Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1991 Jan 11;19(1):33–41. doi: 10.1093/nar/19.1.33

Oestrogen facilitates the binding of ubiquitous and liver-enriched nuclear proteins to the apoVLDL II promoter in vivo.

J Wijnholds 1, E Muller 1, G Ab 1
PMCID: PMC333531  PMID: 2011511

Abstract

Using genomic and in vitro DNasel footprinting, we have analyzed protein-DNA interactions within the promoter region of the oestrogen-inducible gene encoding chicken apoVLDL II. The footprints coincide with previously detected guanosine-protein contacts in vivo. All footprints identified are present in the apoVLDL II-expressing liver exclusively and absent in hormone-naive liver, spleen and oviduct. They comprise recognition sites for the oestrogen receptor, the ubiquitous COUP-transcription factor, the liver-enriched C/EBP and/or DBP and the liver-specific LF-A1. In vitro, binding of protein to the oestrogen response element (ERE) is excluded by the prior binding of a protein, possibly C/EBP or DBP, to an adjacent element. The recognition sequence of the COUP-TF is also a target for LF-A1. The results suggests that oestrogen-dependent liver specific activation of the apoVLDL II promoter is established by the binding of the oestrogen receptor to EREs and multiple liver-enriched factors (C/EBP, DBP and LF-A1) to their nearby recognition sequences. Apparently, several DNA binding nuclear proteins cooperate to keep the promoter in a state that is accessible for the RNA polymerase complex.

Full text

PDF
35

Images in this article

35Image
on p.35
36Image
on p.36
37Image
on p.37
38Image
on p.38
39Image
on p.39

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bakker O., Philipsen J. N., Hennis B. C., Ab G. Estrogen-inducible binding of a nuclear factor to the vitellogenin upstream region. Mol Cell Biol. 1988 Oct;8(10):4557–4560. doi: 10.1128/mcb.8.10.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beato M. Gene regulation by steroid hormones. Cell. 1989 Feb 10;56(3):335–344. doi: 10.1016/0092-8674(89)90237-7. [DOI] [PubMed] [Google Scholar]
  3. Cereghini S., Raymondjean M., Carranca A. G., Herbomel P., Yaniv M. Factors involved in control of tissue-specific expression of albumin gene. Cell. 1987 Aug 14;50(4):627–638. doi: 10.1016/0092-8674(87)90036-5. [DOI] [PubMed] [Google Scholar]
  4. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cordingley M. G., Riegel A. T., Hager G. L. Steroid-dependent interaction of transcription factors with the inducible promoter of mouse mammary tumor virus in vivo. Cell. 1987 Jan 30;48(2):261–270. doi: 10.1016/0092-8674(87)90429-6. [DOI] [PubMed] [Google Scholar]
  6. Costa R. H., Grayson D. R., Darnell J. E., Jr Multiple hepatocyte-enriched nuclear factors function in the regulation of transthyretin and alpha 1-antitrypsin genes. Mol Cell Biol. 1989 Apr;9(4):1415–1425. doi: 10.1128/mcb.9.4.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Courtois G., Morgan J. G., Campbell L. A., Fourel G., Crabtree G. R. Interaction of a liver-specific nuclear factor with the fibrinogen and alpha 1-antitrypsin promoters. Science. 1987 Oct 30;238(4827):688–692. doi: 10.1126/science.3499668. [DOI] [PubMed] [Google Scholar]
  8. Frain M., Swart G., Monaci P., Nicosia A., Stämpfli S., Frank R., Cortese R. The liver-specific transcription factor LF-B1 contains a highly diverged homeobox DNA binding domain. Cell. 1989 Oct 6;59(1):145–157. doi: 10.1016/0092-8674(89)90877-5. [DOI] [PubMed] [Google Scholar]
  9. Friedman A. D., Landschulz W. H., McKnight S. L. CCAAT/enhancer binding protein activates the promoter of the serum albumin gene in cultured hepatoma cells. Genes Dev. 1989 Sep;3(9):1314–1322. doi: 10.1101/gad.3.9.1314. [DOI] [PubMed] [Google Scholar]
  10. Gorski K., Carneiro M., Schibler U. Tissue-specific in vitro transcription from the mouse albumin promoter. Cell. 1986 Dec 5;47(5):767–776. doi: 10.1016/0092-8674(86)90519-2. [DOI] [PubMed] [Google Scholar]
  11. Graves B. J., Johnson P. F., McKnight S. L. Homologous recognition of a promoter domain common to the MSV LTR and the HSV tk gene. Cell. 1986 Feb 28;44(4):565–576. doi: 10.1016/0092-8674(86)90266-7. [DOI] [PubMed] [Google Scholar]
  12. Grosveld F., van Assendelft G. B., Greaves D. R., Kollias G. Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell. 1987 Dec 24;51(6):975–985. doi: 10.1016/0092-8674(87)90584-8. [DOI] [PubMed] [Google Scholar]
  13. Hardon E. M., Frain M., Paonessa G., Cortese R. Two distinct factors interact with the promoter regions of several liver-specific genes. EMBO J. 1988 Jun;7(6):1711–1719. doi: 10.1002/j.1460-2075.1988.tb03000.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Johnson P. F., Landschulz W. H., Graves B. J., McKnight S. L. Identification of a rat liver nuclear protein that binds to the enhancer core element of three animal viruses. Genes Dev. 1987 Apr;1(2):133–146. doi: 10.1101/gad.1.2.133. [DOI] [PubMed] [Google Scholar]
  15. Jones K. A., Kadonaga J. T., Rosenfeld P. J., Kelly T. J., Tjian R. A cellular DNA-binding protein that activates eukaryotic transcription and DNA replication. Cell. 1987 Jan 16;48(1):79–89. doi: 10.1016/0092-8674(87)90358-8. [DOI] [PubMed] [Google Scholar]
  16. Klein-Hitpass L., Schorpp M., Wagner U., Ryffel G. U. An estrogen-responsive element derived from the 5' flanking region of the Xenopus vitellogenin A2 gene functions in transfected human cells. Cell. 1986 Sep 26;46(7):1053–1061. doi: 10.1016/0092-8674(86)90705-1. [DOI] [PubMed] [Google Scholar]
  17. Kok K., Snippe L., Ab G., Gruber M. Nuclease-hypersensitive sites in chromatin of the estrogen-inducible apoVLDL II gene of chicken. Nucleic Acids Res. 1985 Jul 25;13(14):5189–5202. doi: 10.1093/nar/13.14.5189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Landschulz W. H., Johnson P. F., Adashi E. Y., Graves B. J., McKnight S. L. Isolation of a recombinant copy of the gene encoding C/EBP. Genes Dev. 1988 Jul;2(7):786–800. doi: 10.1101/gad.2.7.786. [DOI] [PubMed] [Google Scholar]
  20. LeBowitz J. H., Kobayashi T., Staudt L., Baltimore D., Sharp P. A. Octamer-binding proteins from B or HeLa cells stimulate transcription of the immunoglobulin heavy-chain promoter in vitro. Genes Dev. 1988 Oct;2(10):1227–1237. doi: 10.1101/gad.2.10.1227. [DOI] [PubMed] [Google Scholar]
  21. Lichtsteiner S., Schibler U. A glycosylated liver-specific transcription factor stimulates transcription of the albumin gene. Cell. 1989 Jun 30;57(7):1179–1187. doi: 10.1016/0092-8674(89)90055-x. [DOI] [PubMed] [Google Scholar]
  22. Lichtsteiner S., Wuarin J., Schibler U. The interplay of DNA-binding proteins on the promoter of the mouse albumin gene. Cell. 1987 Dec 24;51(6):963–973. doi: 10.1016/0092-8674(87)90583-6. [DOI] [PubMed] [Google Scholar]
  23. Maire P., Wuarin J., Schibler U. The role of cis-acting promoter elements in tissue-specific albumin gene expression. Science. 1989 Apr 21;244(4902):343–346. doi: 10.1126/science.2711183. [DOI] [PubMed] [Google Scholar]
  24. Maniatis T., Goodbourn S., Fischer J. A. Regulation of inducible and tissue-specific gene expression. Science. 1987 Jun 5;236(4806):1237–1245. doi: 10.1126/science.3296191. [DOI] [PubMed] [Google Scholar]
  25. Martinez E., Givel F., Wahli W. The estrogen-responsive element as an inducible enhancer: DNA sequence requirements and conversion to a glucocorticoid-responsive element. EMBO J. 1987 Dec 1;6(12):3719–3727. doi: 10.1002/j.1460-2075.1987.tb02706.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  27. Metzger D., White J. H., Chambon P. The human oestrogen receptor functions in yeast. Nature. 1988 Jul 7;334(6177):31–36. doi: 10.1038/334031a0. [DOI] [PubMed] [Google Scholar]
  28. Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
  29. Monaci P., Nicosia A., Cortese R. Two different liver-specific factors stimulate in vitro transcription from the human alpha 1-antitrypsin promoter. EMBO J. 1988 Jul;7(7):2075–2087. doi: 10.1002/j.1460-2075.1988.tb03047.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mueller C. R., Maire P., Schibler U. DBP, a liver-enriched transcriptional activator, is expressed late in ontogeny and its tissue specificity is determined posttranscriptionally. Cell. 1990 Apr 20;61(2):279–291. doi: 10.1016/0092-8674(90)90808-r. [DOI] [PubMed] [Google Scholar]
  31. Ofverstedt L. G., Hammarström K., Balgobin N., Hjertén S., Pettersson U., Chattopadhyaya J. Rapid and quantitative recovery of DNA fragments from gels by displacement electrophoresis (isotachophoresis). Biochim Biophys Acta. 1984 Jun 16;782(2):120–126. doi: 10.1016/0167-4781(84)90014-9. [DOI] [PubMed] [Google Scholar]
  32. Pauli U., Chrysogelos S., Stein G., Stein J., Nick H. Protein-DNA interactions in vivo upstream of a cell cycle-regulated human H4 histone gene. Science. 1987 Jun 5;236(4806):1308–1311. doi: 10.1126/science.3035717. [DOI] [PubMed] [Google Scholar]
  33. Philipsen J. N., Hennis B. C., Ab G. In vivo footprinting of the estrogen-inducible vitellogenin II gene from chicken. Nucleic Acids Res. 1988 Oct 25;16(20):9663–9676. doi: 10.1093/nar/16.20.9663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Piña B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. doi: 10.1016/0092-8674(90)90087-u. [DOI] [PubMed] [Google Scholar]
  35. Ptashne M. How eukaryotic transcriptional activators work. Nature. 1988 Oct 20;335(6192):683–689. doi: 10.1038/335683a0. [DOI] [PubMed] [Google Scholar]
  36. Saluz H., Jost J. P. Optimized genomic sequencing as a tool for the study of cytosine methylation in the regulatory region of the chicken vitellogenin II gene. Gene. 1986;42(2):151–157. doi: 10.1016/0378-1119(86)90291-x. [DOI] [PubMed] [Google Scholar]
  37. Schmid W., Strähle U., Schütz G., Schmitt J., Stunnenberg H. Glucocorticoid receptor binds cooperatively to adjacent recognition sites. EMBO J. 1989 Aug;8(8):2257–2263. doi: 10.1002/j.1460-2075.1989.tb08350.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schüle R., Muller M., Otsuka-Murakami H., Renkawitz R. Cooperativity of the glucocorticoid receptor and the CACCC-box binding factor. Nature. 1988 Mar 3;332(6159):87–90. doi: 10.1038/332087a0. [DOI] [PubMed] [Google Scholar]
  39. Seiler-Tuyns A., Walker P., Martinez E., Mérillat A. M., Givel F., Wahli W. Identification of estrogen-responsive DNA sequences by transient expression experiments in a human breast cancer cell line. Nucleic Acids Res. 1986 Nov 25;14(22):8755–8770. doi: 10.1093/nar/14.22.8755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Strähle U., Schmid W., Schütz G. Synergistic action of the glucocorticoid receptor with transcription factors. EMBO J. 1988 Nov;7(11):3389–3395. doi: 10.1002/j.1460-2075.1988.tb03212.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Thomas G. H., Elgin S. C. Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J. 1988 Jul;7(7):2191–2201. doi: 10.1002/j.1460-2075.1988.tb03058.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tsai S. Y., Sagami I., Wang H., Tsai M. J., O'Malley B. W. Interactions between a DNA-binding transcription factor (COUP) and a non-DNA binding factor (S300-II). Cell. 1987 Aug 28;50(5):701–709. doi: 10.1016/0092-8674(87)90328-x. [DOI] [PubMed] [Google Scholar]
  43. Tsai S. Y., Tsai M. J., O'Malley B. W. Cooperative binding of steroid hormone receptors contributes to transcriptional synergism at target enhancer elements. Cell. 1989 May 5;57(3):443–448. doi: 10.1016/0092-8674(89)90919-7. [DOI] [PubMed] [Google Scholar]
  44. Wall L., deBoer E., Grosveld F. The human beta-globin gene 3' enhancer contains multiple binding sites for an erythroid-specific protein. Genes Dev. 1988 Sep;2(9):1089–1100. doi: 10.1101/gad.2.9.1089. [DOI] [PubMed] [Google Scholar]
  45. Wang L. H., Tsai S. Y., Cook R. G., Beattie W. G., Tsai M. J., O'Malley B. W. COUP transcription factor is a member of the steroid receptor superfamily. Nature. 1989 Jul 13;340(6229):163–166. doi: 10.1038/340163a0. [DOI] [PubMed] [Google Scholar]
  46. Wijnholds J., Philipsen J. N., Ab G. Tissue-specific and steroid-dependent interaction of transcription factors with the oestrogen-inducible apoVLDL II promoter in vivo. EMBO J. 1988 Sep;7(9):2757–2763. doi: 10.1002/j.1460-2075.1988.tb03130.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Zinn K., Maniatis T. Detection of factors that interact with the human beta-interferon regulatory region in vivo by DNAase I footprinting. Cell. 1986 May 23;45(4):611–618. doi: 10.1016/0092-8674(86)90293-x. [DOI] [PubMed] [Google Scholar]
  48. de Vries E., van Driel W., van den Heuvel S. J., van der Vliet P. C. Contactpoint analysis of the HeLa nuclear factor I recognition site reveals symmetrical binding at one side of the DNA helix. EMBO J. 1987 Jan;6(1):161–168. doi: 10.1002/j.1460-2075.1987.tb04734.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. van het Schip A. D., Meijlink F. C., Strijker R., Gruber M., van Vliet A. J., van de Klundert J. A., Ab G. The nucleotide sequence of the chicken apo very low density lipoprotein II gene. Nucleic Acids Res. 1983 May 11;11(9):2529–2540. doi: 10.1093/nar/11.9.2529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. van het Schip F., Strijker R., Samallo J., Gruber M., Geert A. B. Conserved sequence motifs upstream from the co-ordinately expressed vitellogenin and apoVLDLII genes of chicken. Nucleic Acids Res. 1986 Nov 11;14(21):8669–8680. doi: 10.1093/nar/14.21.8669. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES