Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-05T10:14:30.738Z Has data issue: false hasContentIssue false

Influence of vitamin A status on the regulation of uridine (5′-)diphosphate-glucuronosyltransferase (UGT) 1A1 and UGT1A6 expression by L-triiodothyronine

Published online by Cambridge University Press:  09 March 2007

Valérie Haberkorn
Affiliation:
Unité de Biochimie-Pharmacologie-Toxicologie, Université de Bourgogne, 7 bd Jeanne d'Arc, BP 87900-21079, Dijon Cédex, France
Jean-Marie Heydel
Affiliation:
Unité de Biochimie-Pharmacologie-Toxicologie, Université de Bourgogne, 7 bd Jeanne d'Arc, BP 87900-21079, Dijon Cédex, France
Jacques Mounie
Affiliation:
Unité de Biochimie-Pharmacologie-Toxicologie, Université de Bourgogne, 7 bd Jeanne d'Arc, BP 87900-21079, Dijon Cédex, France
Yves Artur
Affiliation:
Unité de Biochimie-Pharmacologie-Toxicologie, Université de Bourgogne, 7 bd Jeanne d'Arc, BP 87900-21079, Dijon Cédex, France
Hervé Goudonnet*
Affiliation:
Unité de Biochimie-Pharmacologie-Toxicologie, Université de Bourgogne, 7 bd Jeanne d'Arc, BP 87900-21079, Dijon Cédex, France
*
**Corresponding author: Dr Hervé Goudonnet, fax +33 3 80 39 32 18, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The uridine (5′-)diphosphate-glucuronosyltransferases (UGT) are involved in the phase II of various xenobiotics and endogenous compounds. They are responsible for glucuronidation of many substrates, especially including bilirubin (UGT1A1) and phenolic compounds (UGT1A6). We previously showed that the expression of both isoforms is regulated at the transcriptional level by thyroid hormone in rat liver. In this present study, effects of vitamin A dietary intake (0, 1.72, 69 ug retinol acetate/g food) on the regulation of UGT1A1 and UGT1A6 activity and expression by 3,5,3′ triiodo-L-THYRONINE (l-T3) were examined in the same organ. Activities were determined toward bilirubin and 4-nitrophenol. UGT mRNA were analysed by reverse transcription and amplification methods (reverse transcription–polymerase chain reaction) and quantified by capillary electrophoresis. In rats fed a vitamin A-balanced diet, a single injection of l-T3 (500 μg/kg body weight) increased UGT1A6 mRNA expression whereas this hormone decreased UGT1A1 mRNA expression. In addition we observed that the specific effect of l-T3 on UGT1A1 and UGT1A6 was reduced in animals receiving a vitamin A-enriched diet and disappeared in those fed a vitamin A-free diet. The modulations observed in mRNA expression are concomitant with those found for UGT activities. Our results demonstrate for the first time the existence of a strong interaction between vitamin A and thyroid hormone on the regulation of genes encoding cellular detoxification enzymes, in this case the UGT.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2001

References

Bendik, I & Pfahl, M (1994) Similar ligand-induced conformation changes of thyroid hormone receptors regulate homo- and heterodimeric functions. Journal of Biological Chemistry 270, 31073114.CrossRefGoogle Scholar
Colin-Neiger, A, Kauffman, I, Boutin, JA, Fournel, S, Siest, G, Batt, AM & Magdalou, J (1984) Assessment of the Mulder and Van Doorn kinetic procedure and rapid centrifugal analysis of UDP-glucuronosyltransferase activities. Journal of Biochemical and Biophysical Methods 9, 6979.CrossRefGoogle Scholar
Decaux, JF, Juanes, M, Bossard, P & Girard, J (1997) Effects of triiodothyronine and retinoic acid on glucokinase gene expression in neonatal rat hepatocytes. Molecular Cell Endocrinology 130, 6167.CrossRefGoogle ScholarPubMed
De #Sandro, V, Catinot, R, Kriszt, W, Cordier, A & Richert, L (1992) Male rat hepatic UDP-glucuronosyltransferase activity toward thyroxine activation and induction properties – relation with thyroxine plasma disappearance rate. Biochemical Pharmacology 43, 15631569.CrossRefGoogle ScholarPubMed
Goudonnet, H, Magdalou, J, Mounié, J, Naoumi, A, Viriot, ML, Escousse, A, Siest, G & Truchot, R (1990) Differential action of thyroid hormones and chemically related compounds on the activity of UDP-glucuronosyltransferases and cytochrome P-450 isozymes in rat liver. Biochemica et Biophysica Acta 1035, 1219.CrossRefGoogle ScholarPubMed
Haq, RU & Chytil, F (1992) Effect of retinoids on nuclear retinoic acid receptors mRNA in adipose tissue of retinol-deficient rats. Journal of Lipidic Research 33, 381384.Google Scholar
Heiger, DN & Cohen, AS (1990) Separation of DNA restriction fragments by high performance capillary electrophoresis with two and zero crosslinked polyacrylamide using continuous electric fields. Journal of Chromatography 516, 3348.CrossRefGoogle Scholar
Heirwerg, KPM, Van de Vijver, M & Fevery, J (1972) Assay and properties of digitonin-activated bilirubin uridine diphosphate glucuronosyltransferase from rat liver. Biochemical Journal 129, 605618.CrossRefGoogle Scholar
Hogeboom, HG (1955) Fractionation of cell components of animals tissues. Methods in Enzymology 1, 1619.CrossRefGoogle Scholar
Iyanagi, T, Haniu, M, Sogawa, K, Fujii-Kuriyama, Y, Watanabe, S, Shively, JE & Anan, KF (1986) Cloning and characterization of cDNA encoding 3-methylcholanthrene inducible rat mRNA for UDP-glucuronosyltransferase. Journal of Biological Chemistry 261, 1560715614.CrossRefGoogle ScholarPubMed
Jezequel-Cuer, M, Le Moel, G, Mounie, J, Le Bizec, C, Vernet, MH, Artur, Y, Laschi-Loquerie, A & Troupel, S (1995) Determination of serum or plasma alpha-tocopherol by high performance liquid chromatography: optimization of operative models. Annales de Biologie Clinique (Paris) 53, 343352.Google ScholarPubMed
Kostner, Ch, Nikolov, J & Riedel, E (1990) Analytical method for determination of iodothyronineglucuronides for evaluation of kinetic parameters of UDP-glucuronosyltransferase. Fresenius Journal of Analytical Chemistry 337, 5657.Google Scholar
Lehman, JM, Zhang, X-K, Graupner, G, Lee, M, Hermann, T, Hoffmann, B & Pfahl, M (1993) Formation of retinoid X receptor homodimer leads to repression of T3 reponse: hormonal cross talk by ligand-induced squelching. Molecular and Cellular Biology 13, 76987707.Google Scholar
Li, YO, Prentice, DA, Howard, ML, Mashford, ML & Desmond, PV (1999) The effects of hormones on the expression of five isoforms of UDP-glucuronosyltransferase in primary cultures of rat hepatocytes. Pharmaceutical Research 16, 191197.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJ (1951) Protein measurement with the Folin-phenol reagent. Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
Ma, XJ, Salati, LM, Ash, SE, Mitchell, DA, Kantley, SA, Fantozzi, DA & Goodridge, AG (1990) Nutritional regulation and tissue-specific expression of the malic enzyme gene in the chicken: transcriptional control and chromatin structure. Journal of Biological Chemistry 265, 1843518441.CrossRefGoogle ScholarPubMed
Mackenzie, PI, Owens, IS, Burchell, B, Bock, KW, Bairoch, A, Belanger, A, Fournel-Gigleux, S, Green, M, Hum, DW, Ianagy, T, Lancet, D, Louisot, P, Magdalou, J, Chowdhury, JR, Ritter, JK, Schachter, H, Tephly, TR, Tipton, KF & Nebert, DW (1997) The UDP-glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 7, 255269.CrossRefGoogle ScholarPubMed
Mano, H, Mori, R, Ozawa, T, Takeyama, K, Yoshizawa, Y, Kojima, R, Arao, Y, Masushige, S & Kato, S (1994) Positive and negative regulation of retinoid X receptor gene expression by thyroid hormone in the rat. Journal of Biological Chemistry 269, 15911594.CrossRefGoogle ScholarPubMed
Masmoudi, T, Planells, R, Mounié, J, Artur, Y, Magdalou, J & Goudonnet, H (1996) Opposite regulation of bilirubin and 4-nitrophenol UDP-glucuronosyltransferase mRNA levels by 3,3′,5 triiodo-L-thyronine in rat liver. FEBS Letters 379, 181185.CrossRefGoogle ScholarPubMed
