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. 1981 May 11;9(9):2153–2172. doi: 10.1093/nar/9.9.2153

Structural organization of the 16S ribosomal RNA from E. coli. Topography and secondary structure.

P Stiegler, P Carbon, M Zuker, J P Ebel, C Ehresmann
PMCID: PMC326832  PMID: 6170942

Abstract

Extensive studies in our laboratory using different ribonucleases resulted in valuable data on the topography of the E.coli 16S ribosomal RNA within the native 30S subunit, within partially unfolded 30S subunits, in the free state, and in association with individual ribosomal proteins. Such studies have precise details on the accessibility of certain residues and delineated highly accessible RNA regions. Furthermore, they provided evidence that the 16S rRNA is organized in its subunit into four distinct domains. A secondary structure model of the E.coli 16S rRNA has been derived from these topographical data. Additional information from comparative sequence analyses of the small ribosomal subunit RNAs from other species sequenced so far has been used.

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Selected References

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  1. Baer R., Dubin D. T. The 3'-terminal sequence of the small subunit ribosomal RNA from hamster mitochondria. Nucleic Acids Res. 1980 Nov 11;8(21):4927–4941. doi: 10.1093/nar/8.21.4927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brosius J., Palmer M. L., Kennedy P. J., Noller H. F. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4801–4805. doi: 10.1073/pnas.75.10.4801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carbon P., Ehresmann C., Ehresmann B., Ebel J. P. The complete nucleotide sequence of the ribosomal 16-S RNA from Excherichia coli. Experimental details and cistron heterogeneities. Eur J Biochem. 1979 Oct 15;100(2):399–410. doi: 10.1111/j.1432-1033.1979.tb04183.x. [DOI] [PubMed] [Google Scholar]
  4. Carbon P., Ehresmann C., Ehresmann B., Ebel J. P. The sequence of Escherichia coli ribosomal 16 S RNA determined by new rapid gel methods. FEBS Lett. 1978 Oct 1;94(1):152–156. doi: 10.1016/0014-5793(78)80926-0. [DOI] [PubMed] [Google Scholar]
  5. Chapman N. M., Noller H. F. Protection of specific sites in 16 S RNA from chemical modification by association of 30 S and 50 S ribosomes. J Mol Biol. 1977 Jan 5;109(1):131–149. doi: 10.1016/s0022-2836(77)80049-1. [DOI] [PubMed] [Google Scholar]
  6. Donis-Keller H., Maxam A. M., Gilbert W. Mapping adenines, guanines, and pyrimidines in RNA. Nucleic Acids Res. 1977 Aug;4(8):2527–2538. doi: 10.1093/nar/4.8.2527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ehresmann C., Stiegler P., Carbon P., Ungewickell E., Garrett R. A. A topographical study of the 5'-region of 16 S rna of Escherichia coli in the presence and absence of protein S4. FEBS Lett. 1977 Sep 1;81(1):188–192. doi: 10.1016/0014-5793(77)80956-3. [DOI] [PubMed] [Google Scholar]
  8. Ehresmann C., Stiegler P., Carbon P., Ungewickell E., Garrett R. A. The topography of the 5' end of 16-S RNA in the presence and absence of ribosomal proteins S4 and S20. Eur J Biochem. 1980 Feb;103(3):439–446. doi: 10.1111/j.1432-1033.1980.tb05967.x. [DOI] [PubMed] [Google Scholar]
  9. Ehresmann C., Stiegler P., Fellner P., Ebel J. P. The determination of the primary structure of the 16S ribosomal RNA of Escherichia coli. III. Further studies. Biochimie. 1975;57(6-7):711–748. doi: 10.1016/s0300-9084(75)80047-2. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Glotz C., Brimacombe R. An experimentally-derived model for the secondary structure of the 16S ribosomal RNA from Escherichia coli. Nucleic Acids Res. 1980 Jun 11;8(11):2377–2395. doi: 10.1093/nar/8.11.2377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Herr W., Chapman N. M., Noller H. F. Mechanism of ribosomal subunit association: discrimination of specific sites in 16 S RNA essential for association activity. J Mol Biol. 1979 Jun 5;130(4):433–449. doi: 10.1016/0022-2836(79)90433-9. [DOI] [PubMed] [Google Scholar]
  14. Hogan J. J., Noller H. F. Altered topography of 16S RNA in the inactive form of Escherichia coli 30S ribosomal subunits. Biochemistry. 1978 Feb 21;17(4):587–593. doi: 10.1021/bi00597a005. [DOI] [PubMed] [Google Scholar]
  15. Jordan B. R., Latil-Damotte M., Jourdan R. Sequence of the 3'-terminal portion of Drosophila melanogaster 18 S rRNA and of the adjoining spacer: comparison with corresponding prokaryotic and eukaryotic sequences. FEBS Lett. 1980 Aug 11;117(1):227–231. doi: 10.1016/0014-5793(80)80951-3. [DOI] [PubMed] [Google Scholar]
  16. Muto A., Ehresmann C., Fellner P., Zimmermann R. A. RNA-protein interactions in the ribosome. I. Characterization and ribonuclease digestion of 16 S RNA-ribosomal protein complexes. J Mol Biol. 1974 Jun 25;86(2):411–432. doi: 10.1016/0022-2836(74)90028-x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Rinke J., Ross A., Brimacombe R. Characterisation of RNA fragments obtained by mild nuclease digestion of 30-S ribosomal subunits from Escherichia coli. Eur J Biochem. 1977 Jun 1;76(1):189–196. doi: 10.1111/j.1432-1033.1977.tb11584.x. [DOI] [PubMed] [Google Scholar]
  20. Rinke J., Yuki A., Brimacombe R. Studies on the environment of protein S7 within the 30-S subunit Escherichia coli ribosomes. Eur J Biochem. 1976 Apr 15;64(1):77–89. doi: 10.1111/j.1432-1033.1976.tb10276.x. [DOI] [PubMed] [Google Scholar]
  21. Rubtsov P. M., Musakhanov M. M., Batchikova N. V., Skriabin K. S., Baev A. A. Opredelenie pervichnoi struktury fragmentov ribosomnogo operona pekarskikh drozhzhei, kodiruiushchikh 18 S rRNK. Dokl Akad Nauk SSSR. 1979;248(3):760–762. [PubMed] [Google Scholar]
  22. Rubtsov P. M., Musakhanov M. M., Zakharyev V. M., Krayev A. S., Skryabin K. G., Bayev A. A. The structure of the yeast ribosomal RNA genes. I. The complete nucleotide sequence of the 18S ribosomal RNA gene from Saccharomyces cerevisiae. Nucleic Acids Res. 1980 Dec 11;8(23):5779–5794. doi: 10.1093/nar/8.23.5779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Samols D. R., Hagenbuchle O., Gage L. P. Homology of the 3' terminal sequences of the 18S rRNA of Bombyx mori and the 16S rRNA of Escherchia coli. Nucleic Acids Res. 1979 Nov 10;7(5):1109–1119. doi: 10.1093/nar/7.5.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanger F., Brownlee G. G., Barrell B. G. A two-dimensional fractionation procedure for radioactive nucleotides. J Mol Biol. 1965 Sep;13(2):373–398. doi: 10.1016/s0022-2836(65)80104-8. [DOI] [PubMed] [Google Scholar]
  25. Sor F., Fukuhara H. Séquence nucléotidique du gène de l'ARN ribosomique 15S mitochondrial de la levure. C R Seances Acad Sci D. 1980 Dec 8;291(12):933–936. [PubMed] [Google Scholar]
  26. Stiegler P., Carbon P., Zuker M., Ebel J. P., Ehresmann C. Structure secondaire et topographie du RNA ribosomique 16S d'Escherichia coli. C R Seances Acad Sci D. 1980 Dec 8;291(12):937–940. [PubMed] [Google Scholar]
  27. Ungewickell E., Ehresmann C., Stiegler P., Garrett R. Evidence for tertiary structural RNA-RNA interactions within the protein S4 binding site at the 5'-end of 16S ribosomal RNA of Escherichia coli.+. Nucleic Acids Res. 1975 Oct;2(10):1867–1888. doi: 10.1093/nar/2.10.1867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ungewickell E., Garrett R. A. Further characterisation of the RNA structure in the binding region of protein S4 on 16 S ribosomal RNA of Escherichia coli. FEBS Lett. 1977 Sep 1;81(1):193–198. doi: 10.1016/0014-5793(77)80957-5. [DOI] [PubMed] [Google Scholar]
  29. Ungewickell E., Garrett R., Ehresmann C., Stiegler P., Fellner P. An investigation of the 16-S RNA binding sites of ribosomal proteins S4, S8, S15, and S20 FROM Escherichia coli. Eur J Biochem. 1975 Feb 3;51(1):165–180. doi: 10.1111/j.1432-1033.1975.tb03917.x. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Vasilenko S. K., Ryte V. C. [Isolation of highly purified ribonuclease from cobra (Naja oxiana) venom]. Biokhimiia. 1975 May-Jun;40(3):578–583. [PubMed] [Google Scholar]
  32. Wishnia A., Boussert A., Graffe M., Dessen P. H., Grunberg-Manago M. Kinetics of the reversible association of ribosomal subunits: stopped-flow studies of the rate law and of the effect of Mg2+. J Mol Biol. 1975 Apr 25;93(4):499–415. doi: 10.1016/0022-2836(75)90242-9. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Yuan R. C., Steitz J. A., Moore P. B., Crothers D. M. The 3' terminus of 16S rRNA: secondary structure and interaction with ribosomal protein S1. Nucleic Acids Res. 1979 Dec 20;7(8):2399–2418. doi: 10.1093/nar/7.8.2399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yuki A., Brimacombe R. Nucleotide sequences of Escherichia coli 16-S RNA associated with ribosomal proteins S7, S9, S10, S14 and S19. Eur J Biochem. 1975 Aug 1;56(1):23–34. doi: 10.1111/j.1432-1033.1975.tb02203.x. [DOI] [PubMed] [Google Scholar]
  36. Zimmermann R. A., Mackie G. A., Muto A., Garrett R. A., Ungewickell E., Ehresmann C., Stiegler P., Ebel J. P., Fellner P. Location and characteristics of ribosomal protein binding sites in the 16S RNA of Escherichia coli. Nucleic Acids Res. 1975 Feb;2(2):279–302. doi: 10.1093/nar/2.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zimmermann R. A., Singh-Bergmann K. Binding sites for ribosomal proteins S8 and S15 in the 16 S RNA of Escherichia coli. Biochim Biophys Acta. 1979 Jul 26;563(2):422–431. doi: 10.1016/0005-2787(79)90061-3. [DOI] [PubMed] [Google Scholar]
  38. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981 Jan 10;9(1):133–148. doi: 10.1093/nar/9.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zwieb C., Brimacombe R. Localisation of a series of intra-RNA cross-links in 16S RNA, induced by ultraviolet irradiation of Escherichia coli 30S ribosomal subunits. Nucleic Acids Res. 1980 Jun 11;8(11):2397–2411. doi: 10.1093/nar/8.11.2397. [DOI] [PMC free article] [PubMed] [Google Scholar]

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