Abstract
Bacterial biofilms are inherently resistant to antimicrobial agents and are difficult to eradicate with conventional antimicrobial agents, resulting in many persistent and chronic bacterial infections. In this contribution, a new strategy for reversing the biofilm-associated antibiotic resistance has been explored by induction of a carborane ruthenium(II)-arene complex (FcRuSB). Our results demonstrate that the FcRuSB could be utilized as an inducer to efficiently reverse the biofilm-associated antibiotic resistance of multidrug-resistant (MDR) clinical isolates of Staphylococcus aureus and Pseudomonas aeruginosa. The induced effect of FcRuSB is correlated with a considerable decrease in the expression of extracellular matrix proteins (EMP) of the two strains. The considerable decrease of the EMP of induced cells, resulting in the reduction of adherence and biofilm formation ability of the two types of MDR pathogens, and then can cause significantly enhanced sensitivity of them to antibiotics.
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Liu HL, Chen JN, Jiang J, Giesy JP, Yu HX, Wang XR. Cytotoxicity of HC Orange NO. 1 to L929 fibroblast cells. Environ Toxicol Phar, 2008, 26: 309–314
Potera C. Forging a link between biofilms and disease. Science, 1999, 283: 1837–1839
Davey ME, O’toole GA. Microbial biofilms: From ecology to molec ular genetics. Microbiol Mol Biol R, 2000, 64: 847–867
Smith K, Perez A, Ramage G, Gemmell CG, Lang S. Comparison of biofilm-associated cell survival following in vitro exposure of meticillin-resistant Staphylococcus aureus biofilms to the antibiotics clin-damycin, daptomycin, linezolid, tigecycline and vancomycin. Int J Antimicrob Ag, 2009, 33: 374–378
Gilbert P, Das J, Foley I. Biofilm susceptibility to antimicrobials. Adv Dent Res, 1997, 11: 160–167
Lefebvre F, Putaj P, Basset JM, Wang XX, Fu XZ. Modification of the adsorption and catalytic properties of micro- and mesoporous materials by reactions with organometallic complexes. Science China-chemistry, 2010, 53: 1862–1869
Fish RH, Jaouen G. Bioorganometallic chemistry: Structural diversity of organometallic complexes with bioligands and molecular recognition studies of several supramolecular hosts with biomolecules, alkalimetal ions, and organometallic pharmaceuticals. Organometallics, 2003, 22: 2166–2177
van Staveren DR, Metzler-Nolte N. Bioorganometallic chemistry of ferrocene. Chem Rev, 2004, 104: 5931–5985
Chantson JT, Falzacappa MVV, Crovella S, Metzler-Nolte N. Antibacterial activities of ferrocenoyl- and cobaltocenium-peptide bioconjugates. J Organomet Chem, 2005, 690: 4564–4572
Asghar F, Badshah A, Shah A, Rauf MK, Ali MI, Tahir MN, Nosheen E, Rehman Z, Qureshi R. Synthesis, characterization and DNA binding studies of organoantimony(V) ferrocenyl benzoates. J Organomet Chem, 2012, 717: 1–8
Arbi ME, Pigeon P, Top S, Rhouma A, Aifa S, Rebai A, Vessières A, Plamont MA, Jaouen G. Evaluation of bactericidal and fungicidal activity of ferrocenyl or phenyl derivatives in the diphenyl butene series. J Organomet Chem, 2011, 696: 1038–1048
Plażuk D, Rychlik B, Blauz A, Domagała S. Synthesis, electrochemistry and anticancer activity of novel ferrocenyl phenols prepared via azide-alkyne 1,3-cycloaddition reaction. J Organomet Chem, 2012, 715: 102–112
Ornelas C. Application of ferrocene and its derivatives in cancer research. New J Chem, 2011, 35: 1973–1985
Delhaes L, Biot C, Berry L, Delcourt P, Maciejewski LA, Camus D, Brocard JS, Dive D. Synthesis of ferroquine enantiomers: First investigation of effects of metallocenic chirality upon antimalarial activity and cytotoxicity. ChemBioChem, 2002, 3: 418–423
Biot C, Taramelli D, Forfar-Bares I, Maciejewski LA, Boyce M, Nowogrocki G, Brocard JS, Basilico N, Olliaro P, Egan TJ. Insights into the mechanism of action of ferroquine. Relationship between physicochemical properties and antiplasmodial activity. Mol Pharmaceutics, 2005, 2: 185–193
Biot C, Delhaes L, Abessolo H, Domarle O, Maciejewski LA, Mortuaire M, Delcourt P, Deloron P, Camus D, Dive D, Brocard JS. Novel metallocenic compounds as antimalarial agents. Study of the position of ferrocene in chloroquine. J Organomet Chem, 1999, 589: 59–65
Jaouen G, Top S, Vessieres A, Leclercq G, McGlinchey MJ. The first organometallic selective estrogen receptor modulators (SERMs) and their relevance to breast cancer. Curr Med Chem, 2004, 11: 2505–2517
Top S, Vessieres A, Leclercq G, Quivy J, Tang J, Vaissermann J, Huche M, Jaouen G. Synthesis, biochemical properties and molecular modelling studies of organometallic specific estrogen receptor modulators (SERMs), the ferrocifens and hydroxyferrocifens: Evidence for an antiproliferative effect of hydroxyferrocifens on both hormone-dependent and hormone-independent breast cancer cell lines. Chem-Eur J, 2003, 9: 5223–5236
Edwards EI, Epton R, Marr G. Organometallic derivatives of penicillins and cephalosporins a new class of semi-synthetic antibiotics. J Organomet Chem, 1975, 85: C23–C25
Edwards EI, Epton R, Marr G. A new class of semi-synthetic antibiotics: Ferrocenyl-penicillins and -cephalosporins. J Organomet Chem, 1976, 107: 351–357
Valliant JF, Guenther KJ, King AS, Morel P, Schaffer P, Sogbein OO, Stephenson KA. The medicinal chemistry of carboranes. Coord Chem Re, 2002, 232: 173–230
Wu CH, Ye HD, Jiang H, Wang XM, Yan H. Study on specific interaction of new ferrocene-substituted carborane conjugates with hemoglobin protein. Sci China Chem, 2012, 55: 594–603
Armstrong AF, Valliant JF. The bioinorganic and medicinal chemistry of carboranes: From new drug discovery to molecular imaging and therapy. Dalton T, 2007, 4240-4251
Li SH, Wu CY, Lv XY, Tang X, Zhao XQ, Yan H, Jiang H, Wang XM. Discovery of ferrocene-carborane derivatives as novel chemical antimicrobial agents against multidrug-resistant bacteria. Sci China Chem, 2012, 55: 2388–2395
Bregadze VI, Sivaev IB, Glazun SA. Polyhedral boron compounds as potential diagnostic and therapeutic antitumor agents. Anticancer Agents Med Chem, 2006, 6: 75–109
Soloway AH, Tjarks W, Barnum BA, Rong FG, Barth RF, Codogni IM, Wilson JG. The chemistry of neutron capture therapy. Chem Rev, 1998, 98: 1515–1562
Miyajima Y, Nakamura H, Kuwata Y, Lee JD, Masunaga S, Ono K, Maruyama K. Transferrin-loaded nido-carborane liposomes: Tumor-targeting boron delivery system for neutron capture therapy. Bioconjugate Chem, 2006, 17: 1314–1320
Wu CH, Wu DH, Liu X, Guoyiqibayi G, Guo DD, Lv G, Wang XM, Yan H, Jiang H, Lu ZH. Ligand-based neutral ruthenium(II) arene complex: Selective anticancer action. Inorg chem, 2009, 48: 2352–2354
Wu DH, Wu CH, Li YZ, Guo DD, Wang XM, Yan H. Addition of ethynylferrocene to transition-metal complexes containing a chelating 1,2-dicarba-closo-dodecaborane-1,2-dichalcogenolate ligand—in vitro cooperativity of a ruthenium compound on cellular uptake of an anticancer drug. Dalton T, 2009, 285-290
Wu C, Ye H, Bai W, Li Q, Guo D, Lv G, Yan H, Wang X. New potential anticancer agent of carborane derivatives: Selective cellular interaction and activity of ferrocene-substituted dithio-o-carborane conjugates. Bioconjugate Chem, 2011, 22: 16–25
Xu BH, Peng XQ, Li YZ, Yan H. Reactions of 16e CpCo half-sandwich complexes containing a chelating 1,2-dicarba-closo-dodecaborane-1,2-dichalcogenolate ligand with ethynylferrocene and dimethyl acetylenedicarboxylate. Chem-Eur J, 2008, 14: 9347–9356
Xu BH, Peng XQ, Xu ZW, Li YZ, Yan H. Cobalt(III)-mediated disulfuration and hydrosulfuration of alkynes. Inorg Chem, 2008, 47: 7928–7933
Wu C, Xu B, Zhao J, Jiang Q, Wei F, Jiang H, Wang X, Yan H. Ferrocene-substituted dithio-o-carborane isomers: Influence on the native conformation of myoglobin protein. Chem-Eur J, 2010, 16: 8914–8922
Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved standard, 8th ed, Document M7-A8, Wayne, PA: CLSI, 2008
Pettit RK, Weber CA, Kean MJ, Hoffmann H, Pettit GR, Tan R, Franks KS, Horton ML. Microplate alamar blue assay for Staphylococcus epidermidis biofilm susceptibility testing. Antimicrob Agents Ch, 2005, 49: 2612–2617
Hirose I, Sano K, Shioda I, Kumano M, Nakamura K, Yamane K. Proteome analysis of Bacillus subtilis extracellular proteins: A two-dimensional protein electrophoretic study. Microbiology+, 2000, 146: 65–75
Tunney MM, Ramage G, Field TR, Moriarty TF, Storey DG. Rapid colorimetric assay for antimicrobial susceptibility testing of Pseudomonas aeruginosa. Antimicrob Agents Ch, 2004, 48: 1879–1881
Kwon AS, Park GC, Ryu SY, Lim DH, Lim DY, Choi CH, Park Y, Lim Y. Higher biofilm formation in multidrug-resistant clinical isolates of Staphylococcus aureus. Int J Antimicrob Ag, 2008, 32: 68–72
Corrigan RM, Rigby D, Handley P, Foster TJ. The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology+, 2007, 153: 2435–2446
Mengodin E, Bajolet O, Cutrona J, Bonnet N, Dupuit F, Puchelle E, de Bentzmann S. Fibronectin-binding proteins of Staphylococcus aureus are involved in adherence to human airway epithelium. Infect Immun, 2002, 70: 620–630
Joh D, Wann ER, Kreikemeyer B, Speziale P, Höök M. Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol, 1999, 18: 211–223
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Li, S., Wu, C., Tang, X. et al. New strategy for reversing biofilm-associated antibiotic resistance through ferrocene-substituted carborane ruthenium(II)-arene complex. Sci. China Chem. 56, 595–603 (2013). https://doi.org/10.1007/s11426-012-4812-6
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DOI: https://doi.org/10.1007/s11426-012-4812-6