Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1987 Oct;7(10):3503–3510. doi: 10.1128/mcb.7.10.3503

Transcriptionally inactive oocyte-type 5S RNA genes of Xenopus laevis are complexed with TFIIIA in vitro.

L J Peck 1, L Millstein 1, P Eversole-Cire 1, J M Gottesfeld 1, A Varshavsky 1
PMCID: PMC368002  PMID: 3683391

Abstract

An extract from whole oocytes of Xenopus laevis was shown to transcribe somatic-type 5S RNA genes approximately 100-fold more efficiently than oocyte-type 5S RNA genes. This preference was at least 10-fold greater than the preference seen upon microinjection of 5S RNA genes into oocyte nuclei or upon in vitro transcription in an oocyte nuclear extract. The approximately 100-fold transcriptional bias in favor of the somatic-type 5S RNA genes observed in vitro in the whole oocyte extract was similar to the transcriptional bias observed in developing Xenopus embryos. We also showed that in the whole oocyte extract, a promoter-binding protein required for 5S RNA gene transcription, TFIIIA, was bound both to the actively transcribed somatic-type 5S RNA gene and to the largely inactive oocyte-type 5S RNA genes. These findings suggest that the mechanism for the differential expression of 5S RNA genes during Xenopus development does not involve differential binding of TFIIIA to 5S RNA genes.

Full text

PDF
3503

Images in this article

3506Image
on p.3506
3506Image
on p.3506
3508Image
on p.3508

Selected References

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

  1. Bieker J. J., Roeder R. G. Physical properties and DNA-binding stoichiometry of a 5 S gene-specific transcription factor. J Biol Chem. 1984 May 25;259(10):6158–6164. [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., 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]
  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. Brown D. D. How a simple animal gene works. Harvey Lect. 1980;76:27–44. [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. Brown D. D. The role of stable complexes that repress and activate eucaryotic genes. Cell. 1984 Jun;37(2):359–365. doi: 10.1016/0092-8674(84)90366-0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Gargiulo G., Razvi F., Worcel A. Assembly of transcriptionally active chromatin in Xenopus oocytes requires specific DNA binding factors. Cell. 1984 Sep;38(2):511–521. doi: 10.1016/0092-8674(84)90506-3. [DOI] [PubMed] [Google Scholar]
  10. Gilbert D. M. Temporal order of replication of Xenopus laevis 5S ribosomal RNA genes in somatic cells. Proc Natl Acad Sci U S A. 1986 May;83(9):2924–2928. doi: 10.1073/pnas.83.9.2924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ginsberg A. M., King B. O., Roeder R. G. Xenopus 5S gene transcription factor, TFIIIA: characterization of a cDNA clone and measurement of RNA levels throughout development. Cell. 1984 Dec;39(3 Pt 2):479–489. doi: 10.1016/0092-8674(84)90455-0. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Gottesfeld J., Bloomer L. S. Assembly of transcriptionally active 5S RNA gene chromatin in vitro. Cell. 1982 Apr;28(4):781–791. doi: 10.1016/0092-8674(82)90057-5. [DOI] [PubMed] [Google Scholar]
  14. Guinta D. R., Korn L. J. Differential order of replication of Xenopus laevis 5S RNA genes. Mol Cell Biol. 1986 Jul;6(7):2536–2542. doi: 10.1128/mcb.6.7.2536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kmiec E. B., Razvi F., Worcel A. The role of DNA-mediated transfer of TFIIIA in the concerted gyration and differential activation of the Xenopus 5S RNA genes. Cell. 1986 Apr 25;45(2):209–218. doi: 10.1016/0092-8674(86)90385-5. [DOI] [PubMed] [Google Scholar]
  16. Korn L. J., Gurdon J. B. The reactivation of developmentally inert 5S genes in somatic nuclei injected into Xenopus oocytes. Nature. 1981 Feb 5;289(5797):461–465. doi: 10.1038/289461a0. [DOI] [PubMed] [Google Scholar]
  17. Korn L. J. Transcription of Xenopus 5S ribosomal RNA genes. Nature. 1982 Jan 14;295(5845):101–105. doi: 10.1038/295101a0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  20. Miller J. R., Cartwright E. M., Brownlee G. G., Fedoroff N. V., Brown D. D. The nucleotide sequence of oocyte 5S DNA in Xenopus laevis. II. The GC-rich region. Cell. 1978 Apr;13(4):717–725. doi: 10.1016/0092-8674(78)90221-0. [DOI] [PubMed] [Google Scholar]
  21. Miller J. R., Melton D. A. A transcriptionally active pseudogene in xenopus laevis oocyte 5S DNA. Cell. 1981 Jun;24(3):829–835. doi: 10.1016/0092-8674(81)90108-2. [DOI] [PubMed] [Google Scholar]
  22. Miller J., McLachlan A. D., Klug A. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 1985 Jun;4(6):1609–1614. doi: 10.1002/j.1460-2075.1985.tb03825.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pelham H. R., Brown D. D. A specific transcription factor that can bind either the 5S RNA gene or 5S RNA. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4170–4174. doi: 10.1073/pnas.77.7.4170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sakonju S., Brown D. D. Contact points between a positive transcription factor and the Xenopus 5S RNA gene. Cell. 1982 Dec;31(2 Pt 1):395–405. doi: 10.1016/0092-8674(82)90133-7. [DOI] [PubMed] [Google Scholar]
  25. Schlissel M. S., Brown D. D. The transcriptional regulation of Xenopus 5s RNA genes in chromatin: the roles of active stable transcription complexes and histone H1. Cell. 1984 Jul;37(3):903–913. doi: 10.1016/0092-8674(84)90425-2. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Shastry B. S., Honda B. M., Roeder R. G. Altered levels of a 5 S gene-specific transcription factor (TFIIIA) during oogenesis and embryonic development of Xenopus laevis. J Biol Chem. 1984 Sep 25;259(18):11373–11382. [PubMed] [Google Scholar]
  29. 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]
  30. Teo I., Sedgwick B., Kilpatrick M. W., McCarthy T. V., Lindahl T. The intracellular signal for induction of resistance to alkylating agents in E. coli. Cell. 1986 Apr 25;45(2):315–324. doi: 10.1016/0092-8674(86)90396-x. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. 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]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES