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. 1989 Nov 25;17(22):9381–9394.

Sequences preceding the minimal promoter of the Xenopus somatic 5S RNA gene increase binding efficiency for transcription factors.

W F Reynolds 1
PMCID: PMC335139  PMID: 2587260

Abstract

Sequences preceding the minimal promoter play a role in the differential expression of the Xenopus somatic and oocyte-type 5S RNA genes. In this report, the somatic sequences between -32 and +37 are shown to increase transcriptional activity in microinjected embryos, yet have little to no effect in microinjected oocyte nuclei. In vitro, these sequences increase activity in whole oocyte S150 extracts, but not in oocyte nuclear extracts. In S150 extracts, these somatic sequences facilitate binding by a commonly required factor(s), other than TFIIIA, which forms a stable complex with the 5S gene. This transcriptional enhancement is also apparent in a reconstituted system using purified TFIIIA and partially purified TFIIIB and TFIIIC.

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Selected References

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  1. Andrews D. L., Millstein L., Hamkalo B. A., Gottesfeld J. M. Competition between Xenopus satellite I sequences and Pol III genes for stable transcription complex formation. Nucleic Acids Res. 1984 Oct 25;12(20):7753–7769. doi: 10.1093/nar/12.20.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birkenmeier E. H., Brown D. D., Jordan E. A nuclear extract of Xenopus laevis oocytes that accurately transcribes 5S RNA genes. Cell. 1978 Nov;15(3):1077–1086. doi: 10.1016/0092-8674(78)90291-x. [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. Bogenhagen D. F., Wormington W. M., Brown D. D. Stable transcription complexes of Xenopus 5S RNA genes: a means to maintain the differentiated state. Cell. 1982 Feb;28(2):413–421. doi: 10.1016/0092-8674(82)90359-2. [DOI] [PubMed] [Google Scholar]
  5. Braun B. R., Riggs D. L., Kassavetis G. A., Geiduschek E. P. Multiple states of protein-DNA interaction in the assembly of transcription complexes on Saccharomyces cerevisiae 5S ribosomal RNA genes. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2530–2534. doi: 10.1073/pnas.86.8.2530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown D. D., Schlissel M. S. A positive transcription factor controls the differential expression of two 5S RNA genes. Cell. 1985 Oct;42(3):759–767. doi: 10.1016/0092-8674(85)90272-7. [DOI] [PubMed] [Google Scholar]
  7. Burke D. J., Söll D. Functional analysis of fractionated Drosophila Kc cell tRNA gene transcription components. J Biol Chem. 1985 Jan 25;260(2):816–823. [PubMed] [Google Scholar]
  8. Carey M. F., Gerrard S. P., Cozzarelli N. R. Analysis of RNA polymerase III transcription complexes by gel filtration. J Biol Chem. 1986 Mar 25;261(9):4309–4317. [PubMed] [Google Scholar]
  9. Ciliberto G., Castagnoli L., Cortese R. Transcription by RNA polymerase III. Curr Top Dev Biol. 1983;18:59–88. doi: 10.1016/s0070-2153(08)60579-7. [DOI] [PubMed] [Google Scholar]
  10. Clarkson S. G., Kurer V., Smith H. O. Sequence organization of a cloned tDNA met fragment from Xenopus laevis. Cell. 1978 Jul;14(3):713–724. doi: 10.1016/0092-8674(78)90253-2. [DOI] [PubMed] [Google Scholar]
  11. Cozzarelli N. R., Gerrard S. P., Schlissel M., Brown D. D., Bogenhagen D. F. Purified RNA polymerase III accurately and efficiently terminates transcription of 5S RNA genes. Cell. 1983 Oct;34(3):829–835. doi: 10.1016/0092-8674(83)90540-8. [DOI] [PubMed] [Google Scholar]
  12. Engelke D. R., Ng S. Y., Shastry B. S., Roeder R. G. Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes. Cell. 1980 Mar;19(3):717–728. doi: 10.1016/s0092-8674(80)80048-1. [DOI] [PubMed] [Google Scholar]
  13. Fedoroff N. V., Brown D. D. The nucleotide sequence of oocyte 5S DNA in Xenopus laevis. I. The AT-rich spacer. Cell. 1978 Apr;13(4):701–716. doi: 10.1016/0092-8674(78)90220-9. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Glikin G. C., Ruberti I., Worcel A. Chromatin assembly in Xenopus oocytes: in vitro studies. Cell. 1984 May;37(1):33–41. doi: 10.1016/0092-8674(84)90298-8. [DOI] [PubMed] [Google Scholar]
