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Articles

Docking analysis insights quercetin can be a non-antibiotic adjuvant by inhibiting Mmr drug efflux pump in Mycobacterium sp. and its homologue EmrE in Escherichia coli

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Pages 1819-1834 | Received 11 Apr 2014, Accepted 05 Oct 2014, Published online: 05 Nov 2014

References

  • Abbas, Z., Blank, R., Wein, S., & Wolffram, S. (2013). Effect of quercetin on the toxicokinetics of ochratoxin A in rats. Food Additives & Contaminants: Part A, 30, 861–866. doi:10.1080/19440049.2013.79382310.1080/19440049.2013.793823
  • Aherne, S. A., & O’Brien, N. M. (2002). Dietary flavonols: Chemistry, food content, and metabolism. Nutrition, 18, 75–81.10.1016/S0899-9007(01)00695-5
  • Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.10.1093/nar/25.17.3389
  • Balganesh, M., Kuruppath, S., Marcel, N., Sharma, S., Nair, A., & Sharma, U. (2010). Rv1218c, an ABC transporter of Mycobacterium tuberculosis with implications in drug discovery. Antimicrobial Agents and Chemotherapy, 54, 5167–5172. doi:10.1128/aac.00610-1010.1128/AAC.00610-10
  • Bay, D. C., & Turner, R. J. (2012). Spectroscopic analysis of small multidrug resistance protein EmrE in the presence of various quaternary cation compounds. Biochimica et Biophysica Acta, 1818, 1318–1331. doi:10.1016/j.bbamem.2012.01.02210.1016/j.bbamem.2012.01.022
  • Berger, O., Edholm, O., & Jahnig, F. (1997). Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophysical Journal, 72, 2002–2013. doi:10.1016/s0006-3495(97)78845-310.1016/S0006-3495(97)78845-3
  • Bernal, P., Zloh, M., & Taylor, P. W. (2009). Disruption of D-alanyl esterification of Staphylococcus aureus cell wall teichoic acid by the β-lactam resistance modifier (-)-epicatechin gallate. Journal of Antimicrobial Chemotherapy, 63, 1156–1162. doi:10.1093/jac/dkp09410.1093/jac/dkp094
  • Bischoff, S. C. (2008). Quercetin: Potentials in the prevention and therapy of disease. Current Opinion in Clinical Nutrition and Metabolic Care, 11, 733–740. doi:10.1097/MCO.0b013e32831394b810.1097/MCO.0b013e32831394b8
  • Choudhuri, B. S., Bhakta, S., Barik, R., Basu, J., Kundu, M., & Chakrabarti, P. (2002). Overexpression and functional characterization of an ABC (ATP-binding cassette) transporter encoded by the genes drrA and drrB of Mycobacterium tuberculosis. Biochemical Journal, 367, 279–285. doi:10.1042/bj2002061510.1042/BJ20020615
  • De Rossi, E., Ainsa, J. A., & Riccardi, G. (2006). Role of mycobacterial efflux transporters in drug resistance: An unresolved question. FEMS Microbiology Reviews, 30, 36–52. doi:10.1111/j.1574-6976.2005.00002.x10.1111/fmr.2006.30.issue-1
  • De Rossi, E., Branzoni, M., Cantoni, R., Milano, A., Riccardi, G., & Ciferri, O. (1998). Mmr, a Mycobacterium tuberculosis gene conferring resistance to small cationic dyes and inhibitors. Journal of Bacteriology, 180, 6068–6071.
  • Farha, M. A., & Brown, E. D. (2013). Discovery of antibiotic adjuvants. Nature Biotechnology, 31, 120–122. doi:10.1038/nbt.250010.1038/nbt.2500
  • Fiser, A., Do, R. K., & Sali, A. (2000). Modeling of loops in protein structures. Protein Science, 9, 1753–1773. doi:10.1110/ps.9.9.175310.1110/(ISSN)1469-896X
  • Fiser, A., & Sali, A. (2003). ModLoop: Automated modeling of loops in protein structures. Bioinformatics, 19, 2500–2501.10.1093/bioinformatics/btg362
  • Fleishman, S. J., Harrington, S. E., Enosh, A., Halperin, D., Tate, C. G., & Ben-Tal, N. (2006). Quasi-symmetry in the cryo-EM Structure of EmrE provides the key to modeling its transmembrane domain. Journal of Molecular Biology, 364, 54–67. doi:10.1016/j.jmb.2006.08.07210.1016/j.jmb.2006.08.072
  • Glide, V. (2011). Schrodinger (Version 2.3). New York, NY: Schrodinger.
  • Gottschalk, K. E., Soskine, M., Schuldiner, S., & Kessler, H. (2004). A structural model of EmrE, a multi-drug transporter from Escherichia coli. Biophysical Journal, 86, 3335–3348. doi:10.1529/biophysj.103.03454610.1529/biophysj.103.034546
  • Hemaiswarya, S., Kruthiventi, A. K., & Doble, M. (2008). Synergism between natural products and antibiotics against infectious diseases. Phytomedicine, 15, 639–652. doi:10.1016/j.phymed.2008.06.00810.1016/j.phymed.2008.06.008
  • Horsburgh Jr., C. R., Haxaire-Theeuwes, M., Lienhardt, C., Wingfield, C., McNeeley, D., … Pyne-Mercier, L., Varaine, F. (2013). Compassionate use of and expanded access to new drugs for drug-resistant tuberculosis. The International Journal of Tuberculosis and Lung Disease, 17, 146–152. doi:10.5588/ijtld.12.001710.5588/ijtld.12.0017
  • Jack, D. L., Yang, N. M., & Saier Jr., M. H. (2001). The drug/metabolite transporter superfamily. European Journal of Biochemistry, 268, 3620–3639.10.1046/j.1432-1327.2001.02265.x
  • Jones, D. T. (1999). Protein secondary structure prediction based on position-specific scoring matrices. Journal of Molecular Biology, 292, 195–202. doi:10.1006/jmbi.1999.309110.1006/jmbi.1999.3091
  • Kaatz, G. W., Moudgal, V. V., Seo, S. M., & Kristiansen, J. E. (2003). Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 47, 719–726.10.1128/AAC.47.2.719-726.2003
  • Kalan, L., & Wright, G. D. (2011). Antibiotic adjuvants: Multicomponent anti-infective strategies. Expert Reviews in Molecular Medicine, 13, e5. doi:10.1017/s146239941000176610.1017/S1462399410001766
  • Kelly, G. S. (2011). Quercetin. Monograph. Alternative Medicine Review, 16, 172–194.
  • Koteiche, H. A., Reeves, M. D., & McHaourab, H. S. (2003). Structure of the substrate binding pocket of the multidrug transporter EmrE: Site-directed spin labeling of transmembrane segment 1. Biochemistry, 42, 6099–6105. doi:10.1021/bi034286710.1021/bi0342867
  • Krivov, G. G., Shapovalov, M. V., & Dunbrack Jr., R. L. (2009). Improved prediction of protein side-chain conformations with SCWRL4. Proteins: Structure, Function, and Bioinformatics, 77, 778–795. doi:10.1002/prot.2248810.1002/prot.v77:4
  • Krogh, A., Larsson, B., von Heijne, G., & Sonnhammer, E. L. (2001). Predicting transmembrane protein topology with a hidden markov model: Application to complete genomes. Journal of Molecular Biology, 305, 567–580. doi:10.1006/jmbi.2000.431510.1006/jmbi.2000.4315
  • Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., & Thornton, J. M. (1996). AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. Journal of Biomolecular NMR, 8, 477–486.
  • Lechner, D., Gibbons, S., & Bucar, F. (2008). Plant phenolic compounds as ethidium bromide efflux inhibitors in Mycobacterium smegmatis. Journal of Antimicrobial Chemotherapy, 62, 345–348. doi:10.1093/jac/dkn17810.1093/jac/dkn178
  • Li, M. H., Luo, Q., Xue, X. G., & Li, Z. S. (2011). Molecular dynamics studies of the 3D structure and planar ligand binding of a quadruplex dimer. Journal of Molecular Modeling, 17, 515–526. doi:10.1007/s00894-010-0746-010.1007/s00894-010-0746-0
  • Li, X. Z., & Nikaido, H. (2009). Efflux-mediated drug resistance in bacteria. Drugs, 69, 1555–1623. doi:10.2165/11317030-000000000-0000010.2165/11317030-000000000-00000
  • Li, X. Z., Poole, K., & Nikaido, H. (2003). Contributions of MexAB-OprM and an EmrE homolog to intrinsic resistance of Pseudomonas aeruginosa to aminoglycosides and dyes. Antimicrobial Agents and Chemotherapy, 47, 27–33.10.1128/AAC.47.1.27-33.2003
  • LigPrep (2011). Schrodinger (Version 2.3). New York, NY: Schrodinger.
  • Lin, R. D., Chin, Y. P., & Lee, M. H. (2005). Antimicrobial activity of antibiotics in combination with natural flavonoids against clinical extended-spectrum beta-lactamase (ESBL)-producing Klebsiella pneumoniae. Phytotherapy Research, 19, 612–617. doi:10.1002/ptr.169510.1002/(ISSN)1099-1573
  • Malkhed, V., Mustyala, K. K., Potlapally, S. R., & Vuruputuri, U. (2014). Identification of novel leads applying in silico studies for Mycobacterium multidrug resistant (MMR) protein. Journal of Biomolecular Structure & Dynamics, 32, 1889–1906. doi:10.1080/07391102.2013.842185
  • Mazumdar, K., Dastidar, S. G., Park, J. H., & Dutta, N. K. (2009). The anti-inflammatory non-antibiotic helper compound diclofenac: An antibacterial drug target. European Journal of Clinical Microbiology and Infectious Diseases, 28, 881–891. doi:10.1007/s10096-009-0739-z10.1007/s10096-009-0739-z
  • Middleton Jr., E., Kandaswami, C., & Theoharides, T. C. (2000). The effects of plant flavonoids on mammalian cells: Implications for inflammation, heart disease, and cancer. Pharmacological Reviews, 52, 673–751.
  • Moller, S., Croning, M. D., & Apweiler, R. (2001). Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics, 17, 646–653.10.1093/bioinformatics/17.7.646
  • Mordoch, S. S., Granot, D., Lebendiker, M., & Schuldiner, S. (1999). Scanning cysteine accessibility of EmrE, an H+-coupled multidrug transporter from Escherichia coli, reveals a hydrophobic pathway for solutes. Journal of Biological Chemistry, 274, 19480–19486.10.1074/jbc.274.27.19480
  • Muth, T. R., & Schuldiner, S. (2000). A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE. The EMBO Journal, 19, 234–240. doi:10.1093/emboj/19.2.23410.1093/emboj/19.2.234
  • Pao, S. S., Paulsen, I. T., & Saier Jr., M. H. (1998). Major facilitator superfamily. Microbiology and Molecular Biology Reviews, 62(1), 1–34.
  • Paulsen, I. T., Brown, M. H., Littlejohn, T. G., Mitchell, B. A., & Skurray, R. A. (1996). Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: Membrane topology and identification of residues involved in substrate specificity. Proceedings of the National Academy of Sciences, 93, 3630–3635.10.1073/pnas.93.8.3630
  • Paulsen, I. T., Skurray, R. A., Tam, R., Saier Jr., M. H., Turner, R. J., Weiner, J. H., … Grinius, L. L. (1996). The SMR family: A novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs. Molecular Microbiology, 19, 1167–1175.10.1111/mmi.1996.19.issue-6
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera?A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25, 1605–1612. doi:10.1002/jcc.2008410.1002/(ISSN)1096-987X
  • Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., … Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845–854. doi: 10.1093/bioinformatics/btt05510.1093/bioinformatics/btt055
  • Putman, M., van Veen, H. W., & Konings, W. N. (2000). Molecular properties of bacterial multidrug transporters. Microbiology and Molecular Biology Reviews, 64, 672–693.10.1128/MMBR.64.4.672-693.2000
  • Rodrigues, L., Villellas, C., Bailo, R., Viveiros, M., & Ainsa, J. A. (2013). Role of the Mmr Efflux pump in drug resistance in Mycobacterium tuberculosis. Antimicrobial Agents and Chemotherapy, 57, 751–757. doi:10.1128/aac.01482-1210.1128/AAC.01482-12
  • Santhosh, R. S., & Suriyanarayanan, B. (2014). Plants: a source for new antimycobacterial drugs. Planta Medica, 80, 9–21. doi:10.1055/s-0033-1350978
  • Schmitt, L., & Tampe, R. (2002). Structure and mechanism of ABC transporters. Current Opinion in Structural Biology, 12, 754–760.10.1016/S0959-440X(02)00399-8
  • Schuttelkopf, A. W., & van Aalten, D. M. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica. Section D, Biological Crystallography, 60, 1355–1363. doi:10.1107/s090744490401167910.1107/S0907444904011679
  • Shakya, T., Stogios, P. J., Waglechner, N., Evdokimova, E., Ejim, L., Blanchard, J. E., … Wright, G. D. (2011). A small molecule discrimination map of the antibiotic resistance kinome. Chemistry & Biology, 18, 1591–1601. doi:10.1016/j.chembiol.2011.10.018
  • Shapovalov, M. V., Wang, Q., Xu, Q., Andrake, M., & Dunbrack Jr., R. L. (2014). Bioassemblymodeler (BAM): User-friendly homology modeling of protein homo- and heterooligomers. PLoS ONE, 9, e98309. doi:10.1371/journal.pone.009830910.1371/journal.pone.0098309
  • Sharoni, M., Steiner-Mordoch, S., & Schuldiner, S. (2005). Exploring the binding domain of EmrE, the smallest multidrug transporter. Journal of Biological Chemistry, 280, 32849–32855. doi:10.1074/jbc.M50491020010.1074/jbc.M504910200
  • Shu, M., Lin, Z., Zhang, Y., Wu, Y., Mei, H., & Jiang, Y. (2011). Molecular dynamics simulation of oseltamivir resistance in neuraminidase of avian influenza H5N1 virus. Journal of Molecular Modeling, 17, 587–592. doi:10.1007/s00894-010-0757-x10.1007/s00894-010-0757-x
  • Sikora, C. W., & Turner, R. J. (2005). Investigation of ligand binding to the multidrug resistance protein EmrE by isothermal titration calorimetry. Biophysical Journal, 88, 475–482. doi:10.1529/biophysj.104.04924710.1529/biophysj.104.049247
  • Suriyanarayanan, B., Shanmugam, K., & Santhosh, R. S. (2013). Synthetic quercetin inhibits mycobacterial growth possibly by interacting with DNA gyrase. Romanian Biotechnological Letters, 18, 8587–8593.
  • Touze, T., Eswaran, J., Bokma, E., Koronakis, E., Hughes, C., & Koronakis, V. (2004). Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Molecular Microbiology, 53, 697–706. doi:10.1111/j.1365-2958.2004.04158.x10.1111/mmi.2004.53.issue-2
  • Tseng, T. T., Gratwick, K. S., Kollman, J., Park, D., Nies, D. H., Goffeau, A., & Saier Jr., M. H. (1999). The RND permease superfamily: An ancient, ubiquitous and diverse family that includes human disease and development proteins. Journal of Molecular Microbiology and Biotechnology, 1, 107–125.
  • Ubarretxena-Belandia, I., Baldwin, J. M., Schuldiner, S., & Tate, C. G. (2003). Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer. The EMBO Journal, 22, 6175–6181. doi:10.1093/emboj/cdg61110.1093/emboj/cdg611
  • Van Bambeke, F., Pages, J. M., & Lee, V. J. (2006). Inhibitors of bacterial efflux pumps as adjuvants in antibiotic treatments and diagnostic tools for detection of resistance by efflux. Recent Patents on Anti-Infective Drug Discovery, 1, 157–175.10.2174/157489106777452692
  • Wallner, B., & Elofsson, A. (2003). Can correct protein models be identified? Protein Science, 12, 1073–1086. doi:10.1110/ps.023680310.1110/(ISSN)1469-896X
  • Winstone, T. L., Jidenko, M., le Maire, M., Ebel, C., Duncalf, K. A., & Turner, R. J. (2005). Organic solvent extracted EmrE solubilized in dodecyl maltoside is monomeric and binds drug ligand. Biochemical and Biophysical Research Communications, 327, 437–445. doi:10.1016/j.bbrc.2004.11.16410.1016/j.bbrc.2004.11.164
  • Worthington, R. J., & Melander, C. (2013). Combination approaches to combat multidrug-resistant bacteria. Trends in Biotechnology, 31, 177–184. doi:10.1016/j.tibtech.2012.12.00610.1016/j.tibtech.2012.12.006
  • Xiang, Z. (2006). Advances in homology protein structure modeling. Current Protein and Peptide Science, 7, 217–227.10.2174/138920306777452312
  • van Zanden, J. J., Geraets, L., Wortelboer, H. M., van Bladeren, P. J., Rietjens, I. M., & Cnubben, N. H. (2004). Structural requirements for the flavonoid-mediated modulation of glutathione S-transferase P1-1 and GS-X pump activity in MCF7 breast cancer cells. Biochemical Pharmacology, 67, 1607–1617. doi:10.1016/j.bcp.2003.12.03210.1016/j.bcp.2003.12.032
  • Zhong, W., Gallivan, J. P., Zhang, Y., Li, L., Lester, H. A., & Dougherty, D. A. (1998). From ab initio quantum mechanics to molecular neurobiology: A cation-pi binding site in the nicotinic receptor. Proceedings of the National Academy of Sciences, 95, 12088–12093.10.1073/pnas.95.21.12088

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