Time-Resolved Binding of Azithromycin to Escherichia coli Ribosomes

Journal of Molecular Biology

Volumn 385, Issue 4, 2009, Pages 1179-1192

  Petropoulos, Alexandros D ^a   Kouvela, Ekaterini C ^a   Starosta, Agata L ^b   Wilson, Daniel N ^b   Dinos, George P ^a   Kalpaxis, Dimitrios L ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

azithromycin; peptide exit tunnel; peptidyl transferase; ribosome; slow binding inhibitors

Indexed keywords

AZITHROMYCIN; CYTOSINE; MAGNESIUM ION; NUCLEOSIDE; POLYAMINE; RIBOSOME RNA; URACIL;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CONCENTRATION RESPONSE; DRUG BINDING; ESCHERICHIA COLI; GENE MUTATION; KINETICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOOTPRINTING; RIBOSOME;

BACTERIA (MICROORGANISMS); DEINOCOCCUS RADIODURANS; ESCHERICHIA COLI;

EID: 58149326730     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.11.042     Document Type: Article

References (42)

1. Fiese E.F., and Steffen S.H. Comparison of the acid stability of azithromycin and erythromycin A. J. Antimicrob. Chemother. 25 (1990) 39-47
2. Lalak N.J., and Morris D.L. Azithromycin clinical pharmacokinetics. Clin. Pharmacokinet. 25 (1993) 370-374
3. Zuckerman M.D. The newer macrolides: azithromycin and clarithromycin. Infect. Dis. Clin. North Am. 14 (2000) 449-462
4. Gordillo M.E., Singh K.V., and Murray B.E. In vitro activity of azithromycin against bacterial enteric pathogens. Antimicrob. Agents Chemother. 37 (1993) 1203-1205
5. Garza-Ramos G., Xiong L., Zhong P., and Mankin A.S. Binding site of macrolide antibiotics on the ribosome: new resistance mutation identifies a specific interaction of ketolides with rRNA. J. Bacteriol. 183 (2001) 6898-6907
6. Vaara M. Outer membrane permeability barrier to azithromycin, clarithromycin, and roxithromycin in gram-negative enteric bacteria. Antimicrob. Agents Chemother. 37 (1993) 354-356
7. Imamura Y., Higashiyama Y., Tomono K., Izumikawa K., Yanagihara K., Ohno H., et al. Azithromycin exhibits bactericide effects on Pseudomonas aeruginosa through interaction with the outer membrane. Antimicrob. Agents Chemother. 49 (2005) 1377-1380
8. Retsema J., Girard A., Schelkly W., Manousos M., Anderson M., Bright G., et al. Spectrum and mode of action of azithromycin (CP-62, 993), a new 15-membered-ring macrolide with improved potency against gram-negative organisms. Antimicrob. Agents Chemother. 31 (1987) 1939-1947
9. Goldman R.C., Fesik S.W., and Doran C.C. Role of protonated and neutral forms of macrolides in binding to ribosomes from Gram-positive and Gram-negative bacteria. Antimicrob. Agents Chemother. 34 (1990) 426-431
10. Dinos G.P., Michelinaki M., and Kalpaxis D.L. Insights into the mechanism of azithromycin interaction with an Escherichia coli functional ribosomal complex. Mol. Pharmacol. 59 (2001) 1441-1445
11. Yan K., Hunt E., Berge J., May E., Copeland R.A., and Gontarek R.R. Fluorescence polarization method to characterize macrolide-ribosome interactions. Antimicrob. Agents Chemother. 49 (2005) 3367-3372
12. Vester B., and Douthwaite S. Macrolide resistance conferred by base substitutions in 23S rRNA. Antimicrob. Agents Chemother. 45 (2001) 1-12
13. Leclercq R., and Courvalin P. Resistance to macrolides and related antibiotics in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 46 (2002) 2727-2734
14. Farrell D.J., Douthwaite S., Morrissey I., Bakker S., Poehlsgaard J., Jakobsen L., and Felmingham D. Macrolide resistance by ribosomal mutation in clinical isolates of Streptococcus pneumoniae from the PROTECT 1999-2000 study. Antimicrob. Agents Chemother. 47 (2003) 1777-1783
15. Katz L., and Ashley G.W. Translation and protein synthesis: macrolides. Chem. Rev. 105 (2005) 499-527
16. Pfister P., Corti N., Hobbie S., Bruell C., Zarivach R., Yonath A., and Böttger E.C. 23S rRNA base pair 2057-2611 determines ketolide susceptibility and fitness cost of the macrolide resistance mutation 2058A→G. Proc. Natl Acad. Sci. USA 102 (2005) 5180-5185
17. Pereyre S., Renaudin H., Charron A., Bébéar C., and Bébéar C.M. Emergence of a 23S rRNA mutation in Mycoplasma hominis associated with a loss of the intrinsic resistance to erythromycin and azithromycin. J. Antimicrob. Chemother. 57 (2006) 753-756
18. Lovmar M., Tenson T., and Ehrenberg M. Kinetics of macrolide action: the josamycin and erythromycin cases. J. Biol. Chem. 279 (2004) 53506-53515
19. Chittum H.S., and Champney W.S. Erythromycin inhibits the assembly of the large ribosomal subunit in growing Escherichia coli cells. Curr. Microbiol. 30 (1995) 273-279
