Eugenol exhibits anti-virulence properties by competitively binding to quorum sensing receptors

References

• Abbas HA, Serry FM, EL-Masry EM. 2012. Combating Pseudomonas aeruginosa biofilms by potential biofilm inhibitors. Asian J Res Pharm Sci. 2:66–72.
   Google Scholar
• Ashraf W, Bayston R, Stevenson O. 2010. The development of an antimicrobial EVD catheter to protect against multi-resistant hospital “superbugs”. Cerebrospinal Fluid Res. 7:S46. doi: 10.1186/1743-8454-7-S1-S46
   Google Scholar
• Aswathanarayan JB, Rai VR. 2015. Quorum-sensing systems in Pseudomonas. In: Kalia Vc, editor. Quorum sensing vs quorum quenching: a battle with no end in sight. Springer; p. 73–84.
   Google Scholar
• Bosso JA. 2005. The antimicrobial armamentarium: evaluating current and future treatment options. Pharmacotherapy: J Human Pharmacol Drug Therapy. 25:55S–62S. doi: 10.1592/phco.2005.25.10part2.55S
   Google Scholar
• Brelles-Mariño G, Bedmar EJ. 2001. Detection, purification and characterisation of quorum-sensing signal molecules in plant-associated bacteria. J Biotechnol. 91:197–209. doi: 10.1016/S0168-1656(01)00330-3
   PubMed Web of Science ®Google Scholar
• Chang MW, Ayeni C, Breuer S, Torbett BE. 2010. Virtual screening for HIV protease inhibitors: a comparison of AutoDock 4 and Vina. PLoS ONE. 5:e11955. doi: 10.1371/journal.pone.0011955
   PubMed Web of Science ®Google Scholar
• Choi Y, Park H-Y, Park SJ, Park S-J, Kim S-K, Ha C, Im S-J, Lee J-H. 2011. Growth phase-differential quorum sensing regulation of anthranilate metabolism in Pseudomonas aeruginosa. Mol Cell. 32:57–65. doi: 10.1007/s10059-011-2322-6
   Web of Science ®Google Scholar
• CLSI W. 2006. Clinical and laboratory standards institute methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobicall. Approve Standard M7-A7. 7th ed. Pennsylvania (USA): CLSI.
   Google Scholar
• Cox CD, Adams P. 1985. Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect Immun.48:130–138.
   PubMed Web of Science ®Google Scholar
• Das MC, Sandhu P, Gupta P, Rudrapaul P, De UC, Tribedi P, Akhter Y, Bhattacharjee S. 2016. Attenuation of Pseudomonas aeruginosa biofilm formation by Vitexin: a combinatorial study with azithromycin and gentamicin. Sci Rep. 6:23367.
   PubMed Web of Science ®Google Scholar
• Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JT, Greenberg E. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science. 280:295–298. doi: 10.1126/science.280.5361.295
   PubMed Web of Science ®Google Scholar
• DeLano W. 2015. The PyMOL molecular graphics system, Version 1.7. 4. Portland, Oregon (USA): Schrödinger, LLC.
   Google Scholar
• Flemming H-C, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol. 8:623–633.
   PubMed Web of Science ®Google Scholar
• Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C. 2002. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol. 184:6472–6480. doi: 10.1128/JB.184.23.6472-6480.2002
   PubMed Web of Science ®Google Scholar
• Hodgkinson JT, Galloway WR, Wright M, Mati IK, Nicholson RL, Welch M, Spring DR. 2012. Design, synthesis and biological evaluation of non-natural modulators of quorum sensing in Pseudomonas aeruginosa. Org Biomol Chem. 10:6032–6044. doi: 10.1039/c2ob25198a
   PubMed Web of Science ®Google Scholar
• Huerta V, Mihalik K, Crixell S, Vattem D. 2008. Herbs, spices and medicinal plants used in Hispanic traditional medicine can decrease quorum sensing dependent virulence in Pseudomonas aeruginosa. Int J Appl Res Nat Prod. 1:9–15.
