Novel insight into antimicrobial resistance and sensitivity phenotypes associated to qac and norA genotypes in Staphylococcus aureus

Microbiological Research

Volumn 170, Issue , 2015, Pages 184-194

  Marchi, Emmanuela ^a   Furi, Leonardo ^b   Arioli, Stefania ^c   Morrissey, Ian ^d,e   Di Lorenzo, Valeria ^d,e   Mora, Diego ^c   Giovannetti, Luciana ^a   Oggioni, Marco Rinaldo ^b,f   Viti, Carlo ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

^c La Nutrizione e l'Ambiente   (Italy)

^d Quotient Bioresearch Ltd   (United Kingdom)

^e International Health Management Associates Europe Sàrl   (Switzerland)

^f UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Multidrug resistance; NorA promoter mutations; Phenotype microarray; QAC transporters; Staphylococcus aureus

Indexed keywords

BACTERIA; SUBSTRATES;

8-HYDROXYQUINOLINE; ANTIMICROBIAL RESISTANCES; GUANIDINE HYDROCHLORIDE; MULTIDRUG RESISTANCE; NORA PROMOTER MUTATIONS; QAC TRANSPORTERS; SPECIFIC SUBSTRATES; SUBSTRATE SPECIFICITY;

STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CARRIER PROTEIN; MULTIDRUG RESISTANCE PROTEIN; NORA PROTEIN, STAPHYLOCOCCUS; QACA PROTEIN, STAPHYLOCOCCUS AUREUS;

ANTIBIOTIC RESISTANCE; CLUSTER ANALYSIS; DRUG EFFECTS; GENETICS; GENOTYPE; HUMAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHENOTYPE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CLUSTER ANALYSIS; DRUG RESISTANCE, BACTERIAL; GENOTYPE; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PHENOTYPE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 85050314138     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2014.07.001     Document Type: Article

References (57)

1. Andersson D.I., Levin B.R. The biological cost of antibiotic resistance. Curr Opin Microbiol 1999, 2:489-493.
2. Bay D.C., O'Neil J.D., Court D.A. The influence of sterols on the conformation of recombinant mitochondrial porin in detergent. Biochem Cell Biol 2008, 86:539-545.
3. Bjorland J., Steinum T., Sunde M., Waage S., Heir E. Novel plasmid-borne gene qacJ mediates resistance to quaternary ammonium compounds in equine Staphylococcus aureus, Staphylococcus simulans, and Staphylococcus intermedius. Antimicrob Agents Chemother 2003, 47:3046-3052.
4. Bochner B.R., Gadzinski P., Panomitros E. Phenotype MicroArrays for high-throughput phenotypic testing and assay of gene function. Genome Res 2001, 11:1246-1255.
5. Bochner B.R., Giovannetti L., Viti C. Important discoveries from analysing bacterial phenotypes. Mol Microbiol 2008, 70:274-280.
6. Bonde M., Hojland D.H., Kolmos H.J., Kallipolitis B.H., Klitgaard J.K. Thioridazine affects transcription of genes involved in cell wall biosynthesis in methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 2011, 318:168-176.
7. Ciusa M.L., Furi L., Knight D., Decorosi F., Fondi M., Raggi C., et al. A novel resistance mechanism to triclosan that suggests horizontal gene transfer and demonstrates a potential selective pressure for reduced biocide susceptibility in clinical strains of Staphylococcus aureus. Int J Antimicrob Agents 2012, 40:210-220.
8. CLSI Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; Approved standard 2009, CLSI, Wayne, PA, USA.
9. Corona G.L., Santagostino G., Facino Rm, Pirillo D. Cell membrane modifications in rabbit isolated hepatocytes following a chronic amitryptiline treatment. Biochem Pharmacol 1973, 22:849-856.
10. Correa J.E., De Paulis A., Predari S., Sordelli D.O., Jeric P.E. First report of qacG, qacH and qacJ genes in Staphylococcus haemolyticus human clinical isolates. J Antimicrob Chemother 2008, 62:956-960.
11. Couto I., Costa S.S., Viveiros M., Martins M., Amaral L. Efflux-mediated response of Staphylococcus aureus exposed to ethidium bromide. J Antimicrob Chemother 2008, 62:504-513.
12. Cui L.Z., Murakami H., Kuwahara-Arai K., Hanaki H., Hiramatsu K. Contribution of a thickened cell wall and its glutamine nonamidated component to the vancomycin resistance expressed by Staphylococcus aureus Mu50. Antimicrob Agents Chemother 2000, 44:2276-2285.
13. Decorosi F., Lori L., Santopolo L., Tatti E., Giovannetti L., Viti C. Characterization of a Cr(VI)-sensitive Pseudomonas corrugata 28 mutant impaired in a pyridine nucleotide transhydrogenase gene. Res Microbiol 2011, 162:747-755.
14. Decorosi F., Tatti E., Mini A., Giovannetti L., Viti C. Characterization of two genes involved in chromate resistance in a Cr(VI)-hyper-resistant bacterium. Extremophiles 2009, 13:917-923.
15. Desaphy J.F., Dipalma A., De Bellis M., Costanza T., Gaudioso C., Delmas P., et al. Involvement of voltage-gated sodium channels blockade in the analgesic effects of orphenadrine. Pain 2009, 142:225-235.
16. Dey S., Hafkemeyer P., Pastan I., Gottesman M.M. A single amino acid residue contributes to distinct mechanisms of inhibition of the human multidrug transporter by stereoisomers of the dopamine receptor antagonist flupentixol. Biochemistry 1999, 38:6630-6639.
17. Dutta N.K., Mehra S., Kaushal D. A Mycobacterium tuberculosis sigma factor network responds to cell-envelope damage by thepromising anti-mycobacterial thioridazine. PLoS One 2010, 5.
18. Eady E.A., Ross J.I., Tipper J.L., Walters C.E., Cove J.H., Noble W.C. Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci. J Antimicrob Chemother 1993, 31:211-217.
19. Floyd J.L., Smith K.P., Kumar S.H., Floyd J.T., Varela M.F. LmrS is a multidrug efflux pump of the major facilitator superfamily from Staphylococcus aureus. Antimicrob Agents Chemother 2010, 54:5406-5412.
20. Fraser R.S., Creanor J. The mechanism of inhibition of ribonucleic acid synthesis by 8-hydroxyquinoline and the antibiotic lomofungin. Biochem J 1975, 147:401-410.
21. Furi L., Ciusa M.L., Knight D., Di Lorenzo V., Tocci N., Cirasola D., et al. Evaluation of reduced susceptibility to quaternary ammonium compounds and bisbiguanides in clinical isolates and laboratory-generated mutants of Staphylococcus aureus. Antimicrob Agents Chemother 2013, 57:3488-3497.
22. Gokel G.W., Leevy W.M., Weber M.E. Crown ethers: sensors for ions and molecular scaffolds for materials and biological models. Chem Rev 2004, 104:2723-2750.
23. Grinius L., Dreguniene G., Goldberg E.B., Liao C.H., Projan S.J. A staphylococcal multidrug resistance gene-product is a member of a new-protein family. Plasmid 1992, 27:119-129.
24. Heir E., Sundheim G., Holck A.L. The Staphylococcus qacH gene product: a new member of the SMR family encoding multidrug resistance. FEMS Microbiol Lett 1998, 163:49-56.
25. Heir E., Sundheim G., Holck A.L. The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J Appl Microbiol 1999, 86:378-388.
26. Kaatz G.W., Moudgal V.V., Seo S.M., Kristiansen J.E. Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrob Agents Chemother 2003, 47:719-726.
27. Kaatz G.W., Seo S.M., Ruble C.A. Efflux-mediated fluoroquinolone resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1993, 37:1086-1094.
28. Kawai M., Yamada S., Ishidoshiro A., Oyamada Y., Ito H., Yamagishi J. Cell-wall thickness: possible mechanism of acriflavine resistance in meticillin-resistant Staphylococcus aureus. J Med Microbiol 2009, 58:331-336.
29. Koo B.M., Yoon M.J., Lee C.R., Nam T.W., Choe Y.J., Jaffe H., et al. A novel fermentation/respiration switch protein regulated by enzyme IIA(Glc) in Escherichia coli. J Biol Chem 2004, 279:31613-31621.
30. Leclercq R. Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Clin Infect Dis 2002, 34:482-492.
31. Leelaporn A., Paulsen I.T., Tennent J.M., Littlejohn T.G., Skurray R.A. Multidrug-resistance to antiseptics and disinfectants in coagulase-negative staphylococci. J Med Microbiol 1994, 40:214-220.
32. Littlejohn T.G., Paulsen I.T., Gillespie M.T., Tennent J.M., Midgley M., Jones I.G., et al. Substrate-specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol Lett 1992, 95:259-266.
33. Longtin J., Seah C., Siebert K., McGeer A., Simor A., Longtin Y., et al. Distribution of antiseptic resistance genes qacA, qacB, and smr in methicillin-resistant Staphylococcus aureus isolated in Toronto, Canada, from 2005 to 2009. Antimicrob Agents Chemother 2011, 55:2999-3001.
34. Mayer S., Boos M., Beyer A., Fluit A.C., Schmitz F.J. Distribution of the antiseptic resistance genes qacA, qacB and qacC in 497 methicillin-resistant and -susceptible European isolates of Staphylococcus aureus. J Antimicrob Chemother 2001, 47:896-897.
35. Mitchell B.A., Brown M.H., Skurray R.A. QacA multidrug efflux pump from Staphylococcus aureus: comparative analysis of resistance to diamidines, biguanidines, and guanylhydrazones. Antimicrob Agents Chemother 1998, 42:475-477.
36. Mitchell B.A., Paulsen I.T., Brown M.H., Skurray R.A. Bioenergetics of the staphylococcal multidrug export protein QacA - Identification of distinct binding sites for monovalent and divalent cations. J Biol Chem 1999, 274:3541-3548.
37. Molnar J., Foldeak S., Nakamura M.J., Rausch H., Domonkos K., Szabo M. Antiplasmid activity - loss of bacterial-resistance to antibiotics. APMIS 1992, 100:24-31.
38. Nakaminami H., Noguchi N., Sasatsu M. Fluoroquinolone efflux by the plasmid-mediated multidrug efflux pump QacB variant QacBIII in Staphylococcus aureus. Antimicrob Agents Chemother 2010, 54:4107-4111.
39. Noguchi N., Hase M., Kitta M., Sasatsu M., Deguchi K., Kono M. Antiseptic susceptibility and distribution of antiseptic-resistance genes in methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 1999, 172:247-253.
40. Noguchi N., Suwa J., Narui K., Sasatsu M., Ito T., Hiramatsu K., et al. Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J Med Microbiol 2005, 54:557-565.
41. Patel D., Kosmidis C., Seo S.M., Kaatz G.W. Ethidium bromide MIC screening for enhanced efflux pump gene expression or efflux activity in Staphylococcus aureus. Antimicrob Agents Chemother 2010, 54:5070-5073.
42. Paulsen I.T., Brown M.H., Dunstan S.J., Skurray R.A. Molecular characterization of the staphylococcal multidrug-resistance export protein QacC. J Bacteriol 1995, 177:2827-2833.
43. Paulsen I.T., Brown M.H., Littlejohn T.G., Mitchell B.A., Skurray R.A. Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: membrane topology and identification of residues involved in substrate specificity. Proc Natl Acad Sci USA 1996, 93:3630-3635.
44. Pechere J.C. Macrolide resistance mechanisms in Gram-positive cocci. J Antimicrob Chemother 2001, 18:S25-S28.
45. Poole K. Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 2005, 56:20-51.
46. Rubbo C.A., Albert A., Gibson M.I. The influence of chemical constitution on antibacterial activity. V. The antibacterial action of 8-hydroxyquinoline (oxine). Br J Exp Pathol 1950, 31:425-441.
47. Shearer J.E.S., Wireman J., Hostetler J., Forberger H., Borman J., Gill J., et al. Major families of multiresistant plasmids from geographically and epidemiologically diverse staphylococci. G3 2011, 1:581-591.
48. Short B.R.D., Vargas M.A., Thomas J.C., O'Hanlon S., Enright M.C. In vitro activity of a novel compound, the metal ion chelating agent AQ(+), against clinical isolates of Staphylococcus aureus. J Antimicrob Chemother 2006, 57:104-109.
49. Sureda F.X., Gabriel C., Pallas M., Adan J., Martinez J.M., Escubedo E., et al. In vitro and in vivo protective effect of orphenadrine on glutamate neurotoxicity. Neuropharmacology 1999, 38:671-677.
50. Tennent J.M., Lyon B.R., Midgley M., Jones I.G., Purewal A.S., Skurray R.A. Physical and biochemical characterization of the qacA gene encoding antiseptic and disinfectant resistance in Staphylococcus aureus. J Gen Microbiol 1989, 135:1-10.
51. Ubukata K., Itohyamashita N., Konno M. Cloning and expression of the norA gene for fluoroquinolone resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1989, 33:1535-1539.
52. Viti C., Decorosi F., Mini A., Tatti E., Giovannetti L. Involvement of the oscA gene in the sulphur starvation response and in Cr(VI) resistance in Pseudomonas corrugata 28. Microbiology 2009, 155:95-105.
53. Viti C., Decorosi F., Tatti E., Giovannetti L. Characterization of chromate-resistant and -reducing bacteria by traditional means and by a high-throughput phenomic technique for bioremediation purposes. Biotechnol Prog 2007, 23:553-559.
54. Winterberg K.M., Luecke J., Bruegl A.S., Reznikoff W.S. Phenotypic screening of Escherichia coli K-12 Tn5 insertion libraries, using whole-genome oligonucleotide microarrays. Appl Environ Microbiol 2005, 71:451-459.
55. Yoshida H., Bogaki M., Nakamura S., Ubukata K., Konno M. Nucleotide-sequence and characterization of the Staphylococcus aureus norA gene, which confers resistance to quinolones. J Bacteriol 1990, 172:6942-6949.
56. Yu J.L., Grinius L., Hooper D.C. NorA functions as a multidrug efflux protein in both cytoplasmic membrane vesicles and reconstituted proteoliposomes. J Bacteriol 2002, 184:1370-1377.
57. Zhang M., O'Donoghue M.M., Ito T., Hiramatsu K., Boost M.V. Prevalence of antiseptic-resistance genes in Staphylococcus aureus and coagulase-negative staphylococci colonising nurses and the general population in Hong Kong. J Hosp Infect 2011, 78:113-117.