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  • [1]Poole, K.: Efflux-mediated resistance to fluoroquinolones in Gram-negative bacteria. Antimicrob Agents Chemother 44, 2233-2241 (2000)

  • [2]van Veen, H. W., K. Venema, H. Bolhuis, I. Oussenko, J. Kok, B. Poolman, A. J. Driessen, and W. N. Konings: Multidrug resistance mediated by a bacterial homolog of the human multidrug transporter MDR1. Proc Natl Acad Sci 93, 10668-10672 (1996)

  • [3]Borges-Walmsley, M. I., K. S. McKeegan, and A. R. Walmsley: Structure and function of efflux pumps that confer resistance to drugs. Biochem J 376, 313-338 (2003)

  • [4]Ullah, F., S. A. Malik, J. Ahmed, F. Ullah, S. M. Shah, M. Ayaz, S. Hussain, Khatoon, L: Investigation of the genetic basis of tetracycline resistance in Staphylococcus aureus from Pakistan. Trop J Pharm Res 11, 925-931 (2012)

  • [5]Webber, M., and L. Piddock: The importance of efflux pumps in bacterial antibiotic resistance. J Antimicrob Chemother 51, 9-11 (2003)

  • [6]Piddock, L. J.: Multidrug-resistance efflux pumps? not just for resistance. Nat Rev Microbiol 4, 629-636 (2006)

  • [7]Roberts, M. C.: Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol Rev 19, 1-24 (1996)

  • [8]Ramos, J.: Pseudomonas Virulence and Gene Regulation. In Kluwer Academic/Plenum Publishers, New York, Boston, Dordrecht, London, Moscow. (2004)

  • [9]Putman, M.H., W. van Veen, and W. N. Konings: Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev 64, 672-693 (2000)

  • [10]Nikaido, H.: Multidrug efflux pumps of Gram-negative bacteria. J Bacteriol 178, 5853-5859 (1996)

  • [11]Chang, G.: Multi drug resistance ABC transporters. FEBS Lett 555, 102–105 (2003)

  • [12]Lynch, A. S.: Efflux systems in bacterial pathogens: an opportunity for therapeutic intervention? An industry view. J Biochem Pharmacol 71, 949–956 (2006)

  • [13]Lage, H.: ABC-transporters: Implications on drug resistance from microorganisms to human cancer. Int J Antimicrob Agents 22, 188-199 (2003)

  • [14]Méndez, C., and J. Salas: The role of ABC transporters in antibiotic producing organisms: drug secretion and resistance mechanism. Res Microbiol 152, 341-352 (2001)

  • [15]Ross, J. I., E. A. Eady, J. H. Cove, W. J. Cunliffe, S. Baumberg, and J. C. Wooton: Inducible erythromycin resistance in Staphylococci is encoded by a member of ATP-binding transporter super-gene family. Mol Microbiol 4, 1207-1214 (1990)

  • [16]Poelarends, G. J., P. Mazurkiewicz, and W. N. Konings: Multidrug transporters and antibiotic resistance in Lactococcus lactis. Biochim Biophys Acta 1555, 1-7 (2002)

  • [17]Lee, E. W., M. N. Huda, T. Kuroda, T. Mizushima, and T. Tsuchiya: EfrAB, and ABC multidrug efflux in pump in Enterococcus faecalis. J Antimicrob Agents Chemother 47, 3733-3738 (2003)

  • [18]Huda, N., E. W. Lee, J. Chen, Y. Morita, T. Kuroda, T. Mizushima, and T. Tsuchiya: Molecular cloning and characterisation of an ABC multidrug efflux pump, VcaM, in non-O1 Vibrio cholerae. Antimicrob Agents Chemother 47, 2413-2417 (2003)

  • [19]Raherison, S., P. Gonzalez, H. Renaudin, A. Charron, C. Bébéar, and C. M. Bébéar: Evidence of active efflux pump in resistance to ciprofloxacin and to ethidium bromide by Mycoplasma hominis. Antimicrob Agents Chemothe 46, 672-679 (2002)

  • [20]Schinkel, A H., and J. W. Jonker: Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 55, 3–29 (2003)

  • [21]Juliano, R. L., and V. Ling: A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 152–162 (1976)

  • [22]Senior, A. E., and D. C. Gadsby: ATP hydrolysis cycles and mechanism in P-glycoprotein and CFTR, Semin Cancer Biol 8, 143–150 (1997)

  • [23]Huisman, M. T., J. W. Smit, and A. H. Schinkel.: Significance of P-glycoprotein for the pharmacology and clinical use of HIV protease inhibitors. AIDS 14, 237–242 (2000)

  • [24]Cole, S. P., G. Bhardwaj, J. H. Gerlach, J. E. Mackie, C. E. Grant, K. C. Almquist, A. J. Stewart, E. U. Kurz, A. M. Duncan, and R. G. Deeley: Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258, 1650-1654 (1992)

  • [25]Cole, S. P., K. E. Sparks, K. Fraser, D. W. Loe, C. E. Grant, G. M. Wilson, and R. G. Deeley: Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 54, 5902-5910 (1994)

  • [26]Hipfner, D., R. G. Deeley and C. Cole: Structural, mechanistic and clinical aspects of MRP1. Biochim Biophys Acta 1461, 359–376 (1999)

  • [27]Hooijberg, J. H., H. J. Broxterman, M. Kool, Y. G. Assaraf, G. J. Peters, P. Noordhuis, R. J. Scheper, P. Borst, H. M. Pinedo, and G. Jansen: Antifolate resistance mediated by the multidrug resistance proteins MRP1and MRP2. Cancer Res 59, 2532–2535 (1999)

  • [28]Breuninger, L. M., S. Paul, K. Gaughan, T. Miki, A. Chan, S. A. Aaronson, and G. D. Kruh: Expression of multidrug resistance associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res 55, 5342–5347 (1995)

  • [29]Konig, J., A. T. Nies, Y. Cui, I. Leier, and D. Keppler: Conjugate export pumps of the multi drug resistance protein (MRP) family: localization, substrate specificity, and MRP2-me-diated drug resistance. Biochim Biophys Acta 1461, 377–394. (1999)

  • [30]Oude Elferink, R. P., D. K. Meijer, F. Kuipers, P. L. Jansen, A. K. Groen, and G. M. Groothuis: Hepatobiliary secretion of organic compounds; molecular mechanisms of membrane transport. Biochim Biophys Acta 1241, 215–268 (1995)

  • [31]Mayer, R., J. Kartenbeck, M. Büchler, G. Jedlitschky, I. Leier, and D. Keppler: Expression of the MRP gene-encoded conjugate export pump in liver and its selective absence from the canalicular membrane in transport-deficient mutant hepatocytes. J Cell Biol 131, 137-150 (1995)

  • [32]Borst, P., R. Evers, M. Kool, and J. Wijnholds: A family of drug transporters: the multi drug resistance-associated proteins. J Natl Cancer Inst 92, 1295–1302 (2000)

  • [33]Hirohashi, T., H. Suzuki, H. Takikawa, and Y. Sugiyama: ATP-dependent transport of bile salts by multidrug resistance-associated protein 3 (Mrp3). J Biol Chem 275, 2905-2910 (2000)

  • [34]Zeng, H., G. Liu, P. A. Rea, and G. Kruh: Transport of amphipathic anions by human multidrug resistance protein 3. Cancer Res 60, 4779–4784 (2000)

  • [35]Zelcer, N., T. Saeki, G. Reid, J. H. Beijnen, and P. Borst: Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J Biol Chem 276, 46400–46407 (2001)

  • [36]Lee, K., M. G. Belinsky, D. W. Bell, J. R. Testa, and G. D. Kruh: Isolation of MOAT-B, a widely expressed multidrug resistance-associated protein/canalicular multispecific organic anion transporter-related transporter. Cancer Res 58, 2741–2747 (1998)

  • [37]Schuetz, J. D., M. C. Connelly, D. Sun, S. G. Paibir, P. M. Flynn, R. V. Srinivas, A. Kumar, and A. Fridland: MRP4: A previously unidentified factor in resistance to nucleotide-based antiviral drugs. Nat Med 5, 1048–1051 (1999)

  • [38]Chen, Z. S., K. Lee, and G. D. Kruh: Transport of cyclic nucleotides and estradiol 17-beta-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J Biol Chem 276, 33747–33754 (2001)

  • [39]McAleer, M. A., M. A. Breen, N. L. White, and N. Matthews: pABC11 (also known as MOAT-C and MRP5), a member of the ABC family of proteins, has anion transporter activity but does not confer multidrug resistance when overexpressed in human embryonic kidney 293 cells. J Biol Chem 274, 23541–23548 (1999)

  • [40]Wijnholds, J., C. A. Mol, L. vanDeemter, M. de Haas, G. L. Scheffer, F. Baas, J. H. Beijnen, R. J. Scheper, S. Hatse, E. de Clercq, J. Balzarini, and P. Borst: Multidrug-resistance protein 5 is a multispecific organic anion transporterable to transport nucleotide analogs. Proc Natl Acad Sci USA 97, 7476-7481 (2000)

  • [41]Bronchud, M. H., M. Foote, G. Giaccone, O. I. Olopade and P. Workman: Principles of Molecular Oncology. Springer Press (2008)

  • [42]Biedler, J. L., and H. Riehm: Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radio autographic,and cytogenetic studies. Cancer Res 30, 1174-1184 (1970)

  • [43]Paulsen, I. T., M. H. Brown, and R. A. Skurray: Proton-dependent multi-drug efflux systems. Microbiol Rev 60, 575-608 (1996)

  • [44]Barrasa, M. I., J. A. Tercero, R. A. Lacalle, and A. Jimenez: The ard1 gene from Streptomyces capreolus encodes a polypeptide of the ABC- transporters superfamily which confers resistance to the aminonucleoside antibiotic A201A. Eur J Biochem 228, 562-569 (1995)

  • [45]Linton, K. J., H. N. Cooper, I. S. Hunter, and P. F. Leadlay: An ABC-transporter from Streptomyces longisporoflavus confers resistance to the polyether-ionophore antibiotic tetronasin. Mol Microbiol 11, 777-785 (1994)

  • [46]Bolhuis, H., D. Molenaar, G. Poelarends, H. W. van Veen, B. Poolman, A. J. Driessen, and W. N. Konings: Proton motive force-driven and ATP-dependent drug extrusion systems in multidrug-resistant Lactococcus lactis. J Bacteriol 176, 6957-696 (1994)

  • [47]Young, J., and I. B. Holland: ABC transporters: bacterial exporters revisited five years on. Biochim Biophys Acta 1461, 177-200 (1999)

  • [48]Higgins, C. F.: ABC transporters from microorganisms to man. Annu Rev Cell Biol 8, 67-113 (1992)

  • [49]McGrath, J. P., and A. Varshavsky: The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nat Rev Microbiol, 340, 400-404 (1989)

  • [50]Bissinger, P. H., and K. Kuchler: Molecular cloning and expression of the Saccharomyce scerevisiae STS1 gene product: A yeast ABC transporter conferring mycotoxin resistance. J Biol Chem 269, 4180-4186 (1994)

  • [51]Wood, V., R. Gwilliam, M. A. Rajandream, M. A et al.: The genome sequence of Schizosaccharomyces pombe. Nature 415, 871-880 (2002)

  • [52]Nishi, K., M. Yoshida, M. Nishimura, M. Nishikawa, M. Nishiyama, S Horinouchi, and T Beppu: A leptomycin B resistance gene of Schizosaccharomyces pombe encodes a protein similar to the mammalian P-glycoproteins. Mol Microbiol 6, 761-769 (1992)

  • [53]Nagao, K., Y. Taguchi, M. Arioka, H. Kadukura, A. Takatsuki, K. Yoda, and M Yamasaki: bfr1+, a novel gene of Schizosaccharomyces pombe which confers brefeldin A resistance, is structurally related to the ATP-binding cassette super family. J Bacteriol 177, 1536-1543 (1995)

  • [54]Sanglard, D., and F. C. Odds: Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect Dis, 2, 73-85 (2002)

  • [55]Prasad, R., P. De Wergifosse, A. Goffeau, and E. Balzi: Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr Genet 27, 320-329 (1995)

  • [56]Olliaro, P., J. Cattani, and D. Wirth: Malaria, the submerged disease. J Am Med Assoc 275, 230-233 (1996)

  • [57]Foote, S. J., J. K. Thompson, A. F. Cowman, and D. Kemp: Amplification of the multidrug resistance gene in some chloroquine resistant isolates of Plasmodium falciparum. Cell 57, 921-930 (1989)

  • [58]Wilson, C. M., A. E. Serrano, A. Wasley, M. P. Bogenschutz, A. H. Shankar, and D. F. Wirth: Amplification of a gene related to mammalian mdr genes in drug resistant Plasmodium falciparum. Science 244, 1184-1186 (1989)

  • [59]Cowman, A. F., S. Karcz, D. Galatis, and J. G. Culvenor: A P-glycoprotein homologue of Plasmodium falciparum is localized on the digestive vacuole. J Cell Biol 113, 1033-1042 (1991)

  • [60]Reed, M. B., K.J. Salba, S. R. Caruana, K. Kirk, and A. F. Cowman: Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 403, 906-909 (2000)

  • [61]Hirst, S. I., and L. A. Stapley: Parasitology: the dawn of a new millennium. Parasitol Today 16, 1-3 (2000)

  • [62]Marsella, R., and R. Ruiz de Gopegui: Leishmaniasis: a re-emerging zoonosis. Intern J Dermatol, 37, 801-814 (1998)

  • [63]Faraut-Gambarelli, F., R. Piarroux, M. Deniau, B. Giusiano, P. Marty, G. Michel, B. Faugère, and H Dumon: In vitro and in vivo resistance of Leishmania infantum to meglumine antimoniate: a study of 37 strains collected from patients with visceral leishmaniasis. Antimicrob Agents Chemother 41, 827-83 (1997)

  • [64]Légaré, D., S. Cayer, A. K. Singh, D. Richard, B. Papadopoulou, and M. Ouellette: ABC proteins of Leishmania. J Bioenerg Biomembr 33, 469-474 (2001)

  • [65]Ouellette, M., A. Haimeur, K. Grondin, D. Légaré, and B. Papadopoulou: Amplification of ABC transporter gene pgpA and of other heavy metal resistance genes in Leishmania tarentolae and their study by gene transfection and gene disruption. Methods Enzymol 292, 182-193 (1998)

  • [66]Callahan, H. L., and S. M. Beverley: Heavy metal resistance: a new role for P-glycoproteins in Leishmania. J Biol Chem, 266, 18427-18430 (1991)

  • [67]Henderson, D. M., C. D. Sifri, M. Rodgers, D. F. Wirth, N. Hendrickson, and B. Ullman: Multidrug resistance in Leishmania donovani is conferred by amplification of a gene homologous to the mammalian mdr1 gene. Mol Cell Biol 12, 2855-2865 (1992)

  • [68]Cedeño, J. R, D. J. Krogstad: Susceptibility testing of Entamoeba histolytica. J Infect Dis 148, 1090-1095 (1983)

  • [69]Samarawickrema, N. A., D. M. Brown, J. A. Upcroft, N. Thammapalerd, and P. Upcroft: Involvement of superoxide dismutase and pyruvate: ferredoxin oxidoreductase in mechanisms of metronidazole resistance in Entamoeba histolytica. J Antimicrob Chemother 40, 833-840 (1997)

  • [70]Samuelson, J., P. Ayala, E. Orozco, and D. Whirth: Emetine-resistant mutants of Entamoeba histolytica overexpress mRNAs for multidrug resistance. Mol Biochem Parasitol 38, 281-290 (1990)

  • [71]Borst, P., M. Oualette: New mechanisms of drug resistance in parasitic protozoa. Annu Rev Microbiol, 49, 427-260 (1995)

  • [72]Barrasa, M. I., J. A. Tercero, R. A. Lacalle, and A. Jimenez: The ard1 gene from Streptomyces capreolus encodes a polypeptide of the ABC- transporters superfamily which confers resistance to the amino- nucleoside antibiotic A201A. Eur J Biochem 228 562-569 (1995)

  • [73]Linton, K. J., H. N. Cooper, I. S. Hunter, and P. F.Leadlay: An ABC-transporter from Streptomyces longisporoflavus confers resistance to the polyether-ionophore antibiotic tetronasin. Mol Microbiol, 11, 777-785 (1994)

  • [74]Guilfoile, P. G., and C. R. Hutchinson: A bacterial analog of the mdr gene of mammalian tumor cells is present in Streptomyces peucetius,the producer of daunorubicin and doxorubicin. Natl Acad Sci USA 88, 8553-8557 (1991)

  • [75]Ross, J. I., E. A. Eady, J. H. Cove, W. J. Cunliffe, S. Baumberg, and J. C. Wooton: Inducible erythromycin resistance in Staphylococci is encoded by a member of ATP-binding transporter super-gene family. Mol Microbiol 4, 1207-1214 (1990)

  • [76]Poelarends, G. J., P. Mazurkiewicz, and W. N. Konings: Multidrug transporters and antibiotic resistance in Lactococcus lactis. Biochim Biophys Acta 1555, 1-7 (2002)

  • [77]Simpson, W. J., and A. R. Smith: Factors affecting antibacterial activity of hop compounds and their derivatives. J Appl Bacteriol 72, 327-334 (1992)

  • [78]Miyauchi, S., M. Komatsubara, M., and N. Kamo: In archaebacteria, there is a doxorubicin efflux pump similar to mammalian P-glycoprotein. Biochim Biophys Acta 1110, 144 -150 (1992)

  • [79]Kaidoh, K., S. Miyauchi, A. Abe, S. Tanabu, T. Nara, N. Kamo: Rhodamine123 efflux transporter in Haloferax volcanii is induced when cultured under‘metabolic stress’ by amino acids: the efflux system resembles that in a doxorubicin-resistant mutant. Biochem J 314, 355-359 (1996)

  • [80]Bissinger, P. H., and K. Kuchler: Molecular cloning and expression of the Saccharomyce scerevisiae STS1 gene product: A yeast ABC transporter conferring mycotoxin resistance. J Biol Chem 269, 4180-4186 (1994)

  • [81]Kolaczkowski, M., M. van der Rest, A. Cybularz-Kolaczkowska, J. P. Soumillion, W. N. Konings, and A. Goffeau: Anticancer drugs,ionophoric peptides, and steroids as substrates of the yeast multidrug transporter Pdr5p. J Biol Chem 271, 31543-31548 (1996)

  • [82]Sanglard, D., F. C. Odds: Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect Dis 2, 73-85 (2002)

  • [83]Shukla, S., P. Saini, Smriti, S. Jha, S. V. Ambudkar, R. Prasad R: Functional characterization of Candida albicans ABC transporter Cdr1p. Eukaryot Cell. 2(6), 1361-1375 (2003)

  • [84]Jha, S., N. Dabas, N. Karnani, P. Saini, R. Prasad: ABC multidrug transporter Cdr1p of Candida albicans has divergent nucleotide-binding domains which display functional asymmetry. FEMS Yeast Res. 5(1), 63-72 (2004)

  • [85]Sarah, T., F. Rahkhoodaee , M. Raymond: Relative Contributions of the Candida albicansABC Transporters Cdr1p and Cdr2p to Clinical Azole Resistance. Antimicrob. Agents Chemother 53(4), 1344-1352 (2009)

  • [86]Szczepaniak, J., M. Łukaszewicz, A. Krasowska: Estimation of Candida albicans ABC transporter behavior in real-time via fluorescence. Front. Microbiol. 6:1382 (2015)

  • [87]Légaré, D., S. Cayer, A. K. Singh, D. Richard, B. Papadopoulou, and M. Ouellette: ABC proteins of Leishmania. J Bioenerg Biomembr, 33, 469-474 (2001)

  • [88]Perez-Victoria, J. M., A. Parodi-Talice, C. Torres, F. Gamarro, S. Castanys: ABC transporters in the protozoan parasite Leishmania. Int Microbiol 4, 159-166 (2001)

  • [89]Haimeur, A., M. Ouellette: Gene Amplification in Leishmania tarentolae selected for resistance to sodium stibogluconate. Antimicrob Agents Chemother 42(7), 1689-1694 (1998)

  • [90]Baldwin, S. A.: Mammalian passive glucose transporters: members of a ubiquitous family of active and passive transport proteins. Biochim Biophys Acta 1154(1), 17-49 (1993)

  • [91]Saier, M. H. Jr., J. T. Beatty, A. Goffeau, K. T. Harley, W. H. M. Heijne, S-C. Huang, D. L. Jack, P. S. Jähn, K. Lew, J. Liu, S. S. Pao, I. T. Paulsen, T-T. Tseng, and P. S. Virk: The major facilitator superfamily. J Mol Microbiol Biotechnol 1(2), 257-279 (1999)

  • [92]Pao, S. S., I. T. Paulsen, and M. H. Jr. Saier: Major facilitator superfamily. Microbiol Mol Biol Rev 62(1), 1-34 (1998)

  • [93]Goswitz, V. C., and R. J.Brooker: Structural features of the uniporter/symporter/antiporter superfamily. Protein Sci 4(3), 534-537 (1995)

  • [94]Reddy, V. S., M. A. Shlykov, R. Castillo, E. I. Sun, and M. H. Jr. Saier.: The major facilitator superfamily (MFS) revisited. FEBS J 279(11), 2022–2035 (2012)

  • [95]Henderson, P. J., and M. C.Maiden: Homologous sugar transport proteins in Escherichia coli and their relatives in both prokaryotes and eukaryotes. Philos Trans Roy Soc Lond B Biol Sci 326(1236), 391-410 (1990)

  • [96]Griffith, J. K., M. E. Baker, D. A. Rouch, M. G. Page, R. A. Skurray, I. T. Paulsen, K. F. Chater, S. A. Baldwin, and P. J. Henderson: Membrane transport proteins: implications of sequence comparisons. Curr Opin Cell Biol 4(4), 684-695 (1992)

  • [97]Maiden, M. C., M. C. Jones-Mortimer, and P. J. Henderson: The cloning, DNA sequence, and overexpression of the gene araE coding for arabinose-proton symport in Escherichia coli K12. J BiolChem 263(17), 8003-8010 (1988)

  • [98]Martinez, J., S. Steenbergen, and E. Vimr: Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain. J Bacteriol 177(20), 6005-6010 (1995)

  • [99]Tamai, I., H. Takanaga, H. Maeda, Y. Sai, T. Ogihara, T. Higashida, and A. Tsuji: Participation of a proton-cotransporter, MCT1, in the intestinal transport of monocarboxylic acids. Biochem Biophys Res Commun 214(2), 482-489 (1995)

  • [100]Garcia, C. K., J. L. Goldstein, R. K. Pathak, R. G. Anderson, and M. S. Brown: Molecular characterization of a membrane transporter for lactate, pyruvate, and other monocarboxylates: implications for the Cori cycle. Cell 76(5), 865-873 (1994)

  • [101]Goffeau, A., J. Park, I. T. Paulsen, K. L. Jonniaux, T. Dinh, P. Mordant, and M. H. Jr. Saier: Multidrug resistant transport proteins in yeast: complete inventory and phylogenetic characterization of yeast open reading frames within the major facilitator superfamily. Yeast 13(1), 43-54 (1997)

  • [102]Sung, Y. C., and J. A. Fuchs: Characterization of the cyn operon in Escherichia coli K12. J Biol Chem 263(29), 14769-14775 (1988)

  • [103]Chung, Y. K., and M. H. Jr. Saier: SMR-type multidrug resistance pumps. Curr Opin Drug Discov Devel 4(2), 237-245 (2001)

  • [104]Yerushalmi, H., M. Lebendiker, and S. Schuldiner: Negative dominance studies demonstrate the oligomeric structure of EmrE, a multidrug antiporter from Escherichia coli. J Biol Chem 271(49), 31044-31048 (1996)

  • [105]Morita, Y., K. Kodama, S. Shiota, T. Mine, A. Kataoka, T. Mizushima, T. Tsuchiya: NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Chemother 42(7), 1778-1782 (1998)

  • [106]Begum, A., M. M. Rahman, W. Ogawa, T. Mizushima, T. Kuroda, and T. Tsuchiya: Gene cloning and characterization of four MATE family multidrug efflux pumps from Vibrio cholerae NonO1. Microbiol Immunol 49(11), 949-957 (2005)

  • [107]Huda, M., J. Chen, Y. Morita, T. Kuroda, T. Mizushima, and T. Tsuchiya: Gene cloning and characterization of VcrM, a Na+ -coupled multidrug efflux pump, from Vibrio cholerae NonO1. Microbiol Immunol 47(6), 419-427 (2003)

  • [108]McAleese, F., P. Petersen, A. Ruzin, P. M. Dunman, E. Murphy, S. J. Projan, and P. A Bradford: A novel MATE family efflux pump contributes to the reduced susceptibility of laboratory-derived Staphylococcus aureus mutants to tigecycline. Antimicrob Agents Chemother 49(5), 1865-1871 (2005)

  • [109]Otsuka, M., M. Yasuda, Y. Morita, C. Otsuka, T. Tsuchiya, H. Omote, Y. Moriyama: Identification of essential amino acid residues of the NorM Na+/multidrug antiporter in Vibrio parahaemolyticus. J Bacteriol 187(5), 1552-1558 (2005)

  • [110]Shiomi, N., H. Fukuda, Y. Fukuda, K. Murata, and A. Kimura: Nucleotide sequence and characterization of a gene conferring resistance to ethionine in yeast Saccharomyces cerevisiae. J Ferment Bioeng, 71(4), 211-215 (1991)

  • [111]He, G.-X., T. Kuroda, T, Mima, Y, Morita, T. Mizushima, and T. Tsuchiya: An H+-coupled multidrug efflux pump, PmpM, a member of the MATE family of transporters, from Pseudomonas aeruginosa. J Bacteriol 186, 262–265 (2004)

  • [112]Xu, X. J., X. Z. Su, Y. Morita, T, Kuroda, T. Muzushima, and T. Tsuchiya: Molecular cloning and characterization of the HmrM multidrug efflux pump from Haemophilus influenzae. J Microbiol Immunol 47, 937–943 (2003)

  • [113]Braibant, M., L. Guilloteau, and M. S. Zygmunt: Functional characterization of Brucella melitensis NorMI, an efflux pump belonging to the multidrug and toxic compound extrusion family. J Antimicrob Agents Chemother 46, 3050–3053 (2002)

  • [114]Kaatz, G. W., F. McAleese, and S. M. Seo: Multidrug resistance in Staphylococcus aureus due to overexpression of a novel multidrug and toxin extrusion (MATE) transport protein. J Antimicrob Agents Chemother 49, 1857–1864 (2005)

  • [115]McAleese, F., P. Petersen, A. Ruzin, P. M. Dunman, E. Murphy, S. J. Projan, and P. A Bradford: A novel MATE family efflux pump contributes to the reduced susceptibility of laboratory-derived Staphylococcus aureus mutants to tigecycline. Antimicrob Agents Chemother 49, 1865–1871 (2005)

  • [116]Su, X.-Z., J Chen, T, Mizushima, T. Kuroda, and T, Tsuchiya: AbeM, an H+ coupled Acinetobacter baumannii multidrug efflux pump belonging to the MATE family of transporters. J Antimicrob Agents Chemother 49, 4362–4364 (2005)

  • [117]Dridi, L., J. Tankovic, and J. C. Petit: CdeA of Clostridium difficile, a new multidrug efflux transporter of the MATE family. Microb Drug Resist 10, 191–196 (2004)

  • [118]Begum, A., M. M. Rahman, W. Ogawa, T. Mizushima, T. Kuroda, and T. Tsuchiya: Gene cloning and characterization of four MATE family multidrug efflux pumps from Vibrio cholerae. J Microbiol Immunol 49, 949–957 (2005)

  • [119]Miyamae, S., O. Ueda, F. Yoshimura, J. Hwang, Y. Tanaka, and H. Nikaido: A MATE family multidrug effluxtransporter pumps out fluoroquinolones in Bacteroides thetaiotaomicron. J Antimicrob Chemother 45, 3341–3346 (2001)

  • [120]Shiomi, N., H. Fukuda, Y. Fukuda, K. Murata, and A. Kimura: Nucleotide sequence and characterization of a gene conferring resistance to ethionine in yeast Saccharomyces cerevisiae. J Ferment.Bioeng 71(4), 211–215 (1991)

  • [121]Burse, A., H, Weingart, and M. S. Ulrich: NorM, an Erwinia amylovora multidrug efflux pump involved in invitro competition with other epiphytic bacteria. Appl Environ Microbiol 70, 693–703 (2004)

  • [122]Schulz, G. E.,: Bacterial porins: structure and function. Curr Opin Cell Biol 5(4), 701-707 (1993)

  • [123]Plésiat, P., and H. Nikaido: Outer membranes of Gram-negative bacteria are permeable to steroid probes. Mol Microbiol 6(10), 1323-1333 (1992)

  • [124]Ma, D., D. N. Cook, M. Alberti, N. G. Pon, H. Nikaido, H., and J. E. Hearst: Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J Bacteriol 175(19), 6299-6313 (1993)

  • [125]Tseng, T.-T., K. S. Gratwick, J. Kollman, D. Park, D. H. Nies, A. Goffeau, and M. H. Jr. Saier: The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol 1(1), 107-125 (1999)

  • [126]Zgurskaya, H. I., and H. Nikaido: Multidrug resistance mechanisms: drug efflux across two membranes. Mol Microbiol 37(2), 219-225 (2000)

  • [127]Poole, K.: Multidrug resistance in Gram-negative bacteria. Curr Opin Microbiol 4(5), 500-508 (2001)

  • [128]Elkins, C., H. Nikaido: Substrate specificity of the RND type multidrug efflux pumps AcrB and AcrD of Escherichia coli is determined predominately by two large periplasmic loops. J Bacteriol 148, 6490–6498 (2002)

  • [129]Pos, K. M.: Drug transport mechanism of the AcrB efflux pump. Biochim Biophy Acta 1794, 782–793 (2009)

  • [130]Köhler, T., C. van Delden, L. K. Curty, M. M. Hamzehpour, and J. C. Pechere: Overexpression of the MexEF-OprN multidrug efflux system affects cell to cell signaling in Pseudomonas aeroginosa. J Bacteriol 183, 5213-5222 (2001)

  • [131]Westbrock-Wadman, S., D. R. Sherman, M. J. Hickey, S. N. Coulter, Y. Q. Zhu, P. Warrener, L. Y. Nguyen, R. M. Shawar, K. R. Folger and C. K. Stover: Characterization of Pseudomonas aeroginosa efflux pump contributing to aminoglycoside resistance. Antimicrob Agents Chemother 43, 2975-2983 (1999)

  • [132]Govan, J. R., V. Deretic: Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Mol Biol Rev, 60(3), 539-574 (1996)

  • [133]Moore, R. A., S. Reckseidler-Zenteno, H. Kim, W. Nierman, Y. Yu, A. Tuanyok, J. Warawa, D. DeShazer, and D. E. Woods: Contribution of gene loss to the pathogenic evolution of Burkholderia pseudomallei and Burkholderia mallei. Infect Immun 72(7), 4172-4187 (2004)

  • [134]Quinn, J.: Clinical problems posed by multiresistant nonfermenting Gram-negative pathogens. Clin Infect Dis 27 Suppl 1, S117-124 (1998)

  • [135]Lomovskaya, O., M. S. Warren, A. Lee, J. Galazzo, R. Fronko, M. Lee, J. Blais, D. Cho, S. Chamberland, T. Renau, R. Leger, S. Hecker, W. Watkins, K, Hoshino, H. Ishida, and V. J. Lee: Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob Agents Chemother 45(1), 105-116 (2001)

  • [136]Ayaz, M., F. Subhan, J. Ahmed, A-U. Khan, F. Ullah, A. Sadiq, N-I-H. Syed, I. Ullah, and S. Hussain: Citalopram and venlafaxine differentially augments antimicrobial properties of antibiotics. Acta Polon Pharmac Drug Res 72(6), 1269-1278 (2015)

  • [137]Ayaz, M., F. Subhan, J. Ahmed, A. U. Khan, F. Ullah, I. Ullah, G. Ali, N. I. Syed and S. Hussain: Sertraline enhances the activity of antimicrobial agents against pathogens of clinical relevance. J Biol Res (Thessalon) 22(1), 4 (2015)

  • [138]Kamal, Z. Midrarullah, S. Ahmad, F. Ullah, A. Sadiq, M. Ayaz, A. Zeb, and M. Imran: Ex-vivo antibacterial, phytotoxic and cytotoxic, potential in the crude natural phytoconstituents of Rumex hastatus d. Don. Pak J Bot 47(SI), 293-299 (2015)

  • [139]Shah, S. M., M. Ayaz, A-U. Khan, F. Ullah, Farhan, A. U. Shah, H. Iqbal and S. Hussain: 1,1-Diphenyl,2-picrylhydrazyl free radical scavenging, bactericidal, fungicidal and leishmanicidal properties of Teucrium stocksianum. Toxicol Indu Health 31(11), 1037–1043 (2015)

  • [140]Neyfakh, A. A., V. E. Bidnenko, L. B. Chen: Efflux-mediated multi-drug resistance in Bacillus subtilis: similarities and dissimilarities with the mammalian system. Proc Natl Acad Sci USA 88(11), 4781–4785 (1991)

  • [141]Klyachko, K. A., S. Schuldiner, Neyfakh, A. A: Mutations affecting substrate specificity of the Bacillus subtilis multidrug transporter Bmr. J Bacteriol 179(7), 2189–2193 (1997)

  • [142]Brenwald, N. P., M. J. Gill, Wise, R: The effect of reserpine, an inhibitor of multi-drug efflux pumps, on the in-vitro susceptibilities of fluoroquinolone-resistant strains of Streptococcus pneumoniae to norfloxacin. J Antimicrob Chemother 40(3), 458–460 (1997)

  • [143]Markham, P. N: Inhibition of the emergence of ciprofloxacin resistance in Streptococcus pneumoniae by the multidrug efflux inhibitor reserpine. Antimicrob Agents Chemother, 43(4), 988–989 (1999)

  • [144]Schmitz, F. J., A. C. Fluit., M. Luckefahr., B. Engler., B. Hofmann., J. Verhoef., H. P Heinz., U. Hadding., M. E. Jones: The effect of reserpine, an inhibitor of multidrug efflux pumps, on the in-vitro activities of ciprofloxacin, sparfloxacin and moxifloxacin against clinical isolates of Staphylococcus aureus. J Antimicrob Chemother 42(6), 807–810 (1998)

  • [145]Gibbons, S., E. E. Udo: The effect of reserpine, a modulator of multidrug efflux pumps, on the in vitro activity of tetracycline against clinical isolates of methicillin resistant Staphylococcus aureus (MRSA) possessing the tet(K) determinant. Phytother Res 14(2), 139–140 (2000)

  • [146]Hamilton-Miller, J. M. T., S. Shah: Activity of the tea component epicatechin gallate and analogues against methicillin resistant Staphylococcus aureus. J Antimicrob Chemother 46(5), 852–853 (2000)

  • [147]Roccaro, A. S., A. R. Blanco., F. Giuliano., D. Rusciano., V. Enea: Epigallocatechin-gallate enhances the activity of tetracycline in staphylococci by inhibiting its efflux from bacterial cells. Antimicrob Agents Chemother 48(6), 1968–1973 (2004)

  • [148]Gibbons S, Moser E, Kaatz GW. Catechin gallates inhibit multidrug resistance (MDR) in Staphylococcus aureus. Planta Med 70, 1240–1242 (2004)

  • [149]Oluwatuyi, M., G. W. Kaatz., S. Gibbons: Antibacterial and resistance modifying activity of Rosmarinus officinalis. Phytochemistry 65(24) 3249–3254 (2004)

  • [150]Gibbons, S., M. Oluwatuyi, N. C Veitch, A. I. Gray: Bacterial resistance modifying agents from Lycopus europaeus. Phytochemistry 62(1) 83–87 (2003)

  • [151]Stermitz, F.R., P. Lorenz, J. N. Tawara, L. A. Zenewicz, K. Lewis: Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 5′-methoxyhydnocarpin, a multidrug pump inhibitor. Proc Natl Acad Sci USA 97(4), 1433–1437 (2000)

  • [152]Stermitz, F. R., L. N. Scriven, G. Tegos, K, Lewis: Two flavonols from Artemisia annua which potentiate the activity of berberine and norfloxacin against a resistant strain of Staphylococcus aureus. Planta Med 68, 1140–1 (2002)

  • [153]Morel, C., F. R. Stermitz, G. Tegos, G, K. Lewis: Isoflavones as potentiators of antibacterial activity. J Agric Food Chem 51, 5677–5679 (2003)

  • [154]Kourtesi, C., Ball, A. R, Huang, Y. M. S. Jachak, D. M. A. Vera, P. Khondkar, S. Gibbons, M. R. Hamblin, G. P. Tegos: Microbial efflux systems and inhibitors: Approaches to drug discovery and the challenge of clinical implementation. The Open Microbiol J 7(Suppl 1 -M 3) 34-52 (2013)

  • [155]Liu, K. C. S., S. L.Yang, M. F. Roberts, B. C. Elford, J. D. Phillipson: Antimalarial activity of Artemisia annua flavonoids from whole plants and cell cultures. Plant Cell Rep 11(12), 637–40 (1992)

  • [156]Belofsky, G., D. Percivill, K. Lewis, G. P. Tegos, and J. Ekart: Phenolic metabolites of Dalea versicolor that enhance antibiotic activity against model pathogenic bacteria. J Nat Prod 67, 481-484 (2004)

  • [157]Belofsky, G., R. Carreno, K. Lewis, A. Ball, G. Casadei, and G. P. Tegos: Metabolites of the ‘smoke tree’, Dalea spinosa, potentiate antibiotic activity against multidrug-resistant Staphylococcus aureus. J Nat Prod 69, 261-264 (2006)

  • [158]Marquez, B., L. Neuville, N. J. Moreau, J. P. Genet, A. F. dos Santos, M. C. Caño de Andrade, and A. E. Sant’Ana: Multidrug resistance reversal agent from Jatropha elliptica. Phytochem 66, 1804–1811 (2005)

  • [159]Hohmann, J., J. Molnár, D. Rédei, F. Evanics, P. Forgo, A. Kálmán, G. Argay, and P. Szabó: Discovery and biological evaluation of a new family of potent modulators of multidrug resistance: reversal of multidrug resistance of mouse lymphoma cells by new natural jatrophane diterpenoids isolated from Euphorbia species. J Med Chem 45, 2425–2431 (2002)

  • [160]Hohmann, J., D. Rédei, P. Forgo, J. Molnár, G. Dombi, and T. Zorig: Jatrophane diterpenoids from Euphorbia mongolicas modulators of the multidrug resistance of L5128 mouse lymphoma cells. J Nat Prod 66, 976–979 (2003)

  • [161]Pereda-Miranda, R., G. W. Kaatz, and S. Gibbons: Polyacylated oligosaccharides from medicinal Mexican morning glory species as antibacterials and inhibitors of multidrug resistance in Staphylococcus aureus. J Nat Prod 69, 406–409 (2006)

  • [162]Oluwatuyi, M., G. W. Kaatz, and S. Gibbons: Antibacterial and resistance modifying activity of Rosmarinus officinalis. Phytochem 65, 3249–3254 (2004)

  • [163]Fujita, M., S. Shiota, T. Kuroda, T. Hatano, T. Yoshida, T. Mizushima, and T. Tsuchiya: Remarkable synergies between baicalein and tetracycline, and baicalein and beta-lactams against methicillin-resistant Staphylococcus aureus. Microbiol Immunol, 49, 391–396 (2005)

  • [164]Abulrob, A. N., M. T. Suller, M. Gumbleton, C. Simons, and A. D. Russell: Identification and biological evaluation of grapefruit oil components as potential novel efflux pump modulators in methicillin-resistant Staphylococcus aureus bacterial strains. Phytochem 65, 3021–3027 (2004)

  • [165]Khan, I. A., Z. M. Mirza, A. Kumar, V. Verma, and G. N. Qazi: Piperine, a phytochemical potentiator of ciprofloxacin against Staphylococcus aureus . Antimicrob Agents Chemother 50, 810–812 (2006)

  • [166]Ayaz, M., M. Junaid, F. Ullah, A. Sadiq, M. A. Khan, W. Ahmad, M. R. Shah, M. Imran, and S. Ahmad: Comparative chemical profiling, cholinesterase inhibitions and anti-radicals properties of essential oils from Polygonum hydropiper L: A Preliminary anti-Alzheimer’s study. Lipids Health Dis 14(1), 141 (2015)

  • [167]Ayaz, M., M. Junaid, F. Subhan, F. Ullah, A. Sadiq, S. Ahmad, M. Imran, Z. Kamal, S. Hussain, and S. M. Shah.: Heavy metals analysis, phytochemical, phytotoxic and anthelmintic investigations of crude methanolic extract, subsequent fractions and crude saponins from Polygonum hydropiper L. BMC Complement Altern Med 14, 465 (2014)

  • [168]Ayaz, M., M. Junaid, J. Ahmed, F. Ullah, A. Sadiq, S. Ahmad, and M. Imran: Phenolic contents, antioxidant and anticholinesterase potentials of crude extract, subsequent fractions and crude saponins from Polygonum hydropiper L. BMC Complement Altern Med 14-145 (2014)

  • [169]Ahmad, S., F. Ullah, A. Sadiq, M. Ayaz, M. Imran, I. Ali, A. Zeb, F. Ullah, and M. Shah: Chemical composition, antioxidant and anticholinesterase potentials of essential oil of Rumex hastatus D. Don collected from the North West of Pakistan. BMC Complement Altern Med 16, 29 (2016)

  • [170]Ayaz, M., M. Junaid, F. Ullah, A. Sadiq, F. Subhan, M. A. Khan,W. Ahmad, G. Ali, M. Imran, and S. Ahmad: Molecularly characterized solvent extracts and saponins from Polygonum hydropiper L. show high anti-angiogenic, anti-tumor, brine shrimp, and fibroblast NIH/3T3 cell line cytotoxicity. Front Pharmacol 7:74(2016)

  • [171]Ahmad, S., F. Ullah, M. Ayaz, A. Zeb, F. Ullah, and A. Sadiq: Antitumor and anti-angiogenic potentials of isolated crude saponins and various fractions of Rumex hastatus D. Don. Biol Res 49, 18 (2016)

  • [172]Zeb, A., A. Sadiq, F. Ullah, S. Ahmad, and M. Ayaz: Investigations of anticholinesterase and antioxidant potentials of methanolic extract, subsequent fractions, crude saponins and flavonoids isolated from Isodon rugosus. Biol Res 47, 76 (2014)

  • [173]Khan, S.U., A. U. Khan, A. U. Shah, S. M. Shah, S. Hussain, M. Ayaz, and S. Ayaz: Heavy metals content, phytochemical composition, antimicrobial and insecticidal evaluation of Elaeagnus angustifolia. Toxicol Ind Health 32(1), 154–161 (2016)

  • [174]Zeb, A., A. Sadiq, F. Ullah, S. Ahmad, and M. Ayaz, M.: Phytochemical and toxicological investigations of crude methanolic extracts, subsequent fractions and crude saponins of Isodon rugosus. Biol Res 47, 57 (2014)

  • [175]Teodori, E., S. Dei, C. Martelli, S. Scapecchi, and F. Gualtieri: The functions and structure of ABC transporters: implications for the design of new inhibitors of Pgp and MRP1 to control multidrug resistance (MDR). Curr Drug Targets 7, 893–909 (2006)

  • [176]Markham, P. N., A. A. Neyfakh: Inhibition of the multidrug transporter NorA prevents emergence of norfloxacin resistance in Staphylococcus aureus. Antimicrob Agents Chemother, 40(11), 2673-2674 (1996)

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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.

1 Jan 2017Review

Cellular efflux transporters and the potential role of natural products in combating efflux mediated drug resistance

Muhammad Ayaz 1,*, Fazal Subhan 2, Abdul Sadiq 1, Farhat Ullah 1, Jawad Ahmed 3, Robert D. E. Sewell 4
Affiliations
Article Info

1 Department of Pharmacy, University of Malakand, Khyber Pakhtunkhwa (KP) 18000, Pakistan

2 Department of Pharmacy, University of Peshawar, Peshawar, Pakistan

3 Institute of Basic Medical Sciences (IBMS), Khyber Medical University (KMU) Peshawar, Pakistan

4 Cardiff School of Pharmacy and Pharmaceutical Sciences, Cardiff University, Cardiff CF10 3NU, U.K

Abstract

Efflux mediated multidrug resistance (MDR) is a major problem in the treatment of bacterial, fungal and protozoal infections in addition to cancer chemotherapy. Among other well known mechanisms, efflux pumps are significant contributors to chemo-resistance. Efflux mediated resistance generally occurs through up-regulation of genes responsible for the expression of transporter proteins extruding drugs from the cell to create intracellular sub-therapeutic concentrations leading to resistance. The rapid expansion of MDR pathogens necessitates the discovery of resistance modifying drugs, which in combination with antimicrobial or chemotherapeutic agents would tend to reinstate the action of these drugs and avert the emergence of acquired resistance. This review describes the existence of efflux pumps in prokaryotes and eukaryotes as well as their role in chemo-resistance with a special focus on natural product-derived efflux pump inhibitors.

Keywords

  • Efflux Pumps
  • EPIs
  • Natural Products
  • Chemo-resistance
  • MDR
  • Infectious Diseases
  • Review

References