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. 1997 Sep 15;25(18):3705–3711. doi: 10.1093/nar/25.18.3705

A functional YY1 binding site is necessary and sufficient to activate Surf-1 promoter activity in response to serum growth factors.

E G Cole 1, K Gaston 1
PMCID: PMC146936  PMID: 9278494

Abstract

The human Surf-1 and Surf-2 housekeeping genes are divergently transcribed and share a bi-directional, TATA-less promoter. Housekeeping promoters typically contain complex arrays of transcription factor binding sites and several studies have suggested that many of these sites might be functionally redundant. The Surf-1/Surf-2 promoter region contains four factor binding sites; members of the ETS family of transcription factors bind to two of these sites whilst YY1 binds to a third site immediately downstream of the major Surf-1 transcription start point. Here we show that Sp1 binds to the fourth transcription factor binding site. Although YY1 and Sp1 have previously been shown to interact both in vitro and in vivo, these proteins function independently at the Surf-1/Surf-2 promoter. The binding of Sp1 alone is sufficient to bring about full promoter activity in the Surf-2 direction. In contrast, both Sp1 and ETS proteins are required to bring about full promoter activity in the Surf-1 direction. The YY1 binding site is not required for basal transcription in either direction. The YY1 binding site is, however, both necessary and sufficient to confer growth factor inducibility on transcription in the Surf-1 direction. Our data suggest that functionally redundant transcription factor binding sites might not be a general feature of housekeeping promoters.

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Selected References

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  1. Antequera F., Macleod D., Bird A. P. Specific protection of methylated CpGs in mammalian nuclei. Cell. 1989 Aug 11;58(3):509–517. doi: 10.1016/0092-8674(89)90431-5. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Boyes J., Felsenfeld G. Tissue-specific factors additively increase the probability of the all-or-none formation of a hypersensitive site. EMBO J. 1996 May 15;15(10):2496–2507. [PMC free article] [PubMed] [Google Scholar]
  4. Cedar H. DNA methylation and gene activity. Cell. 1988 Apr 8;53(1):3–4. doi: 10.1016/0092-8674(88)90479-5. [DOI] [PubMed] [Google Scholar]
  5. Chung S., Perry R. P. The importance of downstream delta-factor binding elements for the activity of the rpL32 promoter. Nucleic Acids Res. 1993 Jul 11;21(14):3301–3308. doi: 10.1093/nar/21.14.3301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Colombo P., Yon J., Garson K., Fried M. Conservation of the organization of five tightly clustered genes over 600 million years of divergent evolution. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6358–6362. doi: 10.1073/pnas.89.14.6358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gaston K., Fried M. CpG methylation has differential effects on the binding of YY1 and ETS proteins to the bi-directional promoter of the Surf-1 and Surf-2 genes. Nucleic Acids Res. 1995 Mar 25;23(6):901–909. doi: 10.1093/nar/23.6.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gaston K., Fried M. YY1 is involved in the regulation of the bi-directional promoter of the Surf-1 and Surf-2 genes. FEBS Lett. 1994 Jun 27;347(2-3):289–294. doi: 10.1016/0014-5793(94)00567-2. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Hastie N. D., Bishop J. O. The expression of three abundance classes of messenger RNA in mouse tissues. Cell. 1976 Dec;9(4 Pt 2):761–774. doi: 10.1016/0092-8674(76)90139-2. [DOI] [PubMed] [Google Scholar]
  12. Huxley C., Fried M. The mouse surfeit locus contains a cluster of six genes associated with four CpG-rich islands in 32 kilobases of genomic DNA. Mol Cell Biol. 1990 Feb;10(2):605–614. doi: 10.1128/mcb.10.2.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kelly K., Cochran B. H., Stiles C. D., Leder P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell. 1983 Dec;35(3 Pt 2):603–610. doi: 10.1016/0092-8674(83)90092-2. [DOI] [PubMed] [Google Scholar]
  14. Lee J. S., Galvin K. M., Shi Y. Evidence for physical interaction between the zinc-finger transcription factors YY1 and Sp1. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6145–6149. doi: 10.1073/pnas.90.13.6145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Lennard A., Gaston K., Fried M. The Surf-1 and Surf-2 genes and their essential bidirectional promoter elements are conserved between mouse and human. DNA Cell Biol. 1994 Nov;13(11):1117–1126. doi: 10.1089/dna.1994.13.1117. [DOI] [PubMed] [Google Scholar]
  17. Lewis B. A., Tullis G., Seto E., Horikoshi N., Weinmann R., Shenk T. Adenovirus E1A proteins interact with the cellular YY1 transcription factor. J Virol. 1995 Mar;69(3):1628–1636. doi: 10.1128/jvi.69.3.1628-1636.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Marcu K. B., Bossone S. A., Patel A. J. myc function and regulation. Annu Rev Biochem. 1992;61:809–860. doi: 10.1146/annurev.bi.61.070192.004113. [DOI] [PubMed] [Google Scholar]
  19. Means A. L., Farnham P. J. Transcription initiation from the dihydrofolate reductase promoter is positioned by HIP1 binding at the initiation site. Mol Cell Biol. 1990 Feb;10(2):653–661. doi: 10.1128/mcb.10.2.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Melton D. W., McEwan C., McKie A. B., Reid A. M. Expression of the mouse HPRT gene: deletional analysis of the promoter region of an X-chromosome linked housekeeping gene. Cell. 1986 Jan 31;44(2):319–328. doi: 10.1016/0092-8674(86)90766-x. [DOI] [PubMed] [Google Scholar]
  21. Natesan S., Gilman M. Z. DNA bending and orientation-dependent function of YY1 in the c-fos promoter. Genes Dev. 1993 Dec;7(12B):2497–2509. doi: 10.1101/gad.7.12b.2497. [DOI] [PubMed] [Google Scholar]
  22. Natesan S., Gilman M. YY1 facilitates the association of serum response factor with the c-fos serum response element. Mol Cell Biol. 1995 Nov;15(11):5975–5982. doi: 10.1128/mcb.15.11.5975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Osborne T. F., Gil G., Brown M. S., Kowal R. C., Goldstein J. L. Identification of promoter elements required for in vitro transcription of hamster 3-hydroxy-3-methylglutaryl coenzyme A reductase gene. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3614–3618. doi: 10.1073/pnas.84.11.3614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pugh B. F., Tjian R. Diverse transcriptional functions of the multisubunit eukaryotic TFIID complex. J Biol Chem. 1992 Jan 15;267(2):679–682. [PubMed] [Google Scholar]
  25. Seto E., Lewis B., Shenk T. Interaction between transcription factors Sp1 and YY1. Nature. 1993 Sep 30;365(6445):462–464. doi: 10.1038/365462a0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Shrivastava A., Calame K. An analysis of genes regulated by the multi-functional transcriptional regulator Yin Yang-1. Nucleic Acids Res. 1994 Dec 11;22(24):5151–5155. doi: 10.1093/nar/22.24.5151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shrivastava A., Saleque S., Kalpana G. V., Artandi S., Goff S. P., Calame K. Inhibition of transcriptional regulator Yin-Yang-1 by association with c-Myc. Science. 1993 Dec 17;262(5141):1889–1892. doi: 10.1126/science.8266081. [DOI] [PubMed] [Google Scholar]
  29. Somma M. P., Pisano C., Lavia P. The housekeeping promoter from the mouse CpG island HTF9 contains multiple protein-binding elements that are functionally redundant. Nucleic Acids Res. 1991 Jun 11;19(11):2817–2824. doi: 10.1093/nar/19.11.2817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Williams T. J., Fried M. The MES-1 murine enhancer element is closely associated with the heterogeneous 5' ends of two divergent transcription units. Mol Cell Biol. 1986 Dec;6(12):4558–4569. doi: 10.1128/mcb.6.12.4558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Williams T., Yon J., Huxley C., Fried M. The mouse surfeit locus contains a very tight cluster of four "housekeeping" genes that is conserved through evolution. Proc Natl Acad Sci U S A. 1988 May;85(10):3527–3530. doi: 10.1073/pnas.85.10.3527. [DOI] [PMC free article] [PubMed] [Google Scholar]

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