2-Aminoimidazoles as potent inhibitors of contaminating brewery biofilms

References

• Allen RC, Popat R, Diggle SP, Brown SP. 2014. Targeting virulence: can we make evolution-proof drugs? Nat Rev Microbiol. 12:300–308. doi:10.1038/nrmicro3232
   PubMed Web of Science ®Google Scholar
• Arnaouteli S, Matoz-Fernandez DA, Porter M, Kalamara M, Abbott J, MacPhee E, Davidson FA, Stanley-Wall NR. 2019. Pulcherrimin formation controls growth arrest of the Bacillus subtilis biofilm. Proc Natl Acad Sci USA. 116:13553–13562. doi:10.1073/pnas.1903982116
   PubMed Web of Science ®Google Scholar
• Bakar J, Ahangari R, Abdul Rahman R, Karim R. 2017. Antibacterial properties of tannic acid incorporated rice starch-gelatin film. Int Proc Chem Biol Environ Eng. 100.
   Google Scholar
• Bjarnsholt T. 2011. Introduction to biofilms. In: Bjarnsholt T, Jensen P, Moser C, Høiby N, editors. Biofilm infections. New York, NY: Springer; p. 1–9.
   Google Scholar
• Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling. 27:1017–1032. doi:10.1080/08927014.2011.626899
   PubMed Web of Science ®Google Scholar
• Burmolle M, Ren D, Bjarnsholt T, Sorensen SJ. 2014. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 22:84–91. doi:10.1016/j.tim.2013.12.004
   PubMed Web of Science ®Google Scholar
• Cai H, Archambault M, Prescott JF. 2003. 16S ribosomal RNA sequence-based identification of veterinary clinical bacteria. J Vet Diagn Invest. 15:465–469. doi:10.1177/104063870301500511
   PubMed Web of Science ®Google Scholar
• Cai W, Fu Y, Zhang W, Chen X, Zhao J, Song W, Li Y, Huang Y, Wu Z, Sun R, et al. 2016. Synergistic effects of baicalein with cefotaxime against Klebsiella pneumoniae through inhibiting CTX-M-1 gene expression. BMC Microbiol. 16:181. doi:10.1186/s12866-016-0797-1
   PubMed Web of Science ®Google Scholar
• Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A. 1999. The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol. 37:1771–1776. doi:10.1128/JCM.37.6.1771-1776.1999
   PubMed Web of Science ®Google Scholar
• Chambers J, Sauer K. 2013. Small RNAs and their role in biofilm formation. Trends Microbiol. 21:39–49. doi:10.1016/j.tim.2012.10.008
   PubMed Web of Science ®Google Scholar
• Chan BCL, Ip M, Lau CBS, Lui SL, Jolivalt C, Ganem-Elbaz C, Litaudon M, Reiner NE, Gong H, See RH, et al. 2011. Synergistic effects of baicalein with ciprofloxacin against NorA over-expressed methicillin-resistant Staphylococcus aureus (MRSA) and inhibition of MRSA pyruvate kinase. J Ethnopharmacol. 137:767–773. doi:10.1016/j.jep.2011.06.039
   PubMed Web of Science ®Google Scholar
• Chen Y, Liu T, Wang K, Hou C, Cai S, Huang Y, Du Z, Huang H, Kong J, Chen Y. 2016. Baicalein inhibits Staphylococcus aureus biofilm formation and the quorum sensing system in vitro. PLoS One. 11:e0153468. doi:10.1371/journal.pone.0153468
   PubMed Web of Science ®Google Scholar
• Chen M, Su C, Yang J, Lu C, Hou Y, Wu J, Hsu Y. 2018. Baicalin, baicalein, and Lactobacillus rhamnosus JB3 alleviated Helicobacter pylori infections in vitro and in vivo. J Food Sci. 83:3118–3125. doi:10.1111/1750-3841.14372
   PubMed Web of Science ®Google Scholar
• Chung KT, Wong TY, Wei CI, Huang YW, Lin Y. 1998. Tannins and human health: a review. Crit Rev Food Sci Nutr. 38:421–464. doi:10.1080/10408699891274273
   PubMed Web of Science ®Google Scholar
• Claes B, Boudewijns T, Muchez L, Hooyberghs G, Van der Eycken E, Vanderleyden J, Steenackers H, De Vos DE. 2017. Smart metal-organic framework coatings: triggered antibiofilm compound release . ACS Appl Mater Interfaces. 9:4440–4449. doi:10.1021/acsami.6b14152
   PubMed Web of Science ®Google Scholar
• Delimont NM, Haub MD, Lindshield BL. 2017. The impact of tannin consumption on iron bioavailability and status: a narrative review. Curr Dev Nutr. 1:1–12. doi:10.3945/cdn.116.000042
   PubMed Web of Science ®Google Scholar
• Di Somma A, Moretta A, Canè C, Cirrilo A, Duilio A. 2020. Inhibition of bacterial biofilm formation. In: Dincer S, Özdenefe MS, Arkut A, editors. Bacterial biofilms. London: IntechOpen.
