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. 1991 Feb 11;19(3):435–441. doi: 10.1093/nar/19.3.435

The different positioning of the proximal sequence element in the Xenopus RNA polymerase II and III snRNA promoters is a key determinant which confers RNA polymerase III specificity.

A Lescure 1, P Carbon 1, A Krol 1
PMCID: PMC333630  PMID: 2011518

Abstract

We and others have previously described the TATA motif as a major determinant for Pol III specificity of the U6 promoter. Surprisingly, however, the data documented here show that the sole introduction of a TATA sequence into a U1 Pol II snRNA gene is not sufficient to confer Pol III transcription. Rather, this promoter element can mediate optimal Pol III transcription only if the PSE, the second promoter element, is shifted 4 bp upstream of the position it occupies in Pol II snRNA genes. As a result, the PSE-TATA-start site spacing introduced into the U1 Pol II gene is identical to that of the U6 gene and is strictly required to produce properly initiated Pol III transcripts. Thus, Pol II and Pol III PSEs, although similar in sequence, are not positionally equivalent. Competitive experiments raise the possibility that vertebrate U6 genes contain other, as yet unidentified, promoter elements.

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Selected References

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

  1. Bark C., Weller P., Zabielski J., Janson L., Pettersson U. A distant enhancer element is required for polymerase III transcription of a U6 RNA gene. Nature. 1987 Jul 23;328(6128):356–359. doi: 10.1038/328356a0. [DOI] [PubMed] [Google Scholar]
  2. Bogenhagen D. F., Brown D. D. Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell. 1981 Apr;24(1):261–270. doi: 10.1016/0092-8674(81)90522-5. [DOI] [PubMed] [Google Scholar]
  3. Bogenhagen D. F., Sakonju S., Brown D. D. A control region in the center of the 5S RNA gene directs specific initiation of transcription: II. The 3' border of the region. Cell. 1980 Jan;19(1):27–35. doi: 10.1016/0092-8674(80)90385-2. [DOI] [PubMed] [Google Scholar]
  4. Brow D. A., Guthrie C. Transcription of a yeast U6 snRNA gene requires a polymerase III promoter element in a novel position. Genes Dev. 1990 Aug;4(8):1345–1356. doi: 10.1101/gad.4.8.1345. [DOI] [PubMed] [Google Scholar]
  5. Carbon P., Murgo S., Ebel J. P., Krol A., Tebb G., Mattaj L. W. A common octamer motif binding protein is involved in the transcription of U6 snRNA by RNA polymerase III and U2 snRNA by RNA polymerase II. Cell. 1987 Oct 9;51(1):71–79. doi: 10.1016/0092-8674(87)90011-0. [DOI] [PubMed] [Google Scholar]
  6. Ciliberto G., Dathan N., Frank R., Philipson L., Mattaj I. W. Formation of the 3' end on U snRNAs requires at least three sequence elements. EMBO J. 1986 Nov;5(11):2931–2937. doi: 10.1002/j.1460-2075.1986.tb04589.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Das G., Henning D., Wright D., Reddy R. Upstream regulatory elements are necessary and sufficient for transcription of a U6 RNA gene by RNA polymerase III. EMBO J. 1988 Feb;7(2):503–512. doi: 10.1002/j.1460-2075.1988.tb02838.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Earley J. M., 3rd, Roebuck K. A., Stumph W. E. Three linked chicken U1 RNA genes have limited flanking DNA sequence homologies that reveal potential regulatory signals. Nucleic Acids Res. 1984 Oct 11;12(19):7411–7421. doi: 10.1093/nar/12.19.7411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Galli G., Hofstetter H., Birnstiel M. L. Two conserved sequence blocks within eukaryotic tRNA genes are major promoter elements. Nature. 1981 Dec 17;294(5842):626–631. doi: 10.1038/294626a0. [DOI] [PubMed] [Google Scholar]
  10. Geiduschek E. P., Tocchini-Valentini G. P. Transcription by RNA polymerase III. Annu Rev Biochem. 1988;57:873–914. doi: 10.1146/annurev.bi.57.070188.004301. [DOI] [PubMed] [Google Scholar]
  11. Hernandez N., Lucito R. Elements required for transcription initiation of the human U2 snRNA gene coincide with elements required for snRNA 3' end formation. EMBO J. 1988 Oct;7(10):3125–3134. doi: 10.1002/j.1460-2075.1988.tb03179.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kassavetis G. A., Braun B. R., Nguyen L. H., Geiduschek E. P. S. cerevisiae TFIIIB is the transcription initiation factor proper of RNA polymerase III, while TFIIIA and TFIIIC are assembly factors. Cell. 1990 Jan 26;60(2):235–245. doi: 10.1016/0092-8674(90)90739-2. [DOI] [PubMed] [Google Scholar]
  13. Krol A., Carbon P., Ebel J. P., Appel B. Xenopus tropicalis U6 snRNA genes transcribed by Pol III contain the upstream promoter elements used by Pol II dependent U snRNA genes. Nucleic Acids Res. 1987 Mar 25;15(6):2463–2478. doi: 10.1093/nar/15.6.2463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Krol A., Lund E., Dahlberg J. E. The two embryonic U1 RNA genes of Xenopus laevis have both common and gene-specific transcription signals. EMBO J. 1985 Jun;4(6):1529–1535. doi: 10.1002/j.1460-2075.1985.tb03813.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kunkel G. R., Pederson T. Upstream elements required for efficient transcription of a human U6 RNA gene resemble those of U1 and U2 genes even though a different polymerase is used. Genes Dev. 1988 Feb;2(2):196–204. doi: 10.1101/gad.2.2.196. [DOI] [PubMed] [Google Scholar]
  16. Lewin B. Commitment and activation at pol II promoters: a tail of protein-protein interactions. Cell. 1990 Jun 29;61(7):1161–1164. doi: 10.1016/0092-8674(90)90675-5. [DOI] [PubMed] [Google Scholar]
  17. Lobo S. M., Hernandez N. A 7 bp mutation converts a human RNA polymerase II snRNA promoter into an RNA polymerase III promoter. Cell. 1989 Jul 14;58(1):55–67. doi: 10.1016/0092-8674(89)90402-9. [DOI] [PubMed] [Google Scholar]
  18. Lobo S. M., Ifill S., Hernandez N. cis-acting elements required for RNA polymerase II and III transcription in the human U2 and U6 snRNA promoters. Nucleic Acids Res. 1990 May 25;18(10):2891–2899. doi: 10.1093/nar/18.10.2891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lund E., Bostock C. J., Dahlberg J. E. The transcription of Xenopus laevis embryonic U1 snRNA genes changes when oocytes mature into eggs. Genes Dev. 1987 Mar;1(1):47–56. doi: 10.1101/gad.1.1.47. [DOI] [PubMed] [Google Scholar]
  20. Mattaj I. W., Dathan N. A., Parry H. D., Carbon P., Krol A. Changing the RNA polymerase specificity of U snRNA gene promoters. Cell. 1988 Nov 4;55(3):435–442. doi: 10.1016/0092-8674(88)90029-3. [DOI] [PubMed] [Google Scholar]
  21. McNamara K. J., Stumph W. E. Site-directed mutational analysis of a U4 small nuclear RNA gene proximal sequence element. Localization and identification of functional nucleotides. J Biol Chem. 1990 Jun 15;265(17):9728–9731. [PubMed] [Google Scholar]
  22. Murphy J. T., Skuzeski J. T., Lund E., Steinberg T. H., Burgess R. R., Dahlberg J. E. Functional elements of the human U1 RNA promoter. Identification of five separate regions required for efficient transcription and template competition. J Biol Chem. 1987 Feb 5;262(4):1795–1803. [PubMed] [Google Scholar]
  23. Murphy S., Di Liegro C., Melli M. The in vitro transcription of the 7SK RNA gene by RNA polymerase III is dependent only on the presence of an upstream promoter. Cell. 1987 Oct 9;51(1):81–87. doi: 10.1016/0092-8674(87)90012-2. [DOI] [PubMed] [Google Scholar]
  24. Murphy S., Moorefield B., Pieler T. Common mechanisms of promoter recognition by RNA polymerases II and III. Trends Genet. 1989 Apr;5(4):122–126. doi: 10.1016/0168-9525(89)90043-7. [DOI] [PubMed] [Google Scholar]
  25. Murphy S., Pierani A., Scheidereit C., Melli M., Roeder R. G. Purified octamer binding transcription factors stimulate RNA polymerase III--mediated transcription of the 7SK RNA gene. Cell. 1989 Dec 22;59(6):1071–1080. doi: 10.1016/0092-8674(89)90763-0. [DOI] [PubMed] [Google Scholar]
  26. Parry H. D., Mattaj I. W. Positive and negative functional interactions between promoter elements from different classes of RNA polymerase III-transcribed genes. EMBO J. 1990 Apr;9(4):1097–1104. doi: 10.1002/j.1460-2075.1990.tb08215.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Parry H. D., Tebb G., Mattaj I. W. The Xenopus U2 gene PSE is a single, compact, element required for transcription initiation and 3' end formation. Nucleic Acids Res. 1989 May 25;17(10):3633–3644. doi: 10.1093/nar/17.10.3633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sharp S. J., Schaack J., Cooley L., Burke D. J., Söll D. Structure and transcription of eukaryotic tRNA genes. CRC Crit Rev Biochem. 1985;19(2):107–144. doi: 10.3109/10409238509082541. [DOI] [PubMed] [Google Scholar]
  29. Simmen K. A., Mattaj I. W. Complex requirements for RNA polymerase III transcription of the Xenopus U6 promoter. Nucleic Acids Res. 1990 Oct 11;18(19):5649–5657. doi: 10.1093/nar/18.19.5649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sollner-Webb B. Surprises in polymerase III transcription. Cell. 1988 Jan 29;52(2):153–154. doi: 10.1016/0092-8674(88)90500-4. [DOI] [PubMed] [Google Scholar]
  31. Tanaka M., Grossniklaus U., Herr W., Hernandez N. Activation of the U2 snRNA promoter by the octamer motif defines a new class of RNA polymerase II enhancer elements. Genes Dev. 1988 Dec;2(12B):1764–1778. doi: 10.1101/gad.2.12b.1764. [DOI] [PubMed] [Google Scholar]
  32. Waibel F., Filipowicz W. RNA-polymerase specificity of transcription of Arabidopsis U snRNA genes determined by promoter element spacing. Nature. 1990 Jul 12;346(6280):199–202. doi: 10.1038/346199a0. [DOI] [PubMed] [Google Scholar]

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