Antifungal Activity of Cisatracurium Against Fluconazole-Resistant Candida Isolates and its Antibiofilm Effects

References

• Bongomin F , GagoS , OladeleRO , DenningDW. Global and multi-national prevalence of fungal diseases–estimate precision. J. Fungi3(4), 57 (2017).
   Web of Science ®Google Scholar
• Firacative C . Invasive fungal disease in humans: are we aware of the real impact?Mem. Inst. Oswaldo Cruz115(9), e200430 (2020).
   PubMedGoogle Scholar
• Motta AL , de AlmeidaGMD , deAlmeida Júnior JN , BurattiniMN , RossiF. Candidemia epidemiology and susceptibility profile in the largest Brazilian teaching hospital complex. Braz. J. Infect. Dis.14(5), 441–448 (2010).
   PubMed Web of Science ®Google Scholar
• Carmona EM , LimperAH. Overview of treatment approaches for fungal infections. Clin. Chest Med.38(3), 393–402 (2017).
   PubMed Web of Science ®Google Scholar
• Wiederhold NP . Antifungal resistance: current trends and future strategies to combat. Infect. Drug Resist.10, 249–259 (2017).
   PubMed Web of Science ®Google Scholar
• Revie NM , IyerKR , RobbinsN , CowenLE. Antifungal drug resistance: evolution, mechanisms and impact. Curr. Opin. Microbiol.45, 70–76 (2018).
   PubMed Web of Science ®Google Scholar
• Del Pozo JL . Biofilm-related disease. Expert Rev. Anti. Infect. Ther.16(1), 51–65 (2018).
   PubMed Web of Science ®Google Scholar
• Winter MB , SalcedoEC , LohseMBet al. Global identification of biofilm-specific proteolysis in Candida albicans. MBio7(5), 10.1128/mbio.01514-16 (2016).
   Web of Science ®Google Scholar
• Foletto VS , SerafinMB , da RosaTFet al. Fluoxetine and paroxetine: repositioning as a therapeutic alternative in the treatment of various diseases. Am. J. Ther.27(5), e547–e551 (2020).
   PubMed Web of Science ®Google Scholar
• Liu N , TuJ , DongG , WangY , ShengC. Emerging new targets for the treatment of resistant fungal infections. J. Med. Chem.61(13), 5484–5511 (2018).
   PubMed Web of Science ®Google Scholar
• Pappas PG , KauffmanCA , AndesDRet al. Clinical Practice Guideline for the Management of Candidiasis: 2016 Update by the Infectious Diseases Society of America. Clin. Infect. Dis.62(4), e1–e50 (2015).
   PubMedGoogle Scholar
• Acharya N , ManoharK , NayakS , ChatterjeeA , DaleiA. DNA polymerase: a putative drug target against candidiasis. Front. Life Sci. (August), 12–22 (2016).
   Google Scholar
• Huang CY , ChenYC , Wu-HsiehBA , FangJM , ChangZF. The Ca-loop in thymidylate kinase is critical for growth and contributes to pyrimidine drug sensitivity of Candida albicans. J. Biol. Chem.294(27), 10686–10697 (2019).
   PubMed Web of Science ®Google Scholar
• Ge Y , WuZ , ChenHet al. Structural insights into telomere protection and homeostasis regulation by yeast CST complex. Nat. Struct. Mol. Biol.27(8), 752–762 (2020).
   PubMed Web of Science ®Google Scholar
• Znosko BM , KennedySD , WillePC , KrughTR , TurnerDH. Structural features and thermodynamics of the J4/5 loop from the Candida albicans and Candida dubliniensis Group I introns. Biochemistry43(50), 15822–15837 (2004).
   PubMed Web of Science ®Google Scholar
• Schatzman SS , PetersonRL , TekaMet al. Copper-only superoxide dismutase enzymes and iron starvation stress in Candida fungal pathogens. J. Biol. Chem.295(2), 570–583 (2020).
   PubMed Web of Science ®Google Scholar
• Zheng P , ChenL , ZhongSet al. A Cu-only superoxide dismutase from stripe rust fungi functions as a virulence factor deployed for counter defense against host-derived oxidative stress. Environ. Microbiol.22(12), 5309–5326 (2020).
