Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1989 Mar;9(3):1155–1164. doi: 10.1128/mcb.9.3.1155

Avian retroviral long terminal repeats bind CCAAT/enhancer-binding protein.

T A Ryden 1, K Beemon 1
PMCID: PMC362706  PMID: 2725492

Abstract

DNA-protein interactions involving enhancer and promoter sequences within the U3 regions of several avian retroviral long terminal repeats (LTRs) were studied by DNase I footprinting. The rat CCAAT/enhancer-binding protein, C/EBP, bound to all four viral LTRs examined. The Rous sarcoma virus binding site corresponded closely to the 5' limit of the LTR enhancer; nucleotides -225 to -188 were protected as a pair of adjacent binding domains. The Fujinami sarcoma virus LTR bound C/EBP at a single site at nucleotides -213 to -195. C/EBP also bound to the promoter region of the enhancerless Rous-associated virus-0 LTR at nucleotides -77 to -57. The avian myeloblastosis virus LTR bound C/EBP at three sites: nucleotides -262 to -246, -154 to -134, and -55 to -39. We have previously observed binding of C/EBP to an enhancer in the gag gene of avian retroviruses. A heat-treated nuclear extract from chicken liver bound to all of the same retroviral sequences as did C/EBP. Alignment of the avian retroviral binding sequences with the published binding sites for C/EBP in two CCAAT boxes and in the simian virus 40, polyoma, and murine sarcoma virus enhancers suggested TTGNNGCTAATG as a consensus sequence for binding of C/EBP. When two bases of this consensus sequence were altered by site-specific mutagenesis of the Rous sarcoma virus LTR, binding of the heat-stable chicken protein was eliminated.

Full text

PDF
1155

Images in this article

Selected References

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

  1. Arrigo S., Yun M., Beemon K. cis-acting regulatory elements within gag genes of avian retroviruses. Mol Cell Biol. 1987 Jan;7(1):388–397. doi: 10.1128/mcb.7.1.388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carlberg K., Ryden T. A., Beemon K. Localization and footprinting of an enhancer within the avian sarcoma virus gag gene. J Virol. 1988 May;62(5):1617–1624. doi: 10.1128/jvi.62.5.1617-1624.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cullen B. R., Raymond K., Ju G. Functional analysis of the transcription control region located within the avian retroviral long terminal repeat. Mol Cell Biol. 1985 Mar;5(3):438–447. doi: 10.1128/mcb.5.3.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cullen B. R., Raymond K., Ju G. Transcriptional activity of avian retroviral long terminal repeats directly correlates with enhancer activity. J Virol. 1985 Feb;53(2):515–521. doi: 10.1128/jvi.53.2.515-521.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Czernilofsky A. P., DeLorbe W., Swanstrom R., Varmus H. E., Bishop J. M., Tischer E., Goodman H. M. The nucleotide sequence of an untranslated but conserved domain at the 3' end of the avian sarcoma virus genome. Nucleic Acids Res. 1980 Jul 11;8(13):2967–2984. doi: 10.1093/nar/8.13.2967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  7. Flamant F., Le Guellec D., Verdier G., Nigon V. M. Tissue specificity of retrovirus expression in inoculated avian embryos revealed by in situ hybridization to whole-body section. Virology. 1987 Sep;160(1):301–304. doi: 10.1016/0042-6822(87)90079-1. [DOI] [PubMed] [Google Scholar]
  8. Goodwin G. H. Identification of three sequence-specific DNA-binding proteins which interact with the Rous sarcoma virus enhancer and upstream promoter elements. J Virol. 1988 Jun;62(6):2186–2190. doi: 10.1128/jvi.62.6.2186-2190.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gowda S., Rao A. S., Kim Y. W., Guntaka R. V. Identification of sequences in the long terminal repeat of avian sarcoma virus required for efficient transcription. Virology. 1988 Jan;162(1):243–247. doi: 10.1016/0042-6822(88)90415-1. [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. Hatamochi A., Golumbek P. T., Van Schaftingen E., de Crombrugghe B. A CCAAT DNA binding factor consisting of two different components that are both required for DNA binding. J Biol Chem. 1988 Apr 25;263(12):5940–5947. [PubMed] [Google Scholar]
  13. Herman S. A., Coffin J. M. Differential transcription from the long terminal repeats of integrated avian leukosis virus DNA. J Virol. 1986 Nov;60(2):497–505. doi: 10.1128/jvi.60.2.497-505.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Herr W., Gluzman Y. Duplications of a mutated simian virus 40 enhancer restore its activity. Nature. 1985 Feb 21;313(6004):711–714. doi: 10.1038/313711a0. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Jones N. C., Rigby P. W., Ziff E. B. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNA tumor viruses. Genes Dev. 1988 Mar;2(3):267–281. doi: 10.1101/gad.2.3.267. [DOI] [PubMed] [Google Scholar]
  17. Kane S. E., Beemon K. Inhibition of methylation at two internal N6-methyladenosine sites caused by GAC to GAU mutations. J Biol Chem. 1987 Mar 5;262(7):3422–3427. [PubMed] [Google Scholar]
  18. Karnitz L., Faber S., Chalkley R. Specific nuclear proteins interact with the Rous sarcoma virus internal enhancer and share a common element with the enhancer located in the long terminal repeat of the virus. Nucleic Acids Res. 1987 Dec 10;15(23):9841–9859. doi: 10.1093/nar/15.23.9841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Khoury G., Gruss P. Enhancer elements. Cell. 1983 Jun;33(2):313–314. doi: 10.1016/0092-8674(83)90410-5. [DOI] [PubMed] [Google Scholar]
  20. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  21. Laimins L. A., Tsichlis P., Khoury G. Multiple enhancer domains in the 3' terminus of the Prague strain of Rous sarcoma virus. Nucleic Acids Res. 1984 Aug 24;12(16):6427–6442. doi: 10.1093/nar/12.16.6427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Landschulz W. H., Johnson P. F., McKnight S. L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. doi: 10.1126/science.3289117. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Luciw P. A., Bishop J. M., Varmus H. E., Capecchi M. R. Location and function of retroviral and SV40 sequences that enhance biochemical transformation after microinjection of DNA. Cell. 1983 Jul;33(3):705–716. doi: 10.1016/0092-8674(83)90013-2. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Norton P. A., Coffin J. M. Characterization of Rous sarcoma virus sequences essential for viral gene expression. J Virol. 1987 Apr;61(4):1171–1179. doi: 10.1128/jvi.61.4.1171-1179.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Overbeek P. A., Lai S. P., Van Quill K. R., Westphal H. Tissue-specific expression in transgenic mice of a fused gene containing RSV terminal sequences. Science. 1986 Mar 28;231(4745):1574–1577. doi: 10.1126/science.3006249. [DOI] [PubMed] [Google Scholar]
  30. Ruddell A., Linial M., Schubach W., Groudine M. Lability of leukosis virus enhancer-binding proteins in avian hematopoeitic cells. J Virol. 1988 Aug;62(8):2728–2735. doi: 10.1128/jvi.62.8.2728-2735.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rushlow K. E., Lautenberger J. A., Reddy E. P., Souza L. M., Baluda M. A., Chirikjian J. G., Papas T. S. Nucleotide sequence analysis of the long terminal repeat of avian myeloblastosis virus and adjacent host sequences. J Virol. 1982 Jun;42(3):840–846. doi: 10.1128/jvi.42.3.840-846.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  34. Sealey L., Chalkley R. At least two nuclear proteins bind specifically to the Rous sarcoma virus long terminal repeat enhancer. Mol Cell Biol. 1987 Feb;7(2):787–798. doi: 10.1128/mcb.7.2.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shibuya M., Wang L. H., Hanafusa H. Molecular cloning of the Fujinami sarcoma virus genome and its comparison with sequences of other related transforming viruses. J Virol. 1982 Jun;42(3):1007–1016. doi: 10.1128/jvi.42.3.1007-1016.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tsichlis P. N., Donehower L., Hager G., Zeller N., Malavarca R., Astrin S., Skalka A. M. Sequence comparison in the crossover region of an oncogenic avian retrovirus recombinant and its nononcogenic parent: genetic regions that control growth rate and oncogenic potential. Mol Cell Biol. 1982 Nov;2(11):1331–1338. doi: 10.1128/mcb.2.11.1331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weber F., Schaffner W. Enhancer activity correlates with the oncogenic potential of avian retroviruses. EMBO J. 1985 Apr;4(4):949–956. doi: 10.1002/j.1460-2075.1985.tb03723.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weiher H., König M., Gruss P. Multiple point mutations affecting the simian virus 40 enhancer. Science. 1983 Feb 11;219(4585):626–631. doi: 10.1126/science.6297005. [DOI] [PubMed] [Google Scholar]
  39. Zenke M., Grundström T., Matthes H., Wintzerith M., Schatz C., Wildeman A., Chambon P. Multiple sequence motifs are involved in SV40 enhancer function. EMBO J. 1986 Feb;5(2):387–397. doi: 10.1002/j.1460-2075.1986.tb04224.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES