Fine Structure of the Peptidyl Transferase Centre on 23 S-like rRNAs Deduced from Chemical Probing of Antibiotic-Ribosome Complexes

Journal of Molecular Biology

Volumn 247, Issue 2, 1995, Pages 224-235

  Rodriguez Fonseca, Cristina ^a,b   Amils, Ricardo ^a   Garrett, Roger A ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Antibiotics; Peptidyl transferase; Phylogeny; Ribosomes

Indexed keywords

ANISOMYCIN; ANTIBIOTIC AGENT; BLASTICIDIN S; BRUCEANTIN; CARBOMYCIN; CHLORAMPHENICOL; DALFOPRISTIN; NARCICLASINE; NUCLEOTIDE; PEPTIDYLTRANSFERASE; RIBOSOME PROTEIN; RIBOSOME RNA; T 2 TOXIN; TYLOSIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DRUG BINDING; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVE SITE; ENZYME INHIBITION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; RIBOSOME; RNA SEQUENCE; RNA STRUCTURE;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 0028924641     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1994.0135     Document Type: Article

References (64)

1. Aagaard, C., Phan, H., Trevisanato, S. & Garrett, R. A. (1994). A spontaneous point mutation in the single 23 S rRNA gene of the thermophilic archaeon Sulfolobus acidocaldarius conferring multiple drug resistance. J. Bacteriol. 176, 7744-7747.
2. Amils, R. & Sanz, J. L. (1986). Inhibitors of protein synthesis as phylogenetic markers. In Structure, Function and Genetics of Ribosomes (Hardesty B. & Kramer, G., eds), pp. 605-620, Springer, New York.
3. Amils, R., Ramirez, L., Sanz, J. L., Marin, I., Pisabarro, A. G. & Urena, D. (1989). The use of functional analysis of the ribosome as a tool to determine archaebacterial phylogeny Can. J. Microbiol. 35, 141-147.
4. Andersson, S. & Kurland, C. G. (1987). Elongating ribosomes in vivo are refractory to erythromycin. Biochimie, 69, 901-904.
5. Arevalo, M. A., Tejedor, F., Polo, F. & Ballesta, J. P. G. (1989). Synthesis and biological activity of photoactive derivatives of erythromycin. J. Med. Chem. 32, 2200-2204.
6. Bakin, A. & Ofengand, J. (1993). Four newly located pseudouridylate residues in Escherichia coli 23 S rRNA are all at the peptidyl transferase center: Analysis by the application of a new sequencing technique. Biochemistry, 32, 9754-9762.
7. Battaner, E. & Vazquez, D. (1971). Preparation of active 60 S and 40 S subunits from yeast ribosomes. Methods Enzymol. 20, 446-449.
8. Cammarano, P., Teichner, A., Londei, P., Acca, M., Nicolaus, B., Sanz, J. L. & Amils, R. (1985). Insensitivity of archaebacterial ribosomes to protein synthesis inhibitors. Evolutionary implications. EMBO J. 4, 811-816.
9. Celma, M. L., Monro, R. E. & Vazquez, D. (1970). Substrate and antibiotic binding sites at the peptidyl transferase centre of E. coli ribosomes. FEBS Letters, 6, 273-277.
10. Christiansen, J., Egebjerg, J., Larsen, N. & Garrett, R. A. (1990). Analysis of rRNA structure. Experimental and theoretical considerations. In Ribosomes and Protein Synthesis: A Practical Approach (Spedding, G., ed.), pp. 229-252, Oxford Univ. Press, Oxford.
11. Cundliffe, E. (1990). In The Ribosome: Structure, Function and Evolution (Hill, W. E., Dahlberg, A., Garrett, R. A., Moore, P. B., Schlessinger, D. & Warner, J. R., eds), pp. 479-490, Amer. Soc. Microbiol. Press, Washington, DC.
12. Cundliffe, E. & Thompson, J. (1981). Concerning the mode of action of micrococcin upon bacterial protein synthesis. Eur. J. Biochem. 118, 47-52.
13. Davies, J. (1990). What are antibiotics? Archaic functions for modern activities. Mol. Microbiol. 4, 1227-1232.
14. Douthwaite, S. (1992a). Functional interactions involving the peptidyl transferase center. J. Bacteriol. 174, 1333-1338.
15. Douthwaite, S. (1992b). Interaction of the antibiotics clindamycin and lincomycin with Escherichia coli 23 S rRNA. Nucl. Acids Res. 20, 4717-4720.
16. Douthwaite, S. & Aagaard, C. (1993). Erythromycin binding is reduced in ribosomes with conformational alterations in the 23 S rRNA peptidyl transferase loop. J. Mol. Biol. 232, 725-737.
17. Egebjerg, J. & Garrett, R. A. (1991). Binding sites of the antibiotics pactamycin and celesticetin on rRNAs. Biochimie, 73, 1145-1149.
18. Egebjerg, J., Douthwaite, S. & Garrett, R. A. (1989). Antibiotic interactions at the GTPase-associated centre within Escherichia coli 23 S rRNA. EMBO J. 8, 607-611.
19. Egebjerg, J., Larsen, N. & Garrett, R. A. (1990). Structural map of 23 S rRNA. In The Ribosome: Structure, Function and Evolution (Hill, W. E., Dahlberg, A., Garrett, R. A., Moore, P. B., Schlessinger, D. & Warner, J. R., eds), pp. 168-179, Amer. Soc. Microbiol. Press, Washington DC.
20. Endo, Y., Gluck, A., Chan, Y-L., Tsurugi, K. & Wool, I. G. (1990) RNA-protein interaction. J. Biol. Chem. 265, 2216-2222.
21. Fernandez-Munoz, R., Monro, R. E., Torres-Pinedo, R. & Vazquez, D. (1971) Substrate and antibiotic-binding sites at the peptidyl-transferase centre of Escherichia coli ribosomes. Eur. J. Biochem. 23, 185-193.
22. Gale, E. F., Cundliffe, E., Reynolds, P. E., Richmond, M. H. & Waring, M. J. (1981). In The Molecular Basis of Antibiotic Action, pp. 402-547, John Wiley and Sons, London.
23. Garrett, R. A. & Rodriguez-Fonseca, C. (1995). The peptidyl transferase center. In Ribosomal RNA: Structure, Evolution, Processing and Function, (Zimmermann, R. A. & Dahlberg, A., eds), CRC Press, Boca Raton Florida in the press.
24. Glück, A., Endo, Y. & Wool, I. G. (1992). rRNA identify elements for ricin A-chain recognition and catalysis: Analysis with tetraloop mutants. J. Mol. Biol. 226, 411-426.
25. Hardesty B., Odom, O. W. & Deng, H.-Y (1986). The movement of tRNA through the ribosome during peptide elongation: the displacement reaction model. In Structure, Function and Genetics of Ribosomes, (Hardesty, B. & Kramer, G., eds), pp. 495-508, Springer Press, New York.
26. Hornig, H., Woolley P. & Luhrmann, R. (1987). Decoding at the ribosomal A-site: Antibiotics, misreading and energy of aminoacyl-tRNA binding. Biochimie, 69, 803-813.
27. Hummel, H. & Bock, A. (1987). 23 S rRNA mutations in halobacteria conferring resistance to the anti-80S ribosome targeted antibiotic anisomycin. Nucl. Acids Res. 15, 2431-2443.
28. Konishita, T., Tanaka, N. & Umezawa, H. (1970). Binding of blasticidin S to ribosomes. J. Antibiot. 23, 288-290.
29. Larsen, N. (1992). Higher order interactions in 23 S rRNAs. Proc. Nat. Acad. Sci, U.S.A. 89, 5044-5048.
30. Leviev, I. G., Rodriguez-Fonseca, C., Phan, H., Garrett, R. A., Heilek, G., Noller, H. F. & Mankin, A. S. (1994). A conserved secondary structural motif in 23 S rRNA defines the site of interaction of amicetin, a universal inhibitor of peptide bond formation. EMBO J. 13, 1682-1686.
31. Maden, E. (1989). The numerous modified nucleotides in eukaryotic rRNA. Prog. Nucl. Acids Res. Mol. Biol. 39, 241-303.
32. Mankin, A. S. & Garrett, R. A. (1991). Chloramphenicol resistance mutations in the single 23 S rRNA gene of the archaeon Halobacterium halobium. J. Bacteriol. 173, 3559-3563.
33. Mankin, A. S. & Kagramanova, V. K. (1986). Complete nucleotide sequence of the single rRNA operon of Halobacterium halobium; secondary structure of the archaebacterial 23 S rRNA. Mol. Gen. Genet. 202, 152-161.
34. Mitchell, P., Osswald, M., Schueler, D. & Brimacombe, R. (1990). 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 23 S RNA. Nucl. Acids Res. 18, 4325-4333.
35. Mitchell, P., Stade, K., Osswald, M. & Brimacombe, R. (1993). 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. Nucl. Acids Res. 21, 887-896.
36. Moazed, D. & Noller, H. F. (1987a). Interaction of antibiotics with functional sites in 16 S rRNA. Nature (London), 327, 389-394.
37. Moazed, D. & Noller, H. F. (1987b). Chloramphenicol, erythromycin, carbomycin and vernamycin B protect overlapping sites in the peptidyl transferase region of 23 S rRNA. Biochimie, 69, 879-884.
38. Moazed, D. & Noller, H. F. (1989a). Interaction of tRNA with 23 S rRNA in the ribosomal A, P, and E sites. Cell, 57, 585-597.
39. Moazed, D. & Noller, H. F. (1989b). Intermediate states in the movement of transfer RNA in the ribosome. Nature (London), 342, 142-148.
40. Moazed, D. & Noller, H. F. (1991) Sites of interaction of the CCA end of peptidyl-tRNA with 23 S rRNA. Proc. Nat. Acad. Sci., U.S.A. 88, 3725-3728.
41. Moazed, D., Robertson, J. M. & Noller, H. F. (1988). Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23 S rRNA. Nature (London), 334, 362-364.
42. Nierhaus, K. H. (1993). Solution of the ribosome riddle: how the ribosome selects the correct aminoacyl-tRNA out of 41 similar contestants. Mol. Microbiol. 9, 661-669.
43. Noller, H. F. (1991). Ribosomal RNA and translation. Annu. Rev. Biochem. 60, 191-227.
44. Odom, O. W. & Hardesty B. (1992). Use of 50 S-binding antibiotics to characterize the ribosomal site to which peptidyl-tRNA is bound. J. Biol. Chem. 267, 19117-19122.
45. Odom, O. W., Picking, W. D. & Hardesty B. (1990). Movement of tRNA but not the nascent peptide during peptide bond formation on ribosomes. Biochemistry, 29, 10734-10744.
46. Pestka, S. (1977). In Molecular Mechanisms of Protein Biosynthesis (Weissbach, H. & Pestka, S., eds), pp. 467-553, Academic Press, New York.
47. Picking, W. D., Odom, O. W. & Hardesty B. (1992). Evidence for RNA in the peptide transferase center of Escherichia coli ribosomes as indicated by fluorescence. Biochemistry, 31, 12565-12570.
48. Powers, T. & Noller, H. F. (1993). Evidence for a functional interaction between EF-Tu and 16 S rRNA. Proc. Nat. Acad. Sci, U.S.A. 90, 1364-1368.
49. Ryabova, L. A., Selivanova, O. M., Baranov, V. I., Vasiliev, V. D. & Spirin, A. S. (1988). Does the channel for the nascent peptide exist inside the ribosome? FEBS Letters, 26, 255-260.
50. 4+ dependent protein synthesis cell-free system for halobacteria. Biochemistry, 27, 8194-8199.
51. Sanz, J. L., Marin, D., Urefla, D. & Amils, R. (1993). Functional analysis of seven ribosomal systems from extreme halophilic archaea. Can. J. Microbiol. 39, 311-317.
52. Skinner, R., Cundliffe, E. & Schmidt, F. J. (1983). Site of action of a rRNA methylase responsible for resistance to erythromycin and other antibiotics. J. Biol. Chem. 258, 12702-12706.
53. Smith, J. E., Cooperman, B. S. & Mitchell, P. (1992). Methylation sites in Escherichia coli rRNA: localization and identification of four new sites of methylation in 23 S rRNA. Biochemistry, 31, 10825-10834.
54. Staehelin, T. & Maglott, D. (1971). Preparation of Escherichia coli ribosomal subunits active in polypeptide synthesis. Methods Enzymol. 20, 449-456.
55. Steiner, G., Kuechler, E. & Barta, A. (1988). 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. 7, 3949-3955.
56. Symons, R. H., Harris, R. J., Greenwell, P, Eckermann, D. J. & Vanin, E. F. (1978). The use of puromycin analogs and related compounds to probe the active centre of peptidyl transferase on Escherichia coli ribosomes. Bioorg. Chem. (Suppl.), 4, 409-436.
57. Vannuffel, P, Di Giambattista, M. & Cocito, C. (1992). ldentification of a single base change in rRNA leading to erythromycin resistance. J. Biol. Chem. 267, 16114-16120.
58. Vazquez, D. (1979). In Inhibitors of Protein Synthesis, Springer Verlag, New York.
59. Veldman, G. M., Klootwijk, J., de Regt, V. C. H. F., Planta, R. J., Branlant, C., Krol, A. & Ebel, J. P (1981). The primary and secondary structure of yeast 26 S rRNA. Nucl. Acids Res. 9, 6935-6952.
60. Vester, B. & Garrett, R. A. (1987). A plasmid-coded and site-directed mutation in Escherichia coli 23 S RNA that confers resistance to erythromycin: implications for the mechanism of action of erythromycin. Biochimie, 69, 891-900.
61. Vester, B. & Garrett, R. A. (1988). The importance of highly conserved nucleotides in the binding region of chloramphenicol at the peptidyl transfer centre of Escherichia coli 23 S rRNA. EMBO J. 7, 3577-3587.
62. Woodcock, J., Moazed, D., Cannon, M., Davies, J. & Noller, H. F. (1991). Interaction of antibiotics with A and P-site-specific bases in 16 S rRNA. EMBO J. 10, 3099-3103.
63. Phederivatives containing azidoadenosine at the 3’-end of the acceptor arm: A model of the tRNA-ribosome complex. Proc. Nat. Acad. Sci., U.S.A. 86, 5232-5236.
64. Zalacain, M. & Cundliffe, E. (1989). Cloning of tlrD, a fourth resistance gene from the tylosin producer, Streptomyces frediae. Gene, 97, 137-142.