Repurposing approved drugs as potential efflux pump inhibitors in multidrug-resistant Pseudomonas aeruginosa

References

• Murray CJ, Ikuta KS, Sharara F et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 399(10325), 629–655 (2022).
   PubMed Web of Science ®Google Scholar
• Azam MW, Khan AU. Updates on the pathogenicity status of Pseudomonas aeruginosa. Drug Discov. Today 24(1), 350–359 (2019).
   PubMed Web of Science ®Google Scholar
• Horcajada JP, Montero M, Oliver A et al. Epidemiology and treatment of multidrug-resistant and extensively drug-resistant Pseudomonas aeruginosa infections. Clin. Microbiol. Rev. 32(4), e00031-19 (2019).
   PubMed Web of Science ®Google Scholar
• Lister PD, Wolter DJ, Hanson ND. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin. Microbiol. Rev. 22(4), 582–610 (2009).
   PubMed Web of Science ®Google Scholar
• Gellatly SL, Hancock REW. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog. Dis. 67(3), 159–173 (2013).
   PubMed Web of Science ®Google Scholar
• Pan YP, Xu YH, Wang ZX, Fang YP, Shen JL. Overexpression of MexAB-OprM efflux pump in carbapenem-resistant Pseudomonas aeruginosa. Arch. Microbiol. 198(6), 565–571 (2016).
   PubMed Web of Science ®Google Scholar
• Islamieh DI, Afshar D, Yousefi M, Esmaeili D. Efflux pump inhibitors derived from natural sources as novel antibacterial agents against Pseudomonas aeruginosa: a review. Int. J. Med. Rev. 5(3), 94–105 (2018).
   Google Scholar
• Lorusso AB, Carrara JA, Barroso CDN, Tuon FF, Faoro H. Role of efflux pumps on antimicrobial resistance in Pseudomonas aeruginosa. Int. J. Mol. Sci. 23(24), 1–21 (2022).
   Web of Science ®Google Scholar
• Sharma A, Gupta VK, Pathania R. Efflux pump inhibitors for bacterial pathogens: from bench to bedside. Indian J. Med. Res. 149(2), 129–145 (2019).
   PubMed Web of Science ®Google Scholar
• Blanco P, Sanz-García F, Hernando-Amado S, Martínez JL, Alcalde-Rico M. The development of efflux pump inhibitors to treat Gram-negative infections. Expert Opin. Drug Discov. 13(10), 919–931 (2018).
   PubMed Web of Science ®Google Scholar
• Aron Z, Opperman TJ. Optimization of a novel series of pyranopyridine RND efflux pump inhibitors. Curr. Opin. Microbiol. 33, 1–6 (2016).
   PubMed Web of Science ®Google Scholar
• Sidrim JJC, Vasconcelos DC, Riello GB et al. Promethazine improves antibiotic efficacy and disrupts biofilms of Burkholderia pseudomallei. Biofouling 33(1), 88–97 (2017).
   PubMed Web of Science ®Google Scholar
• Nzakizwanayo J, Scavone P, Jamshidi S et al. Fluoxetine and thioridazine inhibit efflux and attenuate crystalline biofilm formation by Proteus mirabilis. Sci. Rep. 7(12222), 1–14 (2017).
   PubMedGoogle Scholar
• Brilhante RSN, Oliveira JS, Evangelista AJJ et al. In vitro effects of promethazine on cell morphology and structure and mitochondrial activity of azole-resistant Candida tropicalis. Med. Mycol. 56(8), 1012–1022 (2018).
   PubMed Web of Science ®Google Scholar
• Cordeiro RDA, Portela FV, Pereira LM et al. Efflux pump inhibition controls growth and enhances antifungal susceptibility of Fusarium solani species complex. Future Microbiol. 15(1), 9–20 (2020).
   PubMed Web of Science ®Google Scholar
• Sousa AK, Rocha JE, Souza TG, Freitas TS, Ribeiro-Filho J, Coutinho HDM. New roles of fluoxetine in pharmacology: antibacterial effect and modulation of antibiotic activity. Microb. Pathog. 123, 368–371 (2018).
   PubMed Web of Science ®Google Scholar
• Magiorakos AP, Srinivasan A, Carey RB et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18(3), 268–281 (2012).
   PubMed Web of Science ®Google Scholar
• M-100 Performance Standards for Antimicrobial Susceptibility Testing; Standards M02, M07 and M11 (13th Edition). Clinical and Laboratory Standards Institute M100. Clinical and Laboratory Standards Institute, Wayne, PA (2021).
   Google Scholar
• Stepanović S, Vuković D, Hola V et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115(8), 891–899 (2007).
   PubMed Web of Science ®Google Scholar
• Lehtinen J, Lilius EM. Promethazine renders Escherichia coli susceptible to penicillin G: real-time measurement of bacterial susceptibility by fluoro-luminometry. Int. J. Antimicrob. Agents 30(1), 44–51 (2007).
   PubMed Web of Science ®Google Scholar
• Varga B, Csonka Á, Csonka A, Molnár J, Amaral L, Spengler G. Possible biological and clinical applications of phenothiazines. Anticancer Res. 37(11), 5983–5993 (2017).
   PubMed Web of Science ®Google Scholar
• Ying YC, Yong MO, Kim LC. Synergistic interaction between phenothiazines and antimicrobial agents against Burkholderia pseudomallei. Antimicrob. Agents Chemother. 51(2), 623–630 (2007).
   PubMed Web of Science ®Google Scholar
• Sousa AK, Rocha JE, Souza TG, Freitas TS, Ribeiro-Filho J, Coutinho HDM. New roles of fluoxetine in pharmacology: antibacterial effect and modulation of antibiotic activity. Microb. Pathog. 123, 368–371 (2018).
   PubMed Web of Science ®Google Scholar
• Tekintaş Y, Temel A, Ateş A et al. Antifungal and antibiofilm activities of selective serotonin reuptake inhibitors alone and in combination with fluconazole. Turk. J. Pharm. Sci. 17(6), 667–672 (2020).
   PubMed Web of Science ®Google Scholar
• Al Rashed N, Joji RM, Saeed NK, Bindayna KM. Detection of overexpression of efflux pump expression in fluoroquinolone-resistant Pseudomonas aeruginosa isolates. Int. J. Appl. Basic Med. Res. 10(1), 37–42 (2020).
   PubMedGoogle Scholar
• Fanélus I, Desrosiers RR. Mitochondrial uncoupler carbonyl cyanide M-chlorophenylhydrazone induces the multimer assembly and activity of repair enzyme protein L-isoaspartyl methyltransferase. J. Mol. Neurosci. 50(3), 411–423 (2013).
   PubMed Web of Science ®Google Scholar
• Rehman A, Patrick WM, Lamont IL. Mechanisms of ciprofloxacin resistance in Pseudomonas aeruginosa: new approaches to an old problem. J. Med. Microbiol. 68(1), 1–10 (2019).
   PubMed Web of Science ®Google Scholar
• Zahedi Bialvaei A, Rahbar M, Hamidi-Farahani R et al. Expression of RND efflux pumps mediated antibiotic resistance in Pseudomonas aeruginosa clinical strains. Microb. Pathog. 153, 104789 (2021).
   PubMed Web of Science ®Google Scholar
• Davin-Regli A, Pages JM, Ferrand A. Clinical status of efflux resistance mechanisms in gram-negative bacteria. Antibiotics (Basel) 10(9), 1–23 (2021).
   Web of Science ®Google Scholar
• Huang L, Wu C, Gao H et al. Bacterial multidrug efflux pumps at the frontline of antimicrobial resistance: an overview. Antibiotics (Basel) 11(4), 1–18 (2022).
   Web of Science ®Google Scholar
• Fiallos NM, Aguiar ALR, Silva BN et al. The potential of phenothiazines against endodontic pathogens: a focus on Enterococcus–Candida dual-species biofilm. Antibiotics (Basel) 11(11), 1–13 (2022).
   Web of Science ®Google Scholar
• Ikonomidis A, Tsakris A, Kanellopoulou M, Maniatis AN, Pournaras S. Effect of the proton motive force inhibitor carbonyl cyanide-m-chlorophenylhydrazone (CCCP) on Pseudomonas aeruginosa biofilm development. Lett. Appl. Microbiol. 47(4), 298–302 (2008).
   PubMed Web of Science ®Google Scholar
• Oliveira AS, Martinez-de-Oliveira J, Donders GGG, Palmeira-de-Oliveira R, Palmeira-de-Oliveira A. Anti-Candida activity of antidepressants sertraline and fluoxetine: effect upon pre-formed biofilms. Med. Microbiol. Immunol. 207(3–4), 195–200 (2018).
   PubMed Web of Science ®Google Scholar
• Alav I, Sutton M, Rahman KM. Role of bacterial efflux pumps in biofilm formation. J. Antimicrob. Chemother. 73(8), 2003–2020 (2018).
   PubMed Web of Science ®Google Scholar
• Sirijant N, Sermswan RW, Wongratanacheewin S. Burkholderia pseudomallei resistance to antibiotics in biofilm induced conditions is related to efflux pumps. J. Med. Microbiol. 65(11), 1296–1306 (2016).
   PubMedGoogle Scholar
• Sidrim JJC, Amando BR, Gomes FIF et al. Chlorpromazine-impregnated catheters as a potential strategy to control biofilm-associated urinary tract infections. Future Microbiol. 14(12), 1023–1034 (2019).
   PubMed Web of Science ®Google Scholar
• Blair JMA, Piddock LJV. How to measure export via bacterial multidrug resistance efflux pumps. mBio 7(4), 1–6 (2016).
   Web of Science ®Google Scholar