   Google Scholar
• Dieltjens L, Appermans K, Lissens M, Lories B, Kim W, Van der Eycken EV, Foster KR, Steenackers HP. 2020. Inhibiting bacterial cooperation is an evolutionarily robust anti-biofilm strategy. Nat Commun. 11:107. doi:10.1038/s41467-019-13660-x
   PubMed Web of Science ®Google Scholar
• Dinda B, Dinda S, Dassharma S, Banik R, Chakraborty A, Dinda M. 2017. Therapeutic potentials of baicalin and its aglycone, baicalein against inflammatory disorders. Eur J Med Chem. 131:68–80. doi:10.1016/j.ejmech.2017.03.004
   PubMed Web of Science ®Google Scholar
• Estrela S, Brown SP, Alizon S. 2018. Community interactions and spatial structure shape selection on antibiotic resistant lineages. PLoS Comput Biol. 14:e1006179. doi:10.1371/journal.pcbi.1006179
   PubMed Web of Science ®Google Scholar
• Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F. 2018. Biofilms in the food industry: health aspects and control methods. Front Microbiol. 9:898. doi:10.3389/fmicb.2018.00898
   PubMed Web of Science ®Google Scholar
• Gill R, Kumar V, Robijns S, Steenackers H, Van Der Eycken E, Bariwal J. 2017. Polysubstituted 2-aminoimidazoles as anti-biofilm and antiproliferative agents: discovery of potent lead. Eur J Med Chem. 138:152–169. doi:10.1016/j.ejmech.2017.06.043
   PubMed Web of Science ®Google Scholar
• Halim ALA, Kamari A, Phillip E. 2018. Chitosan, gelatin and methylcellulose films incorporated with tannic acid for food packaging. Int J Biol Macromol. 120: 1119–1126. doi:10.1016/j.ijbiomac.2018.08.169
   PubMed Web of Science ®Google Scholar
• Hanke S, Stettner G. 2012. Use of tannins for beer stabilization during end-filtration. In: Master Brewers Association of the Americas (MBAA), editor. World Brewing Congress 2012. Proceedings of the 2012 World Brewing Congress; Jul 28–Aug 1. Portland, OR. p. 141.
