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. 1990 Jul 25;18(14):4157–4165. doi: 10.1093/nar/18.14.4157

Chromatin studies reveal that an ERE is located far upstream of a vitellogenin gene and that a distal tissue-specific hypersensitive site is conserved for two coordinately regulated vitellogenin genes.

J B Burch 1, A H Fischer 1
PMCID: PMC331173  PMID: 2377458

Abstract

Estrogen induces the expression of three vitellogenin genes in chicken hepatocytes. To survey the vitellogenin III (VTGIII) gene region for possible distal regulatory sequences, we identified tissue-specific hypersensitive (HS) sites within a 45 kb chromatin region spanning this gene. Five constitutive HS sites were found to mark the VTGIII gene region in hormone-naive hepatocytes. Strikingly, the constitutive HS site located 5.5 kb upstream of the VTGIII gene and a previously identified HS site located within the coordinately regulated VTGII gene mapped to nearly identical copies of a 72 bp sequence. Moreover, it would appear that there has been evolutionary pressure to retain specifically this 72 bp of VTGII-like sequence near the VTGIII gene subsequent to the VTGIII and VTGII genes becoming unlinked approximately 16 Myr ago. Two additional sets of HS sites were induced in the VTGIII gene region in response to estrogen. One set mapped immediately upstream of the gene in the vicinity of what we show to be a functional estrogen response element (ERE). The other induced HS site mapped 7.5 kb upstream of the gene. This far-upstream region was sequenced and was found to contain two imperfect ERE consensus sequences spaced 88 bp apart. In transient expression assays neither of these individual imperfect ERE sequences was functional, but a fragment spanning both sequences behaved as a strong ERE. In contrast to this synergism between imperfect ERE sequences, the presence of an NF-1 binding site 23 bp away from the more distal imperfect ERE sequence was not sufficient to render the latter a functional ERE in our assays.

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Selected References

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  1. Berry M., Nunez A. M., Chambon P. Estrogen-responsive element of the human pS2 gene is an imperfectly palindromic sequence. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1218–1222. doi: 10.1073/pnas.86.4.1218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burch J. B., Evans M. I., Friedman T. M., O'Malley P. J. Two functional estrogen response elements are located upstream of the major chicken vitellogenin gene. Mol Cell Biol. 1988 Mar;8(3):1123–1131. doi: 10.1128/mcb.8.3.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burch J. B. Identification and sequence analysis of the 5' end of the major chicken vitellogenin gene. Nucleic Acids Res. 1984 Jan 25;12(2):1117–1135. doi: 10.1093/nar/12.2.1117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burch J. B., Weintraub H. Temporal order of chromatin structural changes associated with activation of the major chicken vitellogenin gene. Cell. 1983 May;33(1):65–76. doi: 10.1016/0092-8674(83)90335-5. [DOI] [PubMed] [Google Scholar]
  5. Chen E. Y., Seeburg P. H. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA. 1985 Apr;4(2):165–170. doi: 10.1089/dna.1985.4.165. [DOI] [PubMed] [Google Scholar]
  6. Döbbeling U., Ross K., Klein-Hitpass L., Morley C., Wagner U., Ryffel G. U. A cell-specific activator in the Xenopus A2 vitellogenin gene: promoter elements functioning with rat liver nuclear extracts. EMBO J. 1988 Aug;7(8):2495–2501. doi: 10.1002/j.1460-2075.1988.tb03096.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Elbrecht A., Lazier C. B., Protter A. A., Williams D. L. Independent developmental programs for two estrogen-regulated genes. Science. 1984 Aug 10;225(4662):639–641. doi: 10.1126/science.6740331. [DOI] [PubMed] [Google Scholar]
  8. Evans M. I., O'Malley P. J., Krust A., Burch J. B. Developmental regulation of the estrogen receptor and the estrogen responsiveness of five yolk protein genes in the avian liver. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8493–8497. doi: 10.1073/pnas.84.23.8493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Evans M. I., Silva R., Burch J. B. Isolation of chicken vitellogenin I and III cDNAs and the developmental regulation of five estrogen-responsive genes in the embryonic liver. Genes Dev. 1988 Jan;2(1):116–124. doi: 10.1101/gad.2.1.116. [DOI] [PubMed] [Google Scholar]
  10. Forrester W. C., Takegawa S., Papayannopoulou T., Stamatoyannopoulos G., Groudine M. Evidence for a locus activation region: the formation of developmentally stable hypersensitive sites in globin-expressing hybrids. Nucleic Acids Res. 1987 Dec 23;15(24):10159–10177. doi: 10.1093/nar/15.24.10159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Greaves D. R., Wilson F. D., Lang G., Kioussis D. Human CD2 3'-flanking sequences confer high-level, T cell-specific, position-independent gene expression in transgenic mice. Cell. 1989 Mar 24;56(6):979–986. doi: 10.1016/0092-8674(89)90631-4. [DOI] [PubMed] [Google Scholar]
  14. Gross D. S., Garrard W. T. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159–197. doi: 10.1146/annurev.bi.57.070188.001111. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Johnson P. F. Transcriptional activators in hepatocytes. Cell Growth Differ. 1990 Jan;1(1):47–52. [PubMed] [Google Scholar]
  18. 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]
  19. Jost J. P., Moncharmont B., Jiricny J., Saluz H., Hertner T. In vitro secondary activation (memory effect) of avian vitellogenin II gene in isolated liver nuclei. Proc Natl Acad Sci U S A. 1986 Jan;83(1):43–47. doi: 10.1073/pnas.83.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Klein-Hitpass L., Ryffel G. U., Heitlinger E., Cato A. C. A 13 bp palindrome is a functional estrogen responsive element and interacts specifically with estrogen receptor. Nucleic Acids Res. 1988 Jan 25;16(2):647–663. doi: 10.1093/nar/16.2.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Krust A., Green S., Argos P., Kumar V., Walter P., Bornert J. M., Chambon P. The chicken oestrogen receptor sequence: homology with v-erbA and the human oestrogen and glucocorticoid receptors. EMBO J. 1986 May;5(5):891–897. doi: 10.1002/j.1460-2075.1986.tb04300.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Luckow B., Schütz G. CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res. 1987 Jul 10;15(13):5490–5490. doi: 10.1093/nar/15.13.5490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maurer R. A., Notides A. C. Identification of an estrogen-responsive element from the 5'-flanking region of the rat prolactin gene. Mol Cell Biol. 1987 Dec;7(12):4247–4254. doi: 10.1128/mcb.7.12.4247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McKnight S. L., Lane M. D., Gluecksohn-Waelsch S. Is CCAAT/enhancer-binding protein a central regulator of energy metabolism? Genes Dev. 1989 Dec;3(12B):2021–2024. doi: 10.1101/gad.3.12b.2021. [DOI] [PubMed] [Google Scholar]
  26. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nowock J., Borgmeyer U., Püschel A. W., Rupp R. A., Sippel A. E. The TGGCA protein binds to the MMTV-LTR, the adenovirus origin of replication, and the BK virus enhancer. Nucleic Acids Res. 1985 Mar 25;13(6):2045–2061. doi: 10.1093/nar/13.6.2045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Raynaud J. P., Bouton M. M., Gallet-Bourquin D., Philibert D., Tournemine C., Azadian-Baulanger G. Comparative study of estrogen action. Mol Pharmacol. 1973 Jul;9(4):520–533. [PubMed] [Google Scholar]
  29. Ryden T. A., Beemon K. Avian retroviral long terminal repeats bind CCAAT/enhancer-binding protein. Mol Cell Biol. 1989 Mar;9(3):1155–1164. doi: 10.1128/mcb.9.3.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schüle R., Muller M., Kaltschmidt C., Renkawitz R. Many transcription factors interact synergistically with steroid receptors. Science. 1988 Dec 9;242(4884):1418–1420. doi: 10.1126/science.3201230. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Silva R., Burch J. B. Evidence that chicken CR1 elements represent a novel family of retroposons. Mol Cell Biol. 1989 Aug;9(8):3563–3566. doi: 10.1128/mcb.9.8.3563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Silva R., Fischer A. H., Burch J. B. The major and minor chicken vitellogenin genes are each adjacent to partially deleted pseudogene copies of the other. Mol Cell Biol. 1989 Aug;9(8):3557–3562. doi: 10.1128/mcb.9.8.3557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Tora L., Gaub M. P., Mader S., Dierich A., Bellard M., Chambon P. Cell-specific activity of a GGTCA half-palindromic oestrogen-responsive element in the chicken ovalbumin gene promoter. EMBO J. 1988 Dec 1;7(12):3771–3778. doi: 10.1002/j.1460-2075.1988.tb03261.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Waterman M. L., Adler S., Nelson C., Greene G. L., Evans R. M., Rosenfeld M. G. A single domain of the estrogen receptor confers deoxyribonucleic acid binding and transcriptional activation of the rat prolactin gene. Mol Endocrinol. 1988 Jan;2(1):14–21. doi: 10.1210/mend-2-1-14. [DOI] [PubMed] [Google Scholar]
  40. Wilks A., Seldran M., Jost J. P. An estrogen-dependent demethylation at the 5' end of the chicken vitellogenin gene is independent of DNA synthesis. Nucleic Acids Res. 1984 Jan 25;12(2):1163–1177. doi: 10.1093/nar/12.2.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. van het Schip F. D., Samallo J., Broos J., Ophuis J., Mojet M., Gruber M., AB G. Nucleotide sequence of a chicken vitellogenin gene and derived amino acid sequence of the encoded yolk precursor protein. J Mol Biol. 1987 Jul 20;196(2):245–260. doi: 10.1016/0022-2836(87)90688-7. [DOI] [PubMed] [Google Scholar]
  42. van het Schip F., Samallo J., Meijlink F., Gruber M., AB G. A new repetitive element of the CR1 family downstream of the chicken vitellogenin gene. Nucleic Acids Res. 1987 May 26;15(10):4193–4202. doi: 10.1093/nar/15.10.4193. [DOI] [PMC free article] [PubMed] [Google Scholar]

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