Volume 12 Issue 1
Feb.  2022
Turn off MathJax
Article Contents
Lan Lu, Mingxing Li, Guojuan Yi, Li Liao, Qiang Cheng, Jie Zhu, Bin Zhang, Yingying Wang, Yong Chen, Ming Zeng. Screening strategies for quorum sensing inhibitors in combating bacterial infections[J]. Journal of Pharmaceutical Analysis, 2022, 12(1): 1-14. doi: 10.1016/j.jpha.2021.03.009
Citation: Lan Lu, Mingxing Li, Guojuan Yi, Li Liao, Qiang Cheng, Jie Zhu, Bin Zhang, Yingying Wang, Yong Chen, Ming Zeng. Screening strategies for quorum sensing inhibitors in combating bacterial infections[J]. Journal of Pharmaceutical Analysis, 2022, 12(1): 1-14. doi: 10.1016/j.jpha.2021.03.009

Screening strategies for quorum sensing inhibitors in combating bacterial infections

doi: 10.1016/j.jpha.2021.03.009
Funds:

This study was funded by the National Natural Science Foundation of China (Grant No.: 81803812).

  • Received Date: Aug. 12, 2020
  • Accepted Date: Mar. 25, 2021
  • Rev Recd Date: Mar. 04, 2021
  • Publish Date: Apr. 02, 2021
  • Interference with quorum sensing (QS) represents an antivirulence strategy with a significant promise for the treatment of bacterial infections and a new approach to restoring antibiotic tolerance. Over the past two decades, a novel series of studies have reported that quorum quenching approaches and the discovery of quorum sensing inhibitors (QSIs) have a strong impact on the discovery of anti-infective drugs against various types of bacteria. The discovery of QSI was demonstrated to be an appropriate strategy to expand the anti-infective therapeutic approaches to complement classical antibiotics and antimicrobial agents. For the discovery of QSIs, diverse approaches exist and develop in-step with the scale of screening as well as specific QS systems. This review highlights the latest findings in strategies and methodologies for QSI screening, involving activity-based screening with bioassays, chemical methods to seek bacterial QS pathways for QSI discovery, virtual screening for QSI screening, and other potential tools for interpreting QS signaling, which are innovative routes for future efforts to discover additional QSIs to combat bacterial infections.
  • loading
  • I. Olsen, Biofilm-specific antibiotic tolerance and resistance, Eur. J. Clin. Microbiol. Infect. Dis. 34(2015)877-886
    H. Cho, T. Uehara, T.G. Bernhardt, Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery, Cell. 159(2014)1300-1311
    G. Mina, C. Chbib, Recent progresses on synthesized LuxS inhibitors:A mini-review, Bioorg. Med. Chem. 27(2019)36-42
    S.B. Levy, B. Marshall, Antibacterial resistance worldwide:causes, challenges and responses, Nat. Med. 10(2004) S122-S129
    V. Roy, B.L. Adams, W.E. Bentley, Developing next generation antimicrobials by intercepting AI-2 mediated quorum sensing, Enzyme. Microb. Technol. 49(2011)113-123
    K. Vadakkan, A.A. Choudhury, R. Gunasekaran, et al., Quorum sensing intervened bacterial signaling:Pursuit of its cognizance and repression, J. Genet. Eng. Biotechnol. 16(2018)239-252
    B. Subhadra, D.H. Kim, K. Woo, et al., Control of biofilm formation in healthcare:recent advances exploiting quorum-sensing interference strategies and multidrug efflux pump inhibitors, Materials.(Basel)11(2018), 1676
    F. Soukarieh, P. Williams, M.J. Stocks, et al., Pseudomonas aeruginosa quorum sensing systems as drug discovery targets:current position and future perspectives, J. Med. Chem. 61(2018)10385-10402
    S. Manner, A. Fallarero, Screening of natural product derivatives identifies two structurally related flavonoids as potent quorum sensing inhibitors against Gram-negative bacteria, Int. J. Mol. Sci. 19(2018), 1346
    S. Haque, F. Ahmad, S.A. Dar, et al., Developments in strategies for quorum sensing virulence factor inhibition to combat bacterial drug resistance, Microb. Pathog. 121(2018)293-302
    X. He, F. Lu, F. Yuan, et al., Biofilm formation caused by clinical Acinetobacter baumannii isolates is associated with overexpression of the AdeFGH efflux pump, Antimicrob. Agents. Chemother. 59(2015)4817-4825
    T. Defoirdt, Quorum-Sensing Systems as Targets for Antivirulence Therapy, Trends. Microbiol. 26(2018)313-328
    H. Gude, Grazing by protozoa as selection factor for activated sludge bacteria, Microb. Ecol. 5(1979)225-237
    K. Papenfort, B.L. Bassler, Quorum sensing signal-response systems in Gram-negative bacteria, Nat. Rev. Microbiol. 14(2016)576-588
    E. Wynendaele, A. Bronselaer, J. Nielandt, et al., Quorumpeps database:chemical space, microbial origin and functionality of quorum sensing peptides, Nucleic. Acids. Res. 41(2013) D655-D659
    F. Verbeke, S. De Craemer, N. Debunne, et al., Peptides as quorum sensing molecules:measurement techniques and obtained levels in vitro and in vivo, Front. Neurosci. 11(2017), 183
    M.A. Welsh, H.E. Blackwell, Chemical probes of quorum sensing:from compound development to biological discovery, FEMS Microbiol. Rev. 40(2016)774-794
    M. Kumar, M. Saxena, A.K. Saxena, et al., Recent breakthroughs in various antimicrobial resistance induced quorum sensing biosynthetic pathway mediated targets and design of their inhibitors, Comb. Chem. High. Throughput. Screen. 23(2020)458-476
    A. Holm, E. Vikstrom, Quorum sensing communication between bacteria and human cells:signals, targets, and functions, Front. Plant. Sci. 5(2014), 309
    Y.H. Dong, J.L. Xu, X.Z. Li, et al., AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora, Proc. Natl. Acad. Sci. U S A 97(2000)3526-3531
    K. Tang, X.H. Zhang, Quorum quenching agents:resources for antivirulence therapy, Mar. Drugs. 12(2014)3245-3282
    S. Fetzner, Quorum quenching enzymes, J. Biotechnol. 201(2015)2-14
    L. Lu, W. Hu, Z. Tian, et al., Developing natural products as potential anti-biofilm agents, Chin. Med. 14(2019), 11
    V.C. Kalia, S.K.S. Patel, Y.C. Kang, et al., Quorum sensing inhibitors as antipathogens:biotechnological applications, Biotechnol. Adv. 37(2019)68-90
    S. Nandi, Recent advances in ligand and structure based screening of potent quorum sensing inhibitors against antibiotic resistance induced bacterial virulence, Recent. Pat. Biotechnol. 10(2016)195-216
    J. Bzdrenga, D. Daude, B. Remy, et al., Biotechnological applications of quorum quenching enzymes, Chem. Biol. Interact. 267(2017)104-115
    C. Grandclement, M. Tannieres, S. Morera, et al., Quorum quenching:role in nature and applied developments, FEMS Microbiol. Rev. 40(2016)86-116
    N. Duran, G.Z. Justo, M. Duran, et al., Advances in Chromobacterium violaceum and properties of violacein-its main secondary metabolite:a review, Biotechnol. Adv. 34(2016)1030-1045
    A.T. Gemiarto, N.N. Ninyio, S.W. Lee, et al., Isoprenyl caffeate, a major compound in manuka propolis, is a quorum-sensing inhibitor in Chromobacterium violaceum, Antonie. Van. Leeuwenhoek. 108(2015)491-504
    H. Zhu, S.J. Sun, Inhibition of bacterial quorum sensing-regulated behaviors by tremella fuciformis extract, Curr. Microbiol. 57(2008)418-422
    F.D. Kong, L.M. Zhou, Q.Y. Ma, et al., Metabolites with Gram-negative bacteria quorum sensing inhibitory activity from the marine animal endogenic fungus Penicillium sp. SCS-KFD08, Arch. Pharm. Res. 40(2017)25-31
    Y. Zhang, Y. Yang, L. Wang, et al., Identification of a Pseudomonas sp. that inhibits RHL system of quorum sensing, Indian. J. Microbiol. 53(2013)28-35
    M.E. Teasdale, K.A. Donovan, S.R. Forschner-Dancause, et al., Gram-positive marine bacteria as a potential resource for the discovery of quorum sensing inhibitors, Mar. Biotechnol.(NY)13(2011)722-732
    M.E. Teasdale, J. Liu, J. Wallace, et al., Secondary metabolites produced by the marine bacterium Halobacillus salinus that inhibit quorum sensing-controlled phenotypes in gram-negative bacteria, Appl. Environ. Microbiol. 75(2009)567-572
    J.L. Meyer, S.P. Gunasekera, R.M. Scott, et al., Microbiome shifts and the inhibition of quorum sensing by black band disease cyanobacteria, ISME J. 10(2016)1204-1216
    M.K. Winson, S. Swift, L. Fish, et al., Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing, FEMS Microbiol. Lett. 163(1998)185-192
    M. Zhang, M. Wang, X. Zhu, et al., Equisetin as potential quorum sensing inhibitor of Pseudomonas aeruginosa, Biotechnol. Lett. 40(2018)865-870
    Y. Du, J. Sun, Q. Gong, et al., New alpha-pyridones with quorum-sensing inhibitory activity from diversity-enhanced extracts of a Streptomyces sp. derived from marine algae, J. Agric. Food. Chem. 66(2018)1807-1812
    L. Wang, S. Zou, S. Yin, et al., Construction of an effective screening system for detection of Pseudomonas aeruginosa quorum sensing inhibitors and its application in bioautographic thin-layer chromatography, Biotechnol. Lett. 33(2011)1381-1387
    B. Gokalsin, B. Aksoydan, B. Erman, et al., Reducing virulence and biofilm of Pseudomonas aeruginosa by potential quorum sensing inhibitor carotenoid:zeaxanthin, Microb. Ecol. 74(2017)466-473
    B. Gokalsin, N.C. Sesal, Lichen secondary metabolite evernic acid as potential quorum sensing inhibitor against Pseudomonas aeruginosa, World. J. Microbiol. Biotechnol. 32(2016), 150
    T.B. Rasmussen, T. Bjarnsholt, M.E. Skindersoe, et al., Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector, J. Bacteriol. 187(2005)1799-1814
    L. Peters, G.M. Konig, A.D. Wright, et al., Secondary metabolites of Flustra foliacea and their influence on bacteria, Appl. Environ. Microbiol. 69(2003)3469-3475
    K.M. Younis, G. Usup, A. Ahmad, Secondary metabolites produced by marine streptomyces as antibiofilm and quorum-sensing inhibitor of uropathogen Proteus mirabilis, Environ. Sci. Pollut. Res. Int. 23(2016)4756-4767
    Y.R. des Essarts, M. Sabbah, A. Comte, et al., N,N'-alkylated Imidazolium-derivatives act as quorum-sensing inhibitors targeting the Pectobacterium atrosepticum-induced symptoms on potato tubers, Int. J. Mol. Sci. 14(2013)19976-19986
    J.A. Gutierrez-Barranquero, F.J. Reen, R.R. McCarthy, et al., Deciphering the role of coumarin as a novel quorum sensing inhibitor suppressing virulence phenotypes in bacterial pathogens, Appl. Microbiol. Biotechnol. 99(2015)3303-3316
    D. Deryabin, A. Galadzhieva, D. Kosyan, et al., Plant-derived inhibitors of AHL-mediated quorum sensing in bacteria:modes of action, Int. J. Mol. Sci. 20(2019), 5588
    C. Joshi, V. Kothari, P. Patel, Importance of selecting appropriate wavelength, while quantifying growth and production of quorum sensing regulated pigments in bacteria, Recent. Pat. Biotechnol. 10(2016)145-152
    J.E. Swatton, P.W. Davenport, E.A. Maunders, et al., Impact of azithromycin on the quorum sensing-controlled proteome of pseudomonas aeruginosa, PLoS. One. 11(2016), e0147698
    S. Ahmed, M. Rudden, T.J. Smyth, et al., Natural quorum sensing inhibitors effectively downregulate gene expression of Pseudomonas aeruginosa virulence factors, Appl. Microbiol. Biotechnol. 103(2019)3521-3535
    K.L. Asfahl, M. Schuster, Additive effects of quorum sensing anti-activators on Pseudomonas aeruginosa virulence traits and transcriptome, Front. Microbiol. 8(2017), 2654
    C. Kong, S.A. Eng, M.P. Lim, et al., Beyond traditional antimicrobials:a Caenorhabditis elegans model for discovery of novel anti-infectives, Front. Microbiol. 7(2016), 1956
    H.B. van der Worp, D.W. Howells, E.S. Sena, et al., Can animal models of disease reliably inform human studies?, PLoS. Med. 7(2010), e1000245
    N.A. Boyle, K.D. Janda, Formats for combinatorial synthesis:solid-phase, liquid-phase and surface, Curr. Opin. Chem. Biol. 6(2002)339-346
    G.D. Geske, J.C. O'Neill, D.M. Miller, et al., Modulation of bacterial quorum sensing with synthetic ligands:systematic evaluation of N-acylated homoserine lactones in multiple species and new insights into their mechanisms of action, J. Am. Chem. Soc. 129(2007)13613-13625
    G.D. Geske, R.J. Wezeman, A.P. Siegel, et al., Small molecule inhibitors of bacterial quorum sensing and biofilm formation, J. Am. Chem. Soc. 127(2005)12762-12763
    G.D. Geske, M.E. Mattmann, H.E. Blackwell, Evaluation of a focused library of N-aryl L-homoserine lactones reveals a new set of potent quorum sensing modulators, Bioorg. Med. Chem. Lett. 18(2008)5978-5981
    Q. Lin, H.E. Blackwell, Rapid synthesis of diketopiperazine macroarrays via Ugi four-component reactions on planar solid supports, Chem. Commun.(Camb)(2006)2884-2886
    Q. Lin, J.C. O'Neill, H.E. Blackwell, Small molecule macroarray construction via Ugi four-component reactions, Org. Lett. 7(2005)4455-4458
    M.D. Bowman, R.C. Jeske, H.E. Blackwell, Microwave-accelerated SPOT-synthesis on cellulose supports, Org. Lett. 6(2004)2019-2022
    M.D. Bowman, M.M. Jacobson, H.E. Blackwell, Discovery of fluorescent cyanopyridine and deazalumazine dyes using small molecule macroarrays, Org. Lett. 8(2006)1645-1648
    T. Praneenararat, A.G. Palmer, H.E. Blackwell, Chemical methods to interrogate bacterial quorum sensing pathways, Org. Biomol. Chem. 10(2012)8189-8199
    T. Praneenararat, G.D. Geske, H.E. Blackwell, Efficient synthesis and evaluation of quorum-sensing modulators using small molecule macroarrays, Org. Lett. 11(2009)4600-4603
    H.E. Blackwell, Hitting the SPOT:small-molecule macroarrays advance combinatorial synthesis, Curr. Opin. Chem. Biol. 10(2006)203-212
    S.A. Fowler, D.M. Stacy, H.E. Blackwell, Design and synthesis of macrocyclic peptomers as mimics of a quorum sensing signal from Staphylococcus aureus, Org. Lett. 10(2008)2329-2332
    D.P. Walsh, Y.T. Chang, Recent advances in small molecule microarrays:applications and technology, Comb. Chem. High. Throughput. Screen. 7(2004)557-564
    D.M. Marsden, R.L. Nicholson, M. Ladlow, et al., 3D small-molecule microarrays, Chem. Commun.(Camb)(2009)7107-7109
    D.M. Marsden, R.L. Nicholson, M.E. Skindersoe, et al., Discovery of a quorum sensing modulator pharmacophore by 3D small-molecule microarray screening, Org. Biomol. Chem. 8(2010)5313-5323
    B.J. Leslie, P.J. Hergenrother, Identification of the cellular targets of bioactive small organic molecules using affinity reagents, Chem. Soc. Rev. 37(2008)1347-1360
    R.J. Spandl, R.L. Nicholson, D.M. Marsden, et al., Synthesis of a Biotin-Labeled Quorum-Sensing Molecule:Towards a General Method for Target Identification, Synlett. 14(2008)2122-2126
    G. Telford, D. Wheeler, P. Williams, et al., The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity, Infect. Immun. 66(1998)36-42
    N. Amara, B.P. Krom, G.F. Kaufmann, et al., Macromolecular inhibition of quorum sensing:enzymes, antibodies, and beyond, Chem. Rev. 111(2011)195-208
    G.F. Kaufmann, R. Sartorio, S.H. Lee, et al., Revisiting quorum sensing:discovery of additional chemical and biological functions for 3-oxo-N-acylhomoserine lactones, Proc. Natl. Acad. Sci. U S A 102(2005)309-314
    B. Remy, S. Mion, L. Plener, et al., Interference in bacterial quorum sensing:a biopharmaceutical perspective, Front. Pharmacol. 9(2018), 203
    G.F. Kaufmann, R. Sartorio, S.H. Lee, et al., Antibody interference with N-acyl homoserine lactone-mediated bacterial quorum sensing, J. Am. Chem. Soc. 128(2006)2802-2803
    J. Park, R. Jagasia, G.F. Kaufmann, et al., Infection control by antibody disruption of bacterial quorum sensing signaling, Chem. Biol. 14(2007)1119-1127
    S. De Lamo Marin, Y. Xu, M.M. Meijler, et al., Antibody catalyzed hydrolysis of a quorum sensing signal found in Gram-negative bacteria, Bioorg. Med. Chem. Lett. 17(2007)1549-1552
    E.V. Piletska, G. Stavroulakis, K. Karim, et al., Attenuation of Vibrio fischeri quorum sensing using rationally designed polymers, Biomacromolecules. 11(2010)975-980
    E.V. Piletska, G. Stavroulakis, L.D. Larcombe, et al., Passive control of quorum sensing:prevention of Pseudomonas aeruginosa biofilm formation by imprinted polymers, Biomacromolecules. 12(2011)1067-1071
    A.S. Breitbach, A.H. Broderick, C.M. Jewell, et al., Surface-mediated release of a synthetic small-molecule modulator of bacterial quorum sensing:gradual release enhances activity, Chem. Commun.(Camb)47(2011)370-372
    S.Y. Tan, S.L. Chua, Y. Chen, et al., Identification of five structurally unrelated quorum-sensing inhibitors of Pseudomonas aeruginosa from a natural-derivative database, Antimicrob. Agents. Chemother. 57(2013)5629-5641
    L. Yang, M.T. Rybtke, T.H. Jakobsen, et al., Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors, Antimicrob. Agents. Chemother. 53(2009)2432-2443
    A. Annapoorani, V. Umamageswaran, R. Parameswari, et al., Computational discovery of putative quorum sensing inhibitors against LasR and RhlR receptor proteins of Pseudomonas aeruginosa, J. Comput. Aided. Mol. Des. 26(2012)1067-1077
    S. Skovstrup, S.T. Le Quement, T. Hansen, et al., Identification of LasR ligands through a virtual screening approach, ChemMedChem. 8(2013)157-163
    M. Kalia, P.K. Singh, V.K. Yadav, et al., Structure based virtual screening for identification of potential quorum sensing inhibitors against LasR master regulator in Pseudomonas aeruginosa, Microb. Pathog. 107(2017)136-143
    S. Rajamanikandan, J. Jeyakanthan, P. Srinivasan, Discovery of potent inhibitors targeting Vibrio harveyi LuxR through shape and e-pharmacophore based virtual screening and its biological evaluation, Microb. Pathog. 103(2017)40-56
    S. Rajamanikandan, J. Jeyakanthan, P. Srinivasan, Molecular Docking, Molecular dynamics simulations, computational screening to design quorum sensing inhibitors targeting LuxP of Vibrio harveyi and its biological evaluation, Appl. Biochem. Biotechnol. 181(2017)192-218
    T. Ding, T. Li, J. Li, Identification of natural product compounds as quorum sensing inhibitors in Pseudomonas fluorescens P07 through virtual screening, Bioorg. Med. Chem. 26(2018)4088-4099
    Z. Zeng, L. Qian, L. Cao, et al., Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa, Appl. Microbiol. Biotechnol. 79(2008)119-126
    M. Kalia, V.K. Yadav, P.K. Singh, et al., Designing quorum sensing inhibitors of Pseudomonas aeruginosa utilizing FabI:an enzymic drug target from fatty acid synthesis pathway, 3 Biotech. 9(2019), 40
    F.A. Almeida, E.L.G. Vargas, D.G. Carneiro, et al., Virtual screening of plant compounds and nonsteroidal anti-inflammatory drugs for inhibition of quorum sensing and biofilm formation in Salmonella, Microb. Pathog. 121(2018)369-388
    J.L. Connell, E.T. Ritschdorff, M. Whiteley, et al., 3D printing of microscopic bacterial communities, Proc. Natl. Acad. Sci. U S A 110(2013)18380-18385
    J. Gomes, A. Grunau, A.K. Lawrence, et al., Bioinspired, releasable quorum sensing modulators, Chem. Commun.(Camb)49(2013)155-157
    C.G. Hebert, A. Gupta, R. Fernandes, et al., Biological nanofactories target and activate epithelial cell surfaces for modulating bacterial quorum sensing and interspecies signaling, ACS Nano. 4(2010)6923-6931
    H. Blackwell, T.-g. Yftah, D. Stacy, inventors; Peptide-based quorum sensing inhibitors for the attenuation of virulence in Staphylococcus aureus, United States patent US2020140489A1. 7 May 2020
    B. Kim, E. Ryu, J. Park, et al., Inventors; Novel brominated furanone derivative, method for preparing same, and pharmaceutical composition containing same as active ingredient, PCT patent WO2019221513A1. 21 November 2019.
    R. Alarcon, A. Mcnulty, Inventors; Targeted Enzymatic Degradation of Quorum Sensing Peptides, United States Patent US2019298872A1. 3 October 2019.
    H. Zhu, S. Sun, Y. Wang, et al., Inventors; Applications of 3,4,5-methyl trihydroxybenzoate in inhibition of the activity of bacterial quorum sensing system, Chinese patent CN110692636A. 17 January 2020.
    B. Choi, E. Ryu, J. Sim, et al., Inventors; Method of Inhibiting Quorum Sensing Using D-Galactose, United States Patent US2019224222A1. 25 July 2019.
    Y. Li, W. Wang, S. Wu, et al., Inventors; Preparation Method and Application of Camphor Essential Oil-Based Bacterial Quorum Sensing Inhibitor, Chinese patent CN109463402A. 15 March 2019.
    N. Klaus N, Inventors; Animal feed additive for quorum sensing inhibition and from timbers, PCT patent WO2018153804A1. 30 August 2018.
    B. Bassler, H. Stone, M. Kim, Inventors; Diagnostic and Therapeutic Quorum-Sensing-Manipulation Molecules that Are Trackable for Healthcare and Industrial Systems, United States patent US2018346525A1. 6 December 2018.
    B. Marte, Inventor; Formulation of banana pseuostem liquid extract and its usesFormulation of banana pseuostem liquid extract and its uses, 2019 Philippine Patent PH12018000039A1. 14 August 2019.
    Liu Z., Dong R., Zeng M., Inventors;Synergist for Food Biological Preservative and Use Method of Synergist, Chinese Patent CN109043290A. 21 December 2018.
    Y. Xiong, Y. Liu, Inventors; Application of Pyrimidine Derivative in Preparing Medicine for Inhibiting Bacterial Quorum Sensing System, Chinese patent CN107019699A. 8 August 2017.
    C. Pearce, J. Kavanaugh, Parlet C, et al., Inventors; Methods and compositions for the inhibition of quorum sensing in bacterial infections, PCT patent WO2017197303A1. 16 November 2017.
    S. Naik, S. Ching, J. Scholin, et al., Inventors; Application of Porous Materials for Bacterial Quorum Sensing Inhibition/disruption, United States patent US2017251674A1. 7 September 2017.
    H. Blackwell, M. Welsh, Inventors; Compound Combinations for Attenuation of Bacterial Virulence, United States patent US2017231962A1. 17 August 2017.
    G. Zheng, W. Tian, C. Yang, Inventors; Novel Application of lotus Plumule Extracts, Chinese Patent CN107951928A. 24 April 2018.
    H. Blackwell, T. Yang, Inventors; Peptidic Modulators of Quorum Sensing in staphylococcus Epidermidis, PCT Patent WO2017192442A2. 9 November 2017.
    H. Blackwell, M. Boursier, Inventors; Synthetic Ligands that Modulate the Activity of the RHLR Quorum Sensing Receptor, PCT patent WO2017190116A1. 2 November 2017.
    The Database of Privately and Publicly Funded Clinical Studies Conducted around the World, U.S. National Library of Medicine, https://www.clinicaltrials.gov/ct2/home. (Accessed 14 October 2020).
    M.F. Azad, A. Schwiertz, H.F. Jentsch, Adjunctive use of essential oils following scaling and root planing-a randomized clinical trial, BMC Complement. Altern. Med. 16(2016), 171
    M.M. Salles, M.M. Badaro, C.N. Arruda, et al., Antimicrobial activity of complete denture cleanser solutions based on sodium hypochlorite and Ricinus communis-a randomized clinical study, J. Appl. Oral. Sci. 23(2015)637-642
    P. Goes, C.S. Dutra, M.R. Lisboa, et al., Clinical efficacy of a 1% Matricaria chamomile L. mouthwash and 0.12% chlorhexidine for gingivitis control in patients undergoing orthodontic treatment with fixed appliances, J. Oral. Sci. 58(2016)569-574
    I. Singh, L.K. Gautam, I.R. Kaur, Effect of oral cranberry extract (standardized proanthocyanidin-A) in patients with recurrent UTI by pathogenic E. coli:a randomized placebo-controlled clinical research study, Int. Urol. Nephrol. 48(2016)1379-1386
    C.N.F. Arruda, M.M. Salles, M.M. Badaro, et al., Effect of sodium hypochlorite and Ricinus communis solutions on control of denture biofilm:a randomized crossover clinical trial, J. Prosthet. Dent. 117(2017)729-734
    H.R. Abdulbaqi, W.H. Himratul-Aznita, N.A. Baharuddin, Evaluation of Salvadora persica L. and green tea anti-plaque effect:a randomized controlled crossover clinical trial, BMC Complement. Altern. Med. 16(2016), 493
    T. Defoirdt, N. Boon, P. Bossier, Can bacteria evolve resistance to quorum sensing disruption?PLoS. Pathog. 6(2010), e1000989
    S. Koul, J. Prakash, A. Mishra, et al., Potential emergence of multi-quorum sensing inhibitor resistant (MQSIR) bacteria, Indian. J. Microbiol. 56(2016)1-18
    K.Y. Hur, M.S. Lee, Gut microbiota and metabolic disorders, Diabetes. Metab. J. 39(2015)198-203
    R.H. Certner, S.V. Vollmer, Inhibiting bacterial quorum sensing arrests coral disease development and disease-associated microbes, Environ. Microbiol. 20(2018)645-657
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(1)

    Article Metrics

    Article views (348) PDF downloads(11) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return