Document Type: Review Article

Author

aDepartment of Pharmaceutical chemistry, Himalayan Institute of Pharmacy Research, Dehradun, (Uttarakhand), 248001, India

Abstract

The misuses of antimicrobials in infectious diseases have led to the progress of extensive resistance in the infectious organisms. The unsuccessful of accessible antimicrobials to control infections makes it essential to discover alternatives to currently existing drugs. Their connection to infectious diseases and their natural ability increase antimicrobial resistance in microbes, has led to a platforms for research focused on new techniques to control them. In this affords we study, the pathogenicity in many bacteria is regulated by Quorum sensing (QS). The inhibition of QS system may causes the reduction of virulence and protect against bacterial infections. These bacteria rely on chemical communication (or QS) to coordinate activities necessary for their survival in groups by some course of action. Their dependence on QS has made those signaling systems within bacteria an attractive target for the design of new anti-infective agents. Compounds that can interrupt these processes are known as QS inhibitors. The QS is the key regulator of virulence in various bacteria. Various plants extracts and their chemical constituents were showed their effects on bacterial virulence factors by inhibiting of QS genes and QS-controlled factors and effects on bacterial growth. The anti-QS approach has promise in the fight against infections pathogens, thereby making the bacteria more susceptible to traditional antimicrobials. The QSIs may provide the newest weapon against infections involving drug-resistant bacterial strains. These QSIs come from a variety of sources and have a wide array of structures.

Graphical Abstract

Keywords

[1]     J.T. Hodgkinson, M. Welch, D.R. Spring, Learning the Language of Bacteria. ACS Chem. Biol, 2(11) 2007, 715-17.

[2]     A. Jayaraman, T.K. Wood, Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu. Rev. Biomed. Eng, 10 2008, 145-67.

[3]     M. Manefield, T.B. Rasmussen, M. Henzter, J.B. Andersen, P. Steinberg, S. Kjelleberg, M. Givskov, Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology, 148(4) 2002, 1119-27.

[4]     R.P. Ryan, J.M. Dow, Diffusible signals and interspecies communication in bacteria. Microbiology, 154(7) 2008, 1845-58.

[5]     C.D. Sifri, Quorum sensing: bacteria talk sense. Clin. Infect. Dis, 47(8) 2008, 1070-76.

[6]     P. Williams, K. Winzer, W.C. Chan, M. Camara, Look who’s talking: communication and quorum sensing in the bacterial world. Phil. Trans. R. Soc. Lond. B, 362 2007, 1119–1134.

[7]     T. Bjarnsholt, M. Givskov, Quorum sensing inhibitory drugs as next generation antimicrobials: worth the effort? Curr. Infect. Dis. Rep, 10(1) 2008, 22-8.

[8]     B. Raffa Robert, R. Iannuzzo Joseph, R. Levine Diana, K. Saeid Kamal, C. Schwartz Rachel, T. Sucic Nicholas, D. Terleckyj Oksana, M. Young Jeffrey, Bacterial communication ("quorum sensing") via ligands and receptors: a novel pharmacologic target for the design of antibiotic drugs. J. Pharmacol. Exp. Ther, 312(2) 2005, 417-23.

[9]     T.B. Rasmussen, M. Givskov, Quorum-sensing inhibitors as antipathogenic drugs. Int. J. Med. Microbiol, 296 (2-3) 2006, 149-61.

[10] B. Rasmussen Thomas, M. Givskov, Quorum sensing inhibitors: a bargain of effects. Microbiology, 152 (Pt 4) 2006, 895-904.

[11] N. Balaban, M. Givskov, T.B. Rasmussen, In Vivo Studies: Inhibiting Biofilm-Associated Bacterial Infections using QSIs. In Control of Biofilm Infections by Signal Manipulation, Balaban, N. Ed. Springer: Berlin, 2 2008, 119-29.

[12] D. Ren, M. Givskov, T. Ramussen, Quorum-Sensing Inhibitory Compounds. In Control of Biofilm Infections by Signal Manipulation, Balaban, N. Ed. Springer: Berlin, 2 2008, 51-77.

[13] M. Hentzer, M. Givskov, L. Eberl, Quorum sensing in biofilms: Gossip in slime city. Microb. Biofilms, 1 2004, 118-40.

[14] C.D. Nadell, J.B. Xavier, S.A. Levin, K.R. Foster, The evolution of quorum sensing in bacterial biofilms. PLoS Biol, 6 (1) 2008, 171-9.

[15] M.R. Parsek, E.P. Greenberg, Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol, 13 (1) 2005, 27-33.

[16] A.R. Horswill, P. Stoodley, P.S. Stewart, M.R. Parsek, The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal. Bioanal. Chem, 387 (2) 2007, 371-80.

[17] M. Li, N. Ni, H.T. Chou, C.D. Lu, P.C. Tai, B. Wang, Structure-based discovery and experimental verification of novel Al-2 quorum sensing inhibitors against Vibrio harveyi. Chem Med Chem, 3 (8) 2008, 1242-49.

[18] J.B. Andersen, A. Heydorn, M. Hentzer, L. Eberl, O. Geisenberger, B.B. Christensen, S. Molin, M. Givskov, gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Appl Environ Microbiol 67 2001, 575-585.

[19] W. Galloway, J. Hodgkinson, S. Bowden, M. Welch, D. Spring, Quorum Sensing in Gram-Negative Bacteria: Small-Molecule Modulation of AHL and AI-2 Quorum Sensing Pathways. Chem. Rev. 111 2011, 28–67.

[20] K.M. Gray, J. Garey, The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology, 147 2001, 2379–2387.

[21] S. Jafra, J.M. van der Wolf, Fast screening method for detection of acyl-HSL-degrading soil isolates. J Microbiol Methods, 57 2004, 415-420.

[22] R. McLean, L. Pierson, C.A. Fuqua, simple screening protocol for the identification of quorum signal antagonists. J. Microbiol. Methods, 58 2004, 351-60.

[23] T. Rasmussen, T. Bjarnsholt, M. Skindersoe, M. Hentzer, P. Kristoffersen, M. Koete, J. Nielsen, L. Eberl, M. Givskov, Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J. Bacteriol, 187(5) 2005, 1799-1814.

[24] M.G. Kociolek, Quorum-Sensing Inhibitors and Biofilms. Anti-Infective Agents in Medicinal Chemistry, 8 2009, 315-326 315.

[25] L. Steindler, V. Venturi, Detection of quorum-sensing N-acyl homo serine lactone signal molecules by bacterial biosensors. FEMS Microbiol. Lett, 266 2007, 1-9.

[26] C. Mendez, J. Salas, The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms. Research in Microbiology, 152 2001, 341-350.

[27] W. Bauer, M. Tepletski, Can plants manipulate bacterial quorum sensing? Australian Journal of Plant Physiology, 28 2001, 913-921.

[28] S. Schauder, B. Bassler, The languages of bacteria. Genes and Development, 15 2001, 1468-1480.

[29] R. Smith, B. Iglewski, Pseudomonas aeruginosa quorum-sensing systems and virulence. Current Opinion in Microbiology, 6 2003, 56-60.

[30] H. Wu, Z. Song, M. Hentzer, J. Andersen, S. Molin, M. Givskov, N. Hoiby, Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. Journal of Antimicrobial Chemotherapy, 53 2004, 1054-1061.

[31] D. Cvitkovitch, Y. Liu, R. Ellen, Quorum sensing and biofilm formation in Streptococcal infections. J Clin Invest, 12 2003, 1626-1632.

[32] E.P. Greenberg, Bacterial communication and group behavior. J Clin Invest, 112 2003, 1288-1290.

[33] J.M. Yarwood, P.M. Schlievert, Quorum sensing in Staphylococcus infections. J Clin Invest, 112 2003, 1620-1625.

[34] C. Arevalo-Ferro, J. Buschmann, G. Reil, A. Gorg, L. Wiehlmann, B. Tummler, L. Eberl, K. Riedel, Proteome analysis of intraclonal diversity of two Pseudomonas aeruginosa TB clone isolates. Proteomics 4 2004, 1241-1246.

[35] J.S Webb, M. Givskov, S. Kjelleberg, Bacterial biofilms: prokaryotic adventures in multicellularity. Curr Opin Microbiol, 6 2003, 578-585.

[36] J. Zhu, J. Mekalanos, Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5 2003, 647-656.

[37] J.M. Dow, L. Crossman, K. Findlay, Y. He, J. Feng, J. Tang, Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci USA, 100 2003, 10995-11000.

[38] K.B. Xavier, B. Bassler, LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol, 6 2003, 191-197.

[39] V. Sperandio, A. Torres, B. Jarvis, J. Nataro, J. Kaper, Bacteria-host communication: The language of hormones. Proc Natl Acad Sci USA, 100 2003, 8951-8956.

[40] S.C. Williams, E. Patterson, N. Carty, J. Griswold, A. Hamood, K. Rumbaugh, Pseudomonas aeruginosa autoinducer enters and functions in mammalian cells. J Bacteriol, 186 2004, 2281-2287.

[41] B. Stevenson, K. von Lackum, R. Wattier, J. McAlister, J. Miller, K. Babb, Quorum sensing by the Lyme disease spirochete. Microbes Infect, 5 2003, 991-997.

[42] D. Ren, T.K. Wood, (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone reduces corrosion from Desulfotomaculum orientis. Environ. Microbiol, 6(5) 2004, 535-40.

[43] T. Rasmussen, M. Manefield, J. Andersen, L. Eberl, U. Anthoni, C. Christophersen, P. Steinberg, S. Kjelleberg, M. Givskov, How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology, 146(12) 2000, 146, 3237-44.

[44] J.M. Henke, B. Bassler, Bacterial social engagements. Trends in Cell Biology, 14 2004, 648-656.

[45] N.A. Whitehead, A. Barnard, H. Slater, Simpson, N.J, Salmond, G.P. Quorum-sensing in Gram-negative bacteria. FEMS Microbiology Reviews, 25 2001, 365-404.

[46] N. Halliday, K. Hardie, P. Williams, K. Winzer, D. Barrett, Quantitative liquid chromatography-tandem mass spectrometry profiling of activated methyl cycle metabolites involved in LuxS-dependent quorum sensing in Escherichia coli. Anal Biochem, 403 2010, 1-2.

[47] S. Hagen, M. Son, J. Weiss, J. Young, Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit. J Biol Phys, 36 2010, 317-27.

[48] V Sperandio, A. Sdi, Sensing of acyl-homoserine lactones by enterohemorrhagic E. coli (EHEC) serotype O157:H7 in the bovine rumen. Gut Microbes, 1 2010, 432-5.

[49] M. Cao, Y. Feng, C. Wang, F. Zheng, M. Li, H. Liao, Y. Mao, X. Pan, J. Wang, D. Hu, F. Hu, J. Tang, Functional definition of LuxS, an autoinducer-2 (AI-2) synthase and its role in full virulence of Streptococcus suis serotype 2. J Microbiol, 49 2011, 1000-11.

[50] S. Von Bodman, W. Bauer, D. Coplin, Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol, 41 2003, 455-482.

[51] Y. Dong, L. Wang, L. Xu, H. Zhang, X. Zhang, L. Zhang, Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature, 411 2001, 813-817.

[52] C. Fuqua, E. Greenberg, Listening in on bacteria: acyl-homoserine lactone signalling. Nature Reviews Molecular and Cellular Biology, 3 2002, 685-695.

[53] C. Fuqua, M. Parsek, E. Greenberg, Regulation of gene expression by cell-to-cell communication: Acyl-homoserine lactone quorum sensing. Annu Rev Genet, 35 2001, 439-468.

[54] N. Decanis, N. Tazi, A. Correia, M. Vilanova, M. Rouabhia, A. Farnesol, a fungal quorum-sensing molecule triggers Candida albicans morphological changes by down regulating the expression of different secreted aspartyl proteinase genes. Open Microbiol J, 5 2011, 119-26.

[55] K. Ohtani, H. Hayashi, T. Shimizu, The LuxS gene is involved in cell-cell signaling for toxin production in Clostridium perfringens. Mol. Microbiol, 44 2000, 171–179.

[56] J. Smith, B. Ahmer, Detection of other microbial species by Salmonella: expression of the SdiA regulon. J. Bacteriol, 185 2003, 1357–1366.

[57] E.W. Debler, G. Kaufmann, R. Kirchdoerfer, J. Mee, K. Janda, I. Wilson, Crystal structures of a quorum-quenching antibody. Journal of Molecular Biology, 368 2007, 1392-1402.

[58] R. Smith, B. Iglewski, Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. Journal of Clinical Investigation, 112 2003, 1460-1465.

[59] T. Hoang, S. Sullivan, J. Cusick, H. Schweizer, {beta}-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. Microbiology, 148 2002, 3849-3856.

[60] Y. Dong, L. Zhang, Quorum sensing and quorum-quenching enzymes. Journal of Microbiology, 43 2005, 101-109.

[61] M. Schuster, E. Greenberg, A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Inter J Med Microbiol, 296 2006, 73-81.

[62] M. Hentzer, L. Eberl, J. Nielsen, M. Givskov, Quorum sensing-A novel target for the treatment of biofilm infections. Bio Drugs, 17 2003, 241-250.

[63] J. Downie, The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev, 34 2010, 150-70.

[64] I. Khafagi, A. Dewedar, The efficiency of random versus ethno-directed research in the evaluation of Sinai medicinal plants for bioactive compounds. Journal of Ethnopharmacology 71 2000, 365-376.

[65] N. Ni, H. Chou, J. Wang, M. Li, C. Lu, P. Tai, B. Wang, Identification of boronic acids as antagonists of bacterial quorum sensing in Vibrio harveyi. Biochem. Biophys. Res. Commun, 369(2) 2008, 590-94.

[66] P. Williams, Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology, 153(12) 2007, 3923-38.

[67] M. Zahin, S. Hasan, F. Aqil, M. Khan, F. Husain, I. Ahmad, Screening of certain medicinal plants from India for their anti-quorum sensing activity. Indian J Exp Biol. 48 2010, 1219-24.

[68] S. Schulz, J. Dickschat, B. Kunze, I. Wagner-Dobler, R. Diestel, F. Sasse, Biological activity of volatiles from marine and terrestrial bacteria. Mar Drugs, 8 2010, 2976-87.

[69] H. Zhu, W. Liu, B. Tian, H. Liu, S. Ning, 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). Int J Med Mushrooms. 13 2011, 559-64.

[70] J.C. Espin, M. Garcia-Conesa, F. Tomas-Barberan, Nutraceuticals: facts and fiction. Phytochemistry, 68 2007, 2986-3008.

[71] D. Vattem, K. Mihalik, S. Crixell, R. McLean, Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia, 78 2007, 302-310.

[72] B. Huber, L. Eberl, W. Feucht, J. Polster, Influence of polyphenols on bacterial biofilm formation and quorum-sensing. Zeitschrift fur Naturforschung Section C, Biosciences. 58 2004, 879-884.

[73] G. Hernandez, J. Olmos, Molecular identification of pathogenic and nonpathogenic strains of Vibrio harveyi using PCR and RAPD. Appl Microbiol Biotechnol, 63 2004, 722-727.

[74] K. Kim, Y. Kim, B. Koh, S. Hwang, S. Kim, F. Lepine, Y. Cho, G. Lee, HHQ and PQS, two Pseudomonas aeruginosa quorum-sensing molecules, down-regulate the innate immune responses through the nuclear factor-kappaB pathway. Immunology, 129 2010, 578-88.

[75] Y. Wang C. Deng, Q. Peng, Z. Chen, D. Huang, J. Zhang, F. Song, Effect of quorum sensing response regulator nprR deletion on expression of cry protein in Bacillus thuringiensis. Wei Sheng Wu Xue Bao, 50 2010, 1550-1555.

[76] L. Diţu, C. Chifiriuc, V. Lazar, G. Mihaescu, Implication of quorum sensing phenomenon in the expression of genes that code for bacteriocines in lactic bacteria. Bacteriol Virusol Parazitol Epidemiol, 54 2009, 147-66. 

[77] V. Lazar, Y. Miyazaki, T. Hanawa, M. Chifiriuc, M. Diţu, L. Maruţescu, C. Bleotu, S. Kamiya, The influence of some probiotic supernatants on the growth and virulence features expression of several selected enteroaggregative E. coli clinical strains. Roum Arch Microbiol Immunol, 68 2009 207-14.

[78] C. Tsao, L. Wang, Y. Hashimoto, H. Yi, J. March, M. DeLisa, T. Wood, J. Valdes, W. Bentley, LuxS coexpression enhances yields of recombinant proteins in Escherichia coli in part through posttranscriptional control of GroEL. Appl Environ Microbiol, 77 2011, 2141-52.

[79] M. Hentzer, M. Givskov, Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest, 112 2003, 1300-1307.

[80] M. Manefield, L. Harris, S. Rice, R. De Nys, S. Kjelleberg, Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl. Environ. Microbiol, 66(5) 2000, 2079-84.

[81] S. West, A. Griffin, A. Gardner, S. Diggle, Social evolution theory for microorganisms. Nat Rev Microbiol, 4 2006, 597–607.

[82] K. Mok, N. Wingreen, B. Bassler, Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J. 22 2003, 870–881.

[83] M. Teplitski, J. Robinson, W. Bauer, Plants secrete substances that mimic bacterial N-acyl homo serine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Molecular Plant-Microbe Interactions. 13 2000, 637-648.

[84] M. Gao, M. Teplitski, J. Robinson, W. Bauer, Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol. Plant Microbe Interact, 16 2003, 827–834.

[85] A. Adonizio, K. Kong, K. Mathee, Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by south Florida plant extracts. Antimicrob. Agents Chemother, 52(1) 2008, 198-203.

[86] D. Hogan, A. Vik, R. Kolter. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol, 54 2004, 1212-1223.

[87] T. Persson, H. Hansen Thomas, B. Rasmussen Thomas, E. Skinderso Mette, M. Givskov, J. Nielsen, J. Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org. Biomol. Chem, 3(2) 2005, 253-62.

[88] T. Rasmussen, M. Skindersoe, T. Bjarnsholt, R. Phipps, K. Christensen, P. Jensen, J. Andersen, J. B. Koch, T. Larsen, M. Hentzer, L. Eberl, N. Hoiby, M. Givskov, Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology, 151(5) 2005, 1325-40.

[89] G. Nascimento, P. Locatelli, P. Freitas, G. Silva, Antimicrobial activity of plant extracts and phyto-chemicals on antibiotic resistant bacteria. Braz. J. Microbiol, 31 2000, 247-256

[90] R. Al-Hussaini, A. Mahasneh, Microbial Growth and Quorum Sensing Antagonist Activities of Herbal Plants Extracts. Molecules. 14 2009, 3425-3435.

[91] C. Boga, L. Forlani, R. Calienni, T. Hindley, A. Hochkoeppler, S. Tozzi, N.  Zanna, on the antibacterial activity of roots of Capparis spinosa L. Nat Prod Res, 25 2011, 417-421.

[92] T. Krishnan, W. Wai-Fong, Yin, K. Chan, Inhibition of Quorum Sensing Controlled Virulence Factor Production in Pseudomonas aeruginosa PAO1 by Ayurveda Spice Clove (Syzygium Aromaticum) Bud Extract. Sensors, 12 2012, 4016-4030.

[93] S. Issac Abraham, A. Palani, B. Ramaswamy, K. Shunmugiah, V. Arumugam, Antiquorum sensing and antibiofilm potential of Capparis spinosa. Arch Med Res, 42 2011, 658-668.

[94] Y. Chong, W. Yin, C. Ho, M. Mustafa, A. Hadi, K. Awang, P. Narrima, C.  Koh,  Malabaricone C from Myristica Cinnamomea exhibits Anti-Quorum sensing activity. Journal of Natural Products, 74 2011, 2261-2264.

[95] B.N. Singh, H. Singh, A. Singh, B. Singh, A. Mishra, C. Nautiyal, Lagerstroemia speciosa fruit extract modulates quorum sensing-controlled virulence factor production and biofilm formation in Pseudomonas. Aeruginosa. Microbiology, 158 2012, 529-538.

[96] L. Tan, W. Yin, K. Chan, Silencing Quorum Sensing through Extracts of Melicope lunu-ankenda. Sensors. 12 2012, 4339-4351.

[97] S. Yeo, F. Tham, Anti-quorum sensing and antimicrobial activities of some traditional Chinese medicinal plants commonly used in South-East Asia. Malaysian Journal of Microbiol, 8 2012, 11-20.

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

[99] M. Rodrigues, L. Krause, E. Caramo, J. Dos Santos, C. Dariva, Vladimir de Oliveira, J. Chemical composition and extraction yield of the extract of Origanum vulgare obtained from sub- and supercritical CO2. Journal of Agricultural and Food Chemistry, 52 2004, 3042-3047.

[100]       F. Chami, N. Chami, S. Bennis, J. Trouillas, A. Remmal, Evaluation of carvacrol and eugenol as prophylaxis and treatment of vaginal candidiasis in an immunosuppressed rat model. Journal of Antimicrobial Chemotherapy.54 2004, 909-914.

[101]       P. Hersch-Martinez, B. Leanos-Miranda, F. Solórzano-Santos, Antibacterial effects of commercial essential oils over locally prevalent pathogenic strains in Mexico. Fitoterapia, 76 2005, 453-457.

[102]       M. Asif Saeed, A. Sabir, Antibacterial activities of some constituents from oleo-gum-resin of Commiphora mukul. Fitoterapia. 75 2004, 204-208.

[103]       B. Girennavar, M. Cepeda, K. Soni, A. Vikram, P. Jesudhasan, G. Jayaprakasha, S. Pillai, B. Patil, Grapefruit juice and its furocoumarins inhibits autoinducer signaling and biofilm formation in bacteria. Int. J. Food Microbiol, 125(2) 2008, 204-8.

[104]       B. Girennavar, G. Jayaprakasha, B. Patil, Potent inhibition of human cytochrome P450 3A4, 2D6, and 2C9 isoenzymes by grapefruit juice and its furocoumarins. J. Food Sci, 72(8) 2007, C417-21.

[105]       K. Lemar, M. Turner, D. Lloyd, Garlic (allium sativum) as an anti-Candida agent: a comparison of the eficacy of fresh garlic and freeze-dried extracts. J. Appl. Microbiol, 93 2002, 398.

[106]       J. Shuford, J. Steckelberg, R. Patel, Effects of fresh garlic extract on candida albicans biofilms. Antimicrob. Agents Chemother, 49(1) 2005, 473.

[107]       T. Bjarnsholt, P. Jensen, T. Rasmussen, L. Christophersen, H. Calum, M. Hentzer, Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology, 151 2005, 3873–3880.

[108]       J. Park, G. Kaufmann, J. Bowen, J. Arbiser, J. Janda, A. Solenopsin, a venom alkaloid from the fire ant Solenopsis invicta, inhibits quorum-sensing signaling in Pseudomonas aeruginosa. J. Infect. Dis, 198(8) 2008, 1198-201.

[109]       J. Arbiser, T. Kau, M. Konar, K. Narra, R. Ramchandran, S. Summers, C. Vlahos, K. Ye, the alkaloidal component of the fire ant (Solenopsis invicta), is a naturally occurring inhibitor of phosphatidylinositol-3-kinase signaling and angiogenesis. Blood, 109(2) 2007, 560-65.

[110]       G. Howell, J. Butler, R. de Shazo, J. Farley, et al. Cardiodepressant and neurologic actions of Solenopsis invicta (imported fire ant) venom alkaloids. Ann. Allergy, Asthma, Immunol, 94(3) 2005, 380-86.

[111]       C. Niu, S. Afre, E. Gilbert, Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett. Appl. Microbiol, 43(5) 2006, 489-94.

[112]       C. Niu, E. Gilbert, Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl. Environ. Microbiol, 70(12) 2004, 6951-56.

[113]       G. Brackman, T. Defoirdt, C. Miyamoto, P. Bossier, S. Van Calenbergh, H. Nelis, T. Coenye, Cinnamaldehyde and cinnamaldehyde derivatives reduce virulence in Vibrio spp. By decreasing the DNA-binding activity of the quorum sensing response regulator LuxR. BMC Microbiol, 8 2008, 149.

[114]       J. Choo, Y. Rukayadi, J. Hwang, Inhibition of bacterial quorum sensing by vanilla extract. Lett. Appl. Microbiol, 42(6) 2006, 637-41.

[115]       A. Adonizio, K. Downum, B. Bennett. K. Mathee, Antiquorum sensing activity of medicinal plants in southern Florida. J. Ethnopharmacol, 103 2006, 427–435.

[116]       B. Huber, L.  Eberl, W. Feucht, J. Polster, Influence of Polyphenols on Bacterial Biofilm Formation and Quorum-sensing. Z. Naturforsch. 58 2003, 879-884.

[117]       N. Ni, G. Choudhary, M. Li, B. Wang, Pyrogallol and its analogs can antagonize bacterial quorum sensing in Vibrio harveyi. Bioorg. Med. Chem. Lett, 18(5) 2008, 1567-72.

[118]       Z. Zeng, L. Qian, L. Cao, Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol, 79(1) 2008, 119-26.

[119]       T. Walker, H. Bais, E. Deziel, H. Schweizer, Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol, 134 2004, 320-331.

[120]       M. Otto, Quorum-sensing control in Staphylococci - a target for antimicrobial drug therapy? FEMS Microbiol. Lett, 241 2004, 24(2) 135-41.

[121]       N. Balaban, L. Collins, J. Cullor, E. Hume, Medina-Acosta, E, Da Motta, O. V, O'Callaghan, R, Rossitto, P. V, Shirtliff, M. E, Da Silveira, L. S, Tarkowski, A, Torres, J. V. Prevention of diseases caused by Staphylococcus aureus using the peptide RIP. Peptides, 21(9) 2000, 1301-11.

[122]       Y. Gov, A. Bitler, G. Dell'Acqua, RNAIII inhibiting peptide (RIP), a global inhibitor of Staphylococcus aureus pathogenesis: structure and function analysis. Peptides (N. Y. NY, USA), 22(10) 2001, 1609-20.

[123]       N. Balaban, O. Cirioni, A. Giacometti, Treatment of Staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP. Antimicrob. Agents Chemother, 51(6) 2007, 2226-9.

[124]       N. Balaban, A. Giacometti, O. Cirioni, Use of the quorum-sensing inhibitor RNAIIIinhibiting peptide to prevent biofilm formation in vivo by drugresistant Staphylococcus epidermidis. J. Infect. Dis, 187(4) 2003, 625-30.

[125]       O. Cirioni, R. Ghiselli, D. Minardi, RNAIII-inhibiting peptide affects biofilm formation in a rat model of Staphylococcal ureteral stent infection. Antimicrob. Agents Chemother, 51(12) 2007, 4518-20.

[126]       G. Dell'Acqua, A. Giacometti, O. Cirioni,  Suppression of drug-resistant staphylococcal infections by the quorum-sensing inhibitor RNA III inhibiting peptide. J. Infect. Dis, 190(2) 2004, 318-20.

[127]       P. Anguita-Alonso, A. Giacometti, RNAIII-inhibiting-peptide-loaded olymethylmethacrylate prevents in vivo Staphylococcus aureus biofilm formation. Antimicrob. Agents Chemother,51(7), 2007, 2594-96.

[128]       N. Balaban, Y. Gov, A chimeric peptide composed of a dermaseptin derivative and an RNA III-inhibiting peptide prevents graftassociated infections by antibiotic-resistant staphylococci. Antimicrob. Agents Chemother, 48(7) 2004, 2544-50.

[129]       O. Cirioni, A. Giacometti, R. Ghiselli, RNAIII-inhibiting peptide significantly reduces bacterial load and enhances the effect of antibiotics in the treatment of central venous catheter-associated Staphylococcus aureus infections. J. Infect. Dis, 193(2) 2006, 180-86.

[130]       P. Domenico, E. Gurzenda, A. Giacometti, Bis EDT and RIP act in synergy to prevent graft infections by resistant staphylococci. Peptides, 25(12) 2004, 2047-53.

[131]       A. Giacometti, O. Cirioni, R. Ghiselli, G. Dell'Acqua, RNAIII-inhibiting peptide improves efficacy of clinically used antibiotics in a murine model of staphylococcal sepsis. Peptides, 2005, 26(2), 169-75.

[132]       Chan, W. C, Coyle, B. J, Williams, P. Virulence Regulation and Quorum Sensing in Staphylococcal Infections: Competitive AgrC Antagonists as Quorum Sensing Inhibitors. J. Med. Chem, 47(19) 2004, 4633-41.

[133]       G. Lyon, P. Mayville, T. Muir, Rational design of a global inhibitor of the virulence response in Staphylococcus aureus, based in part on localization of the site of inhibition to the receptor-histidine kinase, AgrC. Proc. Natl. Acad. Sci. USA, 97(24) 2000, 13330-35.

[134]       G. Lyon, T. Muir, Chemical signaling among bacteria and its inhibition. Chem Biol, 10 2003, 1007-1021.

[135]       J. Wright, R. III, Jin, R. Novick, R. Transient interference with staphylococcal quorum sensing blocks abscess formation. Proc. Natl. Acad. Sci. USA, 102(5) 2005, 1691-96.

[136]       J. Wright, G. III, Lyon, E. George, Hydrophobic interactions drive ligand-receptor recognition for activation and inhibition of staphylococcal quorum sensing. Proc. Natl. Acad. Sci. USA, 101(46) 2004, 16168-73.

[137]       K. Tateda, R. Comte, J. Pechere, T. Kohler,  Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob. Agents Chemother, 45(6) 2001, 1930-33.

[138]       M. Skindersoe, M. Alhede, R. Phipps, Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob. Agents Chemother, 52(10) 2008, 3648-63.

[139]       S. Favre-Bonte, T. Koehler, C. Van Delden, Biofilm formation by Pseudomonas aeruginosa: role of the C4-HSL cell-to-cell signal and inhibition by azithromycin. J. Antimicrob. Chemother, 52(4) 2003, 598-604.

[140]       N. Hoffmann, B. Lee, Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr-/- mice. Antimicrob. Agents Chemother, 51(10) 2007, 3677-87.

[141]       Y. Yoon, J. Sofos, Absence of association of autoinducer-2-based quorum sensing with heat and acid resistance of Salmonella. J Food Sci, 75 2010, 444-448.

[142]       D. Martinelli, G. Grossmann, Effects of natural and chemically synthesized furanones on quorum sensing in Chromobacterium violaceum. BMC Microbiol, 4 2004, 25-36.

[143]       D. Ren, J. Sims, T. Wood, Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone. Environ. Microbiol, 3(11) 2001, 731-6.

[144]       D. Ren, L. Bedzyk, P. Setlow, Differential gene expression to investigate the effect of (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone on Bacillus subtilis. Appl. Environ. Microbiol, 70(8) 2004, 4941-49.

[145]       D. Ren, J. Sims, T. Wood, Inhibition of biofilm formation and swarming of Bacillus subtilis by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone. Lett. Appl. Microbiol, 34(4) 2002, 293-99.

[146]       D. Ren, L. Bedzyk, R. Ye, Stationary-phase quorum-sensing signals affect autoinducer-2 and gene expression in Escherichia coli. Appl. Environ. Microbiol, 70(4) 2004, 2038-43.

[147]       T. Benneche, Z. Hussain, A. Aamdal Scheie,  Synthesis of 5-(bromomethylene)furan-2(5H)-ones and 3-(bromomethylene)isobenzofuran-1(3H)-ones as inhibitors of microbial quorum sensing. New J. Chem, 32(9) 2008, 1567-72.

[148]       K. Mathee, A. Adonizio, F.  Ausubel, Use of Ellagitannins as Inhibitors of Bacterial Quorum Sensing. PCT Int. Appl. WO/2009/114810, 2009.

[149]       H. Liu, K. Koh, J. Kim, Y. Seo, Biotechnol. Bioprocess Eng.13 2008, 458-466.

[150]       K. Stephenson, J. Hoch, Developing inhibitors to selectively target two-component and phosphorelay signal transduction systems of pathogenic microorganisms. Curr Med Chem, 11 2004, 765-773.

[151]       G. Lyon, J. Wright, T. Muir, R. Novick, Key Determinants of Receptor Activation in the agr Autoinducing Peptides of Staphylococcus aureus. Biochemistry, 41(31) 2002, 10095-104.

[152]       V. Denervaud, P. TuQuoc, D. Blanc, S. Favre-Bonte, V. Krishnapillai, Characterization of cell-tocell signaling-deficient Pseudomonas aeruginosa strains colonizing intubated patients. J Clin Microbiol, 42 2004, 554-562.

[153]       K. Duan, C. Dammel J. Stein H. Rabin, Surette MG: Modulation of Pseudomonas aeruginosa gene expression by hostmicroflora through interspecies communication. Mol Microbiol, 50 2003, 1477-1491.

[154]       A. Bozorgian, S. Zarinabadi, A. Samimi, Preparation of Xanthan Magnetic Biocompatible Nano-Composite for Removal of Ni^2+ from Aqueous Solution, Chemical Methodologies, 4 (4) (2020), 477-493

[155]       A. Samimi, S. Zarinabadi, A. Bozorgian, A. Amosoltani, M. Tarkesh, K. Kavousi, Advances of Membrane Technology in Acid Gas Removal in Industries, Progress in Chemical and Biochemical Research, 3 (1) (2020), 46-54

[156]       C. Aguilar, I. Bertani, V. Venturi, Quorum-sensing system and stationary-phase sigma factor (rpoS) of the onion pathogen Burkholderia cepacia genomovar I type strain, ATCC 25416. Appl Environ Microbiol, 69 2003, 1739-1747.

[157]       J. Hornby, S. Jacobitz-Kizzier, D. McNeel, Jensen, Inoculum size effect in dimorphic fungi: extracellular control of yeast-mycelium dimorphism in Ceratocystis ulmi. Appl Environ Microbiol, 70 2004, 1356-1359.

[158]       U. Mathesius, S. Mulders, S. Gao, M. Teplitski, G. Caetano-Anolles, B. Rolfe, Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA, 100 2003, 1444-1449.

[159]       G. Fleet, Yeast interactions and wine flavour. Int J Food Microbiol, 86 2003, 11-22.

[160]       Y. Dong, A. Gusti, Q. Zhang, Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol, 68 2002, 1754-1759.

[161]       L. Molina, F. Constantinescu, Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol Ecol, 45 2003, 71-81.

[162]       F. Xu, T. Byun, Degradation of Nacylhomoserine lactones, the bacterial quorum-sensing molecules, by acylase. J Biotechnol, 101 2003, 89-96.

[163]       M. Pasmore, J.W. Costerton, Biofilms, bacterial signaling, and their ties to marine biology. J Ind Microbiol Biotechnol, 30 2003, 407-413.

[164]       J. Skerratt, J. Bowman, G. Hallegraeff, S. James, Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Australian estuary. Mar Ecol Prog Ser, 244 2002, 1-15.

[165]       A. Valle, M. Bailey, A. Whiteley, N-acyl-Lhomoserine lactones (AHLs) affect microbial community composition and function in activated sludge. Environ Microbiol, 6 2004, 424-433.

[166]       R. Van Houdt, A. Aertsen, A. Jansen, A. Quintana, Biofilm formation and cell-to-cell signalling in Gram-negative bacteria isolated from a food processing environment. J Appl Microbiol, 96 2004, 177-184.

[167]       C. Waters, B. Bassler, Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol, 21 2005, 319–346.

[168]       J. Njoroge, V. Sperandio, Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Med, 1 2009, 201-10.

[169]       P. Ronald, Small protein-mediated quorum sensing in a Gram-negative bacterium: novel targets for control of infectious disease. Discov Med, 12 2011, 461-70.

[170]       T. Czaran, Janus-headed communication promotes bacterial cooperation and cheating: is quorum sensing useful against infections? Virulence, 1 2010, 402-403.

[171]       Y. Dong X. Zhang, Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl Environ Microbiol, 70 2004, 954-960.

[172]       R. Dudler, L. Eberl, Interactions between bacteria and eukaryotes via small molecules. Curr. Opin. Biotechnol, 17 2006, 268–273.

[173]       J. March, W. Bentley, Quorum sensing and bacterial cross-talk in biotechnology. Current Opinion in Biotechnology, 15 2004, 495–502.

[174]       Z. Hosseinzadeh, A. Ramazani, N. Razzaghi-Asl, Plants of the Genus Heracleum as a Source of Coumarin and Furanocoumarin, Journal of chemical reviews, 1(2) 2020, 78-98.

[175]       M. Abdollahbeigi, Optimizing the Process of Di-Isobutyl Phthalate Production Using Vapor Permeation, DAV International Journal of Science, 4(2) (2015), 47-52

[176]       M.J. Choobineh, B. Nasrollahzadeh, M. Abdollahbeigi, Investigation of Contact Resistance Effect on Finned Pipes under Natural and Forced Convection, DAV International Journal of Science, 4(2) (2015), 58-76

[177]       B. Nasrollahzadeh, M.J. Choobineh, M. Abdollahbeigi, Investigation of Hydrate Formation Kinetics and Mechanism of Inhibitors Effect, DAV International Journal of Science, 4 (2015), 49-56

[178]       M. Abdollahbeigi, M.J. Choobineh, B. Nasrollahzadeh, Nano Catalyst, Operation Mechanism and Their Application in Industry, Australian Journal of International Social Research, 1(5) (2015), 1-6

[179]       M. Abdollahbeigi, M.J. Choobineh, B. Nasrollahzadeh, Investigation of Molecular Structure in Gas Hydrate, Science road Journal, 3(12) (2015), 74-79

[180]       M.J. Choobineh, M. Abdollahbeigi, B. Nasrollahzadeh, the formation of gas hydrate and the effect of inhibitors on their formation process, Journal of Fundamental Applied Science 8(2S) (2016), 1150-1159

[181]       A. Bozorgian, S. Zarinabadi, A. Samimi, Optimization of Well Production by Designing a Core pipe in one of the Southwest oil Wells of Iran, Journal of Chemical Reviews, 2(2) (2020), 122-129

[181]      D.Ren, A. Bedzyk Laura, W. Ye Rick, Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli. Biotechnol. Bioeng, 88(5) 2004, 630-42.