Macrolide antibiotics in the ribosome exit tunnel: Species-specific binding and action

Annals of the New York Academy of Sciences

Volumn 1241, Issue 1, 2011, Pages 33-47

  Kannan, Krishna ^a   Mankin, Alexander S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Macrolide; Nascent peptide exit tunnel; Posttranscriptional modifications; Protein synthesis; Ribosome

Indexed keywords

ALKYL GROUP; AZITHROMYCIN; CARBOMYCIN; DIMETHYL SULFATE; ERYTHROMYCIN; JOSAMYCIN; KETOLIDE; MACROLIDE; PEPTIDYLTRANSFERASE; POLYPEPTIDE; RIBOSOME PROTEIN; RNA 23S; SPIRAMYCIN; TELITHROMYCIN; TETRACYCLINE; TROLEANDOMYCIN;

ARTICLE; BINDING AFFINITY; DEINOCOCCUS RADIODURANS; DNA MODIFICATION; DRUG BINDING; DRUG BINDING SITE; DRUG INTERACTION; DRUG MECHANISM; DRUG RESISTANCE; DRUG STRUCTURE; ESCHERICHIA COLI; HALOARCULA MARISMORTUI; HUMAN; LARGE RIBOSOMAL SUBUNIT; MUTATION; PROTEIN SYNTHESIS INHIBITION; SPECIES DIFFERENCE; TRANSLATION INITIATION;

EID: 84255195557     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2011.06315.x     Document Type: Article

References (75)

1. McGuire, J.M., R.L. Bunch, R.C. Anderson, et al 1952. Ilotycin, a new antibiotic. Schweiz Med. Wochenschr. 82: 1064-1065.
2. Ban, N., P. Nissen, J. Hansen, et al 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289: 905-920.
3. Vazquez, D. 1977. Inhibitors of Protein Synthesis. Springer. New York
4. Poulsen, S.M., C. Kofoed & B. Vester 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.
5. Moazed, D. & H.F. Noller 1987. Chloramphenicol, erythromycin, carbomycin and vernamycin B protect overlapping sites in the peptidyl transferase region of 23S ribosomal RNA. Biochimie 69: 879-884.
6. Tejedor, F. & J.P. Ballesta 1985. Components of the macrolide binding site on the ribosome. J. Antimicrob. Chemother. 16(Suppl A): 53-62.
7. Hansen, L.H., P. Mauvais & S. Douthwaite 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.
8. Xiong, L., S. Shah, P. Mauvais & A.S. Mankin 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.
9. Wittmann, H. G., G. Stöffler, D. Apirion, et al 1973. Biochemical and genetic studies on two different types of erythromycin resistant mutants ofEscherichia coliwith altered ribosomal proteins. Mol. Gen. Genet. 127: 175-189.
10. Pardo, D., and R. Rosset 1974. Genetic studies of erythromycin resistant mutants ofEscherichia coli. Mol. Gen. Genet. 135: 257-268.
11. Sigmund, C.D. & E.A. Morgan 1982. Erythromycin resistance due to a mutation in a ribosomal RNA operon ofEscherichia coli. Proc. Natl. Acad. Sci. USA 79: 5602-5606.
12. Ettayebi, M., S.M. Prasad & E.A. Morgan 1985. Chloramphenicol-erythromycin resistance mutations in a 23S rRNA gene ofEscherichia coli. J. Bacteriol. 162: 551-557.
13. Chittum, H.S. & W.S. Champney 1994. Ribosomal protein gene sequence changes in erythromycin-resistant mutants ofEscherichia coli. J. Bacteriol. 176: 6192-6198.
14. Vester, B. & R.A. Garrett 1987. A plasmid-coded and site-directed mutation inEscherichia coli23S RNA that confers resistance to erythromycin: implications for the mechanism of action of erythromycin. Biochimie 69: 891-900.
15. Hummel, H. & A. Bock 1987. 23S ribosomal RNA mutations in halobacteria conferring resistance to the anti-80S ribosome targeted antibiotic anisomycin. Nucl. Acids Res. 15: 2431-2443.
16. Mankin, A.S. & R.A. Garrett 1991. Chloramphenicol resistance mutations in the single 23S rRNA gene of the archaeonHalobacterium halobium. J. Bacteriol. 173: 3559-3563.
17. Bottger, E.C. 1994. Resistance to drugs targeting protein synthesis in mycobacteria. Trends Microbiol. 2: 416-421.
18. Schlunzen, F., R. Zarivach, J. Harms, et al 2001. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413: 814-821.
19. Hansen, J.L., J.A. Ippolito, N. Ban, et al 2002. The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol. Cell 10: 117-128.
20. Bulkley, D., C.A. Innis, G. Blaha & T.A. Steitz 2010. Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc. Natl. Acad. Sci. USA 107: 17158-17163.
21. Dunkle, J.A., L. Xiong, A.S. Mankin & J.H. Cate 2010. Structures of theEscherichia coliribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc. Natl. Acad. Sci. USA 107: 17152-17157.
22. Putnam, S.D., M. Castanheira, G.J. Moet, et al 2010. CEM-101, a novel fluoroketolide: antimicrobial activity against a diverse collection of Gram-positive and Gram-negative bacteria. Diagn. Microbiol. Infect. Dis. 66: 393-401.
23. Llano-Sotelo, B., J. Dunkle, D. Klepacki, et al 2010. Binding and action of CEM-101, a new fluoroketolide antibiotic that inhibits protein synthesis. Antimicrob. Agents Chemother. 54: 4961-4970.
24. Weisblum, B. 1995. Erythromycin resistance by ribosome modification. Antimicrob. Agents Chemother. 39: 577-585.
25. Vazquez-Laslop, N., D. Klepacki, D.C. Mulhearn, et al 2011. Role of antibiotic ligand in nascent peptide-dependent ribosome stalling. Proc. Natl. Acad. Sci. USA 108: 10496-10501.
26. Liu, M. & S. Douthwaite 2002. Resistance to the macrolide antibiotic tylosin is conferred by single methylations at 23S rRNA nucleotides G748 and A2058 acting in synergy. Proc. Natl. Acad. Sci. USA 99: 14658-14663.
27. Pyetan, E., D. Baram, T. Auerbach-Nevo & A. Yonath 2007. Chemical parameters influencing fine-tuning in the binding of macrolide antibiotics to the ribosomal tunnel. Pure Appl. Chem. 79, 955-968.
28. Starosta, A.L., V.V. Karpenko, A.V. Shishkina, et al 2010. Interplay between the ribosomal tunnel, nascent chain, and macrolides influences drug inhibition. Chem. Biol. 17: 504-514.
29. Moore, S.D. & R.T. Sauer 2008. Revisiting the mechanism of macrolide-antibiotic resistance mediated by ribosomal protein L22. Proc. Natl. Acad. Sci. USA 105: 18261-18266.
30. Lovmar, M., K. Nilsson, E. Lukk, et al 2009. Erythromycin resistance by L4/L22 mutations and resistance masking by drug efflux pump deficiency. EMBO J. 28: 736-744.
31. Otaka, T. & A. Kaji 1975. Release of (oligo) peptidyl-tRNA from ribosomes by erythromycin A. Proc. Natl. Acad. Sci. USA 72: 2649-2652.
32. Menninger, J.R. & D.P. Otto 1982. Erythromycin, carbomycin, and spiramycin inhibit protein synthesis by stimulating the dissociation of peptidyl-tRNA from ribosomes. Antimicrob. Agents Chemother. 21: 811-818.
33. Tenson, T., M. Lovmar & M. Ehrenberg 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.
34. Lovmar, M., T. Tenson & M. Ehrenberg 2004. Kinetics of macrolide action: the josamycin and erythromycin cases. J. Biol. Chem. 279: 53506-53515.
35. Andersson, S. & C.G. Kurland 1987. Elongating ribosomes in vivo are refractory to erythromycin. Biochimie 69: 901-904.
36. Lovmar, M., K. Nilsson, V. Vimberg, et al 2006. The molecular mechanism of peptide-mediated erythromycin resistance. J. Biol. Chem. 281: 6742-6750.
37. Tenson, T., L. Xiong, P. Kloss & A.S. Mankin 1997. Erythromycin resistance peptides selected from random peptide libraries. J. Biol. Chem. 272: 17425-17430.
38. Tripathi, S., P.S. Kloss & A.S. Mankin 1998. Ketolide resistance conferred by short peptides. J. Biol. Chem. 273: 20073-20077.
39. BK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121: 257-270.
40. Thompson, J., C.A. Pratt & A.E. Dahlberg 2004. Effects of a number of classes of 50S inhibitors on stop codon readthrough during protein synthesis. Antimicrob. Agents Chemother. 48: 4889-4891.
41. Champney, W.S. & M. Miller 2002. Inhibition of 50S ribosomal subunit assembly inHaemophilus influenzaecells by azithromycin and erythromycin. Curr. Microbiol. 44: 418-424.
42. Siibak, T., L. Peil, L. Xiong, et al 2009. Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition. Antimicrob. Agents Chemother. 53: 563-571.
43. Gyi, J.I. & J. Barber 1991. Nuclear magnetic resonance studies on the mode of action of erythromycin A. Biochem. Soc. Trans. 19: 313S.
44. Stephenson, G.A., J.G. Stowell, P.H. Toma, et al 1997. Solid-state investigations of erythromycin A dihydrate: structure, NMR spectroscopy, and hygroscopicity. J. Pharm. Sci. 86: 1239-1244.
45. Wilson, D.N., J.M. Harms, K.H. Nierhaus, et al 2005. Species-specific antibiotic-ribosome interactions: implications for drug development. Biol. Chem. 386: 1239-1252.
46. Canu, A., B. Malbruny, M. Coquemont, et al 2002. Diversity of ribosomal mutations conferring resistance to macrolides, clindamycin, streptogramin, and telithromycin inStreptococcus pneumoniae. Antimicrob. Agents Chemother. 46: 125-131.
47. Berisio, R., J. Harms, F. Schluenzen, et al 2003. Structural insight into the antibiotic action of telithromycin against resistant mutants. J. Bacteriol. 185: 4276-4279.
48. Schlunzen, F., J.M. Harms, F. Franceschi, et al 2003. Structural basis for the antibiotic activity of ketolides and azalides. Structure 11: 329-338.
49. Borovinskaya, M.A., R.D. Pai, W. Zhang, et al 2007. Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat. Struct. Biol. 14: 727-732.
50. Pioletti, M., F. Schlunzen, J. Harms, et al 2001. Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J. 20: 1829-1839.
51. Brodersen, D.E., W.M. Clemons, Jr, A.P. Carter, et al 2000. The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103: 1143-1154.
52. Voss, N.R., M. Gerstein, T.A. Steitz & P.B. Moore 2006. The geometry of the ribosomal polypeptide exit tunnel. J. Mol. Biol. 360: 893-906.
53. David-Eden, H., A.S. Mankin & Y. Mandel-Gutfreund 2010. Structural signatures of antibiotic binding sites on the ribosome. Nucl. Acids Res. 38: 5982-5994.
54. Petropoulos, A.D., E.C. Kouvela, A.L. Starosta, et al 2009. Time-resolved binding of azithromycin toEscherichia coliribosomes. J. Mol. Biol. 385: 1179-1192.
55. Wang, G., Y. Qiu, D. Niu, et al 43rd Intersci. Conf. Antimicrob. Agents Chemother.Abstract F-1193, 2003.
56. Xiong, L., Y. Korkhin & A.S. Mankin 2005. Binding site of the bridged macrolides in theEscherichia coliribosome. Antimicrob. Agents Chemother. 49: 281-288.
57. Berisio, R., F. Schluenzen, J. Harms, et al 2003. Structural insight into the role of the ribosomal tunnel in cellular regulation. Nat. Struct. Biol. 10: 366-370.
58. Gurel, G., G. Blaha, T.A. Steitz & P.B. Moore 2009. Structures of triacetyloleandomycin and mycalamide A bind to the large ribosomal subunit ofHaloarcula marismortui. Antimicrob. Agents Chemother. 53: 5010-5014.
59. Vester, B. & S. Douthwaite 2001. Macrolide resistance conferred by base substitutions in 23S rRNA. Antimicrob. Agents Chemother. 45: 1-12.
60. Farrell, D.J., S. Douthwaite, I. Morrissey, et al 2003. Macrolide resistance by ribosomal mutation in clinical isolates ofStreptococcus pneumoniaefrom the PROTEKT 1999-2000 study. Antimicrob. Agents Chemother. 47: 1777-1783.
61. Pfister, P., N. Corti & S. Hobbie 2005. 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: 5180-5185.
62. Franceschi, F., Z. Kanyo, E.C. Sherer & J. Sutcliffe 2004. Macrolide resistance from the ribosome perspective. Curr. Drug Targets Infect. Disord. 4: 177-191.
63. Debets-Ossenkopp, Y.J., A.B. Brinkman, E.J. Kuipers, et al 1998. Explaining the bias in the 23S rRNA gene mutations associated with clarithromycin resistance in clinical isolates ofHelicobacter pylori. Antimicrob. Agents Chemother. 42: 2749-2751.
64. Occhialini, A., M. Urdaci, F. Doucet-Populaire, et al 1997. Macrolide resistance inHelicobacter pylori: rapid detection of point mutations and assays of macrolide binding to ribosomes. Antimicrob. Agents Chemother. 41: 2724-2728.
65. Sigmund, C.D., M. Ettayebi & E.A. Morgan 1984. Antibiotic resistance mutations in 16S and 23S ribosomal RNA genes ofEscherichia coli. Nucl. Acids Res. 12: 4653-4663.
66. 5U1939 in 23S rRNA using MALDI mass spectrometry. Nucl. Acids Res. 31: 4738-4746.
67. 1G745-deficient mutant. J. Bacteriol. 180: 359-365.
68. Raychaudhuri, S., L. Niu, J. Conrad, et al 1999. Functional effect of deletion and mutation of theEscherichia coliribosomal RNA and tRNA pseudouridine synthase RluA. J. Biol. Chem. 274: 18880-18886.
69. Mengel-Jorgensen, J., S.S. Jensen, A. Rasmussen, et al 2006. Modifications inThermus thermophilus23 S ribosomal RNA are centered in regions of RNA-RNA contact. J. Biol. Chem. 281: 22108-22117.
70. Douthwaite, S., P.F. Crain, M. Liu & J. Poehlsgaard 2004. The tylosin-resistance methyltransferase RlmA(II) (TlrB) modifies the N-1 position of 23S rRNA nucleotide G748. J. Mol. Biol. 337: 1073-1077.
71. Gregory, S.T. & A.E. Dahlberg 1999. Erythromycin resistance mutations in ribosomal proteins L22 and L4 perturb the higher order structure of 23S ribosomal RNA. J. Mol. Biol. 289: 827-834.
72. Toh, S.M. & A.S. Mankin 2008. An indigenous posttranscriptional modification in the ribosomal peptidyl transferase center confers resistance to an array of protein synthesis inhibitors. J. Mol. Biol. 380: 593-597.
73. Ramu, H., N. Vazquez-Laslop, D. Klepacki, et al 2011. Nascent peptide in the ribosome exit tunnel affects functional properties of the A-site of the peptidyl transferase center. Mol. Cell 41: 321-330.
74. Vazquez-Laslop, N. & A.S. Mankin 2011. Picky nascent peptides do not talk to foreign ribosomes. Proc. Natl. Acad. Sci. USA 108: 5931-5932.
75. Franceschi, F. & E.M. Duffy 2006. Structure-based drug design meets the ribosome. Biochem. Pharmacol. 71: 1016-1025.