Ribosomal protection from tetracycline mediated by Tet(O): Tet(O) interaction with ribosomes is GTP-dependent

Biological Chemistry

Volumn 379, Issue 7, 1998, Pages 847-855

  Trieber, Catharine A ^a   Burkhardt, Nils ^b   Nierhaus, Knud H ^b   Taylor, Diane E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

Ribosomal protection; Tet(O); Tetracycline resistance

Indexed keywords

BACTERIAL PROTEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; RECOMBINANT PROTEIN; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; DRUG BINDING; GEL FILTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RIBOSOME; RNA BINDING;

BACTERIA (MICROORGANISMS);

EID: 0031850047     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/bchm.1998.379.7.847     Document Type: Article

References (46)

1. Ævarsson, A., Brazhnikov, E., Garber, M., Zheltonosova, J., Chirgadze, Y., Al-Karadaghi, S., Svensson, L.A., and Liljas, A. (1994). Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J. 13, 3669-3677.
2. 4+/polyamine system for polyuridine-dependent polyphenylalanine synthesis with near in vivo characteristics. Methods Enzymol. 164, 650-658.
3. Bilgin, N., Claesens, F., Pahverk, H., and Ehrenberg, M. (1992). Kinetic properties of Escherichia coli ribosomes with altered forms of S12. J. Mol. Biol. 224, 1011-1027.
4. Björk, G.R. (1995). Genetic dissection of synthesis and function of modified nucleosides in bacterial transfer RNA. Prog. Nucleic Acid Res. 50, 263-338.
5. Bommer, U., Burkhardt, N., Jünemann, R., Spahn, C.M.T., Triana, F., and Nierhaus, K.H. (1996). Ribosomes and polysomes. In: Subcellular Fractionation. A Practical Approach, J. Graham and D. Rickwoods, eds. (Washington, D.C.: IRL Press). pp. 271-301.
6. Brown, C.M., McCaughan, K.K., and Tate, W.P. (1993). Two regions of the Escherichia coli 16S ribosomal RNA are important for decoding stop signals in polypeptide chain termination. Nucleic Acids Res. 27, 2109-2115.
7. Buck, M.A., and Cooperman, B.S. (1990). Single protein omission reconstitution studies of tetracycline binding to the 30S subunit of Escherichia coli ribosomes. Biochemistry 29, 5374-5379.
8. Burdett, V. (1991). Purification and characterization of Tet(M), a protein that renders ribosomes resistance to tetracycline. J. Biol. Chem. 266, 2872-2877.
9. Burdett, V. (1993). tRNA modification activity is necessary for Tet(M)-mediated tetracycline resistance. J. Bacteriol. 175, 7209-7215.
10. Burdett, V. (1996). Tet(M)-promoted release of tetracycline from ribosomes is GTP dependent. J. Bacteriol. 178, 3246-3251.
11. Burdett, V., Inamine, J., and Rajogapalan, S. (1982). Heterogeneity of tetracycline resistance determinants in Streptococcus. J. Bacteriol. 149, 995-1004.
12. Chopra, I. (1985). Mode of action of the tetracyclines and the nature of bacterial resistance to them. In: The Tetracyclines, Vol. 78, J.J. Hlavka and J.H. Boothe, ed., (Berlin, Germany: Springer-Verlag), pp. 317-392.
13. Chopra, I. (1994). Tetracycline analogs whose primary target is not the bacterial ribosome. Antimicrob. Agents Chemother. 38, 637-640.
14. Chopra, I., Hawkey, P.M., and Hinton, M. (1992). Tetracyclines, molecular and clinical aspects. J. Antimicrob. Chemother. 29, 245-277.
15. Clermont, D., Chesneau, O., De Cespedes, G., and Horaud, T. (1997). New tetracycline-resistance determinants coding for ribosomal protection in Streptococci and nucleotide sequence of tet(T) isolated from Streptococcus pyogenes A498. Antimicrob. Agents and Chemother, 41, 112-116.
16. Czworkowski, J., and Moore, P.B. (1996). The elongation phase of protein synthesis. Prog. Nucleic Acid Res. 54, 293-332.
17. Czworkowski, J.J.W, Steitz, T.A., and Moore, P.B. (1994). The crystal structure of elongation factor G complexed with GDP, at 2.7 Å resolution. EMBO J. 13, 3661-3668.
18. Doyle, K., McDowell, 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.
19. Epe, B., Woolley, P., and Hornig, H. (1987). Competition between tetracycline and the tRNA at both P and A sites of the ribosome of Escherichia coli. FEBS Lett. 213, 443-447.
20. Geigenmüller, U., and Nierhaus, K.H. (1986). Tetracycline can inhibit tRNA binding to the ribosomal P site as well as to the A site. Eur. J. Biochem. 161, 723-726.
21. Goldman, R.A., Hasan, T., Hall, C.C., Strycharz, W.A., and Cooperman, B.S. (1983). Photoincorporation of tetracycline binding into Escherichia coli ribosomes. Identification of the major proteins photolabeled by native tetracycline and tetracycline photoproducts and implications for the inhibitory action of tetracycline on protein synthesis. Biochemistry 22, 359-368.
22. 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 and Chemother. 37, 2645-2649.
23. Hausner, T.P., Geigenmüller, U., and Nierhaus, K.H. (1988). The allosteric three-site model for the ribosomal elongation cycle. J. Biol. Chem. 263, 13103-13111.
24. Kaji, A., and Ryoji, M. (1979). Tetracycline. In: Antibiotics, Vol. 5, F.E. Hahn, ed. (Berlin, Germany: Springer-Verlag), pp. 304-328.
25. Karimi, R., and Ehrenberg, M. (1994). Dissociation rate of cognate peptidyl-tRNA from the A-site of hyper-accurate and error-prone ribosomes. Eur. J. Biochem. 226, 355-360.
26. Levy, S.B. (1992). Active efflux mechanisms for antimicrobial resistance. Antimicrob. Agents Chemother. 36, 695-703.
27. Manavathu, E.K., Hiratsuka, K., and Taylor, D.E. (1988). Nucleotide sequence analysis and expression of a tetracycline-resistance gene from Campylobacterjejuni. Gene 62, 17-26.
28. Manavathu, E.K., Fernandez, C.L., Cooperman, B.S., and Taylor, D.E. (1990). Molecular studies on the mechanism of tetracycline resistance mediated by Tet(O). Antimicrob. Agents Chemother. 34, 71-77.
29. Moazed, D., and Noller, H.F. (1987). Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature, 327, 389-394.
30. Nierhaus, K.H. (1966). The tricks of ribosomal elongation factors. Angew. Chem. Int. Ed. Engl. 35, 2198-2201.
31. Nierhaus, K.H., Beyer, D., Dabrowshi, M., Schäfer, M., Spahn, C.M.T., Wadzack, J., Bittner, J.U., Burkhardt, N., Diedrich, G., Jünemann, R., Kamp, D., Voss, H., and Stuhrmann, H.B. (1955). The elongation ribosome: structural and function aspects. Biochem. Cell Biol. 73, 1011-1021.
32. Oliva, B., Gordon, G., McNicholas, P., Ellestad, G., and Chopra, I. (1992). Evidence that tetracycline analogs whose primary target is not the bacterial ribosome cause lysis of Escherichia coli. Antimicrob. Agents Chemother. 36, 913-919.
33. Rheinberger, H.J., Geigenmüller, U., Wedde, M., and Nierhaus, K.H. (1988). Parameters for the preparation of Escherichia coli ribosomes and ribosomal subunits active in tRNA binding. Methods Enzymol. 164, 658-670.
34. Roberts, M.C. (1994). Epidemiology of tetracycline-resistance determinants. Trends Microbiol. 2, 353-357.
35. Roberts, M.C. (1996). Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol. Lett. 19, 1-24.
36. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory).
37. Schnappinger, D., and Hillen, W. (1996).Tetracyclines: antibiotic action, uptake, and resistance mechanisms. Arch. Microbiol. 165, 350-369.
38. Spahn, C.M.T., Remme, J., Schäfer, M.A., and Nierhaus, K.H. (1996). Mutational analysis of two highly conserved UGG sequences of 23S rRNA from Escherichia coli. J. Biol. Chem. 271, 32849-32856.
39. 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.
40. Strack, B., Lessl, M., Calendar, R., and Lanka, E. (1992). Sequence motif, -E-G-Y-A-T-A-, identified within the primase domains of plasmid-encoded I-and P-type DNA primases and the α protein of the Escherichia coli satellite phage P4. J. Biol. Chem. 267, 13062-13072.
41. Taylor, D.E. (1986). Plasmid-mediated tetracycline resistance in Campylobacterjejuni: expression in Escherichia coli and identification of homology with streptococcal class M determinant. J. Bacteriol. 165, 1037-1039.
42. Taylor, D.E., and Chau, A. (1996). Tetracycline resistance mediated by ribosomal protection. Antimicrob. Agents Chemother. 40, 1-5.
43. 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, 965-979.
44. 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 and Chemother. 42, 59-64.
45. Tritton, T.R. (1977). Ribosome-tetracycline interactions. Biochemistry 16, 4133-4138.
46. Wang, Y., and Taylor, D.E. (1991). A DNA sequence upstream of the tet(O) gene is required for full expression of tetracycline resistance. Antimicrob. Agents Chemother. 35, 2020-2025.