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. 1990 Dec;10(12):6674–6682. doi: 10.1128/mcb.10.12.6674

Activation of chromosomal vitellogenin genes in Xenopus oocytes by pure estrogen receptor and independent activation of albumin genes.

E A McKenzie 1, N A Cridland 1, J Knowland 1
PMCID: PMC362945  PMID: 2247078

Abstract

We generate pure estrogen receptor protein in Xenopus oocytes by injecting them with estrogen receptor mRNA synthesized in vitro. A chromosomal vitellogenin gene, which normally responds to estrogen only in liver cells, is activated. Primer extension shows that initiation is accurate, and ribonuclease mapping shows that the first exon is correctly spliced out of the initial transcript. Long transcripts are produced, one being equal in length to poly(A)- vitellogenin mRNA. Immunochemical estimates of receptor levels in the oocyte nuclei suggest that pure receptor, acting alone, cannot activate oocyte vitellogenin genes unless unusually large amounts are present. However, when a receptor-free extract from liver cells is also injected, the amount of receptor required is reduced. Such an extract, but not pure receptor, can also activate albumin genes in oocytes.

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Selected References

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  1. Brock M. L., Shapiro D. J. Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation. Cell. 1983 Aug;34(1):207–214. doi: 10.1016/0092-8674(83)90151-4. [DOI] [PubMed] [Google Scholar]
  2. Contreras R., Gheysen D., Knowland J., van de Voorde A., Fiers W. Evidence for the direct involvement of DNA replication origin in synthesis of late SV40 RNA. Nature. 1982 Dec 9;300(5892):500–505. doi: 10.1038/300500a0. [DOI] [PubMed] [Google Scholar]
  3. Corthésy B., Cardinaux J. R., Claret F. X., Wahli W. A nuclear factor I-like activity and a liver-specific repressor govern estrogen-regulated in vitro transcription from the Xenopus laevis vitellogenin B1 promoter. Mol Cell Biol. 1989 Dec;9(12):5548–5562. doi: 10.1128/mcb.9.12.5548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Corthésy B., Hipskind R., Theulaz I., Wahli W. Estrogen-dependent in vitro transcription from the vitellogenin promoter in liver nuclear extracts. Science. 1988 Mar 4;239(4844):1137–1139. doi: 10.1126/science.2830672. [DOI] [PubMed] [Google Scholar]
  5. Cridland N. A., Wright C. V., McKenzie E. A., Knowland J. Selective photochemical treatment of oestrogen receptor in a Xenopus liver extract destroys hormone binding and transcriptional activation but not DNA binding. EMBO J. 1990 Jun;9(6):1859–1866. doi: 10.1002/j.1460-2075.1990.tb08311.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fortune J. E. Steroid production by Xenopus ovarian follicles at different developmental stages. Dev Biol. 1983 Oct;99(2):502–509. doi: 10.1016/0012-1606(83)90299-3. [DOI] [PubMed] [Google Scholar]
  7. Gerber-Huber S., Nardelli D., Haefliger J. A., Cooper D. N., Givel F., Germond J. E., Engel J., Green N. M., Wahli W. Precursor-product relationship between vitellogenin and the yolk proteins as derived from the complete sequence of a Xenopus vitellogenin gene. Nucleic Acids Res. 1987 Jun 25;15(12):4737–4760. doi: 10.1093/nar/15.12.4737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gurdon J. B. Methods for nuclear transplantation in amphibia. Methods Cell Biol. 1977;16:125–139. doi: 10.1016/s0091-679x(08)60096-5. [DOI] [PubMed] [Google Scholar]
  9. Hayward M. A., Mitchell T. A., Shapiro D. J. Induction of estrogen receptor and reversal of the nuclear/cytoplasmic receptor ratio during vitellogenin synthesis and withdrawal in Xenopus laevis. J Biol Chem. 1980 Dec 10;255(23):11308–11312. [PubMed] [Google Scholar]
  10. Huber S., Ryffel G. U., Weber R. Thyroid hormone induces competence for oestrogen-dependent vitellogenin synthesis in developing Xenopus laevis liver. Nature. 1979 Mar 1;278(5699):65–67. doi: 10.1038/278065a0. [DOI] [PubMed] [Google Scholar]
  11. Kazmaier M., Brüning E., Ryffel G. U. Post-transcriptional regulation of albumin gene expression in Xenopus liver. EMBO J. 1985 May;4(5):1261–1266. doi: 10.1002/j.1460-2075.1985.tb03770.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Knowland J. Induction of vitellogenin synthesis in Xenopus laevis tadpoles. Differentiation. 1978 Nov 15;12(1):47–51. doi: 10.1111/j.1432-0436.1979.tb00989.x. [DOI] [PubMed] [Google Scholar]
  13. Knowland J., Theulaz I., Wright C. V., Wahli W. Injection of partially purified estrogen receptor protein from Xenopus liver nuclei into oocytes activates the silent vitellogenin locus. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5777–5781. doi: 10.1073/pnas.81.18.5777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kumar V., Chambon P. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell. 1988 Oct 7;55(1):145–156. doi: 10.1016/0092-8674(88)90017-7. [DOI] [PubMed] [Google Scholar]
  15. Kumar V., Green S., Staub A., Chambon P. Localisation of the oestradiol-binding and putative DNA-binding domains of the human oestrogen receptor. EMBO J. 1986 Sep;5(9):2231–2236. doi: 10.1002/j.1460-2075.1986.tb04489.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Marsh J., Tata J. R. Establishment and characterization of Xenopus oviduct cells in primary culture. Exp Cell Res. 1987 Nov;173(1):117–128. doi: 10.1016/0014-4827(87)90337-5. [DOI] [PubMed] [Google Scholar]
