Antioxidant and Anti-quorum Sensing Potential of Acer monspessulanum subsp. monspessulanum Extracts

• Introduction
• Results and Discussion
• Materials and Methods
• Bacterial strains and chemicals
• Plant material
• Obtaining the crude extracts
• Antioxidant activity
• Free radical scavenging activity (DPPH assay)
• Total antioxidant activity by the β-carotene-linoleic acid method
• Determination of total phenolic content
• Quantification of phenolic compounds by RP-HPLC
• Antibacterial activity assay
• Bioassay for QSI activity using CV026
• Violacein inhibition assay
• Anti-swarming in PA01
• Statistical analysis
• Supporting information
• Acknowledgements
• References

Abstract

In this study, anti-quorum sensing, and antioxidant activities, and chemical composition of Acer monspessulanum subsp. monspessulanum extracts were evaluated. Determination of the antioxidant activity was revealed by DPPH radical scavenging activity, the total phenolic content assay, and the β-carotene/linoleic acid assay. The detection of phenolic compounds was determined using RP-HPLC. Anti-quorum sensing activity and violacein inhibition activity were determined using Chromobacterium violaceum CV026 and C. violaceum ATCC 112 472, respectively. The determination of anti-swarming activity was carried out with Pseudomonas aeruginosa PA01. In DPPH and total phenolic content assays, the water extract exhibited good antioxidant activity. In the β-carotene-linoleic acid assay, ethyl acetate and ethanol extracts exhibited good lipid peroxidation inhibition activity, demonstrating 96.95 ± 0.03 % and 95.35 ± 0.00 % at 2.5 mg/mL concentrations, respectively. The predominant phenolic compounds of the extracts were determined as rutin, naringin, catechin hydrate, quercetin, and protocatechuic acid. Ethyl acetate and ethanol extracts were found to contain a high level of violacein inhibition and anti-quorum sensing activity. The ethanol extract also showed weak anti-swarming activity. In this first study that used Acer monspessulanum subsp. monspessulanum extracts, it was revealed that the water extract has antioxidant activity and the ethanol and ethyl acetate extracts have anti-quorum sensing activity depending on the phenolic compounds that it contained.

Introduction

The misuse of antibiotics has contributed to the widespread development of antimicrobial resistance among clinically significant bacterial species [1]. Based on this argument, researchers are increasingly investigating herbal products in the quest for new therapeutic and antipathogenic agents that might act as nontoxic inhibitors of quorum sensing (QS), thus controlling infections without encouraging the appearance of resistant bacterial strains [2]. Generally, large numbers of pathogens are needed to overwhelm host defenses to cause disease, as a single individual pathogen is more easily destroyed. Many bacteria release a low-molecular weight metabolic intermediate as a signal for cooperation in activities such as colony formation and movement [3]. The ability of bacteria to sense and respond to their population density is termed as “cell-to-cell communication” or “quorum sensing” and is mediated by autoinducer molecules [4]. At a threshold population density, N-acyl homoserine lactones (AHLs) signal molecules to interact with cellular receptors and trigger the expression of a set of target genes, including virulence, antibiotic production, biofilm formation, bioluminescense, mobility, and swarming [5].

Also, many factors (UV exposition, ozone, ionizing radiation herbicides, pesticides, pollution, smoking, alcohol, and chemicals) besides the pathogen-derived diseases induce oxidative stress resulting in an overproduction of free radicals. The oxidative stress is associated with lipid and protein peroxidation, resulting in rapid cell structural damage, tissue injury, or gene mutation and ultimately leads to the development of various health disorders, such as Alzheimersʼs disease, cancer, atherosclerosis, diabetes mellitus, hypertension, and ageing [6], [7]. Therefore, antioxidants have widespread applications in medicine and the cosmetics and food industries. Antioxidants from natural sources gain more acceptance due to emerging concerns about safety of synthetic preservatives. Although natural products have been the source of many modern pharmaceuticals, there is now renewed interest in traditional medicine to provide new compounds with potent bioactivities, including much interest in antioxidant activity [8].

The Acer genus, belonging to the Aceraceae family, has 100 species and many subspecies. There are 9 maple species and 19 maple taxons native to Turkey [9]. One of these, Acer monspessulanum L. subsp. monspessulanum, is also known as Montpellier Maple. Because it is used in the production of spoons, this plant is also called “simsir, aksimsir”. Montpellier Maple is native to the mediterrenean region, south of Anatolia, northwest and south of Iran, north of Iraq, Syria, and Lebanon [10].

The red maple species (Acer rubrum L.) are native to eastern North America and have been used for medicinal purposes by the Native Americans [11]. Maplexins isolated from red maple stems have been reported as a new α-glucosidase inhibitor [12]. In Korea, the leaves and stem of Acer tegmentosum Maxim. have been traditionally used for the treatment of hepatic disorders such as hepatitis, hepatic cancer, hepatic cirrhosis, and liver detoxification [13]. Acer oblongifolium Dippel has shown antitumor, cytotoxic, and phytotoxic potential [14]. In addition, previously, antioxidant activities and various phenolic compounds for a number of Acer species have been reported [12], [15], [16], [17], [18], [19], [20], [21], [22]. Their major antioxidant constituents have been identified as gallic acid, (+)-catechin, (−)-epicatechin, avicularin, feniculin, 6′-O-galloyl salidroside, (+)-rhododendrol, and vitexin.

In this screening study, A. monspessulanum subsp. monspessulanumum was selected for further evaluation of its antioxidant and anti-quorum sensing activities. As no previous study describes the antioxidant and anti-quorum sensing potential of the selected plant, the current study will provide useful information in this regard.

Results and Discussion

In the DPPH assay, the water extract demonstrated good DPPH scavenging activity (IC₅₀ = 4.99 ± 0.01 mg/mL), while the ethyl acetate extract exhibited weak activity (IC₅₀ = 47.11 ± 1.15 mg/mL). However, the ethanol extract showed better antioxidant activity (IC₅₀ = 12.01 ± 0.38 mg/mL). The water extract had the highest content of phenolic compounds (358.00 ± 9.09 mg GAE/g) as well as the best antioxidant activity in the DPPH assay. A good correlation was observed between the results of DPPH radical scavenging and total phenolic content. Accordingly, the ethyl acetate extract containing 103.49 ± 4.90 mg GAE/g phenolic content was found to have the lowest DPPH scavenging activity ([Table 1]).

Royer et al. [21] have studied the ethanol and water extracts of A. rubrum (Red maple) tissues to determine their phenolic compounds and radical scavenging capacity. They reported that red maple stem bark extracts constitute potential sources of new antioxidant agents rich in polyphenols. Wan et al. [12] reported that 13 gallic acid derivatives (including five new gallotannins named maplexins A–E) were isolated from A. rubrum (Red maple) root extracts. Amongst these compounds, maplexin E was reported to carry a high level of α-glucosidase and antioxidant activity.

In the β-carotene-linoleic acid assay, the ethyl acetate extract exhibited 96.95 ± 0.025 % inhibition against lipid peroxidation at 2.5 mg/mL, while the ethanol extract exhibited 95.35 ± 0.001 % at the same concentration, less than α-tocopherol ([Table 2]).

Rutin, catechin hydrate, quercetin, naringin, luteolin, and chlorogenic acid in the ethyl acetate extracts and rutin, catechin hydrate, quercetin, naringin, luteolin, gallic acid, chlorogenic acid, and caffeic acid in the ethanol extracts have been identified as major components. Rutin, protocatechuic acid, naringin, caffeic acid, and quercetin have been identified as major components in the water extract ([Table 3]). In the study conducted by Lee at al. [22], the existence of feniculin, aviculate, (+)-catechin, (−)-epicatechin, and 6′-O-galloyl salidroside phenolic compounds in the A. tegmentosum ethyl acetate extracts was revealed. Also, (+)-catechin, pyrogallol, gallic acid [23], and a significant amount of anthocyanidins [24] have been reported in A. rubrum wood and bark extracts.

Bacterial intracellular communication or QS regulates the pathogenesis of many medically important organisms. The QS blockers are known to exist in marine algae, various species seaweed, and higher plants [5], [25], [26], [27], [28], [29]. Unfortunately, most of these QS blockers are unsuitable for human use due to their toxicity and narrow efficacy for treatment of bacterial infections in vivo.

In this study, ethyl acetate and ethanol extracts of A. monspessulanum subsp. monspessulanum revealed a strong QSI potential by inhibiting violacein pigment production in Chromobacterium violaceum ATCC 12 472 ([Table 4] and Fig. 1 S, Supporting Information). Moreover, these plant extracts have not shown any antibacterial activity in this study, even at their higher concentrations. The extracts of A. monspessulanum subsp. monspessulanum used in this study were found to be ineffective on bacterial growth of biomonitor strains. Therefore, it is expected that the QSI concentrations used in this study could exert a selective pressure for the development of bacterial resistance.

A. monspessulanum subsp. monspessulanum extracts showed no antibacterial activity at 20–100 mg/mL concentrations according to the disk diffusion assay. These results indicate that A. monspessulanum subsp. monspessulanum extracts have no effect on the growth of tested biomonitor strains at these concentrations. Therefore, determination of anti-QS activity assays were carried out below 100 mg/mL extract concentrations. This is important as quorum sensing inhibition focuses on the interference of bacterial signalling and not on antimicrobial activity. In this study, the antibacterial activity results show that the contents of A. monspessulanum subsp. monspessulanum extracts have a limited antibacterial effect, but it can prevent the quorum sensing signals. Similar antibacterial activity results were reported by Adonizio et al. [25], Musthafa et al. [30], and Khan et al. [31].

Violacein production was inhibited by extracts of A. monspessulanum subsp. monspessulanum in a concentration-dependent manner. Ethyl acetate and ethanol extracts of the plant showed 100 % violacein inhibition at the 30 mg/mL concentration. Violacein inhibition of ethyl acetate and ethanol extracts at the 20 mg/mL concentration was determined as 51.12 % and 54.92 %, respectively. In the water extracts, only 18.3 % violacein inhibition took place in a 50 mg/mL concentration and there was no such inhibition in concentrations under 30 mg/mL ([Table 4] and Fig. 1 S, Supporting Information). Swarming motility inhibition against Pseudomonas aeruginosa PA01 has only been detected in the ethanol extract with 14.29 % and this effect was not observed in other extracts ([Fig. 1] and Table 1 S, Supporting Information).

In this study, we investigated the screening of A. monspessulanum subsp. monspessulanum extracts for their anti-QS activity. Loss of purple pigmentation in C. violaceum CV026 in the vicinity of the plant extracts indicated QS inhibition ([Fig. 2] and Table 2 S, Supporting Information). Ethyl acetate and ethanol extracts were found to have potent anti-QS activity. The highest anti-QS activity was detected at 100 mg/mL ethanol extract with a 19.50 ± 0.50 mm inhibition zone. The same concentration of ethyl acetate extract showed anti-QS activity with a 19.00 ± 1.00 mm diameter zone.

Among the identified phenolics in A. monspessulanum subsp. monspessulanum extracts, rutin was determined at the highest concentrations. But, when it is compared to the other two extracts, the absence of catechin, chlorogenic acid, and luteolin in the water extract suggests that these three compounds may be effective for anti-quorum sensing activity. In summary, A. monspessulanum extracts may have potential and serve as an important plant in antioxidant activity and inhibiting quorum sensing of bacteria.

Materials and Methods

Bacterial strains and chemicals

C. violaceum CV 12 472, CV026 and P. aeruginosa PA01 were purchased from Spanish Type Culture Collection (CECT). 1,1-Diphenyl-2-picryl hydrazyl (DPPH, ≥ 99 %), α-tocopherol (≥ 9.5 %), L-ascorbic acid (≥ 99 %), β-carotene (≥ 97 %), linoleic acid (≥ 99 %), kanamycin sulfate (≥ 99 %), N-hexanoyl-DL-homoserine lactone (C₆HSL, ≥ 97 %), N-decanoyl-DL-homoserine lactone (C₁₀HSL, ≥ 97 %), and ethyl acetate (≥ 99.7 %) were purchased from Sigma-Aldrich. Gallic acid, protocatechuic acid, (+)-catechin, p-hydroxy benzoic acid, chlorogenic acid, caffeic acid, (−)-epicatechin, syringic acid, vanillin, p-coumaric acid, ferulic acid, sinapic acid, benzoic acid, o-coumaric acid, rutin, naringin, hesperidin, rosmarinic acid, eriodictyol, cinnamic acid, quercetin, luteolin, kaempferol, and apigenin (purity of standards ≥ 99 %) were purchased from Sigma-Aldrich. All media used in the study and other chemicals were purchased from Merck. All antibiotic discs were purchased from Oxoid.

Plant material

The leaves of A. monspessulanum subsp. monspessulanum were collected in June-July 2013. A voucher specimen identified by Mehtap Dönmez Sahin, Assoc. Prof. Dr. of Botany in the Education Faculty of Usak University, has been deposited in the Herbarium of the Faculty of Education, University of Usak under acquisition number 1110.

Obtaining the crude extracts

The air-dried and powdered leaves of A. monspessulanum subsp. monspessulanum were extracted successively with ethyl acetate, ethanol, and water in a soxhlet apparatus until the last portion of the extract became colorless. Ethyl acetate and ethanol extracts were removed under low vacuum by using rotary evaporation. The aqueous extract was lyophilized using a freeze-dryer (Christ alpha 1–4 LSC). Crude extracts were maintained at 4 °C until usage.

Antioxidant activity

Free radical scavenging activity (DPPH assay)

The free radical scavenging activity was performed using the stable DPPH assay [32], [33]. Fifty µL of various extract concentrations (1.25, 2.5, 5, 25, and 50 mg/mL in ethanol) were added to 5 mL DPPH solution (0.004 %) in ethanol. After incubation at room temperature for 30 min, the absorbance of each solution was determined at 517 nm. Percentage of inhibition and the concentration of sample required for 50 % scavenging of the DPPH free radical (IC₅₀) were determined. α-Tocopherol and ascorbic acid were used as positive controls.

Total antioxidant activity by the β-carotene-linoleic acid method

The total antioxidant activity of the extracts were evaluated using the β-carotene-linoleic acid model [34]. 0.5 mg of the β-carotene in 1 mL of chloroform, 25 µL of linoleic acid, and 200 mg of Tween-40 (polyoxyethylene sorbitan monopalmitate) were mixed together. The chloroform was completely evaporated by using a vacuum evaporator and the resulting solution was diluted with 100 mL of oxygenated water. 1.6 mL aliquots of this mixture were transferred into different tubes containing 0.4 mL of samples at 0.5, 1, and 2.5 mg/mL concentrations in ethanol. The same procedure was repeated with the positive control α-tocopherol and a blank. The emulsion system was incubated for up to 2 h at 50 °C. Absorbance was measured until the color of β-carotene disappeared in the control. After this incubation period, absorbance of the mixtures was measured at 490 nm. All determinations were performed in triplicate. The bleaching rate (R) of β-carotene was calculated using the following formula:

R = ln (a/b)/t

where, ln = natural log, a = absorbance at time 0, b = absorbance at time t (120 min).

The antioxidant activity (AA) was calculated in terms of percent of inhibition relative to the control using the formula

AA = [(R_Control − R_Sample)/R_Control] × 100

Determination of total phenolic content

Folin-Ciocalteu reagent was used for determination of total phenolic content as described earlier [35], [36]. Two hundred microliters of extract solution containing 0.1 mg of extract were added to a test tube. Then, 100 µL Folin-Ciocalteu reagent were added and the tube was shaken vigorously. After 3 min, a 2-mL solution of Na₂CO₃ (0.5 %) was added and the mixture was allowed to stand for 2 h with intermittent shaking. Absorbance was measured at 760 nm. Data are expressed in terms of mg gallic acid equivalents (GAE)/g of extract using the following linear equation based on the calibration curve:

A = 0.0143 C, R² = 0.9713

where A is the absorbance and C gallic acid equivalents.

Quantification of phenolic compounds by RP-HPLC

Phenolic compounds were evaluated by RP-HPLC (Shimadzu Scientific Instruments). Detection quantification was carried out with an LC-10ADvp pump, a diode array detector, a CTO 10Avp column heater, SCL-10Avp system controller, DGU-14 A degasser, and SIL-10ADvp autosampler (Shimadzu Scientific Instruments). Separations were conducted at 30 °C on an Agilent® Eclipse XDB C-18 reversed-phase column (250 mm×4.6 mm length, 5 µm particle size). The eluates were detected at 278 nm. The mobile phases were A: 3.0 % acetic acid in distilled water and B: methanol. For analysis, the samples were dissolved in ethanol: bidistilled water (1 : 1, v/v), and 20 µl of this solution was injected into the column. The elution gradient applied at a flow rate of 0.8 mL · min⁻¹ was: 93 % A/7 % B for 0.1 min, 72 % A/28 % B in 20 min, 75 % A/25 % B in 8 min, 70 % A/30 % B in 7 min and same gradient for 15 min, 67 % A/33 % B in 10 min, 58 % A/42 % B in 2 min, 50 % A/50 % B in 8 min, 30 % A/70 % B in 3 min, 20 % A/80 % B in 2 min 100 % B in 5 min until the end of the run. This method has good repeatability, since several analyses carried out on the same sample produced a repeatability coefficient of percent variation (CV%) of 7 %. Phenolic compositions of the extracts were determined by a modified method of Caponio et al. [37]. Gallic acid, protocatechuic acid, (+)-catechin, p-hydroxy benzoic acid, chlorogenic acid, caffeic acid, (−)-epicatechin, syringic acid, vanillin, p-coumaric acid, ferulic acid, sinapic acid, benzoic acid, o-coumaric acid, rutin, naringin, hesperidin, rosmarinic acid, eriodictyol, cinnamic acid, quercetin, luteolin, kaempferol, and apigenin were used as standards. Identification and quantitative analysis were done by comparison with the standards. The amount of each phenolic compound is expressed as mg per gram of the extract.

Antibacterial activity assay

The antibacterial potential of A. monspessulanum subsp. monspessulanum extracts was performed through a disk diffusion method in Mueller-Hinton agar (MHA) by following the method specified by the CLSI [38]. Twenty µL of A. monspessulanum subsp. monspessulanum extracts in various concentrations (20–100 mg/mL) were loaded onto sterile filter paper discs (6 mm diameter), air-dried in the laminar flow hood on sterile petri plates, and placed onto MHA plates seeded with overnight cultures of CV026, CV12472, and PA01, along with six standard antibiotics discs (diameter 6 mm). They were gentamicine (CN10), ampicillin (AM10), chloramphenicol (C30), tetracycline (T30), penicillin (P10), and streptomycin (S10). The plates were incubated at 30 °C (or 37 °C for PA01) and the zone of growth inhibition was observed after 24 h.

Bioassay for QSI activity using CV026

The quorum sensing inhibition potential of A. monspessulanum subsp. monspessulanum extracts was performed by following the method specified by Koh and Tham [1]. Five milliliters of warm molten Soft Top Agar (1.3 g agar, 2.0 g tryptone, 1.0 g sodium chloride, 200 mL deionized water) were seeded with 100 µL of an overnight CV026 culture and 10 µL kanamycin, and 20 µL of 100 µg/mL C₆HSL were added as an exogenous acyl-homoserine lactone (AHL) source. This was gently mixed and poured immediately over the surface of a solidified LB agar plate as an overlay. Wells of 5 mm in diameter were made on each plate after the overlay had solidified. Each well was filled with 50 µL of filter-sterilized A. monspessulanum subsp. monspessulanum extract. The positive control well was filled with 5 µL of 100 µg/mL C₁₀HSL (N-decanoyl-L-homoserine lactone) and 45 µL of sterile LB broth. A white or cream colored halo around this well against a purple lawn of activated CV026 bacteria was an indication of QSI. A clear halo indicated antimicrobial (AM) activity. The limit of detection of activity was also determined by applying serial dilutions of the extracts (100, 80, 60, 40, 20 mg/mL, using LB broth as the diluent). Each experiment was repeated and the assay plates were incubated at 30 °C for 3 days.

Violacein inhibition assay

A. monspessulanum subsp. monspessulanum extracts were subjected to qualitative analysis to find their QSI potentials against C. violaceum ATCC 12 472 [39]. Overnight culture (10 µL) of C. violaceum (adjusted to 0.4 OD at 600 nm) was added into sterile microtiter plates containing 200 µL of LB broth and incubated in the presence and absence of various concentrations of A. monspessulanum subsp. monspessulanum extracts (5–50 mg/mL). LB broth containing C. violaceum ATCC 12 472 was used as a positive control. These plates were incubated at 30 °C for 24 h and observed for the reduction in violacein pigment production. The absorbance was read at 585 nm. The percentage of violacein inhibition was calculated by following the formula:

Each experiment was performed in triplicate.

Anti-swarming in PA01

The anti-swarming potential of A. monspessulanum subsp. monspessulanum extracts was performed by following the method specified by Yeo and Tham [40]. Fifty microliters of sterile A. monspessulanum subsp. monspessulanum extracts were mixed into 5 mL of molten Soft Top Agar and poured immediately over the surface of a solidified LBA plate as an overlay. The plate was point inoculated with an overnight culture of PA01 once the overlaid agar had solidified and incubated at 37 °C for 3 days. The extent of swarming was determined by measuring the area of the colony in square millimeters using graph paper.

Statistical analysis

All of the experimental results are presented as mean values. The data was entered into a Microsoft Excel database and analyzed using SPSS. The IC₅₀ values were obtained by linear regression analysis. Statistical analysis of the total antioxidant activity was performed using the Kruskal-Wallis test.

Supporting information

The inhibition of violacein production, anti-swarming, and anti-quorum sensing activity results of A. monspessulanum subsp. monspessulanum extracts are available in as Supporting Information.

Acknowledgements

The authors thank Assoc. Prof. Dr. M. D. Sahin, Botanist, Usak University, Usak, Turkey, for providing plant taxonomic identification.

Conflict of Interest

The authors declare no conflict of interest.

• References

• 1 Koh KM, Tham FY. Screening of traditional Chinese medicinal plants for quorum-sensing inhibitors activity. J Microbiol Immunol Infect 2011; 44: 144-148
  CrossrefPubMedSearch in Google Scholar
• 2 Hentzer M, Givskov M. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 2003; 112: 1300-1307
  CrossrefPubMedSearch in Google Scholar
• 3 Dunlap PV. TV-acyl-homoserine lactone autoinducers in bacteria: unity and diversity. In: Shapiro J A, Dworkin M, editors Bacteria as multicellular organisms. London: Oxford University Press; 1997: 69-106
  Search in Google Scholar
• 4 Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 1994; 176: 269-275
  PubMedSearch in Google Scholar
• 5 Manefield M, Rasmussen TB, Henzter M, Andersen JB, Steinberg P, Kjelleberg S, Givskov M. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 2002; 148: 1119-1127
  CrossrefPubMedSearch in Google Scholar
• 6 Laguerre M, Lecomte J, Villeneuve P. Evaluation of the ability of anti oxidants to counteract lipid oxidation: existing methods, new trends and challenges. Prog Lipid Res 2007; 46: 244-282
  CrossrefPubMedSearch in Google Scholar
• 7 Auten RL, Davis JM. Oxygen toxicity and reactive oxygen species: the devil is in the details. Pediatr Res 2009; 66: 121-127
  CrossrefPubMedSearch in Google Scholar
• 8 Liu J, Henkel T. Traditional Chinese medicine (TCM): are polyphenols and saponins the key ingredients triggering biological activities?. Curr Med Chem 2002; 9: 1483-1485
  CrossrefPubMedSearch in Google Scholar
• 9 Yaltirik F. Contributions to the taxonomy of woods in Turkish maples with relation to the humidity of the sites. J Inst Wood Sci 1970; 5: 43-48
  PubMedSearch in Google Scholar
• 10 Zohary M. Geobotanical foundations of the Middle East, Vol. I, II. Stuttgart: Gustav Fischer; 1973
  Search in Google Scholar
• 11 Arnason T, Hebda RJ, Johns T. Use of plants for food and medicine by native peoples of eastern Canada. Can J Bot 1981; 59: 2189-2325
  CrossrefPubMedSearch in Google Scholar
• 12 Wan C, Yuan T, Li L, Kandhi V, Cech NB, Xie M, Seeram NP. Maplexins, new a-glucosidase inhibitors from red maple (Acer rubrum) stems. Bioorg Med Chem Lett 2012; 22: 597-600
  CrossrefPubMedSearch in Google Scholar
• 13 Hur JM, Yang EJ, Choi SH, Song KS. Isolation of phenolic glucosides from the stems of Acer tegmentosum Max. J Korean Soc Appl Biol Chem 2006; 49: 149-152
  PubMedSearch in Google Scholar
• 14 Inayatullah S, Irum R, Rehman A, Chaudhary MF, Mirza B. Biological evaluation of some selected plant species of Pakistan. Pharm Biol 2007; 45: 397-403
  CrossrefPubMedSearch in Google Scholar
• 15 Jiang CB, Chang MJ, Wen CL, Lin YP, Hsu FL, Lee MH. Natural products of cosmetics: analysis of extracts of plants endemic to Taiwan for the presence of tyrosinase-inhibitory, melanin-reducing, and free radical scavenging activities. J Food Drug Anal 2006; 14: 346-352
  PubMedSearch in Google Scholar
• 16 Lee MH, Jiang CB, Juan SH, Lin RD, Hou WC. Antioxidant and heme oxygenase-1 (HO-1)-induced effects of selected Taiwanese plants. Fitoterapia 2006; 77: 109-115
  CrossrefPubMedSearch in Google Scholar
• 17 Kim JH, Lee BC, Sim GS, Lee DH, Lee KE, Yun YP, Pyo HB. The isolation and antioxidative effects of vitexin from Acer palmatum . Arch Pharm Res 2005; 28: 195-202
  CrossrefPubMedSearch in Google Scholar
• 18 Hou WC, Lin RD, Cheng KT, Hung YT, Cho CH, Chen CH, Hwang SY, Lee MH. Free radical-scavenging activity of Taiwanese native plants. Phytomedicine 2003; 10: 170-175
  CrossrefPubMedSearch in Google Scholar
• 19 van den Berg AK, Perkins TD. Contribution of anthocyanins to the antioxidant capacity of juvenile and senescing sugar maple (Acer saccharum) leaves. Funct Plant Biol 2007; 34: 714-719
  CrossrefPubMedSearch in Google Scholar
• 20 Inayatullah S, Prenzler PD, Obied HK, Rehman A, Mirza B. Bioprospecting traditional Pakistani medicinal plants for potent antioxidants. Food Chem 2012; 132: 222-229
  CrossrefPubMedSearch in Google Scholar
• 21 Royer M, Diouf PN, Stevanovic T. Polyphenol contents and radical scavenging capacities of red maple (Acer rubrum L.) extracts. Food Chem Toxicol 2011; 49: 2180-2188
  CrossrefPubMedSearch in Google Scholar
• 22 Lee JE, Kim GS, Park SM, Kim YH, Kim MB, Lee WS, Jeong SW, Lee SJ, Jin JS, Shin SC. Determination of chokeberry (Aronia melanocarpa) polyphenol components using liquid chromatography-tandem mass spectrometry: Overall contribution to antioxidant activity. Food Chem 2014; 146: 1-5
  CrossrefPubMedSearch in Google Scholar
• 23 Narayanan V, Seshadri TR. Chemical components of Acer rubrum wood and bark: occurrence of procyanidin dimer and trimer. Indian J Chem 1969; 7: 213-214
  PubMedSearch in Google Scholar
• 24 Sibley JL, Ruter JM. Bark anthocyanin levels differ with location in cultivars of red maple. HortScience 1999; 34: 137-139
  PubMedSearch in Google Scholar
• 25 Adonizio AL, Downum K, Bennett BC, Mathee K. Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol 2006; 105: 427-435
  CrossrefPubMedSearch in Google Scholar
• 26 Bosgelmez-Tinaz G, Ulusoy S, Ugur A, Ceylan O. Inhibition of quorum sensing-regulated behaviors by Scorzonera sandrasica . Curr Microbiol 2007; 55: 114-118
  CrossrefPubMedSearch in Google Scholar
• 27 Donabedian H. Quorum sensing and its relevance to infectious disease. J Infect 2003; 46: 207-214
  CrossrefPubMedSearch in Google Scholar
• 28 Singh BN, Singh BR, Singh RL, Prakash D, Dhakarey R, Upadhyay G, Singh HB. Oxidative DNA damage protective activity, antioxidant and anti-quorum sensing potentials of Moringa oleifera . Food Chem Toxicol 2009; 47: 1109-1116
  CrossrefPubMedSearch in Google Scholar
• 29 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: 778-786
  CrossrefPubMedSearch in Google Scholar
• 30 Musthafa KS, Ravi AV, Annapoorani A, Packiavathy ISV, Pandian SK. Evaluation of anti-quorum-sensing activity of edible plants and fruits through inhibition of the N-acyl-homoserine lactone system in Chromobacterium violaceum and Pseudomonas aeruginosa . Chemotherapy 2010; 56: 333-339
  CrossrefPubMedSearch in Google Scholar
• 31 Khan MSA, 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: 354-360
  CrossrefPubMedSearch in Google Scholar
• 32 Cuendet M, Hostettmann K, Potterat O, Dyatmiko W. Iridoid glucosides with free radical scavenging properties from Fagraea blumei . Helv Chim Acta 1997; 80: 1144-1152
  CrossrefPubMedSearch in Google Scholar
• 33 Kirby AJ, Schmidt RJ. The antioxidant activity of chinese herbs for eczema and of placebo herbs – I. J Ethnopharmacol 1997; 56: 103-108
  CrossrefPubMedSearch in Google Scholar
• 34 Jayaprakasha GK, Rao LJ. Phenolic constituents from lichen Parmotrema stuppeum (Nyl.). Hale and their antioxidant activity. Z Naturforsch C 2000; 55: 1018-1022
  PubMedSearch in Google Scholar
• 35 Slinkard K, Singleton VL. Total phenol analyses: automation and comparison with manual methods. Am J Enol Vitic 1977; 28: 49-55
  PubMedSearch in Google Scholar
• 36 Chandler SF, Dodds JH. The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasidine in callus cultures of Solanum lacinitum . Plant Cell Rep 1983; 2: 105-108
  CrossrefPubMedSearch in Google Scholar
• 37 Caponio F, Alloggio V, Gomes T. Phenolic compounds of virgin olive oil: ınfluence of paste preparation techniques. Food Chem 1999; 64: 203-209
  CrossrefPubMedSearch in Google Scholar
• 38 Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; 16th informational supplement (CLSI Document M100-S16). Wayne PA: CLSI; 2006
  Search in Google Scholar
• 39 McLean RJC, Pierson III LS, Fuqua C. A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 2004; 58: 351-360
  CrossrefPubMedSearch in Google Scholar
• 40 Yeo SS, Tham F. Anti-quorum sensing and antimicrobial activities of some traditional Chinese medicinal plants commonly used in South-East Asia. Malays J Microbiol 2012; 8: 11-20
  PubMedSearch in Google Scholar

Correspondence

• References

• 1 Koh KM, Tham FY. Screening of traditional Chinese medicinal plants for quorum-sensing inhibitors activity. J Microbiol Immunol Infect 2011; 44: 144-148
  CrossrefPubMedSearch in Google Scholar
• 2 Hentzer M, Givskov M. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 2003; 112: 1300-1307
  CrossrefPubMedSearch in Google Scholar
• 3 Dunlap PV. TV-acyl-homoserine lactone autoinducers in bacteria: unity and diversity. In: Shapiro J A, Dworkin M, editors Bacteria as multicellular organisms. London: Oxford University Press; 1997: 69-106
  Search in Google Scholar
• 4 Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 1994; 176: 269-275
  PubMedSearch in Google Scholar
• 5 Manefield M, Rasmussen TB, Henzter M, Andersen JB, Steinberg P, Kjelleberg S, Givskov M. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 2002; 148: 1119-1127
  CrossrefPubMedSearch in Google Scholar
• 6 Laguerre M, Lecomte J, Villeneuve P. Evaluation of the ability of anti oxidants to counteract lipid oxidation: existing methods, new trends and challenges. Prog Lipid Res 2007; 46: 244-282
  CrossrefPubMedSearch in Google Scholar
• 7 Auten RL, Davis JM. Oxygen toxicity and reactive oxygen species: the devil is in the details. Pediatr Res 2009; 66: 121-127
  CrossrefPubMedSearch in Google Scholar
• 8 Liu J, Henkel T. Traditional Chinese medicine (TCM): are polyphenols and saponins the key ingredients triggering biological activities?. Curr Med Chem 2002; 9: 1483-1485
  CrossrefPubMedSearch in Google Scholar
• 9 Yaltirik F. Contributions to the taxonomy of woods in Turkish maples with relation to the humidity of the sites. J Inst Wood Sci 1970; 5: 43-48
  PubMedSearch in Google Scholar
• 10 Zohary M. Geobotanical foundations of the Middle East, Vol. I, II. Stuttgart: Gustav Fischer; 1973
  Search in Google Scholar
• 11 Arnason T, Hebda RJ, Johns T. Use of plants for food and medicine by native peoples of eastern Canada. Can J Bot 1981; 59: 2189-2325
  CrossrefPubMedSearch in Google Scholar
• 12 Wan C, Yuan T, Li L, Kandhi V, Cech NB, Xie M, Seeram NP. Maplexins, new a-glucosidase inhibitors from red maple (Acer rubrum) stems. Bioorg Med Chem Lett 2012; 22: 597-600
  CrossrefPubMedSearch in Google Scholar
• 13 Hur JM, Yang EJ, Choi SH, Song KS. Isolation of phenolic glucosides from the stems of Acer tegmentosum Max. J Korean Soc Appl Biol Chem 2006; 49: 149-152
  PubMedSearch in Google Scholar
• 14 Inayatullah S, Irum R, Rehman A, Chaudhary MF, Mirza B. Biological evaluation of some selected plant species of Pakistan. Pharm Biol 2007; 45: 397-403
  CrossrefPubMedSearch in Google Scholar
• 15 Jiang CB, Chang MJ, Wen CL, Lin YP, Hsu FL, Lee MH. Natural products of cosmetics: analysis of extracts of plants endemic to Taiwan for the presence of tyrosinase-inhibitory, melanin-reducing, and free radical scavenging activities. J Food Drug Anal 2006; 14: 346-352
  PubMedSearch in Google Scholar
• 16 Lee MH, Jiang CB, Juan SH, Lin RD, Hou WC. Antioxidant and heme oxygenase-1 (HO-1)-induced effects of selected Taiwanese plants. Fitoterapia 2006; 77: 109-115
  CrossrefPubMedSearch in Google Scholar
• 17 Kim JH, Lee BC, Sim GS, Lee DH, Lee KE, Yun YP, Pyo HB. The isolation and antioxidative effects of vitexin from Acer palmatum . Arch Pharm Res 2005; 28: 195-202
  CrossrefPubMedSearch in Google Scholar
• 18 Hou WC, Lin RD, Cheng KT, Hung YT, Cho CH, Chen CH, Hwang SY, Lee MH. Free radical-scavenging activity of Taiwanese native plants. Phytomedicine 2003; 10: 170-175
  CrossrefPubMedSearch in Google Scholar
• 19 van den Berg AK, Perkins TD. Contribution of anthocyanins to the antioxidant capacity of juvenile and senescing sugar maple (Acer saccharum) leaves. Funct Plant Biol 2007; 34: 714-719
  CrossrefPubMedSearch in Google Scholar
• 20 Inayatullah S, Prenzler PD, Obied HK, Rehman A, Mirza B. Bioprospecting traditional Pakistani medicinal plants for potent antioxidants. Food Chem 2012; 132: 222-229
  CrossrefPubMedSearch in Google Scholar
• 21 Royer M, Diouf PN, Stevanovic T. Polyphenol contents and radical scavenging capacities of red maple (Acer rubrum L.) extracts. Food Chem Toxicol 2011; 49: 2180-2188
  CrossrefPubMedSearch in Google Scholar
• 22 Lee JE, Kim GS, Park SM, Kim YH, Kim MB, Lee WS, Jeong SW, Lee SJ, Jin JS, Shin SC. Determination of chokeberry (Aronia melanocarpa) polyphenol components using liquid chromatography-tandem mass spectrometry: Overall contribution to antioxidant activity. Food Chem 2014; 146: 1-5
  CrossrefPubMedSearch in Google Scholar
• 23 Narayanan V, Seshadri TR. Chemical components of Acer rubrum wood and bark: occurrence of procyanidin dimer and trimer. Indian J Chem 1969; 7: 213-214
  PubMedSearch in Google Scholar
• 24 Sibley JL, Ruter JM. Bark anthocyanin levels differ with location in cultivars of red maple. HortScience 1999; 34: 137-139
  PubMedSearch in Google Scholar
• 25 Adonizio AL, Downum K, Bennett BC, Mathee K. Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol 2006; 105: 427-435
  CrossrefPubMedSearch in Google Scholar
• 26 Bosgelmez-Tinaz G, Ulusoy S, Ugur A, Ceylan O. Inhibition of quorum sensing-regulated behaviors by Scorzonera sandrasica . Curr Microbiol 2007; 55: 114-118
  CrossrefPubMedSearch in Google Scholar
• 27 Donabedian H. Quorum sensing and its relevance to infectious disease. J Infect 2003; 46: 207-214
  CrossrefPubMedSearch in Google Scholar
• 28 Singh BN, Singh BR, Singh RL, Prakash D, Dhakarey R, Upadhyay G, Singh HB. Oxidative DNA damage protective activity, antioxidant and anti-quorum sensing potentials of Moringa oleifera . Food Chem Toxicol 2009; 47: 1109-1116
  CrossrefPubMedSearch in Google Scholar
• 29 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: 778-786
  CrossrefPubMedSearch in Google Scholar
• 30 Musthafa KS, Ravi AV, Annapoorani A, Packiavathy ISV, Pandian SK. Evaluation of anti-quorum-sensing activity of edible plants and fruits through inhibition of the N-acyl-homoserine lactone system in Chromobacterium violaceum and Pseudomonas aeruginosa . Chemotherapy 2010; 56: 333-339
  CrossrefPubMedSearch in Google Scholar
• 31 Khan MSA, 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: 354-360
  CrossrefPubMedSearch in Google Scholar
• 32 Cuendet M, Hostettmann K, Potterat O, Dyatmiko W. Iridoid glucosides with free radical scavenging properties from Fagraea blumei . Helv Chim Acta 1997; 80: 1144-1152
  CrossrefPubMedSearch in Google Scholar
• 33 Kirby AJ, Schmidt RJ. The antioxidant activity of chinese herbs for eczema and of placebo herbs – I. J Ethnopharmacol 1997; 56: 103-108
  CrossrefPubMedSearch in Google Scholar
• 34 Jayaprakasha GK, Rao LJ. Phenolic constituents from lichen Parmotrema stuppeum (Nyl.). Hale and their antioxidant activity. Z Naturforsch C 2000; 55: 1018-1022
  PubMedSearch in Google Scholar
• 35 Slinkard K, Singleton VL. Total phenol analyses: automation and comparison with manual methods. Am J Enol Vitic 1977; 28: 49-55
  PubMedSearch in Google Scholar
• 36 Chandler SF, Dodds JH. The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasidine in callus cultures of Solanum lacinitum . Plant Cell Rep 1983; 2: 105-108
  CrossrefPubMedSearch in Google Scholar
• 37 Caponio F, Alloggio V, Gomes T. Phenolic compounds of virgin olive oil: ınfluence of paste preparation techniques. Food Chem 1999; 64: 203-209
  CrossrefPubMedSearch in Google Scholar
• 38 Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; 16th informational supplement (CLSI Document M100-S16). Wayne PA: CLSI; 2006
  Search in Google Scholar
• 39 McLean RJC, Pierson III LS, Fuqua C. A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 2004; 58: 351-360
  CrossrefPubMedSearch in Google Scholar
• 40 Yeo SS, Tham F. Anti-quorum sensing and antimicrobial activities of some traditional Chinese medicinal plants commonly used in South-East Asia. Malays J Microbiol 2012; 8: 11-20
  PubMedSearch in Google Scholar

• Supplementary Material