An Update on Staphylococcus aureus NorA Efflux Pump Inhibitors

Author(s): Kadja Luana Chagas Monteiro, Thiago Mendonça de Aquino, Francisco Jaime B. Mendonça Junior*

Journal Name: Current Topics in Medicinal Chemistry

Volume 20 , Issue 24 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Background: Methicillin-resistant and vancomycin-resistant Staphylococcus aureus are pathogens causing severe infectious diseases that pose real public health threats problems worldwide. In S. aureus, the most efficient multidrug-resistant system is the NorA efflux pump. For this reason, it is critical to identify efflux pump inhibitors.

Objective: In this paper, we present an update of the new natural and synthetic compounds that act as modulators of antibiotic resistance through the inhibition of the S. aureus NorA efflux pump.

Results: Several classes of compounds capable of restoring the antibiotic activity have been identified against resistant-S. aureus strains, acting as NorA efflux pump inhibitors. The most promising classes of compounds were quinolines, indoles, pyridines, phenols, and sulfur-containing heterocycles. However, the substantial degree structural diversity of these compounds makes it difficult to establish good structure- activity correlations that allow the design of compounds with more promising activities and properties.

Conclusion: Despite substantial efforts put forth in the search for new antibiotic adjuvants that act as efflux pump inhibitors, and despite several promising results, there are currently no efflux pump inhibitors authorized for human or veterinary use, or in clinical trials. Unfortunately, it appears that infection control strategies have remained the same since the discovery of penicillin, and that most efforts remain focused on discovering new classes of antibiotics, rather than trying to prolong the life of available antibiotics, and simultaneously fighting mechanisms of bacterial resistance.

Keywords: Methicilin-resistant Staphylococcus aureus, Efflux pump inhibitors, NorA efflux pump, Antibacterial agents, Drug design, Multidrug resistance.

[1]
Brockhurst, M.A.; Harrison, F.; Veening, J.W.; Harrison, E.; Blackwell, G.; Iqbal, Z.; Maclean, C. Assessing evolutionary risks of resistance for new antimicrobial therapies. Nat. Ecol. Evol., 2019, 3(4), 515-517.
[http://dx.doi.org/10.1038/s41559-019-0854-x ] [PMID: 30886376]
[2]
Cattoir, V.; Felden, B. Future Antibacterial Strategies: From Basic Concepts to Clinical Challenges. J. Infect. Dis., 2019, 220(3), 350-360.
[http://dx.doi.org/10.1093/infdis/jiz134 ] [PMID: 30893436]
[3]
Pontes, D.S.; de Araujo, R.S.A.; Dantas, N.; Scotti, L.; Scotti, M.T.; de Moura, R.O.; Mendonça-Junior, F.J.B. Genetic mechanisms of antibiotic resistance and the role of antibiotic adjuvants. Curr. Top. Med. Chem., 2018, 18(1), 42-74.
[http://dx.doi.org/10.2174/1568026618666180206095224 ] [PMID: 29412107]
[4]
World Health Organization (WHO). Antimicrobial Resistance: Global Report on Surveillance 2014; WHO: Geneva, 2014.
[5]
Landecker, H. Antimicrobials before antibiotics: war, peace, and disinfectants. Palgrave Commun., 2019, 5, 45.
[http://dx.doi.org/10.1057/s41599-019-0251-8]
[6]
Donaghy, J.A.; Jagadeesan, B.; Goodburn, K. Relationship of sanitizers, disinfectants, and cleaning agents with antimicrobial resistance. J. Food Protec. , 82(5), 889-902.
[7]
da Cruz, R.M.D.; Zelli, R.; Benshain, S.; da Cruz, R.M.D.; Siqueira‐Júnior, J.P.; Décout, J-L.; Mingeot‐Leclercq, M-P.; Mendonça-Junior, F.J.B. Synthesis and evaluation of 2‐aminothiophene derivatives as Staphylococcus aureus efflux pump inhibitors. ChemMedChem, 2020, 15(8), 716-725.
[http://dx.doi.org/10.1002/cmdc.201900688.]
[8]
Sabatini, S.; Gosetto, F.; Serritella, S.; Manfroni, G.; Tabarrini, O.; Iraci, N.; Brincat, J.P.; Carosati, E.; Villarini, M.; Kaatz, G.W.; Cecchetti, V. Pyrazolo[4,3-c][1,2]benzothiazines 5,5-dioxide: a promising new class of Staphylococcus aureus NorA efflux pump inhibitors. J. Med. Chem., 2012, 55(7), 3568-3572.
[http://dx.doi.org/10.1021/jm201446h ] [PMID: 22432682]
[9]
Du, D.; Wang-Kan, X.; Neuberger, A.; Van Veen, H.W.; Pos, K.M.; Piddock, L.J.V.; Luisi, B.F. Multidrug efflux pumps: structure, function and regulation. Nat. Rev. Microbiol., 2018, 16, 523-539.
[http://dx.doi.org/10.1038/s41579-018-0048-6]
[10]
Costa, S.S.; Viveiros, M.; Amaral, L.; Couto, I. Multidrug efflux pumps in Staphylococcus aureus: An update. Open Microbiol. J., 2013, 7(Suppl. 1-M5), 59-71.
[11]
Kalia, N.P.; Mahajan, P.; Mehra, R.; Nargotra, A.; Sharma, J.P.; Koul, S.; Khan, I.A. Capsaicin, a novel inhibitor of the NorA efflux pump, reduces the intracellular invasion of Staphylococcus aureus. J. Antimicrob. Chemother., 2012, 67(10), 2401-2408.
[http://dx.doi.org/10.1093/jac/dks232 ] [PMID: 22807321]
[12]
Handzlik, J.; Matys, A.; Kieć-Kononowicz, K. Recent advances in multi-drug resistance (mdr) efflux pump inhibitors of gram-positive bacteria s. aureus. Antibiotics (Basel), 2013, 2(1), 28-45.
[http://dx.doi.org/10.3390/antibiotics2010028 ] [PMID: 27029290]
[13]
Abdi, S.N.; Ghotaslou, R.; Ganbarov, K.; Mobed, A.; Tanomand, A.; Yousefi, M.; Asgharzadeh, M.; Kafil, H.S. Acinetobacter baumannii efflux pumps and antibiotic resistance. Infect. Drug Resist., 2020, 13, 423-434.
[http://dx.doi.org/10.2147/IDR.S228089 ] [PMID: 32104014]
[14]
Poole, K.; Lomovskaya, O. Can efflux inhibitors really counter resistance? Drug Discov. Today, 2006, 3, 145-152.
[15]
Mahamoud, A.; Chevalier, J.; Alibert-Franco, S.; Kern, W.V.; Pages, J.M. Antibiotic efflux pumps in Gram-negative bacteria: The inhibitor response strategy. J. Antimicrob. Chemother, 2007, 59, 1223-1229. Staphylococcus aureus: visiting a strain of clinical importance. J. Bras. Patol. Med. Lab., 2007, 43(6), 413-423.
[16]
dos Santos, A.L.; Santos, D.O.; de Freitas, C.C.; Ferreira, B.L.A.; Afonso, I.F.; Rodrigues, C.R.; Castro, H.C. Staphylococcus aureus: visiting a strain of clinical importance. J. Bras. Patol. Med. Lab., 2007, 43(6), 413-423.
[17]
Kadariya, J.; Thapaliya, D.; Bhatta, S.; Mahatara, R.L.; Bempah, S.; Dhakal, N.; Smith, T.C. Multidrug-resistant staphylococcus aureus colonization in healthy adults is more common in bhutanese refugees in nepal than those resettled in ohio. BioMed Res. Int., 2019, 20195739247
[http://dx.doi.org/10.1155/2019/5739247 ] [PMID: 31355270]
[18]
Santajit, S.; Indrawattana, N. Mechanisms of antimicrobial resistance in ESKAPE pathogens. BioMed Res. Int., 2016, •••20162475067
[http://dx.doi.org/10.1155/2016/2475067 ] [PMID: 27274985]
[19]
Roch, M.; Clair, P.; Renzoni, A.; Reverdy, M.E.; Dauwalder, O.; Bes, M.; Martra, A.; Freydière, A.M.; Laurent, F.; Reix, P.; Dumitrescu, O.; Vandenesch, F. Exposure of Staphylococcus aureus to subinhibitory concentrations of β-lactam antibiotics induces heterogeneous vancomycin-intermediate Staphylococcus aureus. Antimicrob. Agents Chemother., 2014, 58(9), 5306-5314.
[http://dx.doi.org/10.1128/AAC.02574-14 ] [PMID: 24957836]
[20]
Finks, J.; Wells, E.; Dyke, T.L.; Husain, N.; Plizga, L.; Heddurshetti, R.; Wilkins, M.; Rudrik, J.; Hageman, J.; Patel, J.; Miller, C. Vancomycin-resistant Staphylococcus aureus, Michigan, USA, 2007. Emerg. Infect. Dis., 2009, 15(6), 943-945.
[http://dx.doi.org/10.3201/eid1506.081312 ] [PMID: 19523298]
[21]
Garoy, E.Y.; Gebreab, Y.B.; Achila, O.O.; Tekeste, D.G.; Kesete, R.; Ghirmay, R.; Kiflay, R.; Tesfu, T. Methicillin-resistant staphylococcus aureus (mrsa): prevalence and antimicrobial sensitivity pattern among patients-a multicenter study in asmara, eritrea. Can. J. Infect. Dis. Med. Microbiol., 2019, 20198321834
[http://dx.doi.org/10.1155/2019/8321834 ] [PMID: 30881532]
[22]
Tsiodras, S.; Gold, H.S.; Sakoulas, G.; Eliopoulos, G.M.; Wennersten, C.; Venkataraman, L.; Moellering, R.C.; Ferraro, M.J. Linezolid resistance in a clinical isolate of Staphylococcus aureus. Lancet, 2001, 358(9277), 207-208.
[http://dx.doi.org/10.1016/S0140-6736(01)05410-1 ] [PMID: 11476839]
[23]
Werth, B.J.; Jain, R.; Hahn, A.; Cummings, L.; Weaver, T.; Waalkes, A.; Sengupta, D.; Salipante, S.J.; Rakita, R.M.; Butler-Wu, S.M. Emergence of dalbavancin non-susceptible, vancomycin-intermediate Staphylococcus aureus (VISA) after treatment of MRSA central line-associated bloodstream infection with a dalbavancin- and vancomycin-containing regimen. Clin. Microbiol. Infect., 2018, 24(4), 429.e1-429.e5.
[http://dx.doi.org/10.1016/j.cmi.2017.07.028 ] [PMID: 28782651]
[24]
Andersen, J.L.; He, G-X.; Kakarla, P. K c, R.; Kumar, S.; Lakra, W.S.; Mukherjee, M.M.; Ranaweera, I.; Shrestha, U.; Tran, T.; Varela, M.F. Multidrug efflux pumps from Enterobacteriaceae, Vibrio cholerae and Staphylococcus aureus bacterial food pathogens. Int. J. Environ. Res. Public Health, 2015, 12(2), 1487-1547.
[http://dx.doi.org/10.3390/ijerph120201487 ] [PMID: 25635914]
[25]
Kumar, S.; Varela, M.F. Biochemistry of bacterial multidrug efflux pumps. Int. J. Mol. Sci., 2012, 13(4), 4484-4495.
[http://dx.doi.org/10.3390/ijms13044484 ] [PMID: 22605991]
[26]
Otto, M. Methicillin-resistant Staphylococcus aureus infection is associated with increased mortality. Future Microbiol., 2012, 7(2), 189-191.
[http://dx.doi.org/10.2217/fmb.11.156 ] [PMID: 22324988]
[27]
Costa, L.M.; de Macedo, E.V.; Oliveira, F.A.; Ferreira, J.H.; Gutierrez, S.J.; Peláez, W.J.; Lima, F.C.; de Siqueira Júnior, J.P.; Coutinho, H.D.; Kaatz, G.W.; de Freitas, R.M.; Barreto, H.M. Inhibition of the NorA efflux pump of Staphylococcus aureus by synthetic riparins. J. Appl. Microbiol., 2016, 121(5), 1312-1322.
[http://dx.doi.org/10.1111/jam.13258 ] [PMID: 27537678]
[28]
Abd El-Baky, R.M.; Sandle, T.; John, J.; Abuo-Rahma, G.E.A.; Hetta, H.F. A novel mechanism of action of ketoconazole: inhibition of the NorA efflux pump system and biofilm formation in multidrug-resistant Staphylococcus aureus. Infect. Drug Resist., 2019, 12, 1703-1718.
[http://dx.doi.org/10.2147/IDR.S201124 ] [PMID: 31354319]
[29]
Van Bambeke, F.; Glupczynski, Y.; Plésiat, P.; Pechère, J.C.; Tulkens, P.M. Antibiotic efflux pumps in prokaryotic cells: occurrence, impact on resistance and strategies for the future of antimicrobial therapy. J. Antimicrob. Chemother., 2003, 51(5), 1055-1065.
[http://dx.doi.org/10.1093/jac/dkg224 ] [PMID: 12697642]
[30]
Webber, M.A.; Piddock, L.J.V. The importance of efflux pumps in bacterial antibiotic resistance. J. Antimicrob. Chemother., 2003, 51(1), 9-11.
[http://dx.doi.org/10.1093/jac/dkg050 ] [PMID: 12493781]
[31]
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(12), 5406-5412.
[http://dx.doi.org/10.1128/AAC.00580-10 ] [PMID: 20855745]
[32]
Ogawa, W.; Onishi, M.; Ni, R.; Tsuchiya, T.; Kuroda, T. Functional study of the novel multidrug efflux pump KexD from Klebsiella pneumoniae. Gene, 2012, 498(2), 177-182.
[http://dx.doi.org/10.1016/j.gene.2012.02.008 ] [PMID: 22391093]
[33]
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(8), 3630-3635.
[http://dx.doi.org/10.1073/pnas.93.8.3630 ] [PMID: 8622987]
[34]
Borges-Walmsley, M.I.; Walmsley, A.R. The structure and function of drug pumps. Trends Microbiol., 2001, 9(2), 71-79.
[http://dx.doi.org/10.1016/S0966-842X(00)01920-X ] [PMID: 11173246]
[35]
Borges-Walmsley, M.I.; McKeegan, K.S.; Walmsley, A.R. Structure and function of efflux pumps that confer resistance to drugs. Biochem. J., 2003, 376(Pt 2), 313-338.
[http://dx.doi.org/10.1042/bj20020957 ] [PMID: 13678421]
[36]
Jarmuła, A.; Obłąk, E.; Wawrzycka, D.; Gutowicz, J. [Effluxmediated antimicrobial multidrug resistance]. Postepy Hig. Med. Dosw., 2011, 65, 216-227.
[PMID: 21502698]
[37]
Yan, N. Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem. Sci., 2013, 38(3), 151-159.
[http://dx.doi.org/10.1016/j.tibs.2013.01.003 ] [PMID: 23403214]
[38]
Kaback, H.R.; Sahin-Tóth, M.; Weinglass, A.B. The kamikaze approach to membrane transport. Nat. Rev. Mol. Cell Biol., 2001, 2(8), 610-620.
[http://dx.doi.org/10.1038/35085077 ] [PMID: 11483994]
[39]
Dantas, N.; de Aquino, T.M.; de Araújo-Júnior, J.X.; da Silva-Júnior, E.; Gomes, E.A.; Gomes, A.A.S.; Siqueira-Júnior, J.P.; Mendonça, Junior, F.J.B. Aminoguanidine hydrazones (AGH’s) as modulators of norfloxacin resistance in Staphylococcus aureus that overexpress NorA efflux pump. Chem. Biol. Interact., 2018, 280, 8-14.
[http://dx.doi.org/10.1016/j.cbi.2017.12.009 ] [PMID: 29208359]
[40]
Neyfakh, A.A.; Borsch, C.M.; Kaatz, G.W. Fluoroquinolone resistance protein NorA of Staphylococcus aureus is a multidrug efflux transporter. Antimicrob. Agents Chemother., 1993, 37(1), 128-129.
[http://dx.doi.org/10.1128/AAC.37.1.128 ] [PMID: 8431010]
[41]
Kaatz, G.W.; Seo, S.M. Inducible NorA-mediated multidrug resistance in Staphylococcus aureus. Antimicrob. Agents Chemother., 1995, 39(12), 2650-2655.
[http://dx.doi.org/10.1128/AAC.39.12.2650 ] [PMID: 8592996]
[42]
Lewis, K. In search of natural substrates and inhibitors of MDR pumps. J. Mol. Microbiol. Biotechnol., 2001, 3(2), 247-254.
[PMID: 11321580]
[43]
Smith, E.C.; Williamson, E.M.; Wareham, N.; Kaatz, G.W.; Gibbons, S. Antibacterials and modulators of bacterial resistance from the immature cones of Chamaecyparis lawsoniana. Phytochemistry, 2007, 68(2), 210-217.
[http://dx.doi.org/10.1016/j.phytochem.2006.10.001 ] [PMID: 17109904]
[44]
Pagès, J.M.; Amaral, L.; Fanning, S. An original deal for new molecule: reversal of efflux pump activity, a rational strategy to combat gram-negative resistant bacteria. Curr. Med. Chem., 2011, 18(19), 2969-2980.
[http://dx.doi.org/10.2174/092986711796150469 ] [PMID: 21651484]
[45]
Lamut, A.; Peterlin Mašič, L.; Kikelj, D.; Tomašič, T. Efflux pump inhibitors of clinically relevant multidrug resistant bacteria. Med. Res. Rev., 2019, 39(6), 2460-2504.
[http://dx.doi.org/10.1002/med.21591 ] [PMID: 31004360]
[46]
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., 1999, 43(10), 2404-2408.
[http://dx.doi.org/10.1128/AAC.43.10.2404 ] [PMID: 10508015]
[47]
Schindler, B.D.; Jacinto, P.; Kaatz, G.W. Inhibition of drug efflux pumps in staphylococcus aureus: current status of potentiating existing antibiotics. Chemother., 1968, 16, 843-846.
[48]
Dreier, J.; Ruggerone, P. Interaction of antibacterial compounds with RND efflux pumps in Pseudomonas aeruginosa. Front. Microbiol., 2015, 6, 660.
[http://dx.doi.org/10.3389/fmicb.2015.00660 ] [PMID: 26217310]
[49]
Kaatz, G.W.; Seo, S.M. Mechanisms of fluoroquinolone resistance in genetically related strains of Staphylococcus aureus. Antimicrob. Agents Chemother., 1997, 41(12), 2733-2737.
[http://dx.doi.org/10.1128/AAC.41.12.2733 ] [PMID: 9420048]
[50]
Stavri, M.; Piddock, L.J.V.; Gibbons, S. Bacterial efflux pump inhibitors from natural sources. J. Antimicrob. Chemother., 2007, 59(6), 1247-1260.
[http://dx.doi.org/10.1093/jac/dkl460 ] [PMID: 17145734]
[51]
Abreu, A.C.; McBain, A.J.; Simões, M. Plants as sources of new antimicrobials and resistance-modifying agents. Nat. Prod. Rep., 2012, 29(9), 1007-1021.
[http://dx.doi.org/10.1039/c2np20035j ] [PMID: 22786554]
[52]
Gibbons, S. Anti-staphylococcal plant natural products. Nat. Prod. Rep., 2004, 21(2), 263-277.
[http://dx.doi.org/10.1039/b212695h ] [PMID: 15042149]
[53]
Zhang, L.; Ma, S. Efflux pump inhibitors: a strategy to combat P-glycoprotein and the NorA multidrug resistance pump. ChemMedChem, 2010, 5(6), 811-822.
[http://dx.doi.org/10.1002/cmdc.201000006 ] [PMID: 20373322]
[54]
Gibbons, S.; Oluwatuyi, M.; Kaatz, G.W. A novel inhibitor of multidrug efflux pumps in Staphylococcus aureus. J. Antimicrob. Chemother., 2003, 51(1), 13-17.
[http://dx.doi.org/10.1093/jac/dkg044 ] [PMID: 12493782]
[55]
German, N.; Wei, P.; Kaatz, G.W.; Kerns, R.J. Synthesis and evaluation of fluoroquinolone derivatives as substrate-based inhibitors of bacterial efflux pumps. Eur. J. Med. Chem., 2008, 43(11), 2453-2463.
[http://dx.doi.org/10.1016/j.ejmech.2008.01.042 ] [PMID: 18358571]
[56]
Cecchetti, V.; Fravolini, A.; Lorenzini, M.C.; Tabarrini, O.; Terni, P.; Xin, T. Studies on 6-aminoquinolones: synthesis and antibacterial evaluation of 6-amino-8-methylquinolones. J. Med. Chem., 1996, 39(2), 436-445.
[http://dx.doi.org/10.1021/jm950558v ] [PMID: 8558512]
[57]
Pieroni, M.; Dimovska, M.; Brincat, J.P.; Sabatini, S.; Carosati, E.; Massari, S.; Kaatz, G.W.; Fravolini, A. From 6-aminoquinolone antibacterials to 6-amino-7-thiopyranopyridinylquinolone ethyl esters as inhibitors of Staphylococcus aureus multidrug efflux pumps. J. Med. Chem., 2010, 53(11), 4466-4480.
[http://dx.doi.org/10.1021/jm1003304 ] [PMID: 20446747]
[58]
Doléans-Jordheim, A.; Veron, J.B.; Fendrich, O.; Bergeron, E.; Montagut-Romans, A.; Wong, Y.S.; Furdui, B.; Freney, J.; Dumontet, C.; Boumendjel, A. 3-Aryl-4-methyl-2-quinolones targeting multiresistant Staphylococcus aureus bacteria. ChemMedChem, 2013, 8(4), 652-657.
[http://dx.doi.org/10.1002/cmdc.201200551 ] [PMID: 23436688]
[59]
Sabatini, S.; Gosetto, F.; Manfroni, G.; Tabarrini, O.; Kaatz, G.W.; Patel, D.; Cecchetti, V. Evolution from a natural flavones nucleus to obtain 2-(4-Propoxyphenyl)quinoline derivatives as potent inhibitors of the S. aureus NorA efflux pump. J. Med. Chem., 2011, 54(16), 5722-5736.
[http://dx.doi.org/10.1021/jm200370y ] [PMID: 21751791]
[60]
Sabatini, S.; Gosetto, F.; Iraci, N.; Barreca, M.L.; Massari, S.; Sancineto, L.; Manfroni, G.; Tabarrini, O.; Dimovska, M.; Kaatz, G.W.; Cecchetti, V. Re-evolution of the 2-phenylquinolines: ligand-based design, synthesis, and biological evaluation of a potent new class of Staphylococcus aureus NorA efflux pump inhibitors to combat antimicrobial resistance. J. Med. Chem., 2013, 56(12), 4975-4989.
[http://dx.doi.org/10.1021/jm400262a ] [PMID: 23710549]
[61]
Sabatini, S.; Piccioni, M.; Felicetti, T.; De Marco, S.; Manfroni, G.; Pagiotti, R.; Nocchetti, M.; Cecchetti, V.; Pietrella, D. Investigation on the Effect of Known Potent: S. Aureus NorA Efflux Pump Inhibitors on the Staphylococcal Biofilm Formation. RSC Advances, 2017, 7, 37007-37014.
[http://dx.doi.org/10.1039/C7RA03859C]
[62]
Carotti, A.; Ianni, F.; Sabatini, S.; Di Michele, A.; Sardella, R.; Kaatz, G.W.; Lindner, W.; Cecchetti, V.; Natalini, B. The “racemic approach” in the evaluation of the enantiomeric NorA efflux pump inhibition activity of 2-phenylquinoline derivatives. J. Pharm. Biomed. Anal., 2016, 129, 182-189.
[http://dx.doi.org/10.1016/j.jpba.2016.07.003 ] [PMID: 27429367]
[63]
Felicetti, T.; Cannalire, R.; Pietrella, D.; Latacz, G.; Lubelska, A.; Manfroni, G.; Barreca, M.L.; Massari, S.; Tabarrini, O.; Kieć-Kononowicz, K.; Schindler, B.D.; Kaatz, G.W.; Cecchetti, V.; Sabatini, S. 2-Phenylquinoline s. aureus nora efflux pump inhibitors: evaluation of the importance of methoxy group introduction. J. Med. Chem., 2018, 61(17), 7827-7848.
[http://dx.doi.org/10.1021/acs.jmedchem.8b00791 ] [PMID: 30067360]
[64]
Felicetti, T.; Cannalire, R.; Nizi, M.G.; Tabarrini, O.; Massari, S.; Barreca, M.L.; Manfroni, G.; Schindler, B.D.; Cecchetti, V.; Kaatz, G.W.; Sabatini, S. Studies on 2-phenylquinoline Staphylococcus aureus NorA efflux pump inhibitors: New insights on the C-6 position. Eur. J. Med. Chem., 2018, 155, 428-433.
[http://dx.doi.org/10.1016/j.ejmech.2018.06.013 ] [PMID: 29908437]
[65]
Stermitz, F.R.; Lorenz, P.; Tawara, J.N.; Zenewicz, L.A.; Lewis, K. Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 5′-methoxyhydnocarpin, a multidrug pump inhibitor. Proc. Natl. Acad. Sci. USA, 2000, 97(4), 1433-1437.
[http://dx.doi.org/10.1073/pnas.030540597 ] [PMID: 10677479]
[66]
Stermitz, F.R.; Tawara-Matsuda, J.; Lorenz, P.; Mueller, P.; Zenewicz, L.; Lewis, K. 5′-Methoxyhydnocarpin-D and pheophorbide A: Berberis species components that potentiate berberine growth inhibition of resistant Staphylococcus aureus. J. Nat. Prod., 2000, 63(8), 1146-1149.
[http://dx.doi.org/10.1021/np990639k ] [PMID: 10978214]
[67]
Guz, N.R.; Stermitz, F.R.; Johnson, J.B.; Beeson, T.D.; Willen, S.; Hsiang, J.; Lewis, K. Flavonolignan and flavone inhibitors of a Staphylococcus aureus multidrug resistance pump: structure-activity relationships. J. Med. Chem., 2001, 44(2), 261-268.
[http://dx.doi.org/10.1021/jm0004190 ] [PMID: 11170636]
[68]
Fujita, M.; Shiota, S.; Kuroda, T.; Hatano, T.; Yoshida, T.; Mizushima, T.; Tsuchiya, T. Remarkable synergies between baicalein and tetracycline, and baicalein and β-lactams against methicillin-resistant Staphylococcus aureus. Microbiol. Immunol., 2005, 49(4), 391-396.
[http://dx.doi.org/10.1111/j.1348-0421.2005.tb03732.x ] [PMID: 15840965]
[69]
Chan, B.C.L.; Ip, M.; Lau, C.B.S.; Lui, S.L.; Jolivalt, C.; Ganem-Elbaz, C.; Litaudon, M.; Reiner, N.E.; Gong, H.; See, R.H.; Fung, K.P.; Leung, P.C. Synergistic effects of baicalein with ciprofloxacin against NorA over-expressed methicillin-resistant Staphylococcus aureus (MRSA) and inhibition of MRSA pyruvate kinase. J. Ethnopharmacol., 2011, 137(1), 767-773.
[http://dx.doi.org/10.1016/j.jep.2011.06.039 ] [PMID: 21782012]
[70]
Falcão-Silva, V.S.; Silva, D.A. Souza, Mde.F.; Siqueira-Junior, J.P. Modulation of drug resistance in Staphylococcus aureus by a kaempferol glycoside from Herissantia tiubae (Malvaceae). Phytother. Res., 2009, 23(10), 1367-1370.
[http://dx.doi.org/10.1002/ptr.2695 ] [PMID: 19224523]
[71]
Holler, J.G.; Christensen, S.B.; Slotved, H.C.; Rasmussen, H.B.; Gúzman, A.; Olsen, C.E.; Petersen, B.; Mølgaard, P. Novel inhibitory activity of the Staphylococcus aureus NorA efflux pump by a kaempferol rhamnoside isolated from Persea lingue Nees. J. Antimicrob. Chemother., 2012, 67(5), 1138-1144.
[http://dx.doi.org/10.1093/jac/dks005 ] [PMID: 22311936]
[72]
Randhawa, H.K.; Hundal, K.K.; Ahirrao, P.N.; Jachak, S.M.; Nandanwar, H.S. Efflux Pump Inhibitory Activity of Flavonoids Isolated from Alpinia Calcarata against Methicillin-Resistant Staphylococcus Aureus. Biol., 2016, 71, 484-493.
[http://dx.doi.org/10.1515/biolog-2016-0073]
[73]
Roy, S.K.; Kumari, N.; Pahwa, S.; Agrahari, U.C.; Bhutani, K.K.; Jachak, S.M.; Nandanwar, H.; Nor, A. NorA efflux pump inhibitory activity of coumarins from Mesua ferrea. Fitoterapia, 2013, 90, 140-150.
[http://dx.doi.org/10.1016/j.fitote.2013.07.015 ] [PMID: 23892000]
[74]
Wang, D.; Xie, K.; Zou, D.; Meng, M.; Xie, M. Inhibitory effects of silybin on the efflux pump of methicillin resistant Staphylococcus aureus. Mol. Med. Rep., 2018, 18(1), 827-833.
[PMID: 29845191]
[75]
Diniz-Silva, H.T.; Magnani, M.; de Siqueira, S.; de Souza, E.L.; de Siqueira-Júnior, J.P. Fruit flavonoids as modulators of norfloxacin resistance in staphylococcus aureus that overexpresses NorA. Lebensm. Wiss. Technol., 2017, 85, 324-326.
[http://dx.doi.org/10.1016/j.lwt.2016.04.003]
[76]
Sharma, P.; Kumar, S.; Ali, F.; Anthal, S.; Gupta, V.K.; Khan, I.A.; Singh, S.; Sangwan, P.L.; Suri, K.A.; Gupta, B.D.; Gupta, D.K.; Dutt, P.; Vishwakarma, R.A.; Satti, N.K. Synthesis and biologic activities of some novel heterocyclic chalcone derivatives. Med. Chem. Res., 2013, 22, 3969-3983.
[http://dx.doi.org/10.1007/s00044-012-0401-7]
[77]
Pfeifer, H.J.; Greenblatt, D.K.; Koch-Wester, J. Clinical toxicity of reserpine in hospitalized patients: a report from the boston collaborative drug surveillance program. Am. J. Med. Sci., 1976, 271(3), 269-276.
[http://dx.doi.org/10.1097/00000441-197605000-00002 ] [PMID: 937377]
[78]
Schmitz, F.J.; Fluit, A.C.; Lückefahr, M.; Engler, B.; Hofmann, B.; Verhoef, J.; Heinz, H.P.; Hadding, U.; Jones, M.E. 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., 1998, 42(6), 807-810.
[http://dx.doi.org/10.1093/jac/42.6.807 ] [PMID: 10052906]
[79]
Ball, A.R.; Casadei, G.; Samosorn, S.; Bremner, J.B.; Ausubel, F.M.; Moy, T.I.; Lewis, K. Conjugating berberine to a multidrug efflux pump inhibitor creates an effective antimicrobial. ACS Chem. Biol., 2006, 1(9), 594-600.
[http://dx.doi.org/10.1021/cb600238x ] [PMID: 17168555]
[80]
Samosorn, S.; Bremner, J.B.; Ball, A.; Lewis, K. Synthesis of functionalized 2-aryl-5-nitro-1H-indoles and their activity as bacterial NorA efflux pump inhibitors. Bioorg. Med. Chem., 2006, 14(3), 857-865.
[http://dx.doi.org/10.1016/j.bmc.2005.09.019 ] [PMID: 16203150]
[81]
Dai, Y.; Zhang, X.; Zhang, X.; Wang, H.; Lu, Z. DFT and GA studies on the QSAR of 2-aryl-5-nitro-1H-indole derivatives as NorA efflux pump inhibitors. J. Mol. Model., 2008, 14(9), 807-812.
[http://dx.doi.org/10.1007/s00894-008-0328-6 ] [PMID: 18575902]
[82]
Ambrus, J.I.; Kelso, M.J.; Bremner, J.B.; Ball, A.R.; Casadei, G.; Lewis, K. Structure-activity relationships of 2-aryl-1H-indole inhibitors of the NorA efflux pump in Staphylococcus aureus. Bioorg. Med. Chem. Lett., 2008, 18(15), 4294-4297.
[http://dx.doi.org/10.1016/j.bmcl.2008.06.093 ] [PMID: 18632270]
[83]
Samosorn, S.; Tanwirat, B.; Muhamad, N.; Casadei, G.; Tomkiewicz, D.; Lewis, K.; Suksamrarn, A.; Prammananan, T.; Gornall, K.C.; Beck, J.L.; Bremner, J.B. Antibacterial activity of berberine-NorA pump inhibitor hybrids with a methylene ether linking group. Bioorg. Med. Chem., 2009, 17(11), 3866-3872.
[http://dx.doi.org/10.1016/j.bmc.2009.04.028 ] [PMID: 19419877]
[84]
Tomkiewicz, D.; Casadei, G.; Larkins-Ford, J.; Moy, T.I.; Garner, J.; Bremner, J.B.; Ausubel, F.M.; Lewis, K.; Kelso, M.J. Berberine-INF55 (5-nitro-2-phenylindole) hybrid antimicrobials: effects of varying the relative orientation of the berberine and INF55 components. Antimicrob. Agents Chemother., 2010, 54(8), 3219-3224.
[http://dx.doi.org/10.1128/AAC.01715-09 ] [PMID: 20498327]
[85]
Hequet, A.; Burchak, O.N.; Jeanty, M.; Guinchard, X.; Le Pihive, E.; Maigre, L.; Bouhours, P.; Schneider, D.; Maurin, M.; Paris, J.M.; Denis, J.N.; Jolivalt, C. 1-(1H-indol-3-yl)ethanamine derivatives as potent Staphylococcus aureus NorA efflux pump inhibitors. ChemMedChem, 2014, 9(7), 1534-1545.
[http://dx.doi.org/10.1002/cmdc.201400042 ] [PMID: 24677763]
[86]
Caspar, Y.; Jeanty, M.; Blu, J.; Burchak, O.; Le Pihive, E.; Maigre, L.; Schneider, D.; Jolivalt, C.; Paris, J.M.; Hequet, A.; Minassian, F.; Denis, J.N.; Maurin, M. Novel synthetic bis-indolic derivatives with antistaphylococcal activity, including against MRSA and VISA strains. J. Antimicrob. Chemother., 2015, 70(6), 1727-1737.
[http://dx.doi.org/10.1093/jac/dkv015 ] [PMID: 25691323]
[87]
Lepri, S.; Buonerba, F.; Goracci, L.; Velilla, I.; Ruzziconi, R.; Schindler, B.D.; Seo, S.M.; Kaatz, G.W.; Cruciani, G. Indole based weapons to fight antibiotic resistance: a structure-activity relationship study. J. Med. Chem., 2016, 59(3), 867-891.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01219 ] [PMID: 26757340]
[88]
Buonerba, F.; Lepri, S.; Goracci, L.; Schindler, B.D.; Seo, S.M.; Kaatz, G.W.; Cruciani, G. Improved potency of indole-based nora efflux pump inhibitors: from serendipity toward rational design and development. J. Med. Chem., 2017, 60(1), 517-523.
[http://dx.doi.org/10.1021/acs.jmedchem.6b01281 ] [PMID: 27977195]
[89]
Radix, S.; Jordheim, A.D.; Rocheblave, L.; N’Digo, S.; Prignon, A.L.; Commun, C.; Michalet, S.; Dijoux-Franca, M.G.; Mularoni, A.; Walchshofer, N.N. N′-disubstituted cinnamamide derivatives potentiate ciprofloxacin activity against overexpressing NorA efflux pump Staphylococcus aureus 1199B strains. Eur. J. Med. Chem., 2018, 150, 900-907.
[http://dx.doi.org/10.1016/j.ejmech.2018.03.028 ] [PMID: 29597171]
[90]
Rath, S.K.; Singh, S.; Kumar, S.; Wani, N.A.; Rai, R.; Koul, S.; Khan, I.A.; Sangwan, P.L. Synthesis of amides from (E)-3-(1-chloro-3,4-dihydronaphthalen-2-yl)acrylic acid and substituted amino acid esters as NorA efflux pump inhibitors of Staphylococcus aureus. Bioorg. Med. Chem., 2019, 27(2), 343-353.
[http://dx.doi.org/10.1016/j.bmc.2018.12.008 ] [PMID: 30552006]
[91]
Morandi, F.; Caselli, E.; Morandi, S.; Focia, P.J.; Blázquez, J.; Shoichet, B.K.; Prati, F. Nanomolar inhibitors of AmpC β-lactamase. J. Am. Chem. Soc., 2003, 125(3), 685-695.
[http://dx.doi.org/10.1021/ja0288338 ] [PMID: 12526668]
[92]
Livermore, D.M.; Mushtaq, S. Activity of biapenem (RPX2003) combined with the boronate β-lactamase inhibitor RPX7009 against carbapenem-resistant Enterobacteriaceae. J. Antimicrob. Chemother., 2013, 68(8), 1825-1831.
[http://dx.doi.org/10.1093/jac/dkt118 ] [PMID: 23580564]
[93]
Fontaine, F.; Hequet, A.; Voisin-Chiret, A.S.; Bouillon, A.; Lesnard, A.; Cresteil, T.; Jolivalt, C.; Rault, S. First identification of boronic species as novel potential inhibitors of the Staphylococcus aureus NorA efflux pump. J. Med. Chem., 2014, 57(6), 2536-2548.
[http://dx.doi.org/10.1021/jm401808n ] [PMID: 24499135]
[94]
Fontaine, F.; Héquet, A.; Voisin-Chiret, A.S.; Bouillon, A.; Lesnard, A.; Cresteil, T.; Jolivalt, C.; Rault, S. Boronic species as promising inhibitors of the Staphylococcus aureus NorA efflux pump: study of 6-substituted pyridine-3-boronic acid derivatives. Eur. J. Med. Chem., 2015, 95, 185-198.
[http://dx.doi.org/10.1016/j.ejmech.2015.02.056 ] [PMID: 25817769]
[95]
Marquez, B.; Neuville, L.; Moreau, N.J.; Genet, J.P.; dos Santos, A.F.; Caño de Andrade, M.C.; Sant’Ana, A.E.G. Multidrug resistance reversal agent from Jatropha elliptica. Phytochemistry, 2005, 66(15), 1804-1811.
[http://dx.doi.org/10.1016/j.phytochem.2005.06.008 ] [PMID: 16051285]
[96]
Khan, I.A.; Mirza, Z.M.; Kumar, A.; Verma, V.; Qazi, G.N. Piperine, a phytochemical potentiator of ciprofloxacin against Staphylococcus aureus. Antimicrob. Agents Chemother., 2006, 50(2), 810-812.
[http://dx.doi.org/10.1128/AAC.50.2.810-812.2006 ] [PMID: 16436753]
[97]
Mohtar, M.; Johari, S.A.; Li, A.R.; Isa, M.M.; Mustafa, S.; Ali, A.M.; Basri, D.F. Inhibitory and resistance-modifying potential of plant-based alkaloids against methicillin-resistant Staphylococcus aureus (MRSA). Curr. Microbiol., 2009, 59(2), 181-186.
[http://dx.doi.org/10.1007/s00284-009-9416-9 ] [PMID: 19475447]
[98]
Kumar, A.; Khan, I.A.; Koul, S.; Koul, J.L.; Taneja, S.C.; Ali, I.; Ali, F.; Sharma, S.; Mirza, Z.M.; Kumar, M.; Sangwan, P.L.; Gupta, P.; Thota, N.; Qazi, G.N. Novel structural analogues of piperine as inhibitors of the NorA efflux pump of Staphylococcus aureus. J. Antimicrob. Chemother., 2008, 61(6), 1270-1276.
[http://dx.doi.org/10.1093/jac/dkn088 ] [PMID: 18334493]
[99]
Sangwan, P.L.; Koul, J.L.; Koul, S.; Reddy, M.V.; Thota, N.; Khan, I.A.; Kumar, A.; Kalia, N.P.; Qazi, G.N. Piperine analogs as potent Staphylococcus aureus NorA efflux pump inhibitors. Bioorg. Med. Chem., 2008, 16(22), 9847-9857.
[http://dx.doi.org/10.1016/j.bmc.2008.09.042 ] [PMID: 18848780]
[100]
Wani, N.A.; Singh, S.; Farooq, S.; Shankar, S.; Koul, S.; Khan, I.A.; Rai, R. Amino acid amides of piperic acid (PA) and 4-ethylpiperic acid (EPA) as NorA efflux pump inhibitors of Staphylococcus aureus. Bioorg. Med. Chem. Lett., 2016, 26(17), 4174-4178.
[http://dx.doi.org/10.1016/j.bmcl.2016.07.062 ] [PMID: 27503686]
[101]
Bharate, J.B.; Singh, S.; Wani, A.; Sharma, S.; Joshi, P.; Khan, I.A.; Kumar, A.; Vishwakarma, R.A.; Bharate, S.B. Discovery of 4-acetyl-3-(4-fluorophenyl)-1-(p-tolyl)-5-methylpyrrole as a dual inhibitor of human P-glycoprotein and Staphylococcus aureus Nor A efflux pump. Org. Biomol. Chem., 2015, 13(19), 5424-5431.
[http://dx.doi.org/10.1039/C5OB00246J ] [PMID: 25865846]
[102]
Vidaillac, C.; Guillon, J.; Arpin, C.; Forfar-Bares, I.; Ba, B.B.; Grellet, J.; Moreau, S.; Caignard, D.H.; Jarry, C.; Quentin, C. Synthesis of omeprazole analogues and evaluation of these as potential inhibitors of the multidrug efflux pump NorA of Staphylococcus aureus. Antimicrob. Agents Chemother., 2007, 51(3), 831-838.
[http://dx.doi.org/10.1128/AAC.01306-05 ] [PMID: 17101679]
[103]
Thota, N.; Koul, S.; Reddy, M.V.; Sangwan, P.L.; Khan, I.A.; Kumar, A.; Raja, A.F.; Andotra, S.S.; Qazi, G.N. Citral derived amides as potent bacterial NorA efflux pump inhibitors. Bioorg. Med. Chem., 2008, 16(13), 6535-6543.
[http://dx.doi.org/10.1016/j.bmc.2008.05.030 ] [PMID: 18524600]
[104]
Thota, N.; Reddy, M.V.; Kumar, A.; Khan, I.A.; Sangwan, P.L.; Kalia, N.P.; Koul, J.L.; Koul, S. Substituted dihydronaphthalenes as efflux pump inhibitors of Staphylococcus aureus. Eur. J. Med. Chem., 2010, 45(9), 3607-3616.
[http://dx.doi.org/10.1016/j.ejmech.2010.05.006 ] [PMID: 20605275]
[105]
Sundaramoorthy, N.S.; Mitra, K.; Ganesh, J.S.; Makala, H.; Lotha, R.; Bhanuvalli, S.R.; Ulaganathan, V.; Tiru, V.; Sivasubramanian, A.; Nagarajan, S. Ferulic acid derivative inhibits NorA efflux and in combination with ciprofloxacin curtails growth of MRSA in vitro and in vivo. Microb. Pathog., 2018, 124, 54-62.
[http://dx.doi.org/10.1016/j.micpath.2018.08.022 ] [PMID: 30118803]
[106]
Zimmermann, S.; Klinger-Strobel, M.; Bohnert, J.A.; Wendler, S.; Rödel, J.; Pletz, M.W.; Löffler, B.; Tuchscherr, L. Clinically approved drugs inhibit the staphylococcus aureus multidrug nora efflux pump and reduce biofilm formation. Front. Microbiol., 2019, 10, 2762.
[http://dx.doi.org/10.3389/fmicb.2019.02762 ] [PMID: 31849901]
[107]
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(2), 719-726.
[http://dx.doi.org/10.1128/AAC.47.2.719-726.2003 ] [PMID: 12543683]
[108]
Sabatini, S.; Kaatz, G.W.; Rossolini, G.M.; Brandini, D.; Fravolini, A. From phenothiazine to 3-phenyl-1,4-benzothiazine derivatives as inhibitors of the Staphylococcus aureus NorA multidrug efflux pump. J. Med. Chem., 2008, 51(14), 4321-4330.
[http://dx.doi.org/10.1021/jm701623q ] [PMID: 18578473]
[109]
Fournier dit Chabert, J.; Marquez, B.; Neville, L.; Joucla, L.; Broussous, S.; Bouhours, P.; David, E.; Pellet-Rostaing, S.; Marquet, B.; Moreau, N.; Lemaire, M. Synthesis and evaluation of new arylbenzo[b]thiophene and diarylthiophene derivatives as inhibitors of the nora multidrug transporter of staphylococcus aureus. Bioorg. Med. Chem., 2007, 15, 4482-4497.
[110]
Liger, F.; Bouhours, P.; Ganem-Elbaz, C.; Jolivalt, C.; Pellet-Rostaing, S.; Popowycz, F.; Paris, J.M.; Lemaire, M. C2 Arylated benzo[b]thiophene derivatives as staphylococcus aureus nora efflux pump inhibitors. ChemMedChem, 2016, 11(3), 320-330.
[http://dx.doi.org/10.1002/cmdc.201500463 ] [PMID: 26732895]
[111]
Lowrence, R.C.; Raman, T.; Makala, H.V.; Ulaganathan, V.; Subramaniapillai, S.G.; Kuppuswamy, A.A.; Mani, A.; Chittoor Neelakantan, S.; Nagarajan, S. Dithiazole thione derivative as competitive NorA efflux pump inhibitor to curtail multi drug resistant clinical isolate of MRSA in a zebrafish infection model. Appl. Microbiol. Biotechnol., 2016, 100(21), 9265-9281.
[http://dx.doi.org/10.1007/s00253-016-7759-2 ] [PMID: 27531512]
[112]
Pereira, P.S.; Lima, M.D.C.A.; Neto, P.P.M.; Oliveira-Tintino, C.D.M.; Tintino, S.R.; Menezes, I.R.A.; de Oliveira, J.F.; Marchand, P.; Coutinho, H.D.M.; Rodrigues, M.D.D.; da Silva, T.G. Thiazolidinedione and thiazole derivatives potentiate norfloxacin activity against NorA efflux pump over expression in Staphylococcus aureus 1199B strains. Bioorg. Med. Chem., 2019, 27(17), 3797-3804.
[http://dx.doi.org/10.1016/j.bmc.2019.07.006 ] [PMID: 31320212]
[113]
Brincat, J.P.; Carosati, E.; Sabatini, S.; Manfroni, G.; Fravolini, A.; Raygada, J.L.; Patel, D.; Kaatz, G.W.; Cruciani, G. Discovery of novel inhibitors of the NorA multidrug transporter of Staphylococcus aureus. J. Med. Chem., 2011, 54(1), 354-365.
[http://dx.doi.org/10.1021/jm1011963 ] [PMID: 21141825]
[114]
Kalle, A.M.; Rizvi, A. Inhibition of bacterial multidrug resistance by celecoxib, a cyclooxygenase-2 inhibitor. Antimicrob. Agents Chemother., 2011, 55(1), 439-442.
[http://dx.doi.org/10.1128/AAC.00735-10 ] [PMID: 20937780]
[115]
Gibbons, S.; Moser, E.; Kaatz, G.W. Catechin gallates inhibit multidrug resistance (MDR) in Staphylococcus aureus. Planta Med., 2004, 70(12), 1240-1242.
[http://dx.doi.org/10.1055/s-2004-835860 ] [PMID: 15643566]
[116]
Yam, T.S.; Hamilton-Miller, J.M.T.; Shah, S. The effect of a component of tea (Camellia sinensis) on methicillin resistance, PBP2′ synthesis, and beta-lactamase production in Staphylococcus aureus. J. Antimicrob. Chemother., 1998, 42(2), 211-216.
[http://dx.doi.org/10.1093/jac/42.2.211 ] [PMID: 9738838]
[117]
Hamilton-Miller, J.M.T.; Shah, S. Activity of the tea component epicatechin gallate and analogues against methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother., 2000, 46(5), 852-853.
[http://dx.doi.org/10.1093/jac/46.5.852 ] [PMID: 11062217]
[118]
Hamilton-Miller, J.M.T.; Shah, S. Disorganization of cell division of methicillin-resistant Staphylococcus aureus by a component of tea (Camellia sinensis): a study by electron microscopy. FEMS Microbiol. Lett., 1999, 176(2), 463-469.
[http://dx.doi.org/10.1111/j.1574-6968.1999.tb13698.x ] [PMID: 10427729]
[119]
Belofsky, G.; Percivill, D.; Lewis, K.; Tegos, G.P.; Ekart, J. Phenolic metabolites of Dalea versicolor that enhance antibiotic activity against model pathogenic bacteria. J. Nat. Prod., 2004, 67(3), 481-484.
[http://dx.doi.org/10.1021/np030409c ] [PMID: 15043439]
[120]
Michalet, S.; Cartier, G.; David, B.; Mariotte, A.M.; Dijoux-franca, M.G.; Kaatz, G.W.; Stavri, M.; Gibbons, S. N-caffeoylphenalkylamide derivatives as bacterial efflux pump inhibitors. Bioorg. Med. Chem. Lett., 2007, 17(6), 1755-1758.
[http://dx.doi.org/10.1016/j.bmcl.2006.12.059 ] [PMID: 17275293]
[121]
Shiu, W.K.P.; Malkinson, J.P.; Rahman, M.M.; Curry, J.; Stapleton, P.; Gunaratnam, M.; Neidle, S.; Mushtaq, S.; Warner, M.; Livermore, D.M.; Evangelopoulos, D.; Basavannacharya, C.; Bhakta, S.; Schindler, B.D.; Seo, S.M.; Coleman, D.; Kaatz, G.W.; Gibbons, S. A new plant-derived antibacterial is an inhibitor of efflux pumps in Staphylococcus aureus. Int. J. Antimicrob. Agents, 2013, 42(6), 513-518.
[http://dx.doi.org/10.1016/j.ijantimicag.2013.08.007 ] [PMID: 24119569]
[122]
Tintino, S.R.; Oliveira-Tintino, C.D.M.; Campina, F.F.; Silva, R.L.P. Costa, Mdo.S.; Menezes, I.R.; Calixto-Júnior, J.T.; Siqueira-Junior, J.P.; Coutinho, H.D.; Leal-Balbino, T.C.; Balbino, V.Q. Evaluation of the tannic acid inhibitory effect against the NorA efflux pump of Staphylococcus aureus. Microb. Pathog., 2016, 97, 9-13.
[http://dx.doi.org/10.1016/j.micpath.2016.04.003 ] [PMID: 27057677]
[123]
Park, K.S.; Choo, H.; Kim, M.K.; Chong, Y. Quercetin 7-O-Glutamate Potentiates Staphylococcus Aureus to Fluoroquinolone Antibiotics. Bull. Korean Chem. Soc., 2016, 37, 1515-1517.
[http://dx.doi.org/10.1002/bkcs.10901]
[124]
Singh, S.; Kalia, N.P.; Joshi, P.; Kumar, A.; Sharma, P.R.; Kumar, A.; Bharate, S.B.; Khan, I.A.; Boeravinone, B. Boeravinone B, a novel dual inhibitor of nora bacterial efflux pump of staphylococcus aureus and human p-glycoprotein, reduces the biofilm formation and intracellular invasion of bacteria. Front. Microbiol., 2017, 8, 1868.
[http://dx.doi.org/10.3389/fmicb.2017.01868 ] [PMID: 29046665]
[125]
Dos Santos, J.F.S.; Tintino, S.R.; de Freitas, T.S.; Campina, F.F. de A Menezes, I.R.; Siqueira-Júnior, J.P.; Coutinho, H.D.M.; Cunha, F.A.B. In vitro e in silico evaluation of the inhibition of Staphylococcus aureus efflux pumps by caffeic and gallic acid. Comp. Immunol. Microbiol. Infect. Dis., 2018, 57, 22-28.
[http://dx.doi.org/10.1016/j.cimid.2018.03.001 ] [PMID: 30017074]
[126]
Smith, E.C.J.; Kaatz, G.W.; Seo, S.M.; Wareham, N.; Williamson, E.M.; Gibbons, S. The phenolic diterpene totarol inhibits multidrug efflux pump activity in Staphylococcus aureus. Antimicrob. Agents Chemother., 2007, 51(12), 4480-4483.
[http://dx.doi.org/10.1128/AAC.00216-07 ] [PMID: 17664318]
[127]
Coêlho, M.L.; Ferreira, J.H.L.; de Siqueira Júnior, J.P.; Kaatz, G.W.; Barreto, H.M.; de Carvalho Melo Cavalcante, A.A. Inhibition of the NorA multi-drug transporter by oxygenated monoterpenes. Microb. Pathog., 2016, 99, 173-177.
[http://dx.doi.org/10.1016/j.micpath.2016.08.026 ] [PMID: 27565089]
[128]
Sun, Z.L.; Liu, T.; Gibbons, S.; Mu, Q. A Structure-Activity Relationship Study of Phenyl Sesquiterpenoids on Efflux Inhibition against Staphylococcus Aureus. Med. Chem. Res., 2019, 28, 1308-1318.
[http://dx.doi.org/10.1007/s00044-019-02375-9]
[129]
Cégiéla-Carlioz, P.; Bessière, J.M.; David, B.; Mariotte, A.M.; Gibbons, S.; Dijoux-Franca, M.G. Modulation of multi-drug resistance (mdr) in staphylococcus aureus by osha (ligusticum porteri l., apiaceae) essential oil compounds. Flavour Fragrance J., 2005, 20, 671-675.
[http://dx.doi.org/10.1002/ffj.1584]
[130]
de Morais Oliveira-Tintino, C.D.; Tintino, S.R.; Limaverde, P.W.; Figueredo, F.G.; Campina, F.F.; da Cunha, F.A.B.; da Costa, R.H.S.; Pereira, P.S.; Lima, L.F.; de Matos, Y.M.L.S.; Coutinho, H.D.M.; Siqueira-Júnior, J.P.; Balbino, V.Q.; da Silva, T.G. Inhibition of the essential oil from Chenopodium ambrosioides L. and α-terpinene on the NorA efflux-pump of Staphylococcus aureus. Food Chem., 2018, 262, 72-77.
[http://dx.doi.org/10.1016/j.foodchem.2018.04.040 ] [PMID: 29751924]
[131]
Silva, S.W.C.; Monção, N.B.N.; Araújo, B.Q.; Arcanjo, D.D.R.; Ferreira, J.H.L.; Lima Neto, J.S.; Citó, A.M.G.L.; de Siqueira Júnior, J.P.; Kaatz, G.W.; Barreto, H.M. Antimicrobial activity of Mimosa caesalpiniifolia Benth and its interaction with antibiotics against Staphylococcus aureus strains overexpressing efflux pump genes. Lett. Appl. Microbiol., 2019, 69(1), 57-63.
[http://dx.doi.org/10.1111/lam.13163 ] [PMID: 31002429]
[132]
de Sousa Andrade, L.M.; de Oliveira, A.B.M.; Leal, A.L.A.B.; de Alcântara Oliveira, F.A.; Portela, A.L.; de Sousa Lima Neto, J.; de Siqueira-Júnior, J.P.; Kaatz, G.W.; da Rocha, C.Q.; Barreto, H.M. Antimicrobial activity and inhibition of the NorA efflux pump of Staphylococcus aureus by extract and isolated compounds from Arrabidaea brachypoda. Microb. Pathog., 2020, 140, 103935
[http://dx.doi.org/10.1016/j.micpath.2019.103935 ] [PMID: 31857236]
[133]
Braga Ribeiro, A.M.; Sousa, J.N.; Costa, L.M.; Oliveira, F.A.A.; Dos Santos, R.C.; Silva Nunes, A.S.; da Silva, W.O.; Marques Cordeiro, P.J.; de Sousa Lima Neto, J.; de Siqueira-Júnior, J.P.; Kaatz, G.W.; Barreto, H.M.; de Oliveira, A.P. Antimicrobial activity of Phyllanthus amarus Schumach. & Thonn and inhibition of the NorA efflux pump of Staphylococcus aureus by Phyllanthin. Microb. Pathog., 2019, 130, 242-246.
[http://dx.doi.org/10.1016/j.micpath.2019.03.012 ] [PMID: 30876871]
[134]
Pereda-Miranda, R.; Kaatz, G.W.; Gibbons, S. Polyacylated oligosaccharides from medicinal Mexican morning glory species as antibacterials and inhibitors of multidrug resistance in Staphylococcus aureus. J. Nat. Prod., 2006, 69(3), 406-409.
[http://dx.doi.org/10.1021/np050227d ] [PMID: 16562846]
[135]
Chérigo, L.; Pereda-Miranda, R.; Fragoso-Serrano, M.; Jacobo-Herrera, N.; Kaatz, G.W.; Gibbons, S. Inhibitors of bacterial multidrug efflux pumps from the resin glycosides of Ipomoea murucoides. J. Nat. Prod., 2008, 71(6), 1037-1045.
[http://dx.doi.org/10.1021/np800148w ] [PMID: 18500841]
[136]
Chérigo, L.; Pereda-Miranda, R.; Gibbons, S. Bacterial resistance modifying tetrasaccharide agents from Ipomoea murucoides. Phytochemistry, 2009, 70(2), 222-227.
[http://dx.doi.org/10.1016/j.phytochem.2008.12.005 ] [PMID: 19136125]
[137]
Zhang, J.; Sun, Y.; Wang, Y.; Lu, M.; He, J.; Liu, J.; Chen, Q.; Zhang, X.; Zhou, F.; Wang, G.; Sun, X. Non-antibiotic agent ginsenoside 20(S)-Rh2 enhanced the antibacterial effects of ciprofloxacin in vitro and in vivo as a potential NorA inhibitor. Eur. J. Pharmacol., 2014, 740, 277-284.
[http://dx.doi.org/10.1016/j.ejphar.2014.07.020 ] [PMID: 25054686]
[138]
Abulrob, A.N.; Suller, M.T.E.; Gumbleton, M.; Simons, C.; Russell, A.D. Identification and biological evaluation of grapefruit oil components as potential novel efflux pump modulators in methicillin-resistant Staphylococcus aureus bacterial strains. Phytochemistry, 2004, 65(22), 3021-3027.
[http://dx.doi.org/10.1016/j.phytochem.2004.08.044 ] [PMID: 15504436]
[139]
Felicetti, T.; Cannalire, R.; Burali, M.S.; Massari, S.; Manfroni, G.; Barreca, M.L.; Tabarrini, O.; Schindler, B.D.; Sabatini, S.; Kaatz, G.W.; Cecchetti, V. Searching for novel inhibitors of the S. aureus NorA efflux pump: synthesis and biological evaluation of the 3-phenyl-1,4-benzothiazine analogues. ChemMedChem, 2017, 12(16), 1293-1302.
[http://dx.doi.org/10.1002/cmdc.201700286 ] [PMID: 28598572]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 24
Year: 2020
Page: [2168 - 2185]
Pages: 18
DOI: 10.2174/1568026620666200704135837
Price: $65

Article Metrics

PDF: 34
HTML: 8