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. 1990 Jan;10(1):371–376. doi: 10.1128/mcb.10.1.371

Estradiol and estrogen receptor-dependent stabilization of a minivitellogenin mRNA lacking 5,100 nucleotides of coding sequence.

D A Nielsen 1, D J Shapiro 1
PMCID: PMC360757  PMID: 2294409

Abstract

We have developed a transfection assay to investigate the estrogen-mediated stabilization of cytoplasmic vitellogenin mRNA. A minivitellogenin (MV5) gene containing the 5' and 3' untranslated and coding regions but lacking 5,075 nucleotides of internal coding sequence was constructed. Cotransfection of the MV5 plasmid and a Xenopus estrogen receptor expression plasmid into Xenopus liver tissue culture cells yielded a 529-nucleotide MV5 mRNA, which was specifically stabilized by estrogen. MV5 mRNA exhibited the increased stability indicative of positive regulation when the estradiol-estrogen receptor complex was present and was not destabilized by unliganded estrogen receptor. Transfected estrogen receptor, estradiol, and 529 nucleotides of the 5,604-nucleotide vitellogenin B1 mRNA were sufficient for stabilization.

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Selected References

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  1. Baldi A., Boyle D. M., Wittliff J. L. Estrogen receptor is associated with protein and phospholipid kinase activities. Biochem Biophys Res Commun. 1986 Mar 13;135(2):597–606. doi: 10.1016/0006-291x(86)90035-5. [DOI] [PubMed] [Google Scholar]
  2. Brawerman G. mRNA decay: finding the right targets. Cell. 1989 Apr 7;57(1):9–10. doi: 10.1016/0092-8674(89)90166-9. [DOI] [PubMed] [Google Scholar]
  3. Brewer G., Ross J. Poly(A) shortening and degradation of the 3' A+U-rich sequences of human c-myc mRNA in a cell-free system. Mol Cell Biol. 1988 Apr;8(4):1697–1708. doi: 10.1128/mcb.8.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brock M. L., Shapiro D. J. Estrogen regulates the absolute rate of transcription of the Xenopus laevis vitellogenin genes. J Biol Chem. 1983 May 10;258(9):5449–5455. [PubMed] [Google Scholar]
  5. 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]
  6. Brown A. M., Jeltsch J. M., Roberts M., Chambon P. Activation of pS2 gene transcription is a primary response to estrogen in the human breast cancer cell line MCF-7. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6344–6348. doi: 10.1073/pnas.81.20.6344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carrazana E. J., Pasieka K. B., Majzoub J. A. The vasopressin mRNA poly(A) tract is unusually long and increases during stimulation of vasopressin gene expression in vivo. Mol Cell Biol. 1988 Jun;8(6):2267–2274. doi: 10.1128/mcb.8.6.2267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  9. Daar I. O., Maquat L. E. Premature translation termination mediates triosephosphate isomerase mRNA degradation. Mol Cell Biol. 1988 Feb;8(2):802–813. doi: 10.1128/mcb.8.2.802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dani C., Blanchard J. M., Piechaczyk M., El Sabouty S., Marty L., Jeanteur P. Extreme instability of myc mRNA in normal and transformed human cells. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7046–7050. doi: 10.1073/pnas.81.22.7046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eckert R. L., Katzenellenbogen B. S. Physical properties of estrogen receptor complexes in MCF-7 human breast cancer cells. Differences with anti-estrogen and estrogen. J Biol Chem. 1982 Aug 10;257(15):8840–8846. [PubMed] [Google Scholar]
  12. Eick D., Piechaczyk M., Henglein B., Blanchard J. M., Traub B., Kofler E., Wiest S., Lenoir G. M., Bornkamm G. W. Aberrant c-myc RNAs of Burkitt's lymphoma cells have longer half-lives. EMBO J. 1985 Dec 30;4(13B):3717–3725. doi: 10.1002/j.1460-2075.1985.tb04140.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  15. Graves R. A., Pandey N. B., Chodchoy N., Marzluff W. F. Translation is required for regulation of histone mRNA degradation. Cell. 1987 Feb 27;48(4):615–626. doi: 10.1016/0092-8674(87)90240-6. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Hoekema A., Kastelein R. A., Vasser M., de Boer H. A. Codon replacement in the PGK1 gene of Saccharomyces cerevisiae: experimental approach to study the role of biased codon usage in gene expression. Mol Cell Biol. 1987 Aug;7(8):2914–2924. doi: 10.1128/mcb.7.8.2914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. McKnight S. L., Gavis E. R., Kingsbury R., Axel R. Analysis of transcriptional regulatory signals of the HSV thymidine kinase gene: identification of an upstream control region. Cell. 1981 Aug;25(2):385–398. doi: 10.1016/0092-8674(81)90057-x. [DOI] [PubMed] [Google Scholar]
  20. Mead D. A., Szczesna-Skorupa E., Kemper B. Single-stranded DNA 'blue' T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Eng. 1986 Oct-Nov;1(1):67–74. doi: 10.1093/protein/1.1.67. [DOI] [PubMed] [Google Scholar]
  21. Morris T., Marashi F., Weber L., Hickey E., Greenspan D., Bonner J., Stein J., Stein G. Involvement of the 5'-leader sequence in coupling the stability of a human H3 histone mRNA with DNA replication. Proc Natl Acad Sci U S A. 1986 Feb;83(4):981–985. doi: 10.1073/pnas.83.4.981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Muschel R., Khoury G., Reid L. M. Regulation of insulin mRNA abundance and adenylation: dependence on hormones and matrix substrata. Mol Cell Biol. 1986 Jan;6(1):337–341. doi: 10.1128/mcb.6.1.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Müllner E. W., Kühn L. C. A stem-loop in the 3' untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm. Cell. 1988 Jun 3;53(5):815–825. doi: 10.1016/0092-8674(88)90098-0. [DOI] [PubMed] [Google Scholar]
  24. Paek I., Axel R. Glucocorticoids enhance stability of human growth hormone mRNA. Mol Cell Biol. 1987 Apr;7(4):1496–1507. doi: 10.1128/mcb.7.4.1496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pandey N. B., Marzluff W. F. The stem-loop structure at the 3' end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability. Mol Cell Biol. 1987 Dec;7(12):4557–4559. doi: 10.1128/mcb.7.12.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Parker B. A., Stark G. R. Regulation of simian virus 40 transcription: sensitive analysis of the RNA species present early in infections by virus or viral DNA. J Virol. 1979 Aug;31(2):360–369. doi: 10.1128/jvi.31.2.360-369.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Riegel A. T., Martin M. B., Schoenberg D. R. Transcriptional and post-transcriptional inhibition of albumin gene expression by estrogen in Xenopus liver. Mol Cell Endocrinol. 1986 Mar;44(3):201–209. doi: 10.1016/0303-7207(86)90125-5. [DOI] [PubMed] [Google Scholar]
  28. Ross J., Kobs G. H4 histone messenger RNA decay in cell-free extracts initiates at or near the 3' terminus and proceeds 3' to 5'. J Mol Biol. 1986 Apr 20;188(4):579–593. doi: 10.1016/s0022-2836(86)80008-0. [DOI] [PubMed] [Google Scholar]
  29. Ross J. The turnover of messenger RNA. Sci Am. 1989 Apr;260(4):48–55. doi: 10.1038/scientificamerican0489-48. [DOI] [PubMed] [Google Scholar]
  30. Salton S. R., Blum M., Jonassen J. A., Clayton R. N., Roberts J. L. Stimulation of pituitary luteinizing hormone secretion by gonadotropin-releasing hormone is not coupled to beta-luteinizing hormone gene transcription. Mol Endocrinol. 1988 Nov;2(11):1033–1042. doi: 10.1210/mend-2-11-1033. [DOI] [PubMed] [Google Scholar]
  31. Santos G. F., Scott G. K., Lee W. M., Liu E., Benz C. Estrogen-induced post-transcriptional modulation of c-myc proto-oncogene expression in human breast cancer cells. J Biol Chem. 1988 Jul 15;263(20):9565–9568. [PubMed] [Google Scholar]
  32. Shapiro D. J., Baker H. J. Purification and characterization of Xenopus laevis vitellogenin messenger RNA. J Biol Chem. 1977 Aug 10;252(15):5244–5250. [PubMed] [Google Scholar]
  33. Shapiro D. J., Blume J. E., Nielsen D. A. Regulation of messenger RNA stability in eukaryotic cells. Bioessays. 1987 May;6(5):221–226. doi: 10.1002/bies.950060507. [DOI] [PubMed] [Google Scholar]
  34. Shapiro R. A., Herrick D., Manrow R. E., Blinder D., Jacobson A. Determinants of mRNA stability in Dictyostelium discoideum amoebae: differences in poly(A) tail length, ribosome loading, and mRNA size cannot account for the heterogeneity of mRNA decay rates. Mol Cell Biol. 1988 May;8(5):1957–1969. doi: 10.1128/mcb.8.5.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986 Aug 29;46(5):659–667. doi: 10.1016/0092-8674(86)90341-7. [DOI] [PubMed] [Google Scholar]
  36. Treisman R. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5' element and c-fos 3' sequences. Cell. 1985 Oct;42(3):889–902. doi: 10.1016/0092-8674(85)90285-5. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Wolffe A. P., Glover J. F., Martin S. C., Tenniswood M. P., Williams J. L., Tata J. R. Deinduction of transcription of Xenopus 74-kDa albumin genes and destabilization of mRNA by estrogen in vivo and in hepatocyte cultures. Eur J Biochem. 1985 Feb 1;146(3):489–496. doi: 10.1111/j.1432-1033.1985.tb08678.x. [DOI] [PubMed] [Google Scholar]
  39. Yen T. J., Machlin P. S., Cleveland D. W. Autoregulated instability of beta-tubulin mRNAs by recognition of the nascent amino terminus of beta-tubulin. Nature. 1988 Aug 18;334(6183):580–585. doi: 10.1038/334580a0. [DOI] [PubMed] [Google Scholar]

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