Masmoudi, T, Hihi, AK, Vazquez, M, Desvergne, B, Wahli, W, Artur, Y & Goudonnet, H (1997 a) Transcriptional regulation by triiodothyronine UDP-glucuronosyltransferase family 1 gene complex in rat liver. Comparison with induction by 3-methylcholanthrene. Journal of Biological Chemistry 272, 1717117175.CrossRefGoogle ScholarPubMed
Masmoudi, T, Mounié, J, Artur, Y, Magdalou, J & Goudonnet, H (1997 b) Comparative quantification of two hepatic UDP-glucuronosyltransferase bilirubin isoform mRNA in various thyroid states in rats. Biochemical Pharmacology 53, 10131017.CrossRefGoogle Scholar
Mitsuhashi, T & Nikodem, V (1989) Regulation of expression of the alternative mRNAs of the rat α-thyroid hormone receptor gene. Journal of Biological Chemistry 264, 89008904.CrossRefGoogle ScholarPubMed
Mulder, RG & Van Doorn, A (1975) A rapid NAD+-linked assay for microsomal UDP-glucuronosyltransferases of rat liver and some observation on substrate specificity of the enzyme. Biochemistry Journal 151, 131140.CrossRefGoogle Scholar
Nagaya, T, Murata, Y, Yamaguchi, S, Nomura, Y, Ohmori, S, Fujieda, M, Katunuma, N, Yen, PM, Chin, WW & Seo, H (1998) Intracellular proteolitic cleavage of 9-cis-retinoic acid receptor a by cathepsin L-type protease is a potential mechanism for modulating thyroid hormone action Journal of Biological Chemistry 273, 3316633173.CrossRefGoogle Scholar
Nesi, M, Righetti, PG, Patrosso, MC, Ferlini, A & Chiari, M (1994) Capillary electrophoresis of polymerase chain reactionamplified products in polymer networks: the case of Kennedy's disease. Electrophoresis 15, 644646.CrossRefGoogle ScholarPubMed
Nudel, U, Zakut, R, Shani, M, Neuman, S, Levy, Z & Yaffe, D (1983) The nucleotide sequence of the rat cytoplasmic beta-actin gene. Nucleic Acids Research 11, 17591771.CrossRefGoogle ScholarPubMed
Oppenheimer, JH, Silva, E, Schwartz, HL & Surks, ML (1977) Stimulation of hepatic mitochondrial alpha-glycerophosphate deshydrogenase and malic enzyme by L-triiodothyronine. Characteristics of the response with specific nuclear thyroid hormone binding sites fully saturated. Journal of Clinical Investigation 59, 517527.CrossRefGoogle Scholar
Pailler-Rodde, I, Garcin, H & Higueret, P (1991 a) Effect of retinoids on protein kinase C activity and on the binding characteristics of the tri-iodothyronine nuclear receptor. Journal of Endocrinology 128, 245251.CrossRefGoogle ScholarPubMed
Pailler-Rodde, I, Garcin, H, Higueret, P & Begueret, J (1991 b) c-erb-A mRNA content and triiodothyronine nuclear receptor binding capacity in rat liver according to vitamin A status. FEBS Letters 289, 3336.CrossRefGoogle ScholarPubMed
Park, EJ, Schroen, DJ, Yang, M, Li, H, Li, L & Don Chen, J (1999) SMRTe, a silencing mediator for retinoid and thyroid hormone receptors-extended isoform that is more related to the nuclear receptor corepressor. Proceedings of National Academy of Sciences USA 96, 35193524.CrossRefGoogle Scholar
Potier de #courcy, G, Durand, G, Abraham, J & Gueguen, L (1989) Recommendations of the feeding conditions of the laboratory animals (rats and mice). Sciences des Aliments 9, 209217.Google Scholar
Ratanasavanh, X (1990) Effect of retinol and retinoic acid supplemented diets on cytochrome P-450 content and UDPGT activities in vitamin A-deficient rat liver. Food Additives and Contaminants 7, S103-S105.CrossRefGoogle Scholar
Samuels, HH, Forman, BM, Horowitz, ZD & Ye, ZS (1988) Regulation of gene expression by thyroid hormone. Journal of Clinical Investigation 81, 957967.CrossRefGoogle ScholarPubMed
Sap, J, Munoz, A, Damm, K, Goldberg, Y, Ghysdael, J, Leutz, A, Beug, H & Vennströ#m, B (1986) The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature 324, 635640.CrossRefGoogle ScholarPubMed
Sato, H, Koïwai, O, Tanabe, K & Kashiwamata, S (1990) Isolation and sequencing of the rat liver bilirubin UDP-glucuronosyltransferase cDNA: possible alternate splicing of a common primary transcript. Biochemical and Biophysical Research Communications 169, 260264.??CrossRefGoogle ScholarPubMed
Schwartz, HE, Ulfelder, K, Sunzeri, FJ, Busch, MP & Brownlee, RG (1991) Analysis of DNA restriction fragments and polymerase chain reaction products towards detection of the AIDS (HIV1) virus in blood. Journal of Chromatography 559, 267283.CrossRefGoogle ScholarPubMed
Tzameli, I & Zannis, V (1996) Binding specificity and modulation of the ApoA-1 promoter activity by homo- and heterodimers of nuclear receptor. Journal of Biological Chemistry 271, 84028415.CrossRefGoogle Scholar
Verma, AJ, Shoemaker, A, Simsiman, R, Denning, M & Zachman, R (1992) Expression of retinoic acid nuclear receptors and tissue transglutaminase is altered in various tissues of rats fed a vitamin A-deficient diet. Journal of Nutrition 122, 21442152.CrossRefGoogle ScholarPubMed
Visser, TJ, Kaptein, E, Van Raaij, JAGM, Joe, CTT, Ebner, T & Burchell, B (1993) Multiple UDP-glucuronosyltransferases for the glucuronidation of thyroid hormone with preference for 3,3′,5′-triodothyronine (reverse T3). FEBS Letters 315, 6568.CrossRefGoogle Scholar
Zhang, X-K, Hoffmann, B, Tran, P, Graupner, G & Pfahl, M (1992) Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature 358, 587591.CrossRefGoogle Scholar