   Google Scholar
• Hantsis-Zacharov E, Halpern M. 2007. Culturable psychrotrophic bacterial communities in raw milk and their proteolytic and lipolytic traits. Appl Environ Microbiol. 73:7162–7168. doi:10.1128/AEM.00866-07
   PubMed Web of Science ®Google Scholar
• Hathroubi S, Mekni MA, Domenico P, Nguyen D, Jacques M. 2017. Biofilms: microbial shelters against antibiotics. Microb Drug Resist. 23:147–156. doi:10.1089/mdr.2016.0087
   PubMed Web of Science ®Google Scholar
• Hsieh C, Hall K, Ha T, Li C, Krishnaswamy G, Chi DS. 2007. Baicalein inhibits IL-1beta- and TNF-alpha-induced inflammatory cytokine production from human mast cells via regulation of the NF-kappaB pathway . Clin Mol Allergy. 5:5. doi:10.1186/1476-7961-5-5
   PubMedGoogle Scholar
• Javed H, Ojha S. 2019. Therapeutic potential of baicalein in Parkinson’s disease: focus on inhibition of α -synuclein oligomerization and aggregation. In: Surguchov A, editor. Synucleins – biochemistry and role in diseases. London: IntechOpen.
   Google Scholar
• Li J, Tian C, Xia Y, Mutanda I, Wang K, Wang Y. 2019. Production of plant-specific flavones baicalein and scutellarein in an engineered E. coli from available phenylalanine and tyrosine. Metab Eng. 52:124–133. doi:10.1016/j.ymben.2018.11.008
   PubMed Web of Science ®Google Scholar
• Liu H, Dong Y, Gao Y, Du Z, Wang Y, Cheng P, Chen A, Huang H. 2016. The fascinating effects of baicalein on cancer: a review. IJMS. 17:1681. doi:10.3390/ijms17101681
   Web of Science ®Google Scholar
• Liu Y, Zhao Y, Guo D, Liu W, Liu Y. 2017. Synergistic antimicrobial activity of berberine hydrochloride, baicalein and borneol against Candida albicans. Chin Herb Med. 9:353–357. doi:10.1016/S1674-6384(17)60115-1
   Web of Science ®Google Scholar
• Lories B, Roberfroid S, Dieltjens L, De Coster D, Foster KR, Steenackers HP. 2020. Biofilm bacteria use stress responses to detect and respond to competitors. Curr Biol. 30:1231–1244.e4. doi:10.1016/j.cub.2020.01.065
   PubMed Web of Science ®Google Scholar
• Maifreni M, Frigo F, Bartolomeoli I, Buiatti S, Picon S, Marino M. 2015. Bacterial biofilm as a possible source of contamination in the microbrewery environment. Food Control. 50:809–814. doi:10.1016/j.foodcont.2014.10.032
   Web of Science ®Google Scholar
• Mastanjevic K, Krstanovic V, Lukinac J, Jukic M, Vulin Z, Mastanjevic K. 2018. Beer – the importance of colloidal stability (non-biological haze). Fermentation. 4:91. doi:10.3390/fermentation4040091
   Google Scholar
• Pandin C, Le Coq D, Canette A, Aymerich S, Briandet R. 2017. Should the biofilm mode of life be taken into consideration for microbial biocontrol agents? Microb Biotechnol. 10:719–734. doi:10.1111/1751-7915.12693
   PubMed Web of Science ®Google Scholar
• Parijs IP, Steenackers H. 2018. Competitive inter-species interactions underlie the increased antimicrobial tolerance in multispecies brewery biofilms. Isme J. 12:2061–2075. doi:10.1038/s41396-018-0146-5
   PubMed Web of Science ®Google Scholar
