Generic placeholder image

Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Mini-Review Article

Plant-based Natural Products as inhibitors for Efflux Pumps to Reverse Multidrug Resistance in Staphylococcus aureus: A Mini Review

Author(s): Shalini Ramalingam, Moola Joghee Nanjan Chandrasekar*, Ganesh G.N. Krishnan and Moola Joghee Nanjan*

Volume 24, Issue 3, 2024

Published on: 27 April, 2023

Page: [272 - 288] Pages: 17

DOI: 10.2174/1389557523666230406092128

Price: $65

conference banner
Abstract

Wounds provide a favourable site for microbial infection. Wound infection makes the healing more complex and does not proceed in an orchestrated manner leading to the chronic wound. Clinically infected wounds require proper antimicrobial therapy. Broad-spectrum antibiotics are usually prescribed first before going to targeted therapy. The current conventional mode of therapy mainly depends on the use of antibiotics topically or systemically. Repeated and prolonged use of antibiotics, however, leads to multidrug resistance. Staphylococcus aureus is the most common multidrugresistant microorganism found in wounds. It effectively colonizes the wound and produces many toxins, thereby reducing the host immune response and causing recurrent infection, thus making the wound more complex. The overexpression of efflux pumps is one of the major reasons for the emergence of multidrug resistance. Inhibition of efflux pumps is, therefore, a potential strategy to reverse this resistance. The effective therapy to overcome this antibiotic resistance is to use combination therapy, namely the combination of an inhibitor, and a non-antibiotic compound with an antibiotic for their dual function. Many synthetic efflux pump inhibitors to treat wound infections are still under clinical trials. In this connection, several investigations have been carried out on plant-based natural products as multidrug resistance-modifying agents as they are believed to be safe, inexpensive and suitable for chronic wound infections.

Graphical Abstract

[1]
Hemant Kumar, N.; Amit Kumar, S.; Srivastava, R. MadanLal, K.; Chandel, HS; Ranawat, M.S. Pharmacological investigation of the wound healing activity of cestrum nocturnum (L.) Ointment in Wistar Albino Rats. J. Pharm., 2016, 2016, 1-8. Available from: https://www.hindawi.com/journals/jphar/2016/9249040/
[2]
Percival, S.L.; Emanuel, C.; Cutting, K.F.; Williams, D.W. Microbiology of the skin and the role of biofilms in infection. Int. Wound J., 2012, 9(1), 14-32.
[http://dx.doi.org/10.1111/j.1742-481X.2011.00836.x] [PMID: 21973162]
[3]
Martin, J.M.; Zenilman, J.M.; Lazarus, G.S. Molecular microbiology: New dimensions for cutaneous biology and wound healing. J. Invest. Dermatol., 2010, 130(1), 38-48.
[http://dx.doi.org/10.1038/jid.2009.221] [PMID: 19626034]
[4]
Slade, E.A.; Thorn, R.M.S.; Young, A.; Reynolds, D.M. An in vitro collagen perfusion wound biofilm model; with applications for antimicrobial studies and microbial metabolomics. BMC Microbiol., 2019, 19(1), 310.
[http://dx.doi.org/10.1186/s12866-019-1682-5] [PMID: 31888471]
[5]
Moeini, A.; Pedram, P.; Makvandi, P.; Malinconico, M.; Gomez d’Ayala, G. Wound healing and antimicrobial effect of active secondary metabolites in chitosan-based wound dressings: A review. Carbohydr. Polym., 2020, 233, 115839.
[http://dx.doi.org/10.1016/j.carbpol.2020.115839] [PMID: 32059889]
[6]
Howell-Jones, R.S.; Wilson, M.J.; Hill, K.E.; Howard, A.J.; Price, P.E.; Thomas, D.W. A review of the microbiology, antibiotic usage and resistance in chronic skin wounds. J. Antimicrob. Chemother., 2005, 55(2), 143-149.
[http://dx.doi.org/10.1093/jac/dkh513] [PMID: 15649989]
[7]
O’Donnell, J.A.; Gelone, S.P.; Safdar, A. Topical Antibacterials. In: Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases; Elsevier: Amsterdam, Netherlands, 2015; pp. 452-462.
