Abstract
Two long terminal repeat (LTR) enhancer-binding proteins which may regulate high rates of avian leukosis virus (ALV) LTR-enhanced c-myc transcription during bursal lymphomagenesis have been identified (A. Ruddell, M. Linial, and M. Groudine, Mol. Cell. Biol. 9:5660-5668, 1989). The genes encoding the a1/EBP and a3/EBP binding factors were cloned by expression screening of a lambda gt11 cDNA library from chicken bursal lymphoma cells. The a1/EBP cDNA encodes a novel leucine zipper transcription factor (W. Bowers and A. Ruddell, J. Virol. 66:6578-6586, 1992). The partial a3/EBP cDNA clone encodes amino acids 84 to 313 of vitellogenin gene-binding protein (VBP), a leucine zipper factor that binds the avian vitellogenin II gene promoter (S. Iyer, D. Davis, and J. Burch, Mol. Cell. Biol. 11:4863-4875, 1991). Multiple VBP mRNAs are expressed in B cells in a pattern identical to that previously observed for VBP in other cell types. The LTR-binding activities of VBP, a1/EBP, and B-cell nuclear extract protein were compared and mapped by gel shift, DNase I footprinting, and methylation interference assays. The purified VBP and a1/EBP bacterial fusion proteins bind overlapping but distinct subsets of CCAAT/enhancer elements in the closely related ALV and Rous sarcoma virus (RSV) LTR enhancers. Protein binding to these CCAAT/enhancer elements accounts for most of the labile LTR enhancer-binding activity observed in B-cell nuclear extracts. VBP and a1/EBP could mediate the high rates of ALV and RSV LTR-enhanced transcription in bursal lymphoma cells and many other cell types.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akira S., Isshiki H., Sugita T., Tanabe O., Kinoshita S., Nishio Y., Nakajima T., Hirano T., Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 1990 Jun;9(6):1897–1906. doi: 10.1002/j.1460-2075.1990.tb08316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baba T. W., Giroir B. P., Humphries E. H. Cell lines derived from avian lymphomas exhibit two distinct phenotypes. Virology. 1985 Jul 15;144(1):139–151. doi: 10.1016/0042-6822(85)90312-5. [DOI] [PubMed] [Google Scholar]
- Birkenmeier E. H., Gwynn B., Howard S., Jerry J., Gordon J. I., Landschulz W. H., McKnight S. L. Tissue-specific expression, developmental regulation, and genetic mapping of the gene encoding CCAAT/enhancer binding protein. Genes Dev. 1989 Aug;3(8):1146–1156. doi: 10.1101/gad.3.8.1146. [DOI] [PubMed] [Google Scholar]
- Bizub D., Katz R. A., Skalka A. M. Nucleotide sequence of noncoding regions in Rous-associated virus-2: comparisons delineate conserved regions important in replication and oncogenesis. J Virol. 1984 Feb;49(2):557–565. doi: 10.1128/jvi.49.2.557-565.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bowers W. J., Ruddell A. a1/EBP: a leucine zipper protein that binds CCAAT/enhancer elements in the avian leukosis virus long terminal repeat enhancer. J Virol. 1992 Nov;66(11):6578–6586. doi: 10.1128/jvi.66.11.6578-6586.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Coppola J. A., Cole M. D. Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment. Nature. 1986 Apr 24;320(6064):760–763. doi: 10.1038/320760a0. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drolet D. W., Scully K. M., Simmons D. M., Wegner M., Chu K. T., Swanson L. W., Rosenfeld M. G. TEF, a transcription factor expressed specifically in the anterior pituitary during embryogenesis, defines a new class of leucine zipper proteins. Genes Dev. 1991 Oct;5(10):1739–1753. doi: 10.1101/gad.5.10.1739. [DOI] [PubMed] [Google Scholar]
- Ellenberger T. E., Brandl C. J., Struhl K., Harrison S. C. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein-DNA complex. Cell. 1992 Dec 24;71(7):1223–1237. doi: 10.1016/s0092-8674(05)80070-4. [DOI] [PubMed] [Google Scholar]
- Evan G. I., Wyllie A. H., Gilbert C. S., Littlewood T. D., Land H., Brooks M., Waters C. M., Penn L. Z., Hancock D. C. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 1992 Apr 3;69(1):119–128. doi: 10.1016/0092-8674(92)90123-t. [DOI] [PubMed] [Google Scholar]
