Revisiting the mechanism of macrolide-antibiotic resistance mediated by ribosomal protein L22

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 47, 2008, Pages 18261-18266

  Moore, Sean D ^a,b   Sauer, Robert T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

ermC; Erythromycin; Ribosome; TolC

Indexed keywords

ACRAB PROTEIN; MACROLIDE; PROTEIN DERIVATIVE; RIBOSOMAL PROTEIN L22; RIBOSOME PROTEIN; TOLC PROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ESCHERICHIA COLI; IN VITRO STUDY; MUTATION; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; STEADY STATE; WILD TYPE;

BASE SEQUENCE; DNA PRIMERS; DRUG RESISTANCE, MICROBIAL; ERYTHROMYCIN; ESCHERICHIA COLI; MACROLIDES; RIBOSOMAL PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 57449088414     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0810357105     Document Type: Article

References (46)

1. Vester B, Douthwaite S (2001) Macrolide resistance conferred by base substitutions in 23S rRNA. Antimicrob Agents Chemother 45:1-12.
2. Roberts MC (2008) Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 282:147-159.
3. Schlünzen F, et al. (2001) Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413:814-821.
4. 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.
5. Contreras A, Vázquez D (1977) Cooperative and antagonistic interactions of peptidyl-tRNA and antibiotics with bacterial ribosomes. Eur J Biochem 74:539-547.
6. Andersson S, Kurland CG (1987) Elongating ribosomes in vivo are refractory to erythromycin. Biochimie 69:901-904.
7. 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.
8. Wittmann HG, et al. (1973) Biochemical and genetic studies on two different types of erythromycin resistant mutants of Escherichia coli with altered ribosomal proteins. Mol Gen Genet 127:175-189.
9. Douthwaite S, Powers T, Lee JY, Noller HF (1989) Defining the structural requirements for a helix in 23 S ribosomal RNA that confers erythromycin resistance. J Mol Biol 209:655-665.
10. Zaman S, Fitzpatrick M, Lindahl L, Zengel J (2007) Novel mutations in ribosomal proteins L4 and L22 that confer erythromycin resistance in Escherichia coli. Mol Microbiol 66:1039-1050.
11. Apirion D (1967) Three genes that affect Escherichia coli ribosomes. J Mol Biol 30:255-275.
12. Chittum HS, Champney WS (1994) Ribosomal protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli. J Bacteriol 176:6192-6198.
13. Gregory ST, Dahlberg AE (1999) Erythromycin resistance mutations in ribosomal proteins L22 and L4 perturb the higher order structure of 23 S ribosomal RNA. J Mol Biol 289:827-834.
14. Clark C, et al. (2002) In vitro selection of resistance in Haemophilus influenzae by amoxicillin-clavulanate, cefpodoxime, cefprozil, azithromycin, and clarithromycin. Antimicrob Agents Chemother 46:2956-2962.
15. Pardo D, Rosset R (1977) Properties of ribosomes from erythromycin resistant mutants of Escherichia coli. Mol Gen Genet 156:267-271.
16. Schuwirth BS, et al. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science 310:827-834.
17. Voss NR, Gerstein M, Steitz TA, Moore PB (2006) The geometry of the ribosomal polypeptide exit tunnel. J Mol Biol 360:893-906.
18. Gabashvili IS, et al. (2001) The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol Cell 8:181-188.
19. Davydova N, Streltsov V, Wilce M, Liljas A, Garber M (2002) L22 ribosomal protein and effect of its mutation on ribosome resistance to erythromycin. J Mol Biol 322:635-644.
20. Moore SD, Baker TA, Sauer RT (2008) Forced extraction of targeted components from complex macromolecular assemblies. Proc Natl Acad Sci USA 105:11685-11690.
21. 14C]erythromycin to Escherichia coli ribosomes. Antimicrob Agents Chemother 6:474-478.
22. 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 232:725-731.
23. Lovmar M, Tenson T, Ehrenberg M (2004) Kinetics of macrolide action: The josamycin and erythromycin cases. J Biol Chem 279:53506-53515.
24. Petropoulos AD, Kouvela EC, Dinos GP, 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.
25. Lomovskaya O, et al. (2001) Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: Novel agents for combination therapy. Antimicrob Agents Chemother 45:105-116.
26. Chollet R, Chevalier J, Bryskier A, Pagès JM (2004) The AcrAB-TolC pump is involved in macrolide resistance but not in telithromycin efflux in Enterobacter aerogenes and Escherichia coli. Antimicrob Agents Chemother 48:3621-3624.
27. Skinner R, Cundliffe E, Schmidt FJ (1983) Site of action of a ribosomal RNA methylase responsible for resistance to erythromycin and other antibiotics. J Biol Chem 258:12702-12706.
28. Denoya CD, Dubnau D (1987) Site and substrate specificity of the ermC 23S rRNA methyltransferase. J Bacteriol 169:3857-3860.
29. Moazed D, Noller HF (1987) Chloramphenicol, erythromycin, carbomycin and vernamycin B protect overlapping sites in the peptidyl transferase region of 23S ribosomal RNA. Biochimie 69:879-884.
30. Zengel JM, Jerauld A, Walker A, Wahl MC, Lindahl L (2003) The extended loops of ribosomal proteins L4 and L22 are not required for ribosome assembly or L4-mediated autogenous control. RNA 9:1188-1197.
31. Nikaido H (1998) Multiple antibiotic resistance and efflux. Curr Opin Microbiol 1:516-523.
32. Kobayashi N, Nishino K, Yamaguchi A (2001) Novel macrolide-specific ABC-type efflux transporter in Escherichia coli. J Bacteriol 183:5639-5644.
33. Jellen-Ritter AS, Kern WV (2001) Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants Selected with a fluoroquinolone. Antimicrob Agents Chemother 45:1467-1472.
34. Nishino K, Senda Y, Yamaguchi A (2008) The AraC-family regulator GadX enhances multidrug resistance in Escherichia coli by activating expression of mdtEF multidrug efflux genes. J Infect Chemother 14:23-29.
35. Dennis PP, Bremer H (1974) Macromolecular composition during steady-state growth of Escherichia coli B-r. J Bacteriol 119:270-281.
36. Nakatogawa H, Ito K (2002) The ribosomal exit tunnel functions as a discriminating gate. Cell 108:629-636.
37. Vazquez-Laslop N, Thum C, Mankin AS (2008) Molecular mechanism of drug-dependent ribosome stalling. Mol Cell 30:190-202.
38. Otsuji N, Soejima T, Maki S, Shinagawa H (1982) Cloning of colicin E1 tolerant tolC (mtcB) gene of Escherichia coli K12 and identification of its gene product. Mol Gen Genet 187:30-36.
39. Kawabe T, Fujihira E, Yamaguchi A (2000) Molecular construction of a multidrug exporter system, AcrAB: Molecular interaction between AcrA and AcrB, and cleavage of the N-terminal signal sequence of AcrA. J Biochem 128:195-200.
40. Rosenberg EY, Bertenthal D, Nilles ML, Bertrand KP, Nikaido H (2003) Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol Microbiol 48:1609-1619.
41. Peric M, et al. (2004) Inability of L22 ribosomal protein alteration to increase macrolide MICs in the absence of efflux mechanism in Haemophilus influenzae HMC-S. J Antimicrob Chemother 54:393-400.
42. Cagliero C, Mouline C, Cloeckaert A, Payot S (2006) Synergy between efflux pump CmeABC and modifications in ribosomal proteins L4 and L22 in conferring macrolide resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother 50:3893-3896.
43. Baba T, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2:1-11.
44. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645.
45. Datta S, Costantino N, Court DL (2006) A set of recombineering plasmids for gram-negative bacteria. Gene 379:109-115.
46. Moazed D, Robertson JM, Noller HF (1988) Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature 334:362-364.