• Peeters E, Hooyberghs G, Robijns S, De Weerdt A, Kucharíková S, Tournu H, Braem A, Čeh K, Majdič G, Španič T, et al. 2019. An antibiofilm coating of 5-aryl-2-aminoimidazole covalently attached to a titanium surface . J Biomed Mater Res B Appl Biomater. 107:1908–1919. doi:10.1002/jbm.b.34283
   PubMed Web of Science ®Google Scholar
• Peeters E, Hooyberghs G, Robijns S, Waldrant K, De Weerdt A, Delattin N, Liebens V, Kucharíková S, Tournu H, Verstraeten N, et al. 2016. Modulation of the substitution pattern of 5-aryl-2-aminoimidazoles allows fine-tuning of their antibiofilm activity spectrum and toxicity. Antimicrob Agents Chemother. 60:6483–6497. doi:10.1128/AAC.00035-16
   PubMed Web of Science ®Google Scholar
• Pizzi A, Stracke P, Trosa A. 1997. Industrial tannin/hexamine low-emission exterior particleboards. Holz Als Roh-Und Werkstoff. 55:168–168. doi:10.1007/BF02990538
   Google Scholar
• Priha O, Raulio M, Cooke K, Fisher L, Hill C, Hylkinen S, Kelly P, Navabpour P, Ostovarpour S, Tapani K, et al. 2015. Microbial populations on brewery filling hall surfaces – progress towards functional coatings. Food Control. 55:1–11. doi:10.1016/j.foodcont.2015.02.022
   Web of Science ®Google Scholar
• Priha O, Raulio M, Maukonen J, Vehviläinen A, Storgards E. 2016. Bacterial populations on brewery filling hall surfaces as revealed by next-generation sequencing. Biofouling. 32:571–581. doi:10.1080/08927014.2016.1154946
   PubMed Web of Science ®Google Scholar
• Qvortrup K, Hultqvist LD, Nilsson M, Jakobsen TH, Jansen CU, Uhd J, Andersen JB, Nielsen TE, Givskov M, Tolker-Nielsen T. 2019. Small molecule anti-biofilm agents developed on the basis of mechanistic understanding of biofilm formation. Front Chem. 7:742 doi:10.3389/fchem.2019.00742
   PubMed Web of Science ®Google Scholar
• Rabin N, Zheng Y, Opoku-Temeng C, Du Y, Bonsu E, Sintim HO. 2015. Agents that inhibit bacterial biofilm formation. Future Med Chem. 7:647–671. doi:10.4155/fmc.15.7
   PubMed Web of Science ®Google Scholar
• Rehmanji M, Gopal C, Mola A. 2005. Beer stabilization technology – clearly a matter of choice. Mbaa Tq. 42:332–338.
   Google Scholar
• Rezzoagli C, Wilson D, Weigert M, Wyder S, Kümmerli R. 2018. Probing the evolutionary robustness of two repurposed drugs targeting iron uptake in Pseudomonas aeruginosa. Evol Med Public Health. 2018:246–259. doi:10.1093/emph/eoy026
   PubMedGoogle Scholar
• Ross-Gillespie A, Weigert M, Brown S, Kümmerli R. 2014. Gallium-mediated siderophore quenching as an evolutionarily robust antibacterial treatment. Evol Med Public Health. 2014:18–29. doi:10.1093/emph/eou003
   PubMedGoogle Scholar
• Schwartz S. 2008. Psychoactive herbs in veterinary behavior medicine. New Jersey, NJ: Wiley.
   Google Scholar
• Si D, Wang Y, Zhou Y, Guo Y, Wang J, Zhou H, Li ZS, Fawcett JP. 2009. Mechanism of CYP2C9 inhibition by flavones and flavonols. Drug Metab Dispos. 37:629–634. doi:10.1124/dmd.108.023416
   PubMed Web of Science ®Google Scholar
• Singh AP, Kumar S. 2019. Applications of tannins in industry. In: Aires A, editor. Tannins – Structural properties, biological properties and current knowledge. London: IntechOpen.
   Google Scholar
• Steenackers H, Dubey A, Robijns S, Ermolat'Ev D, Delattin N, Dovgan B, Girandon L, Fröhlich M, De Brucker K, Cammue BPA, et al. 2014. Evaluation of the toxicity of 5-aryl-2-aminoimidazole-based biofilm inhibitors against eukaryotic cell lines, bone cells and the nematode Caenorhabditis elegans. Molecules. 19:16707–16723. doi:10.3390/molecules191016707
   PubMed Web of Science ®Google Scholar
• Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SCJ. 2012. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int. 45:502–531. doi:10.1016/j.foodres.2011.01.038
   Web of Science ®Google Scholar
• Steenackers HPL, Ermolat'ev DS, Savaliya B, Weerdt AD, Coster DD, Shah A, Van der Eycken EV, De Vos DE, Vanderleyden J, De Keersmaecker SCJ. 2011. Structure-activity relationship of 2-hydroxy-2-aryl-2,3-dihydro-imidazo[1,2-a]pyrimidinium salts and 2N-substituted 4(5)-aryl-2-amino-1H-imidazoles as inhibitors of biofilm formation by Salmonella Typhimurium and Pseudomonas aeruginosa. Bioorg Med Chem. 19:3462–3473. doi:10.1016/j.bmc.2011.04.026
   PubMed Web of Science ®Google Scholar
• Stowe SD, Richards JJ, Tucker AT, Thompson R, Melander C, Cavanagh J. 2011. Anti-biofilm compounds derived from marine sponges. Mar Drugs. 9:2010–2035. doi:10.3390/md9102010
   PubMed Web of Science ®Google Scholar
• Tabbene O, Azaiez S, Di Grazia A, Karkouch I, Ben Slimene I, Elkahoui S, Alfeddy MN, Casciaro B, Luca V, Limam F, et al. 2016. Bacillomycin D and its combination with amphotericin B: promising antifungal compounds with powerful antibiofilm activity and wound-healing potency. J Appl Microbiol. 120:289–300. doi:10.1111/jam.13030
   PubMed Web of Science ®Google Scholar
• Timke M, Wang-Lieu NQ, Altendorf K, Lipski A. 2008. Identity, beer spoiling and biofilm forming potential of yeasts from beer bottling plant associated biofilms. Antonie Van Leeuwenhoek. 93:151–161. doi:10.1007/s10482-007-9189-8
   PubMed Web of Science ®Google Scholar
• Timke M, Wolking D, Wang-Lieu NQ, Altendorf K, Lipski A. 2004. Microbial composition of biofilms in a brewery investigated by fatty acid analysis, fluorescence in situ hybridisation and isolation techniques. Appl Microbiol Biotechnol. 66:100–107. doi:10.1007/s00253-004-1601-y
   PubMed Web of Science ®Google Scholar
• Tintino SR, Morais-Tintino CD, Campina FF, Costa MDS, Menezes IRA, de Matos YMLS, Calixto-Júnior JT, Pereira PS, Siqueira-Junior JP, Leal-Balbino TC, et al. 2017. Tannic acid affects the phenotype of Staphylococcus aureus resistant to tetracycline and erythromycin by inhibition of efflux pumps. Bioorg Chem. 74:197–200. doi:10.1016/j.bioorg.2017.08.004
   PubMed Web of Science ®Google Scholar
• Walker SL, Fourgialakis M, Cerezo B, Livens S. 2007. Removal of microbial biofilms from dispense equipment: the effect of enzymatic pre-digestion and detergent treatment. J Inst Brew. 113:61–66. doi:10.1002/j.2050-0416.2007.tb00257.x
   Web of Science ®Google Scholar
• Wang Y, Li J, Li B. 2016. Nature-inspired one-step green procedure for enhancing the antibacterial and antioxidant behavior of a chitin film: controlled interfacial assembly of tannic acid onto a chitin film. J Agric Food Chem. 64:5736–5741. doi:10.1021/acs.jafc.6b01859
   PubMed Web of Science ®Google Scholar
• Wasowski C, Marder M. 2012. Flavonoids as GABAA receptor ligands: the whole story? J Exp Pharmacol. 4:9–24. doi:10.2147/JEP.S23105
   PubMedGoogle Scholar
• White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc A Guid to Methods Appl. 31:315–322.
   Google Scholar
• Worthington RJ, Richards JJ, Melander C. 2012. Small molecule control of bacterial biofilms. Org Biomol Chem. 10:7457–7474. doi:10.1039/c2ob25835h
   PubMed Web of Science ®Google Scholar