Chapter 2 : Tetracycline Resistance Due to Ribosomal Protection Proteins

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There have been 11 ribosomal protection genes identified which code for cytoplasmic proteins that protect the ribosomes from the action of tetracycline in vitro and in vivo and confer resistance to tetracycline, doxycycline, and minocycline to the host. The ribosomal protection proteins are thought to interact with the base of h34 protein, within the ribosome, causing an allosteric disruption of the primary tetracycline binding site(s). This releases the tetracycline molecules from the ribosome and allows the ribosome to return to its normal posttranslocational conformational state, which was altered by the binding of tetracycline. Glycylcyclines compete with tetracycline for ribosomal binding sites because they have either identical or overlapping sites on the ribosome and have the same mode of action as tetracycline. The differences in host range may be partially due to the type of element that each gene is associated with. This may be relevant because conjugative transposons, in general, have less host specificity than do plasmids and are able to be transferred to unrelated species and genera. The ribosomal protection genes are associated with plasmids, transposons, and conjugative transposons. Conjugative transfer appears to be influenced by the flanking sequences which correlate with the location of the Tn-Tn family inserted into the chromosome.

Citation: Roberts M. 2005. Tetracycline Resistance Due to Ribosomal Protection Proteins, p 19-28. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch2
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1. Agerso, Y.,, L. B. Jensen,, M. Givskov,, and M. C. Roberts. 2002. The identification of a tetracycline resistance gene tet(M), on a Tn 916-like transposon, in the Bacillus cereus group. FEMS Micobiol. Lett. 214: 251 256.
2. Aminov, R. I.,, N. Garrigues-Jeanjean,, and R. I. Mackie. 2001. Molecular ecology of tetracycline resistance: development and validation of primers of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl. Environ. Microbiol. 67: 22 32.
3. Andres, M. T.,, W. O. Chung,, M. C. Roberts,, and J. F. Fierro. 1998. Antimicrobial susceptibilities of Porphyromonas gingivalis, Prevotella intermedia and Prevotella nigrescens isolated in Spain. Antimicrob. Agents Chemother. 42: 3022 3023.
4. Atkinson, B. A.,, A. Abu-Al-Jaibat,, and D. J. LeBlanc. 1997. Antibiotic resistance among enterococci isolated from clinical specimens between 1953 and 1954. Antimicrob. Agents Chemother. 41: 1598 1600.
5. Barbosa, T. M.,, K. P. Scott,, and H. J. Flint. 1999. Evidence for recent intergeneric transfer of a new tetracycline resistance gene, tet(W), isolated from Butyrivibrio fibrisolens, and the occurrence of tet(O) in ruminal bacteria. Environ. Microbiol. 1: 53 64.
6. Bauer, G.,, C. Berens,, S. J. Projan,, and W. Hillen. 2004. Comparison of tetracycline and tigecycline binding to ribosomes mapped by dimethylsulphate and drug-directed Fe 2+ cleavage of 16S rRNA. J. Antimicrob. Chemother. 53: 592 599.
7. Bertram, J.,, M. Stratz,, and P. Durre. 1991. Natural transfer of conjugative transposon Tn 916 between Gram-positive and Gram-negative bacteria. J. Bacteriol. 173: 443 448.
8. Billington, S. J.,, J. G. Songer,, and B. H. Jost. 2002. Widespread distribution of a Tet W determinant among tetracycline-resitant isolates of the animal pathogen Arcanobacterium pyogenes. Antimicrob. Agents Chemother. 46: 1281 1287.
8a.. Brenciani, A.,, K. K. Ojo,, A. Monachetti,, S. Menzo,, M. C. Roberts,, P. E. Varaldo,, and E. Giovanetti. 2004. Distribution and molecular analysis of mef(A)-containing elements in tetracycline- susceptible and -resistant Streptococcus pyogenes clinical isolates with efflux-mediated erythromycin resistance. J. Antimicrob. Chemother. 54: 991 998.
9. Brodersen, D. E.,, W. M. Clemons,, A. P. Carter,, R. J. Morgan- Warren,, B. T. Wimberly,, and V. T. Ramakrishnan. 2000. The structural basis for the action of the antibiotic tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103: 1143 1154.
10. Brown, B. A.,, R. J. Wallace,, and G. Onyi. 1996. Activities of the glycylcyclines N, N-dimethylglycylamido-minocycline and N, N-dimethylglycylamido-6-demethyl-6-deoxytetracycline against Nocardia spp. and tetracycline-resistant isolates of rapidly growing mycobacteria. Antimicrob. Agents Chemother. 40: 874 878.
11. Brown, J. T.,, and M. C. Roberts. 1987. Cloning and characterization of tetM from a Ureaplasma urealyticum strain. Antimicrob. Agents Chemother. 31: 1852 1854.
12. Burdett, V. 1991. Purification and characterization of Tet(M), a protein that renders ribosomes resistant to tetracycline. J. Biol. Chem. 266: 2872 2877.
13. Burdett, V. 1993. tRNA modification activity is necessary for Tet(M)-mediated tetracycline resistance. J. Bacteriol. 175: 7209 7215.
14. Burdett, V. 1996. Tet(M)-promoted release of tetracycline from ribosomes is GTP dependent. J. Bacteriol. 178: 3246 3251.
15. Charpentier, E.,, G. Gerbaud,, and P. Courvalin. 1994. Presence of the Listeria tetracycline resistance gene tet(S) in Enterococcus faecalis. Antimicrob. Agents Chemother. 38: 2330 2335.
16. Charpentier, E.,, and P. Courvalin. 1994. Presence of the Listeria tetracycline resistance gene tet(S) in Enterococcus faecalis. Antimicrob. Agents Chemother. 38: 2330 2335.
17. Charpentier, E.,, and P. Courvalin. 1999. Antibiotic resistance in Listeria spp. Antimicrob. Agents Chemother. 43: 2103 2108.
18. Chaslus-Dancla, E.,, M.-C. Lesage-Descauses,, S. Leroy-Setrin,, J.-L. Marel,, and J.-P. Lafont. 1995. Tetracycline resistance determinants, Tet B and Tet M detected in Pasteurella haemolytica and Pasteurella multocida from bovine herds. J. Antimicrob. Chemother. 36: 815 819.
19. Chopra, I.,, and M. C. Roberts. 2001. Tetracycline antibiotics: Mode of action, applications, molecular biology and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65: 232 260.
20. Chung, W. O.,, K. Young,, Z. Leng,, and M. C. Roberts. 1999. Mobile elements carrying ermF and tetQ genes in Gram-positive and Gram-negative bacteria. J. Antimicrob. Chemother. 44: 329 335.
21. Chung, W. O.,, J. Gabany,, G. R. Persson,, and M. C. Roberts. 2002. Distribution of erm(F) and tet(Q) genes in four oral bacterial species and genotypic variation between resistant and susceptible isolates. J. Clin. Periodontol. 29: 152 158.
22. Clermont, D.,, O. Chesneau,, G. De Cespedes,, and T. Horaud. 1997. New tetracycline resistance determinants coding for ribosomal protection in streptococci and nucleotide sequence of tet(T) isolated from Streptococcus pyogens A498. Antimicrob. Agents Chemother. 41: 112 116.
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24. Connell, S. R.,, D. M. Tracz,, K. H. Nierhaus,, and D. E. Taylor. 2003. Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrob. Agents Chemother. 47: 3675 3681.
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27. DePaola, A.,, and M. C. Roberts. 1995. Class D and E tetracycline resistance determinants in gram-negative catfish pond bacteria. Mol. Cell. Probes 9: 311 313.
28. Dittrich, W.,, and H. Schrempf. 1992. The unstable tetracycline resistance gene of Streptomyces lividans 1326 encodes a putative protein with similarities to translational elongation factors and Tet (M) and Tet (O) proteins. Antimicrob. Agents Chemother. 36: 1119 1124.
29. Facinelli, B.,, M. C. Roberts,, E. Giovanetti,, C. Casolari,, U. Fabio,, and P. E. Varaldo. 1993. Genetic basis of tetracycline resistance in food borne isolates of Listeria innocua. Appl. Environ. Microbiol. 59: 614 616.
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33. Francois, B.,, M. Charles,, and P. Courvalin. 1997. Conjugative transfer of tet(S) between strains of Enterococcus faecalis is associated with the exchange of large fragments of chromosomal DNA. Microbiology 143: 2145 2154.
34. Giovanetti, E.,, A. Brenciani,, R. Lupidi,, M. C. Roberts,, and P. E. Varaldo. 2003. The presence of the tet(O) gene in erythromycin and tetracycline-resistant strains of Streptococcus pyogenes. Antimicrob. Agents Chemother. 47: 2844 2849.
35. Hartley, D. L.,, K. R. Hones,, J. A. Tobian,, D. J. LeBlanc,, and F. L. Macrina. 1984. Disseminated tetracycline resistance in oral streptococci: Implication of a conjugative transposon. Infect. Immun. 45: 13 17.
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40. Knapp, J. S.,, S. R. Johnson,, J. M. Zenilman,, M. C. Roberts,, and S. A. Morse. 1988. High-level tetracycline resistance resulting from TetM in strains of Neisseria species, Kingella denitrificans, and Eikenella corrodens. Antimicrob. Agents Chemother. 32: 765 767.
41. Lacroix, J.-M.,, and C. B. Walker. 1993. Detection and incidence of the tetracycline resistance determinant tet(M) in the microflora associated with adult periodontitis. J. Periodontol. 66: 102 108.
41a.. Lancaster, H.,, A. P. Roberts,, R. Bedi,, M. Wilson,, and P. Mullany. 2004. Characterization of Tn 916S, a Tn 916-like element containing the tetracycline resistance determinant tet(S). J. Bacteriol. 186: 4395 4398.
42. Leipe, D.,, Y. I. Wolf,, E. V. Koonin,, and L. Aravind. 2002. Classification of and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317: 41 72.
43. Leng, Z.,, D. E. Riley,, R. E. Berger,, J. N. Krieger,, and M. C. Roberts. 1997. Distribution and mobility of the tetracycline resistant determinant Tet Q. J. Antimicrob. Chemother. 40: 551 559.
44. Levy, S. B.,, L. M. McMurry,, T. M. Barbosa,, V. Burdett,, P. Courvalin,, W. Hillen,, M. C. Roberts,, J. I. Rood,, and D. E. Taylor. 1999. Nomenclature for new tetracycline resistance determinants. Antimicrob. Agents Chemother. 43: 1523 1524.
45. Li, L.-Y.,, N. B. Shoemaker,, and A. A. Salyers. 1995. Location and characteristics of the transfer region of Bacteriodes conjugative transposon and regulation of transfer genes. J. Bacteriol. 177: 4992 4999.
46. Luna, V. A.,, and M. C. Roberts. 1998. The presence of the tetO gene in a variety of tetracycline resistant Streptococcus pneumoniae serotypes from Washington State. J. Antimicrob. Chemother. 42: 613 619.
47. Luna, V. A.,, P. Coates,, E. A. Eady,, J. Cove,, T. T. H. Nguyen,, and M. C. Roberts. 1999. A variety of Gram-positive bacteria carry mobile mef genes. J. Antimicrob. Chemother. 44: 19 25.
48. Lyras, D.,, and J. I. Rood. 1996. Genetic organization and distribution of tetracycline resistance determinants in Clostridium perfringes. Antimicrob. Agents Chemother. 40: 2500 2504.
49. Lyras, D.,, and J. I. Rood. 2000. Transposition of Tn 4451 and Tn 4453 involves a circular intermediate that forms a promoter for the large resolvase, TnpX. Mol. Microbiol. 38: 588 601.
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53. Morse, S. A.,, S. J. Johnson,, J. W. Biddle,, and M. C. Roberts. 1986. High-level tetracycline resistance in Neisseria gonorrhoeae due to the acquisition of the tetM determinant. Antimicrob. Agents Chemother. 30: 664 670.
54. Naglich, J. G.,, and R. E. Andrews, Jr. 1988. Tn 916-dependent conjugal transfer of pC194 and pUB110 from Bacillus subtillis into Bacillus thuringiensis subsp. israelensis. Plasmid 20: 113 126.
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58. Pioletti, M.,, F. Schlunzen,, J. Harms,, R. Zarivach,, M. Gluhmann,, H. Avila,, A. Bashan,, H. Bartels,, T. Auerbach,, C. Jacobi,, T. Hartsch,, A. Yonath,, and F. Franceschi. 2001. Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J. 20: 1829 1839.
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62. Riley, D. E.,, M. C. Roberts,, T. Takayama,, and J. N. Krieger. 1992. Development of polymerase chain reaction-based (PCR) diagnosis of Trichomonas vaginalis using cloned, genomic sequences. J. Clin. Microbiol. 30: 465 472.
63. Roberts, M. C., 1989. Gene transfer in the urogenital and respiratory tract, p. 347 375. In S. B. Levy, and R. V. Miller (ed.), Gene Transfer in the Environment. McGraw-Hill Publishing Co., New York, N.Y.
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66. Roberts, M. C. 1989. Plasmid-mediated Tet M in Haemophilus ducreyi. Antimicrob. Agents Chemother. 33: 1611 1613.
67. Roberts, M. C. 1991. Tetracycline resistance in Peptostreptococcus species. Antimicrob. Agents Chemother. 35: 1682 1684.
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68. Roberts, M. C.,, and J. S. Knapp. 1988. Host range of the conjugative 25.2 Mdal tetracycline resistance plasmid from Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 32: 488 491.
69. Roberts, M. C.,, and J. S. Knapp. 1988. Transfer of β-lactamase plasmids from Neisseria gonorrhoeae to Neisseria meningitidis and commensal Neisseria species by the 25.2-megadalton conjugative plasmid. Antimicrob. Agents Chemother. 32: 1430 1432.
70. Roberts, M. C.,, and J. S. Knapp. 1989. Transfer frequency of various 25.2 Mdal TetM-containing plasmids in Neisseria gonorrhoeae. Sex. Trans. Dis. 16: 91 94.
71. Roberts, M. C.,, and J. Lansciardi. 1990. Transferable Tet M in Fusobacterium nucleatum. Antimicrob. Agents Chemother. 34: 1836 1838.
72. Roberts, M. C.,, and B. J. Moncla. 1988. Tetracycline resistance and TetM in oral anaerobic bacteria and Neisseria perflava- N. sicca. Antimicrob. Agents Chemother. 32: 1271 1273.
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79. Schwarz, S.,, M. C. Roberts,, C. Werckenthin,, Y. Pang,, and C. Lange. 1998. Tetracycline resistance in Staphylococcus spp. from domestic and pet animals. Vet. Microbiol. 63: 217 228.
80. Scott, K. P.,, T. M. Barbosa,, K. J. Forbes,, and H. J. Flint. 1997. High-frequency transfer of a naturally occurring chromosomal tetracycline resistance element in the ruminal anaerobe Butyrivibrio fibrisolvens. Appl. Environ. Microbiol. 63: 3405 3411.
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87. Su, Y. A.,, P. He,, and D. B. Clewell. 1992. Characterization of the tet( M) determinant of Tn 916: evidence for regulation by transcription attenuation. Antimicrob. Agents Chemother. 36: 769 778.
88. Taylor, D. E. 1986. Plasmid-mediated tetracycline resistance in Campylobacter jejuni: Expression in Escherichia coli and identification of homology with streptococcal class M determinant. J. Bacteriol. 165: 1037 1039.
89. Taylor, D. E.,, and A. Chau. 1996. Tetracycline resistance mediated by ribosomal protection. Antimicrob. Agents Chemother. 40: 1 5.
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91. Villedieu, A.,, M. L. Diaz-Torres,, N. Hunt,, R. McNab,, D. A. Spratt,, M. Wilson,, and P. Mullany. 2003. Prevalence of tetracycline resistance genes in oral bacteria. Antimicrob. Agents Chemother. 47: 878 882.
92. Wang, Y.,, and D. E. Taylor. 1991. A DNA sequence upstream of the tet(O) gene is required for full expression of tetracycline resistance. Antimicrob. Agents Chemother. 35: 2020 2025.
93. Weaver, K. E.,, L. B. Rice,, and G. Churchward,. 2002. Plasmids and transposons, p. 219 263. In M. S. Gilmore (ed.), The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance. ASM Press, Washington, D.C.
94. Whittle, G.,, T. R. Whitehead,, N. Hamburger,, N. B. Shoemaker,, M. A. Cotta,, and A. A. Salyers. 2003. Identification of a new ribosomal protection type of tetracycline resistance gene, tet(36), from swine manure pits. Appl. Environ. Microbiol. 69: 4151 4158.
95. Widdowson, C. A.,, K. P. Klugman,, and D. Hanslo. 1996. Identification of the tetracycline resitance gene, tetO, in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 40: 2891 2893.


Generic image for table
Table 1

G+C content of ribosomal protection genes

Percentages are rounded off to the next whole number.

Citation: Roberts M. 2005. Tetracycline Resistance Due to Ribosomal Protection Proteins, p 19-28. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch2
Generic image for table
Table 2

Distribution of ribosomal protection genes

Data from references .

Citation: Roberts M. 2005. Tetracycline Resistance Due to Ribosomal Protection Proteins, p 19-28. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch2

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