Insights into the mode of action of novel fluoroketolides, potent inhibitors of bacterial protein synthesis

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 1, 2014, Pages 472-480

  Krokidis, Marios G ^a   Márquez, Viter ^b,c   Wilson, Daniel N ^b,c   Kalpaxis, Dimitrios L ^a   Dinos, George P ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b Munich Center for Integrated Protein Science   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; CETHROMYCIN; ERYTHROMYCIN; FLUORINE; LACTONE; RNA 23S; TELITHROMYCIN;

ARTICLE; BACTERICIDAL ACTIVITY; BINDING SITE; CONTROLLED STUDY; ESCHERICHIA COLI; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RIBOSOME; SPECIES DIFFERENCE; WILD TYPE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; ERYTHROMYCIN; ESCHERICHIA COLI; KETOLIDES; MICROBIAL SENSITIVITY TESTS; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, RIBOSOMAL, 23S;

EID: 84891528175     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01994-13     Document Type: Article

References (50)

1. Omura S. 2002. Macrolide antibiotics: Chemistry, biology and practice. Academic Press, Orlando, FL.
2. Poehlsgaard J, Douthwaite S. 2003. Macrolide antibiotic interaction and resistance on the bacterial ribosome. Curr. Opin. Investig. Drugs 4:140-148.
3. Gaynor M, Mankin AS. 2003. Macrolide antibiotics: Binding site, mechanism of action, resistance. Curr. Top. Med. Chem. 3:949-961. http://dx.doi.org/10. 2174/1568026033452159.
4. Mankin AS. 2008. Macrolide myths. Curr. Opin. Microbiol. 11:414-421. http://dx.doi.org/10.1016/j.mib.2008.08.003.
5. Poehlsgaard J, Douthwaite S. 2005. The bacterial ribosome as a target for antibiotics. Nat. Rev. Microbiol. 3:870-881. http://dx.doi.org/10.1038/ nrmicro1265.
6. Katz L, Ashley GW. 2005. Translation and protein synthesis: Macrolides. Chem. Rev. 105:499-527. http://dx.doi.org/10.1021/cr030107f.
7. Llano-Sotelo B, Dunkle J, Klepacki D, Zhang W, Fernandes P, Cate JH, Mankin AS. 2011. Binding and action of CEM-101, a new fluoroketolide antibiotic that inhibits protein synthesis. Antimicrob. Agents Chemother. 54:4961-4970. http://dx.doi.org/10.1128/AAC.00860-10.
8. Kirst HA. 2010. New macrolide, lincosaminide and streptogramin B antibiotics. Expert Opin. Ther. Pat. 20:1343-1357. http://dx.doi.org/10.1517/ 13543776.2010.505921.
9. Harvey C, Puglisi J, Pande V, Cane D, Khosla C. 2012. Precursor directed biosynthesis of an orthogonally functional erythromycin analogue: Selectivity in the ribosome macrolide binding pocket. J. Am. Chem. Soc. 134:12259-12265. http://dx.doi.org/10.1021/ja304682q.
10. Bryskier A. 2000. Ketolides-telithromycin, an example of a new class of antibacterial agents. Clin. Microbiol. Infect. 6:661-669. http://dx.doi.org/10. 1046/j.1469-0691.2000.00185.x.
11. Hammerschlag MR, Sharma R. 2008. Use of cethromycin, a new ketolide, for treatment of community-acquired respiratory infections. Expert Opin. Invest. Drugs 17:387-400. http://dx.doi.org/10.1517/13543784.17.3.387.
12. Rafie S, MacDougall C, James CL. 2010. Cethromycin: A promising new ketolide antibiotic for respiratory infections. Pharmacotherapy 30:290-303. http://dx.doi.org/10.1592/phco.30.3.290.
13. Ying L, Tang D. 2010. Recent advances in the medicinal chemistry of novel erythromycin-derivatized antibiotics. Curr. Top. Med. Chem. 10: 1441-1469. http://dx.doi.org/10.2174/156802610792232042.
14. Kannan K, Vázquez-Laslop N, Mankin AS. 2012. Selective protein synthesis by ribosomes with a drug-obstructed exit tunnel. Cell 151:508-520. http://dx.doi.org/10.1016/j.cell.2012.09.018.
15. Menninger JR, Otto DP. 1982. Erythromycin, carbomycin, and spiramycin inhibit protein synthesis by stimulating the dissociation of peptidyltRNA from ribosomes. Antimicrob. Agents Chemother. 21:811-818. http://dx.doi.org/10.1128/ AAC.21.5.811.
16. Menninger JR. 1995. Mechanism of inhibition of protein synthesis by macrolide and lincosamide antibiotics. J. Basic Clin. Physiol. Pharmacol. 6:229-250.
17. Tenson T, Lovmar M, Ehrenberg M. 2003. The mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome. J. Mol. Biol. 330:1005-1014. http://dx.doi.org/10.1016/ S0022-2836(03)00662-4.
18. Horinouchi S, Weisblum B. 1980. Posttranscriptional modification of mRNA conformation: Mechanism that regulates erythromycin-induced resistance. Proc. Natl. Acad. Sci. U. S. A. 77:7079-7083. http://dx.doi.org/10.1073/pnas.77.12. 7079.
19. Vazquez-Laslop N, Thum C, Mankin AS. 2008. Molecular mechanism of drug-dependent ribosome stalling. Mol. Cell 30:190-202. http://dx.doi org/10.1016/j.molcel.2008.02.026.
20. Ramu H, Vázquez-Laslop N, Klepacki D, Dai Q, Piccirilli J, Micura R, Mankin AS. 2011. Nascent peptide in the ribosome exit tunnel affects functional properties of the A-site of the peptidyl transferase center. Mol. Cell 47:321-330. http://dx.doi.org/10.1016/j.molcel.2010.12.031.
21. Schlünzen F, Zarivach R, Harms J, Bashan A, Tocilj A, Albrecht R, Yonath A, Franceschi F. 2001. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413: 814-821. http://dx.doi.org/10.1038/35101544.
22. Tu D, Blaha G, Moore PB, Steitz TA. 2005. Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121:257-270. http://dx.doi.org/10.1016/j.cell.2005.02.005.
23. Bulkley D, Innis CA, Blaha G, Steitz TA. 2010. Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc. Natl. Acad. Sci. U. S. A. 107: 17158-17163. http://dx.doi.org/10.1073/pnas.1008685107.
24. Dunkle JA, Xiong L, Mankin AS, Cate JH. 2010. Structures of the Escherichia coli ribosome with ntibiotics bound near the peptidyl trans-ferase center explain spectra of drug action. Proc. Natl. Acad. Sci. U. S. A. 107:17152-17157. http://dx.doi.org/10.1073/pnas.1007988107.
25. Blaha G, Stelzl U, Spahn CM, Agrawal RK, Frank J, Nierhaus KH. 2000. Preparation of functional ribosomal complexes and the effect of buffer conditions on tRNA positions observed by cryoelectron microscopy. Methods Enzymol. 317:292-309. http://dx.doi.org/10.1016/S0076-6879(00)17021-1.
26. Rheinberger HJ, Geigenmuller U, Wedde M, Nierhaus KH. 1988. Parameters for the preparation of Escherichia coli ribosomes and ribosomal subunits active in tRNA binding. Methods Enzymol. 164:658-670. http://dx.doi.org/10.1016/S0076- 6879(88)64076-6.
27. Bommer U, Burkhardt N, Junemann R, Spahn CMT, Triana-Alonso FJ, Nierhaus KH. 1996. Ribosomes and polysomes, p 271-301. In Graham J, Rickwoods D (ed), Subcellular fractionation. A practical approach. Oxford University Press, New York, NY.
28. Dinos G, Wilson DN, Teraoka Y, Szaflarski W, Fucini P, Kalpaxis D, Nierhaus KH. 2004. Dissecting the ribosomal inhibition mechanisms of edeine and pactamycin: The universally conserved residues G693 and C795 regulate P-site RNA binding. Mol. Cell 13:113-124. http://dx.doi.org/10.1016/S1097-2765(04)00002-4.
29. Karahalios P, Kalpaxis D, Fu H, Katz L, Wilson DN, Dinos GP. 2006. On the mechanism of action of 9-O-arylalkyloxime derivatives of 6- Omycaminosyltylonolide, a new class of 16-membered macrolide antibiotics. Mol. Pharmacol. 70:1271-1280. http://dx.doi.org/10.1124/mol.106.026567.
30. Starosta A, Karpenko VV, Shishkina AV, Mikolajka A, Sumbatyan NV, Schluenzen F, Korshunova GA, Bogdanov A, Wilson DN. 2010. Interplay between the ribosomal tunnel, nascent chain, and macrolides influences drug inhibition. Chem. Biol. 17:504-514. http://dx.doi.org/10.1016/j.chembiol.2010.04.008.
31. Stern S, Moazed D, Noller HF. 1988. Structural analysis of RNA using chemical and enzymatic probing monitored by primer extension. Methods Enzymol. 164: 481-489. http://dx.doi.org/10.1016/S0076-6879(88)64064-X.
32. Merryman C, Noller HF. 1998. Footprinting and modificationinterference analysis of binding sites on RNA, p 237-253. In Smith CWJ (ed), RNA:protein interactions, a practical approach. Oxford University Press, Oxford, United Kingdom.
33. Bailey M, Chettiath T, Mankin AS. 2008. Induction of erm(C) expression by noninducing antibiotics. Antimicrob. Agents Chemother. 52:866-874. http://dx.doi.org/10.1128/AAC.01266-07.
34. Garza-Ramos G, Xiong L, Zhong P, Mankin A. 2001. Binding site of macrolide antibiotics on the ribosome: new resistance mutation identifies a specific interaction of ketolides with rRNA. J. Bacteriol. 183:6898-6907. http://dx.doi.org/10.1128/JB.183.23.6898-6907.2001.
35. Xiong L, Korkhin Y, Mankin AS. 2005. Binding site of the bridged macrolides in the Escherichia coli ribosome. Antimicrob. Agents Chemother. 49:281-288. http://dx.doi.org/10.1128/AAC.49.1.281-288.2005.
36. Kouvela EC, Kalpaxis DL, Wilson DN, Dinos GP. 2009. Distinct mode of interaction of a novel ketolide antibiotic that displays enhanced antimicrobial activity. Antimicrob. Agents Chemother. 53:1411-1419. http://dx.doi.org/10.1128/ AAC.01425-08.
37. Kostopoulou ON, Petropoulos AD, Dinos GP, Choli-Papadopoulou T, Kalpaxis DL. 2012. Investigating the entire course of telithromycin binding to Escherichia coli ribosomes. Nucleic Acids Res. 40:5078-5087. http://dx.doi.org/10.1093/nar/gks174.
38. Mamos P, Krokidis M, Papadas A, Karahalios P, Starosta A, Wilson DN, Kalpaxis D, Dinos G. 2013. On the use of the antibiotic chloramphenicol to target polypeptide chain mimics to the ribosomal exit tunnel. Biochimie 95:1765-1772. http://dx.doi.org/10.1016/j.biochi.2013.06.004.
39. Picking WD, Odom OW, Tsalkova T, Serdyuk I, Hardesty B. 1991. The conformation of nascent polylysine and polyphenylalanine peptides on ribosomes. J. Biol. Chem. 266:1534-1542.
40. Berisio R, Harms J, Schluenzen F, Zarivach R, Hansen HA, Fucini P, Yonath A. 2003. Structural insight into the antibiotic action of telithromycin against resistant mutants. J. Bacteriol. 185:4276-4279. http://dx.doi.org/10.1128/JB. 185.14.4276-4279.2003.
41. Wilson DN, Harms JM, Nierhaus KH, Schlünzen F, Fucini P. 2005. Species-specific antibiotic-ribosome interactions: Implications for drug development. Biol. Chem. 386:1239-1252. http://dx.doi.org/10.1515/BC.2005.141.
42. Hansen JL, Schmeing TM, Moore PB, Steitz TA. 2002. Structural insights into peptide bond formation. Proc. Natl. Acad. Sci. U. S. A. 99: 11670-11675. http://dx.doi.org/10.1073/pnas.172404099.
43. Schlünzen F, Harms J, Franceschi F, Hansen H, Bartels H, Zarivach R, Yonath A. 2003. Structural basis for the antibiotic activity of ketolides and azalides. Structure 11:329-338. http://dx.doi.org/10.1016/S0969-2126(03)00022-4.
44. Hansen LH, Mauvais P, Douthwaite S. 1999. The macrolide-ketolide antibiotic binding site is formed by structures in domains II and V of 23S ribosomal RNA. Mol. Microbiol. 31:623-631. http://dx.doi.org/10.1046/j.1365- 2958.1999.01202.x.
45. Poulsen S, Kofoed MC, Vester B. 2000. Inhibition of the ribosomal peptidyl transferase reaction by the mycarose moiety of the antibiotics carbomycin, spiramycin and tylosin. J. Mol. Biol. 304:471-481. http://dx.doi.org/10.1006/jmbi.2000.4229.
46. Xiong L, Shah S, Mauvais P, Mankin AS. 1999. A ketolide resistance mutation in domain II of 23S rRNA reveals the proximity of hairpin 35 to the peptidyl transferase centre. Mol. Microbiol. 31:633-639. http://dx.doi.org/10. 1046/j.1365-2958.1999.01203.x.
47. Kannan K, Mankin AS. 2011. Macrolide antibiotics in the ribosome exit tunnel: Species-specific binding and action. Ann. N. Y. Acad. Sci. 1241:33- 47. http://dx.doi.org/10.1111/j.1749-6632.2011.06315.x.
48. Petropoulos AD, Kouvela EC, Dinos G, Kalpaxis DL. 2008. Stepwise binding of tylosin and erythromycin to Escherichia coli ribosomes, characterized by kinetic and footprinting analysis. J. Biol. Chem. 283:4756-4765. http://dx.doi.org/10.1074/jbc.M708371200.
49. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 A resolution. Science 310:827-834. http://dx.doi.org/10.1126/science.1117230.
50. Keyes RF, Carter J, Englund EE, Daly MM, Stone GG, Nilius AM, Ma Z. 2003. Synthesis and antibacterial activity of 6-O-arylbutynyl ketolides with improved activity against some key erythromycin-resistant pathogens. J. Med. Chem. 46:1795-1798. http://dx.doi.org/10.1021/jm025580k.