Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Jun;85(11):3802–3804. doi: 10.1073/pnas.85.11.3802

Electron microscopic study of crystals of the Xenopus laevis transcription factor IIIA-5S ribosomal RNA complex.

R S Brown 1, C Ferguson 1, A Kingswell 1, F K Winkler 1, K R Leonard 1
PMCID: PMC280307  PMID: 3375242

Abstract

A novel method has been developed to grow crystals of the Xenopus laevis transcription factor IIIA-5S RNA complex directly on grids for examination by electron microscopy. Microcrystals were examined in negative stain and in thin sections to reveal a hexagonal lattice with unit-cell dimensions a = b = 87.1 +/- 4.4 A and c = 143.8 +/- 12.7 A. Optical diffraction patterns from micrographs were obtained about the major crystal axes extending to about 40-A resolution. A packing scheme is proposed for which there are three or six transcription factor IIIA-5S RNA complexes in the unit cell related by 3(1) symmetry along the long cell axis. This would require that the 5S RNA molecules are arranged end-to-end, with the terminal loops of adjacent molecules overlapping.

Full text

PDF
3802

Images in this article

3803Image
on p.3803
3803Image
on p.3803
3803Image
on p.3803
3803Image
on p.3803
3803Image
on p.3803
3803Image
on p.3803

Selected References

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

  1. Abdel-Meguid S. S., Moore P. B., Steitz T. A. Crystallization of a ribonuclease-resistant fragment of Escherichia coli 5 S ribosomal RNA and its complex with protein L25. J Mol Biol. 1983 Dec 5;171(2):207–215. doi: 10.1016/s0022-2836(83)80353-2. [DOI] [PubMed] [Google Scholar]
  2. Barrett P., Kloetzel P. M., Sommerville J. Specific interaction of proteins with 5 S RNA and tRNA in the 42 S storage particle of Xenopus oocytes. Biochim Biophys Acta. 1983 Sep 9;740(4):347–354. doi: 10.1016/0167-4781(83)90081-7. [DOI] [PubMed] [Google Scholar]
  3. Berriman J., Leonard K. R. Methods for specimen thickness determination in electron microscopy. II. Changes in thickness with dose. Ultramicroscopy. 1986;19(4):349–366. doi: 10.1016/0304-3991(86)90095-1. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Brown R. S., Argos P. Fingers and helices. Nature. 1986 Nov 20;324(6094):215–215. doi: 10.1038/324215a0. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Chothia C. Principles that determine the structure of proteins. Annu Rev Biochem. 1984;53:537–572. doi: 10.1146/annurev.bi.53.070184.002541. [DOI] [PubMed] [Google Scholar]
  8. Chowdhury K., Deutsch U., Gruss P. A multigene family encoding several "finger" structures is present and differentially active in mammalian genomes. Cell. 1987 Mar 13;48(5):771–778. doi: 10.1016/0092-8674(87)90074-2. [DOI] [PubMed] [Google Scholar]
  9. Christiansen J., Brown R. S., Sproat B. S., Garrett R. A. Xenopus transcription factor IIIA binds primarily at junctions between double helical stems and internal loops in oocyte 5S RNA. EMBO J. 1987 Feb;6(2):453–460. doi: 10.1002/j.1460-2075.1987.tb04775.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Denis H., Picard B., le Maire M., Clerot J. C. Biochemical research on oogenesis. The storage particles of the teleost fish Tinca tinca. Dev Biol. 1980 Jun 1;77(1):218–223. doi: 10.1016/0012-1606(80)90468-6. [DOI] [PubMed] [Google Scholar]
  11. Denis H., Wegnez M. Biochemical research on oogenesis: oocytes of Xenopus laevis synthesize but do not accumulate 5S RNA of somatic type. Dev Biol. 1977 Jul 1;58(1):212–217. doi: 10.1016/0012-1606(77)90087-2. [DOI] [PubMed] [Google Scholar]
  12. Denis H., le Maire M. Thesaurisomes, a novel kind of nucleoprotein particle. Subcell Biochem. 1983;9:263–297. doi: 10.1007/978-1-4613-3533-7_3. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Ford P. J., Southern E. M. Different sequences for 5S RNA in kidney cells and ovaries of Xenopus laevis. Nat New Biol. 1973 Jan 3;241(105):7–12. doi: 10.1038/newbio241007a0. [DOI] [PubMed] [Google Scholar]
  16. Frankel A. D., Berg J. M., Pabo C. O. Metal-dependent folding of a single zinc finger from transcription factor IIIA. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4841–4845. doi: 10.1073/pnas.84.14.4841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Jésior J. C. The grid sectioning technique: a study of catalase platelets. EMBO J. 1982;1(11):1423–1428. doi: 10.1002/j.1460-2075.1982.tb01333.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Leonard K., Wingfield P., Arad T., Weiss H. Three-dimensional structure of ubiquinol:cytochrome c reductase from Neurospora mitochondria determined by electron microscopy of membrane crystals. J Mol Biol. 1981 Jun 25;149(2):259–274. doi: 10.1016/0022-2836(81)90301-6. [DOI] [PubMed] [Google Scholar]
  21. Mattaj I. W., Lienhard S., Zeller R., DeRobertis E. M. Nuclear exclusion of transcription factor IIIA and the 42s particle transfer RNA-binding protein in Xenopus oocytes: a possible mechanism for gene control? J Cell Biol. 1983 Oct;97(4):1261–1265. doi: 10.1083/jcb.97.4.1261. [DOI] [PMC free article] [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. Morikawa K., Fujiyoshi Y., Ishizuka K., Sugiyama J., Kawakami M., Takemura S. Electron microscopic study of 5S rRNA crystals from Thermus thermophilus HB8. J Microsc. 1986 May;142(Pt 2):247–258. doi: 10.1111/j.1365-2818.1986.tb02761.x. [DOI] [PubMed] [Google Scholar]
  24. Morikawa K., Kawakami M., Takemura S. Crystallization and preliminary X-ray diffraction study of 5 S rRNA from Thermus thermophilus HB8. FEBS Lett. 1982 Aug 23;145(2):194–196. doi: 10.1016/0014-5793(82)80166-x. [DOI] [PubMed] [Google Scholar]
  25. Morikawa K., Kawakami M., Takemura S. Single crystals of 5S rRNA from Thermus thermophilus HB8 and preliminary X-ray diffraction data. Nucleic Acids Symp Ser. 1982;(11):173–176. [PubMed] [Google Scholar]
  26. 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]
  27. Müller J. J., Zalkova T. N., Zirwer D., Misselwitz R., Gast K., Serdyuk I. N., Welfle H., Damaschun G. Comparison of the structure of ribosomal 5S RNA from E. coli and from rat liver using X-ray scattering and dynamic light scattering. Eur Biophys J. 1986;13(5):301–307. doi: 10.1007/BF00254212. [DOI] [PubMed] [Google Scholar]
  28. Pays E., Murphy N. B. DNA-binding fingers encoded by a trypanosome retroposon. J Mol Biol. 1987 Sep 5;197(1):147–148. doi: 10.1016/0022-2836(87)90617-6. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Ruiz i Altaba A., Perry-O'Keefe H., Melton D. A. Xfin: an embryonic gene encoding a multifingered protein in Xenopus. EMBO J. 1987 Oct;6(10):3065–3070. doi: 10.1002/j.1460-2075.1987.tb02613.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Taylor W., Jackson I. J., Siegel N., Kumar A., Brown D. D. The developmental expression of the gene for TFIIIA in Xenopus laevis. Nucleic Acids Res. 1986 Aug 11;14(15):6185–6195. doi: 10.1093/nar/14.15.6185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tso J. Y., Van Den Berg D. J., Korn L. J. Structure of the gene for Xenopus transcription factor TFIIIA. Nucleic Acids Res. 1986 Mar 11;14(5):2187–2200. doi: 10.1093/nar/14.5.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Vincent A., O'Connell P., Gray M. R., Rosbash M. Drosophila maternal and embryo mRNAs transcribed from a single transcription unit use alternate combinations of exons. EMBO J. 1984 May;3(5):1003–1013. doi: 10.1002/j.1460-2075.1984.tb01920.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vincent A. TFIIIA and homologous genes. The 'finger' proteins. Nucleic Acids Res. 1986 Jun 11;14(11):4385–4391. doi: 10.1093/nar/14.11.4385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wegnez M., Monier R., Denis H. Sequence heterogeneity of 5 S RNA in Xenopus laevis. FEBS Lett. 1972 Sep 1;25(1):13–20. doi: 10.1016/0014-5793(72)80443-5. [DOI] [PubMed] [Google Scholar]
  38. Westhof E., Dumas P., Moras D. Crystallographic refinement of yeast aspartic acid transfer RNA. J Mol Biol. 1985 Jul 5;184(1):119–145. doi: 10.1016/0022-2836(85)90048-8. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES