Context-specific inhibition of translation by ribosomal antibiotics targeting the peptidyl transferase center

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

Volumn 113, Issue 43, 2016, Pages 12150-12155

  Marks, James ^a   Kannan, Krishna ^a,b   Roncase, Emily J ^a,c   Klepacki, Dorota ^a   Kefi, Amira ^a   Orelle, Cédric ^a,d   Vázquez Laslop, Nora ^a   Mankin, Alexander S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b Synthetic Genomics Inc   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITÉ LYON 1   (France)

Author keywords

Antibiotics; Nascent peptide; Oxazolidinones; Protein synthesis; Ribosome

Indexed keywords

ALANINE; AMINOACYL TRANSFER RNA; CHLORAMPHENICOL; GLYCINE; LINEZOLID; MESSENGER RNA; PEPTIDYLTRANSFERASE; SERINE; THREONINE; AMINO ACID; PROTEIN BINDING;

BACTERIAL CELL; CONFERENCE PAPER; CONTROLLED STUDY; DRUG MECHANISM; DRUG TARGETING; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN TARGETING; RIBOSOME; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULAR MODEL;

AMINO ACIDS; BINDING SITES; CHLORAMPHENICOL; ESCHERICHIA COLI; LINEZOLID; MODELS, MOLECULAR; PEPTIDYL TRANSFERASES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, TRANSFER, AMINO ACYL;

EID: 84992358910     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1613055113     Document Type: Article

References (47)

1. Beringer M, Rodnina MV (2007) The ribosomal peptidyl transferase. Mol Cell 26(3):311-321.
2. Weinger JS, Parnell KM, Dorner S, Green R, Strobel SA (2004) Substrate-assisted catalysis of peptide bond formation by the ribosome. Nat Struct Mol Biol 11(11):1101-1106.
3. Erlacher MD, et al. (2005) Chemical engineering of the peptidyl transferase center reveals an important role of the 2'-hydroxyl group of A2451. Nucleic Acids Res 33(5):1618-1627.
4. Polikanov YS, Steitz TA, Innis CA (2014) A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. Nat Struct Mol Biol 21(9):787-793.
5. Polacek N, Gaynor M, Yassin A, Mankin AS (2001) Ribosomal peptidyl transferase can withstand mutations at the putative catalytic nucleotide. Nature 411(6836):498-501.
6. Youngman EM, Brunelle JL, Kochaniak AB, Green R (2004) The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 117(5):589-599.
7. Sievers A, Beringer M, Rodnina MV, Wolfenden R (2004) The ribosome as an entropy trap. Proc Natl Acad Sci USA 101(21):7897-7901.
8. Wilson DN (2009) The A-Z of bacterial translation inhibitors. Crit Rev Biochem Mol Biol 44(6):393-433.
9. Pestka S (1975) Chloramphenicol. Antibiotics: Mechanism of Action of Antimicrobial and Antitumor Agents, eds Corcoran JW, Hahn FE (Springer, Berlin), Vol III, pp 370-395.
10. Dunkle JA, Xiong L, Mankin AS, Cate JH (2010) Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc Natl Acad Sci USA 107(40):17152-17157.
11. Bulkley D, Innis CA, Blaha G, Steitz TA (2010) Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc Natl Acad Sci USA 107(40):17158-17163.
12. Schlünzen F, et al. (2001) Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413(6858):814-821.
13. Wilson DN (2011) On the specificity of antibiotics targeting the large ribosomal subunit. Ann N Y Acad Sci 1241:1-16.
14. Kucan Z, Lipmann F (1964) Differences in chloramphenicol sensitivity of cell-free amino acid polymerization systems. J Biol Chem 239(2):516-520.
15. Vazquez D (1966) Antibiotics affecting chloramphenicol uptake by bacteria. Their effect on amino acid incorporation in a cell-free system. Biochim Biophys Acta 114(2):289-295.
16. Cannon M (1968) The puromycin reaction and its inhibition by chloramphenicol. Eur J Biochem 7(1):137-145.
17. Lovett PS (1990) Translational attenuation as the regulator of inducible cat genes. J Bacteriol 172(1):1-6.
18. Kloss P, Xiong L, Shinabarger DL, Mankin AS (1999) Resistance mutations in 23 S rRNA identify the site of action of the protein synthesis inhibitor linezolid in the ribosomal peptidyl transferase center. J Mol Biol 294(1):93-101.
19. Leach KL, et al. (2007) The site of action of oxazolidinone antibiotics in living bacteria and in human mitochondria. Mol Cell 26(3):393-402.
20. Wilson DN, et al. (2008) The oxazolidinone antibiotics perturb the ribosomal peptidyltransferase center and effect tRNA positioning. Proc Natl Acad Sci USA 105(36):13339-13344.
21. Ippolito JA, et al. (2008) Crystal structure of the oxazolidinone antibiotic linezolid bound to the 50S ribosomal subunit. J Med Chem 51(12):3353-3356.
22. Shinabarger DL, et al. (1997) Mechanism of action of oxazolidinones: Effects of linezolid and eperezolid on translation reactions. Antimicrob Agents Chemother 41(10):2132-2136.
23. Lin AH, Murray RW, Vidmar TJ, Marotti KR (1997) The oxazolidinone eperezolid binds to the 50S ribosomal subunit and competes with binding of chloramphenicol and lincomycin. Antimicrob Agents Chemother 41(10):2127-2131.
24. Hartz D, McPheeters DS, Traut R, Gold L (1988) Extension inhibition analysis of translation initiation complexes. Methods Enzymol 164:419-425.
25. Orelle C, et al. (2013) Tools for characterizing bacterial protein synthesis inhibitors. Antimicrob Agents Chemother 57(12):5994-6004.
26. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324(5924):218-223.
27. Davis AR, Gohara DW, Yap MN (2014) Sequence selectivity of macrolide-induced translational attenuation. Proc Natl Acad Sci USA 111(43):15379-15384.
28. Kannan K, et al. (2014) The general mode of translation inhibition by macrolide antibiotics. Proc Natl Acad Sci USA 111(45):15958-15963.
29. Nakahigashi K, et al. (2016) Comprehensive identification of translation start sites by tetracycline-inhibited ribosome profiling. DNA Res 23(3):193-201.
30. Oh E, et al. (2011) Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147(6):1295-1308.
31. Becker AH, Oh E, Weissman JS, Kramer G, Bukau B (2013) Selective ribosome profiling as a tool for studying the interaction of chaperones and targeting factors with nascent polypeptide chains and ribosomes. Nat Protoc 8(11):2212-2239.
32. Kannan K, Vázquez-Laslop N, Mankin AS (2012) Selective protein synthesis by ribosomes with a drug-obstructed exit tunnel. Cell 151(3):508-520.
33. Lovett PS (1996) Translation attenuation regulation of chloramphenicol resistance in bacteria-a review. Gene 179(1):157-162.
34. Alexieva Z, Duvall EJ, Ambulos NP, Jr, Kim UJ, Lovett PS (1988) Chloramphenicol induction of cat-86 requires ribosome stalling at a specific site in the leader. Proc Natl Acad Sci USA 85(9):3057-3061.
35. Li GW, Oh E, Weissman JS (2012) The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484(7395):538-541.
36. Nakahigashi K, et al. (2014) Effect of codon adaptation on codon-level and gene-level translation efficiency in vivo. BMC Genomics 15:1115.
37. Mohammad F, Woolstenhulme CJ, Green R, Buskirk AR (2016) Clarifying the translational pausing landscape in bacteria by ribosome profiling. Cell Rep 14(4):686-694.
38. Sothiselvam S, et al. (2016) Binding of macrolide antibiotics leads to ribosomal selection against specific substrates based on their charge and size. Cell Rep 16(7):1789-1799.
39. Starosta AL, et al. (2010) Interplay between the ribosomal tunnel, nascent chain, and macrolides influences drug inhibition. Chem Biol 17(5):504-514.
40. Lovett PS (1994) Nascent peptide regulation of translation. J Bacteriol 176(21):6415-6417.
41. Ito K, Chiba S (2013) Arrest peptides: Cis-acting modulators of translation. Annu Rev Biochem 82:171-202.
42. Afgan E, et al. (2016) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res 44(W1):W3-W10.
43. Vazquez-Laslop N, Thum C, Mankin AS (2008) Molecular mechanism of drugdependent ribosome stalling. Mol Cell 30(2):190-202.
44. Orelle C, et al. (2013) Identifying the targets of aminoacyl-tRNA synthetase inhibitors by primer extension inhibition. Nucleic Acids Res 41(14):e144.
45. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-675.
46. Arenz S, et al. (2014) Molecular basis for erythromycin-dependent ribosome stalling during translation of the ErmBL leader peptide. Nat Commun 5:3501.
47. O'Shea JP, et al. (2013) pLogo: A probabilistic approach to visualizing sequence motifs. Nat Methods 10(12):1211-1212.