[http://dx.doi.org/10.1016/B978-1-4557-4801-3.00037-0]
[8]
Silver, L.L. Challenges of antibacterial discovery. Clin. Microbiol. Rev., 2011, 24(1), 71-109.
[http://dx.doi.org/10.1128/CMR.00030-10] [PMID: 21233508]
[9]
Sritharadol, R.; Nakpheng, T.; Wan Sia Heng, P.; Srichana, T. Development of a topical mupirocin spray for antibacterial and wound-healing applications. Drug Dev. Ind. Pharm., 2017, 43(10), 1715-1728.
[http://dx.doi.org/10.1080/03639045.2017.1339077] [PMID: 28581830]
[10]
Tintino, S.R.; Souza, V.C.A. Vitamin K enhances the effect of antibiotics inhibiting the efflux pumps of Staphylococcus aureus strains. Med. Chem. Res., 2020, 10(6), 130.
[11]
Negi, N.; Prakash, P.; Gupta, M.L.; Mohapatra, T.M. Possible role of curcumin as ection an efflux pump inhibitor in multi drug resistant clinical isolates of pseudomonas aeruginosa. J. Clin. Diagn. Res., 2014, 8(10), DC04-DC07.
[http://dx.doi.org/10.7860/JCDR/2014/8329.4965] [PMID: 25478340]
[12]
Osei Sekyere, J.; Amoako, D.G. Carbonyl cyanide m-chlorophenylhydrazine (CCCP) reverses resistance to colistin, but not to carbapenems and tigecycline in multidrug-resistant enterobacteriaceae. Front. Microbiol., 2017, 8, 228.
[http://dx.doi.org/10.3389/fmicb.2017.00228] [PMID: 28261184]
[13]
Lomovskaya, O.; Warren, M.S.; Lee, A.; Galazzo, J.; Fronko, R.; Lee, M.; Blais, J.; Cho, D.; Chamberland, S.; Renau, T.; Leger, R.; Hecker, S.; Watkins, W.; Hoshino, K.; Ishida, H.; Lee, V.J. Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: Novel agents for combination therapy. Antimicrob. Agents Chemother., 2001, 45(1), 105-116.
[http://dx.doi.org/10.1128/AAC.45.1.105-116.2001] [PMID: 11120952]
[14]
Jang, S. Multidrug efflux pumps in Staphylococcus aureus and their clinical implications. J. Microbiol., 2016, 54(1), 1-8.
[http://dx.doi.org/10.1007/s12275-016-5159-z] [PMID: 26727895]
[15]
Fiamegos, Y.C.; Kastritis, P.L.; Exarchou, V.; Han, H.; Bonvin, A.M.J.J.; Vervoort, J.; Lewis, K.; Hamblin, M.R.; Tegos, G.P. Antimicrobial and efflux pump inhibitory activity of caffeoylquinic acids from Artemisia absinthium against gram-positive pathogenic bacteria. PLoS One, 2011, 6(4), e18127.
[http://dx.doi.org/10.1371/journal.pone.0018127] [PMID: 21483731]
[16]
Lipsky, B.A.; Hoey, C. Topical antimicrobial therapy for treating chronic wounds. Clin. Infect. Dis., 2009, 49(10), 1541-1549.
[http://dx.doi.org/10.1086/644732] [PMID: 19842981]
[17]
Shettigar, K.; Murali, T.S. Virulence factors and clonal diversity of Staphylococcus aureus in colonization and wound infection with emphasis on diabetic foot infection. Eur. J. Clin. Microbiol. Infect. Dis., 2020, 39(12), 2235-2246.
[http://dx.doi.org/10.1007/s10096-020-03984-8] [PMID: 32683595]
[18]
Ramirez-Acuña, J.M.; Cardenas-Cadena, S.A.; Marquez-Salas, P.A.; Garza-Veloz, I.; Perez-Favila, A.; Cid-Baez, M.A.; Flores-Morales, V.; Martinez-Fierro, M.L. Diabetic foot ulcers: Current advances in antimicrobial therapies and emerging treatments. Antibiotics, 2019, 8(4), 193.