  17. May F. E., Knowland J. Oestrogen receptor levels and vitellogenin synthesis during development of Xenopus laevis. Nature. 1981 Aug 27;292(5826):853–855. doi: 10.1038/292853a0. [DOI] [PubMed] [Google Scholar]
  18. May F. E., Knowland J. Patterns of protein synthesis in livers of Xenopus laevis during metamorphosis: effects of estrogen in normal and thyrostatic animals. Dev Biol. 1981 Feb;82(1):158–167. doi: 10.1016/0012-1606(81)90437-1. [DOI] [PubMed] [Google Scholar]
  19. May F. E., Weber R., Westley B. R. Isolation and characterisation of the Xenopus laevis albumin genes: loss of 74K albumin gene sequences by library amplification. Nucleic Acids Res. 1982 May 11;10(9):2791–2807. doi: 10.1093/nar/10.9.2791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McKenzie E. A., Knowland J. High concentrations of estrogen stabilize vitellogenin mRNA against cytoplasmic degradation but physiological concentrations do not. Mol Endocrinol. 1990 Jun;4(6):807–811. doi: 10.1210/mend-4-6-807. [DOI] [PubMed] [Google Scholar]
  21. Rudack D., Wallace R. A. On the site of phosvitin synthesis in Xenopus laevis. Biochim Biophys Acta. 1968 Jan 29;155(1):299–301. doi: 10.1016/0005-2787(68)90361-4. [DOI] [PubMed] [Google Scholar]
  22. Schäfer B. W., Blakely B. T., Darlington G. J., Blau H. M. Effect of cell history on response to helix-loop-helix family of myogenic regulators. Nature. 1990 Mar 29;344(6265):454–458. doi: 10.1038/344454a0. [DOI] [PubMed] [Google Scholar]
  23. Seiler-Tuyns A., Mérillat A. M., Haefliger D. N., Wahli W. The human estrogen receptor can regulate exogenous but not endogenous vitellogenin gene promoters in a Xenopus cell line. Nucleic Acids Res. 1988 Sep 12;16(17):8291–8305. doi: 10.1093/nar/16.17.8291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Smith R. C., Knowland J. Protein synthesis in dorsal and ventral regions of Xenopus laevis embryos in relation to dorsal and ventral differentiation. Dev Biol. 1984 Jun;103(2):355–368. doi: 10.1016/0012-1606(84)90324-5. [DOI] [PubMed] [Google Scholar]
  25. Theulaz I., Hipskind R., ten Heggeler-Bordier B., Green S., Kumar V., Chambon P., Wahli W. Expression of human estrogen receptor mutants in Xenopus oocytes: correlation between transcriptional activity and ability to form protein-DNA complexes. EMBO J. 1988 Jun;7(6):1653–1660. doi: 10.1002/j.1460-2075.1988.tb02992.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Thorburn A., Knowland J. A novel nuclear transcription system which responds correctly to cloned estrogen receptor. Nucleic Acids Res. 1988 Nov 25;16(22):10469–10476. doi: 10.1093/nar/16.22.10469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tora L., Mullick A., Metzger D., Ponglikitmongkol M., Park I., Chambon P. The cloned human oestrogen receptor contains a mutation which alters its hormone binding properties. EMBO J. 1989 Jul;8(7):1981–1986. doi: 10.1002/j.1460-2075.1989.tb03604.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wahli W. Evolution and expression of vitellogenin genes. Trends Genet. 1988 Aug;4(8):227–232. doi: 10.1016/0168-9525(88)90155-2. [DOI] [PubMed] [Google Scholar]
  29. Walker P., Germond J. E., Brown-Luedi M., Givel F., Wahli W. Sequence homologies in the region preceding the transcription initiation site of the liver estrogen-responsive vitellogenin and apo-VLDLII genes. Nucleic Acids Res. 1984 Nov 26;12(22):8611–8626. doi: 10.1093/nar/12.22.8611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Walter P., Green S., Greene G., Krust A., Bornert J. M., Jeltsch J. M., Staub A., Jensen E., Scrace G., Waterfield M. Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7889–7893. doi: 10.1073/pnas.82.23.7889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Watson C. S., Torres T. Expression and translocation of cloned human estrogen receptor in the Xenopus oocyte does not induce expression of the endogenous oocyte vitellogenin genes. Mol Endocrinol. 1990 Apr;4(4):565–572. doi: 10.1210/mend-4-4-565. [DOI] [PubMed] [Google Scholar]
  32. Weiler I. J., Lew D., Shapiro D. J. The Xenopus laevis estrogen receptor: sequence homology with human and avian receptors and identification of multiple estrogen receptor messenger ribonucleic acids. Mol Endocrinol. 1987 May;1(5):355–362. doi: 10.1210/mend-1-5-355. [DOI] [PubMed] [Google Scholar]
  33. Weintraub H., Tapscott S. J., Davis R. L., Thayer M. J., Adam M. A., Lassar A. B., Miller A. D. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5434–5438. doi: 10.1073/pnas.86.14.5434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Westley B., Knowland J. An estrogen receptor from Xenopus laevis liver possibly connected with vitellogenin synthesis. Cell. 1978 Oct;15(2):367–374. doi: 10.1016/0092-8674(78)90005-3. [DOI] [PubMed] [Google Scholar]
  35. Wright C. V., Wright S. C., Knowland J. Partial purification of estradiol receptor from Xenopus laevis liver and levels of receptor in relation to estradiol concentration. EMBO J. 1983;2(6):973–977. doi: 10.1002/j.1460-2075.1983.tb01530.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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