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. 1982 Nov 25;10(22):7323–7344. doi: 10.1093/nar/10.22.7323

Generalized structures of the 5S ribosomal RNAs.

N Delihas, J Andersen
PMCID: PMC327007  PMID: 7155895

Abstract

The sequences of 5S ribosomal RNAs from a wide-range of organisms have been compared. All sequences fit a generalized 5S RNA secondary structural model. Twenty-three nucleotide positions are found universally, i.e., in 5S RNAs of eukaryotes, prokaryotes, archaebacteria, chloroplasts and mitochondria. One major distinguishing feature between the prokaryotic and eukaryotic 5S RNAs is the number of nucleotide positions between certain universal positions, e.g., prokaryotic 5S RNAs have three positions between the universal positions PuU40 and G44 (using the E. coli numbering system) and eukaryotic 5S RNAs have two. The archaebacterial 5S RNAs appear to resemble the eukaryotic 5S RNAs to varying degrees depending on the species of archaebacteria although all the RNAs conform with the prokaryotic "rule" of chain length between PuU40 and G44. The green plant chloroplast and wheat mitochondrial 5S RNAs appear prokaryotic-like when comparing the number of positions between universal nucleotides. Nucleotide positions common to eukaryotic 5S RNAs have been mapped; in addition, nucleotide sequences, helix lengths and looped-out residues specific to phyla are proposed. Several of the common nucleotides found in the 5S RNAs of metazoan somatic tissue differ in the 5S RNAs of oocytes. These changes may indicate an important functional role of the 5S RNA during oocyte maturation.

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Selected References

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  1. Alexander L. J., Stewart T. S. Nucleotide sequence of Lactobacillus viridescens 5S RNA. Nucleic Acids Res. 1980 Mar 11;8(5):979–987. doi: 10.1093/nar/8.5.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aoyama K., Hidaka S., Tanaka T., Ishikawa K. The nucleotide sequence of 5S RNA from rat liver ribosomes. J Biochem. 1982 Jan;91(1):363–367. doi: 10.1093/oxfordjournals.jbchem.a133696. [DOI] [PubMed] [Google Scholar]
  3. Bellemare G., Jordan B. R., Rocca-Serra J., Monier R. Accessibility of Escherichia coli 5S RNA base residues to chemical reagents. Influence of chemical alterations on the affinity of 5S RNA for the 50S subunit structure. Biochimie. 1972;54(11):1453–1466. doi: 10.1016/s0300-9084(72)80087-7. [DOI] [PubMed] [Google Scholar]
  4. Benhamou J., Jordan B. R. Nucleotide sequence of Drosophila melanogaster 5S RNA: evidence for a general 5S RNA model. FEBS Lett. 1976 Feb 15;62(2):146–149. doi: 10.1016/0014-5793(76)80039-7. [DOI] [PubMed] [Google Scholar]
  5. Bogenhagen D. F., Sakonju S., Brown D. D. A control region in the center of the 5S RNA gene directs specific initiation of transcription: II. The 3' border of the region. Cell. 1980 Jan;19(1):27–35. doi: 10.1016/0092-8674(80)90385-2. [DOI] [PubMed] [Google Scholar]
  6. Brownlee G. G., Cartwright E. M. The nucleotide sequence of the 5S RNA of chicken embryo fibroblasts. Nucleic Acids Res. 1975 Dec;2(12):2279–2288. doi: 10.1093/nar/2.12.2279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Butler M. H., Wall S. M., Luehrsen K. R., Fox G. E., Hecht R. M. Molecular relationships between closely related strains and species of nematodes. J Mol Evol. 1981;18(1):18–23. doi: 10.1007/BF01733207. [DOI] [PubMed] [Google Scholar]
  8. Corry M. J., Payne P. I., Dyer T. A. The nucleotide sequence of 5 S rRNA from the blue-green alga Anacystis nidulans. FEBS Lett. 1974 Sep 15;46(1):63–66. doi: 10.1016/0014-5793(74)80335-2. [DOI] [PubMed] [Google Scholar]
  9. Darlix J. L., Rochaix J. D. Nucleotide sequence and structure of cytoplasmic 5S RNA and 5.8S RNA of Chlamydomonas reinhardii. Nucleic Acids Res. 1981 Mar 25;9(6):1291–1299. doi: 10.1093/nar/9.6.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. De Wachter R., Chen M. W., Vandenberghe A. Conservation of secondary structure in 5 S ribosomal RNA: a uniform model for eukaryotic, eubacterial, archaebacterial and organelle sequences is energetically favourable. Biochimie. 1982 May;64(5):311–329. doi: 10.1016/s0300-9084(82)80436-7. [DOI] [PubMed] [Google Scholar]
  11. Delihas N., Andersen J., Andresini W., Kaufman L., Lyman H. The 5S ribosomal RNA of Euglena gracilis cytoplasmic ribosomes is closely homologous to the 5S RNA of the trypanosomatid protozoa. Nucleic Acids Res. 1981 Dec 11;9(23):6627–6633. doi: 10.1093/nar/9.23.6627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Delihas N., Andersen J., Sprouse H. M., Dudock B. The nucleotide sequence of the chloroplast 5S ribosomal RNA from spinach. Nucleic Acids Res. 1981 Jun 25;9(12):2801–2805. doi: 10.1093/nar/9.12.2801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Delihas N., Andersen J., Sprouse H. M., Kashdan M., Dudock B. The nucleotide sequence of spinach cytoplasmic 5 S ribosomal RNA. J Biol Chem. 1981 Jul 25;256(14):7515–7517. [PubMed] [Google Scholar]
  14. Delihas N., Dunn J. J., Erdmann V. A. The reaction of 5S RNA in 70S ribosomes with kethoxal. FEBS Lett. 1975 Oct 15;58(1):76–80. doi: 10.1016/0014-5793(75)80229-8. [DOI] [PubMed] [Google Scholar]
  15. Digweed M., Erdmann V. A., Odom O. W., Hardesty B. Fluorescence modification of Escherichia coli 5S RNA. Nucleic Acids Res. 1981 Jul 10;9(13):3187–3198. doi: 10.1093/nar/9.13.3187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DuBuy B., Weissman S. M. Nucleotide sequence of Pseudomonas fluorescens 5 S ribonucleic acid. J Biol Chem. 1971 Feb 10;246(3):747–761. [PubMed] [Google Scholar]
  17. Dyer T. A., Bowman C. M. Nucleotide sequences of chloroplast 5S ribosomal ribonucleic acid in flowering plants. Biochem J. 1979 Dec 1;183(3):595–604. doi: 10.1042/bj1830595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Erdmann V. A. Collection of published 5S and 5.8S RNA sequences and their precursors. Nucleic Acids Res. 1982 Jan 22;10(2):r93–115. doi: 10.1093/nar/10.2.762-c. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ford P. J., Brown R. D. Sequences of 5S ribosomal RNA from Xenopus mulleri and the evolution of 5S gene-coding sequences. Cell. 1976 Aug;8(4):485–493. doi: 10.1016/0092-8674(76)90216-6. [DOI] [PubMed] [Google Scholar]
  20. Forget B. G., Weissman S. M. The nucleotide sequence of ribosomal 5 S ribonucleic acid from KB cells. J Biol Chem. 1969 Jun 25;244(12):3148–3165. [PubMed] [Google Scholar]
  21. 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]
  22. Hinnebusch A. G., Klotz L. C., Blanken R. L., Loeblich A. R., 3rd An evaluation of the phylogenetic position of the dinoflagellate Crypthecodinium cohnii based on 5S rRNA characterization. J Mol Evol. 1981;17(6):334–337. doi: 10.1007/BF01734355. [DOI] [PubMed] [Google Scholar]
  23. Hori H., Osawa S., Iwabuchi M. The nucleotide sequence of 5S rRNA from a cellular slime mold Dictyostelium discoideum. Nucleic Acids Res. 1980 Dec 11;8(23):5535–5539. doi: 10.1093/nar/8.23.5535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hori H., Osawa S., Murao K., Ishikura H. The nucleotide sequence of 5S ribosomal RNA from Micrococcus lysodeikticus. Nucleic Acids Res. 1980 Nov 25;8(22):5423–5426. doi: 10.1093/nar/8.22.5423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hori H., Sawada M., Osawa S., Murao K., Ishikura H. The nucleotide sequence of 5S rRNA from Mycoplasma capricolum. Nucleic Acids Res. 1981 Oct 24;9(20):5407–5410. doi: 10.1093/nar/9.20.5407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kawata Y., Ishikawa H. Nucleotide sequence and thermal property of 5S rRNA from the elder aphid. Acyrthosiphon magnoliae. Nucleic Acids Res. 1982 Mar 25;10(6):1833–1840. doi: 10.1093/nar/10.6.1833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kay B. K., Gall J. G. 5S ribosomal RNA genes of the newt Notophthalmus viridescens. Nucleic Acids Res. 1981 Dec 11;9(23):6457–6469. doi: 10.1093/nar/9.23.6457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Komiya H., Kawakami M., Takemura S. Nucleotide sequence of 5S ribosomal RNA from the posterior silk glands of Bombyx mori. J Biochem. 1981 Mar;89(3):717–722. doi: 10.1093/oxfordjournals.jbchem.a133251. [DOI] [PubMed] [Google Scholar]
  29. Komiya H., Shimizu N., Kawakami M., Takemura S. Nucleotide sequence of 5S ribosomal RNA from Lingula anatina. A study on the molecular evolution of 5S ribosomal RNA from a living fossil. J Biochem. 1980 Nov;88(5):1449–1456. doi: 10.1093/oxfordjournals.jbchem.a133114. [DOI] [PubMed] [Google Scholar]
  30. Komiya H., Takemura S. The nucleotide sequence of 5S ribosomal RNA from slime mold Physarum polycephalum. J Biochem. 1981 Dec;90(6):1577–1581. doi: 10.1093/oxfordjournals.jbchem.a133631. [DOI] [PubMed] [Google Scholar]
  31. Kumagai I., Digweed M., Erdmann V. A., Watanabe K., Oshima T. The nucleotide sequence of 5S rRNA from an extreme thermophile, Thermus thermophilus HB8. Nucleic Acids Res. 1981 Oct 10;9(19):5159–5162. doi: 10.1093/nar/9.19.5159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Larrinúa I., Delihas N. Modification of the guanine in the invariant sequence 5' CCG44AAC3' of the Escherichia coli 5 S RNA in solution by kethoxal. FEBS Lett. 1979 Dec 1;108(1):181–184. doi: 10.1016/0014-5793(79)81205-3. [DOI] [PubMed] [Google Scholar]
  33. Lu A. L., Steege D. A., Stafford D. W. Nucleotide sequence of a 5S ribosomal RNA gene in the sea urchin Lytechinus variegatus. Nucleic Acids Res. 1980 Apr 25;8(8):1839–1853. doi: 10.1093/nar/8.8.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Luehrsen K. R., Fox G. E., Kilpatrick M. W., Walker R. T., Domdey H., Krupp G., Gross H. J. The nucleotide sequence of the 5S rRNA from the archaebacterium Thermoplasma acidophilum. Nucleic Acids Res. 1981 Feb 25;9(4):965–970. doi: 10.1093/nar/9.4.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Luehrsen K. R., Nicholson D. E., Eubanks D. C., Fox G. E. An archaebacterial 5S rRNA contains a long insertion sequence. Nature. 1981 Oct 29;293(5835):755–756. doi: 10.1038/293755a0. [DOI] [PubMed] [Google Scholar]
  37. MacKay R. M., Doolittle W. F. Nucleotide sequences of Acanthamoeba castellanii 5S and 5.8S ribosomal ribonucleic acids: phylogenetic and comparative structural analyses. Nucleic Acids Res. 1981 Jul 24;9(14):3321–3334. doi: 10.1093/nar/9.14.3321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. MacKay R. M., Gray M. W., Doolittle W. F. Nucleotide sequence of Crithidia fasciculata cytosol 5S ribosomal ribonucleic acid. Nucleic Acids Res. 1980 Nov 11;8(21):4911–4917. doi: 10.1093/nar/8.21.4911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mackay R. M., Spencer D. F., Doolittle W. F., Gray M. W. Nucleotide sequences of wheat-embryo cytosol 5-S and 5.8-S ribosomal ribonucleic acids. Eur J Biochem. 1980 Dec;112(3):561–576. doi: 10.1111/j.1432-1033.1980.tb06122.x. [DOI] [PubMed] [Google Scholar]
  40. Mao J., Appel B., Schaack J., Sharp S., Yamada H., Söll D. The 5S RNA genes of Schizosaccharomyces pombe. Nucleic Acids Res. 1982 Jan 22;10(2):487–500. doi: 10.1093/nar/10.2.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Marotta C. A., Varricchio F., Smith I., Weissman S. M. The primary structure of Bacillus subtilis and Bacillus stearothermophilus 5 S ribonucleic acids. J Biol Chem. 1976 May 25;251(10):3122–3127. [PubMed] [Google Scholar]
  42. Mashkova T. D., Serenkova T. I., Mazo A. M., Avdonina T. A., Timofeyeva MYa, Kisselev L. L. The primary structure of oocyte and somatic 5S rRNAs from the loach Misgurnus fossilis. Nucleic Acids Res. 1981 May 11;9(9):2141–2151. doi: 10.1093/nar/9.9.2141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Nazar R. N., Matheson A. T., Bellemare G. Nucleotide sequence of Halobacterium cutirubrum ribosomal 5 S ribonucleic acid. An altered secondary structure in halophilic organisms. J Biol Chem. 1978 Aug 10;253(15):5464–5469. [PubMed] [Google Scholar]
  44. Nazar R. N., Matheson A. T. Nucleotide sequence of Thermus aquaticus ribosomal 5 S ribonucleic acid. Sequence homologies in thermophilic organisms. J Biol Chem. 1977 Jun 25;252(12):4256–4261. [PubMed] [Google Scholar]
  45. Nishikawa K., Takemura S. Structure and function of 5S ribosomal ribonucleic acid from Torulopsis utilis. II. Partial digestion with ribonucleases and derivation of the complete sequence. J Biochem. 1974 Nov;76(5):935–947. [PubMed] [Google Scholar]
  46. Nishikawa K., Takemura S. Structure and function of 5S ribosomal ribonucleic acid from Torulopsis utilis. III. Detection of single-stranded regions by digestion with nuclease S1. J Biochem. 1977 Apr;81(4):995–1003. doi: 10.1093/oxfordjournals.jbchem.a131566. [DOI] [PubMed] [Google Scholar]
  47. Noller H. F., Garrett R. A. Structure of 5 S ribosomal RNA from Escherichia coli: identification of kethoxal-reactive sites in the A and B conformations. J Mol Biol. 1979 Aug 25;132(4):621–636. doi: 10.1016/0022-2836(79)90378-4. [DOI] [PubMed] [Google Scholar]
  48. Noller H. F., Herr W. Letters to the editor: Accessibility of 5 S RNA in 50 S ribosomal subunits. J Mol Biol. 1974 Nov 25;90(1):181–184. doi: 10.1016/0022-2836(74)90266-6. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Piechulla B., Hahn U., McLaughlin L. W., Küntzel H. Nucleotide sequence of 5S ribosomal RNA from Aspergillus nidulans and Neurospora crassa. Nucleic Acids Res. 1981 Mar 25;9(6):1445–1450. doi: 10.1093/nar/9.6.1445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Pribula C. D., Fox G. E., Woese C. R. Nucleotide sequence of Bacillus megaterium 5 S RNA. FEBS Lett. 1974 Aug 30;44(3):322–323. doi: 10.1016/0014-5793(74)81168-3. [DOI] [PubMed] [Google Scholar]
  52. Rabin D., Crothers D. M. Analysis of RNA secondary structure by photochemical reversal of psoralen crosslinks. Nucleic Acids Res. 1979 Oct 10;7(3):689–703. doi: 10.1093/nar/7.3.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Roy K. L. A proposed nucleotide sequence for the 5S ribosomal ribonucleic acid of rainbow trout (Salmo gairdneri). Can J Biochem. 1978 Jan;56(1):60–65. doi: 10.1139/o78-009. [DOI] [PubMed] [Google Scholar]
  54. Roy K. L., Enns L. Nucleotide sequence of 5 S ribosomal ribonucleic acid of Iguana iguana. J Biol Chem. 1976 Oct 25;251(20):6352–6354. [PubMed] [Google Scholar]
  55. Roy K. L. The nucleotide sequence of turtle (Terrapene carolina) 5 S ribosomal ribonucleic acid. FEBS Lett. 1977 Aug 15;80(2):266–270. doi: 10.1016/0014-5793(77)80454-7. [DOI] [PubMed] [Google Scholar]
  56. Selker E. U., Yanofsky C., Driftmier K., Metzenberg R. L., Alzner-DeWeerd B., RajBhandary U. L. Dispersed 5S RNA genes in N. crassa: structure, expression and evolution. Cell. 1981 Jun;24(3):819–828. doi: 10.1016/0092-8674(81)90107-0. [DOI] [PubMed] [Google Scholar]
  57. Sogin S. J., Sogin M. L., Woese C. R. Phylogenetic measurement in procaryotes by primary structural characterization. J Mol Evol. 1971;1(1):173–184. [PubMed] [Google Scholar]
  58. Spencer D. F., Bonen L., Gray M. W. Primary sequence of wheat mitochondrial 5S ribosomal ribonucleic acid: functional and evolutionary implications. Biochemistry. 1981 Jul 7;20(14):4022–4029. doi: 10.1021/bi00517a011. [DOI] [PubMed] [Google Scholar]
  59. Stahl D. A., Luehrsen K. R., Woese C. R., Pace N. R. An unusual 5S rRNA, from Sulfolobus acidocaldarius, and its implications for a general 5S rRNA structure. Nucleic Acids Res. 1981 Nov 25;9(22):6129–6137. doi: 10.1093/nar/9.22.6129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Studnicka G. M., Eiserling F. A., Lake J. A. A unique secondary folding pattern for 5S RNA corresponds to the lowest energy homologous secondary structure in 17 different prokaryotes. Nucleic Acids Res. 1981 Apr 24;9(8):1885–1904. doi: 10.1093/nar/9.8.1885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Tabata S. Structure of the 5-S ribosomal RNA gene and its adjacent regions in Torulopsis utilis. Eur J Biochem. 1980 Sep;110(1):107–114. doi: 10.1111/j.1432-1033.1980.tb04845.x. [DOI] [PubMed] [Google Scholar]
  62. Tinoco I., Jr, Uhlenbeck O. C., Levine M. D. Estimation of secondary structure in ribonucleic acids. Nature. 1971 Apr 9;230(5293):362–367. doi: 10.1038/230362a0. [DOI] [PubMed] [Google Scholar]
  63. Troutt A., Savin T. J., Curtiss W. C., Celentano J., Vournakis J. N. Secondary structure of Bombyx mori and Dictyostelium discoideum 5S rRNA from S1 nuclease and cobra venom ribonuclease susceptibility, and computer assisted analysis. Nucleic Acids Res. 1982 Jan 22;10(2):653–664. doi: 10.1093/nar/10.2.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Woese C. R., Luehrsen K. R., Pribula C. D., Fox G. E. Sequence characterization of 5S ribosomal RNA from eight gram positive procaryotes. J Mol Evol. 1976 Aug 3;8(2):143–153. doi: 10.1007/BF01739100. [DOI] [PubMed] [Google Scholar]
  65. Woese C. R., Magrum L. J., Fox G. E. Archaebacteria. J Mol Evol. 1978 Aug 2;11(3):245–251. doi: 10.1007/BF01734485. [DOI] [PubMed] [Google Scholar]
  66. Woese C. R., Pribula C. D., Fox G. E., Zablen L. B. The nucleotide sequence of the 5S ribosomal RNA from a photobacterium. J Mol Evol. 1975 Jun 9;5(1):35–46. doi: 10.1007/BF01732012. [DOI] [PubMed] [Google Scholar]
  67. 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]

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