Antibiotic efflux pumps

Biochemical Pharmacology

Volumn 60, Issue 4, 2000, Pages 457-470

  Van Bambeke, Françoise ^a   Balzi, Elisabetta ^a   Tulkens, Paul M ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Antibiotic; Chemotherapy; Efflux pump; Infection; Resistance; Transport

Indexed keywords

ABC TRANSPORTER; AMINOGLYCOSIDE ANTIBIOTIC AGENT; ANTIBIOTIC AGENT; BETA LACTAM ANTIBIOTIC; FUSIDIC ACID; GLYCOPROTEIN P; LINCOSAMIDE DERIVATIVE; MACROLIDE; PENICILLIN DERIVATIVE; PENICILLIN G; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; RIFAMYCIN; SULFADIAZINE; TETRACYCLINE DERIVATIVE;

ANTIBIOTIC RESISTANCE; CELL TRANSPORT; DRUG ACCUMULATION; ENZYME SPECIFICITY; EUKARYOTE; GENE MUTATION; INFECTION; MULTIDRUG RESISTANCE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PUMP; REVIEW;

EID: 0034664167     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(00)00291-4     Document Type: Article

References (118)

1. Kolaczkowski M., Goffeau A. Active efflux by multidrug transporters as one of the strategies to evade chemotherapy and novel practical implications of yeast pleiotropic drug resistance. Pharmacol Ther. 76:1997;219-242.
2. Ishikawa T., Li Z.S., Lu Y.P., Rea P.A. The GS-X pump in plant, yeast, and animal cells Structure, function, and gene expression . Biosci Rep. 17:1997;189-207.
3. Wacher V.J., Silverman J.A., Zhang Y., Benet L.Z. Role of P-glycoprotein and cytochrome P450 3A in limiting oral absorption of peptides and peptidomimetics. J Pharm Sci. 87:1998;1322-1330.
4. Hall S.D., Thummel K.E., Watkins P.B., Lown K.S., Benet L.Z., Paine M.F., Wrighton S.A. Molecular and physical mechanisms of first-pass extraction. Drug Metab Dispos. 27:1999;161-166.
5. Suzuki H., Sugiyama Y. Excretion of GSSG and glutathione conjugates mediated by MRP1 and cMOAT/MRP2. Semin Liver Dis. 18:1998;359-376.
6. Paulsen I.T., Sliwinski M.K., Saier M.H. Jr. Microbial genome analyses Global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities . J Mol Biol. 277:1998;573-592.
7. Paulsen I.T., Sliwinski M.K., Nelissen B., Goffeau A., Saier M.H. Jr. Unified inventory of established and putative transporters encoded within the complete genome of Saccharomyces cerevisiae. FEBS Lett. 430:1998;116-125.
8. Mendez C., Salas J.A. ABC transporters in antibiotic-producing actinomycetes. FEMS Microbiol Lett. 158:1998;1-8.
9. Paulsen I.T., Skurray R.A., Tam R., Saier M.H., Turner R.J., Weiner J.H., Grinius L.L. The SMR family A novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs . Mol Microbiol. 19:1996;1167-1175.
10. Hogue D.L., Ellison M.J., Young J.D., Cass C.E. Identification of a novel membrane transporter associated with intracellular membranes by phenotypic complementation in the yeast Saccharomyces cerevisiae. J Biol Chem. 271:1996;9801-9808.
11. Hogue D.L., Kerby L., Ling V. A mammalian lysosomal membrane protein confers multidrug resistance upon expression in Saccharomyces cerevisiae. J Biol Chem. 274:1999;12877-12882.
12. Tseng T.T., Gratwick K.S., Kolman J., Park D., Nies D.H., Goffeau A., Saier M.H. The RND permease superfamily An ancient, ubiquitous and diverse family that includes human disease and development proteins . J Mol Microbiol Biotechnol. 1:1999;107-125.
13. Saier M.H., Paulsen I.T., Sliwinski M.K., Pao S.S., Skurray R.A., Nikaido H. Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. FASEB J. 12:1998;265-274.
14. Paulsen I.T., Brown M.H., Skurray R.A. Proton-dependent multidrug efflux systems. Microbiol Rev. 60:1996;575-608.
15. Marger M.D., Saier M.H. A major superfamily of membrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci. 18:1993;13-20.
