Abstract
Rainbow trout estrogen receptor (rtER) concentration was highly induced in the liver after in vivo estradiol (E2) treatment or in vitro, in hepatocyte aggregate culture. Determination of transcription rate and mRNA half-life demonstrated that E2-induction of hepatic rtER level is caused essentially by an increase in the transcriptional and post-transcriptional activity of rtER gene. However, the expression of rtER gene in the liver seems to be down-regulated by glucocorticoids. We have used transient transfection assays with reporter plasmids linked to 5′ flanking regions of the rtER gene promoter, to identify cis-elements responsible for E2 inducibility. Deletion analysis localized a functional estrogen-responsive-element (ERE), near the transcription start site, with one mutation on the first base compared to the consensus sequence. This element and 200 bp fragment of the rtER promoter encompassing the ERE appear to be the major cis-acting element involved in the regulation of the gene. Data obtained from transfection experiments and footprinting analysis, suggested that the receptor is one of the major trans-factors implicated in the regulation of its own gene. However, interaction of ER with other transcription factors is required for maximal E2-stimulation.
Similar content being viewed by others
References cited
Auffray, C. and Rougeon, F. 1980. Purification of mouse immunoglobin heavy-chain messenger RNAs from total meyelona tumor RN. Eur. J. Biochem. 107: 306–314.
Barton, M.C. and Shapiro, D.J. 1988. Transient administration of estradiol 17-ß establishes and autoregulatory loop permanently inducing estrogen receptor mRNA. Proc. Nat. Acad. Sci. USA 85: 7119–7123.
Brock, M.L. and Shapiro, D.J. 1983. Estrogen stabilizes vitellogenin messenger RNA against cytoplasmic degradation. Cell 34: 207–214.
Chauchereau, A., Savouret, J.F. and Milgrom, E. 1992. Control of biosynthesis and post-transcriptional modification of the progesterone receptor. Biol. Reprod. 46: 174–177.
Cheley, S. and Anderson, R. 1984. A reproductible microanalytical method for the detection of specific RNA sequence by Dot-Blot hybridization. Anal. Biochem. 137: 15–19.
Evans, M.I., O'Malley, P.J., Krust, A. and Burch, J.B.E. 1987. Developmental regulation of the estrogen receptor and the estrogen responsiveness of five yolk protein genes in the avian liver. Proc. Nat. Acad. Sci. USA 84: 8493–8497.
Evans, R.M. 1988. The steroid and thyroid hormone receptor superfamily. Science 240: 889–895.
Flouriot, G., Pakdel, F. and Valotaire, Y. 1996. Transcriptional and post-transcriptional regulation of rainbow trout estrogen receptor and vitellogenin gene expression. Mol. Cell. Endocrinol. 124: 173–183.
Flouriot, G., Vaillant, C., Salbert, G., Pelissero, C., Guiraud, J.M. and Valotaire, Y. 1993. Monolayer and agregate cultures of hepatocytes: long-term and stable liver-specific expression in agregates. J. Cell Sci. 105: 407–416.
Freyschuss, B., Sahlin, L., Masironi, B. and Eriksson, H. 1994. The hormonal regulation of the oestrogen receptor in rat liver: an interplay involving growth hormone, thyroid hormones and glucocorticoids. J. Endocrinol. 142: 285–298.
Groudine, M., Peretz, M. and Weintraub, H. 1981. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol. Cell. Biol. 1: 281–288.
Ham, J. and Parker, M.G. 1989. Regulation of gene expression by nuclear hormone receptors. Curr. Opin. Cell. Biol. 1: 503–511.
Hayward, M.A., Brock, M.L. and Shapiro, D.J. 1982. The role of estrogen receptor in Xenopus laevis vitellogenin gene expression. Am. J. Physiol. 243: L1–L6.
Klein-Hitpass, L., Kaling, M. and Ryffel, G.U. 1988. Synergism of closely adjacent estrogen responsive elements increases their regulatory potential. J. Mol. Biol. 201: 537–544.
Klock, G., Stähle, U. and Schütz, G. 1987. Oestrogen and glucocorticoid responsive elements are closely related but distinct. Nature, Lond. 329: 734–736.
Lazennec, G., Kern, L., Salbert, G., Saligaut, D. and Valotaire, Y. 1996. Cooperation between the human estrogen receptor and MCF-7 cell-specific transcription factors elicits high activity of an estrogen inducible enhancer from the trout ER gene promoter. Mol. Endocrinol. 10: 1116–1126.