20. Nalca Y., Jänsch L., Bredenbruch F., Geffers R., Buer J., and Häussler S. Quorum-sensing antagonistic activities of azithromycin in Pseudomonas aeruginosa PAO1: a global approach. Antimicrob. Agents Chemother. 50 (2006) 1680-1688
21. Hansen J.L., Ippolito J.A., Ban N., Nissen P., Moore P.B., and Steitz T.A. The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol. Cell 10 (2002) 117-128
22. Schlünzen F., Harms J.M., Franceschi F., Hansen H.A.S., Bartels H., Zarivach R., and Yonath A. Structural basis for the antibiotic activity of ketolides and azalides. Structure 11 (2003) 329-338
23. Wilson D.N., Harms J.M., Nierhaus K.H., Schlünzen F., and Fucini P. Species-specific antibiotic-ribosome interactions: implications for drug development. Biol. Chem. 386 (2005) 1239-1252
24. BK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121 (2005) 257-270
25. Berisio R., Corti N., Pfister P., Yonath A., and Böttger E.C. 23S rRNA 2058A → G alteration mediates ketolide resistance in combination with deletion in L22. Antimicrob. Agents Chemother. 50 (2006) 3816-3823
26. Bertho G., Gharbi-Benarous J., Delaforge M., and Girault J.P. Transferred nuclear Overhauser effect study of macrolide-ribosome interactions: correlation between antibiotic activities and bound conformations. Bioorg. Med. Chem. 6 (1998) 209-221
27. Novak P., Tatić I., Tepeš P., Koštrum S., and Barber J. Systematic approach to understanding macrolide-ribosome interactions: NMR and modeling studies of oleandomycin and its derivatives. J. Phys. Chem. A 110 (2006) 572-579
28. Dinos G., Synetos D., and Coutsogeorgopoulos C. Interaction between the antibiotic spiramycin and a ribosomal complex active in peptide bond formation. Biochemistry 32 (1993) 10638-10647
29. Poulsen S.M., Kofoed C., and Vester B. 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
30. Petropoulos A.D., Kouvela E.C., Dinos G.P., and Kalpaxis D.L. Step-wise binding of tylosin and erythromycin to Escherichia coli ribosomes, characterized by kinetic and footprinting analysis. J. Biol. Chem. 283 (2008) 4756-4765
31. Xiong L., Shah S., Mauvais P., and Mankin A.S. A ketolide resistant mutation in domain II of 23S rRNA reveals the proximity of hairpin 35 to the peptidyl transferase centre. Mol. Microbiol. 31 (1999) 633-639
32. Szaflarski W., Vesper O., Teraoka Y., Phitta B., Wilson D.N., and Nierhaus K.H. New features of the ribosome and ribosomal inhibitors: non enzymatic recycling, misreading and back-translocation. J. Mol. Biol. 380 (2008) 193-205
33. Egebjerg J., Larsen N., and Garrett R.A. Structural map of 23S rRNA. In: Dahlberg A., Hill W.E., Garrett R.A., Moore P.B., Schlessinger D., and Warner J.R. (Eds). The Ribosome: Structure, Function and Evolution (1990), American Society for Microbiology, Washington, DC 168-179
34. Morrison J.F., and Walsh C.T. The behavior and significance of slow-binding enzyme inhibitors. Adv. Enzymol. Relat. Areas Mol. Biol. 61 (1988) 201-301
35. Fuentes F., Izquierdo J., Martin M.M., Gomez-Lus M.L., and Prieto J. Postantibiotic and sub-MIC effects of azithromycin and isepamicin against Staphylococcus aureus and Escherichia coli. Antimicrob. Agents Chemother. 42 (1998) 414-418
36. Bailey M., Chettiath T., and Mankin A.S. Induction of erm(C) expression by noninducing antibiotics. Antimicrob. Agents Chemother. 52 (2008) 866-874
37. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310 (2005) 827-834
38. Davydova N., Streltsov V., Wilce M., Liljas A., and Garber M. L22 ribosomal protein and effect of its mutation on ribosome resistance to erythromycin. J. Mol. Biol. 322 (2002) 635-644
39. Schlünzen F., Zarivach R., Harms J., Bashan A., Tocilj A., Albrecht R., et al. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413 (2001) 814-821
40. Xaplanteri M.A., Petropoulos A.D., Dinos G.P., and Kalpaxis D.L. Localization of spermine binding sites in 23S rRNA by photoaffinity labeling: parsing the spermine contribution to ribosomal 50S subunit functions. Nucleic Acids Res. 33 (2005) 2792-2805
41. Dinos G., Wilson D.N., Teraoka Y., Szaflarski W., Fucini P., Kalpaxis D.L., and Nierhaus K.H. Dissecting the ribosomal inhibition mechanisms of edeine and pactamycin: the universally conserved residues G693 and C795 regulate P-site RNA binding. Mol. Cell 13 (2004) 113-124
42. Stern S., Moazed D., and Noller H.F. Structural analysis of RNA using chemical and enzymatic probing monitored by primer extension. Methods Enzymol. 164 (1988) 481-489