Functional Diversity of Quorum Sensing Receptors in Pathogenic Bacteria: Interspecies, Intraspecies and Interkingdom Level

Author(s): Fazlurrahman Khan, Aqib Javaid, Young-Mog Kim*.

Journal Name: Current Drug Targets

Volume 20 , Issue 6 , 2019

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

The formation of biofilm by pathogenic bacteria is considered as one of the most powerful mechanisms/modes of resistance against the action of several antibiotics. Biofilm is formed as a structural adherent over the surfaces of host, food and equipments etc. and is further functionally coordinated by certain chemicals produced itself. These chemicals are known as quorum sensing (QS) signaling molecules and are involved in the cross talk at interspecies, intraspecies and interkingdom levels thus resulting in the production of virulence factors leading to pathogenesis. Bacteria possess receptors to sense these chemicals, which interact with the incoming QS molecules. It is followed by the secretion of virulence molecules, regulation of bioluminescence, biofilm formation, antibiotic resistance development and motility behavioral responses. In the natural environment, different bacterial species (Gram-positive and Gram-negative) produce QS signaling molecules that are structurally and functionally different. Recent and past research shows that various antagonistic molecules (naturally and chemically synthesized) are characterized to inhibit the formation of biofilm and attenuation of bacterial virulence by blocking the QS receptors. This review article describes about the diverse QS receptors at their structural, functional and production levels. Thus, by blocking these receptors with inhibitory molecules can be a potential therapeutic approach to control pathogenesis. Furthermore, these receptors can also be used as a structural platform to screen the most potent inhibitors with the help of bioinformatics approaches.

Keywords: Bacteria, inhibitor, pathogenesis, quorum sensing receptor, biofilm, quorum sensing (QS).

[1]
Wu X, Lu Y, Zhou S, Chen L, Xu B. Impact of climate change on human infectious diseases: Empirical evidence and human adaptation. Environ Int 2016; 86: 14-23.
[2]
Berne C, Ducret A, Hardy GG, Brun YV. Adhesins involved in attachment to abiotic surfaces by Gram-negative bacteria. Microbiol Spectr 2015; 3(4)
[3]
Bogino PC, Oliva Mde L, Sorroche FG, Giordano W. The role of bacterial biofilms and surface components in plant-bacterial associations. Int J Mol Sci 2013; 14(8): 15838-59.
[4]
Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004; 2(2): 95-108.
[5]
Reffuveille F, Josse J, Vallé Q, et al. Staphylococcus aureus biofilms and their impact on the medical field, The rise of virulence and antibiotic resistance; Shymaa Enany and Laura E.Crotty Alexander,. Ed. Rijeka: InTech 2017; p. Ch. 11..
[6]
Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 2010; 35(4): 322-32.
[7]
Li YH, Tian X. Quorum sensing and bacterial social interactions in biofilms. Sensors (Basel) 2012; 12(3): 2519-38.
[8]
Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005; 21: 319-46.
[9]
Parker CT, Sperandio V. Cell-to-cell signalling during pathogenesis. Cell Microbiol 2009; 11(3): 363-9.
[10]
Kendall MM, Sperandio V. Cell-to-cell signaling in E. coli and Salmonella. Ecosal Plus 2014; 6(1)
[11]
LaSarre B, Federle MJ. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 2013; 77(1): 73-111.
[12]
Atkinson S, Williams P. Quorum sensing and social networking in the microbial world. J R Soc Interface 2009; 6(40): 959-78.
[13]
Zhou J, Lyu Y, Richlen M, Anderson DM, Cai Z. Quorum sensing is a language of chemical signals and plays an ecological role in algal-bacterial interactions. CRC Crit Rev Plant Sci 2016; 35(2): 81-105.
[14]
Deep A, Chaudhary U, Gupta V. Quorum sensing and bacterial pathogenicity: from molecules to disease. J Lab Physicians 2011; 3(1): 4-11.
[15]
Chen X, Schauder S, Potier N, et al. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 2002; 415(6871): 545-9.
[16]
Pereira CS, Thompson JA, Xavier KB. AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 2013; 37(2): 156-81.
[17]
Quinones B, Dulla G, Lindow SE. Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact 2005; 18(7): 682-93.
[18]
Doganer BA, Yan LK, Youk H. Autocrine signaling and quorum sensing: extreme ends of a common spectrum. Trends Cell Biol 2016; 26(4): 262-71.
[19]
Antunes LCM, Ferreira RBR, Buckner MMC, Finlay BB. Quorum sensing in bacterial virulence. Microbiol 2010; 156(8): 2271-82.
[20]
Patel R. Biofilms and antimicrobial resistance. Clin Orthop Relat Res 2005; (437): 41-7.
[21]
Beceiro A, Tomás M, Bou G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin Microbiol Rev 2013; 26(2): 185-230.
[22]
Ashima KB, Kittappa V, Neha R. Bacterial quorum sensing inhibitors: Attractive alternatives for control of infectious pathogens showing multiple drug resistance. Recent Pat Antiinfect Drug Discov 2013; 8(1): 68-83.
[23]
Fuqua C, Greenberg EP. Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 2002; 3(9): 685-95.
[24]
Sperandio V, Torres AG, Kaper JB. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 2002; 43(3): 809-21.
[25]
Li J, Attila C, Wang L, et al. Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 2007; 189(16): 6011-20.
[26]
Sperandio V, Li CC, Kaper JB. Quorum-sensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 2002; 70(6): 3085-93.
[27]
Kim T, Duong T, Wu CA, et al. Structural insights into the molecular mechanism of Escherichia coli SdiA, a quorum-sensing receptor. Acta Crystallogr D Biol Crystallogr 2014; 70(3): 694-707.
[28]
Lim JY, Sheng H, Seo KS, Park YH, Hovde CJ. Characterization of an Escherichia coli O157:H7 plasmid O157 deletion mutant and its survival and persistence in cattle. Appl Environ Microbiol 2007; 73(7): 2037-47.
[29]
Curtis MM, Russell R, Moreira CG, et al. QseC inhibitors as an antivirulence approach for Gram-negative pathogens. MBio 2014; 5(6): e02165.
[30]
Eibergen NR, Moore JD, Mattmann ME, Blackwell HE. Potent and selective modulation of the RhlR quorum sensing receptor by using non-native ligands: An emerging target for virulence control in Pseudomonas aeruginosa. Chembiochem 2015; 16(16): 2348-56.
[31]
Moore JD, Rossi FM, Welsh MA, Nyffeler KE, Blackwell HE. A comparative analysis of synthetic quorum sensing modulators in Pseudomonas aeruginosa: New insights into mechanism, active efflux susceptibility, phenotypic response, and next-generation ligand design. J Am Chem Soc 2015; 137(46): 14626-39.
[32]
Pearson JP, Gray KM, Passador L, et al. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci USA 1994; 91(1): 197-201.
[33]
Oinuma K, Greenberg EP. Acyl-homoserine lactone binding to and stability of the orphan Pseudomonas aeruginosa quorum-sensing signal receptor QscR. J Bacteriol 2011; 193(2): 421-8.
[34]
Lee JH, Lequette Y, Greenberg EP. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 2006; 59(2): 602-9.
[35]
Lintz MJ, Oinuma K, Wysoczynski CL, Greenberg EP, Churchill ME. Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc Natl Acad Sci USA 2011; 108(38): 15763-8.
[36]
Pesci EC, Milbank JB, Pearson JP, et al. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 1999; 96(20): 11229-34.
[37]
Rabin N, Delago A, Inbal B, Krief P, Meijler MM. Tailor-made LasR agonists modulate quorum sensing in Pseudomonas aeruginosa. Org Biomol Chem 2013; 11(41): 7155-63.
[38]
Yang L, Rybtke MT, Jakobsen TH, et al. Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrob Agents Chemother 2009; 53(6): 2432-43.
[39]
Smith KM, Bu Y, Suga H. Induction and inhibition of Pseudomonas aeruginosa quorum sensing by synthetic autoinducer analogs. Chem Biol 2003; 10(1): 81-9.
[40]
Smith KM, Bu Y, Suga H. Library screening for synthetic agonists and antagonists of a Pseudomonas aeruginosa autoinducer. Chem Biol 2003; 10(6): 563-71.
[41]
Geske GD, O’Neill JC, Miller DM, Mattmann ME, Blackwell HE. 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 2007; 129(44): 13613-25.
[42]
Ishida T, Ikeda T, Takiguchi N, et al. Inhibition of quorum sensing in Pseudomonas aeruginosa by N-acyl cyclopentylamides. Appl Environ Microbiol 2007; 73(10): 3183-8.
[43]
Amara N, Mashiach R, Amar D, et al. Covalent inhibition of bacterial quorum sensing. J Am Chem Soc 2009; 131(30): 10610-9.
[44]
Morkunas B, Galloway WRJD, Wright M, et al. Inhibition of the production of the Pseudomonas aeruginosa virulence factor pyocyanin in wild-type cells by quorum sensing autoinducer-mimics. Org Biomol Chem 2012; 10(42): 8452-64.
[45]
Rasmussen TB, Skindersoe ME, Bjarnsholt T, et al. Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiol 2005; 151(5): 1325-40.
[46]
Müh U, Schuster M, Heim R, et al. Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high-throughput screen. Antimicrob Agents Chemother 2006; 50(11): 3674-9.
[47]
Borlee BR, Geske GD, Blackwell HE, Handelsman J. Identification of synthetic inducers and inhibitors of the quorum-sensing regulator LasR in Pseudomonas aeruginosa by high-throughput screening. Appl Environ Microbiol 2010; 76(24): 8255-8.
[48]
Hirakawa H, Tomita H. Interference of bacterial cell-to-cell communication: a new concept of antimicrobial chemotherapy breaks antibiotic resistance. Frontin Microbiol 2013; 4: 114.
[49]
Kim HS, Lee SH, Byun Y, Park HD. 6-Gingerol reduces Pseudomonas aeruginosa biofilm formation and virulence via quorum sensing inhibition. Sci Rep 2015; 5: 8656.
[50]
Kumar L, Chhibber S, Kumar R, Kumar M, Harjai K. Zingerone silences quorum sensing and attenuates virulence of Pseudomonas aeruginosa. Fitoterapia 2015; 102: 84-95.
[51]
Pui CF, Wong WC, Chai LC, et al. Simultaneous detection of Salmonella spp., Salmonella typhi and Salmonella typhimurium in sliced fruits using multiplex PCR. Food Control 2011; 22(2): 337-42.
[52]
Patankar AV, Gonzalez JE. Orphan LuxR regulators of quorum sensing. FEMS Microbiol Rev 2009; 33(4): 739-56.
[53]
Ahmer BM. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 2004; 2(4): 933-45.
[54]
Sperandio V. SdiA bridges chemical signaling between Salmonella enterica Serovar Typhimurium and Yersinia enterocolitica in mice. J Bacteriol 2010; 192(1): 21-2.
[55]
Swift S, Winson MK, Chan PF, et al. A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR: LuxI superfamily in enteric bacteria. Mol Microbiol 1993; 10(3): 511-20.
[56]
Dyszel JL, Smith JN, Lucas DE, et al. Salmonella enterica Serovar Typhimurium can detect acyl homoserine lactone production by Yersinia enterocolitica in mice. J Bacteriol 2010; 192(1): 29-37.
[57]
Smith JN, Dyszel JL, Soares JA, et al. SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS One 2008; 3(7): e2826.
[58]
Joo H-S, Otto M. Molecular basis of in-vivo biofilm formation by bacterial pathogens. Chem Biol 2012; 19(12): 1503-13.
[59]
Ji G, Beavis RC, Novick RP. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc Natl Acad Sci USA 1995; 92(26): 12055-9.
[60]
Novick RP, Projan SJ, Kornblum J, et al. The agr P2 operon: an autocatalytic sensory transduction system in Staphylococcus aureus. Mol Gen Genet 1995; 248(4): 446-58.
[61]
Tal-Gan Y, Ivancic M, Cornilescu G, Blackwell HE. Characterization of structural elements in native autoinducing peptides and non-native analogues that permit the differential modulation of AgrC-type quorum sensing receptors in Staphylococcus aureus. Org Biomol Chem 2016; 14(1): 113-21.
[62]
Yang T, Tal-Gan Y, Paharik AE, Horswill AR, Blackwell HE. Structure-function analyses of a Staphylococcus epidermidis autoinducing peptide reveals motifs critical for AgrC-type receptor modulation. ACS Chem Biol 2016; 11(7): 1982-91.
[63]
Sung JML, Chantler PD, Lloyd DH. Accessory gene regulator locus of Staphylococcus intermedius. Infect Immun 2006; 74(5): 2947-56.
[64]
Robinson DA, Monk AB, Cooper JE, Feil EJ, Enright MC. Evolutionary genetics of the accessory gene regulator (agr) locus in Staphylococcus aureus. J Bacteriol 2005; 187(24): 8312-21.
[65]
Abdelnour A, Arvidson S, Bremell T, Ryd Ã. ©n C, Tarkowski A. The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect Immun 1993; 61(9): 3879-85.
[66]
Gomes-Fernandes M, Laabei M, Pagan N, et al. Accessory gene regulator (Agr) functionality in Staphylococcus aureus derived from lower respiratory tract infections. PLOS ONE 2017; 12(4): e0175552.
[67]
Desouky SE, Shojima A, Singh RP, et al. Cyclodepsipeptides produced by actinomycetes inhibit cyclic-peptide-mediated quorum sensing in Gram-positive bacteria. FEMS Microbiol Lett 2015; 362(14)
[68]
Osman KM, Zolnikov TR, Samir A, Orabi A. Prevalence, pathogenic capability, virulence genes, biofilm formation, and antibiotic resistance of Listeria in goat and sheep milk confirms need of hygienic milking conditions. Pathog Glob Health 2014; 108(1): 21-9.
[69]
Begley Mi, Kerr C, Hill C. Exposure to bile influences biofilm formation by Listeria monocytogenes. Gut Pathog 2009; 1(1): 11.
[70]
Reis-Teixeira FBd Alves VF, de Martinis ECP. Growth, viability and architecture of biofilms of Listeria monocytogenes formed on abiotic surfaces. Braz J Microbiol 2017; 48(3): 587-91.
[71]
Chen CC, Wang L, Plikus MV, et al. Organ-level quorum sensing directs regeneration in hair stem cell populations. Cell 2015; 161(2): 277-90.
[72]
McDougald D, Rice SA, Kjelleberg S. Bacterial quorum sensing and interference by naturally occurring biomimics. Anal Bioanal Chem 2007; 387(2): 445-53.
[73]
Gonzalez JE, Keshavan ND. Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 2006; 70(4): 859-75.
[74]
Ismail AS, Valastyan JS, Bassler BL. A host-produced autoinducer-2 mimic activates bacterial quorum sensing. Cell Host Microbe 2016; 19(4): 470-80.
[75]
Kendall MM, Sperandio V. What a dinner party! mechanisms and functions of interkingdom signaling in host-pathogen associations. MBio 2016; 7(2): e01748.
[76]
Hughes DT, Clarke MB, Yamamoto K, Rasko DA, Sperandio V. The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC). PLoS Pathog 2009; 5(8): e1000553.
[77]
Lee JH, Lee J. Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 2010; 34(4): 426-44.
[78]
Lee JH, Wood TK, Lee J. Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 2015; 23(11): 707-18.
[79]
Hu M, Zhang C, Mu Y, Shen Q, Feng Y. Indole affects biofilm formation in bacteria. Indian J Microbiol 2010; 50(4): 362-8.
[80]
Bommarius B, Anyanful A, Izrayelit Y, et al. A family of indoles regulate virulence and Shiga toxin production in pathogenic E. coli. PLoS One 2013; 8(1): e54456.
[81]
Rasmussen TB, Manefield M, Andersen JB, et al. How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiol 2000; 146(12): 3237-44.
[82]
Gopu V, Kothandapani S, Shetty PH. Quorum quenching activity of Syzygium cumini (L.) Skeels and its anthocyanin malvidin against Klebsiella pneumoniae. Microb Pathog 2015; 79: 61-9.
[83]
Nakashima K, Sugiura A, Momoi H, Mizuno T. Phosphotransfer signal transduction between two regulatory factors involved in the osmoregulated kdp operon in Escherichia coli. Mol Microbiol 1992; 6(13): 1777-84.
[84]
Jung K, Fried L, Behr S, Heermann R. Histidine kinases and response regulators in networks. Curr Opin Microbiol 2012; 15(2): 118-24.
[85]
Clarke MB, Sperandio V. Transcriptional regulation of flhDC by QseBC and sigma (FliA) in enterohaemorrhagic Escherichia coli. Mol Microbiol 2005; 57(6): 1734-49.
[86]
Reading NC, Rasko DA, Torres AG, Sperandio V. The two-component system QseEF and the membrane protein QseG link adrenergic and stress sensing to bacterial pathogenesis. Proc Natl Acad Sci USA 2009; 106(14): 5889-94.
[87]
Njoroge JW, Nguyen Y, Curtis MM, Moreira CG, Sperandio V. Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli. MBio 2012; 3(5): e00280-12.
[88]
Veron W, Lesouhaitier O, Pennanec X, et al. Natriuretic peptides affect Pseudomonas aeruginosa and specifically modify lipopolysaccharide biosynthesis. FEBS J 2007; 274(22): 5852-64.
[89]
Blier AS, Veron W, Bazire A, et al. C-type natriuretic peptide modulates quorum sensing molecule and toxin production in Pseudomonas aeruginosa. Microbiol 2011; 157(7): 1929-44.
[90]
Zaborina O, Lepine F, Xiao G, et al. Dynorphin activates quorum sensing quinolone signaling in Pseudomonas aeruginosa. PLoS Pathog 2007; 3(3): e35.
[91]
Schuster M, Sexton DJ, Diggle SP, Greenberg EP. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol 2013; 67: 43-63.
[92]
Beury-Cirou A, Tannieres M, Minard C, et al. At a supra-physiological concentration, human sexual hormones act as quorum-sensing inhibitors. PLoS One 2013; 8(12): e83564.
[93]
Hoyland-Kroghsbo NM, Maerkedahl RB, Svenningsen SL. A quorum-sensing-induced bacteriophage defense mechanism. MBio 2013; 4(1): e00362-12.
[94]
Gopu V, Shetty PH. Cyanidin inhibits quorum signalling pathway of a food borne opportunistic pathogen. J Food Sci Technol 2016; 53(2): 968-76.
[95]
Beltz S, Bassler J, Schultz JE. Regulation by the quorum sensor from Vibrio indicates a receptor function for the membrane anchors of adenylate cyclases. Elife 2016; 5.
[96]
Zhao M, Yu Y, Hua Y, et al. Design, synthesis and biological evaluation of N-sulfonyl homoserine lactone derivatives as inhibitors of quorum sensing in Chromobacterium violaceum. Mol 2013; 18(3): 3266-78.
[97]
Goh WK, Gardner CR, Chandra Sekhar KV, et al. Synthesis, quorum sensing inhibition and docking studies of 1,5-dihydropyrrol-2-ones. Bioorg Med Chem 2015; 23(23): 7366-77.
[98]
Singh RP, Okubo K, Ohtani K, et al. Rationale design of quorum-quenching peptides that target the VirSR system of Clostridium perfringens. FEMS Microbiol Lett 2015; 362(22)
[99]
Taha MO, Al-Bakri AG, Zalloum WA. Discovery of potent inhibitors of pseudomonal quorum sensing via pharmacophore modeling and in silico screening. Bioorg Med Chem Lett 2006; 16(22): 5902-6.
[100]
Wei G, Lo C, Walsh C, Hiller NL, Marculescu R. In Silico evaluation of the impacts of quorum sensing inhibition (qsi) on strain competition and development of qsi resistance. Sci Rep 2016; 6: 35136.
[101]
Vasavi HS, Sudeep HV, Lingaraju HB, Shyam Prasad K. Bioavailability-enhanced Resveramax modulates quorum sensing and inhibits biofilm formation in Pseudomonas aeruginosa PAO1. Microb Pathog 2017; 104: 64-71.
[102]
Ahumedo M, Drosos JC, Vivas-Reyes R. Application of molecular docking and ONIOM methods for the description of interactions between anti-quorum sensing active (AHL) analogues and the Pseudomonas aeruginosa LasR binding site. Mol Biosyst 2014; 10(5): 1162-71.
[103]
Gerdt JP, McInnis CE, Schell TL, Rossi FM, Blackwell HE. Mutational analysis of the quorum-sensing receptor LasR reveals interactions that govern activation and inhibition by nonlactone ligands. Chem Biol 2014; 21(10): 1361-9.
[104]
Kim C, Kim J, Park HY, et al. Furanone derivatives as quorum-sensing antagonists of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 2008; 80(1): 37-47.
[105]
Park J, Kaufmann GF, Bowen JP, et al. a venom alkaloid from the fire ant Solenopsis invicta, inhibits quorum-sensing signaling in Pseudomonas aeruginosa. J Infect Dis 2008; 198(8): 1198-201.
[106]
Niu C, Afre S, Gilbert ES. Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett Appl Microbiol 2006; 43(5): 489-94.
[107]
Bucio-Cano A, Reyes-Arellano A, Correa-Basurto J, et al. Targeting quorum sensing by designing azoline derivatives to inhibit the N-hexanoyl homoserine lactone-receptor CviR: Synthesis as well as biological and theoretical evaluations. Bioorg Med Chem 2015; 23(24): 7565-77.
[108]
Garner AL, Yu J, Struss AK, et al. Synthesis of ‘clickable’ acylhomoserine lactone quorum sensing probes: unanticipated effects on mammalian cell activation. Bioorg Med Chem Lett 2011; 21(9): 2702-5.
[109]
Challan Belval S, Gal L, Margiewes S, et al. Assessment of the roles of LuxS, S-ribosyl homocysteine, and autoinducer 2 in cell attachment during biofilm formation by Listeria monocytogenes EGD-e. Appl Environ Microbiol 2006; 72(4): 2644-50.
[110]
Sela S, Frank S, Belausov E, Pinto R. A mutation in the luxS gene influences Listeria monocytogenes biofilm formation. Appl Environ Microbiol 2006; 72(8): 5653-8.
[111]
Garmyn D, Gal L, Lemaitre J-P, Hartmann A, Piveteau P. Communication and autoinduction in the species Listeria monocytogenes: A central role for the agr system. Commun Integr Biol 2009; 2(4): 371-4.
[112]
Rajamanikandan S, Jeyakanthan J, Srinivasan P. Molecular docking, molecular dynamics simulations, computational screening to design quorum sensing inhibitors targeting LuxP of Vibrio harveyi and its biological evaluation. Appl Biochem Biotechnol 2017; 181(1): 192-218.
[113]
Nandi S. Recent advances in ligand and structure based screening of potent quorum sensing inhibitors against antibiotic resistance induced bacterial virulence. Recent Pat Biotechnol 2016; 10(2): 195-216.
[114]
Lee J, Jayaraman A, Wood TK. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 2007; 7: 42.
[115]
Rezzonico F, Smits THM, Duffy B. Detection of AI-2 receptors in genomes of Enterobacteriaceae suggests a role of type-2 quorum sensing in closed ecosystems. Sensors 2012; 12(5): 6645.
[116]
Walters M, Sperandio V. Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect Immun 2006; 74(10): 5445-55.
[117]
Riedel CU, Monk IR, Casey PG, et al. AgrD-dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes. Mol Microbiol 2009; 71(5): 1177-89.
[118]
Garmyn D, Augagneur Y, Gal L, Vivant AL, Piveteau P. Listeria monocytogenes differential transcriptome analysis reveals temperature-dependent Agr regulation and suggests overlaps with other regulons. PLoS One 2012; 7(9): e43154.
[119]
Auger S, Krin E, Aymerich S, Gohar M. Autoinducer 2 affects biofilm formation by Bacillus cereus. Appl Environ Microbiol 2006; 72(1): 937-41.
[120]
Cabrera R, Rodriguez-Romero A, Guarneros G, de la Torre M. New insights into the interaction between the quorum-sensing receptor NprR and its DNA target, or the response regulator Spo0F. FEBS Lett 2016; 590(18): 3243-53.
[121]
Ledgham F, Ventre I, Soscia C, et al. Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol Microbiol 2003; 48(1): 199-210.
[122]
Ilangovan A, Fletcher M, Rampioni G, et al. Structural basis for native agonist and synthetic inhibitor recognition by the Pseudomonas aeruginosa quorum sensing regulator PqsR (MvfR). PLoS Pathog 2013; 9(7): e1003508.
[123]
Xiao G, Deziel E, He J, et al. MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 2006; 62(6): 1689-99.
[124]
Croda-Garcia G, Grosso-Becerra V, Gonzalez-Valdez A, Servin-Gonzalez L, Soberon-Chavez G. Transcriptional regulation of Pseudomonas aeruginosa rhlR: role of the CRP orthologue Vfr (virulence factor regulator) and quorum-sensing regulators LasR and RhlR. Microbiol 2011; 157(Pt 9): 2545-55.
[125]
Gambello MJ, Iglewski BH. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 1991; 173(9): 3000-9.
[126]
Henke JM, Bassler BL. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 2004; 186(20): 6902-14.
[127]
Cao JG, Meighen EA. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J Biol Chem 1989; 264(36): 21670-6.
[128]
Jung SA, Chapman CA, Ng WL. Quadruple quorum-sensing inputs control Vibrio cholerae virulence and maintain system robustness. PLoS Pathog 2015; 11(4): e1004837.
[129]
Papenfort K, Silpe JE, Schramma KR, et al. A Vibrio cholerae autoinducer-receptor pair that controls biofilm formation. Nat Chem Biol 2017; 13(5): 551-7.
[130]
Miller ST, Xavier KB, Campagna SR, et al. Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol Cell 2004; 15(5): 677-87.
[131]
Almeida FA, Pinto UM, Vanetti MC. Novel insights from molecular docking of SdiA from Salmonella Enteritidis and Escherichia coli with quorum sensing and quorum quenching molecules. Microb Pathog 2016; 99: 178-90.
[132]
Ahmer BM, van Reeuwijk J, Timmers CD, Valentine PJ, Heffron F. Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J Bacteriol 1998; 180(5): 1185-93.
[133]
Armbruster CE, Pang B, Murrah K, et al. RbsB (NTHI_0632) mediates quorum signal uptake in nontypeable Haemophilus influenzae strain 86-028NP. Mol Microbiol 2011; 82(4): 836-50.
[134]
Wang B, Zhao A, Xie Q, et al. Functional plasticity of the AgrC receptor histidine kinase required for Staphylococcal virulence. Cell Chem Biol 2017; 24(1): 76-86.
[135]
Brameyer S, Heermann R. Quorum sensing and LuxR solos in Photorhabdus. Curr Top Microbiol Immunol 2017; 402: 103-19.
[136]
Takayama Y, Kato N. Switch of SpnR function from activating to inhibiting quorum sensing by its exogenous addition. Biochem Biophys Res Commun 2016; 477(4): 993-7.
[137]
Dong G, Tian XL, Cyr K, et al. Membrane Topology and structural insights into the peptide pheromone receptor ComD, a quorum-sensing histidine protein kinase of Streptococcus mutans. Sci Rep 2016; 6: 26502.
[138]
Gerdt JP, Wittenwyler DM, Combs JB, et al. Chemical interrogation of LuxR-type quorum sensing receptors reveals new insights into receptor selectivity and the Potential for Interspecies Bacterial Signaling. ACS Chem Biol 2017; 12(9): 2457-64.
[139]
Shi K, Brown CK, Gu ZY, et al. Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis. Proc Natl Acad Sci USA 2005; 102(51): 18596-601.
[140]
Tan KH, Tan JY, Yin WF, Chan KG. Genome analysis of quorum sensing Cedecea neteri SSMD04 leads to identification of its novel signaling synthase (cneI), cognate receptor (cneR) and an orphan receptor. PeerJ 2015; 3: e1216.
[141]
Bassler BL, Swem LR, Ulrich SM, O’Loughlin CT. Small molecule antagonists of bacterial quorum-sensing receptors. Google Patents 2012.
[142]
Gelhaus HC, Rozak DA, Nierman WC, et al. Exogenous Yersinia pestis quorum sensing molecules N-octanoyl-homoserine lactone and N-(3-oxooctanoyl)-homoserine lactone regulate the LcrV virulence factor. Microb Pathog 2009; 46(5): 283-7.
[143]
Rader BA, Wreden C, Hicks KG, Sweeney EG, Ottemann KM, Guillemin K. Helicobacter pylori perceives the quorum-sensing molecule AI-2 as a chemorepellent via the chemoreceptor TlpB. Microbiol 2011; 157(Pt 9): 2445-1455.
[144]
Ravichandiran V, Shanmugam K, Solomon AP. Screening of SdiA inhibitors from Melia dubia seeds extracts towards the hold back of uropathogenic E.coli quorum sensing-regulated factors. Med Chem 2013; 9(6): 819-927.
[145]
Rooks MG, Veiga P, Reeves AZ, et al. QseC inhibition as an antivirulence approach for colitis-associated bacteria. Proc Natl Acad Sci USA 2017; 114(1): 142-7.
[146]
O’Loughlin CT, Miller LC, Siryaporn A, Drescher K, Semmelhack MF, Bassler BL. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci USA 2013; 110(44): 17981-6.
[147]
Liu HB, Lee JH, Kim JS, Park S. Inhibitors of the Pseudomonas aeruginosa quorum-sensing regulator, QscR. Biotechnol Bioeng 2010; 106(1): 119-26.
[148]
Jakobsen TH, Bragason SK, Phipps RK, et al. Food as a source for quorum sensing inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl Environ Microbiol 2012; 78(7): 2410-21.
[149]
Li M, Ni N, Chou HT, et al. Structure-based discovery and experimental verification of novel AI-2 quorum sensing inhibitors against Vibrio harveyi. ChemMedChem 2008; 3(8): 1242-9.
[150]
Ni N, Choudhary G, Peng H, et al. Inhibition of quorum sensing in Vibrio harveyi by boronic acids. Chem Biol Drug Des 2009; 74(1): 51-6.
[151]
Peng H, Cheng Y, Ni N, et al. Synthesis and evaluation of new antagonists of bacterial quorum sensing in Vibrio harveyi. ChemMedChem 2009; 4(9): 1457-68.
[152]
Sabag-Daigle A, Soares JA, Smith JN, Elmasry ME, Ahmer BM. The acyl homoserine lactone receptor, SdiA, of Escherichia coli and Salmonella enterica serovar Typhimurium does not respond to indole. Appl Environ Microbiol 2012; 78(15): 5424-31.
[153]
Mansson M, Nielsen A, Kjaerulff L, et al. Inhibition of virulence gene expression in Staphylococcus aureus by novel depsipeptides from a marine photobacterium. Mar Drugs 2011; 9(12): 2537-52.
[154]
Lyon GJ, Mayville P, Muir TW, Novick RP. 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 2000; 97(24): 13330-5.
[155]
Sabbah M, Soulere L, Reverchon S, Queneau Y, Doutheau A. LuxR dependent quorum sensing inhibition by N,N′-disubstituted imidazolium salts. Bioorg Med Chem 2011; 19(16): 4868-75.
[156]
Tao Y, Morohoshi T, Kato N, Ikeda T, Zhuang H. The function of SpnR and the inhibitory effects by halogenated furanone on quorum sensing in Serratia marcescens AS-1. Wei Sheng Wu Xue Bao 2008; 48(3): 391-7.
[157]
Hentzer M, Wu H, Andersen JB, et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 2003; 22(15): 3803-15.
[158]
Kordbacheh H, Eftekhar F, Ebrahimi SN. Anti-quorum sensing activity of Pistacia atlantica against Pseudomonas aeruginosa PAO1 and identification of its bioactive compounds. Microb Pathog 2017; 110: 390-8.
[159]
Ramanathan S, Ravindran D, Arunachalam K, Arumugam VR. Inhibition of quorum sensing-dependent biofilm and virulence genes expression in environmental pathogen Serratia marcescens by petroselinic acid. Antonie Van Leeuwenhoek 2018; 111(4): 501-15.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 6
Year: 2019
Page: [655 - 667]
Pages: 13
DOI: 10.2174/1389450120666181123123333
Price: $65

Article Metrics

PDF: 38
HTML: 5
EPUB: 1
PRC: 1