The structural basis of macrolide-ribosome binding assessed using mutagenesis of 23 S rRNA positions 2058 and 2059

Journal of Molecular Biology

Volumn 342, Issue 5, 2004, Pages 1569-1581

  Pfister, Peter ^a   Jenni, Simon ^b   Poehlsgaard, Jacob ^c   Thomas, Ashley ^a   Douthwaite, Stephen ^c   Ban, Nenad ^b   Böttger, Erik C ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

23 S rRNA mutants; macrolides; peptide tunnel; ribosome

Indexed keywords

11 AMINO 11 DEOXY 5 O DESOSAMINYL 3 OXO 6 O [3 (3 QUINOLYL)ALLYL] ERYTHRONOLIDE A 11,12 CYCLIC CARBAMATE; AZITHROMYCIN; BACTERIAL PROTEIN; BACTERIAL RNA; CARBOMYCIN; CETHROMYCIN; CLARITHROMYCIN; ERYTHROMYCIN; MACROLIDE; PEPTIDE; PROTEIN SUBUNIT; RNA 23S; ROXITHROMYCIN; SPIRAMYCIN; TELITHROMYCIN; TROLEANDOMYCIN; TYLOSIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANTIMICROBIAL ACTIVITY; ARTICLE; CRYSTAL STRUCTURE; DRUG BINDING SITE; DRUG CONFORMATION; DRUG DETERMINATION; DRUG PROTEIN BINDING; GENE MUTATION; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RIBOSOME SUBUNIT; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS;

ARCHAEA; BACTERIA (MICROORGANISMS); MYCOBACTERIUM; MYCOBACTERIUM SMEGMATIS;

EID: 4444300505     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.095     Document Type: Article

References (45)