  16. Hanas J. S., Bogenhagen D. F., Wu C. W. Cooperative model for the binding of Xenopus transcription factor A to the 5S RNA gene. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2142–2145. doi: 10.1073/pnas.80.8.2142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hipskind R. A., Clarkson S. G. 5'-flanking sequences that inhibit in vitro transcription of a xenopus laevis tRNA gene. Cell. 1983 Oct;34(3):881–890. doi: 10.1016/0092-8674(83)90545-7. [DOI] [PubMed] [Google Scholar]
  18. Huibregtse J. M., Engelke D. R. Genomic footprinting of a yeast tRNA gene reveals stable complexes over the 5'-flanking region. Mol Cell Biol. 1989 Aug;9(8):3244–3252. doi: 10.1128/mcb.9.8.3244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kassavetis G. A., Riggs D. L., Negri R., Nguyen L. H., Geiduschek E. P. Transcription factor IIIB generates extended DNA interactions in RNA polymerase III transcription complexes on tRNA genes. Mol Cell Biol. 1989 Jun;9(6):2551–2566. doi: 10.1128/mcb.9.6.2551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Klekamp M. S., Weil P. A. Properties of yeast class III gene transcription factor TFIIIB. Implications regarding mechanism of action. J Biol Chem. 1987 Jun 5;262(16):7878–7883. [PubMed] [Google Scholar]
  21. Larson D., Bradford-Wilcox J., Young L. S., Sprague K. U. A short 5' flanking region containing conserved sequences is required for silkworm alanine tRNA gene activity. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3416–3420. doi: 10.1073/pnas.80.11.3416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lassar A. B., Martin P. L., Roeder R. G. Transcription of class III genes: formation of preinitiation complexes. Science. 1983 Nov 18;222(4625):740–748. doi: 10.1126/science.6356356. [DOI] [PubMed] [Google Scholar]
  23. Miller K. G., Tower J., Sollner-Webb B. A complex control region of the mouse rRNA gene directs accurate initiation by RNA polymerase I. Mol Cell Biol. 1985 Mar;5(3):554–562. doi: 10.1128/mcb.5.3.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Morton D. G., Sprague K. U. In vitro transcription of a silkworm 5S RNA gene requires an upstream signal. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5519–5522. doi: 10.1073/pnas.81.17.5519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ottonello S., Rivier D. H., Doolittle G. M., Young L. S., Sprague K. U. The properties of a new polymerase III transcription factor reveal that transcription complexes can assemble by more than one pathway. EMBO J. 1987 Jul;6(7):1921–1927. doi: 10.1002/j.1460-2075.1987.tb02452.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Peck L. J., Millstein L., Eversole-Cire P., Gottesfeld J. M., Varshavsky A. Transcriptionally inactive oocyte-type 5S RNA genes of Xenopus laevis are complexed with TFIIIA in vitro. Mol Cell Biol. 1987 Oct;7(10):3503–3510. doi: 10.1128/mcb.7.10.3503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Peterson R. C., Doering J. L., Brown D. D. Characterization of two xenopus somatic 5S DNAs and one minor oocyte-specific 5S DNA. Cell. 1980 May;20(1):131–141. doi: 10.1016/0092-8674(80)90241-x. [DOI] [PubMed] [Google Scholar]
  28. Pieler T., Hamm J., Roeder R. G. The 5S gene internal control region is composed of three distinct sequence elements, organized as two functional domains with variable spacing. Cell. 1987 Jan 16;48(1):91–100. doi: 10.1016/0092-8674(87)90359-x. [DOI] [PubMed] [Google Scholar]
  29. Raymond G. J., Johnson J. D. The role of non-coding DNA sequences in transcription and processing of a yeast tRNA. Nucleic Acids Res. 1983 Sep 10;11(17):5969–5988. doi: 10.1093/nar/11.17.5969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Reynolds W. F., Azer K. Sequence differences upstream of the promoters are involved in the differential expression of the Xenopus somatic and oocyte 5S RNA genes. Nucleic Acids Res. 1988 Apr 25;16(8):3391–3403. doi: 10.1093/nar/16.8.3391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Reynolds W. F. Effect of sequence differences between somatic and oocyte 5S RNA genes on transcriptional efficiency in an oocyte S150 extract. Mol Cell Biol. 1988 Nov;8(11):5056–5058. doi: 10.1128/mcb.8.11.5056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sakonju S., Bogenhagen D. F., Brown D. D. A control region in the center of the 5S RNA gene directs specific initiation of transcription: I. The 5' border of the region. Cell. 1980 Jan;19(1):13–25. doi: 10.1016/0092-8674(80)90384-0. [DOI] [PubMed] [Google Scholar]
  33. Sakonju S., Brown D. D., Engelke D., Ng S. Y., Shastry B. S., Roeder R. G. The binding of a transcription factor to deletion mutants of a 5S ribosomal RNA gene. Cell. 1981 Mar;23(3):665–669. doi: 10.1016/0092-8674(81)90429-3. [DOI] [PubMed] [Google Scholar]
  34. Segall J., Matsui T., Roeder R. G. Multiple factors are required for the accurate transcription of purified genes by RNA polymerase III. J Biol Chem. 1980 Dec 25;255(24):11986–11991. [PubMed] [Google Scholar]
  35. Setzer D. R., Brown D. D. Formation and stability of the 5 S RNA transcription complex. J Biol Chem. 1985 Feb 25;260(4):2483–2492. [PubMed] [Google Scholar]
  36. Shastry B. S., Ng S. Y., Roeder R. G. Multiple factors involved in the transcription of class III genes in Xenopus laevis. J Biol Chem. 1982 Nov 10;257(21):12979–12986. [PubMed] [Google Scholar]
  37. Smith D. R., Jackson I. J., Brown D. D. Domains of the positive transcription factor specific for the Xenopus 5S RNA gene. Cell. 1984 Jun;37(2):645–652. doi: 10.1016/0092-8674(84)90396-9. [DOI] [PubMed] [Google Scholar]
  38. Tower J., Culotta V. C., Sollner-Webb B. Factors and nucleotide sequences that direct ribosomal DNA transcription and their relationship to the stable transcription complex. Mol Cell Biol. 1986 Oct;6(10):3451–3462. doi: 10.1128/mcb.6.10.3451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ullu E., Weiner A. M. Upstream sequences modulate the internal promoter of the human 7SL RNA gene. 1985 Nov 28-Dec 4Nature. 318(6044):371–374. doi: 10.1038/318371a0. [DOI] [PubMed] [Google Scholar]
  40. Wakefield L., Gurdon J. B. Cytoplasmic regulation of 5S RNA genes in nuclear-transplant embryos. EMBO J. 1983;2(9):1613–1619. doi: 10.1002/j.1460-2075.1983.tb01632.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Weil P. A., Segall J., Harris B., Ng S. Y., Roeder R. G. Faithful transcription of eukaryotic genes by RNA polymerase III in systems reconstituted with purified DNA templates. J Biol Chem. 1979 Jul 10;254(13):6163–6173. [PubMed] [Google Scholar]
  42. Wolffe A. P., Brown D. D. Differential 5S RNA gene expression in vitro. Cell. 1987 Dec 4;51(5):733–740. doi: 10.1016/0092-8674(87)90096-1. [DOI] [PubMed] [Google Scholar]
  43. Wolffe A. P., Jordan E., Brown D. D. A bacteriophage RNA polymerase transcribes through a Xenopus 5S RNA gene transcription complex without disrupting it. Cell. 1986 Feb 14;44(3):381–389. doi: 10.1016/0092-8674(86)90459-9. [DOI] [PubMed] [Google Scholar]
  44. Wolffe A. P. Transcription fraction TFIIIC can regulate differential Xenopus 5S RNA gene transcription in vitro. EMBO J. 1988 Apr;7(4):1071–1079. doi: 10.1002/j.1460-2075.1988.tb02915.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wormington W. M., Bogenhagen D. F., Jordan E., Brown D. D. A quantitative assay for Xenopus 5S RNA gene transcription in vitro. Cell. 1981 Jun;24(3):809–817. doi: 10.1016/0092-8674(81)90106-9. [DOI] [PubMed] [Google Scholar]
  46. Wormington W. M., Brown D. D. Onset of 5 S RNA gene regulation during Xenopus embryogenesis. Dev Biol. 1983 Sep;99(1):248–257. doi: 10.1016/0012-1606(83)90273-7. [DOI] [PubMed] [Google Scholar]
  47. Yoshinaga S. K., Boulanger P. A., Berk A. J. Resolution of human transcription factor TFIIIC into two functional components. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3585–3589. doi: 10.1073/pnas.84.11.3585. [DOI] [PMC free article] [PubMed] [Google Scholar]

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