Furanone loaded aerogels are effective antibiofilm therapeutics in a model of chronic Pseudomonas aeruginosa wound infection

Biofilm - Tập 5 - Trang 100128 - 2023
Chris R. Proctor1,2,3, Megan G. Taggart1, Barry M.G. O'Hagan4, Paul A. McCarron2, Ronan R. McCarthy3, Nigel G. Ternan1
1Nutrition Innovation Centre for Food and Health (NICHE), School of Biomedical Sciences, Ulster University, Northern Ireland, UK
2School of Pharmacy and Pharmaceutical Sciences, Ulster University, Northern Ireland, UK
3Division of Biosciences, Department of Life Sciences, College of Health and Life Sciences, Brunel University London, Uxbridge, UB8 3PH, UK
4Genomic Medicine Research Group, School of Biomedical Sciences, Ulster University, Northern Ireland, UK

Tài liệu tham khảo

Abisado, 2018, Bacterial quorum sensing and microbial community interactions, mBio, 9, 10.1128/mBio.02331-17 Choi, 2014, Inhibitory effects of 4-hydroxy-2,5-dimethyl-3(2H)-furanone (HDMF) on acyl-homoserine lactone-mediated virulence factor production and biofilm formation in Pseudomonas aeruginosa PAO1, J Microbiol, 52, 734, 10.1007/s12275-014-4060-x Aldawsari, 2021, Tackling virulence of Pseudomonas aeruginosa by the natural furanone sotolon, Antibiotics, 10, 871, 10.3390/antibiotics10070871 Attinger, 2012, Clinically addressing biofilm in chronic wounds, Adv Wound Care, 1, 127, 10.1089/wound.2011.0333 Brandenburg, 2015, Inhibition of Pseudomonas aeruginosa biofilm formation on wound dressings, Wound Repair Regen, 23, 1, 10.1111/wrr.12365 Bruschi, 2015, Mathematical models of drug release, 63 Cady, 2012, Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural products-inspired organosulfur compounds, PLoS One, 7, 10.1371/journal.pone.0038492 Dabiri, 2016, Choosing a wound dressing based on common wound characteristics, Adv Wound Care, 5, 32, 10.1089/wound.2014.0586 Deligianni, 2010, Pseudomonas aeruginosa cystic fibrosis isolates of similar RAPD genotype exhibit diversity in biofilm forming ability in vitro, BMC Microbiol, 10, 38, 10.1186/1471-2180-10-38 Denkbaş, 2004, Norfloxacin-loaded chitosan sponges as wound dressing material, J Biomater Appl, 18, 291, 10.1177/0885328204041510 Di Domenico, 2019, Microbial biofilm correlates with an increased antibiotic tolerance and poor therapeutic outcome in infective endocarditis, BMC Microbiol, 19, 228, 10.1186/s12866-019-1596-2 Dunne, 1993, Diffusion of rifampin and vancomycin through a Staphylococcus epidermidis biofilm, Antimicrob Agents Chemother, 37, 2522, 10.1128/AAC.37.12.2522 Francolini, 2004, Usinic acid, a natural antimicroial agent able to inhibit bacterial biofilm formation on polymer surfaces, Antimicrob Agents Chemother, 48, 4360, 10.1128/AAC.48.11.4360-4365.2004 García-Contreras, 2013, Resistance to the quorum-quenching compounds brominated furanone C-30 and 5-fluorouracil in Pseudomonas aeruginosa clinical isolates, Pathog Dis, 68, 8, 10.1111/2049-632X.12039 García-Lara, 2015, Inhibition of quorum-sensing-dependent virulence factors and biofilm formation of clinical and environmental Pseudomonas aeruginosa strains by ZnO nanoparticles, Lett Appl Microbiol, 61, 299, 10.1111/lam.12456 Ghoreishi, 2020, Inhibition of quorum sensing-controlled virulence factors with natural substances and novel protease, obtained from Halobacillus karajensis, Microb Pathog, 149 Goimil, 2017, Supercritical processing of starch aerogels and aerogel-loaded poly(ε-caprolactone) scaffolds for sustained release of ketoprofen for bone regeneration, J CO2 Util, 18, 237, 10.1016/j.jcou.2017.01.028 Gómez, 2018, Antibacterial activity against Staphylococcus aureus of chitosan/chondroitin sulfate nanocomplex aerogels alone and enriched with erythromycin and elephant garlic (Allium ampeloprasum