A structural basis for streptomycin-induced misreading of the genetic code

Nature Communications

Volumn 4, Issue , 2013, Pages

  Demirci, Hasan ^a   Murphy, Frank ^b   Murphy, Eileen ^a   Gregory, Steven T ^a   Dahlberg, Albert E ^a   Jogl, Gerwald ^a  

^a BROWN UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBOSOME PROTEIN; RIBOSOME RNA; RNA 16S; STREPTOMYCIN;

AMINO ACID; CRYSTAL STRUCTURE; GENETIC ENGINEERING; GENETIC STRUCTURE; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; RNA;

3' UNTRANSLATED REGION; ANTICODON; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENETIC CODE; HYDROGEN BOND; PROTEIN RNA BINDING; RIBOSOME SUBUNIT; RNA STRUCTURE; THERMUS THERMOPHILUS; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DRUG EFFECT; GENETICS; OPEN READING FRAME; SMALL RIBOSOMAL SUBUNIT; STATIC ELECTRICITY;

CRYSTALLOGRAPHY, X-RAY; GENETIC CODE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; OPEN READING FRAMES; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, RIBOSOMAL, 16S; STATIC ELECTRICITY; STREPTOMYCIN; THERMUS THERMOPHILUS;

MLCS; MLOWN;

EID: 84879178582     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2346     Document Type: Article

References (46)

1. Poehlsgaard, J. & Douthwaite, S. The bacterial ribosome as a target for antibiotics. Nat. Rev. Microbio. 3, 870-881 (2005). (Pubitemid 41693182)
2. Gale, E.F., Cundliffe, E., Reynolds, P.E., Richmond, M.H. & Waring, M.J. The Molecular Basis of Antibiotic Action 402-547 (Wiley & Sons, 1981).
3. Gorini, L., Gundersen, W. & Burger, M. Genetics of regulation of enzyme synthesis in the arginine biosynthetic pathway of Escherichia coli. Cold Spring Harbor Symp. Quant. Biol. 26, 173-182 (1961).
4. Davies, J., Gilbert, W. & Gorini, L. Streptomycin, suppression, and the code. Proc. Natl Acad. Sci. USA 51, 883-890 (1964).
5. Gorini, L., Jacoby, G.A. & Breckenridge, L. Ribosomal ambiguity. Cold Spring Harbor Symp. Quant. Biol. 31, 657-664 (1966).
6. Gromadski, K.B. & Rodnina, M.V. Streptomycin interferes with conformational coupling between codon recognition and GTPase activation on the ribosome. Nat. Struct. Mol. Biol. 11, 316-322 (2004). (Pubitemid 38436795)
7. Gromadski, K.B. & Rodnina, M.V. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell 13, 191-200 (2004). (Pubitemid 38183266)
8. Carter, A.P. et al. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407, 340-348 (2000).
9. Ogle, J.M. et al. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292, 897-902 (2001). (Pubitemid 32422480)
10. Clemons, Jr W.M. et al. Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: purification, crystallization and structure determination. J. Mol. Biol. 310, 827-843 (2001). (Pubitemid 32695698)
11. Demirci, H. et al. Modification of 16S ribosomal RNA by the KsgA methyltransferase restructures the 30S subunit to optimize ribosome function. RNA 16, 2319-2324 (2010).
12. Wimberly, B.T. et al. Structure of the 30S ribosomal subunit. Nature 407, 327-339 (2000).
13. Ogle, J.M., Murphy, F.V., Tarry, M.J. & Ramakrishnan, V. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111, 721-732 (2002). (Pubitemid 35446316)
14. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221, 2010).
15. Walter, F., Vicens, Q. & Westhof, E. Aminoglycoside-RNA interactions. Curr. Opin. Chem. Biol. 3, 694-704 (1999).
16. Willis, B. & Arya, D.P. An expanding view of aminoglycoside-nucleic acid recognition. Adv. Carbohydr. Chem. Biochem. 60, 251-302 (2006). (Pubitemid 43783388)
17. Davies, J. & Davis, B.D. Misreading of ribonucleic acid code words induced by aminoglycoside antibiotics. The effect of drug concentration. J. Biol. Chem. 243, 3312-3316 (1968).
18. Dahlberg, A.E., Horodyski, F. & Keller, P. Interaction of neomycin with ribosomes and ribosomal ribonucleic acid. Antimicrob. Agents Chemother. 13, 331-339 (1978). (Pubitemid 8281002)
19. Sharma, D., Cukras, A.R., Rogers, E.J., Southworth, D.R. & Green, R. Mutational analysis of S12 protein and implications for the accuracy of decoding by the ribosome. J. Mol. Biol. 374, 1065-1076 (2007). (Pubitemid 350052100)
20. Borovinskaya, M.A. et al. Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat. Struct. Mol. Biol. 14, 727-732 (2007). (Pubitemid 47220057)
21. Li, M., Tzagoloff, A., Underbrink-Lyon, K. & Martin, N.C. Identification of the paromomycin-resistance mutation in the 15 S rRNA gene of yeast mitochondria. J. Biol. Chem. 257, 5921-5928 (1982). (Pubitemid 12012053)
22. Spangler, E.A. & Blackburn, E.H. The nucleotide sequence of the 17S ribosomal RNA gene of Tetrahymena thermophila and the identification of point mutations resulting in resistance to the antibiotics paromomycin and hygromycin. J. Biol. Chem. 260, 6334-6340 (1985). (Pubitemid 15071338)
23. Carter, A.P. et al. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291, 498-501 (2001). (Pubitemid 32097077)
24. Senior, B.W. & Holland, I.B. Effect of colicin E3 upon the 30S ribosomal subunit of Escherichia coli. Proc. Natl Acad. Sci. USA 68, 959-963 (1971).
25. Ng, C.L. et al. Structural basis for 16S ribosomal RNA cleavage by the cytotoxic domain of colicin E3. Nat. Struct. Mol. Biol. 17, 1241-1246 (2010).
26. Milon, P., Konevega, A.L., Gualerzi, C.O. & Rodnina, M.V. Kinetic checkpoint at a late step in translation initiation. Mol. Cell 30, 712-720 (2008). (Pubitemid 351815123)
27. Dahlberg, A.E., Lund, E., Kjeldgaard, N.O., Bowman, C.M. & Nomura, M. Colicin E3 induced cleavage of 16S ribosomal ribonucleic acid; blocking effects of certain antibiotics. Biochemistry 12, 948-950 (1973).
28. Johansson, M., Zhang, J. & Ehrenberg, M. Genetic code translation displays a linear trade-off between efficiency and accuracy of tRNA selection. Proc. Natl Acad. Sci. USA 109, 131-136 (2012).
29. Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. & Yusupova, G. A new understanding of the decoding principle on the ribosome. Nature 484, 256-259 (2012).
30. Gregory, S.T., Carr, J.F. & Dahlberg, A.E. A mutation in the decoding center of Thermus thermophilus 16S rRNA suggests a novel mechanism of streptomycin resistance. J. Bacteriol. 187, 2200-2202 (2005). (Pubitemid 40316251)
31. Lynch, S.R. & Puglisi, J.D. Structural origins of aminoglycoside specificity for prokaryotic ribosomes. J. Mol. Biol. 306, 1037-1058 (2001). (Pubitemid 33030004)
32. Lynch, S.R., Gonzalez, R.L. & Puglisi, J.D. Comparison of X-ray crystal structure of the 30S subunit-antibiotic complex with NMR structure of decoding site oligonucleotide-paromomycin complex. Structure 11, 43-53 (2003). (Pubitemid 36071495)
33. Rabl, J., Leibundgut, M., Ataide, S.F., Haag, A. & Ban, N. Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 331, 730-736 (2011).
34. Pioletti, M. et al. Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J. 20, 1829-1839 (2001). (Pubitemid 32397386)
35. Yusupova, G.Z., Yusupov, M.M., Cate, J.H.D. & Noller, H.F. The path of messenger RNA through the ribosome. Cell 106, 233-241 (2001). (Pubitemid 32772633)
36. Poldermans, B., Van Buul, C.P. & Van Knippenberg, P.H. Studies on the function of two adjacent N6, N6-dimethyladenosines near the 3 end of 16 S ribosomal RNA of Escherichia coli. II. The effect of the absence of the methyl groups on initiation of protein biosynthesis. J. Biol. Chem. 254, 9090-9093 (1979).
37. Poldermans, B., Bakker, H. & Van Knippenberg, P.H. Studies on the function of two adjacent N6, N6-dimethyladenosines near the 3 end of 16S ribosomal RNA of Escherichia coli. IV. The effect of the methylgroups on ribosomal subunit interaction. Nucleic Acids Res. 8, 143-151 (1980). (Pubitemid 10154679)
38. van Buul, C.P., Visser, W. & van Knippenberg, P.H. Increased translational fidelity caused by the antibiotic kasugamycin and ribosomal ambiguity in mutants harbouring the ksgA gene. FEBS Lett. 177, 119-124 (1984). (Pubitemid 15216046)
39. Lelong, J.C., Gros, D., Cousin, M.A., Grunberg-Manago, M. & Gros, F. Streptomycin induced release of fMet-tRNA from the ribosomal initiation complex. Biochem. Biophys. Res. Commun. 42, 530-537 (1971).
40. Modolell, J. & Davis, B.D. Breakdown by streptomycin of initiation complexes formed on ribosomes of Escherichia coli. Proc. Natl Acad. Sci. USA 67, 1148-1155 (1970).
41. Qin, D., Liu, Q., Devaraj, A. & Fredrick, K. Role of helix 44 of 16S rRNA in the fidelity of translation initiation. RNA 18, 485-495 (2012).
42. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
43. Kabsch, W. XDS. Acta. Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
44. Kurata, S. et al. Modified uridines with C5-methylene substituents at the first position of the tRNA anticodon stabilize U.G wobble pairing during decoding. J. Biol. Chem. 283, 18801-18811 (2008).
45. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta. Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
46. Schroedinger, L. The PyMOL Molecular Graphics System. Version 1.5 (Schroedinger, 2012).