   Google Scholar
• Johnson JR, Kuskowski MA, Wilt TJ. 2006. Systematic review: antimicrobial urinary catheters to prevent catheter-associated urinary tract infection in hospitalized patients. Ann Intern Med. 144:116–126. doi: 10.7326/0003-4819-144-2-200601170-00009
   PubMed Web of Science ®Google Scholar
• Kim H-S, Lee S-H, Byun Y, Park H-D. 2015. 6-Gingerol reduces Pseudomonas aeruginosa biofilm formation and virulence via quorum sensing inhibition. Sci Rep. 5:551–561. doi: 10.1038/srep08656
   Web of Science ®Google Scholar
• Kong K-F, Jayawardena SR, Indulkar SD, del Puerto A, Koh C-L, Hoiby N, Mathee K. 2005. Pseudomonas aeruginosa AmpR is a global transcriptional factor that regulates expression of AmpC and PoxB β-lactamases, proteases, quorum sensing, and other virulence factors. Antimicrob Agents Chemother. 49:4567–4575. doi: 10.1128/AAC.49.11.4567-4575.2005
   PubMed Web of Science ®Google Scholar
• Kong X, Liu X, Li J, Yang Y. 2014. Advances in pharmacological research of eugenol. Curr Opin Complement Alternat Med. 1:8–11.
   Google Scholar
• Kumar R, Chhibber S, Harjai K. 2009. Quorum sensing is necessary for the virulence of Pseudomonas aeruginosa during urinary tract infection. Kidney Int. 76:286–292. doi: 10.1038/ki.2009.183
   PubMed Web of Science ®Google Scholar
• Kumar L, Chhibber S, Harjai K. 2013. Zingerone inhibit biofilm formation and improve antibiofilm efficacy of ciprofloxacin against Pseudomonas aeruginosa PAO1. Fitoterapia. 90:73–78. doi: 10.1016/j.fitote.2013.06.017
   PubMed Web of Science ®Google Scholar
• Kumar L, Chhibber S, Kumar R, Kumar M, Harjai K. 2015. Zingerone silences quorum sensing and attenuates virulence of Pseudomonas aeruginosa. Fitoterapia. 102:84–95. doi: 10.1016/j.fitote.2015.02.002
   PubMed Web of Science ®Google Scholar
• Lee J, Zhang L. 2015. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell.6:26–41. doi: 10.1007/s13238-014-0100-x
   PubMed Web of Science ®Google Scholar
• Lyczak JB, Cannon CL, Pier GB. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microb Infect. 2:1051–1060. doi: 10.1016/S1286-4579(00)01259-4
   PubMed Web of Science ®Google Scholar
• McInnis CE, Blackwell HE. 2011. Design, synthesis, and biological evaluation of abiotic, non-lactone modulators of LuxR-type quorum sensing. Bioorg Med Chem. 19:4812–4819. doi: 10.1016/j.bmc.2011.06.072
   PubMed Web of Science ®Google Scholar
• Meng X-Y, Zhang H-X, Mezei M, Cui M. 2011. Molecular docking: a powerful approach for structure-based drug discovery. Curr Comput Aided Drug Des. 7:146–157. doi: 10.2174/157340911795677602
   PubMed Web of Science ®Google Scholar
• Moore JD, Gerdt JP, Eibergen NR, Blackwell HE. 2014. Active efflux influences the potency of quorum sensing inhibitors in Pseudomonas aeruginosa. ChemBioChem. 15:435–442. doi: 10.1002/cbic.201300701
   PubMed Web of Science ®Google Scholar
• Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. 1998. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem. 19:1639–1662. doi: 10.1002/(ISSN)1096-987X
   Web of Science ®Google Scholar
• Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem. 30:2785–2791. doi: 10.1002/jcc.v30:16
   PubMed Web of Science ®Google Scholar
• Ni N, Li M, Wang J, Wang B. 2009. Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev. 29:65–124. doi: 10.1002/med.v29:1
   PubMed Web of Science ®Google Scholar
• Nielsen SS. 2003. Phenol–sulfuric acid method for total carbohydrates. In: Nelson SS, editor. Food analysis laboratory manual. Boston (MA): Springer; p. 39–44. doi: 10.1007/978-1-4757-5250-2
   Google Scholar
• Ohman D, Cryz S, Iglewski B. 1980. Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase. J Bacteriol. 142:836–842.
   PubMed Web of Science ®Google Scholar
• Pearson JP, Passador L, Iglewski BH, Greenberg EP. 1995. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 92:1490–1494. doi: 10.1073/pnas.92.5.1490
   PubMed Web of Science ®Google Scholar
• Pesci EC, Pearson JP, Seed PC, Iglewski BH. 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol. 179:3127–3132. doi: 10.1128/jb.179.10.3127-3132.1997
   PubMed Web of Science ®Google Scholar
• Raad I, Mohamed JA, Reitzel RA, Jiang Y, Raad S, Al Shuaibi M, Chaftari A-M, Hachem RY. 2012. Improved antibiotic-impregnated catheters with extended-spectrum activity against resistant bacteria and fungi. Antimicrob Agents Chemother. 56:935–941. doi: 10.1128/AAC.05836-11
   PubMed Web of Science ®Google Scholar
• Rathinam P, Viswanathan P. 2014. Effects of antibiotics upon quorum sensing regulated characters: a propitious scheme against device associated infections. Int J Pharm Pharm Sci. 6:85–90.
   Google Scholar
• Saini H, Chhibber S, Harjai K. 2016. Antimicrobial and antifouling efficacy of urinary catheters impregnated with a combination of macrolide and fluoroquinolone antibiotics against Pseudomonas aeruginosa. Biofouling. 32:511–522. doi: 10.1080/08927014.2016.1155564
   PubMed Web of Science ®Google Scholar
• Sarabhai S, Sharma P, Capalash N. 2013. Ellagic acid derivatives from Terminalia chebula retz. downregulate the expression of quorum sensing genes to attenuate Pseudomonas aeruginosa PAO1 virulence. PLoS ONE. 8:e53441. doi: 10.1371/journal.pone.0053441
   PubMed Web of Science ®Google Scholar
• Seghal Kiran GS, Priyadharshini S, Dobson AD, Gnanamani E, Selvin J. 2016. Degradation intermediates of polyhydroxy butyrate inhibits phenotypic expression of virulence factors and biofilm formation in luminescent Vibrio sp. PUGSK8. NPJ Biofilms Microbiomes. 2:13. doi: 10.1038/npjbiofilms.2016.2
   Web of Science ®Google Scholar
• Shi Y, van Steenbergen MJ, Teunissen EA, Novo LS, Gradmann S, Baldus M, van Nostrum CF, Hennink WE. 2013. Π–Π stacking increases the stability and loading capacity of thermosensitive polymeric micelles for chemotherapeutic drugs. Biomacromolecules. 14:1826–1837. doi: 10.1021/bm400234c
   PubMed Web of Science ®Google Scholar
• Soto SM. 2014. Importance of biofilms in urinary tract infections: new therapeutic approaches. Adv Biol. 2014:1–13.
   Google Scholar
• Venturi V. 2006. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev. 30:274–291. doi: 10.1111/j.1574-6976.2005.00012.x
   PubMed Web of Science ®Google Scholar
• Viswanathan P, Rathinam P, Suneeva S. 2015. Plant quorum sensing inhibitors: food, medicinal plants, and others. In: Kalia Vc, editor. Quorum sensing vs quorum quenching: a battle with no end in sight. New Delhi, India: Springer; p. 269–281.
   Google Scholar
• Winzer K, Falconer C, Garber NC, Diggle SP, Camara M, Williams P. 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J Bacteriol. 182:6401–6411. doi: 10.1128/JB.182.22.6401-6411.2000
   PubMed Web of Science ®Google Scholar
• Yang Y-H, Lee T-H, Kim JH, Kim EJ, Joo H-S, Lee C-S, Kim B-G. 2005. High throughput detection method of quorum sensing molecules by colorimetric assay and its applications. Anal Biochem. 356:297–299.
   Web of Science ®Google Scholar
• Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE, Goldner M, Dessaux Y, Camara M, Smith H. 2002. N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun.70:5635–5646. doi: 10.1128/IAI.70.10.5635-5646.2002
   PubMed Web of Science ®Google Scholar
• Zhou L, Zheng H, Tang Y, Yu W, Gong Q. 2013. Eugenol inhibits quorum sensing at sub-inhibitory concentrations. Biotechnol Lett.35:631–637. doi: 10.1007/s10529-012-1126-x
   PubMed Web of Science ®Google Scholar
• Zhu H, Thuruthyil SJ, Willcox MD. 2002. Determination of quorum-sensing signal molecules and virulence factors of Pseudomonas aeruginosa isolates from contact lens-induced microbial keratitis. J Med Microbiol. 51:1063–1070. doi: 10.1099/0022-1317-51-12-1063
   PubMed Web of Science ®Google Scholar