Tetracycline antibiotics and resistance mechanisms

Biological Chemistry

Volumn 395, Issue 5, 2014, Pages 559-575

  Nguyen, Fabian ^a   Starosta, Agata L ^a   Arenz, Stefan ^a   Sohmen, Daniel ^a   Dönhöfer, Alexandra ^a   Wilson, Daniel N ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Glycylcycline; Resistance; Ribosome; Tetracycline; Tigecycline; Translation

Indexed keywords

BACTERIAL PROTEIN; CHLORTETRACYCLINE; DOXYCYCLINE; ERAVACYCLINE; GLYCYLCYCLINE DERIVATIVE; MINOCYCLINE; OMADACYCLINE; OXYTETRACYCLINE; RNA 16S; TETM PROTEIN; TETO PROTEIN; TETRACYCLINE; TIGECYCLINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; TETRACYCLINE DERIVATIVE;

ANTIBIOTIC RESISTANCE; BACTERIUM; DRUG BINDING SITE; DRUG DEGRADATION; DRUG MECHANISM; DRUG STRUCTURE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; RIBOSOME; DRUG RESISTANCE; HUMAN;

ANTI-BACTERIAL AGENTS; DRUG RESISTANCE; HUMANS; TETRACYCLINES;

EID: 84900875411     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2013-0292     Document Type: Review

References (96)

1. Agwuh, K.N. and MacGowan, A. (2006). Pharmacokinetics and pharmacodynamics of the tetracyclines including glycylcyclines. J. Antimicrob. Chemother. 58, 256-265. (Pubitemid 44294934)
2. Backus, E.J., Duggar, B.M., and Campbell, T.H. (1954). Variation in Streptomyces aureofaciens. Ann. NY Acad. Sci. 60, 86-101.
3. Barden, T.C., Buckwalter, B.L., Testa, R.T., Petersen, P.J., and Lee, V.J. (1994). "Glycylcyclines". 3. 9-Aminodoxycyclinecarboxamides. J. Med. Chem. 37, 3205-3211.
4. Barile, S., Devirgiliis, C., and Perozzi, G. (2012). Molecular characterization of a novel mosaic tet(S/M) gene encoding tetracycline resistance in foodborne strains of Streptococcus bovis. Microbiology 158, 2353-2362.
5. Bauer, G., Berens, C., Projan, S., and Hillen, W. (2004). Comparison of tetracycline and tigecycline binding to ribosomes mapped by dimethylsulphate and drug-directed Fe2+ cleavage of 16S rRNA. J. Antimicrob. Chemother. 53, 592-599. (Pubitemid 38499772)
6. Ben-Shem, A., Garreau de Loubresse, N., Melnikov, S., Jenner, L., Yusupova, G., and Yusupov, M. (2011). The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334, 1524-1529.
7. Bergeron, J., Ammirati, M., Danley, D., James, L., Norcia, M., Retsema, J., Strick, C.A., Su, W.G., Sutcliffe, J., and Wondrack, L. (1996). Glycylcyclines bind to the high-affinity tetracycline ribosomal binding site and evade Tet(M)- and Tet(O)-mediated ribosomal protection. Antimicrob. Agents Chemother. 40, 2226-2228. (Pubitemid 26296281)
8. Blackwood, R.K., Beereboom, J.J., Rennhard, H.H., von Wittenau, M.S., and Stephens, C.R. (1961). 6-methylenetetracyclines.1 I. a new class of tetracycline antibiotics. J. Am. Chem. Soc. 83, 2773-2775.
9. Blanchard, S.C., Gonzalez, R.L., Kim, H.D., Chu, S., and Puglisi, J.D. (2004). tRNA selection and kinetic proofreading in translation. Nat. Struct. Mol. Biol. 11, 1008-1014. (Pubitemid 39315306)
10. Boothe, J.H., Kende, A.S., Fields, T.L., and Wilkinson, R.G. (1959). Total synthesis of tetracyclines. I. (±) -dedimethylamino-12a-deoxy-6- demethylanhydrochlortetracycline. J. Am. Chem. Soc. 81, 1006-1007.
11. Bradford, P.A., and Jones, C.H. (2012). Tetracyclines. In: Antibiotic Discovery and Development, Dougherty, T.J. and Puccim, M.J., eds. (New York: Springer), pp. 147-179.
12. Brodersen, D.E., Clemons, W.M., Carter, A.P., Morgan-Warren, R.J., Wimberly, B.T., and Ramakrishnan, V. (2000). The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103, 1143-1154. (Pubitemid 32037400)
13. Budkevich, T.V., El'skaya, A.V., and Nierhaus, K.H. (2008). Features of 80S mammalian ribosome and its subunits. Nucleic Acids Res. 36, 4736-4744.
14. Burdett, V. (1991). Purification and characterization of Tet(M), a protein that renders ribosomes resistant to tetracycline. J. Biol. Chem. 266, 2872-2877. (Pubitemid 21909148)
15. Burdett, V. (1993). transfer-RNA modification activity is necessary for Tet(M)-mediated tetracycline resistance. J. Bacteriol. 175, 7209-7215. (Pubitemid 23339297)
16. Burdett, V. (1996). Tet(M)-promoted release of tetracycline from ribosomes is GTP dependent. J. Bacteriol. 178, 3246-3251. (Pubitemid 26169368)
17. Caryl, J.A., Cox, G., Trimble, S., and O'Neill, A.J. (2012). "tet(U)" is not a tetracycline resistance determinant. Antimicrob. Agents Chemother. 56, 3378-3379.
18. Chopra, I. and Roberts, M. (2001). Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65, 232-260. (Pubitemid 32538179)
19. Connell, S.R., Trieber, C.A., Stelzl, U., Einfeldt, E., Taylor, D.E., and Nierhaus, K.H. (2002). The tetracycline resistance protein Tet(O) perturbs the conformation of the ribosomal decoding centre. Mol. Microbiol. 45, 1463-1472. (Pubitemid 35231967)
20. Connell, S.R., Tracz, D.M., Nierhaus, K.H., and Taylor, D.E. (2003a). Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrob. Agents Chemother. 47, 3675-3681. (Pubitemid 37484970)
21. Connell, S.R., Trieber, C.A., Dinos, G.P., Einfeldt, E., Taylor, D.E., and Nierhaus, K.H. (2003b). Mechanism of Tet(O)-mediated tetracycline resistance. EMBO J. 22, 945-953. (Pubitemid 36227796)
22. Conover, L.H., Moreland, W.T., English, A.R., Stephens, C.R., and Pilgrim, F.J. (1953). Terramycin. Xi. Tetracycline. J. Am. Chem. Soc. 75, 4622-4623.
23. Dailidiene, D., Bertoli, M.T., Miciuleviciene, J., Mukhopadhyay, A.K., Dailide, G., Pascasio, M.A., Kupcinskas, L., and Berg, D.E. (2002). Emergence of tetracycline resistance in Helicobacter pylori: multiple mutational changes in 16S ribosomal DNA and other genetic loci. Antimicrob. Agents Chemother. 46, 3940-3946. (Pubitemid 35403272)
24. Dantley, K., Dannelly, H., and Burdett, V. (1998). Binding interaction between Tet(M) and the ribosome: requirements for binding. J. Bacteriol. 180, 4089-4092. (Pubitemid 28373510)
25. Dönhöfer, A., Franckenberg, S., Wickles, S., Berninghausen, O., Beckmann, R., and Wilson, D.N. (2012). Structural basis for TetM-mediated tetracycline resistance. Proc. Natl. Acad. Sci. USA 109, 16900-16905.
26. Doyle, D., McDowall, K.J., Butler, M.J., and Hunter, I.S. (1991). Characterization of an oxytetracycline-resistance gene, otrA, of Streptomyces rimosus. Mol. Microbiol. 5, 2923-2933. (Pubitemid 21896025)
27. Draper, M.P., Weir, S., Macone, A., Donatelli, J., Trieber, C.A., Tanaka, S.K., and Levy, S.B. (2013). The mechanism of action of the novel aminomethylcycline antibiotic omadacycline.Antimicrob. Agents Chemother. Sep 16. [Epub ahead of print] doi: 10.1128/AAC.01066-13.
28. Duggar, B.M. (1948). Aureomycin; a product of the continuing search for new antibiotics. Ann. NY Acad. Sci. 51, 177-181.
29. Esberg, B. and Bjork, G.R. (1995). The methylthio group (ms(2)) of N-6-(4-hydroxyisopentenyl)-2-methylthioadenosine (ms(2)io(6) A) present next to the anticodon contributes to the decoding efficiency of the tRNA. J. Bacteriol. 177, 1967-1975.
30. Finlay, A.C., Hobby, G.L., P'an, S.Y., Regna, P.P., Routien, J.B., Seeley, D.B., Shull, G.M., Sobin, B.A., Solomons, I.A., Vinson, J.W., et al. (1950). Terramycin, a new antibiotic. Science 111, 85.
31. Gale, E.F., Cundliffe, E., Reynolds, P.E., Richmond, M.H., and Waring, M.J. (1981). Antibiotic inhibitors of ribosome function. In: The Molecular Basis of Antibiotic Action (Bristol, UK: John Wiley and Sons), pp. 278-379.
32. Gao, Y.G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C., and Ramakrishnan, V. (2009). The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694-699.
33. Geggier, P., Dave, R., Feldman, M.B., Terry, D.S., Altman, R.B., Munro, J.B., and Blanchard, S.C. (2010). Conformational sampling of aminoacyl-tRNA during selection on the bacterial ribosome. J. Mol. Biol. 399, 576-595.
34. Gerrits, M.M., de Zoete, M.R., Arents, N.L., Kuipers, E.J., and Kusters, J.G. (2002). 16S rRNA mutation-mediated tetracycline resistance in Helicobacter pylori. Antimicrob. Agents Chemother. 46, 2996-3000.
35. Gerrits, M.M., Berning, M., Van Vliet, A.H., Kuipers, E.J., and Kusters, J.G. (2003). Effects of 16S rRNA gene mutations on tetracycline resistance in Helicobacter pylori. Antimicrob. Agents Chemother. 47, 2984-2986. (Pubitemid 37040282)
36. Grewal, J., Manavathu, E.K., and Taylor, D.E. (1993). Effect of mutational alteration of Asn-128 in the putative GTP-binding domain of tetracycline resistance determinant Tet(O) from Campylobacter jejuni. Antimicrob. Agents Chemother. 37, 2645-2649. (Pubitemid 23357861)
37. Grossman, T.H., Starosta, A.L., Fyfe, C., O'Brien, W., Rothstein, D.M., Mikolajka, A., Wilson, D.N., and Sutcliffe, J.A. (2012). Targetand resistance-based mechanistic studies with TP-434, a novel fluorocycline antibiotic. Antimicrob. Agents Chemother. 56, 2559-2564.
38. Guay, G.G., Tuckman, M., and Rothstein, D.M. (1994). Mutations in the tetA(B) gene that cause a change in substrate specificity of the tetracycline efflux pump. Antimicrob. Agents Chemother. 38, 857-860. (Pubitemid 24114031)
39. Guillaume, G., Ledent, V., Moens, W., and Collard, J.M. (2004). Phylogeny of efflux-mediated tetracycline resistance genes and related proteins revisited. Microb. Drug Resist. 10, 11-26. (Pubitemid 38529712)
40. Hillen, W. and Berens, C. (1994). Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Annu. Rev. Microbiol. 48, 345-369. (Pubitemid 24334101)
41. Hinrichs, W., Kisker, C., Duvel, M., Muller, A., Tovar, K., Hillen, W., and Saenger, W. (1994). Structure of the Tet repressortetracycline complex and regulation of antibiotic resistance. Science 264, 418-420. (Pubitemid 24178904)
42. Hochstein, F.A., Stephens, C.R., Conover, L.H., Regna, P.P., Pasternack, R., Gordon, P.N., Pilgrim, F.J., Brunings, K.J., and Woodward, R.B. (1953). The structure of terramycin1,2. J. Am. Chem. Soc. 75, 5455-5475.
43. Jenner, L., Starosta, A.L., Terry, D.S., Mikolajka, A., Filonava, L., Yusupov, M., Blanchard, S.C., Wilson, D.N., and Yusupova, G. (2013). Structural basis for potent inhibitory activity of the antibiotic tigecycline during protein synthesis. Proc. Natl. Acad. Sci. USA 110, 3812-3816.
44. Jiang, D., Zhao, Y., Wang, X., Fan, J., Heng, J., Liu, X., Feng, W., Kang, X., Huang, B., Liu, J., et al. (2013). Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A. Proc. Natl. Acad. Sci. USA 110, 14664-14669.
45. 2+ reveals mechanism of antibiotic resistance. J. Mol. Biol. 247, 260-280.
46. Li, W., Atkinson, G.C., Thakor, N.S., Allas, U., Lu, C.C., Chan, K.Y., Tenson, T., Schulten, K., Wilson, K.S., Hauryliuk, V., et al. (2013). Mechanism of tetracycline resistance by ribosomal protection protein Tet(O). Nat. Commun. 4, 1477.
47. Martell, M.J., Jr. and Boothe, J.H. (1967). The 6-deoxytetracyclines. VII. Alkylated aminotetracyclines possessing unique antibacterial activity. J. Med. Chem. 10, 44-46.
48. McCormick, J.R.D., Sjolander, N.O., Hirsch, U., Jensen, E.R., and Doerschuk, A.P. (1957). A new family of antibiotics: the demethyltetracyclines. J. Am. Chem. Soc. 79, 4561-4563.
49. McCormick, J.R.D., Hirsch, U., Sjolander, N.O., and Doerschuk, A.P. (1960). Cosynthesis of tetracyclines by pairs of Streptomyces aureofaciens mutants. J. Am. Chem. Soc. 82, 5006-5007.
50. Mikolajka, A., Liu, H., Chen, Y., Starosta, A.L., Marquez, V., Ivanova, M., Cooperman, B.S., and Wilson, D.N. (2011). Differential effects of thiopeptide and orthosomycin antibiotics on translational GTPases. Chem. Biol. 18, 589-600.
51. Moazed, D. and Noller, H.F. (1987). Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327, 389-394. (Pubitemid 17075811)
52. Moore, I.F., Hughes, D.W., and Wright, G.D. (2005). Tigecycline is modified by the flavin-dependent monooxygenase TetX. Biochemistry 44, 11829-11835. (Pubitemid 41262717)
53. Nelson, M.L. (2001). The chemistry and cellular biology of the tetracyclines. In: Tetracyclines in Biology, Chemistry and Medicine, M.L. Nelson, W. Hillen, and R.A. Greenwald, eds. (Switzerland: Birkhäuser Verlag), pp. 3-63.
54. Nelson, M.L. and Levy, S.B. (2011). The history of the tetracyclines. Ann. N.Y. Acad. Sci. 1241, 17-32.
55. Nelson, M.L., Ismail, M.Y., McIntyre, L., Bhatia, B., Viski, P., Hawkins, P., Rennie, G., Andorsky, D., Messersmith, D., Stapleton, K., et al. (2003). Versatile and facile synthesis of diverse semisynthetic tetracycline derivatives via Pd-catalyzed reactions. J. Org. Chem. 68, 5838-5851. (Pubitemid 36876896)
56. Nonaka, L., Connell, S.R., and Taylor, D.E. (2005). 16S rRNA mutations that confer tetracycline resistance in Helicobacter pylori decrease drug binding in Escherichia coli ribosomes. J. Bacteriol. 187, 3708-3712. (Pubitemid 40705574)
57. Olson, M.W., Ruzin, A., Feyfant, E., Rush, T.S., 3rd, O'Connell, J., and Bradford, P.A. (2006). Functional, biophysical, and structural bases for antibacterial activity of tigecycline. Antimicrob. Agents Chemother. 50, 2156-2166. (Pubitemid 43807538)
58. Orth, P., Schnappinger, D., Sum, P.E., Ellestad, G.A., Hillen, W., Saenger, W., and Hinrichs, W. (1999). Crystal structure of the tet repressor in complex with a novel tetracycline, 9-(N,N-dimethylglycylamido)- 6-demethyl-6-deoxy-tetracycline. J. Mol. Biol. 285, 455-461. (Pubitemid 29041783)
59. Orth, P., Schnappinger, D., Hillen, W., Saenger, W., and Hinrichs, W. (2000). Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat. Struct. Biol. 7, 215-219. (Pubitemid 30140767)
60. Perlman, D., Heuser, L.J., Dutcher, J.D., Barrett, J.M., and Boska, J.A. (1960). Biosynthesis of tetracycline by 5-hydroxy-tetracyclineproducing cultures of Streptomyces rimosus. J. Bacteriol. 80, 419-420.
61. Petersen, P.J., Jacobus, N.V., Weiss, W.J., Sum, P.E., and Testa, R.T. (1999). In vitro and in vivo antibacterial activities of a novel glycylcycline, the 9-t-butylglycylamido derivative of minocycline (GAR-936). Antimicrob. Agents Chemother. 43, 738-744. (Pubitemid 29165733)
62. Piddock, L.J. (2006). Multidrug-resistance efflux pumps-not just for resistance. Nat. Rev. Microbiol. 4, 629-636. (Pubitemid 44317025)
63. Pioletti, M., Schlunzen, F., Harms, J., Zarivach, R., Gluhmann, M., Avila, H., Bashan, A., Bartels, H., Auerbach, T., Jacobi, C., et al. (2001). Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J. 20, 1829-1839. (Pubitemid 32397386)
64. Ridenhour, M.B., Fletcher, H.M., Mortensen, J.E., and Daneo-Moore, L. (1996). A novel tetracycline-resistant determinant, tet(U), is encoded on the plasmid pKq10 in Enterococcus faecium. Plasmid 35, 71-80. (Pubitemid 26117224)
65. Roberts, M.C. (1994). Epidemiology of tetracycline-resistance determinants. Trends Microbiol. 2, 353-357. (Pubitemid 124001345)
66. Roberts, M.C. (1996). Tetracycline resistance determinants: Mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol. Rev. 19, 1-24. (Pubitemid 26356804)
67. Ross, J.I., Eady, E.A., Cove, J.H., and Cunliffe, W.J. (1998). 16S rRNA mutation associated with tetracycline resistance in a Gram-positive bacterium. Antimicrob. Agents Chemother. 42, 1702-1705. (Pubitemid 28311565)
68. Saenger, W., Orth, P., Kisker, C., Hillen, W., and Hinrichs, W. (2000). The tetracycline repressor-a paradigm for a biological switch. Angew Chem. Int. Ed. Engl. 39, 2042-2052.
69. Schmeing, T.M., Voorhees, R.M., Kelley, A.C., Gao, Y.G., Murphy, F.V.T., Weir, J.R., and Ramakrishnan, V. (2009). The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326, 688-694.
70. Söding, J., Biegert, A., and Lupas, A.N. (2005). The Hhpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248. (Pubitemid 44529917)
71. Sohmen, D., Harms, J.M., Schlunzen, F., and Wilson, D.N. (2009a). Enhanced SnapShot: Antibiotic inhibition of protein synthesis II. Cell 139, 212-212.
72. Sohmen, D., Harms, J.M., Schlunzen, F., and Wilson, D.N. (2009b). SnapShot: antibiotic inhibition of protein synthesis I. Cell 138, 1248.
73. Spahn, C.M., Blaha, G., Agrawal, R.K., Penczek, P., Grassucci, R.A., Trieber, C.A., Connell, S.R., Taylor, D.E., Nierhaus, K.H., and Frank, J. (2001). Localization of the ribosomal protection protein Tet(O) on the ribosome and the mechanism of tetracycline resistance. Mol. Cell 7, 1037-1045. (Pubitemid 32525750)
74. Speer, B.S., Bedzyk, L., and Salyers, A.A. (1991). Evidence that a novel tetracycline resistance gene found on two Bacteroides transposons encodes an NADP-requiring oxidoreductase. J. Bacteriol. 173, 176-183.
75. Starosta, A.L., Qin, H., Mikolajka, A., Leung, G.Y., Schwinghammer, K., Nicolaou, K.C., Chen, D.Y., Cooperman, B.S., and Wilson, D.N. (2009). Identification of distinct thiopeptide-antibiotic precursor lead compounds using translation machinery assays. Chem Biol 16, 1087-1096.
76. Stephens, C.R., Conover, L.H., Hochstein, F.A., Regna, P.P., Pilgrim, F.J., Brunings, K.J., and Woodward, R.B. (1952). Terramycin. VIII. Structure of aureomycin and terramycin. J. Am. Chem. Soc. 74, 4976-4977.
77. Stephens, C.R., Conover, L.H., Pasternack, R., Hochstein, F.A., Moreland, W.T., Regna, P.P., Pilgrim, F.J., Brunings, K.J., and Woodward, R.B. (1954). The structure of Aureomycin1. J. Am. Chem. Soc. 76, 3568-3575.
78. Stephens, C.R., Beereboom, J.J., Rennhard, H.H., Gordon, P.N., Murai, K., Blackwood, R.K., and von Wittenau, M.S. (1963). 6-Deoxytetracyclines. IV.1,2 Preparation, C-6 Stereochemistry, and Reactions. J. Am. Chem. Soc. 85, 2643-2652.
79. Sum, P.E., Lee, V.J., Testa, R.T., Hlavka, J.J., Ellestad, G.A., Bloom, J.D., Gluzman, Y., and Tally, F.P. (1994). Glycylcyclines. 1. A new generation of potent antibacterial agents through modification of 9-aminotetracyclines. J. Med. Chem. 37, 184-188. (Pubitemid 24058829)
80. Sun, C., Wang, Q., Brubaker, J.D., Wright, P.M., Lerner, C.D., Noson, K., Charest, M., Siegel, D.R., Wang, Y.M., and Myers, A.G. (2008). A robust platform for the synthesis of new tetracycline antibiotics. J. Am. Chem. Soc. 130, 17913-17927.
81. Sun, C., Hunt, D.K., Clark, R.B., Lofland, D., O'Brien, W.J., Plamondon, L., and Xiao, X.Y. (2010). Synthesis and antibacterial activity of pentacyclines: a novel class of tetracycline analogs. J. Med. Chem. 54, 3704-3731.
82. Tally, F.T., Ellestad, G.A., and Testa, R.T. (1995). Glycylcyclines: a new generation of tetracyclines. J. Antimicrob. Chemother. 35, 449-452.
83. Taylor, D.E., Jerome, L.J., Grewal, J., and Chang, N. (1995). Tet(O), a protein that mediates ribosomal protection to tetracycline, binds, and hydrolyses GTP. Can. J. Microbiol. 41, 965-970.
84. Taylor, D.E., Trieber, C.A., Trescher, G., and Bekkering, M. (1998). Host mutations (miaA and rpsL) reduce tetracycline resistance mediated by Tet(O) and Tet(M). Antimicrob. Agents Chemother. 42, 59-64. (Pubitemid 28053327)
85. Testa, R.T., Petersen, P.J., Jacobus, N.V., Sum, P.E., Lee, V.J., and Tally, F.P. (1993). In vitro and in vivo antibacterial activities of the glycylcyclines, a new class of semisynthetic tetracyclines. Antimicrob. Agents Chemother. 37, 2270-2277. (Pubitemid 23324443)
86. Thaker, M., Spanogiannopoulos, P., and Wright, G.D. (2010). The tetracycline resistome. Cell. Mol. Life Sci. 67, 419-431.
87. Trieber, C.A. and Taylor, D.E. (2002). Mutations in the 16S rRNA genes of Helicobacter pylori mediate resistance to tetracycline. J. Bacteriol. 184, 2131-2140. (Pubitemid 34259662)
88. Trieber, C.A., Burkhardt, N., Nierhaus, K.H., and Taylor, D.E. (1998). Ribosomal protection from tetracycline mediated by Tet(O) interaction with ribosomes is GTP-dependent. Biol. Chem. 379, 847-855
89. Vacher, J., Grosjean, H., Houssier, C., and Buckingham, R.H. (1984). The effect of point mutations affecting Escherichia coli tryptophan tRNA on anticodon-anticodon interactions and on UGA suppression. J. Mol. Biol. 177, 329-342. (Pubitemid 15241999)
90. Volkers, G., Palm, G.J., Weiss, M.S., Wright, G.D., and Hinrichs, W. (2011). Structural basis for a new tetracycline resistance mechanism relying on the TetX monooxygenase. FEBS Lett. 585, 1061-1066.
91. Volkers, G., Damas, J.M., Palm, G.J., Panjikar, S., Soares, C.M., and Hinrichs, W. (2013). Putative dioxygen-binding sites and recognition of tigecycline and minocycline in the tetracyclinedegrading monooxygenase TetX. Acta Crystallogr. D Biol. Crystallogr. 69, 1758-1767.
92. Voorhees, R.M., Weixlbaumer, A., Loakes, D., Kelley, A.C., and Ramakrishnan, V. (2009). Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol. 16, 528-533.
93. White, J.P. and Cantor, C.R. (1971). Role of magnesium in the binding of tetracycline to Escherichia coli ribosomes. J. Mol. Biol. 58, 397-400.
94. Wilson, D.N. (2009). The A-Z of bacterial translation inhibitors. Crit. Rev. Biochem. Mol. Biol. 44, 393-433.
95. Wilson, D.N. (2013). Ribosome-targeting antibiotics and bacterial resistance mechanisms. Nat. Rev. Microbiol., 12, 35-48.
96. Yang, W., Moore, I.F., Koteva, K.P., Bareich, D.C., Hughes, D.W., and Wright, G.D. (2004). TetX is a flavin-dependent monooxygenase conferring resistance to tetracycline antibiotics. J. Biol. Chem. 279, 52346-52352. (Pubitemid 39656610)