   PubMed Web of Science ®Google Scholar
• Patrick WM , NakataniY , CutfieldSM , SharpeML , RamsayRJ , CutfieldJF. Carbohydrate binding sites in Candida albicans exo-β-1,3-glucanase and the role of the Phe-Phe ‘clamp’ at the active site entrance. FEBS J.277(21), 4549–4561 (2010).
   PubMed Web of Science ®Google Scholar
• Cutfield JF , SullivanPA , CutfieldSM. Minor structural consequences of alternative CUG codon usage (Ser for Leu) in Candida albicans exoglucanase. Protein Eng. Des. Sel.13(10), 735–738 (2000).
   Google Scholar
• van den Berg B , ChembathA , JefferiesD , BasleA , KhalidS , RutherfordJC. Structural basis for Mep2 ammonium transceptor activation by phosphorylation. Nat. Commun.7(1), 11337 (2016).
   PubMedGoogle Scholar
• Fisher N , MeunierB , BiaginiGA. The cytochrome BC1 complex as an antipathogenic target. FEBS Lett.594(18), 2935–2952 (2020).
   PubMed Web of Science ®Google Scholar
• Jourdan JP , BureauR , RochaisC , DallemagneP. Drug repositioning: a brief overview. J. Pharm. Pharmacol.72(9), 1145–1151 (2020).
   PubMed Web of Science ®Google Scholar
• Sun W , SandersonPE , ZhengW. Drug combination therapy increases successful drug repositioning. Drug Discov. Today21(7), 1189–1195 (2016).
   PubMed Web of Science ®Google Scholar
• Bryson HM , FauldsD. Cisatracurium besilate. Drugs53(5), 8848–8866 (1997).
   Google Scholar
• Li S , HuX , TanF , LiW. Effects of cisatracurium, rocuronium, and mivacurium on intraocular pressure during induction of general anesthesia in ophthalmic surgery. Drug Des. Devel. Ther.14, 1203–1208 (2020).
   PubMed Web of Science ®Google Scholar
• de Andrade Neto JB , da SilvaCR , BarrosoFDet al. Synergistic effects of ketamine and azole derivatives on Candida spp. resistance to fluconazole. Future Microbiol.15, 177–188 (2020).
   PubMedGoogle Scholar
• Do Av Sá LG , DaSilva CR , deS Campos Ret al. Synergistic anticandidal activity of etomidate and azoles against clinical fluconazole-resistant Candida isolates. Future Microbiol.14(17), 1477–1488 (2019).
   PubMed Web of Science ®Google Scholar
• Sá LG do AV , da SilvaCR , deAndrade Neto JBet al. Antifungal activity of etomidate against growing biofilms of fluconazole-resistant Candida spp. strains, binding to mannoproteins and molecular docking with the ALS3 protein. J. Med. Microbiol.69(10), 1221–1227 (2020).
   PubMed Web of Science ®Google Scholar
• Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard – Third Edition. CLSI Document M27-A3 . Clinical and Laboratory Standards Institute, PA, USA (2008).
   Google Scholar
• Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Fourth Informational Supplement. CLSI Document M27-S4 . Clinical and Laboratory Standards Institute, PA, USA (2012).
   Google Scholar
• Ji J , DuX , ChenY , FuY , WangH , YuY. In vitro activity of sulbactam in combination with imipenem, meropenem, panipenem or cefoperazone against clinical isolates of Acinetobacter baumannii. Int. J. Antimicrob. Agents41(4), 400–401 (2013).
   PubMed Web of Science ®Google Scholar
• Pierce CG , UppuluriP , TristanARet al. A simple and reproducible 96 well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat. Protoc.3(9), 1494–1500 (2008).
   PubMed Web of Science ®Google Scholar
• Da Silva CR , DeAndrade Neto JB , CostaSidrim JJet al. Synergistic effects of amiodarone and fluconazole on Candida tropicalis resistant to fluconazole. Antimicrob. Agents Chemother.57(4), 1691–1700 (2013).
   PubMed Web of Science ®Google Scholar
• ChemAxon . Marvin A full featured chemical editor for making science accessible on all platforms (2019). https://chemaxon.com/marvin
   Google Scholar
• Csizmadia P . MarvinSketch and MarvinView: molecule applets for the world wide web (2019). https://chemaxon.com/blog/presentation/marvinsketch-and-marvinview-molecule-applets-for-the-world-wide-web
   Google Scholar
• Hanwell MD , CurtisDE , LonieDC , VandermeerschdT , ZurekE , HutchisonGR. Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. J. Cheminform.4, 17 (2012).
   PubMed Web of Science ®Google Scholar
• Huey R , MorrisGM , ForliS. Using Autodock 4 and AutoDock Vina with AutoDockTools: a tutorial (2012). https://dasher.wustl.edu/chem430/software/autodock/tutorial-hiv-protease.pdf
   Google Scholar
• Trott O , OlsonAJ. Software news and update AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem.31(2), 455–461 (2010).
   PubMed Web of Science ®Google Scholar
• Pettersen EF , GoddardTD , HuangCCet al. UCSF Chimera – a visualization system for exploratory research and analysis 25(13), 1605–1612 (2004).
   Google Scholar
• Biovia DS . Discovery Studio Modeling Environment, Release 2017. CA, USA (2016). https://www.3ds.com/products-services/biovia/products/molecular-modeling-simulation/biovia-discovery-studio/
   Google Scholar
• DeLano WL . The PyMOL Molecular Graphics System, Version 2.3 (2020).
   Google Scholar
• Halgren TA . Merck Molecular Force Field. 17(1996), 520–552 (2000).
   Google Scholar
• Trincao J , JohnsonRE , EscalanteCR , PrakashS , PrakashL , AggarwalAK. Structure of the catalytic core of S. cerevisiae DNA polymerase η. Mol. Cell8(2), 417–426 (2001).
   PubMed Web of Science ®Google Scholar
• Yu EY , SunJ , LeiM , LueNF. Analyses of Candida Cdc13 orthologues revealed a novel OB fold dimer arrangement, dimerization-assisted DNA binding, and substantial structural differences between Cdc13 and RPA70. Mol. Cell. Biol.32(1), 186–198 (2012).
   PubMed Web of Science ®Google Scholar
• Gleason JE , GalaleldeenA , PetersonRLet al. Candida albicans SOD5 represents the prototype of an unprecedented class of Cu-only superoxide dismutases required for pathogen defense. Proc. Natl Acad. Sci.111(16), 5866–5871 (2014).
   PubMed Web of Science ®Google Scholar
• Hargrove TY , FriggeriL , WawrzakZet al. Structural analyses of Candida albicans sterol 14α-demethylase complexed with azole drugs address the molecular basis of azole-mediated inhibition of fungal sterol biosynthesis. J. Biol. Chem.292(16), 6728–6743 (2017).
   PubMed Web of Science ®Google Scholar
• Singh SB , KaelinDE , WuJet al. Tricyclic 1,5-naphthyridinone oxabicyclooctane-linked novel bacterial topoisomerase inhibitors as broad-spectrum antibacterial agents-SAR of left-hand-side moiety (Part-2). Bioorg. Med. Chem. Lett.25(9), 1831–1835 (2015).
   PubMed Web of Science ®Google Scholar
• Lange C . Specific roles of protein-phospholipid interactions in the yeast cytochrome BC1 complex structure. EMBO J.20(23), 6591–6600 (2001).
   PubMed Web of Science ®Google Scholar
• Yan J , ZhangG , PanJ , WangY. α-Glucosidase inhibition by luteolin: kinetics, interaction and molecular docking. Int. J. Biol. Macromol.64, 213–23 (2014).
   PubMed Web of Science ®Google Scholar
• Marinho EM , Batistade Andrade Neto J , SilvaJet al. Virtual screening based on molecular docking of possible inhibitors of COVID-19 main protease. Microb. Pathog.148(June), 104365 (2020).
   PubMedGoogle Scholar
• Yusuf D , DavisAM , KleywegtGJ , SchmittS. An alternative method for the evaluation of docking performance: RSR vs RMSD. 1411–1422 (2008).
   Google Scholar
• Shityakov S , FörsterC. In silico predictive model to determine vector-mediated transport properties for the blood-brain barrier choline transporter. Adv. Appl. Bioinform. Chem.7(1), 23–36 (2014).
   PubMedGoogle Scholar
• Kadela-tomanek M , JastrzM , MarciniecK , ChrobakE , EwaB. Lipophilicity, pharmacokinetic properties, and molecular docking study on SARS-CoV-2 target for betulin triazole derivatives with attached 1, 4-quinone. Pharmaceutics13(6), 781 (2021).
   PubMed Web of Science ®Google Scholar
• Imberty A , HardmanKD , CarverJP , PerezS. Molecular modelling of protein-carbohydrate interactions. Docking of monosaccharides in the binding site of concanavalin A. Glycobiology1(6), 631–642 (1991).
   PubMedGoogle Scholar
• Hanci V , CömertF , AyoğluH , KulahC , YurtluS , TuranIO. Evaluation of the antimicrobial effects of atracurium, rocuronium and mivacurium. Antimicrobial effects of muscle relaxants. Drugs Ther. Stud.1(1), 2 (2010).
   Google Scholar
• Graystone S , WellsMF , FarrellDJ. Do intensive care drug infusions support microbial growth?Anaesth. Intensive Care25(6), 640–642 (1997).
   PubMed Web of Science ®Google Scholar
• Weindlmayr-Goettel M , GillyH , KressHG. Does ester hydrolysis change the in vitro degradation rate of cisatracurium and atracurium?Br. J. Anaesth.88(4), 555–562 (2002).
   PubMed Web of Science ®Google Scholar
• Queiroz HA , DaSilva CR , DeAndrade Neto JBet al. Synergistic activity of diclofenac sodium with oxacillin against planktonic cells and biofilm of methicillin-resistant Staphylococcus aureus strains. Future Microbiol.16(6), 375–387 (2021).
   PubMed Web of Science ®Google Scholar
• Foletto VS , da RosaTF , SerafinMB , BottegaA , HörnerR. Repositioning of non-antibiotic drugs as an alternative to microbial resistance: a systematic review. Int. J. Antimicrob. Agents58(3), 106380 (2021).
   PubMed Web of Science ®Google Scholar
• Li WS , ChenYC , KuoSF , ChenFJ , LeeCH. The impact of biofilm formation on the persistence of candidemia. Front. Microbiol.9(June), 1196 (2018).
   PubMedGoogle Scholar
• Zhou Q , YuanJ , LiuY , WuY. Cisatracurium besilate enhances the TRAIL-induced apoptosis of gastric cancer cells via p53 signaling. Bioengineered12(2), 11213–11224 (2021).
   PubMed Web of Science ®Google Scholar
• Zhu D , ShiC , JiangY , ZhuK , WangX , FengW. Cisatracurium inhibits the growth and induces apoptosis of ovarian cancer cells by promoting lincRNA-p21. Bioengineered12(1), 1505–1516 (2021).
   PubMed Web of Science ®Google Scholar
• Wong RSY . Apoptosis in cancer: from pathogenesis to treatment. J. Exp. Clin. Cancer Res.30(1), 87 (2011).
   PubMed Web of Science ®Google Scholar
• Chambers RS , BroughtonMJ , CannonRD , CarneA , EmersonGW , SullivanPA. An exo-B-(1,3)-glucanase of Candida albicans: purification of the enzyme and molecular cloning of the gene. J. Gen. Microbiol.139, 325–334 (1993).
   PubMedGoogle Scholar
• Marichal P , GorrensJ , LaurijssensLet al. Accumulation of 3-ketosteroids induced by itraconazole in azole-resistant clinical Candida albicans isolates. Antimicrob. Agents Chemother.43(11), 2663–2670 (1999).
   PubMed Web of Science ®Google Scholar
• Silva LC , BarbosaAM , TannousIPet al. In silico inhibition of essential Candida albicans proteins by arenicin, a marine antifungal peptide. International Marine Science Journal1(1), 1–9 (2019).
   Google Scholar
• Hunte C , PalsdottirH , TrumpowerBL. Protonmotive pathways and mechanisms in the cytochrome BC1 complex. FEBS Lett.545(1), 39–46 (2003).
   PubMed Web of Science ®Google Scholar
• Vincent BM , LangloisJ , SrinivasRet al. A fungal-selective cytochrome bc1 inhibitor impairs virulence and prevents the evolution of drug resistance. Cell Chem. Biol.23(8), 978–991 (2016).
   PubMed Web of Science ®Google Scholar
• da Silva CR , SáLG do AV , DosSantos EVet al. Evaluation of the antifungal effect of chlorogenic acid against strains of Candida spp. resistant to fluconazole: apoptosis induction and in silico analysis of the possible mechanisms of action. J. Med. Microbiol.71(5), 1–17 (2022).
   Web of Science ®Google Scholar