Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1997 Mar 15;25(6):1254–1264. doi: 10.1093/nar/25.6.1254

Transfer RNA docking pair model in the ribosomal pre- and post-translocational states.

K Nagano 1, N Nagano 1
PMCID: PMC146551  PMID: 9092637

Abstract

A consensus has been reached that the conformation of the anticodon-codon interactions of two adjacent tRNA molecules on the ribosome is a Sundaralingam-type (S-type). Even if it is kept to the S-type, there are still various possibilities. Various experimental data have been supporting an idea that the conformation of A-site tRNA is different from that of P-site tRNA. Those data as well as the recent result of Brimacombe and co-workers that U20:1 of lupin tRNAmMetbound to the A-site was cross-linked to a region, 875-905, of 23S rRNA in combination with the other recent findings of Nierhaus and co-workers about the spin-contrast method of neutron diffraction of the ribosome and the better accessible nucleotide patterns of phosphorothioated tRNAs on the ribosome have led to a new tRNA docking pair model, in which the highly conserved G18 and G19 of D-loop in A-site tRNA and C56 and C61 of TpsiC-loop in P-site tRNA base pair along with the conventional base pairs of adjacent codon-anticodon interactions. This A-P tRNA pair model can be translocated to the P-E tRNA pair model without changing the conformation except the ACCA termini, keeping the position of the growing nascent polypeptide chain.

Full Text

The Full Text of this article is available as a PDF (607.4 KB).

Selected References

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

  1. Abdurashidova G. G., Tsvetkova E. A., Budowsky E. I. Determination of tRNA nucleotide residues directly interacting with proteins in the post- and pretranslocated ribosomal complexes. FEBS Lett. 1990 Sep 3;269(2):398–401. doi: 10.1016/0014-5793(90)81202-y. [DOI] [PubMed] [Google Scholar]
  2. Abdurashidova G. G., Tsvetkova E. A., Budowsky E. I. Nucleotide residues of tRNA, directly interacting with proteins within the complex of the 30 S subunit of E. coli ribosome with poly(U) and NAcPhe-tRNA(Phe). FEBS Lett. 1989 Jan 30;243(2):299–302. doi: 10.1016/0014-5793(89)80149-8. [DOI] [PubMed] [Google Scholar]
  3. Agrawal R. K., Penczek P., Grassucci R. A., Li Y., Leith A., Nierhaus K. H., Frank J. Direct visualization of A-, P-, and E-site transfer RNAs in the Escherichia coli ribosome. Science. 1996 Feb 16;271(5251):1000–1002. doi: 10.1126/science.271.5251.1000. [DOI] [PubMed] [Google Scholar]
  4. Beauclerk A. A., Cundliffe E. The binding site for ribosomal protein L2 within 23S ribosomal RNA of Escherichia coli. EMBO J. 1988 Nov;7(11):3589–3594. doi: 10.1002/j.1460-2075.1988.tb03236.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bertram S., Göringer U., Wagner R. Structural investigation of Phe-tRNAPhe from E.coli bound to the ribosomal A-site. Nucleic Acids Res. 1983 Feb 11;11(3):575–589. doi: 10.1093/nar/11.3.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Biou V., Yaremchuk A., Tukalo M., Cusack S. The 2.9 A crystal structure of T. thermophilus seryl-tRNA synthetase complexed with tRNA(Ser). Science. 1994 Mar 11;263(5152):1404–1410. doi: 10.1126/science.8128220. [DOI] [PubMed] [Google Scholar]
  7. Brimacombe R. The structure of ribosomal RNA: a three-dimensional jigsaw puzzle. Eur J Biochem. 1995 Jun 1;230(2):365–383. [PubMed] [Google Scholar]
  8. Dauber-Osguthorpe P., Roberts V. A., Osguthorpe D. J., Wolff J., Genest M., Hagler A. T. Structure and energetics of ligand binding to proteins: Escherichia coli dihydrofolate reductase-trimethoprim, a drug-receptor system. Proteins. 1988;4(1):31–47. doi: 10.1002/prot.340040106. [DOI] [PubMed] [Google Scholar]
  9. Easterwood T. R., Major F., Malhotra A., Harvey S. C. Orientations of transfer RNA in the ribosomal A and P sites. Nucleic Acids Res. 1994 Sep 11;22(18):3779–3786. doi: 10.1093/nar/22.18.3779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Frank J., Zhu J., Penczek P., Li Y., Srivastava S., Verschoor A., Radermacher M., Grassucci R., Lata R. K., Agrawal R. K. A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature. 1995 Aug 3;376(6539):441–444. doi: 10.1038/376441a0. [DOI] [PubMed] [Google Scholar]
  11. Gauss D. H., Sprinzl M. Compilation of tRNA sequences. Nucleic Acids Res. 1981 Jan 10;9(1):r1–23. [PMC free article] [PubMed] [Google Scholar]
  12. Gautheret D., Damberger S. H., Gutell R. R. Identification of base-triples in RNA using comparative sequence analysis. J Mol Biol. 1995 Apr 21;248(1):27–43. doi: 10.1006/jmbi.1995.0200. [DOI] [PubMed] [Google Scholar]
  13. Geigenmüller U., Nierhaus K. H. Significance of the third tRNA binding site, the E site, on E. coli ribosomes for the accuracy of translation: an occupied E site prevents the binding of non-cognate aminoacyl-tRNA to the A site. EMBO J. 1990 Dec;9(13):4527–4533. doi: 10.1002/j.1460-2075.1990.tb07904.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Giri L., Hill W. E., Wittmann H. G., Wittmann-Liebold B. Ribosomal proteins: their structure and spatial arrangement in prokaryotic ribosomes. Adv Protein Chem. 1984;36:1–78. doi: 10.1016/s0065-3233(08)60295-8. [DOI] [PubMed] [Google Scholar]
  15. Holbrook S. R., Sussman J. L., Warrant R. W., Kim S. H. Crystal structure of yeast phenylalanine transfer RNA. II. Structural features and functional implications. J Mol Biol. 1978 Aug 25;123(4):631–660. doi: 10.1016/0022-2836(78)90210-3. [DOI] [PubMed] [Google Scholar]
  16. Jack A., Ladner J. E., Klug A. Crystallographic refinement of yeast phenylalanine transfer RNA at 2-5A resolution. J Mol Biol. 1976 Dec 25;108(4):619–649. doi: 10.1016/s0022-2836(76)80109-x. [DOI] [PubMed] [Google Scholar]
  17. Johnson A. E., Adkins H. J., Matthews E. A., Cantor C. R. Distance moved by transfer RNA during translocation from the A site to the P site on the ribosome. J Mol Biol. 1982 Mar 25;156(1):113–140. doi: 10.1016/0022-2836(82)90462-4. [DOI] [PubMed] [Google Scholar]
  18. Jørgensen T., Siboska G. E., Wikman F. P., Clark B. F. Different conformations of tRNA in the ribosomal P-site and A-site. Eur J Biochem. 1985 Nov 15;153(1):203–209. doi: 10.1111/j.1432-1033.1985.tb09287.x. [DOI] [PubMed] [Google Scholar]
  19. Lim V., Venclovas C., Spirin A., Brimacombe R., Mitchell P., Müller F. How are tRNAs and mRNA arranged in the ribosome? An attempt to correlate the stereochemistry of the tRNA-mRNA interaction with constraints imposed by the ribosomal topography. Nucleic Acids Res. 1992 Jun 11;20(11):2627–2637. doi: 10.1093/nar/20.11.2627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lin F. L., Kahan L., Ofengand J. Crosslinking of phenylalanyl-tRNA to the ribosomal A site via a photoaffinity probe attached to the 4-thiouridine residue is exclusively to ribosomal protein S19. J Mol Biol. 1984 Jan 5;172(1):77–86. doi: 10.1016/0022-2836(84)90415-7. [DOI] [PubMed] [Google Scholar]
  21. McDonald J. J., Rein R. A stereochemical model of the transpeptidation complex. J Biomol Struct Dyn. 1987 Apr;4(5):729–744. doi: 10.1080/07391102.1987.10507675. [DOI] [PubMed] [Google Scholar]
  22. Mitchell P., Osswald M., Brimacombe R. Identification of intermolecular RNA cross-links at the subunit interface of the Escherichia coli ribosome. Biochemistry. 1992 Mar 24;31(11):3004–3011. doi: 10.1021/bi00126a023. [DOI] [PubMed] [Google Scholar]
  23. Mitchell P., Osswald M., Schueler D., Brimacombe R. Selective isolation and detailed analysis of intra-RNA cross-links induced in the large ribosomal subunit of E. coli: a model for the tertiary structure of the tRNA binding domain in 23S RNA. Nucleic Acids Res. 1990 Aug 11;18(15):4325–4333. doi: 10.1093/nar/18.15.4325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mitchell P., Stade K., Osswald M., Brimacombe R. Site-directed cross-linking studies on the E. coli tRNA-ribosome complex: determination of sites labelled with an aromatic azide attached to the variable loop or aminoacyl group of tRNA. Nucleic Acids Res. 1993 Feb 25;21(4):887–896. doi: 10.1093/nar/21.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mueller F., Döring T., Erdemir T., Greuer B., Jünke N., Osswald M., Rinke-Appel J., Stade K., Thamm S., Brimacombe R. Getting closer to an understanding of the three-dimensional structure of ribosomal RNA. Biochem Cell Biol. 1995 Nov-Dec;73(11-12):767–773. doi: 10.1139/o95-085. [DOI] [PubMed] [Google Scholar]
  26. Nagano K., Harel M. Approaches to a three-dimensional model of E. coli ribosome. Prog Biophys Mol Biol. 1986;48(2):67–101. doi: 10.1016/0079-6107(86)90001-5. [DOI] [PubMed] [Google Scholar]
  27. Nagano K., Harel M., Takezawa M. Prediction of three-dimensional structure of Escherichia coli ribosomal RNA. J Theor Biol. 1988 Sep 17;134(2):199–256. doi: 10.1016/s0022-5193(88)80202-9. [DOI] [PubMed] [Google Scholar]
  28. Nagano K., Takagi H., Harel M. The side-by-side model of two tRNA molecules allowing the alpha-helical conformation of the nascent polypeptide during the ribosomal transpeptidation. Biochimie. 1991 Jul-Aug;73(7-8):947–960. doi: 10.1016/0300-9084(91)90136-o. [DOI] [PubMed] [Google Scholar]
  29. Nierhaus K. H., Beyer D., Dabrowski M., Schäfer M. A., Spahn C. M., Wadzack J., Bittner J. U., Burkhardt N., Diedrich G., Jünemann R. The elongating ribosome: structural and functional aspects. Biochem Cell Biol. 1995 Nov-Dec;73(11-12):1011–1021. doi: 10.1139/o95-108. [DOI] [PubMed] [Google Scholar]
  30. Osawa S., Jukes T. H., Watanabe K., Muto A. Recent evidence for evolution of the genetic code. Microbiol Rev. 1992 Mar;56(1):229–264. doi: 10.1128/mr.56.1.229-264.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Osswald M., Döring T., Brimacombe R. The ribosomal neighbourhood of the central fold of tRNA: cross-links from position 47 of tRNA located at the A, P or E site. Nucleic Acids Res. 1995 Nov 25;23(22):4635–4641. doi: 10.1093/nar/23.22.4635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Paulsen H., Robertson J. M., Wintermeyer W. Topological arrangement of two transfer RNAs on the ribosome. Fluorescence energy transfer measurements between A and P site-bound tRNAphe. J Mol Biol. 1983 Jun 25;167(2):411–426. doi: 10.1016/s0022-2836(83)80342-8. [DOI] [PubMed] [Google Scholar]
  33. Podkowinski J., Gornicki P. Neighbourhood of the central fold of the tRNA molecule bound to the E. coli ribosome--affinity labeling studies with modified tRNAs carrying photoreactive probes attached to the dihydrouridine loop. Nucleic Acids Res. 1991 Feb 25;19(4):801–808. doi: 10.1093/nar/19.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Podkowiński J., Górnicki P. Ribosomal proteins S7 and L1 are located close to the decoding site of E. coli ribosome--affinity labeling studies with modified tRNAs carrying photoreactive probes attached adjacent to the 3'-end of the anticodon. Nucleic Acids Res. 1989 Nov 11;17(21):8767–8782. doi: 10.1093/nar/17.21.8767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Prince J. B., Taylor B. H., Thurlow D. L., Ofengand J., Zimmermann R. A. Covalent crosslinking of tRNA1Val to 16S RNA at the ribosomal P site: identification of crosslinked residues. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5450–5454. doi: 10.1073/pnas.79.18.5450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rinke-Appel J., Jünke N., Osswald M., Brimacombe R. The ribosomal environment of tRNA: crosslinks to rRNA from positions 8 and 20:1 in the central fold of tRNA located at the A, P, or E site. RNA. 1995 Dec;1(10):1018–1028. [PMC free article] [PubMed] [Google Scholar]
  37. Santos M. A., Keith G., Tuite M. F. Non-standard translational events in Candida albicans mediated by an unusual seryl-tRNA with a 5'-CAG-3' (leucine) anticodon. EMBO J. 1993 Feb;12(2):607–616. doi: 10.1002/j.1460-2075.1993.tb05693.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Singhal R. P., Fallis P. A. Structure, function, and evolution of transfer RNAs (with appendix giving complete sequences of 178 tRNAs). Prog Nucleic Acid Res Mol Biol. 1979;23:227–290. doi: 10.1016/s0079-6603(08)60135-x. [DOI] [PubMed] [Google Scholar]
  39. Stade K., Riens S., Bochkariov D., Brimacombe R. Contacts between the growing peptide chain and the 23S RNA in the 50S ribosomal subunit. Nucleic Acids Res. 1994 Apr 25;22(8):1394–1399. doi: 10.1093/nar/22.8.1394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Stark H., Mueller F., Orlova E. V., Schatz M., Dube P., Erdemir T., Zemlin F., Brimacombe R., van Heel M. The 70S Escherichia coli ribosome at 23 A resolution: fitting the ribosomal RNA. Structure. 1995 Aug 15;3(8):815–821. doi: 10.1016/s0969-2126(01)00216-7. [DOI] [PubMed] [Google Scholar]
  41. Steinberg S., Misch A., Sprinzl M. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1993 Jul 1;21(13):3011–3015. doi: 10.1093/nar/21.13.3011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Steiner G., Kuechler E., Barta A. Photo-affinity labelling at the peptidyl transferase centre reveals two different positions for the A- and P-sites in domain V of 23S rRNA. EMBO J. 1988 Dec 1;7(12):3949–3955. doi: 10.1002/j.1460-2075.1988.tb03281.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stout C. D., Mizuno H., Rubin J., Brennan T., Rao S. T., Sundaralingam M. Atomic coordinates and molecular conformation of yeast phenylalanyl tRNA. An independent investigation. Nucleic Acids Res. 1976 Apr;3(4):1111–1123. doi: 10.1093/nar/3.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sussman J. L., Holbrook S. R., Warrant R. W., Church G. M., Kim S. H. Crystal structure of yeast phenylalanine transfer RNA. I. Crystallographic refinement. J Mol Biol. 1978 Aug 25;123(4):607–630. doi: 10.1016/0022-2836(78)90209-7. [DOI] [PubMed] [Google Scholar]
  45. Sylvers L. A., Kopylov A. M., Wower J., Hixson S. S., Zimmermann R. A. Photochemical cross-linking of the anticodon loop of yeast tRNA(Phe) to 30S-subunit protein S7 at the ribosomal A and P sites. Biochimie. 1992 Apr;74(4):381–389. doi: 10.1016/0300-9084(92)90116-v. [DOI] [PubMed] [Google Scholar]
  46. Traub W., Sussman J. L. Adenine-guanine base pairing ribosomal RNA. Nucleic Acids Res. 1982 Apr 24;10(8):2701–2708. doi: 10.1093/nar/10.8.2701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Woo N. H., Roe B. A., Rich A. Three-dimensional structure of Escherichia coli initiator tRNAfMet. Nature. 1980 Jul 24;286(5771):346–351. doi: 10.1038/286346a0. [DOI] [PubMed] [Google Scholar]
  49. Wower J., Hixson S. S., Zimmermann R. A. Labeling the peptidyltransferase center of the Escherichia coli ribosome with photoreactive tRNA(Phe) derivatives containing azidoadenosine at the 3' end of the acceptor arm: a model of the tRNA-ribosome complex. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5232–5236. doi: 10.1073/pnas.86.14.5232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wower J., Hixson S. S., Zimmermann R. A. Photochemical cross-linking of yeast tRNA(Phe) containing 8-azidoadenosine at positions 73 and 76 to the Escherichia coli ribosome. Biochemistry. 1988 Oct 18;27(21):8114–8121. doi: 10.1021/bi00421a021. [DOI] [PubMed] [Google Scholar]
  51. Wower J., Malloy T. A., 4th, Hixson S. S., Zimmermann R. A. Probing tRNA binding sites on the Escherichia coli 30 S ribosomal subunit with photoreactive analogs of the anticodon arm. Biochim Biophys Acta. 1990 Aug 27;1050(1-3):38–44. doi: 10.1016/0167-4781(90)90138-r. [DOI] [PubMed] [Google Scholar]
  52. Wower J., Scheffer P., Sylvers L. A., Wintermeyer W., Zimmermann R. A. Topography of the E site on the Escherichia coli ribosome. EMBO J. 1993 Feb;12(2):617–623. doi: 10.1002/j.1460-2075.1993.tb05694.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wower J., Scheffer P., Sylvers L. A., Wintermeyer W., Zimmermann R. A. Topography of the E site on the Escherichia coli ribosome. EMBO J. 1993 Feb;12(2):617–623. doi: 10.1002/j.1460-2075.1993.tb05694.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Wower J., Wower I. K., Kirillov S. V., Rosen K. V., Hixson S. S., Zimmermann R. A. Peptidyl transferase and beyond. Biochem Cell Biol. 1995 Nov-Dec;73(11-12):1041–1047. doi: 10.1139/o95-111. [DOI] [PubMed] [Google Scholar]
  55. Wower J., Zimmermann R. A. A consonant model of the tRNA-ribosome complex during the elongation cycle of translation. Biochimie. 1991 Jul-Aug;73(7-8):961–969. doi: 10.1016/0300-9084(91)90137-p. [DOI] [PubMed] [Google Scholar]
  56. Wyckoff H. W., Tsernoglou D., Hanson A. W., Knox J. R., Lee B., Richards F. M. The three-dimensional structure of ribonuclease-S. Interpretation of an electron density map at a nominal resolution of 2 A. J Biol Chem. 1970 Jan 25;245(2):305–328. [PubMed] [Google Scholar]
  57. Yamada Y., Ishikura H. Nucleotide sequence of tRNA(Ser)(3) from Escherichia coli. FEBS Lett. 1973 Feb 1;29(3):231–234. doi: 10.1016/0014-5793(73)80026-2. [DOI] [PubMed] [Google Scholar]
  58. Yokogawa T., Suzuki T., Ueda T., Mori M., Ohama T., Kuchino Y., Yoshinari S., Motoki I., Nishikawa K., Osawa S. Serine tRNA complementary to the nonuniversal serine codon CUG in Candida cylindracea: evolutionary implications. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7408–7411. doi: 10.1073/pnas.89.16.7408. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES