Document Type: Review Article

Author

Department of Pharmacy, GRD (PG) IMT, Dehradun, (Uttarakhand), 248009, India

10.33945/SAMI/JCR.2020.1.4

Abstract

Abuse of antibiotics in therapy has led to development of resistance in the target organisms. Failure of the current antibiotics to control infections makes it essential to discover alternative drugs. The pathogenicity in numerous bacteria is regulated by Quorum sensing (QS) signaling systems. The QS inhibition system may cause the reduction of virulence and defense against the bacterial infections. The QS is the main regulator of virulence and biofilm formation in Pseudomonas aeruginosa. A variety of plants showed their effects on P. aeruginosa virulence. Extract of various plants control the regulatory QS genes and factors with marginal effects on bacterial growth. The quorum-quenching (QQ) mechanisms are unrelated to static or cidal effects. In fact, anti-QS have already shown promise in the battle against P. aeruginosa infections.

Graphical Abstract

Keywords

[1] National Nosocomial Infections Surveillance System. (2004). National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control32, 470-485.

[2] Manefield, M., Rasmussen, T. B., Henzter, M., Andersen, J. B., Steinberg, P., Kjelleberg, S., & Givskov, M. (2002). Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology148(4), 1119-1127.

[3] Cumberbatch, A. (2002). Characterization of the Anti-Quorum Sensing Activity Exhibited by Marine Macro algae of South Florida.

[4] Bjarnsholt, T., Jensen, P. Ø., Rasmussen, T. B., Christophersen, L., Calum, H., Hentzer, M., ... & Høiby, N. (2005). Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections . Microbiology151(12), 3873-3880.

[5] Gao, M., Teplitski, M., Robinson, J. B., & Bauer, W. D. (2003). Production of substances by Medicago truncatula that affect bacterial quorum sensing. Molecular Plant-Microbe Interactions16(9), 827-834.

[6] Yoon, Y., & Sofos, J. N. (2010). Absence of association of autoinducer‐2‐based quorum sensing with heat and acid resistance of Salmonella. Journal of food science75(7), M444-M448.

[7] Adonizio, A. L., Downum, K., Bennett, B. C., & Mathee, K. (2006). Anti-quorum sensing activity of medicinal plants in southern Florida. Journal of ethnopharmacology105(3), 427-435.

[8] Bauer, W. D., & Mathesius, U. (2004). Plant responses to bacterial quorum sensing signals. Current opinion in plant biology7(4), 429-433.

[9] Carson, C. F., Riley, T. V., & Cookson, B. D. (1998). Efficacy and safety of tea tree oil as a topical antimicrobial agent. Journal of Hospital Infection40(3), 175-178.

[10] Carson, C. F., & Riley, T. V. (1995). Antimicrobial activity of the major components of the essential oil of Melaleuca alternifolia. Journal of applied bacteriology78(3), 264-269.

[11] Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995). Microbial biofilms. Annu Rev Microbiol49, 711-745.

[12] Bauer, W. D., & Teplitski, M. (2001). Can plants manipulate bacterial quorum sensing?. Functional Plant Biology28(9), 913-921.

[13] Nealson, K. H., Platt, T., & Hastings, J. W. (1970). Cellular control of the synthesis and activity of the bacterial luminescent system. Journal of bacteriology104(1), 313-322.

[14] Hastings, J. W., & Greenberg, E. P. (1999). Quorum sensing: the explanation of a curious phenomenon reveals a common characteristic of bacteria. Journal of Bacteriology181(9), 2667-2668.

[15] Schauder, S., & Bassler, B. L. (2001). The languages of bacteria. Genes & development15(12), 1468-1480.

[16] McLean, R. J., Pierson III, L. S., & Fuqua, C. (2004). A simple screening protocol for the identification of quorum signal antagonists. Journal of Microbiological Methods58(3), 351-360.

[17] Rasmussen, T. B., Manefield, M., Andersen, J. B., Eberl, L., Anthoni, U., Christophersen, C., ... & Givskov, M. (2000). How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology146(12), 3237-3244.

[18] Henke, J. M., & Bassler, B. L. (2004). Bacterial social engagements. Trends in cell biology14(11), 648-656.

[19] Bassler, B. L., Wright, M., Showalter, R. E., & Silverman, M. R. (1993). Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Molecular microbiology9(4), 773-786.

[20] Stevens, A. M., & Greenberg, E. P. (1997). Quorum sensing in Vibrio fischeri: essential elements for activation of the luminescence genes. Journal of Bacteriology179(2), 557-562..

[21] Fuqua, C., & Greenberg, E. P. (1998). Self perception in bacteria: quorum sensing with acylated homoserine lactones. Current opinion in microbiology1(2), 183-189.

[22] Whitehead, N. A., Barnard, A. M., Slater, H., Simpson, N. J., & Salmond, G. P. (2001). Quorum-sensing in Gram-negative bacteria. FEMS microbiology reviews25(4), 365-404.

[23] Cao, M., Feng, Y., Wang, C., Zheng, F., Li, M., Liao, H., ... & Hu, F. (2011). Functional definition of LuxS, an autoinducer-2 (AI-2) synthase and its role in full virulence of Streptococcus suis serotype 2. The Journal of Microbiology49(6), 1000-1011.

[24] Halliday, N. M., Hardie, K. R., Williams, P., Winzer, K., & Barrett, D. A. (2010). Quantitative liquid chromatography–tandem mass spectrometry profiling of activated methyl cycle metabolites involved in LuxS-dependent quorum sensing in Escherichia coli. Analytical biochemistry403(1-2), 20-29.

[25] Hagen, S. J., Son, M., Weiss, J. T., & Young, J. H. (2010). Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit. Journal of biological physics36(3), 317-327.

[26] Sperandio, V. (2010). SdiA sensing of acyl-homoserine lactones by enterohemorrhagic E. coli (EHEC) serotype O157: H7 in the bovine rumen. Gut microbes1(6), 432-435.

[27] Pesci, E. C., Pearson, J. P., Seed, P. C., & Iglewski, B. H. (1997). Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. Journal of bacteriology179(10), 3127-3132.

[28] Surette, M. G., & Bassler, B. L. (1998). Quorum sensing in Escherichia coli and Salmonella typhimurium. Proceedings of the National Academy of Sciences95(12), 7046-7050.

[29] Rodelas, B., Lithgow, J. K., Wisniewski-Dye, F., Hardman, A., Wilkinson, A., Economou, A., ... & Downie, J. A. (1999). Analysis of quorum-sensing-dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. viciae. Journal of Bacteriology181(12), 3816-3823.

[30] von Bodman, S. B., Bauer, W. D., & Coplin, D. L. (2003). Quorum sensing in plant-pathogenic bacteria. Annual review of phytopathology41(1), 455-482.

[31] Fuqua, C., & Greenberg, E. P. (2002). Signalling: listening in on bacteria: acyl-homoserine lactone signalling. Nature reviews Molecular cell biology3(9), 685.

[32] Fuqua, W. C., Winans, S. C., & Greenberg, E. P. (1994). Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. Journal of bacteriology176(2), 269.

[33] Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F., & Zhang, L. H. (2001). Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature411(6839), 813.

[34] Cha, C., Gao, P., Chen, Y. C., Shaw, P. D., & Farrand, S. K. (1998). Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria . Molecular Plant-Microbe Interactions11(11), 1119-1129.

[35] Smith, R. S., & Iglewski, B. H. (2003). Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. The Journal of clinical investigation112(10), 1460-1465.

[36] Smith, R. S., & Iglewski, B. H. (2003). P. aeruginosa quorum-sensing systems and virulence. Current opinion in microbiology6(1), 56-60.

[37] Debler, E. W., Kaufmann, G. F., Kirchdoerfer, R. N., Mee, J. M., Janda, K. D., & Wilson, I. A. (2007). Crystal structures of a quorum-quenching antibody. Journal of molecular biology368(5), 1392-1402.

[38] Hoang, T. T., Sullivan, S. A., Cusick, J. K., & Schweizer, H. P. (2002). β-Ketoacyl acyl carrier protein reductase (FabG) activity of the fatty acid biosynthetic pathway is a determining factor of 3-oxo-homoserine lactone acyl chain lengths. Microbiology148(12), 3849-3856.

[39] Albus, A. M., Pesci, E. C., Runyen-Janecky, L. J., West, S. E., & Iglewski, B. H. (1997). Vfr controls quorum sensing in Pseudomonas aeruginosa. Journal of Bacteriology179(12), 3928-3935.

[40] Dong, Y. H., & Zhang, L. H. (2005). Quorum sensing and quorum-quenching enzymes. The Journal of Microbiology43(1), 101-109..

[41] Schuster, M., & Greenberg, E. P. (2006). A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. International Journal of Medical Microbiology296(2-3), 73-81..

[42] Hentzer, M., & Givskov, M. (2003). Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. The Journal of clinical investigation112(9), 1300-1307..

[43] Whitehead, N.A., Welch, M., Salmond, G.P.C. (2001). Silencing the majority. Nature Biotechnol, 19, 735-736.

[44] Bodey, G. P., Bolivar, R., Fainstein, V., & Jadeja, L. (1983). Infections caused by Pseudomonas aeruginosa. Reviews of infectious diseases5(2), 279-313.

[45] Vasil, M. L. (1986). Pseudomonas aeruginosa: biology, mechanisms of virulence, epidemiology. The Journal of pediatrics108(5), 800-805..

[46] Meyer, J. M., Neely, A., Stintzi, A., Georges, C., & Holder, I. A. (1996). Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infection and immunity64(2), 518-523..

[47] Cox, C. D., & Adams, P. A. T. R. I. C. I. A. (1985). Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infection and immunity48(1), 130-138.

[48] Choi, Y., Park, H. Y., Park, S. J., Park, S. J., Kim, S. K., Ha, C., ... & Lee, J. H. (2011). Erratum to: Growth Phase-Differential Quorum Sensing Regulation of Anthranilate Metabolism in Pseudomonas aeruginosa. Molecules and cells32(6), 597. 

[49] Kessler, E., (1995). Beta-lytic endopeptidases. Methods in Enzymol, 2011, 248, 740-756.

[50] Krcmery, V., Koprnova, J., Gogova, M., Grey, E., & Korcova, J. (2006). Pseudomonas aeruginosa bacteraemia in cancer patients. Journal of infection52(6), 461-463.

[51] Meynard, J. L., Barbut, F., Guiguet, M., Batissel, D., Lalande, V., Lesage, D., ... & Meyohas, M. C. (1999). Pseudomonas aeruginosa infection in human immunodeficiency virus infected patients. Journal of Infection38(3), 176-181.

[52] Foca, M. D. (2002, October). Pseudomonas aeruginosa infections in the neonatal intensive care unit. In Seminars in perinatology (Vol. 26, No. 5, pp. 332-339). WB Saunders.

[53] Robertson, D. M., Petroll, W. M., Jester, J. V., & Cavanagh, H. D. (2007). Current concepts: contact lens related Pseudomonas keratitis. Contact Lens and Anterior Eye30(2), 94-107..

[54] Roland, P. S. (2002). Chronic suppurative otitis media: a clinical overview. Ear, Nose and Throat Journal81(8), S8-S8..

[55] Mowat, E., Paterson, S., Fothergill, J. L., Wright, E. A., Ledson, M. J., Walshaw, M. J., ... & Winstanley, C. (2011). Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. American journal of respiratory and critical care medicine183(12), 1674-1679.

[56] Shi, M., Li, Y., Wang, Y., Huang, J., Huang, X., & Xu, Y. (2009). Regulation of GacA on two phz gene clusters and quorum sensing in Pseudomonas sp. M18. Wei sheng wu xue bao= Acta microbiologica Sinica49(10), 1306-1316.

[57] Pustelny, C., Albers, A., Büldt-Karentzopoulos, K., Parschat, K., Chhabra, S. R., Cámara, M., ... & Fetzner, S. (2009). Dioxygenase-mediated quenching of quinolone-dependent quorum sensing in Pseudomonas aeruginosa. Chemistry & biology16(12), 1259-1267..

[58] Cotar, A. I., Chifiriuc, M. C., Dinu, S., Pelinescu, D., Banu, O., & Lazãr, V. (2010). Quantitative real-time PCR study of the influence of probiotic culture soluble fraction on the expression of Pseudomonas aeruginosa quorum sensing genes. Romanian archives of Microbiology and Immunology69(4), 213-223.

[59] Tsai, M. J., Teng, C. J., Teng, R. J., Lee, P. I., & Chang, M. H. (1996). Necrotizing bowel lesions complicated byPseudomonas septicaemia in previously healthy infants. European journal of pediatrics155(3), 216-218..

[60] Nicolle, L. E. (2002). Resistant pathogens in urinary tract infections. Journal of the American Geriatrics Society50, 230-235.

[61] Sapico, F. L., & Montgomerie, J. Z. (1990). Vertebral osteomyelitis. Infectious disease clinics of North America4(3), 539-550..

[62] Yu, Y., Cheng, A. S., Wang, L., Dunne, W. M., & Bayliss, S. J. (2007). Hot tub folliculitis or hot hand–foot syndrome caused by Pseudomonas aeruginosa. Journal of the American Academy of Dermatology57(4), 596-600..

[63] Adonizio, A., Kong, K. F., & Mathee, K. (2008). Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrobial agents and chemotherapy52(1), 198-203.

[64] Hooper, D. C. (1999). Mode of action of fluoroquinolones. Drugs58(2), 6-10..

[65] Flanders, S. A., Collard, H. R., & Saint, S. (2006). Nosocomial pneumonia: state of the science. American journal of infection control34(2), 84-93.

[66] Donlan, R. M., & Costerton, J. W. (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical microbiology reviews15(2), 167-193.

[67] Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., & Greenberg, E. P. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science280(5361), 295-298.

[68] Hoyle, B. D., & Costerton, J. W. (1991). Bacterial resistance to antibiotics: the role of biofilms. In Progress in Drug Research/Fortschritte der Arzneimittelforschung/Progrès des recherches pharmaceutiques (pp. 91-105). Birkhäuser Basel..

[69] Lyczak, J. B., Cannon, C. L., & Pier, G. B. (2002). Lung infections associated with cystic fibrosis. Clinical microbiology reviews15(2), 194-222.

[70] Lazãr, V., & Chifiriuc, M. C. (2010). Architecture and physiology of microbial biofilms. Roum Arch Microbiol Immunol69(2), 95-107..

[71] Martinez, L. R., & Fries, B. C. (2010). Fungal biofilms: relevance in the setting of human disease. Current fungal infection reports4(4), 266-275.

[72] Sintim, H. O., Smith, J. A., Wang, J., Nakayama, S., & Yan, L. (2010). Paradigm shift in discovering next-generation anti-infective agents: targeting quorum sensing, c-di-GMP signaling and biofilm formation in bacteria with small molecules. Future medicinal chemistry2(6), 1005-1035.

[73] Hentzer, M., & Givskov, M. (2003). Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. The Journal of clinical investigation112(9), 1300-1307..

[74] Smith, R. S., & Iglewski, B. H. (2003). Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. The Journal of clinical investigation112(10), 1460-1465.

[75] McKnight, S. L., Iglewski, B. H., & Pesci, E. C. (2000). The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. Journal of bacteriology182(10), 2702-2708.

[76] Espín, J. C., García-Conesa, M. T., & Tomás-Barberán, F. A. (2007). Nutraceuticals: facts and fiction. Phytochemistry68(22-24), 2986-3008.

[77] Pesci, E. C., Milbank, J. B., Pearson, J. P., McKnight, S., Kende, A. S., Greenberg, E. P., & Iglewski, B. H. (1999). Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences96(20), 11229-11234.

[78] Reimmann, C., Beyeler, M., Latifi, A., Winteler, H., Foglino, M., Lazdunski, A., & Haas, D. (1997). The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N‐butyryl‐homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Molecular microbiology24(2), 309-319..

[79] Throup, J., Winson, M. K., Bainton, N. J., Bycroft, B. W., Williams, P., & Stewart, G. S. A. B. (1995). Signalling in bacteria beyond bioluminescence. Bioluminescence and Chemiluminescence: Fundamentals and Applied Aspects, 89-92.

[80] Calfee, M. W., Coleman, J. P., & Pesci, E. C. (2001). Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences98(20), 11633-11637.

[81] Holden, M. T., Ram Chhabra, S., De Nys, R., Stead, P., Bainton, N. J., Hill, P. J., ... & Rice, S. (1999). Quorum‐sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram‐negative bacteria. Molecular microbiology33(6), 1254-1266.

[82] Li, Q. Q., Ni, H., Meng, S., He, Y., Yu, Z. N., & Li, L. (2011). Suppressing Erwinia carotovora pathogenicity by projecting N-acyl homoserine lactonase onto the surface of Pseudomonas putida cells. Journal of microbiology and biotechnology21(12), 1330-1335.

[83] Van Delden, C., & Iglewski, B. H. (1998). Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerging infectious diseases4(4), 551.

[84] Gambello, M. J., & Iglewski, B. H. (1991). Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. Journal of bacteriology173(9), 3000-3009.

[85] Mathee, K., McPherson, C. J., & Ohman, D. E. (1997). Posttranslational control of the algT (algU)-encoded sigma22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN). Journal of bacteriology179(11), 3711-3720.

[86] Hentzer, M., Riedel, K., Rasmussen, T. B., Heydorn, A., Andersen, J. B., Parsek, M. R., ... & Kjelleberg, S. (2002). Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology148(1), 87-102.

[87] Wu, H., Song, Z., Hentzer, M., Andersen, J. B., Molin, S., Givskov, M., & Høiby, N. (2004). Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. Journal of Antimicrobial Chemotherapy53(6), 1054-1061.

[88] Manefield, M., de Nys, R., Naresh, K., Roger, R., Givskov, M., Peter, S., & Kjelleberg, S. (1999). Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology145(2), 283-291.

[89] Manefield, M., Rasmussen, T. B., Henzter, M., Andersen, J. B., Steinberg, P., Kjelleberg, S., & Givskov, M. (2002). Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology148(4), 1119-1127.

[90] Ren, D., Zuo, R., & Wood, T. K. (2005). Quorum-sensing antagonist (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2 (5H)-furanone influences siderophore biosynthesis in Pseudomonas putida and Pseudomonas aeruginosa. Applied microbiology and biotechnology66(6), 689-695.

[91] Zahin, M., Hasan, S., Aqil, F., Khan, M.S., Husain, F.M., Ahmad, I. (2010). Screening of certain medicinal plants from India for their anti-quorum sensing activity. Indian J Exp Biol. 48, 1219-1224.

[92] Zhu, H., Liu, W., Tian, B., Liu, H., & Ning, S. (2011). Inhibition of quorum sensing in the opportunistic pathogenic bacterium Chromobacterium violaceum by an extract from fruiting bodies of lingzhi or reishi medicinal mushroom, Ganoderma lucidum (w. Curt.: Fr.) p. Karst.(higher basidiomycetes). International journal of medicinal mushrooms13(6), 559-564.

[93] Schulz, S., Dickschat, J. S., Kunze, B., Wagner-Dobler, I., Diestel, R., & Sasse, F. (2010). Biological activity of volatiles from marine and terrestrial bacteria. Marine drugs8(12), 2976-2987.

[94] Balick, M.J., Cox, P.A. (1996). Plants, People, and Culture: The Science of Ethnobotany. New York: Scientific American Library.

[95] Lacassie, E., Marquet, P., Martin-Dupont, S., Gaulier, J. M., & Lachâtre, G. (2000). A non-fatal case of intoxication with foxglove, documented by means of liquid chromatography-electrospray-mass spectrometry. Journal of Forensic Science45(5), 1154-1158.

[96] Bussey, H. I., Hawkins, D. W., Gaspard, J. J., & Walsh, R. A. (1988). A comparative trial of digoxin and digitoxin in the treatment of congestive heart failure. Pharmacotherapy: The Journal of Human Pharmacology and Drug Therapy8(4), 235-240.

[97] Downie, J. A. (2010). The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS microbiology reviews34(2), 150-170.

[98] Khafagi, I. K., & Dewedar, A. (2000). The efficiency of random versus ethno-directed research in the evaluation of Sinai medicinal plants for bioactive compounds. Journal of Ethnopharmacology71(3), 365-376.

[99] Dewick, P. M. (2002). Medicinal natural products: a biosynthetic approach. John Wiley & Sons.

[100] Cowan, M. M. (1999). Plant products as antimicrobial agents. Clinical microbiology reviews12(4), 564-582.

[101] Tsao, C. Y., Wang, L., Hashimoto, Y., Yi, H., March, J. C., DeLisa, M. P., ... & Bentley, W. E. (2011). LuxS coexpression enhances yields of recombinant proteins in Escherichia coli in part through posttranscriptional control of GroEL. Appl. Environ. Microbiol.77(6), 2141-2152.

[102] Kim, K., Kim, Y. U., Koh, B. H., Hwang, S. S., Kim, S. H., Lépine, F., ... & Lee, G. R. (2010). HHQ and PQS, two Pseudomonas aeruginosa quorum‐sensing molecules, down‐regulate the innate immune responses through the nuclear factor‐κB pathway. Immunology129(4), 578-588.

[103] Wang, Y., Deng, C., Peng, Q., Chen, Z., Huang, D., Zhang, J., & Song, F. (2010). Effect of quorum sensing response regulator nprR deletion on expression of cry protein in Bacillus thuringiensis. Wei sheng wu xue bao= Acta microbiologica Sinica50(11), 1550-1555..

[104] Diţu, L. M., Chifiriuc, C., Lazăr, V., & Mihăescu, G. (2009). Implication of quorum sensing phenomenon in the expression of genes that code for bacteriocines in lactic bacteria. Bacteriologia, virusologia, parazitologia, epidemiologia (Bucharest, Romania: 1990)54(4), 147-166. 

[105] Lazar, V., Miyazaki, Y., Hanawa, T., Chifiriuc, M. C., Ditu, L. M., Marutescu, L., ... & Kamiya, S. (2009). The influence of some probiotic supernatants on the growth and virulence features expression of several selected enteroaggregative E. coli clinical strains. Roum Arch Microbiol Immunol68(4), 207-214.

[106] Blumenthal, M., Goldberg, A., & Brinckmann, J. (2000). Herbal Medicine. Expanded Commission E monographs. Integrative Medicine Communications, pp. 519.

[107] Chun, S.S., Vattem, D.A., Lin, Y.T., Shetty, K. (2005). Phenolic antioxidants from clonal oregano (Origanum vulgare) with antimicrobial activity against Helicobacter pylori. Process Biochem, 40, 809-816.

[108] Rodrigues, M.R., Krause, L.C., Caramo, E.B., dos Santos, J.G., Dariva, C., Vladimir de Oliveira, J. (2004). Chemical composition and extraction yield of the extract of Origanum vulgare obtained from sub- and supercritical CO2. J Agricultural & Food Chem, 52, 3042-3047.

[109] Chami, F., Chami, N., Bennis, S., Trouillas, J., & Remmal, A. (2004). Evaluation of carvacrol and eugenol as prophylaxis and treatment of vaginal candidiasis in an immunosuppressed rat model. Journal of antimicrobial chemotherapy54(5), 909-914.

[110] Hersch-Martinez, P., Leanos-Miranda, B. E., & Solorzano-Santos, F. (2005). Antibacterial effects of commercial essential oils over locally prevalent pathogenic strains in Mexico. Fitoterapia76(5), 453-457.

[111] Saeed, M. A., & Sabir, A. W. (2004). Antibacterial activities of some constituents from oleo-gum-resin of Commiphora mukul. Fitoterapia75(2), 204-208.

[112] Méndez, C., & Salas, J. A. (2001). The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms. Research in microbiology152(3-4), 341-350.

[113] Hogan, D. A., Vik, Å., & Kolter, R. (2004). A Pseudomonas aeruginosa quorum‐sensing molecule influences Candida albicans morphology. Molecular microbiology54(5), 1212-1223.

[114] Persson, T., Hansen, T. H., Rasmussen, T. B., Skindersø, M. E., Givskov, M., & Nielsen, J. (2005). Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Organic & biomolecular chemistry3(2), 253-262.

[115] Rasmussen, T. B., Bjarnsholt, T., Skindersoe, M. E., Hentzer, M., Kristoffersen, P., Köte, M., ... & Givskov, M. (2005). Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. Journal of bacteriology187(5), 1799-1814.

[116] Teplitski, M., Robinson, J. B., & Bauer, W. D. (2000). Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Molecular Plant-Microbe Interactions13(6), 637-648..

[117] Vattem, D. A., Mihalik, K., Crixell, S. H., & McLean, R. J. C. (2007). Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia78(4), 302-310..

[118] Nascimento, G. G., Locatelli, J., Freitas, P. C., & Silva, G. L. (2000). Antibacterial activity of plant extracts and phytochemicals on antibiotic-resistant bacteria. Brazilian journal of microbiology31(4), 247-256..

[119] Walker, T. S., Bais, H. P., Déziel, E., Schweizer, H. P., Rahme, L. G., Fall, R., & Vivanco, J. M. (2004). Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant physiology134(1), 320-331.

[120] Huber, B., Eberl, L., Feucht, W., & Polster, J. (2003). Influence of polyphenols on bacterial biofilm formation and quorum-sensing. Zeitschrift für Naturforschung C58(11-12), 879-884.

[121] Al-Hussaini, R., & Mahasneh, A. (2009). Microbial growth and quorum sensing antagonist activities of herbal plants extracts. Molecules14(9), 3425-3435.

[122] Krishnan, T., Yin, W. F., & Chan, K. G. (2012). Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa PAO1 by Ayurveda spice clove (Syzygium aromaticum) bud extract. Sensors12(4), 4016-4030.

[123] Boga, C., Forlani, L., Calienni, R., Hindley, T., Hochkoeppler, A., Tozzi, S., & Zanna, N. (2011). On the antibacterial activity of roots of Capparis spinosa L. Natural product research25(4), 417-421.

[124] Abraham, S. V. P. I., Palani, A., Ramaswamy, B. R., Shunmugiah, K. P., & Arumugam, V. R. (2011). Antiquorum sensing and antibiofilm potential of Capparis spinosa. Archives of Medical Research42(8), 658-668.

[125] Chong, Y. M., Yin, W. F., Ho, C. Y., Mustafa, M. R., Hadi, A. H. A., Awang, K., ... & Chan, K. G. (2011). Malabaricone C from Myristica cinnamomea exhibits anti-quorum sensing activity. Journal of natural products74(10), 2261-2264.

[126] Singh, B. N., Singh, H. B., Singh, A., Singh, B. R., Mishra, A., & Nautiyal, C. S. (2012). Lagerstroemia speciosa fruit extract modulates quorum sensing-controlled virulence factor production and biofilm formation in Pseudomonas aeruginosa. Microbiology158(2), 529-538.

[127] Tan, L. Y., Yin, W. F., & Chan, K. G. (2012). Silencing quorum sensing through extracts of Melicope lunu-ankenda. Sensors12(4), 4339-4351.

[128] Yeo, S. S. M., & Tham, F. Y. (2012). Anti-quorum sensing and antimicrobial activities of some traditional Chinese medicinal plants commonly used in South-East Asia. Malaysian Journal of Microbiology8(1), 11-20.

[129] Ronald, P. C. (2011). Small protein-mediated quorum sensing in a Gram-negative bacterium: novel targets for control of infectious disease. Discov Med., 12, 461-470.

[130] Prunuske, A. J., Waltner, J. K., Kuhn, P., Gu, B., & Craig, E. A. (2012). Role for the molecular chaperones Zuo1 and Ssz1 in quorum sensing via activation of the transcription factor Pdr1. Proceedings of the National Academy of Sciences109(2), 472-477.