ABC-F proteins mediate antibiotic resistance through ribosomal protection

mBio

Volumn 7, Issue 2, 2016, Pages

  Sharkey, Liam K R ^a   Edwards, Thomas A ^a   O’Neill, Alex J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN ABC F; PROTEIN LSA(A); PROTEIN MSR(A); PROTEIN OPTR(A); PROTEIN VGA(A); UNCLASSIFIED DRUG; ABC TRANSPORTER; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BIOCHEMICAL COMPOSITION; CELL PROTECTION; CONTROLLED STUDY; IN VITRO STUDY; INHIBITION KINETICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PURIFICATION; RIBOSOME; STAPHYLOCOCCUS AUREUS; DRUG EFFECTS; GRAM POSITIVE BACTERIUM; METABOLISM; MICROBIAL SENSITIVITY TEST; PROTEIN SYNTHESIS;

ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, BACTERIAL; GRAM-POSITIVE BACTERIA; MICROBIAL SENSITIVITY TESTS; PROTEIN BIOSYNTHESIS; RIBOSOMES;

EID: 84965173406     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01975-15     Document Type: Article

References (50)

1. WHO. 2014. Antimicrobial resistance: global report on surveillance 2014. World Health Organization, Geneva, Switzerland.
2. Review on Antimicrobial Resistance. 2014. Antimicrobial resistance: tackling a crisis for the future health and wealth of nations. Review on Antimicrobial Resistance, London, United Kingdom. http://amrreview.org/Publications.
3. Blair JM, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJ. 2015. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 13: 42–51. http://dx.doi.org/10.1038/nrmicro3380.
4. Kerr ID. 2004. Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem Biophys Res Commun 315:166–173. http://dx.doi.org/10.1016/j.bbrc.2004.01.044.
5. Davidson AL, Dassa E, Orelle C, Chen J. 2008. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364. http://dx.doi.org/10.1128/MMBR.00031-07.
6. Dorrian JM, Kerr ID. 2009. Can ABC proteins confer drug resistance in microorganisms without being export pumps? p 63–77. In Ponte-Sucre A (ed), ABC transporters in microorganisms: research, innovation and value as targets against drug resistance. Caister Academic Press, Norfolk, United Kingdom.
7. Reynolds ED, Cove JH. 2005. Resistance to telithromycin is conferred by msr(A), msrC and msr(D) in Staphylococcus aureus. J Antimicrob Chemother 56:1179–1180. http://dx.doi.org/10.1093/jac/dki378.
8. Novotna G, Janata J. 2006. A new evolutionary variant of the streptogramin A resistance protein, Vga(A)(LC), from Staphylococcus haemolyticus with shifted substrate specificity towards lincosamides. Antimicrob Agents Chemother 50:4070–4076. http://dx.doi.org/10.1128/AAC.00799-06.
9. Singh KV, Weinstock GM, Murray BE. 2002. An Enterococcus faecalis ABC homologue (Lsa) is required for the resistance of this species to clindamycin and quinupristin-dalfopristin. Antimicrob Agents Chemother 46:1845–1850. http://dx.doi.org/10.1128/AAC.46.6.1845-1850.2002.
10. Ross JI, Eady EA, Cove JH, Cunliffe WJ, Baumberg S, Wootton JC. 1990. Inducible erythromycin resistance in staphylococci is encoded by a member of the ATP-binding transport super-gene family. Mol Microbiol 4:1207–1214. http://dx.doi.org/10.1111/j.1365-2958.1990.tb00696.x.
11. Wang Y, Lv Y, Cai J, Schwarz S, Cui L, Hu Z, Zhang R, Li J, Zhao Q, He T, Wang D, Wang Z, Shen Y, Li Y, Feßler AT, Wu C, Yu H, Deng X, Xia X, Shen J. 2015. A novel gene, optrA, that confers transferable resistance to oxazolidinones and phenicols and its presence in Enterococcus faecalis and Enterococcus faecium of human and animal origin. J Antimicrob Chemother 70:2182–2190. http://dx.doi.org/10.1093/jac/dkv116.
12. Gentry DR, McCloskey L, Gwynn MN, Rittenhouse SF, Scangarella N, Shawar R, Holmes DJ. 2008. Genetic characterization of Vga ABC proteins conferring reduced susceptibility to pleuromutilins in Staphylococcus aureus. Antimicrob Agents Chemother 52:4507–4509. http://dx.doi.org/10.1128/AAC.00915-08.
13. Allignet J, Loncle V, el Sohl N. 1992. Sequence of a staphylococcal plasmid gene, vga, encoding a putative ATP-binding protein involved in resistance to virginiamycin A-like antibiotics. Gene 117:45–51. http://dx.doi.org/10.1016/0378-1119(92)90488-B.
14. Tesse S, Trueba F, Berthet N, Hot C, Chesneau O. 2013. Resistance genes underlying the LSA phenotype of French staphylococcal isolates. Antimicrob Agents Chemother 57:4543-4546. http://dx.doi.org/10.1128/AAC.00259-13.
15. Hot C, Berthet N, Chesneau O. 2014. Characterization of sal(A), a novel gene responsible for lincosamide and streptogramin A resistance in Staphylococcus sciuri. Antimicrob Agents Chemother 58:3335–3341. http://dx.doi.org/10.1128/AAC.02797-13.
16. Reynolds E, Ross JI, Cove JH. 2003. Msr(A) and related macrolide/streptogramin resistance determinants: incomplete transporters? Int J Antimicrob Agents 22:228–236. http://dx.doi.org/10.1016/S0924-8579(03)00218-8.
17. Kerr ID, Reynolds ED, Cove JH. 2005. ABC proteins and antibiotic drug resistance: is it all about transport? Biochem Soc Trans 33:1000–1002. http://dx.doi.org/10.1042/BST20051000.
18. Chesneau O, Ligeret H, Hosan-Aghaie N, Morvan A, Dassa E. 2005. Molecular analysis of resistance to streptogramin A compounds conferred by the Vga proteins of staphylococci. Antimicrob Agents Chemother 49: 973–980. http://dx.doi.org/10.1128/AAC.49.3.973-980.2005.
19. Nunez-Samudio V, Chesneau O. 2013. Functional interplay between the ATP binding cassette Msr(D) protein and the membrane facilitator superfamily Mef(E) transporter for macrolide resistance in Escherichia coli. Res Microbiol 164:226–235. http://dx.doi.org/10.1016/j.resmic.2012.12.003.
20. Lenart J, Vimberg V, Vesela L, Janata J, Balikova Novotna G. 2015. Detailed mutational analysis of Vga(A) interdomain linker: implication for antibiotic resistance specificity and mechanism. Antimicrob Agents Chemother 59:1360–1364. http://dx.doi.org/10.1128/AAC.04468-14.
21. Jacquet E, Girard J-M, Ramaen O, Pamlard O, Lévaique H, Betton J-M, Dassa E, Chesneau O. 2008. ATP hydrolysis and pristinamycin IIA inhibition of the Staphylococcus aureus Vga(A), a dual ABC protein involved in streptogramin A resistance. J Biol Chem 283:25332–25339. http://dx.doi.org/10.1074/jbc.M800418200.
22. Matsuoka M, Jánosi L, Endou K, Nakajima Y. 1999. Cloning and sequences of inducible and constitutive macrolide resistance genes in Staphylococcus aureus that correspond to an ABC transporter. FEMS Microbiol Lett 181:91–100. http://dx.doi.org/10.1111/j.1574-6968.1999.tb08830.x.
23. Olano C, Rodríguez AM, Méndez C, Salas JA. 1995. A second ABC transporter is involved in oleandomycin resistance and its secretion by Streptomyces antibioticus. Mol Microbiol 16:333–343. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02305.x.
24. Barre J, Fournet MP, Zini R, Deforges L, Duval J, Tillement JP. 1986. In vitro [3H]-erythromycin binding to Staphylococcus aureus. Biochem Pharmacol 35:1001–1004. http://dx.doi.org/10.1016/0006-2952(86)90090-0.
25. Fredrick K, Ibba M. 2014. The ABCs of the ribosome. Nat Struct Mol Biol 21:115–116. http://dx.doi.org/10.1038/nsmb.2765.
26. Di Giambattista M, Engelborghs Y, Nyssen E, Cocito C. 1987. Kinetics of binding of macrolides, lincosamides, and synergimycins to ribosomes. J Biol Chem 262:8591–8597.
27. Trzcinski K, Cooper BS, Hryniewicz W, Dowson CG. 2000. Expression of resistance to tetracyclines in strains of methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 45:763–770. http://dx.doi.org/10.1093/jac/45.6.763.
28. O’Neill AJ, Chopra I. 2006. Molecular basis of fusB-mediated resistance to fusidic acid in Staphylococcus aureus. Mol Microbiol 59:664-676. http://dx.doi.org/10.1111/j.1365-2958.2005.04971.x.
29. Long KS, Poehlsgaard J, Kehrenberg C, Schwarz S, Vester B. 2006. The Cfr rRNA methyltransferase confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics. Antimicrob Agents Chemother 50:2500–2505. http://dx.doi.org/10.1128/AAC.00131-06.
30. Arenz S, Nguyen F, Beckmann R, Wilson DN. 2015. Cryo-EM structure of the tetracycline resistance protein TetM in complex with a translating ribosome at 3.9-A resolution. Proc Natl Acad Sci U S A 112:5401–5406. http://dx.doi.org/10.1073/pnas.1501775112.
31. Li W, Atkinson GC, Thakor NS, Allas U, Lu CC, Chan KY, Tenson T, Schulten K, Wilson KS, Hauryliuk V, Frank J. 2013. Mechanism of tetracycline resistance by ribosomal protection protein Tet(O). Nat Commun 4:1477. http://dx.doi.org/10.1038/ncomms2470.
32. Boël G, Smith PC, Ning W, Englander MT, Chen B, Hashem Y, Testa AJ, Fischer JJ, Wieden HJ, Frank J, Gonzalez RL, Jr, Hunt JF. 2014. The ABC-F protein EttA gates ribosome entry into the translation elongation cycle. Nat Struct Mol Biol 21:143–151. http://dx.doi.org/10.1038/nsmb.2740.
33. Chen B, Boël G, Hashem Y, Ning W, Fei J, Wang C, Gonzalez RL, Jr, Hunt JF, Frank J. 2014. EttA regulates translation by binding the ribosomal E site and restricting ribosome-tRNA dynamics. Nat Struct Mol Biol 21:152–159. http://dx.doi.org/10.1038/nsmb.2741.
34. Dassa E, Bouige P. 2001. The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms. Res Microbiol 152: 211–229. http://dx.doi.org/10.1016/S0923-2508(01)01194-9.
35. Dassa E. 2011. Natural history of ABC systems: not only transporters. Essays Biochem 50:19–42. http://dx.doi.org/10.1042/bse0500019.
36. CLSI. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard M07-A9, 9th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
37. Forsyth RA, Haselbeck RJ, Ohlsen KL, Yamamoto RT, Xu H, Trawick JD, Wall D, Wang L, Brown-Driver V, Froelich JM, Kedar GC, King P, McCarthy M, Malone C, Misiner B, Robbins D, Tan Z, Zhu Zy ZY, Carr G, Mosca DA. 2002. A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Mol Microbiol 43:1387–1400. http://dx.doi.org/10.1046/j.1365-2958.2002.02832.x.
38. Monk IR, Shah IM, Xu M, Tan MW, Foster TJ. 2012. Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. mBio 3:e00277-11. http://dx.doi.org/10.1128/mBio.00277-11.
39. Ouyang S, Lee CY. 1997. Transcriptional analysis of type 1 capsule genes in Staphylococcus aureus. Mol Microbiol 23:473–482. http://dx.doi.org/10.1046/j.1365-2958.1997.d01-1865.x.
40. Luong TT, Lee CY. 2007. Improved single-copy integration vectors for Staphylococcus aureus. J Microbiol Methods 70:186–190. http://dx.doi.org/10.1016/j.mimet.2007.04.007.
41. Ariza A, Tanner SJ, Walter CT, Dent KC, Shepherd DA, Wu W, Matthews SV, Hiscox JA, Green TJ, Luo M, Elliott RM, Fooks AR, Ashcroft AE, Stonehouse NJ, Ranson NA, Barr JN, Edwards TA. 2013. Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization. Nucleic Acids Res 41:5912–5926. http://dx.doi.org/10.1093/nar/gkt268.
42. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207–234. http://dx.doi.org/10.1016/j.pep.2005.01.016.
43. Cox G, Thompson GS, Jenkins HT, Peske F, Savelsbergh A, Rodnina MV, Wintermeyer W, Homans SW, Edwards TA, O’Neill AJ. 2012. Ribosome clearance by FusB-type proteins mediates resistance to the antibiotic fusidic acid. Proc Natl Acad Sci U S A 109:2102–2107. http://dx.doi.org/10.1073/pnas.1117275109.
44. Murray RW, Melchior EP, Hagadorn JC, Marotti KR. 2001. Staphylococcus aureus cell extract transcription-translation assay: firefly luciferase reporter system for evaluating protein translation inhibitors. Antimicrob Agents Chemother 45:1900–1904. http://dx.doi.org/10.1128/AAC.45.6.1900-1904.2001.
45. Maguire BA, Wondrack LM, Contillo LG, Xu Z. 2008. A novel chromatography system to isolate active ribosomes from pathogenic bacteria. RNA 14:188–195. http://dx.doi.org/10.1261/rna.692408.
46. Burdett V. 1996. Tet(M)-promoted release of tetracycline from ribosomes is GTP dependent. J Bacteriol 178:3246–3251.
47. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725–2729. http://dx.doi.org/10.1093/molbev/mst197.
48. Kim EB, Kopit LM, Harris LJ, Marco ML. 2012. Draft genome sequence of the quality control strain Enterococcus faecalis ATCC 29212. J Bacteriol 194:6006–6007. http://dx.doi.org/10.1128/JB.01423-12.
49. Fairweather N, Kennedy S, Foster TJ, Kehoe M, Dougan G. 1983. Expression of a cloned Staphylococcus aureus alpha-hemolysin determinant in Bacillus subtilis and Staphylococcus aureus. Infect Immun 41:1112–1117.
50. Rogé J, Betton JM. 2005. Use of pIVEX plasmids for protein overproduction in Escherichia coli. Microb Cell Fact 4:18. http://dx.doi.org/10.1186/1475-2859-4-18.