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The influence of dietary vitamin A on triiodothyronine, retinoic acid, and glucocorticoid receptors in liver of hypothyroid rats

Published online by Cambridge University Press:  09 March 2007

M. Coustaut ,
V. Pallet ,
H. Garcin  and
P. Higueret
M. Coustaut
Affiliation:
Laboratoire de Nutrition – ISTAB, Université Bordeaux I, Avenue des Facultés, 33405 Talence-Cedex, France
V. Pallet
Affiliation:
Laboratoire de Nutrition – ISTAB, Université Bordeaux I, Avenue des Facultés, 33405 Talence-Cedex, France
H. Garcin
Affiliation:
Laboratoire de Nutrition – ISTAB, Université Bordeaux I, Avenue des Facultés, 33405 Talence-Cedex, France
P. Higueret
Affiliation:
Laboratoire de Nutrition – ISTAB, Université Bordeaux I, Avenue des Facultés, 33405 Talence-Cedex, France
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Abstract

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The properties of nuclear receptors belonging to the superfamily of receptors acting as transcription factors are modulated by nutritional and hormonal conditions. We showed recently that retinoic acid (RA) restored to normal the expression of receptors attenuated by hypothyroidism. The present study was designed to find out whether dietary vitamin A (as retinol) had the same effect. Propylthiouracil in drinking water induced both hypothyroidism and a vitamin A-deficient status in rats. The maximum binding capacity (Cmax) of triiodothyronine nuclear receptors (TR) was unchanged, while that of nuclear RA receptors (RAR) and nuclear glucocorticoid hormone receptors (GRn) was reduced in the liver of these hypothyroid rats. The reduced Cmax of RAR stemmed from a lower level of RAR mRNA, while the reduced Cmax of GRn was assumed to be due to reduced translocation of the receptor from the cytosol to the nucleus. Feeding the hypothyroid rats with a vitamin A-rich diet did not restore the Cmax of either RAR or GRn to normal. The lack of effect of dietary retinol on RAR expression may be attributed to either genomic (unoccupied TR block the expression of RAR genes) and/or extragenomic (hypothyroidism decreases the availability of retinol and/or its metabolism to RA) mechanisms. Triiodothyronine is thought to favour the translocation of glucocorticoid hormone receptors from cytosol to nucleus. These findings provide more information on the relationship between vitamin A and hormonal status, showing that a vitamin A-rich diet is without apparent effect on the expression of nuclear receptors in hypothyroid rats.

Keywords

RetinolNuclear receptorsHormones
Type
General Nutrition
Information
British Journal of Nutrition , Volume 76 , Issue 2 , August 1996 , pp. 295 - 306
Copyright
Copyright © The Nutrition Society 1996

References

REFERENCES

Akner, G., Wikström, A.-C. & Gustafsson, J.-A. (1995). Subcellular distribution of the glucocorticoid receptor and evidence for its association with microtubules. Journal of Steroid Biochemistry and Molecular Biology 52, 1–16.CrossRefGoogle ScholarPubMed
Audouin-Chevallier, I., Higueret, P., Pallet, V., Higueret, D. & Garcin, H. (1993). Dietary vitamin A modulates the properties of retinoic acid and glucocorticoid receptors in rat liver. Journal of Nutrition 123, 1195–1202.CrossRefGoogle ScholarPubMed
Audouin-Chevallier, I., Pallet, V., Coustaut, M., Alfos, S., Higueret, P. & Garcin, H. (1995). Retinoids modulate the binding capacity of the glucocorticoid receptor and its translocation from cytosol to nucleus in liver cells. Journal of Steroid Biochemistry and Molecular Biology 52, 321–328.CrossRefGoogle ScholarPubMed
Aurichio, F. (1989). Phosphorylation of steroid receptors. Journal of Steroid Biochemistry 32, 613–622.CrossRefGoogle Scholar
Bernal, J., Coleoni, A. H. & De Groot, L. J. (1978). Thyroid hormone receptors from liver nuclei: characteristics of receptor from normal, thyroidectomized, and triiodothyronine-treated rats; measurements of occupied and unoccupied receptors, and chromatin binding of receptors. Endocrinology 103, 403–414.CrossRefGoogle ScholarPubMed
Bodwell, J. E., Hu, J. M., Orti, E. & Munck, A. (1995). Hormone-induced hyperphosphorylated sites in the mouse glucocorticoid receptor. Journal of Steroid Biochemistry and Molecular Biology 52, 135–140.CrossRefGoogle ScholarPubMed
Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 12, 248–254.CrossRefGoogle Scholar
Brent, G. A., Dunn, M. K., Harney, J. W., Gulick, T., Larsen, P. R. & Moore, D. D. (1989). Thyroid hormone aporeceptor represses T3-inducible promoters and blocks activity of the retinoic acid receptor. New Biologist 1, 329–336.Google ScholarPubMed
Chomczynski, P. & Sacchi, N. (1987). Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.CrossRefGoogle ScholarPubMed
Coleoni, A. H. & De Groot, L. J. (1980). Liver nuclear protein phosphorylation in vitro and the effect of triiodothyronine. Endocrinology 106, 1103–1107.CrossRefGoogle Scholar
Daly, A. K., Redfern, C. P. F. & Martin, B. (1990). Identification and analysis of retinoic acid binding protein and receptor from nuclei of mammalian cells. Methods in Enzymology 189, 239–247.CrossRefGoogle ScholarPubMed
Damm, K., Thompson, C. C. & Evans, R. M. (1989). Protein encoded by v-erbA functions as a thyroid-hormone receptor antagonist. Nature 339, 593–597.CrossRefGoogle ScholarPubMed
De Groot, L.J. & Torresani, J. (1975). Triiodothyronine binding to isolated liver cell nuclei. Endocrinology 96, 357–369.CrossRefGoogle ScholarPubMed
Delescluse, C., Cavey, M. T., Martin, B., Bernard, B.A., Reichert, U., Maignan, J., Darmon, M. & Shroot, B. (1991). Selective high affinity retinoic acid receptor α or β-γ ligands. Molecular Pharmacology 40, 556–562.Google ScholarPubMed
Guiochon-Mantel, A. & Milgrom, E. (1993). Cytoplasmic-nuclear trafficking of steroid hormone receptors. Trends in Endocrinology and Metabolism 4, 322–328.CrossRefGoogle ScholarPubMed
Fugassa, E., Gallo, G. & Pertica, M. (1976). Increased in vitro phosphorylation of rat liver nucleolar proteins following triiodothyronine administration. Experientia 32, 1379–1384.CrossRefGoogle ScholarPubMed
Hamada, S., Nakamura, H., Nanno, M. & Imura, H. (1979). Triiodothyronine-induced increase in rat liver nuclear thyroid hormone receptors associated with increased mitochondria1 α-glycerophosphate dehydrogenase activity. Biochemical Journal 182, 371–377.CrossRefGoogle Scholar