16. Pao S.S., Paulsen I.T., Saier M.H. Major facilitator superfamily. Microbiol Mol Biol Rev. 62:1998;1-34.
17. Morita Y., Kodama K., Shiota S., Mine T., Kataoka A., Mizushima T., Tsuchiya T. NorM, a putative multidrug efflux protein of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Chemother. 42:1998;1778-1782.
18. Higgins C.F. ABC transporters From microorganisms to man . Annu Rev Cell Biol. 8:1992;67-113.
19. Decottignies A., Goffeau A. Complete inventory of the yeast ABC proteins. Nat Genet. 15:1997;137-145.
20. Croop J.M. Evolutionary relationships among ABC transporters. Methods Enzymol. 292:1998;101-116.
21. Taglicht D., Michaelis S. Saccharomyces cerevisiae ABC proteins and their relevance to human health and disease. Methods Enzymol. 292:1998;130-162.
22. van Veen H., Konings W.N. The ABC family of multidrug transporters in microorganisms. Biochim Biophys Acta. 1365:1998;31-36.
23. Saurin W., Hofnung M., Dassa E. Getting in or out Early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters . J Mol Evol. 48:1999;22-41.
24. Ruetz S., Brault M., Kast C., Hemenway C., Heitman J., Grant C.E., Cole S.P.C., Deeley R.G., Gros P. Functional expression of the multidrug resistance-associated protein in the yeast Saccharomyces cerevisiae. J Biol Chem. 271:1996;4154-4160.
25. van Veen H.W., Callaghan R., Soceneantu L., Sardini A., Konings W.N., Higgins C.F. A bacterial antibiotic-resistance gene that complements the human multidrug-resistance P-glycoprotein gene. Nature. 391:1998;291-295.
26. Cole S.P.C., Deeley R.G. Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. Bioessays. 20:1998;931-940.
27. Paul S., Breuninger L.M., Tew K.D., Shen H., Kruh G.D. ATP-dependent uptake of natural product cytotoxic drugs by membrane vesicles establishes MRP as a broad specificity transporter. Proc Natl Acad Sci USA. 93:1996;6929-6934.
28. Kolaczkowski M., Kolaczkowska A., Luczynski J., Stanislaw W., Goffeau A. In vivo characterization of the drug resistance profile of the major ABC transporters and other components of the yeast pleiotropic drug resistance network. Microb Drug Resist. 4:1998;143-158.
29. Paulsen I.T., Skurray R.A. Topology, structure and evolution of two families of proteins involved in antibiotic and antiseptic resistance in eukaryotes and prokaryotes - an analysis. Gene. 124:1993;1-11.
30. Maloney P.C. Bacterial and plant antiporters. J Exp Biol. 196:1994;439-442.
31. +-coupled multidrug transporter from Escherichia coli, reveals a hydrophobic pathway for solutes. J Biol Chem. 274:1999;19480-19486.
32. Grinius L.L., Goldberg E.B. Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump. J Biol Chem. 269:1994;29998-30004.
33. Edgar R., Bibi E. A single membrane-embedded negative charge is critical for recognizing positively charged drugs by the Escherichia coli multidrug resistance protein MdfA. EMBO J. 18:1999;822-832.
34. Guan L., Ehrmann M., Yoneyama H., Nakae T. Membrane topology of the xenobiotic-exporting subunit, MexB, of the MexA,B-OprM extrusion pump in Pseudomonas aeruginosa. J Biol Chem. 274:1999;10517-10522.
35. Paulsen I.T., Park J.H., Choi P.S., Saier M.H. A family of Gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol Lett. 156:1997;1-8.
36. Sonveaux N., Shapiro A.B., Goormaghtigh E., Ling V., Ruysschaert J.M. Secondary and tertiary structure changes of reconstituted P-glycoprotein. A Fourier transform attenuated total reflection infrared spectroscopy analysis. J Biol Chem. 271:1996;24617-24624.
37. Sharom F.J. The P-glycoprotein efflux pump How does it transport drugs? J Membr Biol. 160:1997;161-175.
38. 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. 274:1999;3541-3548.
39. Nikaido H. Multidrug efflux pumps of Gram-negative bacteria. J Bacteriol. 178:1996;5853-5859.
40. Nikaido H. Multiple antibiotic resistance and efflux. Curr Opin Microbiol. 1:1998;516-523.
41. Higgins C.F., Gottesman M.M. Is the multidrug transporter a flippase? Trends Biochem Sci. 17:1992;18-21.
42. Wadkins R.M., Houghton P.J. The role of drug-lipid interactions in the biological activity of modulators of multi-drug resistance. Biochim Biophys Acta. 1153:1993;225-236.
43. Bolhuis H., van Veen H.W., Molenaar D., Poolman B., Driessen A.J.M., Konings W.N. Multidrug resistance in Lactococcus lactis Evidence for ATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane . EMBO J. 15:1996;4239-4245.
44. Ashida H., Oonishi T., Uyesaka N. Kinetic analysis of the mechanism of action of the multidrug transporter. J Theor Biol. 195:1998;219-232.
45. Rosenberg M.F., Callaghan R., Ford R.C., Higgins C.F. Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J Biol Chem. 272:1997;10685-10694.
46. Pawagi A.B., Wang J., Silverman M., Reithmeier R.A., Deber C.M. Transmembrane aromatic amino acid distribution in P-glycoprotein. A functional role in broad substrate specificity. J Mol Biol. 235:1994;554-564.
47. Smith A.J., Timmermans-Hereijgers J.L., Roelofsen B., Wirtz K.W., van Blitterswijk W.J., Smit J.J., Schinkel A.H., Borst P. The human MDR3 P-glycoprotein promotes translocation of phosphatidylcholine through the plasma membrane of fibroblasts from transgenic mice. FEBS Lett. 354:1994;263-266.
48. Zhou Y., Gottesman M.M., Pastan I. Studies with human MDR1-MDR2 chimeras demonstrate the functional exchangeability of a major transmembrane segment of the multidrug transporter of phosphatidylcholine flippase. Mol Cell Biol. 19:1999;1450-1459.
49. Sokal A., Pulaski L., Rychlik B., Fortuniak A., Bartosz G. Is the glutathione S-conjugate pump a flippase? Biochem Mol Biol Int. 44:1998;97-105.
50. Decottignies A., Grant A.M., Nichols J.W., de Wet H., McIntosh D.B., Goffeau A. ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J Biol Chem. 273:1998;12612-12622.
51. Hsieh P.C., Siegel S.A., Rogers B., Davis D., Lewis K. Bacteria lacking a multidrug pump A sensitive tool for drug discovery . Proc Natl Acad Sci USA. 95:1998;6602-6606.
52. Nikaido H., Basina M., Nguyen V., Rosenberg E.Y. Multidrug efflux pump AcrAB of Salmonella typhimurium excretes only those β-lactam antibiotics containing lipophilic side chains. J Bacteriol. 180:1998;4686-4692.
53. Nilsen I.W., Bakke I., Vader A., Olsvik O., El-Gewely M.R. Isolation of cmr, a novel Escherichia coli chloramphenicol resistance gene encoding a putative efflux pump. J Bacteriol. 178:1996;3188-3193.
54. Aires J.R., Köhler T., Nikaido H., Plésiat P. Involvement of an active efflux system in the natural resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob Agents Chemother. 43:1999;2624-2628.
55. Moore R.A., DeShazer D., Reckseidler S., Weissman A., Woods D.E. Efflux-mediated aminoglycoside and macrolide resistance in Burkholderia pseudomallei. Antimicrob Agents Chemother. 43:1999;465-470.
56. Mingeot-Leclercq M.P., Glupczynski Y., Tulkens P.M. Aminoglycosides Activity and resistance . Antimicrob Agents Chemother. 43:1999;727-737.
57. Mingeot-Leclercq M.P., Tulkens P.M. Aminoglycosides Nephrotoxicity . Antimicrob Agents Chemother. 43:1999;1003-1012.
58. Cundliffe E. Self-protection mechanisms in antibiotic producers. Ciba Found Symp. 171:1992;208-214.
59. Hancock R.E.W., Farmer S.W. Mechanism of uptake of deglucoteicoplanin amide derivatives across outer membranes of Escherichia coli and Pseudomonas aeruginosa. Antimicrob Agents Chemother. 37:1993;453-456.
60. Nakae T., Yoshihara E., Yoneyama H. Multiantibiotic resistance caused by active drug extrusion in hospital pathogens. J Infect Chemother. 3:1997;173-183.
61. Ball P.R., Shales S.W., Chopra I. Plasmid-mediated tetracycline resistance in Escherichia coli involves increased efflux of the antibiotic. Biochem Biophys Res Commun. 93:1980;74-81.
62. McMurry L., Petrucci R.E. Jr, Levy S.B. Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc Natl Acad Sci USA. 77:1980;3974-3977.
63. Clancy J., Petitpas J., Dib-Hajj F., Yuan W., Cronan M., Kamath A.V., Bergeron J., Retsema J.A. Molecular cloning and functional analysis of a novel macrolide-resistance determinant, mefA, from Streptococcus pyogenes. Mol Microbiol. 22:1996;867-879.
64. Ubukata K., Itoh-Yamashita N., Konno M. Cloning and expression of the norA gene for fluoroquinolone resistance in Staphylococcus aureus. Antimicrob Agents Chemother. 33:1989;1535-1539.
65. Sutcliffe J., Tait-Kamradt A., Wondrack L. Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin A common resistance pattern mediated by an efflux system . Antimicrob Agents Chemother. 40:1996;1817-1824.
66. Brenwald N.P., Gill M.J., Wise R. Prevalence of a putative efflux mechanism among fluoroquinolone-resistant clinical isolates of Streptococcus pneumoniae. Antimicrob Agents Chemother. 42:1998;2032-2035.
67. Kaatz G.W., Seo S.M., Ruble C.A. Efflux-mediated fluoroquinolone resistance in Staphylococcus aureus. Antimicrob Agents Chemother. 37:1993;1086-1094.
68. Li X.-Z., Nikaido H., Poole K. Role of MexA-MexB-OprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 39:1995;1948-1953.
69. Masuda N., Gotoh N., Ishii C., Sakagawa E., Ohya S., Nishino T. Interplay between chromosomal β-lactamase and the MexAB-oprM efflux system in intrinsic resistance to β-lactams in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 43:1999;400-402.
70. Lakaye B., Dubus A., Lepage S., Groslambert S., Frere J.M. When drug inactivation renders the target irrelevant to antibiotic resistance A case story with β-lactams . Mol Microbiol. 31:1999;89-101.
71. Nakae T., Nakajima A., Ono T., Saito K., Yoneyama H. Resistance to β-lactam antibiotics in Pseudomonas aeruginosa due to interplay between the MexAB-OprM efflux pump and β-lactamase. Antimicrob Agents Chemother. 43:1999;1301-1303.
72. Janoir C., Zeller V., Kitzis M.-D., Moreau N.J., Gutmann L. High-level fluoroquinolone resistance in. Streptococcus pneumoniae requires mutations in parC and gyrA. Antimicrob Agents Chemother. 40:1996;2760-2764.
73. Jalal S., Wretlind B. Mechanims of quinolone resistance in clinical strains of Pseudomonas aeruginosa. Microb Drug Resist. 4:1998;257-261.
74. Banerjee S.K., Bhatt K., Rana S., Misra P., Chakraborti P.K. Involvement of an efflux system in mediating high level of fluoroquinolone resistance in Mycobacterium smegmatis. Biochem Biophys Res Commun. 226:1996;362-368.
75. Tanaka M., Sakuma S., Takahashi K., Nagahuzi T., Saika T., Kobayashi I., Kumazawa J. Analysis of quinolone resistance mechanisms in Neisseria gonorrhoeae isolates in vitro. Sex Transm Infect. 74:1998;59-62.
76. Lomovskaya O., Lee A., Hoshino K., Ishida H., Mistry A., Warren M.S., Boyer E., Chamberland S., Lee V.J. Use of a genetic approach to evaluate the consequences of inhibition of efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 43:1999;1340-1346.
77. Li X.-Z., Ma D., Livermore D.M., Nikaido H. Role of efflux pump(s) in intrinsic resistance of Pseudomonas aeruginosa Active efflux as a contributing factor to β-lactam resistance . Antimicrob Agents Chemother. 38:1994;1742-1752.
78. Nikaido H. Antibiotic resistance caused by Gram-negative multidrug efflux pumps. Clin Infect Dis. 27:1998;S32-S41.
79. Balzi E., Goffeau A. Yeast multidrug resistance The PDR network . J Bioenerg Biomembr. 27:1995;71-76.
80. Sanglard D., Kuchler K., Ischer F., Pagani J.-L., Monod M., Bille J. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob Agents Chemother. 39:1995;2378-2386.
81. White T.C., Marr K.A., Bowden R. Clinical, cellular and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev. 11:1998;382-402.
82. Ziha-Zarifi I., Llanes C., Köhler T., Pechere J.-C., Plésiat P. In vivo emergence of multidrug-resistant mutants of Pseudomonas aeruginosa overexpressing the active efflux system MexA-MexB-OprM. Antimicrob Agents Chemother. 43:1999;287-291.
83. Limia A., Jimenez M.L., Delgado T., Sanchez I., Lopez S., Lopez-Brea M. Phenotypic characterization of erythromycin resistance in strains of the genus Streptococcus isolated from clinical specimens. Rev Esp Quimiter. 11:1998;216-220.
84. Orden B., Perez-Trallero E., Montes M., Martinez R. Erythromycin resistance of Streptococcus pyogenes in Madrid. Pediatr Infect Dis J. 17:1998;470-473.
85. Shortridge V.D., Doern G.V., Brueggemann A.B., Beyer J.M., Flamm R.K. Prevalence of macrolide resistance mechanisms in Streptococcus pneumoniae isolates from a multicenter antibiotic resistance surveillance study conducted in the United States in 1994-1995. Clin Infect Dis. 29:1999;1186-1188.
86. Stieger B., Meier P.J. Bile acid and xenobiotic transporters in liver. Curr Opin Cell Biol. 10:1998;462-467.
87. Roch-Ramel F. Renal transport of organic anions. Curr Opin Nephrol Hypertens. 7:1998;517-524.
88. Saitoh H., Fujisaki H., Aungst B.J., Miyazaki K. Restricted intestinal absorption of some β-lactam antibiotics by an energy-dependent efflux system in rat intestine. Pharm Res. 14:1997;645-649.
89. Cavet M.E., West M., Simmons N.L. Transepithelial transport of the fluoroquinolone ciprofloxacin by human airway epithelial Calu-3 cells. Antimicrob Agents Chemother. 41:1997;2693-2698.
90. Dautrey S., Felice K., Petiet A., Lacour B., Carbon C., Farinotti R. Active intestinal elimination of ciprofloxacin in rats Modulation by different substrates . J Pharmacol. 127:1999;1728-1734.
91. Saitoh H., Gerard C., Aungst B.J. The secretory intestinal transport of some beta-lactam antibiotics and anionic compounds A mechanism contributing to poor oral absorption . J Pharmacol Exp Ther. 278:1996;205-211.
92. Snyder N.J., Tabas L.B., Berry D.M., Duckworth D.C., Spry D.O., Dantzig A.H. Structure-activity relationship of carbacephalosporins and cephalosporins Antibacterial activity and interaction with the intestinal proton-dependent dipeptide transport carrier of Caco-2 cells . Antimicrob Agents Chemother. 41:1997;1649-1657.
93. Race J.E., Grassl S.M., Williams W.J., Holtzman E.J. Molecular cloning and characterization of two novel human renal organic anion transporters (hOAT1 and hOAT3). Biochem Biophys Res Commun. 255:1999;508-514.
94. Sasabe H., Terasaki T., Tsuji A., Sugiyama Y. Carrier-mediated hepatic uptake of quinolone antibiotics in the rat. J Pharmacol Exp Ther. 282:1997;162-171.
95. Cao C.X., Silverstein S.C., Neu H.C., Steinberg T.H. J774 macrophages secrete antibiotics via organic anion transporters. J Infect Dis. 165:1992;322-328.
96. Rudin D.E., Gao P.X., Cao C.X., Neu H.C., Silverstein S.C. Gemfibrozil enhances the listericidal effects of fluoroquinolone antibiotics in J774 macrophages. J Exp Med. 176:1992;1439-1447.
97. Nichterlein T., Kretschmar M., Siegsmund M., Hof H. Erythromycin is ineffective against Listeria monocytogenes in multidrug resistant cells. J Chemother. 7:1995;184-188.
98. Nichterlein T., Kretschmar M., Schadt A., Meyer A., Wildfeuer A., Laufen H., Hof H. Reduced intracellular activity of antibiotics against Listeria monocytogenes in multidrug resistant cells. Int J Antimicrob Agents. 10:1998;119-125.
99. Oh Y.K., Straubinger R.M. Cellular delivery of liposome-delivered anionic compounds modulated by a probenecid-sensitive anion transporter. Pharm Res. 14:1997;1203-1209.
100. Testa R.T., Petersen P.J., Jacobus N.V., Sum P.E., Lee V.J., Tally F.P. In vitro and in vivo antibacterial activities of the glycylcyclines, a new class of semisynthetic tetracyclines. Antimicrob Agents Chemother. 37:1993;2270-2277.
101. Chu D.T. Recent developments in macrolides and ketolides. Curr Opin Microbiol. 2:1999;467-474.
102. McCarthy J., Hogle J.M., Karplus M. Use of the multiple copy simultaneous search (MCSS) method to design a new class of picornavirus capsid binding drugs. Proteins. 29:1997;32-58.
103. Litman T., Zeuthen T., Skovsgaard T., Stein W.D. Structure-activity relationships of P-glycoprotein interacting drugs Kinetic characterization of their effects on ATPase activity . Biochim Biophys Acta. 1361:1997;159-168.
104. Ford J.M., Hait W.N. Pharmacologic circumvention of multidrug resistance. Cytotechnology. 12:1993;171-212.
105. Tmej C., Chiba P., Huber M., Richter E., Hitzler M., Schaper K.J., Ecker G. A combined Hansch/Free-Wilson approach as predictive tool in QSAR studies on propafenone-type modulators of multidrug resistance. Arch Pharm (Weinheim). 331:1998;233-240.
106. Dinh T.Q., Smith C.D., Du X., Armstrong R.W. Design, synthesis, and evaluation of the multidrug resistance-reversing activity of D-glucose mimetics of hapalosin. J Med Chem. 41:1998;981-987.
107. Ecker G., Huber M., Schmid D., Chiba P. The importance of a nitrogen atom in modulators of multidrug resistance. Mol Pharmacol. 56:1999;791-796.
108. Markham P.N., Westhaus E., Klyachko K., Johnson M.E., Neyfakh A.A. Multiple novel inhibitors of the NorA multidrug transporter of Staphylococcus aureus. Antimicrob Agents Chemother. 43:1999;2404-2408.
109. Gosland M.P., Lum B.L., Sikic B.I. Reversal by cefoperazone of resistance to etoposide, doxorubicin and vinblastine in multidrug resistant human sarcoma cells. Cancer Res. 49:1989;6901-6905.
110. Crosta L., Candiloro V., Meli M., Tolomeo M., Rausa L., Dusonchet L. Lacidipine and josamycin Two new multidrug resistance modulators . Anticancer Res. 14:1994;2685-2690.
111. Fardel O., Lecureur V., Loyer P., Guillouzo A. Rifampicin enhances anti-cancer drug accumulation and activity in multidrug-resistant cells. Biochem Pharmacol. 49:1995;1255-1260.
112. Phung-Ba V., Warnery A., Scherman D., Wils P. Interaction of pristinamycin IA with P-glycoprotein in human intestinal epithelial cells. Eur J Pharmacol. 288:1995;187-192.
113. Takano M., Hasegawa R., Fukuda T., Yumoto R., Nagai J., Murakami T. Interaction with P-glycoprotein and transport of erythromycin, midazolam and ketoconazole in Caco-2 cells. Eur J Pharmacol. 358:1998;289-294.
114. Raderer M., Scheithauer W. Clinical trials of agents that reverse multidrug resistance. Cancer. 72:1993;3553-3563.
115. Wegener H.C., Aarestrup F.M., Jensen L.B., Hammerum A.M., Bager F. Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerg Infect Dis. 5:1999;329-335.
116. Belinsky M.G., Bain L.J., Testa J.R., Kruh G.D. Characterization of MOAT-C and MOAT-D, new members of the MRP/cMOAT subfamily of transporter proteins. J Natl Cancer Inst. 90:1998;1735-1741.
117. Georges E., Tsuruo T., Ling V. Topology of P-glycoprotein as determined by epitope mapping of MRK-16 monoclonal antibodies. J Biol Chem. 268:1993;1792-1798.
118. Bakos E., Hegedüs T., Hollo Z., Welker E., Tusnady G., Zaman G.J.R., Sarkadi B. Membrane topology and glycosylation of the human multidrug resistance-associated protein. J Biol Chem. 271:1996;12322-12326.