Lazier, C.B., Lonergan, K. and Mommsen, T.P. 1985. Hepatic estrogen receptor and plasma estrogen-binding activity in the Atlantic salmon. Gen. Comp. Endocrinol. 57: 234–245.
Le Dréan, Y., Lazennec, G., Kern, L., Saligaut, D., Pakdel, F. and Valotaire, Y. 1995. Characterization of an estrogen-responsive-element implicated in regulation of the rainbow trout estrogen receptor gene. J. Mol. Endocrinol. 5: 37–47.
Le Dréan, Y., Pakdel, F. and Valotaire, Y. 1994. Structure and regulation of genes for estrogen receptors. Molecular Endocrinology of Fish. In Fish Physiology Vol. 13, pp. 331–366. Edited by N.M. Sherwood and C.L. Hew. Academic Press, New York.
Le Goff, P., Salbert, G., Prunet, P., Saligaut, C., Bjornsson, B., Haux, C. and Valotaire, Y. 1992. Absence of direct regulation of prolactin cells by oestradiol-17ß in rainbow trout (Oncorhynchus mykiss). Mol. Cell. Endocrinol. 90: 133–139.
Le Roux, M.G., Thézé, N., Wolff, J. and Le Pennec, J.P. 1993. Organization of the rainbow trout estrogen receptor gene. Biochem. Biophy. Acta 1172: 226–230.
Lindzey, J., Grossmann, M., Kumar, M.V. and Tindall, D.J. 1993. Regulation of the 5'-flanking region of the mouse androgen receptor gene by cAMP and androgen. Mol. Endocrinol. 7: 1530–1540.
Maitre, J.L., Mercier, L., Dolo, L. and Valotaire, Y. 1985. Caractérisation de récepreur spécifiques à l'oestradiol, induction de la vitellogénine et de son mRNA dans le foie de truite arcen-ciel. Biochimie 67: 215–225.
Maitre, J.L., Valotaire, Y. and Guguen-Guillouzo, C. 1986. Estra-diol 17-ß stimulation of vitellogenin synthesis in primary culture of male rainbow trout hepatocytes. In Vitro 22: 337–343.
Maxam, A.M. and Gilbert, W. 1980. Sequencing end labelled DNA with base-specific cleavages. Meth. Enzymol. 65: 499–560.
McKnight, G.S. and Palmiter, R.D. 1979. Transcriptional regulation of the ovalbumin and conalbumin genes by steroid hormones in chick oviduct. J. Biol. Chem. 254: 9050–9058.
Nielsen, D.A., Chang, T.C. and Shapiro, D.J. 1989. A highly sensitive mixe phase assay for chloramphenicol acetyltransferase activity in transfected cells. Annal. Biochem. 179: 19–23.
Pakdel, F. and Katzenellenbogen, B.S. 1992. Human estrogen receptor mutants with altered estrogen and antiestrogen ligand discrimination. J. Biol. Chem. 267: 3429–3437.
Pakdel, F., Feon, S., Le Gac, F., Le Menn, F. and Valotaire, Y. 1991. In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout. Mol. Cell. Endocrinol. 75: 205–212.
Pakdel, F., Le Gac, F., Le Goff, P. and Valotaire, Y. 1990. Fulllength sequence and in vitro expression of rainbow trout estrogene receptor cDNA. Mol. Cell. Endocrinol. 71: 195–204.
Pakdel, F., Le Guellec, C., Vaillant, C., Le Roux, M.G. and Valotaire, Y. 1989. Identification and estrogen induction of two estrogen receptors (ER) messenger ribonucleic acids in the rainbow trout liver: sequence homology with others ERs. Mol. Endocrinol. 3: 44–51.
Pakdel, F., Petit, F., Anglade, I., Kah, O., Delaunay, F., Bailhache, T. and Valotaire, Y. 1994. Overexpression of rainbow trout estrogen receptor domains in Escherichia coli: Characterization and utilization in the production of antibodies for immunobloting and immunocytochemistry. Mol. Cell. Endocrinol. 104: 81–93.
Petit, F., Valotaire, Y. and Pakdel, F. 1995. Differential functional activities of rainbow trout and human estrogen receptors expressed in the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 233: 584–592.
Ptashne, M. 1988. Howe eukaryotic transcriptional activators work. Nature, Lond. 335: 683–698.
Riegel, A.T., Aitken, S.C., Martin, M.B. and Schoenberg, D.R. 1987. Differential induction of hepatic estrogen receptor and vitellogenin gene transcription in Xenopus laevis. Endocrinology 120: 1283–1290.
Riegel, A.T., Martin, M.B. and Schoenberg, D.R. 1986. Transcriptional and post-transcriptional inhibition of albumin gene expression by estrogen in Xenopus liver. Mol. Cell. Endocrinol. 44: 201–209.
Rosewicz, S., McDonald, A.R., Maddux, B.A., Goldfine, I.D., Miesfeld, R.L. and Logsdon, C.D. 1988. Mechanism of glucocorticoid receptor down-regulation by glucocorticoids. J. Biol. Chem. 263: 2581–2584.
Saceda, M., Lippman, M.E., Chambon, P., Lindsey, R.L., Ponglikitmongkol, M., Puente, M. and Martin, M.B. 1988. Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol. Endocrinol. 2: 1157–1162.
Saceda, M., Lippman, M.E., Lindsey, R.K., Puente, M. and Martin, M.B. 1989. Role of an estrogen receptor-dependent mechanism in the regulation of estrogen receptor mRNA in MCF-7 cells. Mol. Endocrinol. 3: 1782–1787.
Santos, G.F., Scott, G.K., Lee, W.M.F., Liu, E. and Benz, C. 1988. Estrogen-induced post-transcriptional modulation of c-myc proto-oncogene expression in human breast cancer cells. J. Biol. Chem. 263: 9565–9568.
Savouret, J.F., Bailly, A., Misrahi, M., Rauch, C., Redeuilh, G., Chauchereau, A. and Milgrom, E. 1991. Characterization of the hormone responsive element involved in the regulation of the progesterone receptor gene. EMBO J. 10: 1875–1883.
Schibler, U., Hagenbüchle, O., Wellauer, P.K. and Pitted, A.C. 1983. Two promoters of different strengths control the transcription of the mouse alpha-analyse gene amy-1 in the paratid gland and the liver. Cell 33: 501–508.
Schoenberg, D.R., Moskaitis, J.E., Smith, L.H. and Pastori, R.L. 1989. Extranuclear estrogen-regulated destabilization of Xenopus laevis serum albumin mRNA. Mol. Endocrinol. 3: 805–814.
Seglen, P.O. 1973. Preparation of rat liver cells II. Effect of ions and chelators on tissue dispersion. Exp. Cell Res. 76: 25–30.
Rata, J.R., Baker, B.S., Machuca, I., Rabelo, E.M.L. and Yamauchi, K. 1993. Autoinduction of nuclear receptor genes and its significance. J. Ster. Biochem. Molec. Biol. 46: 105–119.
Thomas, P.S. 1980. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Nat. Acad. Sci. USA 77: 5201–5205.
Truss, M., Chalekapis, G. and Beato, M. 1990. Contacts between steroid hormone receptors and thymines in DNA: an interference method. Proc. Nat. Acad. Sci. USA 87: 7180–7184.
Ulisse, S. and Tata, J.R. 1994. Thyroid hormone and glucocorticoid independently regulate the expression of estrogen receptor in male Xenopus liver cells. Mol. Cell. Biol. 105: 45–53.
Vaillant, C., Le Guellec, C., Pakdel, F. and Valotaire, Y. 1988. Vitellogenine gene expression in primary culture of male rainbow trout hepatocytes. Gen. Comp. Endocrinol. 70: 284–290.
Westley, B. and Knowland, J. 1979. Estrogen causes a rapid, large and prolonged rise in the level of nuclear estrogen receptor in Xenopus laevis liver. Biochem. Biophys. Res. Commun. 88: 1167–1172.
Wiskocil, R., Bensky, P., Dower, W., Goldberger, R.F., Gordon, J.I. and Deeley, R.G. 1980. Coordinate regulation of two estrogen-dependent genes in avian liver. Proc. Nat. Acad. Sci. USA 77: 4474–4478.
Wolffe, A.P., Glover, J.F., Martin, S.C., Tenniswood, M.P.R., Williams, J.L. and Tata, J.R. 1985. Deinduction of transcription of Xenopus 74-kDa albumin genes and destabilization of mRNA by estrogen in vivo and in hepatocyte cultures. Eur. J. Biochem. 146: 489–496.
Xiong, F., Liu, D., Le Dréan, Y., Elsholtz, H.P. and Hew, C.L. 1994. Differential recruitment of steroid hormone response elements may dictate the expression of the pituitary gonadotropin IIß subunit gene during salmon maturation. Mol. Endocrinol. 8: 782–793.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pakdel, F., Delaunay, F., Ducouret, B. et al. Regulation of gene expression and biological activity of rainbow trout estrogen receptor. Fish Physiology and Biochemistry 17, 123–133 (1997). https://doi.org/10.1023/A:1007706207857
Issue Date:
DOI: https://doi.org/10.1023/A:1007706207857