- Ewert D. L., de Boer G. F. Avian lymphoid leukosis: mechanisms of lymphomagenesis. Adv Vet Sci Comp Med. 1988;32:37–55. doi: 10.1016/b978-0-12-039232-2.50006-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Friedman A. D., McKnight S. L. Identification of two polypeptide segments of CCAAT/enhancer-binding protein required for transcriptional activation of the serum albumin gene. Genes Dev. 1990 Aug;4(8):1416–1426. doi: 10.1101/gad.4.8.1416. [DOI] [PubMed] [Google Scholar]
- Galas D. J., Schmitz A. DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 1978 Sep;5(9):3157–3170. doi: 10.1093/nar/5.9.3157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Habel D. E., Dohrer K. L., Conklin K. F. Functional and defective components of avian endogenous virus long terminal repeat enhancer sequences. J Virol. 1993 Mar;67(3):1545–1554. doi: 10.1128/jvi.67.3.1545-1554.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hendrickson W., Schleif R. A dimer of AraC protein contacts three adjacent major groove regions of the araI DNA site. Proc Natl Acad Sci U S A. 1985 May;82(10):3129–3133. doi: 10.1073/pnas.82.10.3129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hunger S. P., Ohyashiki K., Toyama K., Cleary M. L. Hlf, a novel hepatic bZIP protein, shows altered DNA-binding properties following fusion to E2A in t(17;19) acute lymphoblastic leukemia. Genes Dev. 1992 Sep;6(9):1608–1620. doi: 10.1101/gad.6.9.1608. [DOI] [PubMed] [Google Scholar]
- Iyer S. V., Davis D. L., Seal S. N., Burch J. B. Chicken vitellogenin gene-binding protein, a leucine zipper transcription factor that binds to an important control element in the chicken vitellogenin II promoter, is related to rat DBP. Mol Cell Biol. 1991 Oct;11(10):4863–4875. doi: 10.1128/mcb.11.10.4863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson P. F. Identification of C/EBP basic region residues involved in DNA sequence recognition and half-site spacing preference. Mol Cell Biol. 1993 Nov;13(11):6919–6930. doi: 10.1128/mcb.13.11.6919. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Kenny S., Guntaka R. V. Localization by mutational analysis of transcription factor binding sequences in the U3 region of Rous sarcoma virus LTR. Virology. 1990 Jun;176(2):483–493. doi: 10.1016/0042-6822(90)90018-m. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Linial M., Gunderson N., Groudine M. Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science. 1985 Dec 6;230(4730):1126–1132. doi: 10.1126/science.2999973. [DOI] [PubMed] [Google Scholar]
- 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]
- Motta J. V., Crittenden L. B., Purchase H. G., Stone H. A., Witter R. L. Low oncogenic potential of avian endogenous RNA tumor virus infection or expression. J Natl Cancer Inst. 1975 Sep;55(3):685–689. doi: 10.1093/jnci/55.3.685. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Nye J. A., Graves B. J. Alkylation interference identifies essential DNA contacts for sequence-specific binding of the eukaryotic transcription factor C/EBP. Proc Natl Acad Sci U S A. 1990 May;87(10):3992–3996. doi: 10.1073/pnas.87.10.3992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Neil K. T., Shuman J. D., Ampe C., DeGrado W. F. DNA-induced increase in the alpha-helical content of C/EBP and GCN4. Biochemistry. 1991 Sep 17;30(37):9030–9034. doi: 10.1021/bi00101a017. [DOI] [PubMed] [Google Scholar]
- Pei D. Q., Shih C. H. Transcriptional activation and repression by cellular DNA-binding protein C/EBP. J Virol. 1990 Apr;64(4):1517–1522. doi: 10.1128/jvi.64.4.1517-1522.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Purchase H. G., Gilmour D. G., Romero C. H., Okazaki W. Post-infection genetic resistance to avian lymphoid leukosis resides in B target cell. Nature. 1977 Nov 3;270(5632):61–62. doi: 10.1038/270061a0. [DOI] [PubMed] [Google Scholar]
- Robinson H. L., Blais B. M., Tsichlis P. N., Coffin J. M. At least two regions of the viral genome determine the oncogenic potential of avian leukosis viruses. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1225–1229. doi: 10.1073/pnas.79.4.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roman C., Platero J. S., Shuman J., Calame K. Ig/EBP-1: a ubiquitously expressed immunoglobulin enhancer binding protein that is similar to C/EBP and heterodimerizes with C/EBP. Genes Dev. 1990 Aug;4(8):1404–1415. doi: 10.1101/gad.4.8.1404. [DOI] [PubMed] [Google Scholar]
- Ruddell A., Linial M. L., Groudine M. Tissue-specific lability and expression of avian leukosis virus long terminal repeat enhancer-binding proteins. Mol Cell Biol. 1989 Dec;9(12):5660–5668. doi: 10.1128/mcb.9.12.5660. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Ryden T. A., de Mars M., Beemon K. Mutation of the C/EBP binding sites in the Rous sarcoma virus long terminal repeat and gag enhancers. J Virol. 1993 May;67(5):2862–2870. doi: 10.1128/jvi.67.5.2862-2870.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
- Sears R. C., Sealy L. Characterization of nuclear proteins that bind the EFII enhancer sequence in the Rous sarcoma virus long terminal repeat. J Virol. 1992 Nov;66(11):6338–6352. doi: 10.1128/jvi.66.11.6338-6352.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh H., LeBowitz J. H., Baldwin A. S., Jr, Sharp P. A. Molecular cloning of an enhancer binding protein: isolation by screening of an expression library with a recognition site DNA. Cell. 1988 Feb 12;52(3):415–423. doi: 10.1016/s0092-8674(88)80034-5. [DOI] [PubMed] [Google Scholar]
- Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
- Suckow M., von Wilcken-Bergmann B., Müller-Hill B. Identification of three residues in the basic regions of the bZIP proteins GCN4, C/EBP and TAF-1 that are involved in specific DNA binding. EMBO J. 1993 Mar;12(3):1193–1200. doi: 10.1002/j.1460-2075.1993.tb05760.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swanstrom R., DeLorbe W. J., Bishop J. M., Varmus H. E. Nucleotide sequence of cloned unintegrated avian sarcoma virus DNA: viral DNA contains direct and inverted repeats similar to those in transposable elements. Proc Natl Acad Sci U S A. 1981 Jan;78(1):124–128. doi: 10.1073/pnas.78.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vinson C. R., Hai T., Boyd S. M. Dimerization specificity of the leucine zipper-containing bZIP motif on DNA binding: prediction and rational design. Genes Dev. 1993 Jun;7(6):1047–1058. doi: 10.1101/gad.7.6.1047. [DOI] [PubMed] [Google Scholar]
- Vinson C. R., LaMarco K. L., Johnson P. F., Landschulz W. H., McKnight S. L. In situ detection of sequence-specific DNA binding activity specified by a recombinant bacteriophage. Genes Dev. 1988 Jul;2(7):801–806. doi: 10.1101/gad.2.7.801. [DOI] [PubMed] [Google Scholar]
- Vinson C. R., Sigler P. B., McKnight S. L. Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science. 1989 Nov 17;246(4932):911–916. doi: 10.1126/science.2683088. [DOI] [PubMed] [Google Scholar]
- Vogt M., Lesley J., Bogenberger J., Volkman S., Haas M. Coinfection with viruses carrying the v-Ha-ras and v-myc oncogenes leads to growth factor independence by an indirect mechanism. Mol Cell Biol. 1986 Oct;6(10):3545–3549. doi: 10.1128/mcb.6.10.3545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wurm F. M., Gwinn K. A., Kingston R. E. Inducible overproduction of the mouse c-myc protein in mammalian cells. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5414–5418. doi: 10.1073/pnas.83.15.5414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zachow K. R., Conklin K. F. CArG, CCAAT, and CCAAT-like protein binding sites in avian retrovirus long terminal repeat enhancers. J Virol. 1992 Apr;66(4):1959–1970. doi: 10.1128/jvi.66.4.1959-1970.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]