400, 75-91 (2005).
30. Yueh, M. F., Tukey, R. H. Nrf2-Keap1 Signaling Pathway Regulates Human UGT1A1 Expression in Vitro and in Transgenic UGT1Mice. J. Biol. Chem 282, 8749-8758 (2007).
31. Chen, S., et al. Intestinal NCoR1, a regulator of epithelial cell maturation, controls neonatal hyperbilirubinemia. Proc Natl Acad SciUSA 114, E1432-E1440 (2017).
32. Nguyen, N., et al. Disruption of the Ugt1 locus in mice resembles human Crigler-Najjar type I disease. J. Biol. Chem 283, 7901-7911(2008).
33. Liu, M., et al. Cadmium and arsenic override NF-kappaB developmental regulation of the intestinal UGT1A1 gene and control ofhyperbilirubinemia. Biochem Pharmacol 110-111, 37-46 (2016).
34. Mendelson, K. G., Contois, L. R., Tevosian, S. G., Davis, R. J., Paulson, K. E. Independent regulation of JNK/p38 mitogen-activatedprotein kinases by metabolic oxidative stress in the liver. Proc Natl Acad Sci USA 93, 12908-12913 (1996).
35. Rizzardini, M., Carelli, M., Cabello Porras, M. R., Cantoni, L. Mechanisms of endotoxin-induced haem oxygenase mRNAaccumulation in mouse liver: Synergism by glutathione depletion and protection by N-acetylcysteine. Biochem. J 304 (Pt 2), 477-483(1994).
36. Jo, Y. S., et al. Phosphorylation of the nuclear receptor corepressor 1 by protein kinase B switches its corepressor targets in the liverin mice. Hepatology 62, 1606-1618 (2015).
37. Keum, Y. S., Owuor, E. D., Kim, B. R., Hu, R., Kong, A. N. Involvement of Nrf2 and JNK1 in the activation of antioxidant responsiveelement (ARE) by chemopreventive agent phenethyl isothiocyanate (PEITC). Pharm. Res 20, 1351-1356 (2003).
38. Xu, C., et al. Mechanism of action of isothiocyanates: The induction of ARE-regulated genes is associated with activation of ERK andJNK and the phosphorylation and nuclear translocation of Nrf2. Mol. Cancer Ther 5, 1918-1926 (2006).
39. Boyanapalli, S. S., et al. Nrf2 knockout attenuates the anti-inflammatory effects of phenethyl isothiocyanate and curcumin. Chem ResToxicol 27, 2036-2043 (2014).
40. Venugopal, R., Jaiswal, A. K. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant responseelement-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. USA 93, 14960-14965 (1996).
41. Nguyen, T., Sherratt, P. J., Pickett, C. B. Regulatory mechanisms controlling gene expression mediated by the antioxidant responseelement. Annu. Rev. Pharmacol. Toxicol 43, 233-260 (2003).
42. Tukey, R. H., Billings, R. E., Tephly, T. R. Separation of oestrone UDP-glucuronyltransferase and p-nitrophenol UDPglucuronyltransferaseactivities. Biochem. J 171, 659-663 (1978).
43. Chen, S., Yueh, M. F., Evans, R. M., Tukey, R. H. The Pregnane-X-receptor controls hepatic glucuronidation during pregnancy andneonatal development in humanized UGT1 Mice. Hepatology 56, 658-667 (2012).
44. Choi, H. K., et al. Protein kinase A phosphorylates NCoR to enhance its nuclear translocation and repressive function in humanprostate cancer cells. J Cell Physiol 228, 1159-1165 (2013).
45. Kawamoto, T., et al. Phenobarbital-responsive nuclear translocation of the receptor CAR in induction of the CYP2B gene. Mol. CellBiol 19, 6318-6322 (1999).
46. Ashino, T., Ohkubo-Morita, H., Yamamoto, M., Yoshida, T., Numazawa, S. Possible involvement of nuclear factor erythroid2-related factor 2 in the gene expression of Cyp2b10 and Cyp2a5. Redox Biol 2, 284-288 (2014).
47. Stocker, R., Glazer, A. N., Ames, B. N. Antioxidant activity of albumin-bound bilirubin. Proc. Natl. Acad. Sci. USA 84, 5918-5922(1987).
48. Temme, E. H., Zhang, J., Schouten, E. G., Kesteloot, H. Serum bilirubin and 10-year mortality risk in a Belgian population. CancerCauses Control 12, 887-894 (2001).
49. Yamamoto, Y., Moore, R., Goldsworthy, T. L., Negishi, M., Maronpot, R. R. The orphan nuclear receptor constitutive active/androstane receptor is essential for liver tumor promotion by phenobarbital in mice. Cancer Res 64, 7197-7200 (2004).
50. Karin, M., Dhar, D. Liver carcinogenesis: From naughty chemicals to soothing fat and the surprising role of NRF2. Carcinogenesis37, 541-546 (2016).