Structural analysis of base substitutions in Thermus thermophilus 16S rRNA conferring streptomycin resistance

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 8, 2014, Pages 4308-4317

  Demirci, Hasan ^a   Murphy IV, Frank V ^b   Murphy, Eileen L ^a   Connetti, Jacqueline L ^a   Dahlberg, Albert E ^a   Jogl, Gerwald ^a   Gregory, Steven T ^a  

^a BROWN UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; RIBOSOMAL PROTEIN S12; RIBOSOME PROTEIN; RNA 16S; STREPTOMYCIN;

ANTIBIOTIC RESISTANCE; BASE PAIRING; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DRUG EFFECTS; GENETICS; HYDROGEN BOND; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POINT MUTATION; PROTEIN SYNTHESIS; SMALL RIBOSOMAL SUBUNIT; THERMUS THERMOPHILUS; X RAY CRYSTALLOGRAPHY;

ANTI-BACTERIAL AGENTS; BASE PAIRING; BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; POINT MUTATION; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, RIBOSOMAL, 16S; STREPTOMYCIN; THERMUS THERMOPHILUS;

EID: 84905390334     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02857-14     Document Type: Article

References (62)

1. Gale EF, Cundliffe E, Reynolds PE, Richmond MH, Waring MJ. 1981. The molecular basis of antibiotic action. John Wiley & Sons, London, United Kingdom.
2. Poehlsgaard J, Douthwaite S. 2005. The bacterial ribosome as a target for antibiotics. Nat. Rev. Microbiol. 3:870-881. http://dx.doi.org/10.1038/ nrmicro1265.
3. Moazed D, Noller HF. 1987. Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327:389-394. http://dx.doi.org/10.1038/ 327389a0.
4. Fourmy D, Recht MI, Blanchard SC, Puglisi JD. 1996. Structure of the A site of Escherichia coli16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274:1367-1371. http://dx.doi.org/10.1126/science.274.5291. 1367.
5. Vicens Q, Westhof E. 2001. Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Structure 9:647-658. http://dx.doi.org/10.1016/S0969-2126 (01) 00629-3.
6. Blaha GM, Polikanov YS, Steitz TA. 2012. Elements of ribosomal drug resistance and specificity. Curr. Opin. Struct. Biol. 22:750-758. http://dx.doi.org/10.1016/j.sbi.2012.07.016.
7. Fourmy D, Yoshizawa S, Puglisi JD. 1998. Paromomycin binding induces a local conformational change in the A-site of 16 S rRNA. J. Mol. Biol. 277:333-345. http://dx.doi.org/10.1006/jmbi.1997.1551.
8. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407:340-348. http://dx.doi.org/10.1038/35030019.
9. Ogle JM, Brodersen DE, Clemons WM, Tarry MJ, Carter AP, Ramakrishnan V. 2001. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292:897-902. http://dx.doi.org/10.1126/science.1060612.
10. Ozaki M, Mizushima S, Nomura M. 1969. Identification and functional characterization of the protein controlled by the streptomycin-resistant locus in E. coli. Nature 222:333-339. http://dx.doi.org/10.1038/222333a0.
11. Funatsu G, Wittmann HG. 1972. Ribosomal proteins. XXXIII. Location of amino-acid replacements in protein S12 isolated from Escherichia coli mutants resistant to streptomycin. J. Mol. Biol. 68:547-550.
12. Montandon PE, Nicolas P, Schürmann P, Stutz E. 1985. Streptomycinresistance of Euglena gracilis chloroplasts: identification of a point mutation in the 16S rRNA gene in an invariant position. Nucleic Acids Res. 13:4299-4310. http://dx.doi.org/10.1093/nar/13.12.4299.
13. Gauthier A, Turmel M, Lemieux C. 1988. Mapping of chloroplast mutations conferring resistance to antibiotics in Chlamydomonas: evidence for a novel site of streptomycin resistance in the small subunit rRNA. Mol. Gen. Genet. 214:192-197. http://dx.doi.org/10.1007/BF00337710.
14. Harris EH, Burkhart BD, Gillham NW, Boynton JE. 1989. Antibiotic resistance mutations in the chloroplast 16S and 23S rRNA genes of Chlamydomonas reinhardtii: correlation of genetic and physical maps of the chloroplast genome. Genetics 123:281-292.
15. Yeh KC, To KY, Sun SW, Wu MC, Lin TY, Chen CC. 1994. Point mutations in the chloroplast 16S rRNA gene confer streptomycin resistance in Nicotiana plumbaginifolia. Curr. Genet. 26:132-135. http://dx.doi.org/10.1007/BF00313800.
16. Honoré N, Cole ST. 1994. Streptomycin resistance in mycobacteria. Antimicrob. Agents Chemother. 38:238-242. http://dx.doi.org/10.1128/AAC.38.2. 238.
17. Meier A, Kirschner P, Bange FC, Vogel U, Böttger EC. 1994. Genetic alterations in streptomycin-resistant Mycobacterium tuberculosis: mapping of mutations conferring resistance. Antimicrob. Agents Chemother. 38:228-233. http://dx.doi.org/10.1128/AAC.38.2.228.
18. Springer B, Kidan YG, Prammananan T, Ellrott K, Böttger EC, Sander P. 2001. Mechanisms of streptomycin resistance: selection ofmutations in the 16S rRNA gene conferring resistance. Antimicrob. Agents Chemother. 45:2877-2884. http://dx.doi.org/10.1128/AAC.45.10.2877-2884.2001.
19. Melançon P, Lemieux C, Brakier-Gingras L. 1988. A mutation in the 530 loop of Escherichia coli 16S ribosomal RNA causes resistance to streptomycin. Nucleic Acids Res. 16:9631-9639. http://dx.doi.org/10.1093/nar/16. 20.9631.
20. Frattali AL, Flynn MK, De Stasio EA, Dahlberg AE. 1990. Effects of mutagenesisof C912in the streptomycin binding region of Escherichia coli 16S ribosomal RNA. Biochim. Biophys. Acta 1050:27-33. http://dx.doi.org/10.1016/ 0167-4781 (90) 90136-P.
21. Leclerc D, Melançon P, Brakier-Gingras L. 1991. Mutations in the 915 region of Escherichia coli 16S ribosomal RNA reduce the binding of streptomycin to the ribosome. Nucleic Acids Res. 19:3973-3977. http://dx.doi.org/10.1093/nar/19.14.3973.
22. Pinard R, Payant C, Melançon P, Brakier-Gingras L. 1993. The 5= proximal helix of 16S rRNA is involved in the binding of streptomycin to the ribosome. FASEB J. 7:173-176.
23. Powers T, Noller HF. 1991. A functional pseudoknot in 16S ribosomal RNA. EMBO J. 10:2203-2214.
24. Gregory ST, Dahlberg AE. 2009. Genetic and structural analysis of base substitutions in the central pseudoknot of Thermus thermophilus 16S ribosomal RNA. RNA 15:215-223. http://dx.doi.org/10.1261/rna.1374809.
25. 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. http://dx.doi.org/10.1016/j.cell.2005.02.005.
26. Blaha G, Gurel G, Schroeder SJ, Moore PB, Steitz TA. 2008. Mutations outside the anisomycin-binding site can make ribosomes drug-resistant. J. Mol. Biol. 379:505-519. http://dx.doi.org/10.1016/j.jmb.2008.03.075.
27. Demirci H, Wang L, Murphy FV, Murphy EL, Carr JF, Blanchard SC, Jogl G, Dahlberg AE, Gregory ST. 2013. The central role of protein S12 in organizing the structure of the decoding site of the ribosome. RNA 19:1791-1801. http://dx.doi.org/10.1261/rna.040030.113.
28. Davies J, Gilbert W, Gorini L. 1964. Streptomycin, suppression, and the code. Proc. Natl. Acad. Sci. U. S. A. 51:883-890. http://dx.doi.org/10.1073/ pnas.51.5.883.
29. Demirci H, Murphy F, IV, Murphy E, Gregory ST, Dahlberg AE, Jogl G. 2013. A structural basis for streptomycin-induced misreading of the genetic code. Nat. Commun. 4:1355. http://dx.doi.org/10.1038/ncomms2346.
30. Timms AR, Steingrimsdottir H, Lehmann AR, Bridges BA. 1992. Mutant sequences in the rpsL gene of Escherichia coli B/r: mechanistic implications for spontaneous and ultraviolet light mutagenesis. Mol. Gen. Genet. 232:89-96. http://dx.doi.org/10.1007/BF00299141.
31. Timms AR, Bridges BA. 1993. Double, independent mutational events in the rpsL gene of Escherichia coli: an example of hypermutability? Mol. Microbiol. 9:335-342. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01694.x.
32. Björkman J, Samuelsson P, Andersson DI, Hughes D. 1999. Novel ribosomal mutations affecting translational accuracy, antibiotic resistance and virulence of Salmonella typhimurium. Mol. Microbiol. 31:53-58. http://dx.doi.org/10.1046/j.1365-2958.1999.01142.x.
33. Okamoto S, Tamaru A, Nakajima C, Nishimura K, Tanaka Y, Tokuyama S, Suzuki Y, Ochi K. 2007. Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol. Microbiol. 63:1096-1106. http://dx.doi.org/10.1111/j.1365-2958.2006.05585.x.
34. Nishimura K, Johansen SK, Inaoka T, Hosaka T, Tokuyama S, Tahara Y, Okamoto S, Kawamura F, Douthwaite S, Ochi K. 2007. Identification of the RsmG methyltransferase target as 16S rRNA nucleotide G527 and characterization of Bacillus subtilis rsmG mutants. J. Bacteriol. 189:6068-6073. http://dx.doi.org/10.1128/JB.00558-07.
35. Gregory ST, Cate J H D, Dahlberg AE. 2001. Streptomycin-resistant and streptomycin-dependent mutants of the extreme thermophile Thermus thermophilus. J. Mol. Biol. 309:333-338. http://dx.doi.org/10.1006/jmbi.2001.4676.
36. Gregory ST, Carr JF, Dahlberg AE. 2005. A mutation in the decoding center of Thermus thermophilus 16S rRNA suggests a novel mechanism of streptomycin resistance. J. Bacteriol. 187:2200-2202. http://dx.doi.org/10.1128/JB.187.6. 2200-2202.2005.
37. Woese CR, Gutell R, Gupta R, Noller HF. 1983. Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol. Rev. 47:621-669.
38. Wimberly BT, Brodersen DE, Clemons WM, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. 2000. Structure of the 30S ribosomal subunit. Nature 407:327-339. http://dx.doi.org/10.1038/35030006.
39. Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M, Janell D, Bashan A, Bartels H, Agmon I, Franceschi F, Yonath A. 2000. Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102:615-623. http://dx.doi.org/10.1016/S0092-8674 (00) 00084-2.
40. Gregory ST, Dahlberg AE. 2008. Transposition of an insertion sequence, ISTth7, in the genome of the extreme thermophile Thermus thermophilus HB8. FEMS Microbiol. Lett. 289:187-192. http://dx.doi.org/10.1111/j.1574-6968.2008.01389. x.
41. Gregory ST, Demirci H, Belardinelli R, Monshupanee T, Gualerzi C, Dahlberg AE, Jogl G. 2009. Structural and functional studies of the Thermus thermophilus 16S rRNA methyltransferase RsmG. RNA 15:1693-1704. http://dx.doi.org/10.1261/rna.1652709.
42. Clemons WM, Jr, Brodersen DE, McCutcheon JP, May J L C, Carter AP, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. 2001. Crystal structure of the 30S ribosomal subunit from Thermus thermophilus: purification, crystallization and structure determination. J. Mol. Biol. 310:827-843. http://dx.doi.org/10. 1006/jmbi.2001.4778.
43. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326. http://dx.doi.org/10.1016/S0076-6879 (97) 76066-X.
44. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221. http://dx.doi.org/10.1107/S0907444909052925.
45. Kurata S, Weixlbaumer A, Ohtsuki T, Shimazaki T, Wada T, Kirino Y, Takai K, Watanabe K, Ramakrishnan V, Suzuki T. 2008. Modified uridines with C5-methylene substituents at the first position of the tRNA stabilize U-G wobble pairing during decoding. J. Biol. Chem. 283:18801-18811. http://dx.doi.org/10. 1074/jbc. M800233200.
46. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501. http://dx.doi.org/ 10.1107/S0907444910007493.
47. Schrödinger L L C. 2012. The PyMOL molecular graphics system, version 1.5. Schrödinger LLC, Mannheim, Germany.
48. Cannone JJ, Subramanian S, Schnare MN, Collett JR, D'Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Müller KM, Pande N, Shang Z, Yu N, Gutell RR. 2002. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:2. http://dx.doi.org/10.1186/1471-2105-3-2.
49. Guymon R, Pomerantz SC, Crain PF, McCloskey JA. 2006. Influence of phylogeny on posttranscriptional modification of rRNA in thermophilic prokaryotes: the complete modification map of 16S rRNA of Thermus thermophilus. Biochemistry 45:4888-4899. http://dx.doi.org/10.1021/bi052579p.
50. Saenger W. 1984. Principles of nucleic acid structure. Springer, New York, NY.
51. Lynch SR, Puglisi JD. 2001. Structural origins of aminoglycoside specificity for prokaryotic ribosomes. J. Mol. Biol. 306:1037-1058. http://dx.doi.org/10.1006/jmbi.2000.4420.
52. Ruusala T, Andersson D, Ehrenberg M, Kurland CG. 1984. Hyperaccurate ribosomes inhibit growth. EMBO J. 3:2575-2580.
53. Kurland CG. 1992. Translational accuracy and the fitness of bacteria. Annu. Rev. Genet. 26:29-50. http://dx.doi.org/10.1146/annurev. ge.26.120192.000333.
54. Pinard R, Côté M, Payant C, Brakier-Gingras L. 1994. Positions 13 and 914 in Escherichia coli 16S ribosomal RNA are involved in the control of translational accuracy. Nucleic Acids Res. 22:619-624. http://dx.doi.org/10.1093/nar/22.4.619.
55. Allen PN, Noller HF. 1989. Mutations in ribosomal proteins S4 and S12 influence the higher order structure of 16 S ribosomal RNA. J. Mol. Biol. 208:457-468. http://dx.doi.org/10.1016/0022-2836 (89) 90509-3.
56. Vaiana AC, Sanbonmatsu KY. 2009. Stochastic gating and drugribosome interactions. J. Mol. Biol. 386:648-661. http://dx.doi.org/10.1016/j.jmb.2008. 12.035.
57. Munro JB, Sanbonmatsu KY, Spahn C M T, Blanchard SC. 2009. Navigating the ribosome's metastable energy landscape. Trends Biochem. Sci. 34:390-400. http://dx.doi.org/10.1016/j.tibs.2009.04.004.
58. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate J H D. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310:827-834. http://dx.doi.org/10.1126/science.1117230.
59. Kowalak JA, Walsh KA. 1996. |3-Methylthio-aspartic acid: identification of a novel posttranslational modification in ribosomal protein S12 from Escherichia coli. Protein Sci. 5:1625-1632. http://dx.doi.org/10.1002/pro. 5560050816.
60. Carr JF, Hamburg D-M, Gregory ST, Limbach PA, Dahlberg AE. 2006. Effects of streptomycin resistance mutations on posttranslational modification of ribosomal protein S12. J. Bacteriol. 188:2020-2023. http://dx.doi.org/10.1128/ JB.188.5.2020-2023.2006.
61. Anton BP, Saleh L, Benner JS, Raleigh EA, Kasif S, Roberts RJ. 2008. RimO, a MiaB-like enzyme, methylthiolates the universally conserved Asp88 residue of ribosomal protein S12 in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 105:1826-1831. http://dx.doi.org/10.1073/pnas.0708608105.
62. Demirci H, Sierra RG, Laksmono H, Shoeman RL, Botha S, Barends T R M, Nass K, Schlichting I, Doak RB, Gati C, Williams GJ, Boutet S, Messerschmidt M, Jogl G, Dahlberg AE, Gregory ST, Bogan MJ. 2013. Serial femtosecond X-ray diffraction of 30S ribosomal subunit microcrystals in liquid suspension at ambient temperature using an X-ray freeelectron laser. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69:1066-1069. http://dx.doi.org/10.1107/ S174430911302099X.