L. var. ampeloprasum) extract, Pure Appl Chem, 90, 885, 10.1515/pac-2016-1112 Green, 1974, Agricultural plants and soil as a reservoir for Pseudomonas aeruginosa, Appl Microbiol, 28, 987, 10.1128/am.28.6.987-991.1974 Hassan, 2000, Structure and morphology of freeze/thawed PVA hydrogels, Macromolecules, 33, 2472, 10.1021/ma9907587 Heacock-Kang, 2018, Two regulators, PA3898 and PA2100, modulate the Pseudomonas aeruginosa multidrug resistance MexAB-OprM and EmrAB efflux pumps and biofilm formation, Antimicrob Agents Chemother, 62, 10.1128/AAC.01459-18 Hentzer, 2002, Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound, Microbiology, 148, 87, 10.1099/00221287-148-1-87 Hentzer, 2003, Attenuation of Pseudomonas aeruginosa virulence by quorum-sensing inhibitors, EMBO J, 22, 3803, 10.1093/emboj/cdg366 Hirsch, 2010, Impact of multidrug-resistant Pseudomonas aeruginosa infection on patient outcomes, Expert Rev Pharmacoecon Outcomes Res, 10, 441, 10.1586/erp.10.49 Hoffman, 2010, Nutrient availability as a mechanism for selection of antibiotic tolerant Pseudomonas aeruginosa within the CF airway, PLoS Pathog, 6, 10.1371/journal.ppat.1000712 Holloway, 2013, The role of crystallization and phase separation in the formation of physically cross-linked PVA hydrogels, Soft Matter, 9, 826, 10.1039/C2SM26763B Huang, 2013, Simulated body fluid electrochemical response of Zr-based metallic glasses with different degrees of crystallization, Mater Sci Eng C, 33, 4183, 10.1016/j.msec.2013.06.007 Ishida, 2007, Inhibition of quorum sensing in Pseudomonas aeruginosa by N-acyl cyclopentylamides, Appl Environ Microbiol, 73, 3183, 10.1128/AEM.02233-06 Lam, 1980, Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis, Infect Immun, 28, 546, 10.1128/iai.28.2.546-556.1980 Limoli, 2015, Bacterial extracellular polysaccharides in biofilm formation and function, Microbiol Spectr, 3, 10.1128/microbiolspec.MB-0011-2014 Lipsky, 2009, Topical antimicrobial therapy for treating chronic wounds, Clin Infect Dis, 49, 1541, 10.1086/644732 Long, 2018, Cellulose aerogels: synthesis, applications, and prospects, Polymers, 8, 1 López-Iglesias, 2019, vol. 204, 223 Ma, 2019, Nanocomposite sponges of sodium alginate/graphene oxide/polyvinyl alcohol as potential wound dressing: In vitro and in vivo evaluation, Compos B Eng, 167, 396, 10.1016/j.compositesb.2019.03.006 Maeda, 2012, Quorum quenching quandary: resistance to antivirulence compounds, ISME J, 6, 493, 10.1038/ismej.2011.122 Malone, 2017, The prevalence of biofilms in chronic wounds: a systematic review and meta-analysis of published data, J Wound Care, 26, 20, 10.12968/jowc.2017.26.1.20 Mehling, 2009, Polysaccharide-based aerogels as drug carriers, J Non-Cryst Solids, 355, 2472, 10.1016/j.jnoncrysol.2009.08.038 Morohoshi, 2007, Inhibition of quorum sensing in Serratia marcescens AS-1 by synthetic analogs of N-acylhomoserine lactone, Appl Environ Microbiol, 73, 6339, 10.1128/AEM.00593-07 Murillo-Cremaes, 2013, Nanostructured silica-based drug delivery vehicles for hydrophobic and moisture sensitive drugs, J Supercrit Fluids, 73, 34, 10.1016/j.supflu.2012.11.006 Murray, 2022, Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis, Lancet, 399, 629, 10.1016/S0140-6736(21)02724-0 Mushin, 1973, An epidemiological study of Pseudomonas aeruginosa in cattle and other animals by pyocine typing, J Hyg, 71, 113, 10.1017/S0022172400046271 Neopane, 2018, In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance, Int J Gen Med, 11, 25, 10.2147/IJGM.S153268 2004, National nosocomial infections surveillance (NNIS) system report, data summary from january 1992 through june 2004, issued october 2004, Am J Infect Control, 32, 470, 10.1016/j.ajic.2004.10.001 Otton, 2017, Influence of twitching and swarming motilities on biofilm formation in Pseudomonas strains, Arch Microbiol, 199, 677, 10.1007/s00203-017-1344-7 Pandian, 2021, In-situ silver nanoparticles incorporated N, O-carboxymethyl chitosan based adhesive, self-healing, conductive, antibacterial and anti-biofilm hydrogel, Int J Biol Macromol, 188, 501, 10.1016/j.ijbiomac.2021.08.040 Park, 2013, Biofilm-inactivating activity of silver nanoparticles: a comparison with silver ions, J Ind Eng Chem, 19, 614, 10.1016/j.jiec.2012.09.013 Peppas, 1975, Turbidimetric studies of aqueous poly(vinyl alcohol) solutions, Makromol Chem, 176, 3433, 10.1002/macp.1975.021761125 Proctor, 2020, Furanone quorum-sensing inhibitors with potential as novel therapeutics against Pseudomonas aeruginosa, J Med Microbiol, jmm001144 Rasamiravaka, 2015, The Formation of biofilms by Pseudomonas aeruginosa : a review of the natural and synthetic compounds interfering with control mechanisms, BioMed Res Int, 1, 10.1155/2015/759348 Ren, 2001, Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5- (bromomethylene) -3- butyl-2 (5H) -furanone, Environ Microbiol, 3, 731, 10.1046/j.1462-2920.2001.00249.x Rezzoagli, 2020, Combining antibiotics with antivirulence compounds can have synergistic effects and reverse selection for antibiotic resistance in Pseudomonas aeruginosa, PLoS Biol, 18, 10.1371/journal.pbio.3000805 Ruffin, 2016, Quorum-sensing inhibition abrogates the deleterious impact of Pseudomonas aeruginosa on airway epithelial repair, FASEB (Fed Am Soc Exp Biol) J, 30, 3011 Sanz, 2017, Role of microbial biofilms in the maintenance of oral health and in the development of dental caries and periodontal diseases. Consensus report of group 1 of the Joint EFP/ORCA workshop on the boundaries between caries and periodontal disease, J Clin Periodontol, 44, S5, 10.1111/jcpe.12682 Scribani Rossi, 2022 Sen, 2019, Human wounds and its burden: an updated compendium of estimates, Adv Wound Care, 8, 39, 10.1089/wound.2019.0946 Singh, 2000, Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms, Nature, 407, 762, 10.1038/35037627 Veronovski, 2012, Synthesis and use of organic biodegradable aerogels as drug carriers, J Biomater Sci Polym Ed, 23, 873, 10.1163/092050611X566126 Waite, 2005, Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms, J Bacteriol, 187, 6571, 10.1128/JB.187.18.6571-6576.2005 Waite, 2006, Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles, BMC Genom, 7, 162, 10.1186/1471-2164-7-162 Wang, 2019, Bioinspired aerogel based on konjac glucomannan and functionalized carbon nanotube for controlled drug release, Int J Biol Macromol, 133, 693, 10.1016/j.ijbiomac.2019.04.148 Witsø, 2014, Thiophenone and furanone in control of Escherichia coli O103:H2 virulence, Pathog Dis, 70, 297, 10.1111/2049-632X.12128 Wolcott, 2008, Biofilms and chronic wound inflammation, J Wound Care, 17, 333, 10.12968/jowc.2008.17.8.30796 Wu, 2004, Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice, J Antimicrob Chemother, 53, 1054, 10.1093/jac/dkh223 Wu, 2019 Wu, 2019, Biofilms in chronic wounds: pathogenesis and diagnosis, Trends Biotechnol, 37, 505, 10.1016/j.tibtech.2018.10.011 Ye, 2018, Morphological, release and antibacterial performances of amoxicillin-loaded cellulose aerogels, Molecules, 23, 10.3390/molecules23082082 Yujie, 2013, The effect of brominated furanones on the formation of Staphylococcus aureus biofilm on PVC, Cell Biochem Biophys, 67, 1501, 10.1007/s12013-013-9652-2 Zhang, 2005, Aligned two- and three-dimensional structures by directional freezing of polymers and nanoparticles, Nat Mater, 4, 787, 10.1038/nmat1487 Zhang, 2014, Advanced materials and processing for drug delivery: the past and the future, Adv Drug Deliv Rev, 65, 104, 10.1016/j.addr.2012.10.003