Resistance mutations in 23 S rRNA identify the site of action of the protein synthesis inhibitor linezolid in the ribosomal peptidyl transferase center

Journal of Molecular Biology

Volumn 294, Issue 1, 1999, Pages 93-101

  Kloss, Patricia ^a   Xiong, Liqun ^a   Shinabarger, Dean L ^b   Mankin, Alexander S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b PFIZER INC   (United States)

Author keywords

Antibiotics; Drug resistance; Oxazolidinone; Peptidyl transferase; Ribosome

Indexed keywords

AGAR; LINEZOLID; OXAZOLIDINONE DERIVATIVE; PEPTIDYLTRANSFERASE; PROTEIN SYNTHESIS INHIBITOR; RNA 16S; RNA 23S;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM MUTANT; CONTROLLED STUDY; DRUG BINDING; ENZYME INHIBITION; GENE CLUSTER; HALOBACTERIUM SALINARUM; NONHUMAN; OPERON; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN;

ARCHAEA; BACTERIA (MICROORGANISMS); HALOBACTERIUM HALOBIUM; HALOBACTERIUM SALINARUM; PROKARYOTA;

EID: 0033584879     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3247     Document Type: Article

References (42)

1. Allen P. N., Noller H. F. A single base substitution in 16 S ribosomal RNA supresses streptomycin dependence and increases the frequency of translational errors. Cell. 66:1991;141-148.
2. Blanc H., Adams C. W., Wallace D. C. Different nucleotide changes in the large rRNA gene of the mitochondrial DNA confer chloramphenicol resistance on two human cell lines. Nucl. Acids Res. 9:1981a;5785-5795.
3. Blanc H., Wright C. T., Bibb M. J., Wallace D. C., Clayton D. A. Mitochondrial DNA of chloramphenicol-resistant mouse cells contains a single nucleotide change in the region encoding the 3′ end of the large ribosomal RNA. Proc. Natl Acad. Sci. USA. 78:1981b;3789-3793.
4. Brickner S. J., Hutchinson D. K., Barbachyn M. R., Manninen P. R., Ulanowicz D. A., Garmon S. A., Grega K. C., Hendges S. K. et al. Synthesis and antibacterial activity of U-100592 and U-100766, two oxazolidinone antibacterial agents for the potential treatment of multidrug-resistant gram-positive bacterial infections. J. Med. Chem. 39:1996;673-679.
5. Burghardt H., Schimz K. L., Müller M. On the target of a novel class of antibiotics, oxazolidinones, active against multidrug-resistant Gram-positive bacteria. FEBS Letters. 425:1998;40-44.
6. Chang F. N., Siddhikol C., Weisblum B. Subunit localization of antibiotic inhibitors of protein biosynthesis. Biochim. Biophys. Acta. 186:1969;396-398.
7. Cline S. W., Lam W. L., Charlebois R. L., Schalkwyk L. C., Doolittle W. F. Transformation methods for halophilic archaebacteria. Can. J. Microbiol. 35:1989;148-152.
8. Douthwaite S. Functional interactions within 23 S rRNA involving the peptidyl transferase center. J. Bacteriol. 174:1992;1333-1338.
9. Egebjerg J., Douthwaite S., Garrett R. A. Antibiotic interactions at the GTPase-associated centre within Escherichia coli 23 S rRNA. EMBO J. 8:1989;607-611.
10. Eustice D. C., Feldman P. A., Zajac I., Slee A. M. Mechanism of action of DuP 721: inhibition of an early event during initiation of protein synthesis. Antimicrob. Agents Chemother. 32:1988;1218-1222.
11. Fourmy D., Yoshizawa S., Puglisi J. D. Paromomycin binding induces a local conformational change in the A-site of 16 S rRNA. J. Mol. Biol. 277:1998;333-345.
12. Garrett R. A., Rodriguez-Fonseca C. The peptidyl transferase center. Zimmermann R. A., Dahlberg A. E. Ribosomal RNA: Structure, Evolution, Processing, and Function in Protein Biosynthesis. 1996;327-355 CRC Press, Boca Raton.
13. Green R., Noller H. F. Ribosomes and translation. Annu. Rev. Biochem. 66:1997;679-716.
14. Hansen L. H., Mauvais P., Douthwaite S. The macrolide-ketolide antibiotic binding site is formed by structures in domains II and V of 23 S ribosomal RNA. Mol. Microbiol. 31:1999;623-632.
15. Hofman J. D., Lau R. H., Doolittle W. F. The number, physical organization and transcription of ribosomal RNA cistrons in archaebacterium Halobacterium halobium. Nucl. Acids Res. 7:1979;1321-1333.
16. Hummel H., Böck A. 23 S ribosomal RNA mutations in halobacteria conferring resistance to the anti-80S ribosome-targeted antibiotic anisomycin. Nucl. Acids Res. 15:1987a;2431-2442.
17. Hummel H., Böck A. Thiostrepton resistance mutations in the gene for 23 S ribosomal RNA of Halobacteria. Biochimie. 69:1987b;857-861.
18. La Teana A., Pon C. L., Gualerzi C. O. Late events in translation initiation. Adjustment of fMet-tRNA in the ribosomal P-site. J. Mol. Biol. 256:1996;667-675.
19. Lázaro E., Rodriguez-Fonseca C., Porse B., Urena D., Garrett R. A., Ballesta J. P. A sparsomycin-resistant mutant of Halobacterium salinarium lacks a modification at nucleotide U2603 in the peptidyl transferase centre of 23 S rRNA. J. Mol. Biol. 261:1996;231-238.
20. Leviev I. G., Rodriguez-Fonseca C., Phan H., Garrett R. A., Heilek G., Noller H. F., Mankin A. S. A conserved secondary structural motif in 23 S rRNA defines the site of interaction of amicetin, a universal inhibitor of peptide bond formation. EMBO J. 13:1994;1682-1686.
21. Lin A. H., Murray R. W., Vidmar T. J., Marotti K. R. The oxazolidinone eperezolid binds to the 50 S ribosomal subunit and competes with binding of chloramphenicol and lincomycin. Antimicrob. Agents Chemother. 41:1997;2127-2131.
22. Mankin A. S. Selection for spontaneous and engineered mutations in the rRNA genes in halophilic archaea. Robb F. T., Place A. R., Sowers K. R., Schreier H. J., DasSarma S., Fleischmann E. M. Archaea, A Laboratoy Manual. 1995;209-216 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
23. Mankin A. S. Pactamycin resistance mutations in functional sites of 16 S rRNA. J. Mol. Biol. 274:1997;8-15.
24. Mankin A. S., Garrett R. A. Chloramphenicol resistance mutations in the single 23 S rRNA gene of the archaeon Halobacterium halobium. J. Bacteriol. 173:1991;3559-3563.
25. Mankin A. S., Kagramanova V. K. Complete nucleotide sequence of the single ribosomal RNA operon of Halobacterium halobium: secondary structure of the archaebacterial 23 S rRNA. Mol. Gen. Genet. 202:1996;152-161.
26. Mankin A. S., Zyrianova I. M., Kagramanova V. K., Garrett R. A. Introducing mutations into the single-copy chromosomal 23 S rRNA gene of the archaeon Halobacterium halobium by using an rRNA operon-based transformation system. Proc. Natl Acad. Sci. USA. 89:1992;6535-6539.
27. Matassova N. B., Rodnina M. V., Endermann R., Kroll H. P., Pleiss U., Wild H., Wintermeyer W. Ribosomal RNA is the target for oxazolidinones, a novel class of translational inhibitors. RNA. 5:1999;939-946.
28. Moazed D., Noller H. F. Chloramphenicol, erythromycin, carbomycin and vernamycin B protect overlapping sites in the peptidyl transferase region of 23 S ribosomal RNA. Biochimie. 69:1987;879-884.
29. Monro R. E., Marcker K. A. Ribosome-catalysed reaction of puromycin with a formylmethionine-containing oligonucleotide. J. Mol. Biol. 25:1967;347-350.
30. Porse B. T., Garrett R. A. Sites of interaction of streptogramin A and B antibiotics in the peptidyl transferase loop of 23 S rRNA and the synergism of their inhibitory mechanisms. J. Mol. Biol. 286:1999;375-387.
31. Porse B. T., Leviev I., Mankin A. S., Garrett R. A. The antibiotic thiostrepton inhibits a functional transition within protein L11 at the ribosomal GTPase centre. J. Mol. Biol. 276:1998;391-404.
32. Porse B. T., Kirillov S. V., Awayez M. J., Ottenheijm H. C., Garrett R. A. Direct crosslinking of the antitumor antibiotic sparsomycin, and its derivatives, to A2602 in the peptidyl transferase center of 23 S-like rRNA within ribosome-tRNA complexes. Proc. Natl Acad. Sci. USA. 96:1999a;9003-9008.
33. Porse B. T., Kirillov S. V., Awayez M. J., Garrett R. A. UV-induced modifications in the peptidyl transferase loop of 23 S rRNA dependent on binding of the streptogramin B antibiotic, pristinamycin IA. RNA. 5:1999b;585-595.
34. Shinabarger D. L., Marotti K. R., Murray R. W., Lin A. H., Melchior E. P., Swaney S. M., Dunyak D. S., Demyan W. F. et al. Mechanism of action of oxazolidinones: Effects of linezolid and eperezolid on translation reactions. Antimicrob. Agents Chemother. 41:1997;2132-2136.
35. Slee A. M., Wuonola M. A., McRipley R. J., Zajac I., Zawada M. J., Bartholomew P. T., Gregory W. A., Forbes M. Oxazolidinones, a new class of synthetic antibacterial agents: in vitro and in vivo activities of DuP 105 and DuP 721. Antimicrob. Agents Chemother. 31:1987;1791-1797.
36. Stoeckenius W., Kunau W. H. Further characterization of particulate fractions from lysed cell envelopes of Halobacterium halobium and isolation of gas vacuole membranes. J. Cell Biol. 38:1968;337-357.
37. Swaney S. M., Aoki H., Ganoza M. C., Shinabarger D. L. The oxazolidinone linezolid inhibits initiation of protein synthesis in bacteria. Antimicrob. Agents Chemother. 42:1998a;3251-3255.
38. Swaney S. M., Shinabarger D. L., Schaadt R. D., Bock J. H., Slightom J. L., Zurenko G. E. Oxazolidinone resistance is associated with a mutation in the peptidyl transferase region of 23 S rRNA. Abstracts of the 38th Interscience Conference on Antimicrobial Agents and Chemotherapy. 1998b;American Society for Microbiology, San Diego. p. 98-99.
39. Tan G. T., DeBlasio A., Mankin A. S. Mutations in the peptidyl transferase center of 23 S rRNA reveal the site of action of sparsomycin, a universal inhibitor of translation. J. Mol. Biol. 261:1996;222-230.
40. Weisblum B. Erythromycin resistance by ribosome modification. Antimicrob. Agents Chemother. 39:1995;577-585.
41. Wower J., Wower I. K., Kirillov S. V., Rosen K. V., Hixson S. S., Zimmermann R. A. Peptidyl transferase and beyond. Biochem. Cell Biol. 73:1995;1041-1047.
42. Xiong L., Shah S., Mauvais P., Mankin A. S. A ketolide resistance mutation in domain II of 23 S rRNA reveals proximity of hairpin 35 to the peptidyl transferase centre. Mol. Microbiol. 31:1999;633-639.