Abstract
A salient feature of mammalian ribosomal protein genes is the location of promoter elements downstream, as well as upstream, of the transcriptional start point. Previous functional studies of the mouse rpL32 gene (Chung and Perry, Mol. Cell. Biol. 9, 2075; 1989) indicated that the first intron of this gene contains such an element. We show here that this element encompasses a binding site for a zinc finger nuclear protein known as delta (YY-1, muE1, UCRBP). The intronic delta site (delta i) is located 32 bp downstream of another delta site in the first exon (delta e). Transfection experiments with genes containing deleterious mutations in one or both delta sites or having alterations in the spacing between the sites indicate that the two delta elements function independently and contribute additively to the overall strength of the rpL32 promoter. Moreover, the contribution of the delta i element is the same whether it is oriented parallel or antiparallel to the delta e element. Together, the two delta elements raise the expression level about 10-fold over that attained by the upstream and initiator portions of the promoter. The positive role of the delta factor in rpL32 expression contrasts strikingly with its repressive role in various other genes.
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- Atchison M. L., Meyuhas O., Perry R. P. Localization of transcriptional regulatory elements and nuclear factor binding sites in mouse ribosomal protein gene rpL32. Mol Cell Biol. 1989 May;9(5):2067–2074. doi: 10.1128/mcb.9.5.2067. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chan Y. L., Wool I. G. The structure of a gene containing introns and encoding rat ribosomal protein P2. Nucleic Acids Res. 1991 Sep 25;19(18):4895–4900. doi: 10.1093/nar/19.18.4895. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen I. T., Roufa D. J. The transcriptionally active human ribosomal protein S17 gene. Gene. 1988 Oct 15;70(1):107–116. doi: 10.1016/0378-1119(88)90109-6. [DOI] [PubMed] [Google Scholar]
- Chung S., Perry R. P. Cell-free transcription of a mouse ribosomal-protein-encoding gene: the effects of promoter mutations. Gene. 1991 Apr;100:173–180. doi: 10.1016/0378-1119(91)90363-g. [DOI] [PubMed] [Google Scholar]
- Chung S., Perry R. P. Importance of introns for expression of mouse ribosomal protein gene rpL32. Mol Cell Biol. 1989 May;9(5):2075–2082. doi: 10.1128/mcb.9.5.2075. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dudov K. P., Perry R. P. The gene family encoding the mouse ribosomal protein L32 contains a uniquely expressed intron-containing gene and an unmutated processed gene. Cell. 1984 Jun;37(2):457–468. doi: 10.1016/0092-8674(84)90376-3. [DOI] [PubMed] [Google Scholar]
- Farnham P. J., Means A. L. Sequences downstream of the transcription initiation site modulate the activity of the murine dihydrofolate reductase promoter. Mol Cell Biol. 1990 Apr;10(4):1390–1398. doi: 10.1128/mcb.10.4.1390. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flanagan J. R., Becker K. G., Ennist D. L., Gleason S. L., Driggers P. H., Levi B. Z., Appella E., Ozato K. Cloning of a negative transcription factor that binds to the upstream conserved region of Moloney murine leukemia virus. Mol Cell Biol. 1992 Jan;12(1):38–44. doi: 10.1128/mcb.12.1.38. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gualberto A., LePage D., Pons G., Mader S. L., Park K., Atchison M. L., Walsh K. Functional antagonism between YY1 and the serum response factor. Mol Cell Biol. 1992 Sep;12(9):4209–4214. doi: 10.1128/mcb.12.9.4209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hariharan N., Kelley D. E., Perry R. P. Delta, a transcription factor that binds to downstream elements in several polymerase II promoters, is a functionally versatile zinc finger protein. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9799–9803. doi: 10.1073/pnas.88.21.9799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hariharan N., Kelley D. E., Perry R. P. Equipotent mouse ribosomal protein promoters have a similar architecture that includes internal sequence elements. Genes Dev. 1989 Nov;3(11):1789–1800. doi: 10.1101/gad.3.11.1789. [DOI] [PubMed] [Google Scholar]
- Hariharan N., Perry R. P. A characterization of the elements comprising the promoter of the mouse ribosomal protein gene RPS16. Nucleic Acids Res. 1989 Jul 11;17(13):5323–5337. doi: 10.1093/nar/17.13.5323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huxley C., Fried M. The mouse rpL7a gene is typical of other ribosomal protein genes in it's 5' region but differs in being located in a tight cluster of CpG-rich islands. Nucleic Acids Res. 1990 Sep 25;18(18):5353–5357. doi: 10.1093/nar/18.18.5353. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee T. C., Shi Y., Schwartz R. J. Displacement of BrdUrd-induced YY1 by serum response factor activates skeletal alpha-actin transcription in embryonic myoblasts. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9814–9818. doi: 10.1073/pnas.89.20.9814. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lennard A. C., Fried M. The bidirectional promoter of the divergently transcribed mouse Surf-1 and Surf-2 genes. Mol Cell Biol. 1991 Mar;11(3):1281–1294. doi: 10.1128/mcb.11.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyuhas O., Klein A. The mouse ribosomal protein L7 gene. Its primary structure and functional analysis of the promoter region. J Biol Chem. 1990 Jul 15;265(20):11465–11473. [PubMed] [Google Scholar]
- Montalvo E. A., Shi Y., Shenk T. E., Levine A. J. Negative regulation of the BZLF1 promoter of Epstein-Barr virus. J Virol. 1991 Jul;65(7):3647–3655. doi: 10.1128/jvi.65.7.3647-3655.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moura-Neto R., Dudov K. P., Perry R. P. An element downstream of the cap site is required for transcription of the gene encoding mouse ribosomal protein L32. Proc Natl Acad Sci U S A. 1989 Jun;86(11):3997–4001. doi: 10.1073/pnas.86.11.3997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Park K., Atchison M. L. Isolation of a candidate repressor/activator, NF-E1 (YY-1, delta), that binds to the immunoglobulin kappa 3' enhancer and the immunoglobulin heavy-chain mu E1 site. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9804–9808. doi: 10.1073/pnas.88.21.9804. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riggs K. J., Merrell K. T., Wilson G., Calame K. Common factor 1 is a transcriptional activator which binds in the c-myc promoter, the skeletal alpha-actin promoter, and the immunoglobulin heavy-chain enhancer. Mol Cell Biol. 1991 Mar;11(3):1765–1769. doi: 10.1128/mcb.11.3.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seto E., Shi Y., Shenk T. YY1 is an initiator sequence-binding protein that directs and activates transcription in vitro. Nature. 1991 Nov 21;354(6350):241–245. doi: 10.1038/354241a0. [DOI] [PubMed] [Google Scholar]
- Shi Y., Seto E., Chang L. S., Shenk T. Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein. Cell. 1991 Oct 18;67(2):377–388. doi: 10.1016/0092-8674(91)90189-6. [DOI] [PubMed] [Google Scholar]
- Siebenlist U., Gilbert W. Contacts between Escherichia coli RNA polymerase and an early promoter of phage T7. Proc Natl Acad Sci U S A. 1980 Jan;77(1):122–126. doi: 10.1073/pnas.77.1.122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh H., Sen R., Baltimore D., Sharp P. A. A nuclear factor that binds to a conserved sequence motif in transcriptional control elements of immunoglobulin genes. Nature. 1986 Jan 9;319(6049):154–158. doi: 10.1038/319154a0. [DOI] [PubMed] [Google Scholar]
- Swergold G. D. Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol. 1990 Dec;10(12):6718–6729. doi: 10.1128/mcb.10.12.6718. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wiedemann L. M., D'Eustachio P., Kelley D. E., Perry R. P. Three functional ribosomal protein genes are unlinked in mouse genome. Somat Cell Mol Genet. 1987 Jan;13(1):77–80. doi: 10.1007/BF02422301. [DOI] [PubMed] [Google Scholar]