1. D. Vázquez Inhibitors of Protein Synthesis 1979 Springer Berlin
2. E.F. Gale, E. Cundliffe, P.E. Reynolds, M.H. Richmond, and M.J. Waring The Molecular Basis of Antibiotic Action 1981 Wiley London
3. T. Tenson, M. Lovmar, and M. Ehrenberg The mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome J. Mol. Biol. 330 2003 1005 1014
4. A.J. Bryskier, J.P. Butzler, H.C. Neu, and P.M. Tulkens Macrolides: Chemistry, Pharmacology and Clinical Uses 1993 Arnette Blackwell Paris
5. A. Bryskier Ketolides-telithromycin, an example of a new class of antibacterial agents Clin. Microbiol. Infect. 6 2000 661 669
6. V.D. Shortridge, P. Zhong, Z. Cao, J.M. Beyer, L.S. Almer, and N.C. Ramer Comparison of in vitro activities of ABT-773 and telithromycin against macrolide-susceptible and -resistant streptococci and staphylococci Antimicrob. Agents Chemother. 46 2002 783 786
7. C.S. Shain, and G.W. Amsden Telithromycin: the first of the ketolides Ann. Pharmacother. 36 2002 452 464
8. J. Jalava, J. Kataja, H. Seppala, and P. Huovinen In vitro activities of the novel ketolide telithromycin (HMR 3647) against erythromycin-resistant Streptococcus species Antimicrob. Agents Chemother. 45 2001 789 793
9. D.J. Farrell, I. Morrissey, S. Bakker, and D. Felmingham Molecular characterization of macrolide resistance mechanisms among Streptococcus pneumoniae and Streptococcus pyogenes isolated from the PROTEKT 1999-2000 study J. Antimicrob. Chemother. 50 2002 39 47
10. R. Leclercq Overcoming antimicrobial resistance: profile of a new ketolide antibacterial, telithromycin J. Antimicrob. Chemother. 48 2001 9 23
11. D. Moazed, and H.F. Noller Chloramphenicol, erythromycin, carbomycin and vernamycin B protect overlapping sites in the peptidyl transferase region of 23 S ribosomal RNA Biochimie 69 1987 879 884
12. C. Rodriguez-Fonseca, R. Amils, and R.A. Garrett Fine structure of the peptidyl transferase centre on 23 S-like rRNAs deduced from chemical probing of antibiotic-ribosome complexes J. Mol. Biol. 247 1995 224 235
13. L. Xiong, S. Shah, P. Mauvais, and A.S. Mankin A ketolide resistance mutation in domain II of 23 S rRNA reveals the proximity of hairpin 35 to the peptidyl transferase centre Mol. Microbiol. 31 1999 633 639
14. L.H. Hansen, P. Mauvais, and S. Douthwaite The macrolide-ketolide antibiotic binding site is formed by structures in domains II and V of 23 S ribosomal RNA Mol. Microbiol. 31 1999 623 631
15. S.M. Poulsen, C. Kofoed, and B. Vester Inhibition of the ribosomal peptidyl transferase reaction by the mycarose moiety of the antibiotics carbomycin, spiramycin and tylosin J. Mol. Biol. 304 2000 471 481
16. F. Schlunzen, R. Zarivach, J. Harms, A. Bashan, A. Tocilj, and R. Albrecht Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria Nature 413 2001 814 821
17. J.L. Hansen, J.A. Ippolito, N. Ban, P. Nissen, P.B. Moore, and T.A. Steitz The structures of four macrolide antibiotics bound to the large ribosomal subunit Mol. Cell 10 2002 117 128
18. F. Schlunzen, J.M. Harms, F. Franceschi, H.A. Hansen, H. Bartels, R. Zarivach, and A. Yonath Structural basis for the antibiotic activity of ketolides and azalides Structure (Camb) 11 2003 329 338
19. R. Berisio, J. Harms, F. Schluenzen, R. Zarivach, H.A. Hansen, P. Fucini, and A. Yonath Structural insight into the antibiotic action of telithromycin against resistant mutants J. Bacteriol. 185 2003 4276 4279
20. R. Berisio, F. Schluenzen, J. Harms, A. Bashan, T. Auerbach, D. Baram, and A. Yonath Structural insight into the role of the ribosomal tunnel in cellular regulation Nature Struct. Biol. 10 2003 366 370
21. A. Yonath Structural insight into functional aspects of ribosomal RNA targeting Chembiochem. 4 2003 1008 1017
22. E.C. Böttger, B. Springer, T. Prammananan, Y. Kidan, and P. Sander Structural basis for selectivity and toxicity of ribosomal antibiotics EMBO Rep. 2 2001 318 323
23. J.J. Cannone, S. Subramanian, M.N. Schnare, J.R. Collett, L.M. D'Souza, and Y. Du The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs BMC Bioinformatics 3 2002 2
24. A. Meier, P. Kirschner, B. Springer, V.A. Steingrube, B.A. Brown, R.J. Wallace Jr, and E.C. Bottger Identification of mutations in 23 S rRNA gene of clarithromycin-resistant Mycobacterium intracellulare Antimicrob. Agents Chemother. 38 1994 381 384
25. B. Vester, and S. Douthwaite Macrolide resistance conferred by base substitutions in 23 S rRNA Antimicrob. Agents Chemother. 45 2001 1 12
26. P. Sander, T. Prammananan, and E.C. Bottger Introducing mutations into a chromosomal rRNA gene using a genetically modified eubacterial host with a single rRNA operon Mol. Microbiol. 22 1996 841 848
27. P. Sander, T. Prammananan, A. Meier, K. Frischkorn, and E.C. Bottger The role of ribosomal RNAs in macrolide resistance Mol. Microbiol. 26 1997 469 480
28. M. Liu, and S. Douthwaite Activity of the ketolide telithromycin is refractory to erm monomethylation of bacterial rRNA Antimicrob. Agents Chemother. 46 2002 1629 1633
29. W.D. Celmer, H. Els, and K. Murai Oleandomycin derivatives, preparation and characterization Antibiot. Annu. 5 1957 476 483
30. S. Douthwaite, L.H. Hansen, and P. Mauvais Macrolide-ketolide inhibition of MLS-resistant ribosomes is improved by alternative drug interaction with domain II of 23 S rRNA Mol. Microbiol. 36 2000 183 193
31. A. Tait-Kamradt, T. Davies, M. Cronan, M.R. Jacobs, P.C. Appelbaum, and J. Sutcliffe Mutations in 23 S rRNA and ribosomal protein L4 account for resistance in pneumococcal strains selected in vitro by macrolide passage Antimicrob. Agents Chemother. 44 2000 2118 2125
32. D.J. Farrell, S. Douthwaite, I. Morrissey, S. Bakker, J. Poehlsgaard, L. Jakobsen, and D. Felmingham Macrolide resistance by ribosomal mutation in clinical isolates of Streptococcus pneumoniae from the PROTEKT 1999-2000 study Antimicrob. Agents Chemother. 47 2003 1777 1783
33. N. Ban, P. Nissen, J. Hansen, P.B. Moore, and T.A. Steitz The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution Science 289 2000 905 920
34. J. Harms, F. Schluenzen, R. Zarivach, A. Bashan, S. Gat, and I. Agmon High resolution structure of the large ribosomal subunit from a mesophilic eubacterium Cell 107 2001 679 688
35. S. Douthwaite, and C. Aagaard Erythromycin binding is reduced in ribosomes with conformational alterations in the 23 S rRNA peptidyl transferase loop J. Mol. Biol. 232 1993 725 731
36. S.T. Gregory, and A.E. Dahlberg Erythromycin resistance mutations in ribosomal proteins L22 and L4 perturb the higher order structure of 23 S ribosomal RNA J. Mol. Biol. 289 1999 827 834
37. I.S. Gabashvili, S.T. Gregory, M. Valle, R. Grassucci, M. Worbs, and M.C. Wahl The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22 Mol. Cell 8 2001 181 188
38. F. Depardieu, and P. Courvalin Mutation in 23 S rRNA responsible for resistance to 16-membered macrolides and streptogramins in Streptococcus pneumoniae Antimicrob. Agents Chemother. 45 2001 319 323
39. M. Liu, and S. Douthwaite Resistance to the macrolide antibiotic tylosin is conferred by single methylations at 23 S rRNA nucleotides G748 and A2058 acting in synergy Proc. Natl Acad. Sci. USA 99 2002 14658 14663
40. P. Pfister, M. Risch, D.E. Brodersen, and E.C. Bottger Role of 16S rRNA helix 44 in ribosomal resistance to Hygromycin B Antimicrob. Agents Chemother. 47 2003 1496 1502
41. T. Prammananan, P. Sander, B. Springer, and E.C. Bottger RecA-mediated gene conversion and aminoglycoside resistance in strains heterozygous for rRNA Antimicrob. Agents Chemother. 43 1999 447 453
42. T.A. Jones, M. Bergdoll, and O.O. Kjeldgaard A macromolecular modeling environment C. Bugg S. Ealick Crystallographic Modeling Methods in Molecular Design 1990 Springer New York 189 195
43. Collaborative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
44. J. Tsai, R. Taylor, C. Chothia, and M. Gerstein The packing density in proteins: standard radii and volumes J. Mol. Biol. 290 1999 253 266
45. P. Nissen, J. Hansen, N. Ban, P.B. Moore, and T.A. Steitz The structural basis of ribosome activity in peptide bond synthesis Science 289 2000 920 930