A benzimidazole-based ruthenium(IV) complex inhibits Pseudomonas aeruginosa biofilm formation by interacting with siderophores and the cell envelope, and inducing oxidative stress

References

• Abebe A, Hailemariam T. 2016. Synthesis and assessment of antibacterial activities of ruthenium(III) mixed ligand complexes containing 1,10-phenanthroline and guanide. Bioinorg Chem Appl. 2016:1–9. doi: 10.1155/2016/3607924
   Google Scholar
• Abu-Dief AM, Mohamed IMA. 2015. A review on versatile applications of transition metal complexes incorporating Schiff bases. Beni-Suef Univ J Basic Appl Sci. 4:119–133. doi: 10.1016/j.bjbas.2015.05.004
   PubMedGoogle Scholar
• Alhama J, Ruiz-Laguna J, Rodriguez-Ariza A, Toribio F, López-Barea J, Pueyo C. 1998. Formation of 8-oxoguanine in cellular DNA of Escherichia coli strains defective in different antioxidant defences. Mutagenesis. 13:589–594. doi: 10.1093/mutage/13.6.589
   PubMed Web of Science ®Google Scholar
• Ali Ezadyar S, Kumbhar AS, Kumbhar AA, Khan A. 2012. Binuclear ruthenium(II) polypyridyl complexes: DNA cleavage and mitochondria mediated apoptosis induction. Polyhedron. 36:45–55. doi: 10.1016/j.poly.2012.01.024
   Web of Science ®Google Scholar
• Alqarni B, Colley B, Klebensberger J, McDougald D, Rice SA. 2016. Expression stability of 13 housekeeping genes during carbon starvation of Pseudomonas aeruginosa. J Microbiol Methods. 127:182–187. doi: 10.1016/j.mimet.2016.06.008
   PubMed Web of Science ®Google Scholar
• Beeton ML, Aldrich-Wright JR, Bolhuis A. 2014. The antimicrobial and antibiofilm activities of copper(II) complexes. J Inorg Biochem. 140:167–172. doi: 10.1016/j.jinorgbio.2014.07.012
   PubMed Web of Science ®Google Scholar
• Bertin C, Pau-Roblot C, Courtois J, Manso-Silván L, Thiaucourt F, Tardy F, Le Grand D, Poumarat F, Gaurivaud P. 2013. Characterization of free exopolysaccharides secreted by Mycoplasma mycoides subsp. mycoides. PLoS One. 8:e68373. doi: 10.1371/journal.pone.0068373
   PubMed Web of Science ®Google Scholar
• Bichara M, Pinet I, Lambert IB, Fuchs RPP. 2007. RecA-mediated excision repair: A novel mechanism for repairing DNA lesions at sites of arrested DNA synthesis. Mol Microbiol. 65:218–229. doi: 10.1111/j.1365-2958.2007.05790.x
   PubMed Web of Science ®Google Scholar
• Borlee BR, Goldman AD, Murakami K, Samudrala R, Wozniak DJ, Parsek MR. 2010. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol. 75:827–842. doi: 10.1111/j.1365-2958.2009.06991.x
   PubMed Web of Science ®Google Scholar
• Britigan BE, Miller RA, Hassett DJ, Pfaller MA, Cormick MLMC, Rasmussen GT. 2001. Antioxidant enzyme expression in clinical isolates of Pseudomonas aeruginosa: identification of an atypical form of manganese superoxide dismutase. Infect Immun. 69:7396–7401. doi: 10.1128/IAI.69.12.7396-7401.2001
   PubMed Web of Science ®Google Scholar
• Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol. 3:3–8.
   PubMedGoogle Scholar
• Casali N. 2003. Escherichia coli host strains. Methods Mol Biol. 235:27–48.
   PubMedGoogle Scholar
• Cieśla J, Bieganowski A, Janczarek M, Urbanik-Sypniewska T. 2011. Determination of the electrokinetic potential of Rhizobium leguminosarum bv trifolii Rt24.2 using Laser Doppler Velocimetry-a methodological study. J Microbiol Methods. 85:199–205. doi: 10.1016/j.mimet.2011.03.004
   PubMed Web of Science ®Google Scholar
• Clarke MJ. 2002. Ruthenium metallopharmaceuticals. Coord Chem Rev. 232:69–93. doi: 10.1016/S0010-8545(02)00025-5
   Web of Science ®Google Scholar
• Cornelis P. 2010. Iron uptake and metabolism in pseudomonads. Appl Microbiol Biotechnol. 86:1637–1645. doi: 10.1007/s00253-010-2550-2
   PubMed Web of Science ®Google Scholar
• Cullen L, Weiser R, Olszak T, Maldonado RF, Slachmuylders L, Brackman G, Paunova-Krasteva TS, Zarnowiec P, Czerwonka G, Reilly J, et al. 2015. Phenotypic characterization of an international Pseudomonas aeruginosa reference panel: strains of cystic fibrosis (CF) origin show less in vivo virulence than non-CF strains. Microbiology 161:1961–1977. doi: 10.1099/mic.0.000155
   PubMed Web of Science ®Google Scholar
• Cussac C, Laval F. 1996. Reduction of the toxicity and mutagenicity of aziridine in mammalian cells harboring the Escherichia coli fpg gene. Nucleic Acids Res. 24:1742–1746. doi: 10.1093/nar/24.9.1742
   PubMed Web of Science ®Google Scholar
• Czerwonka G, Guzy A, Kałuża K, Grosicka M, Dańczuk M, Lechowicz Ł, Gmiter D, Kowalczyk P, Kaca W. 2016. The role of Proteus mirabilis cell wall features in biofilm formation. Arch Microbiol. 198:877–884. doi: 10.1007/s00203-016-1249-x
   PubMed Web of Science ®Google Scholar
• Ezraty B, Gennaris A, Barras F, Collet J-F. 2017. Oxidative stress, protein damage and repair in bacteria. Nat Rev Microbiol. 15:385–396. doi: 10.1038/nrmicro.2017.26
   PubMed Web of Science ®Google Scholar
• Fournier A, Voirol P, Krähenbühl M, Bonnemain C-L, Fournier C, Pantet O, Pagani J-L, Revelly J-P, Dupuis-Lozeron E, Sadeghipour F, et al. 2016. Antibiotic consumption to detect epidemics of Pseudomonas aeruginosa in a burn centre: a paradigm shift in the epidemiological surveillance of Pseudomonas aeruginosa nosocomial infections. Burns. 42:564–570. doi: 10.1016/j.burns.2015.10.030
   PubMed Web of Science ®Google Scholar
• Frederick JR, Elkins JG, Bollinger N, Hassett DJ, McDermott TR. 2001. Factors affecting catalase expression in Pseudomonas aeruginosa biofilms and planktonic cells. Appl Environ Microbiol. 67:1375–1379. doi: 10.1128/AEM.67.3.1375-1379.2001
   PubMed Web of Science ®Google Scholar
• Haiko J, Westerlund-Wikström B. 2013. The role of the bacterial flagellum in adhesion and virulence. Biology (Basel). 2:1242–1267. doi: 10.3390/biology2041242
   PubMedGoogle Scholar
• Hannauer M, Barda Y, Mislin GLA, Shanzer A, Schalk IJ. 2010. The ferrichrome uptake pathway in Pseudomonas aeruginosa involves an iron release mechanism with acylation of the siderophore and recycling of the modified desferrichrome. J Bacteriol. 192:1212–1220. doi: 10.1128/JB.01539-09
   PubMed Web of Science ®Google Scholar
• Hong R, Kang TY, Michels CA, Gadura N. 2012. Membrane lipid peroxidation in copper alloy-mediated contact killing of Escherichia coli. Appl Environ Microbiol. 78:1776–1784. doi: 10.1128/AEM.07068-11
   PubMed Web of Science ®Google Scholar
• Imperi F, Tiburzi F, Visca P. 2009. Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc Natl Acad Sci Usa. 106:20440–20445. doi: 10.1073/pnas.0908760106
   PubMed Web of Science ®Google Scholar
• Jabłońska-Wawrzycka A, Rogala P, Michałkiewicz S, Hodorowicz M, Barszcz B. 2013. Ruthenium complexes in different oxidation states: synthesis, crystal structure, spectra and redox properties. Dalton Trans. 42:6092–6101. doi: 10.1039/c3dt32214a
   PubMedGoogle Scholar
• Johnson NA, Mckenzie R, Mclean L, Sowers LC, Fletcher M. 2004. 8-Oxo-7,8-dihydroguanine is removed by a nucleotide excision repair-like mechanism in Porphyromonas gingivalis W83. J Bacteriol. 186:7697–7703. doi: 10.1128/JB.186.22.7697-7703.2004
   PubMed Web of Science ®Google Scholar
• Jurado J, Saparbaev M, Matray TJ, Greenberg MM, Laval J. 1998. The ring fragmentation product of thymidine C5-hydrate when present in DNA is repaired by the Escherichia coli Fpg and Nth proteins. Biochemistry. 37:7757–7763. doi: 10.1021/bi972982z
   PubMed Web of Science ®Google Scholar
• Kowalczyk P, Borkowski A, Czerwonka G, Cłapa T, Cieśla J, Misiewicz A, Borowiec M, Szala M. 2018. The microbial toxicity of quaternary ammonium ionic liquids is dependent on the type of lipopolysaccharide. J Mol Liq. 266:540–547. doi: 10.1016/j.molliq.2018.06.102
   Web of Science ®Google Scholar
• Laurent Q, Batchelor LK, Dyson PJ. 2018. Applying a Trojan Horse strategy to ruthenium complexes in the pursuit of novel antibacterial agents. Organometallics. 37:915–923. doi: 10.1021/acs.organomet.7b00885
   Web of Science ®Google Scholar
• Laverty G, Gorman S, Gilmore B. 2014. Biomolecular mechanisms of Pseudomonas aeruginosa and Escherichia coli biofilm formation. Pathogens. 3:596–632. doi: 10.3390/pathogens3030596
   PubMedGoogle Scholar
• Lee J, Attila C, Cirillo SLG, Cirillo JD, Wood TK. 2009. Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol. 2:75–90. doi: 10.1111/j.1751-7915.2008.00061.x
   PubMed Web of Science ®Google Scholar
• Lee JH, Kim YG, Cho MH, Kim JA, Lee J. 2012. 7-fluoroindole as an antivirulence compound against Pseudomonas aeruginosa. FEMS Microbiol Lett. 329:36–44. doi: 10.1111/j.1574-6968.2012.02500.x
   PubMed Web of Science ®Google Scholar
• Lemire JA, Harrison JJ, Turner RJ. 2013. Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol. 11:371–384. doi: 10.1038/nrmicro3028
   PubMed Web of Science ®Google Scholar
• Li F, Collins JG, Keene FR. 2015. Ruthenium complexes as antimicrobial agents. Chem Soc Rev. 44:2529–2542. doi: 10.1039/C4CS00343H
   PubMed Web of Science ®Google Scholar
• Li S, Wu C, Tang X, Gao S, Zhao X, Yan H, Wang X. 2013. New strategy for reversing biofilm-associated antibiotic resistance through ferrocene-substituted carborane ruthenium(II)-arene complex. Sci China Chem. 56:595–603. doi: 10.1007/s11426-012-4812-6
   Web of Science ®Google Scholar
• Periasamy S, Nair HAS, Lee KWK, Ong J, Goh JQJ, Kjelleberg S, Rice SA. 2015. Pseudomonas aeruginosa PAO1 exopolysaccharides are important for mixed species biofilm community development and stress tolerance. Front Microbiol. 6:1–10.
   PubMed Web of Science ®Google Scholar
• Pillai SI, Vijayaraghavan K, Subramanian S. 2014. Evaluation of DNA-binding, cleavage, BSA interaction of zn-hydroxy flavone complex. Der Pharma Chem. 6:379–389.
   Google Scholar
• Prosser KE, Chang SW, Saraci F, Le PH, Walsby CJ. 2017. Anticancer copper pyridine benzimidazole complexes: ROS generation, biomolecule interactions, and cytotoxicity. J Inorg Biochem. 167:89–99. doi: 10.1016/j.jinorgbio.2016.11.006
   PubMed Web of Science ®Google Scholar
• Qian J, Ma X, Tian J, Gu W, Shang J, Liu X, Yan S. 2010. Hydrolytic cleavage of double-strand DNA by the water-soluble dicobalt(III) complexes of 1,4,7-Triazacyclononane-N-acetate. J Inorg Biochem. 104:993–999. doi: 10.1016/j.jinorgbio.2010.05.005
   PubMed Web of Science ®Google Scholar
• Quinteros MA, Cano Aristizábal V, Dalmasso PR, Paraje MG, Páez PL. 2016. Oxidative stress generation of silver nanoparticles in three bacterial genera and its relationship with the antimicrobial activity. Toxicol Vitr. 36:216–223. doi: 10.1016/j.tiv.2016.08.007
   PubMed Web of Science ®Google Scholar
• Rajendiran V, Karthik R, Palaniandavar M, Stoeckli-Evans H, Periasamy VS, Akbarsha MA, Srinag BS, Krishnamurthy H. 2007. Mixed-ligand copper(II)-phenolate complexes: effect of coligand on enhanced DNA and protein binding, DNA cleavage, and anticancer activity. Inorg Chem. 46:8208–8221. doi: 10.1021/ic700755p
   PubMed Web of Science ®Google Scholar
• Ramadevi P, Singh R, Prajapati A, Gupta S, Chakraborty D. 2014. Cu (II) complexes of isoniazid Schiff bases: DNA/BSA binding and cytotoxicity studies on A549 cell line. Adv Chem. 2014:1–14. doi: 10.1155/2014/630575
   Google Scholar
• Del Rio D, Stewart AJ, Pellegrini N. 2005. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis. 15:316–328. doi: 10.1016/j.numecd.2005.05.003
   PubMed Web of Science ®Google Scholar
• Rizzoto M. 2012. Metal complexes as antimicrobial agents. Bobbarala, Varaprasad, editors. Rijeka: InTech.
   Google Scholar
• Roy R, Tiwari M, Donelli G, Tiwari V. 2017. Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence. 9:522–554.
   Web of Science ®Google Scholar
• Salahuddin SM, Mazumder A. 2017. Benzimidazoles: biologically active compounds. Arab J Chem. 10:S157–S173. doi: 10.1016/j.arabjc.2012.07.017
   Web of Science ®Google Scholar
• Sambanthamoorthy K, Gokhale AA, Lao W, Parashar V, Neiditch MB, Semmelhack MF, Lee I, Waters CM. 2011. Identification of a novel benzimidazole that inhibits bacterial biofilm formation in a broad-spectrum manner. Antimicrob Agents Chemother. 55:4369–4378. doi: 10.1128/AAC.00583-11
   PubMed Web of Science ®Google Scholar
• Sampath K, Jayabalakrishnan C. 2014. Biomolecular interaction and cytotoxicity of ruthenium(III) benzothiazole substituted ferrocenyl thiosemicarbazone complexes. Arab J Chem. 10:S3207–S3215.
   Google Scholar
• Sathyadevi P, Krishnamoorthy P, Bhuvanesh NSP, Kalaiselvi P, Vijaya Padma V, Dharmaraj N. 2012. Organometallic ruthenium(II) complexes: synthesis, structure and influence of substitution at azomethine carbon towards DNA/BSA binding, radical scavenging and cytotoxicity. Eur J Med Chem. 55:420–431. doi: 10.1016/j.ejmech.2012.08.001
   PubMed Web of Science ®Google Scholar
• Shahabadi N, Kashanian S, Mahdavi M, Sourinejad N. 2011. DNA interaction and DNA cleavage studies of a new platinum(II) complex containing aliphatic and aromatic dinitrogen ligands. Bioinorg Chem Appl. 2011:525794.
   PubMed Web of Science ®Google Scholar
• Sornchuer P, Namchaiw P, Kerdwong J, Charoenlap N, Mongkolsuk S, Vattanaviboon P. 2014. Copper chloride induces antioxidant gene expression but reduces ability to mediate H2O2 toxicity in Xanthomonas campestris. Microbiol. 160:458–466. doi: 10.1099/mic.0.072470-0
   PubMed Web of Science ®Google Scholar
• Stead MB, Agrawal A, Bowden KE, Nasir R, Mohanty BK, Meagher RB, Kushner SR. 2012. RNAsnapTM: a rapid, quantitative and inexpensive, method for isolating total RNA from bacteria. Nucleic Acids Res. 40:1–9.
   PubMed Web of Science ®Google Scholar
• Tergos G, Mylonakis E. 2012. Antimicrobial drug discovery: emerging strategies. Wilson M, editor. Wallingford, Oxfordshire: CABI.
   Google Scholar
• Topală T, Bodoki A, Oprean L, Oprean R. 2014a. Expereimental techniques employed In the study of metal complexes-DNAiInteractions. Farmacia. 62:1049–1061.
   Web of Science ®Google Scholar
• Topală T, Bodoki A, Oprean L, Oprean R. 2014b. Bovine serum albumin interactions with metal complexes. Clujul Med. 87:215–219. doi: 10.15386/cjmed-357
   PubMedGoogle Scholar
• Verma A, Schirm M, Arora SK, Thibault P, Logan SM, Ramphal R. 2006. Glycosylation of b-type flagellin of Pseudomonas aeruginosa: structural and genetic basis. J Bacteriol. 188:4395–4403. doi: 10.1128/JB.01642-05
   PubMedGoogle Scholar
• Viganor L, Howe O, McCarron P, McCann M, Devereux M. 2017. The antibacterial activity of metal complexes containing 1,10-phenanthroline: potential as alternative therapeutics in the era of antibiotic resistance. Curr Top Med Chem. 17:1280–1302. doi: 10.2174/1568026616666161003143333
   PubMed Web of Science ®Google Scholar
• Ward H, Perron GG, MacLean RC. 2009. The cost of multiple drug resistance in Pseudomonas aeruginosa. J Evol Biol. 22:997–1003. doi: 10.1111/j.1420-9101.2009.01712.x
   PubMed Web of Science ®Google Scholar
• Wilton M, Charron-Mazenod L, Moore R, Lewenza S. 2016. Extracellular DNA acidifies biofilms and induces aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 60:544–553. doi: 10.1128/AAC.01650-15
   PubMed Web of Science ®Google Scholar