Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1981 Nov 25;9(22):6167–6189. doi: 10.1093/nar/9.22.6167

Secondary structure model for 23S ribosomal RNA.

H F Noller, J Kop, V Wheaton, J Brosius, R R Gutell, A M Kopylov, F Dohme, W Herr, D A Stahl, R Gupta, C R Waese
PMCID: PMC327592  PMID: 7031608

Abstract

A secondary structure model for 23S ribosomal RNA has been constructed on the basis of comparative sequence data, including the complete sequences from E. coli. Bacillus stearothermophilis, human and mouse mitochondria and several partial sequences. The model has been tested extensively with single strand-specific chemical and enzymatic probes. Long range base-paired interactions organize the molecule into six major structural domains containing over 100 individual helices in all. Regions containing the sites of interaction with several ribosomal proteins and 5S RNA have been located. Segments of the 23S RNA structure corresponding to eucaryotic 5.8S and 25 RNA have been identified, and base paired interactions in the model suggest how they are attached to 28S RNA. Functionally important regions, including possible sites of contact with 30S ribosomal subunits, the peptidyl transferase center and locations of intervening sequences in various organisms are discussed. Models for molecular 'switching' of RNA molecules based on coaxial stacking of helices are presented, including a scheme for tRNA-23S RNA interaction.

Full text

PDF
6167

Images in this article

Selected References

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

  1. Allet B., Rochaix J. D. Structure analysis at the ends of the intervening DNA sequences in the chloroplast 23S ribosomal genes of C. reinhardii. Cell. 1979 Sep;18(1):55–60. doi: 10.1016/0092-8674(79)90353-2. [DOI] [PubMed] [Google Scholar]
  2. Allet B., Spahr P. F. Binding sites of ribosomal proteins on two specific fragments derived from Escherichia coli 50 S ribosomes. Eur J Biochem. 1971 Mar 11;19(2):250–255. doi: 10.1111/j.1432-1033.1971.tb01311.x. [DOI] [PubMed] [Google Scholar]
  3. Bos J. L., Osinga K. A., Van der Horst G., Hecht N. B., Tabak H. F., Van Ommen G. J., Borst P. Splice point sequence and transcripts of the intervening sequence in the mitochondrial 21S ribosomal RNA gene of yeast. Cell. 1980 May;20(1):207–214. doi: 10.1016/0092-8674(80)90248-2. [DOI] [PubMed] [Google Scholar]
  4. Branlant C., Krol A., Sriwdada J., Ebel J. P., Sloof P., Garrett R. A. The binding site of protein L1 ON 23-S ribosomal RNA of Escherichia coli. 2. Identification of the rna region contained in the L1 ribonucleoproteins and determination of the order of the RNA subfragments within this region. Eur J Biochem. 1976 Nov 15;70(2):457–469. doi: 10.1111/j.1432-1033.1976.tb11037.x. [DOI] [PubMed] [Google Scholar]
  5. Branlant C., Krol A., Sriwidada J., Brimacombe R. RNA sequences associated with proteins L1, L9, and L5, L18, L25, in ribonucleoprotein fragments isolated from the 50-S subunit of Escherichia coli ribosomes. Eur J Biochem. 1976 Nov 15;70(2):483–492. doi: 10.1111/j.1432-1033.1976.tb11039.x. [DOI] [PubMed] [Google Scholar]
  6. Branlant C., Widada J. S., Krol A., Ebel J. P. Studies on the primary structure of the ribosomal 23S RNA of Escherichia coli: II. A characterisation and an alignment of 24 sections spanning the entire molecule and its application to the localisation of specific fragments. Nucleic Acids Res. 1977 Dec;4(12):4323–4345. doi: 10.1093/nar/4.12.4323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brosius J., Dull T. J., Noller H. F. Complete nucleotide sequence of a 23S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jan;77(1):201–204. doi: 10.1073/pnas.77.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bruce A. G., Uhlenbeck O. C. Reactions at the termini of tRNA with T4 RNA ligase. Nucleic Acids Res. 1978 Oct;5(10):3665–3677. doi: 10.1093/nar/5.10.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cerná J., Rychlík I., Krayevsky A. A., Gottikh B. P. A contribution to the studies on donor site of peptidyl transferase with acylaminoacyl-nucleoside-5'-monophosphates. Acta Biol Med Ger. 1974;33(5-6):877–883. [PubMed] [Google Scholar]
  10. Contreras R., Fiers W. A new method for partial digestion useful for sequence analysis of polynucleotides. FEBS Lett. 1971 Sep 1;16(4):281–283. doi: 10.1016/0014-5793(71)80370-8. [DOI] [PubMed] [Google Scholar]
  11. Dujon B. Sequence of the intron and flanking exons of the mitochondrial 21S rRNA gene of yeast strains having different alleles at the omega and rib-1 loci. Cell. 1980 May;20(1):185–197. doi: 10.1016/0092-8674(80)90246-9. [DOI] [PubMed] [Google Scholar]
  12. Eckerman D. J., Symons R. H. Sequence at the site of attachment of an affinity-label derivative of puromycin on 23-S ribosomal RNA of Escherichia coli ribosomes. Eur J Biochem. 1978 Jan 2;82(1):225–234. doi: 10.1111/j.1432-1033.1978.tb12015.x. [DOI] [PubMed] [Google Scholar]
  13. Edlind T. D., Bassel A. R. Electron microscopic mapping of secondary structures in bacterial 16S and 23S ribosomal ribonucleic acid and 30S precursor ribosomal ribonucleic acid. J Bacteriol. 1980 Jan;141(1):365–373. doi: 10.1128/jb.141.1.365-373.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Edwards K., Kössel H. The rRNA operon from Zea mays chloroplasts: nucleotide sequence of 23S rDNA and its homology with E.coli 23S rDNA. Nucleic Acids Res. 1981 Jun 25;9(12):2853–2869. doi: 10.1093/nar/9.12.2853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Eperon I. C., Anderson S., Nierlich D. P. Distinctive sequence of human mitochondrial ribosomal RNA genes. Nature. 1980 Jul 31;286(5772):460–467. doi: 10.1038/286460a0. [DOI] [PubMed] [Google Scholar]
  16. Fanning T. G., Traut R. R. Topography of the C. coli 5S RNA-protein complex as determined by crosslinking with dimethyl suberimidate and dimethyl-3,3'-dithiobispropionimidate. Nucleic Acids Res. 1981 Feb 25;9(4):993–1004. doi: 10.1093/nar/9.4.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fox G. E., Woese C. R. 5S RNA secondary structure. Nature. 1975 Aug 7;256(5517):505–507. doi: 10.1038/256505a0. [DOI] [PubMed] [Google Scholar]
  18. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  19. Glotz C., Zwieb C., Brimacombe R., Edwards K., Kössel H. Secondary structure of the large subunit ribosomal RNA from Escherichia coli, Zea mays chloroplast, and human and mouse mitochondrial ribosomes. Nucleic Acids Res. 1981 Jul 24;9(14):3287–3306. doi: 10.1093/nar/9.14.3287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gourse R. L., Gerbi S. A. Fine structure of ribosomal RNA. IV. Extraordinary evolutionary conservation in sequences that flank introns in rDNA. Nucleic Acids Res. 1980 Aug 25;8(16):3623–3637. doi: 10.1093/nar/8.16.3623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gourse R. L., Thurlow D. L., Gerbi S. A., Zimmermann R. A. Specific binding of a prokaryotic ribosomal protein to a eukaryotic ribosomal RNA: implications for evolution and autoregulation. Proc Natl Acad Sci U S A. 1981 May;78(5):2722–2726. doi: 10.1073/pnas.78.5.2722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hall L. M., Maden B. E. Nucleotide sequence through the 18S-28S intergene region of a vertebrate ribosomal transcription unit. Nucleic Acids Res. 1980 Dec 20;8(24):5993–6005. doi: 10.1093/nar/8.24.5993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Herr W., Noller H. F. A fragment of 23S RNA containing a nucleotide sequence complementary to a region of 5S RNA. FEBS Lett. 1975 May 1;53(2):248–252. doi: 10.1016/0014-5793(75)80030-5. [DOI] [PubMed] [Google Scholar]
  24. Herr W., Noller H. F. Nucleotide sequences of accessible regions of 23S RNA in 50S ribosomal subunits. Biochemistry. 1978 Jan 24;17(2):307–315. doi: 10.1021/bi00595a018. [DOI] [PubMed] [Google Scholar]
  25. Herr W., Noller H. F. Protection of specific sites in 23 S and 5 S RNA from chemical modification by association of 30 S and 50 S ribosomes. J Mol Biol. 1979 Jun 5;130(4):421–432. doi: 10.1016/0022-2836(79)90432-7. [DOI] [PubMed] [Google Scholar]
  26. Jordan B. R. '2S' RNA, a new ribosomal RNA component in cultured Drosophila cells. FEBS Lett. 1974 Aug 15;44(1):39–42. doi: 10.1016/0014-5793(74)80301-7. [DOI] [PubMed] [Google Scholar]
  27. Kearsey S. E., Craig I. W. Altered ribosomal RNA genes in mitochondria from mammalian cells with chloramphenicol resistance. Nature. 1981 Apr 16;290(5807):607–608. doi: 10.1038/290607a0. [DOI] [PubMed] [Google Scholar]
  28. King T. C., Rucinsky T., Schlessinger D., Milanovich F. Escherichia coli ribosome unfolding in low Mg2+ solutions observed by laser Raman spectroscopy and electron microscopy. Nucleic Acids Res. 1981 Feb 11;9(3):647–661. doi: 10.1093/nar/9.3.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Krol A., Machatt M. A., Branlant C., Ebel J. P. RNA-RNA interactions in the binding site of protein L24 on 23S ribosomal RNA of E. coli. II. Sequence analysis of the interacting fragments. Nucleic Acids Res. 1978 Dec;5(12):4933–4947. doi: 10.1093/nar/5.12.4933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Luehrsen K. R., Fox G. E. Secondary structure of eukaryotic cytoplasmic 5S ribosomal RNA. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2150–2154. doi: 10.1073/pnas.78.4.2150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Maly P., Rinke J., Ulmer E., Zwieb C., Brimacombe R. Precise localization of the site of cross-linking between protein L4 and 23S ribonucleic acid induced by mild ultraviolet irradiation of Escherichia coli 50S ribosomal subunits. Biochemistry. 1980 Sep 2;19(18):4179–4188. doi: 10.1021/bi00559a007. [DOI] [PubMed] [Google Scholar]
  32. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Müller R., Garrett R. A., Noller H. F. The structure of the RNA binding site of ribosomal proteins S8 and S15. J Biol Chem. 1979 May 25;254(10):3873–3878. [PubMed] [Google Scholar]
  34. Nazar R. N. A 5.8 S rRNA-like sequence in prokaryotic 23 S rRNA. FEBS Lett. 1980 Oct 6;119(2):212–214. doi: 10.1016/0014-5793(80)80254-7. [DOI] [PubMed] [Google Scholar]
  35. Noller H. F., Woese C. R. Secondary structure of 16S ribosomal RNA. Science. 1981 Apr 24;212(4493):403–411. doi: 10.1126/science.6163215. [DOI] [PubMed] [Google Scholar]
  36. Nomiyama H., Sakaki Y., Takagi Y. Nucleotide sequence of a ribosomal RNA gene intron from slime mold Physarum polycephalum. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1376–1380. doi: 10.1073/pnas.78.3.1376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Orozco E. M., Jr, Rushlow K. E., Dodd J. R., Hallick R. B. Euglena gracilis chloroplast ribosomal RNA transcription units. II. Nucleotide sequence homology between the 16 S--23 S ribosomal RNA spacer and the 16 S ribosomal RNA leader regions. J Biol Chem. 1980 Nov 25;255(22):10997–11003. [PubMed] [Google Scholar]
  38. Pace N. R., Walker T. A., Schroeder E. Structure of the 5.8S RNA component of the 5.8S-28S ribosomal RNA junction complex. Biochemistry. 1977 Nov 29;16(24):5321–5328. doi: 10.1021/bi00643a025. [DOI] [PubMed] [Google Scholar]
  39. Pavlakis G. N., Jordan B. R., Wurst R. M., Vournakis J. N. Sequence and secondary structure of Drosophila melanogaster 5.8S and 2S rRNAs and of the processing site between them. Nucleic Acids Res. 1979 Dec 20;7(8):2213–2238. doi: 10.1093/nar/7.8.2213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Peattie D. A. Direct chemical method for sequencing RNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1760–1764. doi: 10.1073/pnas.76.4.1760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Peattie D. A., Herr W. Chemical probing of the tRNA--ribosome complex. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2273–2277. doi: 10.1073/pnas.78.4.2273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rae P. M., Kohorn B. D., Wade R. P. The 10 kb Drosophila virilis 28S rDNA intervening sequence is flanked by a direct repeat of 14 base pairs of coding sequence. Nucleic Acids Res. 1980 Aug 25;8(16):3491–3504. doi: 10.1093/nar/8.16.3491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Roiha H., Miller J. R., Woods L. C., Glover D. M. Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature. 1981 Apr 30;290(5809):749–753. doi: 10.1038/290749a0. [DOI] [PubMed] [Google Scholar]
  44. Sanger F., Coulson A. R. A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. J Mol Biol. 1975 May 25;94(3):441–448. doi: 10.1016/0022-2836(75)90213-2. [DOI] [PubMed] [Google Scholar]
  45. Selker E., Yanofsky C. Nucleotide sequence and conserved features of the 5.8 S rRNA coding region of Neurospora crassa. Nucleic Acids Res. 1979 Jun 11;6(7):2561–2567. doi: 10.1093/nar/6.7.2561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sloof P., Hunter J. B., Garrett R. A., Branlant C. RNA-RNA interactions in the binding site of protein L24 on 23S ribosomal RNA of Escherichia coli: 1. Evidence for their occurrence between widely separated sequence regions. Nucleic Acids Res. 1978 Oct;5(10):3503–3513. doi: 10.1093/nar/5.10.3503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sollner-Webb B., Reeder R. H. The nucleotide sequence of the initiation and termination sites for ribosomal RNA transcription in X. laevis. Cell. 1979 Oct;18(2):485–499. doi: 10.1016/0092-8674(79)90066-7. [DOI] [PubMed] [Google Scholar]
  48. Spierer P., Zimmermann R. A. RNA-protein interactions in the ribosome. Binding of proteins L1, L3, L6, L13 and L23 to specific fragments of the 23S RNA. FEBS Lett. 1976 Sep 15;68(1):71–75. doi: 10.1016/0014-5793(76)80407-3. [DOI] [PubMed] [Google Scholar]
  49. Van Etten R. A., Walberg M. W., Clayton D. A. Precise localization and nucleotide sequence of the two mouse mitochondrial rRNA genes and three immediately adjacent novel tRNA genes. Cell. 1980 Nov;22(1 Pt 1):157–170. doi: 10.1016/0092-8674(80)90164-6. [DOI] [PubMed] [Google Scholar]
  50. Wild M. A., Sommer R. Sequence of a ribosomal RNA gene intron from Tetrahymena. Nature. 1980 Feb 14;283(5748):693–694. doi: 10.1038/283693a0. [DOI] [PubMed] [Google Scholar]
  51. Woese C. R., Magrum L. J., Gupta R., Siegel R. B., Stahl D. A., Kop J., Crawford N., Brosius J., Gutell R., Hogan J. J. Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. Nucleic Acids Res. 1980 May 24;8(10):2275–2293. doi: 10.1093/nar/8.10.2275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wrede P., Erdmann V. A. Escherichia coli 5S RNA binding proteins L18 and L25 interact with 5.8S RNA but not with 5S RNA from yeast ribosomes. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2706–2709. doi: 10.1073/pnas.74.7.2706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yukioka M., Hatayama T., Omori K. Nucleotide sequence of a region in 23-S RNA adjacent to peptidyl transferase catalytic center of Escherichia coli ribosomes. Eur J Biochem. 1977 Mar 1;73(2):449–459. doi: 10.1111/j.1432-1033.1977.tb11337.x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES