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REVIEW ARTICLE
Year : 2018  |  Volume : 6  |  Issue : 1  |  Page : 1-10

Anti-quorum sensing natural compounds


Department of Medical Microbiology and Parasitology, Faculty of Medicine, Princess Al-Jawhara Center of Excellence in Research of Hereditary Disorders, King Abdulaziz University, Jeddah, Saudi Arabia

Date of Web Publication7-May-2018

Correspondence Address:
Dr. Hani Z Asfour
Department of Medical Microbiology and Parasitology, Faculty of Medicine, Princess Al-Jawhara Center of Excellence In Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589
Saudi Arabia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/JMAU.JMAU_10_18

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  Abstract 

Increasing extent of pathogenic resistance to drugs has encouraged the seeking for new anti-virulence drugs. Many pharmacological and pharmacognostical researches are performed to identify new drugs or discover new structures for the development of novel therapeutic agents in the antibiotic treatments. Although many phytochemicals show prominent antimicrobial activity, their power lies in their anti-virulence properties. Quorum sensing (QS) is a bacterial intercellular communication mechanism, which depends on bacterial cell population density and controls the pathogenesis of many organisms by regulating gene expression, including virulence determinants. QS has become an attractive target for the development of novel anti-infective agents that do not rely on the use of antibiotics. Anti-QS compounds are known to have the ability to prohibit bacterial pathogenicity. Medicinal plants offer an attractive repertoire of phytochemicals with novel microbial disease-controlling potential, due to the spectrum of secondary metabolites present in extracts, which include phenolics, quinones, flavonoids, alkaloids, terpenoids, and polyacetylenes. They have recently received considerable attention as a new source of safe and effective QS inhibitory substances. The objective of this review is to give a brief account of the research reports on the plants and natural compounds with anti-QS potential.

Keywords: Anti-virulence, bacterial pathogenicity, natural products, quorum sensing


How to cite this article:
Asfour HZ. Anti-quorum sensing natural compounds. J Microsc Ultrastruct 2018;6:1-10

How to cite this URL:
Asfour HZ. Anti-quorum sensing natural compounds. J Microsc Ultrastruct [serial online] 2018 [cited 2018 Jul 23];6:1-10. Available from: http://www.jmau.org/text.asp?2018/6/1/1/231941


  Introduction Top


Diseases which caused by bacteria, viruses, fungi, and parasites are an important cause of mortality and morbidity, in all regions of the world particularly in the developing countries.[1] Bacteria and fungi resistance to antibiotics has grown in the last decades, but the rate of discovery of new antibiotics has steadily decreased.[2] The cause behind the lack of antibiotic discoveries are diverse and include among others, the poor return on investment compared to drugs for chronic diseases and regulatory burdens for smaller pharmaceutical companies.[3] Infections caused by resistant pathogens can be overcome using a combination of antibiotics with the variable mode of actions. However, the increased prevalence of pathogen resistant and the formation of bacterial biofilms that are difficult to eradicate have targeted the efforts to find alternatives to the current antibiotic therapy,[4] which is inadequate to control the infection of microbes [5] and creates major public health problems.[6] Thus, various pharmacognostical and pharmacological studies are performed to discover new therapeutic measures to prevent infection among drug-resistant bacterial pathogens.[7] An important approach is to target bacterial cell-to-cell communication, commonly known as quorum sensing (QS).[8] It is a way that bacteria use to sense information from other cells.

Quorum sensing mechanism

The QS mechanism is depend on the synthesis, release, and uptake of autoinducers (AIs) in the surrounding medium, whose concentration related to the density of secreting bacteria. AIs, extracellular signaling molecules, which accumulate in the environment in proportion to cell density is utilized for this intercellular communication.[9],[10],[11] Their function is to regulate gene expression in other cells of the community, which in turn, controls a number of bacterial responses. Various bacterial physiological processes, including virulence, motility, luminescence, biofilm formation, sporulation, development of genetic competence, synthesis of peptide antibiotics, production of secreted proteolytic enzymes, and fluorescence are regulated by QS.[12],[13] Xavier and Bassler reported that signal molecule production is depending on an autoinducing mechanism and their type differs between Gram-negative and Gram-positive bacteria.[14] These signaling molecules and their receptors have been broadly divided into three major classes: (1) N- acyl homoserine lactones (AHLs), which vary in the length and oxidation state of the acyl side chain and produced by Gram-negative bacteria to monitor their population density in QS control of gene expression. The signals are synthesized by members of the LuxI family of proteins; (2) oligopeptides or autoinducing peptides, consisting of 5–34 amino acids residues, are generally involved in intercellular communication in Gram-positive bacteria. Many of these peptides are exported by dedicated systems, posttranslationally modified in various ways and finally sensed by other cells through membrane-located receptors that are part of two-component regulatory systems; and (3) AI-2 employed by both Gram-positive and Gram-negative bacteria for interspecies communication. It has been chemically identified as a furanosylborate diester synthesized by members of the LuxS family of proteins.[14],[15],[16] Gram-positive bacteria: the precursor peptide AIs are modified and transported out of the cell by ATP-binding cassette exporter complex. When the concentration of the peptide AIs reaches the threshold value, the sensor kinase protein will be activated and phosphorylate the response regulator protein, which will then binds to the target promoter that will lead to QS gene regulation. However, in Gram-negative bacteria, the AIs are produced and diffused freely out of the cell. When the concentration of the AIs reaches the threshold value, a positive feedback loop will be formed that causes more AIs to be synthesized. The AIs produced will bind to their cognate receptor to form an AI-receptor complex which will then binds to the target promoter that lead to QS gene regulation [Figure 1]. The concentration of the AIs increases proportionally with the growth of a bacterial population, and when it reaches a certain point, those molecules diffuse back into the bacteria to regulate the transcription of specified genes responsible of the formation and release of virulence factors, antibiotic production, and biofilm formation.[17] The modulation of the physiological processes controlled by AHLs induces expression of QS genes.[18] All AHLs thus far reported are composed of an acyl chain with an even number of carbon atoms ranging from 4 to 14 in length, ligated to the homoserine lactone moiety [Figure 2].[19] The components of AHL-driven QS systems are typically members of the protein families: LuxI and LuxR. LuxI generates AHLs and LuxR activates or represses the transcription of specific genes such as virulent genes.[14],[20]
Figure 1: A graphic presentation of QS molecular signaling network of Gram-positive bacteria (a) and Gram-negative bacteria (b)

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Figure 2: Chemical structures of N-acyl homoserine lactones autoinducers

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Quorum sensing pathways inhibition

Because QS is implicated in various pathologically relevant events, it is conceivable that inhibitors of bacterial QS could have therapeutically application. There are different ways for QS inhibition in each pathway. They can be summarized as follows: (1) inhibition of AIs synthesis, (2) AIs receptor antagonism, (3) inhibition of targets downstream of receptor binding, (4) sequestration of AIs using, for example, antibodies against AIs, (5) the degradation of AIs using either catalytic antibodies (abzymes) or enzymes (such as lactonases), (6) inhibition of AI secretion/transport, and (7) antibodies that “cover” and therefore block AIs receptors. Not all seven different types of inhibition have been explored in the various pathways identified.[21],[22]

Disrupting of this communication system or bacterial QS activity leads to attenuation of microbial virulence.[17],[23] Many strategies have been designed to intervene with QS systems, which will have wide application in the control of QS-dependent infections produced by bacterial.[24] This motivated research of inhibition of this process through the utilization of QS inhibitors.[25] The inactivation or degradation of QS signal molecules is known as QS inhibition or quorum quenching (QQ). This can be accomplished by several ways such as through the development of antibodies to QS signal molecules, the enzymatic demolition of QS signal molecules, or through agents which block QS.[26] These strategies interfere with this cell-to-cell communication and monitor the infectious bacteria without stopping their growth, thus averting the development of antibiotics resistance.[25],[26] The ideal QS inhibitors have been defined as chemically stable and highly effective low molecular-mass molecules, which exhibit a high degree of specificity for the QS regulator without toxic side effects on the bacteria or an eventual eukaryotic host. Therefore, the development of new, nontoxic, and broad-spectrum QQ drugs from both plants and microorganisms is of great benefit in recent years. Plants produce diverse compounds such as simple phenolics, flavonoids (FLs), alkaloids, and terpenoids.[5],[27] There is a great interest in the biological activities and therapeutic roles of these natural products in defeating QS pathogens. Since, there is a growing demand for anti-QS agents to overcome the bacterial resistance to antibiotics, it is necessary to examine and identify alternative and safe approaches for controlling pathogens. The plant kingdom has long been a source of medicines, and as such, there have been many ethnobotanically directed searches for agents that can be used to treat infections. The use of plants, plant products, and their purified components could open up the possibility of using these compounds as novel anti-QS agents. Therefore, this review presents the recent reported researches on the plants and natural products as QQ agents.


  Phytochemicals as Quorum Sensing-Inhibitors Top


In this section, an overview of the QS inhibitory activity of the compounds derived plants that have been used since ancient times as traditional medicine. Plant-derived compounds are mostly secondary metabolites, most of which are phenols or their oxygen-substituted derivatives. These secondary metabolites possess various benefits, including antimicrobial properties against pathogenic microbes.[25] Major groups of compounds that are responsible for antimicrobial activity from plants include phenolics, phenolic acids, quinones, saponins, FLs, tannins, coumarins, terpenoids, and alkaloids.[28],[29] Variations in the structure and chemical composition of these compounds result in differences in their QS inhibitory action [Figure 3].
Figure 3: Some phytochemicals as quorum sensing inhibitors

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Halogenated furanones produced by the benthic marine macroalga Delisea pulchra were the first identified anti-QS compounds. They were found to inhibit the QS-regulated behaviors by competitively bind to the LuxR type proteins. Thus, promote their rate of proteolytic degradation without killing the bacteria for their role in inhibiting biofilm formation.[25],[29] Furthermore, the plant constituents such as naringenin, oroidin, salicylic acid, ursolic acid, cinnamaldehyde, methyl eugenol, as well as extracts of garlic and edible fruits, had anti-biofilm properties toward various pathogens.[30]

Dwivedi and Singh 2016 investigated the effects of the natural compounds, embelin and piperine on the biofilm-formation property of Streptococcus mutans using the microtiter plate method. It was found that minimum biofilm inhibitory concentration of embelin was 0.0620 ± 0.03 mg/mL, whereas that of piperine was 0.0407 ± 0.03 mg/mL, which was lower than that of embelin. These compounds might exhibited their effects by inhibiting the activity of receptors and molecules involved in the QS pathway, which is required for biofilm formation.[31]

The anti-QS potential of an anacardic acids mixture (AAM) isolated from Amphipterygium adstringens as well as its hexane extract (HE) on the rhamnolipid and pyocyanin production constraint as well as decrease of elastase activity, all being QS-controlled virulence factors expressed in the pathogenic bacteria Pseudomonas aeruginosa. They induced a 91.6% and 94% inhibition of the violacein production at concentrations 55 and 166 μg/mL, respectively without affecting the viability of the bacterium. Moreover, AAM inhibited pyocyanin (86% at 200 μg/mL) and rhamnolipid (91% at 500 μg/mL) production and decrease the elastase (75% at 500 μg/mL) activity in P. aeruginosa without affecting its development.[32]

Kang et al. reported that piericidin A and glucopiericidin A isolated from Streptomyces xanthocidicus KPP01532 are potential QS inhibitors that suppress the expression of the virulence genes (pelC, pehA, celV, and nip) of Erwinia carotovora subsp. Atroseptica (a plant pathogen that causes blackleg and soft rot diseases on potato stems and tubers).[33] Malabaricone C isolated from the bark of Myristica cinnamomea inhibited violacein production by Chromobacterium violaceum CV026. Furthermore, it inhibited the QS-regulated pyocyanin production and biofilm formation in P. aeruginosa PAO1.[34]

FLs are a large class of phenylpropanoid-derived plant metabolites that are classified according to the degree of oxidation of their C-ring and whose structural diversity results from substitutions of their carbon skeleton through hydroxylation, glycosylation, methylation, acylation, and prenylation.[35],[36] Some FLs have been shown to inhibit gyrase activity, nucleic acid synthesis, type IV topoisomerase, cytoplasmic membrane functions, and energy metabolism.[37] FLs are also known for their implication in cell-to-cell communication mechanisms involved in the establishment of the symbiosis between rhizobia bacteria and their respective legume hosts.[35]

The flavone, baicalein has been shown to inhibit biofilm formation, which is QS dependent in P. aeruginosa PAO1 (at micromolar concentrations) as well as to promote the proteolysis of the Agrobacterium tumefaciens QS-signal receptor TraR in  Escherichia More Details coli cells at millimolar concentrations.[38],[39] Vikram et al. screened many of the citrus plants FLs for their ability to interfere with QS-dependent bioluminescence mechanisms and biofilm formation.[40] The results showed that naringenin reduces the induction of bioluminescence by the QS signals HAI-1 and AI-2 in Vibrio harveyi reporter strains as well as the production of biofilm by V. harveyi BB120 and E. coli 0157:H7. Moreover, the expression of three type III secretion system genes suggested to be controlled by cell-to-cell signaling, is down-regulated by naringenin.[40]

Flavanones, naringenin, eriodictyol, and taxifolin identified in the extract of Combretum albiflorum significantly reduced the production of pyocyanin and elastase in P. aeruginosa without affecting bacterial growth. Further, naringenin and taxifolin reduced the expression of several QS-controlled genes (i.e., lasI, lasR, rhlI, rhlR, lasA, lasB, phzA1, and rhlA) in P. aeruginosa PAO1.[41]

Vandeputte et al. stated that the action of naringenin most probably results from a combination of the reduction of the production of both AHL molecules (which is corroborated by the down-regulation of the expression of the lasI and rhlI genes) and of the capacity of the LuxR-type transcription factors to perceive their cognate molecules, with a consequent reduction of the expression of QS-related genes.[41] It is noteworthy that lasI and rhlI mutants deficient in AHL synthesis is indeed impaired in their capacity to express a wide range of QS genes, among which are lasB (encoding lasB elastase), rhlA (encoding the first protein involved in the production of rhamnolipids), and the phz operon involved in the production of pyocyanin.[42],[43]

Quercetin (80 μg/mL) showed a significant reduction in QS-dependent phenotypes such as violacein production, biofilm formation, exopolysaccharide (EPS) production, motility, and alginate production in a concentration-dependent manner. It can act as a competitive inhibitor for signaling compound toward lasR receptor pathway.[44] Moreover, it significantly inhibited biofilm formation and production of virulence factors, including pyocyanin, protease, and elastase at a lower concentration. Furthermore, the expression levels of lasI, lasR, rhlI, and rhlR were significantly reduced by 34%, 68%, 57%, and 50%, respectively, in response to 16 μg/mL quercetin.[45]

Moreover, catechin isolated from C. albiflorum (Tul.) Jongkind (Combretaceae) had a significant negative effect on pyocyanin and elastase productions and biofilm formation, as well as on the expression of the QS-regulated genes lasB and rhlA and of the key QS regulatory genes lasI, lasR, rhlI, and rhlR. It might interfere with the perception of the QS signal N-butanoyl-l-homoserine lactone by RhlR, leading to a reduction of the production of QS factors.[46]

Gopu and Shetty reported that the naturally occurring anthocyanin-cyanidin significantly inhibited QS-dependent phenotypes such as biofilm formation (72.43%), violacein production (73.96%), and EPS production (68.65%) in the opportunistic pathogen Klebsiella pneumoniae in a concentration-dependent manner.[47] Rosmarinic acid extracted from sweet basil bound to the QS-regulator RhlR of P. aeruginosa PAO1 and competed with the bacterial ligand N-butanoyl-homoserine lactone (C4-HSL). Furthermore, it stimulated a greater increase in RhlR-mediated transcription in vitro than that of C4-HSL. In P. aeruginosa, rosmarinic acid-induced QS-dependent gene expression and increased biofilm formation and the production of the virulence factors pyocyanin and elastase.[48] The disulphides and trisulphides metabolites which are extracted from garlic can inhibit LuxR-based QS inhibition in P. aeruginosa.[49] Naturally occurring furocoumarins from grapefruit showed strong inhibition of AI-1 and AI-2 activities based on the V. harveyi AI bioassay. In addition, they hinder the formation of biofilm in E. coli,  Salmonella More Details typhimurium, and P. aeruginosa.[50] Moreover, obacunone a grapefruit limonoid has been proven to have a strong antagonistic activity against both AHL and AI-2 systems, biofilm formation, and enterohemorrhagic E. coli virulence.[51]

The citrus limonoids, isolimonic acid, and ichangin are potent inhibitors of EHEC biofilm and adhesion to Caco-2 cells. They repressed locus of enterocyte effacement-encoded genes and flhDC. Furthermore, isolimonic acid interferes with AI-3/epinephrine activated cell-to-cell signaling pathway.[52] Moreover, isolimonic acid, deacetylnomilinic acid glucoside, and ichangin demonstrated significant inhibition of AI-mediated cell-to-cell signaling and biofilm formation. In addition, isolimonic acid and ichangin induced expression of the response regulator gene luxO.[53]

The diterpene phytol reduced the biofilm formation, twitching, and flagella motility of P. aeruginosa PAO1. It exhibited good P. aeruginosa pyocyanin inhibitory activity.[54] Carvacrol, one of the major antimicrobial components of oregano oil, inhibited the formation of biofilms of C. violaceum ATCC 12472, Salmonella enterica subsp. Typhimurium DT104, and Staphylococcus aureus 0074. Furthermore, it reduced expression of civil (a gene coding for the N-acyl-L-homoserine lactone synthase), production of violacein, and chitinase activity (both regulated by QS).[55]

The total anthocyanin of Syzygium cumini (STA) specifically inhibited the violacein production in C. violaceum, biofilm formation, and EPS production in K. pneumoniae up to 82%, 79.94%, and 64.29%, respectively. The QS inhibitory activity of S. cumini was attributed to malvidin, which reduce the violacein production, biofilm formation, and EPS production of K. pneumoniae in a concentration-dependent manner.[44]

Mohamed et al. reported that mangostanaxanthone I and α-mangostin isolated from isolated from the pericarp of Garcinia mangostana, possessed QS inhibitory activity against C. violaceum ATCC 12472 with MIC values 2 and 3 μg/mL, respectively compared to (+) - catechin (MIC 2 μg/mL).[1]


  Plant By-Products as Quorum Sensing-Inhibitors Top


Lee et al. (2011) reported that acacia and multifloral Korean honeys at low concentrations (0.5% v/v) were capable of reducing biofilm formation in an enterohemorrhagic E. coli strain due to their contents of fructose and glucose, that appeared to be the main contributors to biofilm formation inhibition.[56] Truchado et al. studied the effect of chestnut honey and its aqueous and methanolic extracts on biofilm formation by  Yersinia More Details enterocolitica, E. carotovora, and Aeromonas hydrophila.[57] Chestnut honey and its aqueous extract showed a significant QS inhibitory activity through the inhibition of AHL production and degradation of AHLs by the bacterial strains. While its methanolic extract did not possess any effect. In another study, Truchado et al. stated that the phenolic compounds, including rutin, ellagic, and chlorogenic acids were capable of reducing the concentration of ALHs on E. carotovora and Y. enterocolitica.[58] Savka et al. showed that the FL pinocembrin, which regulates immune genes in the western honey bee Apis mellifera, can disrupt AHL-dependent QS in bacteria. This referred to the potential role of the phenolic honey constituents as QS inhibitory.[59] Moreover, the study conducted by Truchado et al. on 29 unifloral honeys showed that most of them were capable of interfering with QS, especially chestnut and linden honeys had the highest anti-QS activity.[60] Whereas, orange and rosemary honeys were less effective. Further studies carried out on New Zealand manuka (Leptospermum scoparium) honey revealed that this honey can inhibit biofilm formation of clinically important pathogenic bacteria such as Proteus mirabilis,[61] S. aureus,[62] and Clostridium difficile.[63] Three nectar honeys (eucalyptus, thyme, and forest) and two honeydew honeys (fir and Metcalfa) from Italy were assessed for their anti-QS activities. All inhibited violacein production in C. violaceum in a dose dependent manner, thus demonstrating their ability to affect QS-regulated biofilm formation.[64] Chenia has studied QS inhibitory activity of four extracts of Kigelia africana fruit using the C. violaceum and A. tumefaciens biosensor systems. All extracts showed varying levels of anti-QS activity with zones of violacein inhibition ranging from 9 to 10 mm in the following order: hexane > dichloromethane > ethyl acetate > methanol. Inhibition was concentration dependent, with the ≥90% inhibition being obtained with ≥1.3 mg/mL of the HE. They also affected the LuxI and LuxR activities, indicating that the phytochemicals targeted both QS signal and receptor.[65]

The anti-QS activity of the FL fraction of Psidium guajava L. leaves was determined using a biosensor bioassay with the mutant C. violaceum CV026. In addition, its effect on QS-regulated violacein production in C. violaceum ATCC12472 and pyocyanin production, proteolytic, elastolytic activities, swarming motility, and biofilm formation in P. aeruginosa PAO1 was performed. The FL-fraction showed concentration-dependent decreases in violacein production in C. violaceum 12472 and inhibited pyocyanin production, proteolytic and elastolytic activities, swarming motility, and biofilm formation in P. aeruginosa PAO1. Interestingly, the FL-fraction did not inhibit AHL synthesis. Quercetin and quercetin-3-O-arabinoside the major FLs in FL fraction, inhibited violacein production in C. violaceum 12472, at 50 and 100 μg/mL, respectively.[66] It was also reported that the P. guajava extract guava leaf extract (GLE) significantly down-regulated 816 genes which comprises 19% of the C. violaceum MTCC 2656 genome by at least 3-fold. These genes were distributed throughout the genome and were associated with virulence, motility and other cellular processes, many of which have been described as quorum regulated in C. violaceum and other Gram-negative bacteria. Interestingly, GLE did not affect the growth of the bacteria. However, GLE-treated C. violaceum cells were restrained from causing lysis of human hepatoma cell line, HepG2, indicating a positive relationship between the QS-regulated genes and pathogenicity.[67]

The anti-QS activity of the ethyl acetate fraction (EAF) of S. cumini L. and Pimenta dioica L. was screened using C. violaceum CV026 biosensor bioassay. It is noteworthy that, all the tested plant extracts completely inhibited AHL-mediated violacein production in 0.75–1.0 mg/mL concentration in C. violaceum. However, synthesis of AHL in C. violaceum was not inhibited by the plant extracts.[68] Husain et al. reported that the oil of peppermint (Mentha piperita) at sub-minimum inhibitory concentrations (sub-MICs) strongly interfered with AHLs-regulated virulence factors and biofilm formation in P. aeruginosa and A. hydrophila due to menthol, which interferes with QS systems of various Gram-negative pathogens comprising diverse AHL molecules. It reduced the AHL-dependent production of violacein, virulence factors, and biofilm. Moreover, it significantly enhanced survival of the nematode Caenorhabditis elegans.[69]

Anti-QS-dependent therapeutic function of clove oil was evaluated against P. aeruginosa PAO1 and A. hydrophila WAF-38. Subinhibitory concentrations of the clove oil demonstrated significant reduction of las-regulated and rhl-regulated virulence factors: LasB, total protease, chitinase, and pyocyanin production, swimming motility, and EPS production. Furthermore, it reduced the biofilm forming capability of PAO1 and A. hydrophila WAF-38. Further, the PAO1-preinfected C. elegans displayed an enhanced survival when treated with 1.6% v/v of clove oil.[70]

Khan et al. reported that clove oil showed promising anti-QS activity on both C. violaceum CV12472 and CVO26 with zones of pigment inhibition 19 and 17 mm, respectively, followed by cinnamon, lavender, and peppermint oils. The sub-MICs of clove oil revealed 78.4% reduction in violacein production and up to 78% reduction in swarming motility in P. aeruginosa PAO1.[71]

Trigonella foenum-graecum L. (Fenugreek, Leguminosae) seed methanol extract exhibited significant inhibition of AHL-regulated virulence factors: protease, lasB elastase, pyocyanin production, chitinase, EPS, and swarming motility in P. aeruginosa PAO1 and PAF79. Further, it reduced the QS dependent virulence factor in the aquatic pathogen A. hydrophila WAF38. It decreased the biofilm forming abilities of PAO1, PAF79, and WAF38 and AHL levels and subsequent down-regulation of lasB gene. The major compound detected in the extract is caffeine, which reduced the production of QS regulated virulence factors and biofilm at 200 μg/mL concentration.[72]

Shukla and Bhathena (2016) reported that the extracts rich in hydrolysable tannins of Phyllanthus emblica, Terminalia bellirica, Terminalia chebula, Punica granatum, S. cumini, and Mangifera indica (flower) exhibited a broad spectrum anti-QS activity that is affecting activity of AHLs as well as AIs over a wide range of subinhibitory concentrations. All the extracts showed distinct protein binding ability and may be disrupting QS either by inactivating enzymes responsible for the synthesis of the AIs or by binding to protein receptors of QS signals.[73]

The dichloromethane extract from root barks of Cordia gilletii was found to quench the production of pyocyanin, a QS-dependent virulence factor in P. aeruginosa PAO1. Moreover, it specifically inhibits the expression of several QS-regulated genes (i.e., lasB, rhlA, lasI, lasR, rhlI, and rhlR) and reduces biofilm formation by PAO1.[74]

Six south Florida medicinal plants – Conocarpus erectus (Combretaceae), Chamaecyce hypericifolia (Euphorbiaceae), Callistemon viminalis (Myrtaceae), Bucida buceras (Combretaceae), Tetrazygia bicolor (Melastomataceae), and Quercus virginiana (Fagaceae) were assessed for their anti-QS activities against P. aeruginosa PAO1. The C. erectus, B. buceras, and C. viminalis extracts caused a significant inhibition of lasA protease, lasB elastase, pyoverdin production, and biofilm formation. In addition, each plant presented a distinct effect profile on the las and rhl QS genes and their respective signaling molecules. Furthermore, the extracts of all plants caused inhibition of QS genes and QS-controlled factors, with marginal effects on bacterial growth, suggesting that the QQ mechanisms are unrelated to static or cidal effects.[75]

QS-blocking properties of garlic have been demonstrated by Rasmussen et al., 2005 and Persson et al., reported that the crude extract of garlic specifically inhibits 92 QS-regulated gene expressions in P. aeruginosa and the amounts of mRNA of neither lasI, lasR, rhlI, nor rhlR (the key components of the las and Rhl QS communication systems in P. aeruginosa) were notably affected by the garlic treatment.[76],[77]

The essential oils (EOs) of tea tree (Melaleuca alternifolia [Maiden & Betche] Cheel) and rosemary (Rosmarinus officinalis L.) and extracts of propolis, bee pollen, and pomegranate (P. granatum L.) as well as resveratrol were evaluated for their QS inhibitory activities. All these samples showed a significant drop in violacein production even at the low-tested concentration; 0.125 μL/mL to rosemary, 0.25 to tea tree, 1 μL/mL to propolis, 5 μL/mL to pollen, 20 μg/mL to resveratrol, and 40 μg/mL to pomegranate extract. Their minimum QS inhibitory concentrations are 0.21, 0.21, 1.14, 8.67, 24.87, and 20.80 μL/mL, respectively. These results revealed that tea tree EO and rosemary EO showed the highest anti-QS activity, while resveratrol and pomegranate extract showed the lowest inhibitory activity.[78] Lamberte et al. reported that the extracts of propolis have also been proven to inhibit the production of violacein in C. violaceum, as well as the lasA and lasB protease activities in P. aeruginosa.[79]

Vattem et al. found that raspberry (Rubus idaeus), blueberry (Vaccinium angustifolium), and grape (Vitis sp.) extracts inhibited AHL activity-mediated violacein production by 60%, 42%, and 20%, respectively. Basil (Ocimum basilicum) had the highest activity and decreased the pigment formation by 78%. Thyme (Thymus sp.) and Kale (Brassica oleracea) decreased the pigment formation by 60% and were followed by rosemary (R. officinalis), ginger (Zingiber officinale), and turmeric (Curcuma longa) which decreased violacein formation by 40%. Oregano (Origanum vulgare) did not affect the pigment production in C. violaceum O26 (CVO26).[80]

Vegetables as carrot, chamomile, and water lily as well as an array of peppers have been proven to have anti-QS activity against the LuxI-gfp reporter strain.[29] Moreover, pea seedlings and root exudates are also found to inhibit pigment production, exochitinase activity, and protease activity in C. violaceum.[29]Medicago truncatula, rice, tomato, and soybean can also produce substances that mimic the activities of the AHL.[29],[81]

Plant root-associated fungi such as Phialocephala fortinii and Meliniomyces variabili and an Ascomycete isolate have been found to have the ability to degrade the AHL and have been proposed as an option for diminishing the bacterial virulence.[82]

The leaves extracts of Myoporum laetum G. Forst., Adhatoda vasica Nees, and Bauhinia purpurea L. possessed strong QS inhibitory/AHL-mediated violacein inhibition activities, while extracts of Piper longum L., T. officinale F. H. Wigg., and Lantana camara L. showed moderate QS inhibitory activities.[83] The extracts of C. erectus L.(Combretaceae), C. hypericifolia (L.) Millsp. (Euphorbiaceae), C. viminalis (Sol. ex Gaertn.) G. Don (Myrtaceae), Bucida burceras L. (Combretaceae), T. bicolor (Mill.) Cogn. (Melastomataceae), and Quercus virginiana Mill. (Fagaceae) showed QS inhibition on C. violaceum and A. tumefaciens.[84]

The EOs of Piper bredemeyeri, Piper bogotense, and Piper brachypodom showed inhibiting QS on C. violaceum CV026.[85] The ethanolic extract of Scutellaria baicalensis Georgi was found to inhibit violacein production, a QS-regulated behavior in C. violaceum CV026. In addition, it was also able to inhibit QS-regulated virulence in Pectobacterium carotovorum subsp. Carotovorum.[86]

Ethanolic and methanolic extracts of Manilkara hexandra Roxb (Sapotaceae), and methanolic extract of Pyrus pyrifolia Burm (Rosaceae) seeds enhanced QS-regulated violacein production in C. violaceum.[87]Vanilla planifolia Andrews extract significantly reduced violacein production on C. violaceum CV026 in a concentration-dependent manner.[25]

The EOs of Lippia alba showed anti-QS activity through the inhibition of the QS-controlled violacein pigment production by C. violaceum CV026.[88]

The ethyl acetate extract and butanol fraction of Nymphaea tetragona (Water Lily) significantly inhibited pigment production of C. violaceum.[89] Oregano EO (concentration 0.0156, 0.0312, 0.0625, and 0.125 mg/mL) showed a significant anti-QS activity expressed as inhibition of violacein production by C. violaceum.[90]

The extracts of the Malaysian plants; Parkia speciosa, Cosmos cardatus, Centella asiatica, Manihot esculenta leaf sprigs, Psophocarpus tetragonolobus, Polygonum minus, and Oenanthe javanica were tested for their anti-QS potentials on C. violaceum ATCC 12472. It is noteworthy that the highest anti-QS activity was recorded by P. minus and C. asiatica extracts.[91] The extract of Bellis perennis showed promising anti-QS activity on C. violaceum CV026. It inhibited QS-regulated violacein production in C. violaceum ATCC 12472 and swarming motility in P. aeruginosa PA01.[92]Salvadora persica methanol extract showed inhibition of violacein production in C. violaceum.[93]


  Conclusion Top


In the last few decades, many researches have been learned about the mechanisms used by bacteria to communicate and control virulence traits. New molecules and their effects on microbial virulence continue to be discovered. It is clear that the relation between QS and bacterial virulence represents a promising area from which new, effective anti-virulence drugs can emerge. The examples mentioned here demonstrate that inhibition of virulence through inhibition of QS is possible and somewhat practical. Utilization of these products could also be a more cost-effective way. However, further research is needed to determine their mechanism of action and the optimum levels of anti-QS agents that can be safely applied.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Mohamed GA, Ibrahim SR, Shaaban MI, Ross SA. Mangostanaxanthones I and II, new xanthones from the pericarp of Garcinia mangostana. Fitoterapia 2014;98:215-21.  Back to cited text no. 1
    
2.
Livermore DM; British Society for Antimicrobial Chemotherapy Working Party on the Urgent Need: Regenerating Antibacterial Drug Discovery and Development. Discovery research: The scientific challenge of finding new antibiotics. J Antimicrob Chemother 2011;66:1941-4.  Back to cited text no. 2
    
3.
Silver LL. Challenges of antibacterial discovery. Clin Microbiol Rev 2011;24:71-109.  Back to cited text no. 3
    
4.
Wu H, Moser C, Wang HZ, Høiby N, Song ZJ. Strategies for combating bacterial biofilm infections. Int J Oral Sci 2015;7:1-7.  Back to cited text no. 4
    
5.
Cowan MM. Plant products as antimicrobial agents. Clin Microbiol Rev 1999;12:564-82.  Back to cited text no. 5
    
6.
Bax R, Mullan N, Verhoef J. The millennium bugs – The need for and development of new antibacterials. Int J Antimicrob Agents 2000;16:51-9.  Back to cited text no. 6
    
7.
Newman DJ, Cragg GM, Snader KM. Natural products as sources of new drugs over the period 1981-2002. J Nat Prod 2003;66:1022-37.  Back to cited text no. 7
    
8.
Chong YM, Yin WF, Ho CY, Mustafa MR, Hadi AH, Awang K, et al. Malabaricone C from Mysrista cinnamomea exhibit anti-quorum sensing activity. J Nat Prod 2010;74:2261-4.  Back to cited text no. 8
    
9.
Deep A, Chaudhary U, Gupta V. Quorum sensing and bacterial pathogenicity: From molecules to disease. J Lab Physicians 2011;3:4-11.  Back to cited text no. 9
[PUBMED]  [Full text]  
10.
Kabir AH, Roy AG, Alam MF, Islam R. Detection of quorum sensing signals in gram-negative bacteria by using reporter strain CV026. Notulae Sci Biol 2010;2:72-5.  Back to cited text no. 10
    
11.
Krishnan T, Yin WF, Chan KG. Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa PAO1 by Ayurveda spice clove (Syzygium aromaticum) bud extract. Sensors (Basel) 2012;12:4016-30.  Back to cited text no. 11
    
12.
Singh BN, Singh BR, Singh RL, Prakash D, Sarma BK, Singh HB. Antioxidant and anti-quorum sensing activities of green pod of Acacia nilotica L. Food Chem Toxicol 2009;47:778-86.  Back to cited text no. 12
    
13.
Rocha-Estrada J, Aceves-Diez AE, Guarneros G, de la Torre M. The RNPP family of quorum-sensing proteins in gram-positive bacteria. Appl Microbiol Biotechnol 2010;87:913-23.  Back to cited text no. 13
    
14.
Xavier KB, Bassler BL. LuxS quorum sensing: More than just a numbers game. Curr Opin Microbiol 2003;6:191-7.  Back to cited text no. 14
    
15.
Zhang RG, Pappas KM, Brace JL, Miller PC, Oulmassov T, Molyneaux JM, et al. Structure of a bacterial quorum-sensing transcription factor completed with pheromone and DNA. Nature 2002;417:971-4.  Back to cited text no. 15
    
16.
Choudhary S, Schmidt-Dannert C. Applications of quorum sensing in biotechnology. Appl Microbiol Biotechnol 2010;86:1267-79.  Back to cited text no. 16
    
17.
Finch R, Pritchard D, Bycroft B, Williams P, Stewart G. Quorum sensing – A novel target for anti-infective therapy. J Antimicrob Chemother 1998;42:569-71.  Back to cited text no. 17
    
18.
Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. Quorum- sensing in Gram-negative bacteria. FEMS Microbiol Rev 2001;25:365-404.  Back to cited text no. 18
    
19.
Guan LL, Onuki H, Kamino K. Bacterial growth stimulation with exogenous siderophore and synthetic N-acyl homoserine lactone autoinducers under iron-limited and low-nutrient conditions. Appl Environ Microbiol 2000;66:2797-803.  Back to cited text no. 19
    
20.
Morohoshi T, Kato M, Fukamachi K, Kato N, Ikeda T. N-acylhomoserine lactone regulates violacein production in Chromobacterium violaceum type strain ATCC 12472. FEMS Microbiol Lett 2008;279:124-30.  Back to cited text no. 20
    
21.
d'Angelo-Picard C, Haudecoeur E, Chevrot R, Dessaux Y, Faure D. The plant pathogen Agrobacterium tumefaciens: A model to study the roles of lactonases in the quorum-sensing regulatory network. Biol Plant Microbe Interact 2006;5:353-6.  Back to cited text no. 21
    
22.
De Lamo Marin S, Xu Y, Meijler MM, Janda KD. Antibody catalyzed hydrolysis of a quorum sensing signal found in gram-negative bacteria. Bioorg Med Chem Lett 2007;17:1549-52.  Back to cited text no. 22
    
23.
Smith R, Iglewski B. Pseudomonas aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 2003;6:56-60.  Back to cited text no. 23
    
24.
Ditu LM, Chifiriuc MC, Bezirtzoglou E, Voltsi C, Bleotu C, Pelinescu D, et al. Modulation of virulence and antibiotic susceptibility of enteropathogenic Escherichia coli strains by Enterococcus faecium probiotic strain culture fractions. Anaerobe 2011;17:448-51.  Back to cited text no. 24
    
25.
Choo JH, Rukayadi Y, Hwang JK. Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 2006;42:637-41.  Back to cited text no. 25
    
26.
Chan KG, Atkinson S, Mathee K, Sam CK, Chhabra SR, Cámara M, et al. Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: Co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol 2011;11:51.  Back to cited text no. 26
    
27.
Dewick P. Medicinal Natural Products: A Biosynthetic Approach. 2nd ed. New York: John Wiley & Sons; 2002.  Back to cited text no. 27
    
28.
Hayek SA, Gyawali R, Ibrahim SA. Antimicrobial natural products. In: Mendez-Vilas A, editor. Microbial Pathogens and Strategies for Combating Them: Science, Technology and Education. Vol. 2. Badajoz, Spain: Formatex Research Center; 2013. p. 910-21.  Back to cited text no. 28
    
29.
Teplitski M, Robinson JB, Bauer WD. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 2000;13:637-48.  Back to cited text no. 29
    
30.
Issac Abraham SV, Palani A, Ramaswamy BR, Shunmugiah KP, Arumugam VR. Antiquorum sensing and antibiofilm potential of Capparis spinosa. Arch Med Res 2011;42:658-68.  Back to cited text no. 30
    
31.
Dwivedi D, Singh V. Effects of the natural compounds embelin and piperine on the biofilm-producing property of Streptococcus mutans. J Tradit Complement Med 2016;6:57-61.  Back to cited text no. 31
    
32.
Castillo-Juárez I, García-Contreras R, Velázquez-Guadarrama N, Soto-Hernández M, Martínez-Vázquez M. Amphypterygium adstringens anacardic acid mixture inhibits quorum sensing-controlled virulence factors of Chromobacterium violaceum and Pseudomonas aeruginosa. Arch Med Res 2013;44:488-94.  Back to cited text no. 32
    
33.
Kang JE, Han JW, Jeon BJ, Kim BS. Efficacies of quorum sensing inhibitors, piericidin A and glucopiericidin A, produced by Streptomyces xanthocidicus KPP01532 for the control of potato soft rot caused by Erwinia carotovora subsp. atroseptica. Microbiol Res 2016;184:32-41.  Back to cited text no. 33
    
34.
Chong YM, Yin WF, Ho CY, Mustafa MR, Hadi AH, Awang K, et al. Malabaricone C from Myristica cinnamomea exhibits anti-quorum sensing activity. J Nat Prod 2011;74:2261-4.  Back to cited text no. 34
    
35.
Buer CS, Imin N, Djordjevic MA. Flavonoids: New roles for old molecules. J Integr Plant Biol 2010;52:98-111.  Back to cited text no. 35
    
36.
Dixon RA, Pasinetti GM. Flavonoids and isoflavonoids: From plant biology to agriculture and neuroscience. Plant Physiol 2010;154:453-7.  Back to cited text no. 36
    
37.
Cushnie TP, Lamb AJ. Antimicrobial activity of flavonoids. Int J Antimicrob Agents 2005;26:343-56.  Back to cited text no. 37
    
38.
Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP, et al. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998;280:295-8.  Back to cited text no. 38
    
39.
Zeng Z, Qian L, Cao L, Tan H, Huang Y, Xue X, et al. Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 2008;79:119-26.  Back to cited text no. 39
    
40.
Vikram A, Jayaprakasha GK, Jesudhasan PR, Pillai SD, Patil BS. Suppression of bacterial cell-cell signalling, biofilm formation and type III secretion system by citrus flavonoids. J Appl Microbiol 2010;109:515-27.  Back to cited text no. 40
    
41.
Vandeputte OM, Kiendrebeogo M, Rasamiravaka T, Stévigny C, Duez P, Rajaonson S, et al. The flavanone naringenin reduces the production of quorum sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Microbiology 2011;157:2120-32.  Back to cited text no. 41
    
42.
Wagner VE, Gillis RJ, Iglewski B. Transcriptome analysis of quorum-sensing regulation and virulence factor expression in Pseudomonas aeruginosa. Vaccine 2004;22 Suppl 1:S15-20.  Back to cited text no. 42
    
43.
Schuster M, Lostroh CP, Ogi T, Greenberg EP. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: A transcriptome analysis. J Bacteriol 2003;185:2066-79.  Back to cited text no. 43
    
44.
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.  Back to cited text no. 44
    
45.
Ouyang J, Sun F, Feng W, Sun Y, Qiu X, Xiong L, et al. Quercetin is an effective inhibitor of quorum sensing, biofilm formation and virulence factors in Pseudomonas aeruginosa. J Appl Microbiol 2016;120:966-74.  Back to cited text no. 45
    
46.
Vandeputte OM, Kiendrebeogo M, Rajaonson S, Diallo B, Mol A, El Jaziri M, et al. Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 2010;76:243-53.  Back to cited text no. 46
    
47.
Gopu V, Shetty PH. Cyanidin inhibits quorum signalling pathway of a food borne opportunistic pathogen. J Food Sci Technol 2016;53:968-76.  Back to cited text no. 47
    
48.
Corral-Lugo A, Daddaoua A, Ortega A, Espinosa-Urgel M, Krell T. Rosmarinic acid is a homoserine lactone mimic produced by plants that activates a bacterial quorum-sensing regulator. Sci Signal 2016;9:ra1.  Back to cited text no. 48
    
49.
Rasmussen TB, Skindersoe ME, Bjarnsholt T, Phipps RK, Christensen KB, Jensen PO, et al. Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 2005;151:1325-40.  Back to cited text no. 49
    
50.
Girennavar B, Cepeda ML, Soni KA, Vikram A, Jesudhasan P, Jayaprakasha GK, et al. Grapefruit juice and its furocoumarins inhibits autoinducer signaling and biofilm formation in bacteria. Int J Food Microbiol 2008;125:204-8.  Back to cited text no. 50
    
51.
Vikram A, Jesudhasan PR, Jayaprakasha GK, Pillai BS, Patil BS. Grapefruit bioactive limonoids modulate E. coli O157:H7 TTSS and biofilm. Int J Food Microbiol 2010;140:109-16.  Back to cited text no. 51
    
52.
Vikram A, Jesudhasan PR, Pillai SD, Patil BS. Isolimonic acid interferes with Escherichia coli O157:H7 biofilm and TTSS in QseBC and QseA dependent fashion. BMC Microbiol 2012;12:261.  Back to cited text no. 52
    
53.
Vikram A, Jesudhasan PR, Jayaprakasha GK, Pillai SD, Patil BS. Citrus limonoids interfere with Vibrio harveyi cell-cell signalling and biofilm formation by modulating the response regulator LuxO. Microbiology 2011;157:99-110.  Back to cited text no. 53
    
54.
Pejin B, Ciric A, Glamoclija J, Nikolic M, Sokovic M.In vitro anti-quorum sensing activity of phytol. Nat Prod Res 2015;29:374-7.  Back to cited text no. 54
    
55.
Burt SA, Ojo-Fakunle VT, Woertman J, Veldhuizen EJ. The natural antimicrobial carvacrol inhibits quorum sensing in Chromobacterium violaceum and reduces bacterial biofilm formation at sub-lethal concentrations. PLoS One 2014;9:e93414.  Back to cited text no. 55
    
56.
Lee JH, Park JH, Kim JA, Neupane GP, Cho MH, Lee CS, et al. Low concentrations of honey reduce biofilm formation, quorum sensing and virulence in Escherichia coli O157: H7. Biofouling 2011;27:1095-1104.  Back to cited text no. 56
    
57.
Truchado P, Lopez-Galvevez F, Gil MI, Tomas-Barberan FA, Allende A. Quorum sensing inhibitory and antimicrobial activities of honeys and the relationship with individual phenolics. Food Chem 2009;115:1337-44.  Back to cited text no. 57
    
58.
Truchado P, Tomás-Barberán FA, Larrosa M, Allende A. Food phytochemicals act as quorum sensing inhibitors reducing production and/or degrading autoinducers of Yersinia enterocolitica and Erwinia carotovora. Food Control 2012;24:78-85.  Back to cited text no. 58
    
59.
Savka MA, Dailey L, Popova M, Mihaylova R, Merritt B. Chemical composition and disruption of quorum sensing signaling in geographically diverse United States propolis. J Evid Based Complementary Altern Med 2015;2015:472593-603.  Back to cited text no. 59
    
60.
Truchado P, Gil A, Tomás-Barberán FA, Allende A. Inhibition by chestnut honey of Nacyl-l-homoserine lactones and biofilm formation in Erwinia carotovora, Yersinia enterocolitica and Aeromonas hydrophila. J Agric Food Chem 2009;57:11186-93.  Back to cited text no. 60
    
61.
Majtan J, Bohova J, Horniackova M, Klaudiny J, Majtan V. Anti-biofilm effects of honey against wound pathogens Proteus mirabilis and Enterobacter cloacae. Phytother Res 2014;28:69-75.  Back to cited text no. 61
    
62.
Lu J, Turnbull L, Burke CM, Liu M, Carter DA, Schlothauer RC, et al. Manuka-type honeys can eradicate biofilms produced by Staphylococcus aureus strains with different biofilm-forming abilities. PeerJ 2014;2:e326.  Back to cited text no. 62
    
63.
Hammond EN, Donkor ES, Brown CA. Biofilm formation of Clostridium difficile and susceptibility to Manuka honey. BMC Complement Altern Med 2014;14:329.  Back to cited text no. 63
    
64.
Fidaleo M, Lavecchia R, Zuorro A. Antibacterial and anti-quorum sensing activities of selected Italian honeys against antibiotic-resistant pathogens. Online J Biol Sci 2015;15:236-43.  Back to cited text no. 64
    
65.
Chenia HY. Anti-quorum sensing potential of crude Kigelia africana fruit extracts. Sensors (Basel) 2013;13:2802-17.  Back to cited text no. 65
    
66.
Vasavi HS, Arun AB, Rekha PD. Anti-quorum sensing activity of Psidium guajava L. flavonoids against Chromobacterium violaceum and Pseudomonas aeruginosa PAO1. Microbiol Immunol 2014;58:286-93.  Back to cited text no. 66
    
67.
Ghosh R, Tiwary BK, Kumar A, Chakraborty R. Guava leaf extract inhibits quorum-sensing and Chromobacterium violaceum induced lysis of human hepatoma cells: Whole transcriptome analysis reveals differential gene expression. PLoS One 2014;9:e107703.  Back to cited text no. 67
    
68.
Vasavi HS, Arun AB, Rekha PD. Inhibition of quorum sensing in Chromobacterium violaceum by Syzygium cumini L. and Pimenta dioica L. Asian Pac J Trop Biomed 2013;3:954-9.  Back to cited text no. 68
    
69.
Husain FM, Ahmad I, Khan MS, Ahmad E, Tahseen Q, Khan MS, et al. Sub-MICs of Mentha piperita essential oil and menthol inhibits AHL mediated quorum sensing and biofilm of gram-negative bacteria. Front Microbiol 2015;6:420.  Back to cited text no. 69
    
70.
Husain FM, Ahmad I, Asif M, Tahseen Q. Influence of clove oil on certain quorum-sensing-regulated functions and biofilm of Pseudomonas aeruginosa and Aeromonas hydrophila. J Biosci 2013;38:835-44.  Back to cited text no. 70
    
71.
Khan MS, Zahin M, Hasan S, Husain FM, Ahmad I. Inhibition of quorum sensing regulated bacterial functions by plant essential oils with special reference to clove oil. Lett Appl Microbiol 2009;49:354-60.  Back to cited text no. 71
    
72.
Husain FM, Ahmad I, Khan MS, Al-Shabib NA. Trigonella foenum-graceum (Seed) extract interferes with quorum sensing regulated traits and biofilm formation in the strains of Pseudomonas aeruginosa and Aeromonas hydrophila. Evid Based Complement Alternat Med 2015;2015:879540.  Back to cited text no. 72
    
73.
Shukla V, Bhathena Z. Broad spectrum anti-quorum sensing activity of tannin-rich crude extracts of Indian medicinal plants. Scientifica (Cairo) 2016;2016:5823013.  Back to cited text no. 73
    
74.
Okusa PN, Rasamiravaka T, Vandeputte O, Stévigny C, Jaziri ME, Duez P. Extracts of Cordia gilletii de wild (Boraginaceae) quench the quorum sensing of Pseudomonas aeruginosa PAO1. J Intercult Ethnopharmacol 2014;3:138-43.  Back to cited text no. 74
    
75.
Adonizio A, Kong KF, Mathee K. Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob Agents Chemother 2008;52:198-203.  Back to cited text no. 75
    
76.
Persson T, Hansen TH, Rasmussen TB, Skindersø ME, Givskov M, Nielsen J, et al. Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org Biomol Chem 2005;3:253-62.  Back to cited text no. 76
    
77.
Rasmussen TB, Bjarnsholt T, Skindersoe ME, Hentzer M, Kristoffersen P, Köte M, et al. Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 2005;187:1799-814.  Back to cited text no. 77
    
78.
Alvarez MV, Moreira MR, Ponce A. Antiquorum sensing and antimicrobial activity of natural agents with potential use in food. J Food Safety 2012;32:379387.  Back to cited text no. 78
    
79.
Lamberte LE, Cabrera EC, Rivera WL. Activity of the ethanolic extract of propolis (EEP) as a potential inhibitor of quorum sensing-mediated pigment production in Chromobacterium violaceum and virulence factor production in Pseudomonas aeruginosa. Philipp Agric Sci 2011;94:4-22.  Back to cited text no. 79
    
80.
Vattem DA, Mihalik K, Crixell SH, McLean RJ. Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 2007;78:302-10.  Back to cited text no. 80
    
81.
Daniels R, De Vos DE, Desair J, Raedschelders G, Luyten E, Rosemeyer V, et al. The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J Biol Chem 2002;277:462-8.  Back to cited text no. 81
    
82.
Uroz S, Heinonsalo J. Degradation of N-acyl homoserine lactone quorum sensing signal molecules by forest root-associated fungi. FEMS Microbiol Ecol 2008;65:271-8.  Back to cited text no. 82
    
83.
Zaki AA, Shaaban MI, Hashish NE, Amer MA, Lahloub MF. Assessment of anti-quorum sensing activity for some ornamental and medicinal plants native to Egypt. Sci Pharm 2013;81:251-8.  Back to cited text no. 83
    
84.
Adonizio AL, Downum K, Bennett BC, Mathee K. Anti-quorum sensing activity of medicinal plants in Southern Florida. J Ethnopharmacol 2006;105:427-35.  Back to cited text no. 84
    
85.
Olivero JT, Pájaro NP, Stashenko E. Antiquorum sensing activity of essential oils isolated from different species of the genus Piper. Vitae 2011;18:77-82.  Back to cited text no. 85
    
86.
Song C, Ma H, Zhao Q, Song S, Jia Z. Inhibition of quorum sensing activity by ethanol extract of Scutellaria baicalensis Georgi. J Plant Pathol Microbiol 2012;S7:1-4.  Back to cited text no. 86
    
87.
Chaudhari V, Gosai H, Raval S, Kothari V. Effect of certain natural products and organic solvents on quorum sensing in Chromobacterium violaceum. Asian Pac J Trop Med 2014;7S1:S204-11.  Back to cited text no. 87
    
88.
Olivero-Verbel J, Barreto-Maya A, Bertel-Sevilla A, Stashenko EE. Composition, anti-quorum sensing and antimicrobial activity of essential oils from Lippia alba. Braz J Microbiol 2014;45:759-67.  Back to cited text no. 88
    
89.
Hossain MA, Park JY, Kim JY, Suh JW, Park SC. Synergistic effect and antiquorum sensing activity of Nymphaea tetragona (water lily) extract. Biomed Res Int 2014;2014:562173.  Back to cited text no. 89
    
90.
Alvarez MV, Ortega-Ramirez LA, Gutierrez-Pacheco MM, Bernal-Mercado AT, Rodriguez-Garcia I, Gonzalez-Aguilar GA, et al. Oregano essential oil-pectin edible films as anti-quorum sensing and food antimicrobial agents. Front Microbiol 2014;5:699.  Back to cited text no. 90
    
91.
Abdul Wahab NA, Zain MS, Kader J, Radzi SM, Noor HM. Study on anti-quorum sensing potential of selected local ulam in Malaysia. World J Pharm Pharm Sci 2014;3:203-11.  Back to cited text no. 91
    
92.
Ceylan O, Ugur A, Sarac N.In vitro antimicrobial, antioxidant, antibiofilm and quorum sensing inhibitory activities of Bellis perennis L. J BioSci Biotech 2014;35-42.  Back to cited text no. 92
    
93.
Rezaei A, Ghahroudi AA, Khorsand A, Yaghoobee S, Shayesteh YS, Rokn AR, et al. Methanol extracts of Salvadora persica control periodontitis by quench of quorum sensing. Rom J Biochem 2014;51:43-55.  Back to cited text no. 93
    


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