[http://dx.doi.org/10.3390/antibiotics8040193] [PMID: 31652990]
[19]
Siddiqui, A.R.; Bernstein, J.M. Chronic wound infection: Facts and controversies. Clin. Dermatol., 2010, 28(5), 519-526.
[http://dx.doi.org/10.1016/j.clindermatol.2010.03.009] [PMID: 20797512]
[20]
Idomir, M.; Pirau, R.; Nemet, C. Evaluation of microbiological spectrum of burn wound infections. Bull. Transilv. Univ. Bras., 2012, 1(54), 247-254.
[21]
Shahzad, M.N.; Ahmed, N.; Khan, I.H.; Mirza, A.B.; Waheed, F. Bacterial profile of burn wound infections in burn patients. Ann. Pak. Inst. Med. Sci., 2012, 8(1), 54-57.
[22]
Sarheed, O.; Ahmed, A.; Shouqair, D.; Boateng, J. Antimicrobial dressings for improving wound healing. In: Wound healing-Newinsights into Ancient Challenges; Intech open: London, UK, 2016; p. 373-398.
[http://dx.doi.org/10.5772/63961]
[23]
Hasan, R.; Acharjee, M.; Noor, R. Prevalence of vancomycin resistant Staphylococcus aureus (VRSA) in methicillin resistant S. aureus (MRSA) strains isolated from burn wound infections. Tzu-Chi Med. J., 2016, 28(2), 49-53.
[http://dx.doi.org/10.1016/j.tcmj.2016.03.002] [PMID: 28757721]
[24]
Joshi, P.; Singh, S.; Wani, A.; Sharma, S.; Jain, S.K.; Singh, B.; Gupta, B.D.; Satti, N.K.; Koul, S.; Khan, I.A.; Kumar, A.; Bharate, S.B.; Vishwakarma, R.A. Osthol and curcumin as inhibitors of human Pgp and multidrug efflux pumps of Staphylococcus aureus: Reversing the resistance against frontline antibacterial drugs. Med. Chem. Comm., 2014, 5(10), 1540-1547.
[http://dx.doi.org/10.1039/C4MD00196F]
[25]
Shehreen, S; Chyou, T-y; Fineran, PC Brown, CM Genome-wide correlation analysis suggests different roles of CRISPR-Cas systems in the acquisition of antibiotic resistance genes in diverse species. PHILOS T R SOC B., 2019, 374(1772), 20180384.
[26]
Serra, R.; Grande, R.; Butrico, L.; Rossi, A.; Settimio, U.F.; Caroleo, B.; Amato, B.; Gallelli, L.; de Franciscis, S. Chronic wound infections: The role of Pseudomonas aeruginosa and Staphylococcus aureus. Expert Rev. Anti Infect. Ther., 2015, 13(5), 605-613.
[http://dx.doi.org/10.1586/14787210.2015.1023291] [PMID: 25746414]
[27]
Hussein, M.; Karas, J.A.; Schneider-Futschik, E.K.; Chen, F.; Swarbrick, J.; Paulin, O.K.A.; Hoyer, D.; Baker, M.; Zhu, Y.; Li, J.; Velkov, T. The killing mechanism of teixobactin against methicillin-resistant Staphylococcus aureus: An untargeted metabolomics study. mSystems, 2020, 5(3), e00077-20.
[http://dx.doi.org/10.1128/mSystems.00077-20] [PMID: 32457238]
[28]
Spizek, J.; Rezanka, T. Lincosamides: Chemical structure, biosynthesis, mechanism of action, resistance, and applications. Biochem. Pharmacol., 2016, 133, 20-28.
[PMID: 27940264]
[29]
Lal, J.; Gupta, S.K.; Thavaselvam, D.; Agarwal, D.D. Biological activity, design, synthesis and structure activity relationship of some novel derivatives of curcumin containing sulfonamides. Eur. J. Med. Chem., 2013, 64, 579-588.
[http://dx.doi.org/10.1016/j.ejmech.2013.03.012] [PMID: 23685942]
[30]
Leaper, D.; Assadian, O.; Edmiston, C.E. Approach to chronic wound infections. Br. J. Dermatol., 2015, 173(2), 351-358.
[http://dx.doi.org/10.1111/bjd.13677] [PMID: 25772951]
[31]
Gonzalez, J.R.; Merana, G.R.; Scharschmidt, T.C. Hair of the mouse: A skin bacteria “cocktail” gets follicles back on their feet. Cell Host Microbe, 2021, 29(5), 742-744.
[http://dx.doi.org/10.1016/j.chom.2021.04.011] [PMID: 33984276]
[32]
Thompson, M.G.; Truong-Le, V.; Alamneh, Y.A.; Black, C.C.; Anderl, J.; Honnold, C.L.; Pavlicek, R.L.; Abu-Taleb, R.; Wise, M.C.; Hall, E.R.; Wagar, E.J.; Patzer, E.; Zurawski, D.V. Evaluation of gallium citrate formulations against a multidrug-resistant strain of Klebsiella pneumoniae in a murine wound model of infection. Antimicrob. Agents Chemother., 2015, 59(10), 6484-6493.
[http://dx.doi.org/10.1128/AAC.00882-15] [PMID: 26239978]
[33]
Tan, L.; Zhou, Z.; Liu, X.; Li, J.; Zheng, Y.; Cui, Z.; Yang, X.; Liang, Y.; Li, Z.; Feng, X.; Zhu, S.; Yeung, K.W.K.; Yang, C.; Wang, X.; Wu, S. Overcoming multidrug‐resistant MRSA using conventional aminoglycoside antibiotics. Adv. Sci., 2020, 7(9), 1902070.
[http://dx.doi.org/10.1002/advs.201902070] [PMID: 32382474]
[34]
Uribe, R.V.; Rathmer, C.; Jahn, L.J.; Ellabaan, M.M.H.; Li, S.S.; Sommer, M.O.A. Bacterial resistance to CRISPR-Cas antimicrobials. Sci. Rep., 2021, 11(1), 17267.
[http://dx.doi.org/10.1038/s41598-021-96735-4] [PMID: 34446818]
[35]
Guo, Y.; Song, G.; Sun, M.; Wang, J.; Wang, Y. Prevalence and therapies of antibiotic-resistance in staphylococcus aureus. Front. Cell. Infect. Microbiol., 2020, 10, 107.
[http://dx.doi.org/10.3389/fcimb.2020.00107] [PMID: 32257966]
[36]
Louis, B.R. Mechanism of resistance to antibacterial agents. In: Antimicrobial Stewardship: Principles and Practice; CABI: wallingford, UK, 2017; 5, p. 39-52.
[37]
Shabbir, M.A.B.; Shabbir, M.Z.; Wu, Q.; Mahmood, S.; Sajid, A.; Maan, M.K.; Ahmed, S.; Naveed, U.; Hao, H.; Yuan, Z. CRISPR-cas system: Biological function in microbes and its use to treat antimicrobial resistant pathogens. Ann. Clin. Microbiol. Antimicrob., 2019, 18(1), 21.
[http://dx.doi.org/10.1186/s12941-019-0317-x] [PMID: 31277669]
[38]
Ibrahim, W.H.; Makhlouf, A.M.; Khamis, M.A.; Youness, E.M. Effect of prophylactic antibiotics (Cephalosporin versus Amoxicillin) on preventing post caesarean section infection. Am. J. Sci., 2011, 7(5), 178-187.
[39]
Foster, T.J. Antibiotic resistance in Staphylococcus aureus. current status and future prospects. FEMS Microbiol. Rev., 2017, 41(3), 430-449.
[http://dx.doi.org/10.1093/femsre/fux007] [PMID: 28419231]
[40]
Wani, T.A.; Chandrashekara, H.H.; Kumar, D.; Prasad, R.; Gopal, A.; Sardar, K.K.; Tandan, S.K.; Kumar, D. Wound healing activity of ethanolic extract of Shorea robusta Gaertn resin. Indian J. Exp. Biol., 2012, 50(4), 277-281.
[PMID: 22611916]
[41]
Okur, M.E.; Ayla, Ş.; Yozgatlı, V.; Aksu, N.B.; Yoltaş, A.; Orak, D.; Sipahi, H.; Üstündağ, O.N. Evaluation of burn wound healing activity of novel fusidic acid loaded microemulsion based gel in male Wistar albino rats. Saudi Pharm. J., 2020, 28(3), 338-348.
[http://dx.doi.org/10.1016/j.jsps.2020.01.015] [PMID: 32194336]
[42]
Siyumbwa, S.N.; Ekeuku, S.O.; Amini, F.; Emerald, N.M.; Sharma, D.; Patrick, N.O. Wound healing and antibacterial activities of 2-pentadecanone in streptozotocin-induced type 2 diabetic rats. Pharmacogn. Mag., 2019, 15(62), 71-77.
[43]
De Silva, C.C.; Israni, N.; Zanwar, A.; Jagtap, A.; Leophairatana, P.; Koberstein, J.T.; Modak, S.M. “Smart” polymer enhances the efficacy of topical antimicrobial agents. Burns, 2019, 45(6), 1418-1429.
[http://dx.doi.org/10.1016/j.burns.2019.04.013] [PMID: 31230802]
[44]
Griffith, E.C.; Wallace, M.J.; Wu, Y.; Kumar, G.; Gajewski, S.; Jackson, P.; Phelps, G.A.; Zheng, Z.; Rock, C.O.; Lee, R.E.; White, S.W. The structural and functional basis for recurring sulfa drug resistance mutations in Staphylococcus aureus dihydropteroate synthase. Front. Microbiol., 2018, 9, 1369.
[http://dx.doi.org/10.3389/fmicb.2018.01369] [PMID: 30065703]
[45]
Tal-Gan, Y.; Stacy, D.M.; Foegen, M.K.; Koenig, D.W.; Blackwell, H.E. Highly potent inhibitors of quorum sensing in Staphylococcus aureus revealed through a systematic synthetic study of the group-III autoinducing peptide. J. Am. Chem. Soc., 2013, 135(21), 7869-7882.
[http://dx.doi.org/10.1021/ja3112115] [PMID: 23647400]
[46]
Broderick, A.H.; Stacy, D.M.; Tal-Gan, Y.; Kratochvil, M.J.; Blackwell, H.E.; Lynn, D.M. Surface coatings that promote rapid release of peptide-based AgrC inhibitors for attenuation of quorum sensing in Staphylococcus aureus. Adv. Healthc. Mater., 2014, 3(1), 97-105.
[http://dx.doi.org/10.1002/adhm.201300119] [PMID: 23813683]
[47]
Yu, D.; Zhao, L.; Xue, T.; Sun, B. Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiol., 2012, 12(1), 288.
[http://dx.doi.org/10.1186/1471-2180-12-288] [PMID: 23216979]
[48]
Tang, J.; Guan, H.; Dong, W.; Liu, Y.; Dong, J.; Huang, L. Application of compound polymyxin b ointment in the treatment of chronic refractory wounds. Int. J. Low. Extrem. Wounds, 2020, 153473462094451, 1-5.
[PMID: 32734789]
[49]
Chang, V.S.; Dhaliwal, D.K.; Raju, L.; Kowalski, R.P. Antibiotic resistance in the treatment of staphylococcus aureus keratitis. Cornea, 2015, 34(6), 698-703.
[http://dx.doi.org/10.1097/ICO.0000000000000431] [PMID: 25811722]
[50]
Venter, H.; Mowla, R.; Ohene-Agyei, T.; Ma, S. RND-type drug efflux pumps from Gram-negative bacteria: Molecular mechanism and inhibition. Front. Microbiol., 2015, 6, 377.
[http://dx.doi.org/10.3389/fmicb.2015.00377] [PMID: 25972857]
[51]
Costa, S.S.; Viveiros, M.; Amaral, L.; Couto, I. Multidrug efflux pumps in Staphylococcus aureus: An update. Open Microbiol. J., 2013, 7(1), 59-71.
[http://dx.doi.org/10.2174/1874285801307010059] [PMID: 23569469]
[52]
Rezende-Júnior, L.M.; Andrade, L.M.S.; Leal, A.L.A.B.; Mesquita, A.B.S.; Santos, A.L.P.A.; Neto, J.S.L.; Siqueira-Júnior, J.P.; Nogueira, C.E.S.; Kaatz, G.W.; Coutinho, H.D.M.; Martins, N.; da Rocha, C.Q.; Barreto, H.M. Chalcones isolated from Arrabidaea brachypoda flowers as inhibitors of nora and mepa multidrug efflux pumps of Staphylococcus aureus. Antibiotics, 2020, 9(6), 351.
[http://dx.doi.org/10.3390/antibiotics9060351] [PMID: 32575738]
[53]
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]
[54]
Rodriguez-Cerdeira, C; Sanchez-Blanco, E; Molares-Vila, A Clinical application of development of nonantibiotic macrolides that correct inflammation-driven immune dysfunction in inflammatory skin diseases. Mediat. Inflamm., 2012, 1-16. Available from: https://www.hindawi.com/journals/mi/2012/563709/
[http://dx.doi.org/10.1155/2012/563709]
[55]
Farmer, N.; Hodgetts-Morton, V.; Morris, R.K. Are prophylactic adjunctive macrolides efficacious against caesarean section surgical site infection: A systematic review and meta-analysis. Eur. J. Obstet. Gynecol. Reprod. Biol., 2020, 244, 163-171.
[http://dx.doi.org/10.1016/j.ejogrb.2019.11.026] [PMID: 31810022]
[56]
Arampatzioglou, A.; Papazoglou, D.; Konstantinidis, T.; Chrysanthopoulou, A.; Mitsios, A.; Angelidou, I.; Maroulakou, I.; Ritis, K.; Skendros, P. Clarithromycin enhances the antibacterial activity and wound healing capacity in type 2 diabetes mellitus by increasing LL-37 load on neutrophil extracellular traps. Front. Immunol., 2018, 9, 2064.
[http://dx.doi.org/10.3389/fimmu.2018.02064] [PMID: 30250474]
[57]
Licht, A.; Schneider, E. ATP binding cassette systems: Structures, mechanisms, and functions. Cent. Eur. J. Biol., 2011, 6(5), 785-801.
[58]
Umeh, V.N.; Ilodigwe, E.E.; Ajaghaku, D.L.; Erhirhie, E.O.; Moke, G.E.; Akah, P.A. Wound-healing activity of the aqueous leaf extract and fractions of Ficus exasperata (Moraceae) and its safety evaluation on albino rats. J. Tradit. Complement. Med., 2014, 4(4), 246-252.
[http://dx.doi.org/10.4103/2225-4110.139105] [PMID: 25379466]
[59]
Yoshida, Y.; Matsuo, M.; Oogai, Y.; Kato, F.; Nakamura, N.; Sugai, M.; Komatsuzawa, H. Bacitracin sensing and resistance in Staphylococcus aureus. FEMS Microbiol. Lett., 2011, 320(1), 33-39.
[http://dx.doi.org/10.1111/j.1574-6968.2011.02291.x] [PMID: 21517944]
[60]
Bouarab-Chibane, L.; Forquet, V.; Lantéri, P.; Clément, Y.; Léonard-Akkari, L.; Oulahal, N.; Degraeve, P.; Bordes, C. Antibacterial properties of polyphenols: Characterization and QSAR (quantitative structure-activity relationship) models. Front. Microbiol., 2019, 10, 829.
[http://dx.doi.org/10.3389/fmicb.2019.00829] [PMID: 31057527]
[61]
Espinoza, J.; Urzúa, A.; Sanhueza, L.; Walter, M.; Fincheira, P.; Muñoz, P.; Mendoza, L.; Wilkens, M. Essential oil, extracts, and sesquiterpenes obtained from the heartwood of Pilgerodendron uviferum act as potential inhibitors of the staphylococcus aureus nora multidrug efflux pump. Front. Microbiol., 2019, 10, 337.
[http://dx.doi.org/10.3389/fmicb.2019.00337] [PMID: 30863385]
[62]
Braga, R.A.M.; Sousa, J.N.; Costa, L.M.; Oliveira, F.A.A.; dos Santos, R.C.; Silva, N.A.S.; da Silva, W.O.; Marques, C.P.J.; de Sousa, L.N.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]
[63]
Bame, J.; Graf, T.; Junio, H.; Bussey, R., III; Jarmusch, S.; El-Elimat, T.; Falkinham, J., III; Oberlies, N.; Cech, R.; Cech, N. Sarothrin from Alkanna orientalis is an antimicrobial agent and efflux pump inhibitor. Planta Med., 2013, 79(5), 327-329.
[http://dx.doi.org/10.1055/s-0032-1328259] [PMID: 23468310]
[64]
Roy, S.K.; Kumari, N.; Pahwa, S.; Agrahari, U.C.; Bhutani, K.K.; Jachak, S.M.; Nandanwar, H. 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]
[65]
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]
[66]
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]
[67]
Bazzaz, B.S.F.; Memariani, Z.; Khashiarmanesh, Z.; Iranshahi, M.; Naderinasab, M. Effect of galbanic acid, a sesquiterpene coumarin from Ferula szowitsiana, as an inhibitor of efflux mechanism in resistant clinical isolates of Staphylococcus aureus. Braz. J. Microbiol., 2010, 41(3), 574-580.
[http://dx.doi.org/10.1590/S1517-83822010000300006] [PMID: 24031531]
[68]
Ponnusamy, K.; Ramasamy, M.; Savarimuthu, I.; Paulraj, M.G. Indirubin potentiates ciprofloxacin activity in the NorA efflux pump of Staphylococcus aureus. Scand. J. Infect. Dis., 2010, 42(6-7), 500-505.
[http://dx.doi.org/10.3109/00365541003713630] [PMID: 20380543]
[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, M.F.V.; 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]
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]
[72]
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]
[73]
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]
[74]
Belofsky, G.; Carreno, R.; Lewis, K.; Ball, A.; Casadei, G.; Tegos, G.P. Metabolites of the “smoke tree”, Dalea spinosa, potentiate antibiotic activity against multidrug-resistant Staphylococcus aureus. J. Nat. Prod., 2006, 69(2), 261-264.
[http://dx.doi.org/10.1021/np058057s] [PMID: 16499327]
[75]
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]
[76]
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]
[77]
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]
[78]
Oluwatuyi, M.; Kaatz, G.; Gibbons, S. Antibacterial and resistance modifying activity of. Phytochemistry, 2004, 65(24), 3249-3254.
[http://dx.doi.org/10.1016/j.phytochem.2004.10.009] [PMID: 15561190]
[79]
Stermitz, F.R.; Cashman, K.K.; Halligan, K.M.; Morel, C.; Tegos, G.P.; Lewis, K. Polyacylated neohesperidosides From Geranium caespitosum: Bacterial multidrug resistance pump inhibitors. Bioorg. Med. Chem. Lett., 2003, 13(11), 1915-1918.
[http://dx.doi.org/10.1016/S0960-894X(03)00316-0] [PMID: 12749897]
[80]
Morel, C.; Stermitz, F.R.; Tegos, G.; Lewis, K. Isoflavones as potentiators of antibacterial activity. J. Agric. Food Chem., 2003, 51(19), 5677-5679.
[http://dx.doi.org/10.1021/jf0302714] [PMID: 12952418]
[81]
Stermitz, F.R.; Scriven, L.N.; Tegos, G.; Lewis, K. Two flavonols from Artemisa annua which potentiate the activity of berberine and norfloxacin against a resistant strain of Staphylococcus aureus. Planta Med., 2002, 68(12), 1140-1141.
[http://dx.doi.org/10.1055/s-2002-36347] [PMID: 12494348]
[82]
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]
[83]
De Araujo, A.C.J.; Freitas, P.R.; Barbosa, C.R.D.S.; Muniz, D.F.; De Almeida, R.S. In vitro and in silico inhibition of staphylococcus aureus efflux pump nor a by α-pinene and limonene. Curr. Microbiol., 2021, 78, 3388-3393.
[http://dx.doi.org/10.1007/s00284-021-02611-9] [PMID: 34268598]
[84]
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]
[85]
Cabral, V.; Luo, X.; Junqueira, E.; Costa, S.S.; Mulhovo, S.; Duarte, A.; Couto, I.; Viveiros, M.; Ferreira, M.J.U. Enhancing activity of antibiotics against Staphylococcus aureus: Zanthoxylum capense constituents and derivatives. Phytomedicine, 2015, 22(4), 469-476.
[http://dx.doi.org/10.1016/j.phymed.2015.02.003] [PMID: 25925969]
[86]
Kincses, A.; Varga, B.; Csonka, Á.; Sancha, S.; Mulhovo, S.; Madureira, A.M.; Ferreira, M.J.U.; Spengler, G. Bioactive compounds from the African medicinal plant Cleistochlamys kirkii as resistance modifiers in bacteria. Phytother. Res., 2018, 32(6), 1039-1046.
[http://dx.doi.org/10.1002/ptr.6042] [PMID: 29464798]
[87]
Ramalhete, C.; Spengler, G.; Martins, A.; Martins, M.; Viveiros, M.; Mulhovo, S.; Ferreira, M.J.U.; Amaral, L. Inhibition of efflux pumps in meticillin-resistant Staphylococcus aureus and Enterococcus faecalis resistant strains by triterpenoids from Momordica balsamina. Int. J. Antimicrob. Agents, 2011, 37(1), 70-74.
[http://dx.doi.org/10.1016/j.ijantimicag.2010.09.011] [PMID: 21075604]
[88]
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]
[89]
Gibbons, S.; Udo, E.E. 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., 2000, 14(2), 139-140.
[http://dx.doi.org/10.1002/(SICI)1099-1573(200003)14:2<139:AID-PTR608>3.0.CO;2-8] [PMID: 10685116]
[90]
Kakarla, P.; Floyd, J.; Mukherjee, M.; Devireddy, A.R.; Inupakutika, M.A.; Ranweera, I.; Kc, R. ‘Shrestha, U.; Cheeti, U.R.; Willmon, T.M.; Adams, J.; Bruns, M.; Gunda, S.K.; Varela, M.F. Inhibition of the multidrug efflux pump LmrS from Staphylococcus aureus by cumin spice Cuminum cyminum. Arch. Microbiol., 2017, 199(3), 465-474.
[http://dx.doi.org/10.1007/s00203-016-1314-5] [PMID: 27830269]
[91]
Seukep, A.J.; Kuete, V.; Nahar, L.; Sarker, S.D.; Guo, M. Plant-derived secondary metabolites as the main source of efflux pump inhibitors and methods for identification. J. Pharm. Anal., 2020, 10(4), 277-290.
[http://dx.doi.org/10.1016/j.jpha.2019.11.002] [PMID: 32923005]
[92]
Almeida, R.S.; Freitas, P.R.; Araújo, A.C.J.; Alencar Menezes, I.R.; Santos, E.L.; Tintino, S.R.; Moura, T.F.; Filho, J.R.; Ferreira, V.A.; Silva, A.C.A.; Silva, L.E.; do Amaral, W.; Deschamps, C.; Iriti, M.; Melo Coutinho, H.D. GC-MS profile and enhancement of antibiotic activity by the essential oil of Ocotea odorífera and safrole: Inhibition of Staphylococcus aureus efflux pumps. Antibiotics, 2020, 9(5), 247.
[http://dx.doi.org/10.3390/antibiotics9050247] [PMID: 32408576]
[93]
Marquez, B.; Neuville, L.; Moreau, N.J.; Genet, J.P.; dos Santos, A.F.; Caño de Andrade, M.C.; Sant’Ana, G.A.E. 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]
[94]
Fung, K.P.; Han, Q.B.; Ip, M.; Yang, X.S.; Lau, C.B.S.; Chan, B.C.L. Synergists from Portulaca oleracea with macrolides against methicillin-resistant Staphylococcus aureus and related mechanism. Hong Kong Med. J., 2017, 23(4), 38-42.
[PMID: 28943525]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy