Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1988 Dec 9;16(23):11267–11284. doi: 10.1093/nar/16.23.11267

Xenopus transcription factor IIIA forms a complex of covalent character with 5S DNA.

J Blanco 1, J M Gottesfeld 1
PMCID: PMC339009  PMID: 3205743

Abstract

The 5S gene-specific transcription factor TFIIIA forms an exceptionally stable complex with the internal promoter of the 5S RNA gene. Approximately 1 to 5% of TFIIIA-DNA or deoxyoligonucleotide complexes are stable to harsh denaturation conditions and can be resolved by electrophoresis in the presence of SDS. These complexes are resistant to acidic conditions (0.1 N HCl, 55 degrees C, 2h) suggesting that the interaction may be through a covalent bond. Complex formation does not result in DNA strand scission and studies of the chemical sensitivity of the complex suggest that the TFIIIA-DNA linkage may be through a phosphoramidate bond. Covalent complexes are formed with both the noncoding (RNA-like) and coding strands of the internal control region. The predominant sites of TFIIIA-DNA adducts have been mapped to the 3' end of the 5S gene internal control region, the region previously shown to exhibit essential guanine and phosphate contacts with TFIIIA.

Full text

PDF
11267

Images in this article

11271Image
on p.11271
11272Image
on p.11272
11273Image
on p.11273
11275Image
on p.11275
11276Image
on p.11276
11277Image
on p.11277
11278Image
on p.11278
11279Image
on p.11279
11280Image
on p.11280

Selected References

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

  1. Berg J. M. Potential metal-binding domains in nucleic acid binding proteins. Science. 1986 Apr 25;232(4749):485–487. doi: 10.1126/science.2421409. [DOI] [PubMed] [Google Scholar]
  2. Bieker J. J., Martin P. L., Roeder R. G. Formation of a rate-limiting intermediate in 5S RNA gene transcription. Cell. 1985 Jan;40(1):119–127. doi: 10.1016/0092-8674(85)90315-0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. 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]
  6. Boulay J. L., Dennefeld C., Alberga A. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. 1987 Nov 26-Dec 2Nature. 330(6146):395–398. doi: 10.1038/330395a0. [DOI] [PubMed] [Google Scholar]
  7. Brown R. S., Sander C., Argos P. The primary structure of transcription factor TFIIIA has 12 consecutive repeats. FEBS Lett. 1985 Jul 8;186(2):271–274. doi: 10.1016/0014-5793(85)80723-7. [DOI] [PubMed] [Google Scholar]
  8. Diakun G. P., Fairall L., Klug A. EXAFS study of the zinc-binding sites in the protein transcription factor IIIA. Nature. 1986 Dec 18;324(6098):698–699. doi: 10.1038/324698a0. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Fairall L., Rhodes D., Klug A. Mapping of the sites of protection on a 5 S RNA gene by the Xenopus transcription factor IIIA. A model for the interaction. J Mol Biol. 1986 Dec 5;192(3):577–591. doi: 10.1016/0022-2836(86)90278-0. [DOI] [PubMed] [Google Scholar]
  11. Fried M., Crothers D. M. Equilibria and kinetics of lac repressor-operator interactions by polyacrylamide gel electrophoresis. Nucleic Acids Res. 1981 Dec 11;9(23):6505–6525. doi: 10.1093/nar/9.23.6505. [DOI] [PMC free article] [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. Gronostajski R. M., Sadowski P. D. The FLP recombinase of the Saccharomyces cerevisiae 2 microns plasmid attaches covalently to DNA via a phosphotyrosyl linkage. Mol Cell Biol. 1985 Nov;5(11):3274–3279. doi: 10.1128/mcb.5.11.3274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hanas J. S., Bogenhagen D. F., Wu C. W. Binding of Xenopus transcription factor A to 5S RNA and to single stranded DNA. Nucleic Acids Res. 1984 Mar 26;12(6):2745–2758. doi: 10.1093/nar/12.6.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hanas J. S., Hazuda D. J., Bogenhagen D. F., Wu F. Y., Wu C. W. Xenopus transcription factor A requires zinc for binding to the 5 S RNA gene. J Biol Chem. 1983 Dec 10;258(23):14120–14125. [PubMed] [Google Scholar]
  16. Hartshorne T. A., Blumberg H., Young E. T. Sequence homology of the yeast regulatory protein ADR1 with Xenopus transcription factor TFIIIA. Nature. 1986 Mar 20;320(6059):283–287. doi: 10.1038/320283a0. [DOI] [PubMed] [Google Scholar]
  17. Honda B. M., Roeder R. G. Association of a 5S gene transcription factor with 5S RNA and altered levels of the factor during cell differentiation. Cell. 1980 Nov;22(1 Pt 1):119–126. doi: 10.1016/0092-8674(80)90160-9. [DOI] [PubMed] [Google Scholar]
  18. Hunter T., Sefton B. M. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1311–1315. doi: 10.1073/pnas.77.3.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kadonaga J. T., Carner K. R., Masiarz F. R., Tjian R. Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell. 1987 Dec 24;51(6):1079–1090. doi: 10.1016/0092-8674(87)90594-0. [DOI] [PubMed] [Google Scholar]
  20. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  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. Millstein L., Eversole-Cire P., Blanco J., Gottesfeld J. M. Differential transcription of Xenopus oocyte and somatic-type 5 S genes in a Xenopus oocyte extract. J Biol Chem. 1987 Dec 15;262(35):17100–17110. [PubMed] [Google Scholar]
  24. Muriel W. J., Cole J., Lehmann A. R. Molecular analysis of ouabain-resistant mutants of the mouse lymphoma cell line L5178Y. Mutagenesis. 1987 Sep;2(5):383–389. doi: 10.1093/mutage/2.5.383. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Picard B., Wegnez M. Isolation of a 7S particle from Xenopus laevis oocytes: a 5S RNA-protein complex. Proc Natl Acad Sci U S A. 1979 Jan;76(1):241–245. doi: 10.1073/pnas.76.1.241. [DOI] [PMC free article] [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. Reed R. R., Grindley N. D. Transposon-mediated site-specific recombination in vitro: DNA cleavage and protein-DNA linkage at the recombination site. Cell. 1981 Sep;25(3):721–728. doi: 10.1016/0092-8674(81)90179-3. [DOI] [PubMed] [Google Scholar]
  30. Rhodes D., Klug A. An underlying repeat in some transcriptional control sequences corresponding to half a double helical turn of DNA. Cell. 1986 Jul 4;46(1):123–132. doi: 10.1016/0092-8674(86)90866-4. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. Schuh R., Aicher W., Gaul U., Côté S., Preiss A., Maier D., Seifert E., Nauber U., Schröder C., Kemler R. A conserved family of nuclear proteins containing structural elements of the finger protein encoded by Krüppel, a Drosophila segmentation gene. Cell. 1986 Dec 26;47(6):1025–1032. doi: 10.1016/0092-8674(86)90817-2. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Shabarova Z. A. Synthetic nucleotide-peptides. Prog Nucleic Acid Res Mol Biol. 1970;10:145–182. doi: 10.1016/s0079-6603(08)60564-4. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vincent A., Colot H. V., Rosbash M. Sequence and structure of the serendipity locus of Drosophila melanogaster. A densely transcribed region including a blastoderm-specific gene. J Mol Biol. 1985 Nov 5;186(1):149–166. doi: 10.1016/0022-2836(85)90265-7. [DOI] [PubMed] [Google Scholar]
  39. Vrana K. E., Churchill M. E., Tullius T. D., Brown D. D. Mapping functional regions of transcription factor TFIIIA. Mol Cell Biol. 1988 Apr;8(4):1684–1696. doi: 10.1128/mcb.8.4.1684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wang J. C. DNA topoisomerases. Annu Rev Biochem. 1985;54:665–697. doi: 10.1146/annurev.bi.54.070185.003313. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES