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Regulation of gene expression and biological activity of rainbow trout estrogen receptor

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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.

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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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Brock, M.L. and Shapiro, D.J. 1983. Estrogen stabilizes vitellogenin messenger RNA against cytoplasmic degradation. Cell 34: 207–214.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Evans, R.M. 1988. The steroid and thyroid hormone receptor superfamily. Science 240: 889–895.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Groudine, M., Peretz, M. and Weintraub, H. 1981. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol. Cell. Biol. 1: 281–288.

    Google Scholar 

  • Ham, J. and Parker, M.G. 1989. Regulation of gene expression by nuclear hormone receptors. Curr. Opin. Cell. Biol. 1: 503–511.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Klock, G., Stähle, U. and Schütz, G. 1987. Oestrogen and glucocorticoid responsive elements are closely related but distinct. Nature, Lond. 329: 734–736.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Maxam, A.M. and Gilbert, W. 1980. Sequencing end labelled DNA with base-specific cleavages. Meth. Enzymol. 65: 499–560.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Pakdel, F. and Katzenellenbogen, B.S. 1992. Human estrogen receptor mutants with altered estrogen and antiestrogen ligand discrimination. J. Biol. Chem. 267: 3429–3437.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Ptashne, M. 1988. Howe eukaryotic transcriptional activators work. Nature, Lond. 335: 683–698.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Seglen, P.O. 1973. Preparation of rat liver cells II. Effect of ions and chelators on tissue dispersion. Exp. Cell Res. 76: 25–30.

    Google Scholar 

  • 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.

    Google Scholar 

  • Thomas, P.S. 1980. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Nat. Acad. Sci. USA 77: 5201–5205.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

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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

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