Haq, R., Pfahl, M. & Chytil, F. (1991). Retinoic acid affects the expression of nuclear retinoic acid receptors in tissues of retinol-deficient rats. Proceedings of the National Academy of Sciences, USA 88, 8272–8276.CrossRefGoogle ScholarPubMed
Higueret, P., Pailler, I. & Garcin, H. (1989). Vitamin A deficiency and triiodothyronine action at the cellular level in the rat. Journal of Endocrinology 121, 75–79.CrossRefGoogle ScholarPubMed
Höck, W., Martin, F., Jaggi, R. & Groner, B. (1989). Regulation of glucocorticoid receptor activity. Journal of Steroid Biochemistry 34, 71–78.CrossRefGoogle ScholarPubMed
Kato, S., Mano, H., Kumazawa, T., Yoshizawa, Y., Kojima, R. & Masushige, S. (1992). Effect of retinoid status on α, β and γ retinoic acid receptor mRNA levels in various rat tissues. Biochemical Journal 286, 755–760.CrossRefGoogle ScholarPubMed
Kaufman, S. H. & Shaper, J. H. (1984). Binding of dexamethasone to rat liver nuclei in vivo and in vivo: evidence for two distinct binding sites. Journal of Steroid Biochemistry 20, 699–708.CrossRefGoogle Scholar
Kido, H., Fukusen, N. & Katunuma, N. (1987). Tumor-promoting phorbol ester amplifies the inductions of tyrosine aminotransferase and ornithine decarboxylase by glucocorticoid. Biochemistry 26, 2349–2353.CrossRefGoogle ScholarPubMed
Lavin, T. N., Baxter, J. D. & Horita, S. (1988). The thyroid hormone receptor binds to multiple domains of the rat growth hormone 5'-flanking sequence. Journal of Biological Chemistry 263, 9418–9426.CrossRefGoogle ScholarPubMed
Leclercq, M. & Bourgeay-Causse, M. (1981). Une méthode simple, fiable, rapide:dosage simultané du rétinol et du tocophérol sériques par chromatographie liquide haute performance (A simple method, reliable, fast: simultaneous assay of retinol and serum tocopherol by high-performance liquid chromatography). Revue de I'Institut Pasteur, Lyon 14, 475–494.Google Scholar
Lee, L.-R., Mortensen, R. M., Larson, C. A. & Brent, G. A. (1994). Thyroid hormone receptor-α inhibits retinoic acid-responsive gene expression and modulates retinoic acid-stimulated neural differentiation in mouse embryonic stem cells. Molecular Endocrinology 8, 746–756.Google ScholarPubMed
Levine, M. A., Feldman, A. M., Robishaw, J. D., Ladenson, P. W., Ahn, T. G. & Moroney, J. F. (1990). Influence of thyroid hormone status on expression of gene encoding G protein subunits in rat heart. Journal of Biological Chemistry 265, 3553–3558.CrossRefGoogle ScholarPubMed
Ma, X. J., Salati, L. M., Ash, S. E., Mitchell, D.A, Kantley, S. A. & Fantozzi, D.A. (1990). Nutritional regulation and tissue specific expression of the malic enzyme gene in the chicken. Journal of Biological Chemistry 265, 18435–18441.CrossRefGoogle ScholarPubMed
Miesfield, R., Rusconi, S., Godowski, P. J., Maler, B.A, Okret, S., Wikstroem, A. C., Gustafsson, J. A. & Yamamoto, K. R. (1986). Genetic complementation to a glucocorticoid receptor deficiency by expression of cloned receptor c-DNA Cell 46, 389–399.CrossRefGoogle Scholar
Mitsuhashi, T. & Nikodem, V. (1989). Regulation of expression of the alternative mRNAs of the rat alpha thyroid hormone receptor gene. Journal of Biological Chemistry 264, 8900–8904.CrossRefGoogle ScholarPubMed
Moore, T. (1957). Vitamin A. Amsterdam: Elsevier Publishing Company.Google Scholar
Moudgil, V. K. (1990). Phosphorylation of steroid hormone receptors. Biochimica et Biophysica Acta 1055, 243–258.CrossRefGoogle ScholarPubMed
Muller, M. & Renkawitz, R. (1991). The glucocorticoid receptor. Biochimica et Biophysica Acta 1088, 171–182.CrossRefGoogle ScholarPubMed
Murray, M. B., Zilz, N. D., McCreary, N. L., McDonald, M. J. & Towle, H. C. (1988). Isolation and characterization of rat cDNA clones for two distinct thyroid hormone receptors. Journal of Biological Chemistry 263, 12770–12777.CrossRefGoogle ScholarPubMed
Nakamura, H., Hamada, S. & Imura, H. (1979). Sequential changes in rat liver nuclear tri-iodothyronine receptors and mitocheondrial α-glycerophosphate dehydrogenase activity after administration of tri-iodothyronine. Biochemical Journal 182, 377–382.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, 1759–1771.CrossRefGoogle ScholarPubMed
Orti, E., Bodwell, J. E. & Munck, A. (1992). Phosphorylation of steroid hormone receptors. Endocrine Reviews 13, 105–128.Google ScholarPubMed
Orti, E., Mendel, D. B., Smith, L., Bodwell, J. E. & Munck, A. (1989). A dynamic model of glucocorticoid receptor phosphorylation and cycling in intact cells. Journal of Steroid Biochemistry 34, 85–96.CrossRefGoogle ScholarPubMed
Ozawa, T., Tanaka, M., Ikebe, S.I., Ohno, K., Kondo, T. & Mizuno, Y. (1990). Quantitative determination of deleted mitochondria1 DNA to normal DNA in Parkinsonian striaturn by kinetic PCR analysis. Biochemical and Biophysical Research Communications 172, 483–489.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, 245–251.CrossRefGoogle ScholarPubMed
Pailler-Rodde, I., Garcin, H., Higueret, P. & Bégueret, J. (1991 b). C-erbA mRNA content and triiodothyronine nuclear receptor binding capacity in rat liver according to vitamin A status. FEBS Letters 289, 33–36.CrossRefGoogle Scholar
Pallet, V., Audouin-Chevallier, I., Higueret, D., Garcin, H. & Higueret, P. (1996). Dexamethasone decreases the expression of retinoic acid receptors (RARs) in rat liver. Journal of Steroid Biochemistry and Molecular Biology 57, 161–165.CrossRefGoogle ScholarPubMed
Pallet, V., Audouin-Chevallier, I., Verret, C., Garcin, H. & Higueret, P. (1994). Retinoic acid differentially modulates triiodothyronine and retinoic acid receptors in rat liver according to thyroid status. European Journal of Endocrinology 131, 377–384.CrossRefGoogle ScholarPubMed
Pou, M-A, Bismuth, J., Gharbi-Chihi, J. & Torresani, J. (1986). Triiodothyronine (T3)-induced down-regulation of the nuclear T3, receptor in mouse preadipocyte cell lines. Endocrinology 119, 2360–2367.CrossRefGoogle ScholarPubMed
Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S.J., Higuchi, R., Horn, G. T., Mullis, K. B. & Erlich, H.A. (1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 236, 487–491.CrossRefGoogle Scholar
Siebert, P. D. & Larrick, J. W. (1993). PCR MIMICs: competitive DNA fragments for use as internal standards in quantitative PCR. BioTechniques 14, 244–249.Google ScholarPubMed
Strait, K. A., Schwartz, H. L., Perez-Castillo, A. & Oppenheimer, J. H. (1990). Relationship of c-erbd mRNA content to tissue T3 nuclear binding capacity and function in developing rat and adult rat. Journal of Biological Chemistry 265, 10514–10521.CrossRefGoogle Scholar
Torresani, J. & De Groot, L. J. (1975). Triiodothyronine binding to liver nuclear solubilized proteins in vivo. Endocrinology 96, 1201–1209.CrossRefGoogle Scholar
Tsai, M. J. & O'Malley, B. W. (1994). Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annual Review of Biochemistry 63, 451–486.CrossRefGoogle ScholarPubMed
Ylikomi, T., Bocquel, M. T., Berry, M., Gronemeyer, H. & Chambon, P. (1992). Cooperation of proto-signals for nuclear accumulation of estrogen and progesterone receptors. EMBO Journal 11, 3681–3694.CrossRefGoogle ScholarPubMed
Zelent, A., Krust, A., Petkovich, M., Kastner, P. & Chambon, P. (1989). Cloning of murine α and β retinoic acid receptors and a novel receptor γ predominantly expressed in skin. Nature 339, 714–717.CrossRefGoogle Scholar