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. 1992 Sep 25;20(18):4733–4739. doi: 10.1093/nar/20.18.4733

The yeast actin intron contains a cryptic promoter that can be switched on by preventing transcriptional interference.

S Irniger 1, C M Egli 1, M Kuenzler 1, G H Braus 1
PMCID: PMC334225  PMID: 1408785

Abstract

We show that the single intron of the actin gene of the yeast Saccharomyces cerevisiae contains a cryptic promoter for transcription of the second exon. This promoter is inactive in the normal actin gene, but can be activated when the actin gene promoter is deleted. An identical activation was induced by placing efficient transcriptional terminators at position 61 of the 309 bp intron. In all cases transcripts with identical 5' ends close to the boundary of the intron and the second exon were produced. These results indicate that the cryptic promoter in the actin intron is occluded in the normal actin gene by transcriptional interference with the actin gene promoter. Transcription initiation near the intron/exon 2 boundary is enabled by protection from traversing polymerases, that initiated transcription at the upstream located actin gene promoter. A partial promoter protection using leaky terminators resulted in small amounts of transcripts initiated from the cryptic promoter. Although we do not know any function of the cryptic promoter in actin gene expression, it is tentative to speculate that the cryptic intron promoter might be a relict of a promoter that was functional earlier in evolution.

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Selected References

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

  1. Adhya S., Gottesman M. Promoter occlusion: transcription through a promoter may inhibit its activity. Cell. 1982 Jul;29(3):939–944. doi: 10.1016/0092-8674(82)90456-1. [DOI] [PubMed] [Google Scholar]
  2. Alani E., Kleckner N. A new type of fusion analysis applicable to many organisms: protein fusions to the URA3 gene of yeast. Genetics. 1987 Sep;117(1):5–12. doi: 10.1093/genetics/117.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnes C. A., Johnston G. C., Singer R. A. Expression of lacZ gene fusions affects downstream transcription in yeast. Gene. 1991 Jul 31;104(1):47–54. doi: 10.1016/0378-1119(91)90463-l. [DOI] [PubMed] [Google Scholar]
  4. Bateman E., Paule M. R. Promoter occlusion during ribosomal RNA transcription. Cell. 1988 Sep 23;54(7):985–992. doi: 10.1016/0092-8674(88)90113-4. [DOI] [PubMed] [Google Scholar]
  5. Braus G., Furter R., Prantl F., Niederberger P., Hütter R. Arrangement of genes TRP1 and TRP3 of Saccharomyces cerevisiae strains. Arch Microbiol. 1985 Sep;142(4):383–388. doi: 10.1007/BF00491908. [DOI] [PubMed] [Google Scholar]
  6. Cavalier-Smith T. Intron phylogeny: a new hypothesis. Trends Genet. 1991 May;7(5):145–148. [PubMed] [Google Scholar]
  7. Cullen B. R., Lomedico P. T., Ju G. Transcriptional interference in avian retroviruses--implications for the promoter insertion model of leukaemogenesis. Nature. 1984 Jan 19;307(5948):241–245. doi: 10.1038/307241a0. [DOI] [PubMed] [Google Scholar]
  8. Darnell J. E., Doolittle W. F. Speculations on the early course of evolution. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1271–1275. doi: 10.1073/pnas.83.5.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dibb N. J., Newman A. J. Evidence that introns arose at proto-splice sites. EMBO J. 1989 Jul;8(7):2015–2021. doi: 10.1002/j.1460-2075.1989.tb03609.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Elder R. T., Loh E. Y., Davis R. W. RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci U S A. 1983 May;80(9):2432–2436. doi: 10.1073/pnas.80.9.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  12. Furter R., Paravicini G., Aebi M., Braus G., Prantl F., Niederberger P., Hütter R. The TRP4 gene of Saccharomyces cerevisiae: isolation and structural analysis. Nucleic Acids Res. 1986 Aug 26;14(16):6357–6373. doi: 10.1093/nar/14.16.6357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gallwitz D., Seidel R. Molecular cloning of the actin gene from yeast Saccharomyces cerevisiae. Nucleic Acids Res. 1980 Mar 11;8(5):1043–1059. doi: 10.1093/nar/8.5.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gilbert W. The exon theory of genes. Cold Spring Harb Symp Quant Biol. 1987;52:901–905. doi: 10.1101/sqb.1987.052.01.098. [DOI] [PubMed] [Google Scholar]
  15. Grummt I., Kuhn A., Bartsch I., Rosenbauer H. A transcription terminator located upstream of the mouse rDNA initiation site affects rRNA synthesis. Cell. 1986 Dec 26;47(6):901–911. doi: 10.1016/0092-8674(86)90805-6. [DOI] [PubMed] [Google Scholar]
  16. Henderson S. L., Ryan K., Sollner-Webb B. The promoter-proximal rDNA terminator augments initiation by preventing disruption of the stable transcription complex caused by polymerase read-in. Genes Dev. 1989 Feb;3(2):212–223. doi: 10.1101/gad.3.2.212. [DOI] [PubMed] [Google Scholar]
  17. Henderson S., Sollner-Webb B. A transcriptional terminator is a novel element of the promoter of the mouse ribosomal RNA gene. Cell. 1986 Dec 26;47(6):891–900. doi: 10.1016/0092-8674(86)90804-4. [DOI] [PubMed] [Google Scholar]
  18. Irniger S., Egli C. M., Braus G. H. Different classes of polyadenylation sites in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jun;11(6):3060–3069. doi: 10.1128/mcb.11.6.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kassavetis G. A., Geiduschek E. P. Bacteriophage T4 late promoters: mapping 5' ends of T4 gene 23 mRNAs. EMBO J. 1982;1(1):107–114. doi: 10.1002/j.1460-2075.1982.tb01132.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McStay B., Reeder R. H. A termination site for Xenopus RNA polymerase I also acts as an element of an adjacent promoter. Cell. 1986 Dec 26;47(6):913–920. doi: 10.1016/0092-8674(86)90806-8. [DOI] [PubMed] [Google Scholar]
  22. Minton N. P. Improved plasmid vectors for the isolation of translational lac gene fusions. Gene. 1984 Nov;31(1-3):269–273. doi: 10.1016/0378-1119(84)90220-8. [DOI] [PubMed] [Google Scholar]
  23. Miozzari G., Niederberger P., Hütter R. Tryptophan biosynthesis in Saccharomyces cerevisiae: control of the flux through the pathway. J Bacteriol. 1978 Apr;134(1):48–59. doi: 10.1128/jb.134.1.48-59.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Naito Y., Riggs C. K., Vandergon T. L., Riggs A. F. Origin of a "bridge" intron in the gene for a two-domain globin. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6672–6676. doi: 10.1073/pnas.88.15.6672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ng R., Abelson J. Isolation and sequence of the gene for actin in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3912–3916. doi: 10.1073/pnas.77.7.3912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Osborne B. I., Guarente L. Transcription by RNA polymerase II induces changes of DNA topology in yeast. Genes Dev. 1988 Jun;2(6):766–772. doi: 10.1101/gad.2.6.766. [DOI] [PubMed] [Google Scholar]
  27. Proudfoot N. J. Transcriptional interference and termination between duplicated alpha-globin gene constructs suggests a novel mechanism for gene regulation. Nature. 1986 Aug 7;322(6079):562–565. doi: 10.1038/322562a0. [DOI] [PubMed] [Google Scholar]
  28. Roeder R. G. The complexities of eukaryotic transcription initiation: regulation of preinitiation complex assembly. Trends Biochem Sci. 1991 Nov;16(11):402–408. doi: 10.1016/0968-0004(91)90164-q. [DOI] [PubMed] [Google Scholar]
  29. Rogers J. H. How were introns inserted into nuclear genes? Trends Genet. 1989 Jul;5(7):213–216. doi: 10.1016/0168-9525(89)90084-x. [DOI] [PubMed] [Google Scholar]
  30. Russo P., Sherman F. Transcription terminates near the poly(A) site in the CYC1 gene of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8348–8352. doi: 10.1073/pnas.86.21.8348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  32. Thompson-Jäger S., Domdey H. The intron of the yeast actin gene contains the promoter for an antisense RNA. Curr Genet. 1990 Mar;17(3):269–273. doi: 10.1007/BF00312620. [DOI] [PubMed] [Google Scholar]
  33. Wessler S. R. The splicing of maize transposable elements from pre-mRNA--a minireview. Gene. 1989 Oct 15;82(1):127–133. doi: 10.1016/0378-1119(89)90037-1. [DOI] [PubMed] [Google Scholar]

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