Startseite Comparative analysis of the polyphenols profiles and the antioxidant and cytotoxicity properties of various blue honeysuckle varieties
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Comparative analysis of the polyphenols profiles and the antioxidant and cytotoxicity properties of various blue honeysuckle varieties

  • Yuehua Wang , Xu Xie , Xulong Ran , Shurui Chou , Xinyao Jiao , Enhui Li , Qi Zhang , Xianjun Meng und Bin Li EMAIL logo
Veröffentlicht/Copyright: 9. Juli 2018
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Aus der Zeitschrift Open Chemistry Band 16 Heft 1

Abstract

The polyphenol profile, antioxidant activity (particularly peroxyl radical-scavenging capacity (PSC) and cellular antioxidant activity (CAA)) and cytotoxicity of extracts from seven varieties of blue honeysuckle were compared in this study. Moreover, an analysis of correlations between individual polyphenol profiles and antioxidant activities was also conducted. Seventeen components were found in the investigated blue honeysuckle extracts, with anthocyanins being the prominent bioactive components among polyphenols. Fruit peel contained higher concentrations of individual anthocyanins compared to the fruit pulp. Beilei blue honeysuckle had the highest antioxidant activity. Correlation analysis showed that antioxidant activity values were highly associated with cyanidin-3-glucoside levels. Blue honeysuckle extracts were not cytotoxic over the range of doses tested. Among the varieties analyzed, Beilei possessed the highest antioxidant properties and was found to be the most appropriate source of natural antioxidants.

Keywords: blue honeysuckle; polyphenol profiles; antioxidant activity; cytotoxicity

1 Introduction

Berry fruits have been regarded as rich sources of nutrients and phytochemicals, such as phenolic acids, flavonoids, and anthocyanins. These phytochemicals have been reported to exhibit powerful antioxidant, anti-inflammatory, anticancer, antimicrobial, and anti-aging activities [1,2,3]. Additionally, some polyphenols have been found to act as neurohormetics by stimulating several cellular signaling pathways [4,5, 6,7]. Hence, long-term intake of berries rich in nutrients and phytochemicals reduces the incidence of cardiovascular and degenerative disorders and has a positive impact on human health [8].

Blue honeysuckle (Lonicera caerulea L.), belonging to the family Caprifoliaceae, is mainly found in Russia, Japan, Korea, Inner Mongolia, northeast China, and parts of North America [9]. Blue honeysuckle is rich in polyphenols, contributing to its potential bioactive properties; its polyphenol content is higher than that of some other berries, such as blueberry and raspberry [10,11]. The main identified components of blue honeysuckle are shikimic acid, 5-O-caffeoylquinic acid, 3-O-caffeoylquinfc acid, cyanidin-3-glucoside, cyanidin-3,5-diglucoside, peonidin-3,5-diglucoside, pelargonidin-3-glucoside, and peonidin-3-glucoside [12]. Additionally, iridoid compounds including loganic acid, 7-epi-loganic acid, 8-epi-loganic acid, 7-O-pentoside, loganin, sweroside, secologanin and pentosyl-loganic acid, which have anti-inflammatory properties and reduce the risk of metabolic diseases and cardiovascular disease, were identified in blue honeysuckle [13,14]. Blue honeysuckle extracts have been found to exhibit extensive positive biological effects, such as anti-inflammatory [15,16,17], anti-microbial [18], anti-radiation activities [19]. However, even in different cultivars within a species or different tissues within a fruit, the composition of phytochemicals can vary widely due to genetic variation, growth conditions, degree of maturity and harvesting season, which results in differences in their bioactive properties [20,21]. The in vitro or in vivo activities of different varieties of blueberry and sea buckthorn vary dramatically, as do their phytochemical profiles [22,23].

Although the composition and some biological activities of blue honeysuckle have been reported [9,12,24,25], previous studies mainly focused on a limited number of varieties of wild blue honeysuckle. Moreover, the antioxidant activities of these molecules have only been assessed chemically, usually in terms of oxygen radical absorbance capacity, peroxyl radical-scavenging capacity (PSC), DPPH radical-scavenging capacity, total oxygen radical-scavenging capacity, and ferric-reducing antioxidant power [26,27]. Hence, there is a need to identify polyphenols in more varieties of blue honeysuckle and to assay antioxidant activities using the cellular antioxidant activity (CAA) assay, which is a more accurate measure of CAA and accounts for the absorption, metabolism, and localization of antioxidants in cells [28].

The objectives of this study were (1) to identify and compare the polyphenols profiles, specifically focusing on anthocyanins, of seven varieties of blue honeysuckle; (2) to determine the antioxidant activities, including the PSC, CAA, and DPPH and ABTS radical-scavenging capacity in such varieties; and (3) to analyze the antiproliferative activity against HepG2 human liver cancer cells. In addition, a correlation analysis of these findings with extracellular and cellular antioxidant activities and polyphenols profile composition was performed. The data highlight blue honeysuckle as a potential functional and health food mainly owing to its polyphenol profiles.

2 Materials and methods

2.1 Chemicals and reagents

Analytical grade methanol, ethanol, hexane, ethyl acetate, hydrochloric acid, acetic acid, potassium chloride, sodium acetate, sodium carbonate, sodium hydroxide, potassium phosphate monobasic, and potassium phosphate dibasic were purchased from Mallinckrodt Chemicals (Phillipsburg, NJ, USA). 2′,7′-Dichlorofluorescein diacetate, fluorescein disodium salt, reagent grade sodium borohydride, analytical-grade chloranil and vanillin, catechin hydrate, Folin–Ciocalteu reagent, ascorbic acid, 6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid, chromatography-grade trifluoroacetic acid and acetonitrile, cholera toxin, hydrocortisone, penicillin, streptomycin, and gentamicin were purchased from Sigma-Aldrich, Inc. (St. Louis, MO, USA). Analytical grade tetrahydrofuran was obtained from Fisher Scientific (Fair Lawn, NJ, USA), while gallic acid was purchased from ICN Biomedicals, Inc. (Aurora, OH, USA). 2,2′-Azobis(2-amidinopropane) dihydrochloride was purchased from Wako Chemicals (Richmond, USA), while HepG2 human hepatoma cells were obtained from the American Type Culture Collection (HB-8065). Williams' medium E, Hank’s balanced salt solution, epidermal growth factor, heparin, insulin, and other cell culture reagents were purchased from Gibco U.S. Biotechnology Co. Inc. (Richmond, VA, USA).

2.2 Blue honeysuckle samples

Wild, L-5, Haskap, HSY-24, BKQE, BLS and Beilei blue honeysuckle were harvested in June 2017 from the planting station at the College of Horticulture, Northeast Agricultural University (45°44′25.18″N, 126°43′22.50″E), Haerbin, Heilongjiang province, China. The plants were transported to the College of Food Science, Shenyang Agricultural University, China and stored at -80°C before extraction.

2.3 Extraction of phenolic compounds

For HPLC-MS/MS, ABTS, DPPH, PCS, CAA and cytotoxicity analyses, the extracts were prepared using our previously described method with some modifications [11]. Berries were homogenized after thawing. Homogenate (300 g) was extracted in 600 mL 80% aqueous acetone for 90 min in an ultrasonic bath, and the mixture was clarified by vacuum filtration. The residue was re-extracted using the above procedure until the solvent remained colorless. Extract supernatants were then combined and subjected to rotary evaporation (RE-5203A, Shanghai Bilon Instruments Co., Ltd., China) at 45°C until no acetone remained. The concentrated solution was filtered and then separated through a 400 mL glass column loaded with nonionic polystyrene–divinylbenzene resin (D101, Shanghai, China) at 4°C. Deionized water was passed through the column to remove water-soluble substances, and acetone was used as the eluting solvent. After concentration in the rotary evaporator at 45°C, the collected liquid was freeze-dried into powder using a vacuum freeze dryer (LGO.2, Shenyang Aerospace Xinyang Quick Freezing Equip. Manuf. Co., Ltd., China). The obtained powder was placed in sealed 2-mL centrifuge tubes and stored at -20°C until analysis. The extraction yields of the seven varieties of blue honeysuckle ranged from 1.5% to 2.7% (Table 1).

Table 1

Extraction yields of the seven varieties of blue honeysuckle. Values are expressed as means ± SD (n = 5).

VarietyExtraction yield (% FW)[A]
L-51.5 ± 0.27
Haskap2.3 ± 0.25
Wild2.7 ± 0.14
HSY-241.7 ± 0.31
BKQE2.5 ± 0.47
BLS1.8 ± 0.22
Beilei2.4 ± 0.18

2.4 Identification of phenolic compounds

Peel and pulp were separated using tweezers after the berries were thawed. Phenolic compounds in the peel and pulp of seven varieties of blue honeysuckle were extracted using the procedure described above. Fifteen milligrams of extract were weighed accurately and dissolved in 5 mL of methanol. Samples were filtered through a 0.45 μm filter prior to analysis at 280 nm, 350 nm and 520 nm using an HPLC (Agilent 1100, USA) equipped with a DAD detector (G4212B) and a mass spectrometer (SL, Agilent1100 series LC/MSD Trap, USA). A Dikma Platisil C18 column (4.6 mm × 250 mm, 5 lm) was used. The detailed conditions were as reported in a previous study [11]. Polyphenol= profiles were identified by molecular ions, fragment ions, and the UV/Vis spectra recorded by the DAD detector using HPLC-DAD-EIS-MS2 technology. Cyanidin-3-glucoside, chlorogenic acid, gentistic acid, 5-caffeoylquinic acid, quercetin rutinoside and catechin were used as standards. The standard concentration ranged from 1 to 100 μg/mL.

2.5 ABTS assay

Free radical-scavenging activity of the extracts on ABTS free radicals was analyzed according to the procedures previously described by Caprioli et al. [12]. ABTS was oxidized using MnO2 in distilled water for 30 min in the dark to obtain ABTS•+ solution (5 mM). Next, 50 μL aliquots of extracts in different concentrations and 200 μL of ABTS•+ solution were added to wells in 96-well microtiter plates. After equilibration for 10 min at room temperature, the absorbance was recorded at 734 nm using a microplate reader (FLUOstar Optima, BMG Labtech microplate reader). The results were expressed as Trolox equivalents (TE) per gram of extract.

2.6 DPPH assay

The levels of DPPH radical-scavenging activity in the extracts were determined using appropriate commercial kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China) according to the manufacturer’s instructions. The absorbance was determined at 517 nm. Results were expressed as TE per gram of extract.

2.7 PCS assay

Total antioxidant activity was chemically determined by the PSC assay [26]. In this assay, the thermal degradation of 2,2′-azobis(2-amidinopropane) produces peroxyl radicals (ROO·) that oxidize nonfluorescent dichlorofluorescein to fluorescent dichlorofluorescein. Hence, the inhibition of dichlorofluorescein oxidation radicals is used as the basis for calculating antioxidant activity. Fluorescence was measured on a fluorescent spectrophotometer (Fluoroskan Ascent FL, Thermo Electron Corp., Asheville, NC, USA) at an excitation wavelength of 485 nm and emission wavelength of 538 nm. Antioxidant activity was calculated as milligrams of vitamin C equivalents per 100 g fresh weight, and data are reported as mean ± SD of at least three replicates.

2.8 Cell culture

HepG2 cells were grown at 37°C and 5% CO2 in Williams’ medium E supplemented with 5% fetal bovine serum, 10 mM HEPES, 2 mM L-glutamine, 5 μg/mL insulin, 0.05 μg/mL hydrocortisone, 50 units/mL penicillin, 50 μg/mL streptomycin, and 100 μg/mL gentamycin [29]. Cells between passages 18 and 28 were used for the experiments.

2.9 CAA assay

CAA was measured according to published methods [28]. Briefly, HepG2 cells were seeded at 6 × 104 cells per well on a 96-well microplate containing 100 μL growth medium per well. The growth medium was removed by pipette 24 h post-seeding, and wells were washed with PBS. Triplicate wells were then treated for 1 h with 100 μL medium containing blue honeysuckle extracts and 25 μM dichlorofluorescein diacetate. The wells were then exposed to 600 μM 2,2′-azobis(2-amidinopropane) in 100 μL Hank’s balanced salt solution. For comparison, some wells were washed with 100 μL PBS to remove honeysuckle extracts prior to exposure to 2,2′-azobis(2-amidinopropane). Plates were then read every 5 min for 1 h at an excitation wavelength of 485 nm and an emission wavelength of 538 nm in a Fluoroskan Ascent FL plate reader (Thermo Electron Corp.) operating at 37°C.

2.10 Quantification of CAA

After subtraction of the blank and initial fluorescence, the area under the curve of fluorescence versus time graph was calculated to determine CAA. CAA was expressed as 1 − (∫SA/∫CA), where ∫SA is the integrated area under the curve for the test sample, and ∫CA is the integrated area under the curve for control samples. The median effective dose (EC50) was calculated from a plot of log (∫a/∫u) versus log (dose), where ∫a is the fraction affected by honeysuckle extracts (CAA units) and ∫u is the unaffected fraction (1 − CAA units). Results are reported as micromoles of quercetin equivalents per 100 μg sample.

2.11 Cytotoxicity

Cytotoxicity was measured using the methylene blue assay. Briefly, HepG2 cells were seeded at 4 × 104 cells/well in a 96-well microplate containing 100 μL growth medium/well and allowed to adhere for 24 h at 37°C. The growth medium was then removed, and cells were washed with PBS. Subsequently, cells were incubated for 24 h at 37°C in 100 μL medium supplemented with or without (vehicle controls) different concentrations of blue honeysuckle extracts. Cells were then washed with PBS, stained for 1 h at 37°C with 50 μL methylene blue (98% Hank’s balanced salt solution, 0.67% glutaraldehyde, and 0.6% methylene blue), and washed in deionized water until the wash was clear. Subsequently, cells were extracted for 20 min on a tabletop oscillator using 100 μL 49% PBS, 50% ethanol, and 1% acetic acid, and the absorbance was measured at 570 nm in a microplate reader. Doses were considered cytotoxic if cell viability decreased by >10% in comparison to the control.

2.12 Inhibition of cell proliferation

Antiproliferative effects were assessed in HepG2 cells by the methylene blue colorimetric method. Briefly, HepG2 cells were seeded at 2.5 × 104 cells/well in central wells of a 96-well microplate, while peripheral wells were filled only with 100 μL medium. Plates were then incubated at 37°C for 4 h, at which point media were removed and replaced with 100 μL fresh media supplemented with or without 10, 20, 40, 60, 80, and 100 mg/mL blue honeysuckle extracts. Plates were then incubated at 37°C for 96 h and assayed in triplicate with methylene blue as described. Antiproliferative effects are reported as EC50 values in milligrams of blue honeysuckle extract per milliliter.

2.13 Statistical analyses

Data were reported as the mean ± SD from three replicates per sample. Significant differences in PCS, CAA, ABTS radical-scavenging, DPPH radical-scavenging, cytotoxicity, and antiproliferative effects among the seven varieties were analyzed by ANOVA and Tukey’s test in SPSS (Statistics for Social Science) version 17.0, with statistical significance set at p < 0.05. The correlations between bioactive properties and the content of polyphenols profiles were also analyzed.

Ethical approval: The conducted research is not related to either human or animals use.

3 Results and discussion

3.1 Compositions of phenolic compounds in the peel and pulp

The compositions and contents of phenolic compounds detected in both the peel and pulp of blue honeysuckle berries are shown in Table 2. The chromatogram of Beilei blue honeysuckle extracts is shown in Figure 1, and peaks 1-5 were identified as cyanidin-3-glucoside, quercetin rutinoside, gentistic acid, chlorogenic acid and 5-caffeoylquinic acid, respectively. Anthocyanins [belonging to flavonoids] were the main phenolic compounds in all investigated blue honeysuckle samples. Nine anthocyanins, including cyanidin-3,5-dihexoside, cyanidin-3-glucoside, cyanidin-3-rutinoside, cyanidin-3-acetylhexoside, peonidin-3,5-dihexoside, peonidin-3-glucoside, peonidin-3-rutinoside, pelargonidin-3-glucoside, and delphinidin-3-glucoside, were identified in all varieties of blue honeysuckle. In addition, the identities of three unknown substances, which had MS = 737 [M+H], 897 [M+H], and 765 [M+H] and were suspected to be cyanidin anthocyanins, need to be further confirmed by methods such as NMR. Cyanidin-3-glucoside was the major anthocyanin in the studied cultivars, with markedly higher amounts in the peel than in the pulp. Cyanidin-3-acetylhexoside was exclusively located in the peel of Beilei blue honeysuckle. In general, the peel contained significantly higher concentrations of individual anthocyanins than did the pulp tissue, consistent with results reported by Stojanović et al. [30]. Wild blue honeysuckle (559.6 mg/g DW) contained the highest concentration of cyanidin-3-glucoside, followed by BLS (538 mg/g DW) and Beilei (503.8 mg/g DW), which were higher than those reported in our previous study [31]. Cyanidin was detected as the major anthocyanin both in the peel and pulp of blue honeysuckle. In addition, chlorogenic acid, gentistic acid, 5-caffeoylquinic acid, catechin and quercetin rutinoside were also identified, and they mostly exist in fruit pulp. The composition of phenolic compounds in this study is different from the previous studies reported by Kucharska et al. [13] and Auzanneau et al. [32]. The differences may be attributed to the use of different extraction methods and growth factors.

Figure 1 The chromatogram of Beilei blue honeysuckle extracts analyzed at 350 nm. Peaks 1-5 were speculated to represent cyanidin-3-glucoside, quercetin rutinoside, gentistic acid, chlorogenic acid and 5-caffeoylquinic acid, respectively.
Figure 1

The chromatogram of Beilei blue honeysuckle extracts analyzed at 350 nm. Peaks 1-5 were speculated to represent cyanidin-3-glucoside, quercetin rutinoside, gentistic acid, chlorogenic acid and 5-caffeoylquinic acid, respectively.

Table 2

The identification of major phenolic compounds in extracts from the seven varieties of blue honeysuckle. The results are presented as means ± SD. Cyanidin-3-O-glucoside was used as the standard.

TentativeMolecularFragmentContents (mg/g DW)
identification(m/z)[A](m/z)L-5HaskapWildHSY-24BKQEBLSBeilei
PeelPulpPeelPulpPeelPulpPeelPulpPeelPulpPeelPulpPeelPulp
Anthocyanins
Cyanidin-3,5-dihexoside611 [M+H]449, 28719.7 ±2.34.1 ±0.575.5 ±0.730.8 ±0.123.9 ±0.611.2 ±0.1525.9 ±3.913.73 ±0.747.2 ±1.010.5 ±0.1120.6 ±2.451.2 ±0.3720.9 ±3.434.1 ±0.98
Cyanidin-3-O-glucoside449 [M+H]287376.8 ±15.9178.7 ±8.71179.3 ±14.571.7 ±6.13437.2 ±21.2122.4 ±9.36416.4 ±19.7368.1 ±5.56337.5 ±11.56101.1 ±8.72408.9 ±23.67129.1 ±12.98408.7 ±14.4395.1 ±3.75
Cyanidin-3-rutinoside595 [M+H]449, 287tr[B]n.d.[C]1.6 ±0.450.3 ±0.131.9 ±0.260.4 ±0.140.2 ±0.07tr1.9 ±0.240.7 ±0.061.4 ±0.110.3 ±0.151.4 ±0.25tr
Cyanidin-3-acetylhexoside491 [M+H]287n.d.n.d.n.d.n.d.n.d.n.d.n.d.n.d.n.d.n.d.n.d.n.d.trn.d.
Peonidin-3,5-dihexoside625 [M+H]463, 3010.8 ±0.190.2 ±0.131.9 ±0.260.7 ±0.130.3 ±0.08tr0.8 ±0.14tr0.5 ±0.10tr0.9 ±0.210.7 ±0.151.0 ±0.130.7 ±0.21
Peonidin-3-glucoside463 [M+H]3011.3 ±0.320.6 ±0.140.7 ±0.070.4 ±0.021.8 ±0.281.1 ±0.152.8 ±0.351.4 ±0.124.5 ±0.243.8 ±1.021.7 ±0.370.9 ±0.122.3 ±0.561.6 ±0.27
Peonidin-3-rutinoside609 [M+H]463, 301trn.d.trtrtrn.d.trn.d.trn.d.trn.d.n.d.tr
Pelargonidin-3-glucoside433 [M+H]2712.0 ±0.360.5 ±0.170.5 ±0.120.2 ±0.072.0 ±0.621.2 ±0.273.8 ±0.432.0 ±0.141.0 ±0.110.3 ±0.132.0 ±0.371.0 ±0.171.9 ±0.942.2 ±0.25
Delphinidin-3-glucoside465 [M+H]303n.d.n.d.n.d.n.d.0.4 ±0.080.2 ±0.04n.d.n.d.trn.d.n.d.n.d.n.d.n.d.
Unknown765 [M+H]603, 571, 475, 313, 2870.2 ±0.12n.d.n.d.n.d.n.d.n.d.n.d.n.d.n.d.n.d.0.2 ±0.07n.d.0.4 ±0.13tr
Unknown737 [M+H]575, 557, 423, 329, 287n.d.n.d.n.d.n.d.4.0 ±1.051.4 ±0.72n.d.n.d.2.6 ±0.362.2 ±0.31n.d.n.d.n.d.n.d.
Unknown897 [M+H]735, 573, 449, 2871.6 ±0.641.0 ±0.150.7 ±0.15tr1.6 ±0.351.3 ±0.472.2 ±1.022.1 ±0.821.4 ±0.381.0 ±0.241.7 ±0.171.0 ±0.142.5 ±1.051.6 ±0.85
Phenolic acid
Chlorogenic acid353 [M-H]191, 1791.65 ±0.7443.8 ±11.232.1 ±0.2741.5 ±9.041.3 ±0.4653.1 ±7.341.6 ±0.5658.9 ±16.490.74± 0.1148.4 ±9.471.03 ±0.2357.1 ±5.313.8 ±1.0662.4± 7.84
Gentistic acid153 [M-H]109n.d.10.4 ±2.36n.d12.7 ±1.47n.d.19.2 ±3.982.2 ±0.7620.7 ±5.41n.d.15.1 ±2.072.5 ±0.7517.3 ±3.471.8 ±0.9723.3± 2.69
5-caffeoylquinic acid377 [M+H]355, 163n.d.97.4 ±14.05n.d.132.3± 21.24n.d.223.1± 20.87n.d.204.5± 19.38n.d.198.3± 23.45n.d.216.7 ±12.84n.d.237.5± 15.63
Flavonoids
Catechin289[M-H]245, 203n.d.6.3±1.15n.d.n.d.n.d.5.7 ±1.07n.d.n.d.n.d.4.4 ±1.32n.d.15.1 ±1.15n.d.7.4 ±1.24
Quercetin rutinoside609 [M-H]463, 301,n.d.32.6 ±6.54n.d.n.d.n.d.26.4 ±3.76n.d.n.d.n.d.n.d.n.d.23.7 ±6.31n.d.62.5± 9.73

3.2 Extracellular and intracellular antioxidant activities

PSC was measured to estimate the extracellular antioxidant activity. As can be seen in Figure 2, PSC varied from 595.57 to 2708.67 μmol vitamin C equivalents/100 g fresh weight, with a mean of 1,078 μmol vitamin C equivalents/100 g fresh weight. The values were significantly higher for Beilei than for the other six varieties (p < 0.05). The PSC values were found to be 1057.57, 894.52, 855.36, 748.88, 685.16, and 595.57 μmol vitamin C equivalents/100 g fresh weight in BLS, wild blue honeysuckle, BKQE, L-5, Haskap, and HSY-24, respectively. The data suggested that Beilei and BLS blue honeysuckle have stronger antioxidant activities, presumably as a result of higher levels of polyphenols. We also found that cyanidin-3-glucoside was significantly related to the PSC results of blue honeysuckle extracts (p < 0.05). Notably, the PSC of Beilei blue honeysuckle was higher than that of cranberry (1019.9 μmol vitamin C equivalents/100 g fresh weight) and grape (2018.9 μmol vitamin C equivalents/100 g fresh weight). In addition, values for all honeysuckle varieties were universally higher than that of apple (309.2 μmol vitamin C equivalents/100 g fresh weight) [26]. Moreover, PSC exhibited a significant correlation with DPPH radicalscavenging capacity (R2 = 0.867; p = 0.011).

Figure 2 The antioxidant activities (PSC, CAA, ABTS and DPPH values) of the seven varieties of blue honeysuckle. The results are presented as means ± SD (n=3). Different superscript lowercase letters in the same column denote statistically significant differences at p < 0.05.
Figure 2

The antioxidant activities (PSC, CAA, ABTS and DPPH values) of the seven varieties of blue honeysuckle. The results are presented as means ± SD (n=3). Different superscript lowercase letters in the same column denote statistically significant differences at p < 0.05.

Trolox equivalent antioxidant concentration (TEAC) values were measured in the blue honeysuckle extracts by the ABTS and DPPH radical-scavenging activity assays. As shown in Figure 2, Beilei blue honeysuckle extracts exhibited the highest ABTS radical-scavenging activity (497 μmol TE/g), and HSY-24 blue honeysuckle extracts had 25.8% lower activity. The trend of DPPH radical-scavenging power was similar to that of ABTS radical-scavenging power. In the DPPH assay, HSY-24 blue honeysuckle extracts exhibited a lower scavenging effect, with the IC50 value 0.8 times higher than that of Beilei blue honeysuckle extracts (IC50 = 3.0 μg/mL). Kusznierewicz et al. reported that the ABTS radical-scavenging activity (expressed as TEAC values) of several honeysuckle varieties cultivated in Poland varied from 12.65 to 49.73 mmol TE/100 g [33]. In particular, blue honeysuckle ethanol extracts showed comparable antioxidant activity in ABTS and DPPH tests, with TEAC values of 103 and 421 μmol TE/g, respectively [12]. These differences in ABTS and DPPH radical-scavenging activities may be due to genetic and geographic factors, as well as on the extraction method.

As the CAA assay accounts for the absorption, metabolism, and localization of antioxidants in cells, it is more biologically relevant than chemical methods, and is predictive of the behavior of substances in vivo [34]. Thus, we measured the CAA values of blue honeysuckle (Figure 2) and found that the values were the highest for Beilei (43.02 μmol quercetin equivalents/100 μg sample) and lowest for HSY-24 (7.88 μmol quercetin/100 μg sample), in line with the results obtained with the PSC assay. However, for Haskap, BLS, L-5, BKQE, and wild honeysuckle, the values were 37.76, 27.94, 25.58, 15.45, and 12.78 μmol quercetin/100 μg sample, respectively, which differed from the PSC trends. The discrepancy is likely due to the degradation of bioactive substances during absorption and metabolism. Of note, Liu et al. reported that the result of the CAA of the anthocyanin fraction from wild blue honeysuckle was 14.75 μmol quercetin equivalents/100 mg dry matter [34]. Wang et al. [22] reported that the results from the CAA of blueberry varieties ranged from 60.6 to 201.6 μmol quercetin equivalents/100 g fresh weight, of which 13.5–63.5 μmol quercetin equivalents/100 g fresh weight was taken up by cells.

3.3 Cell proliferation and cytotoxicity

As shown in Figure 3, proliferation in HepG2 cells, as measured by the methylene blue assay, decreased with exposure to increasing concentrations of honeysuckle extracts, with EC50 values between 27.86 and 59.18 mg/mL (data not shown). In particular, the antiproliferative activity was the highest in wild blue honeysuckle, and the lowest in L-5. EC50 values were 34.43, 38.41, 50.18, 50.27, and 55.17 mg/mL for Beilei, Haskap, BKQE, HSY-24, and BLS, respectively. Collectively, the data indicate that blue honeysuckle inhibits proliferation in HepG2 cells in a doseindependent manner, as previously noted [35]. Guo et al. reported that extracts from sea buckthorn (Hippophaë rhamnoides L.) berries were strongly antiproliferative, with an EC50 of 3.31 mg/mL [3].

Figure 3 The cell proliferation and cytotoxicity of the seven varieties of blue honeysuckle. The results are presented as means ± SD (n=3).
Figure 3

The cell proliferation and cytotoxicity of the seven varieties of blue honeysuckle. The results are presented as means ± SD (n=3).

In comparison to the control, all doses of blue honeysuckle extracts reduced cell viability by no more than 10% (Figure 3), indicating that the extracts were not cytotoxic. Furthermore, this result implies that the observed anticancer activity of blue honeysuckle is due to antiproliferative effects rather than cytotoxicity. Strikingly, the inhibition of cancer cell proliferation might be correlated with levels of polyphenols, flavonoids, and antioxidant activities.

4 Conclusions

In this study, we compared the polyphenol profiles, antioxidant activities, cytotoxicities, and antiproliferative activities of extracts from seven varieties of blue honeysuckle. Collectively, the results suggest that blue honeysuckle is a rich source of bioactive molecules, although the profiles of such molecules differed among varieties. Cyanidin, mainly located in the peel, was the prominent bioactive molecule in blue honeysuckle. The isolated molecules were antioxidative, as measured by PSC, CAA, ABTS, and DPPH assays, with the highest antioxidant activity in Beilei blue honeysuckle extracts. Moreover, blue honeysuckle extracts were found to inhibit the proliferation of HepG2 cells without causing cytotoxicity over the doses tested. Our results also indicated that the peel is a rich source of polyphenols profiles, particularly cyanidin-3-O-glucoside. Nevertheless, future research is necessary to investigate the mechanisms underlying these bioactive properties, as well as to develop health-related uses of blue honeysuckle.

  1. Conflict of interest: The authors declare that there are no conflicts of interest.

Acknowledgments

This work was supported by the Young and Middle-aged Technological Innovation Talent Support Program of Shenyang Science and Technology Bureau [Grant number RC170247], Innovative Talent Support Program for Institution of Higher Learning of Liaoning Province [Grant number LR2017038], and the National Natural Science Foundation of China [Grant number 31671863]. We thank Prof. Junwei Huo from Northeast Agricultural University for providing us honeysuckle berries.

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Received: 2018-02-08
Accepted: 2018-05-02
Published Online: 2018-07-09

© 2018 Yuehua Wang et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

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https://doi.org/10.1515/chem-2018-0072
Schlagwörter für diesen Artikel
blue honeysuckle; polyphenol profiles; antioxidant activity; cytotoxicity
Creative Commons
BY-NC-ND 4.0

Artikel in diesem Heft

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  17. Synthesis, characterization, in-vitro antimicrobial properties, molecular docking and DFT studies of 3-{(E)-[(4,6-dimethylpyrimidin-2-yl)imino]methyl} naphthalen-2-ol and Heteroleptic Mn(II), Co(II), Ni(II) and Zn(II) complexes
  18. M-Polynomials and Topological Indices of Dominating David Derived Networks
  19. Human Health Risk Assessment of Trace Metals in Surface Water Due to Leachate from the Municipal Dumpsite by Pollution Index: A Case Study from Ndawuse River, Abuja, Nigeria
  20. Analysis of Bowel Diseases from Blood Serum by Autofluorescence and Atomic Force Microscopy Techniques
  21. Hydrographic parameters and distribution of dissolved Cu, Ni, Zn and nutrients near Jeddah desalination plant
  22. Relationships between diatoms and environmental variables in industrial water biotopes of Trzuskawica S.A. (Poland)
  23. Optimum Conversion of Major Ginsenoside Rb1 to Minor Ginsenoside Rg3(S) by Pulsed Electric Field-Assisted Acid Hydrolysis Treatment
  24. Antioxidant, Anti-microbial Properties and Chemical Composition of Cumin Essential Oils Extracted by Three Methods
  25. Regulatory mechanism of ulinastatin on autophagy of macrophages and renal tubular epithelial cells
  26. Investigation of the sustained-release mechanism of hydroxypropyl methyl cellulose skeleton type Acipimox tablets
  27. Bio-accumulation of Polycyclic Aromatic Hydrocarbons in the Grey Mangrove (Avicennia marina) along Arabian Gulf, Saudi Coast
  28. Dynamic Change of Secondary Metabolites and spectrum-effect relationship of Malus halliana Koehne flowers during blooming
  29. Lipids constituents from Gardenia aqualla Stapf & Hutch
  30. Effect of using microwaves for catalysts preparation on the catalytic acetalization of glycerol with furfural to obtain fuel additives
  31. Effect of Humic Acid on the Degradation of Methylene Blue by Peroxymonosulfate
  32. Serum containing drugs of Gua Lou Xie Bai decoction (GLXB-D) can inhibit TGF-β1-Induced Epithelial to Mesenchymal Transition (EMT) in A549 Cells
  33. Antiulcer Activity of Different Extracts of Anvillea garcinii and Isolation of Two New Secondary Metabolites
  34. Analysis of Metabolites in Cabernet Sauvignon and Shiraz Dry Red Wines from Shanxi by 1H NMR Spectroscopy Combined with Pattern Recognition Analysis
  35. Can water temperature impact litter decomposition under pollution of copper and zinc mixture
  36. Released from ZrO2/SiO2 coating resveratrol inhibits senescence and oxidative stress of human adipose-derived stem cells (ASC)
  37. Validated thin-layer chromatographic method for alternative and simultaneous determination of two anti-gout agents in their fixed dose combinations
  38. Fast removal of pollutants from vehicle emissions during cold-start stage
  39. Review Article
  40. Catalytic activities of heterogeneous catalysts obtained by copolymerization of metal-containing 2-(acetoacetoxy)ethyl methacrylate
  41. Antibiotic Residue in the Aquatic Environment: Status in Africa
  42. Regular Articles
  43. Mercury fractionation in gypsum using temperature desorption and mass spectrometric detection
  44. Phytosynthetic Ag doped ZnO nanoparticles: Semiconducting green remediators
  45. Epithelial–Mesenchymal Transition Induced by SMAD4 Activation in Invasive Growth Hormone-Secreting Adenomas
  46. Physicochemical properties of stabilized sewage sludge admixtures by modified steel slag
  47. In Vitro Cytotoxic and Antiproliferative Activity of Cydonia oblonga flower petals, leaf and fruit pellet ethanolic extracts. Docking simulation of the active flavonoids on anti-apoptotic protein Bcl-2
  48. Synthesis and Characterization of Pd exchanged MMT Clay for Mizoroki-Heck Reaction
  49. A new selective, and sensitive method for the determination of lixivaptan, a vasopressin 2 (V2)-receptor antagonist, in mouse plasma and its application in a pharmacokinetic study
  50. Anti-EGFL7 antibodies inhibit rat prolactinoma MMQ cells proliferation and PRL secretion
  51. Density functional theory calculations, vibration spectral analysis and molecular docking of the antimicrobial agent 6-(1,3-benzodioxol-5-ylmethyl)-5-ethyl-2-{[2-(morpholin-4-yl)ethyl] sulfanyl}pyrimidin-4(3H)-one
  52. Effect of Nano Zeolite on the Transformation of Cadmium Speciation and Its Uptake by Tobacco in Cadmium-contaminated Soil
  53. Effects and Mechanisms of Jinniu Capsule on Methamphetamine-Induced Conditioned Place Preference in Rats
  54. Calculating the Degree-based Topological Indices of Dendrimers
  55. Efficient optimization and mineralization of UV absorbers: A comparative investigation with Fenton and UV/H2O2
  56. Metabolites of Tryptophane and Phenylalanine as Markers of Small Bowel Ischemia-Reperfusion Injury
  57. Adsorption and determination of polycyclic aromatic hydrocarbons in water through the aggregation of graphene oxide
  58. The role of NR2C2 in the prolactinomas
  59. Chromium removal from industrial wastewater using Phyllostachys pubescens biomass loaded Cu-S nanospheres
  60. Hydrotalcite Anchored Ruthenium Catalyst for CO2 Hydrogenation Reaction
  61. Preparation of Calcium Fluoride using Phosphogypsum by Orthogonal Experiment
  62. The mechanism of antibacterial activity of corylifolinin against three clinical bacteria from Psoralen corylifolia L
  63. 2-formyl-3,6-bis(hydroxymethyl)phenyl benzoate in Electrochemical Dry Cell
  64. Electro-photocatalytic degradation of amoxicillin using calcium titanate
  65. Effect of Malus halliana Koehne Polysaccharides on Functional Constipation
  66. Structural Properties and Nonlinear Optical Responses of Halogenated Compounds: A DFT Investigation on Molecular Modelling
  67. DMFDMA catalyzed synthesis of 2-((Dimethylamino)methylene)-3,4-dihydro-9-arylacridin-1(2H)-ones and their derivatives: in-vitro antifungal, antibacterial and antioxidant evaluations
  68. Production of Methanol as a Fuel Energy from CO2 Present in Polluted Seawater - A Photocatalytic Outlook
  69. Study of different extraction methods on finger print and fatty acid of raw beef fat using fourier transform infrared and gas chromatography-mass spectrometry
  70. Determination of trace fluoroquinolones in water solutions and in medicinal preparations by conventional and synchronous fluorescence spectrometry
  71. Extraction and determination of flavonoids in Carthamus tinctorius
  72. Therapeutic Application of Zinc and Vanadium Complexes against Diabetes Mellitus a Coronary Disease: A review
  73. Study of calcined eggshell as potential catalyst for biodiesel formation using used cooking oil
  74. Manganese oxalates - structure-based Insights
  75. Topological Indices of H-Naphtalenic Nanosheet
  76. Long-Term Dissolution of Glass Fibers in Water Described by Dissolving Cylinder Zero-Order Kinetic Model: Mass Loss and Radius Reduction
  77. Topological study of the para-line graphs of certain pentacene via topological indices
  78. A brief insight into the prediction of water vapor transmissibility in highly impermeable hybrid nanocomposites based on bromobutyl/epichlorohydrin rubber blends
  79. Comparative sulfite assay by voltammetry using Pt electrodes, photometry and titrimetry: Application to cider, vinegar and sugar analysis
  80. MicroRNA delivery mediated by PEGylated polyethylenimine for prostate cancer therapy
  81. Reversible Fluorescent Turn-on Sensors for Fe3+ based on a Receptor Composed of Tri-oxygen Atoms of Amide Groups in Water
  82. Sonocatalytic degradation of methyl orange in aqueous solution using Fe-doped TiO2 nanoparticles under mechanical agitation
  83. Hydrotalcite Anchored Ruthenium Catalyst for CO2 Hydrogenation Reaction
  84. Production and Analysis of Recycled Ammonium Perrhenate from CMSX-4 superalloys
  85. Topical Issue on Agriculture
  86. New phosphorus biofertilizers from renewable raw materials in the aspect of cadmium and lead contents in soil and plants
  87. Survey of content of cadmium, calcium, chromium, copper, iron, lead, magnesium, manganese, mercury, sodium and zinc in chamomile and green tea leaves by electrothermal or flame atomizer atomic absorption spectrometry
  88. Biogas digestate – benefits and risks for soil fertility and crop quality – an evaluation of grain maize response
  89. A numerical analysis of heat transfer in a cross-current heat exchanger with controlled and newly designed air flows
  90. Freshwater green macroalgae as a biosorbent of Cr(III) ions
  91. The main influencing factors of soil mechanical characteristics of the gravity erosion environment in the dry-hot valley of Jinsha river
  92. Free amino acids in Viola tricolor in relation to different habitat conditions
  93. The influence of filler amount on selected properties of new experimental resin dental composite
  94. Effect of poultry wastewater irrigation on nitrogen, phosphorus and carbon contents in farmland soil
  95. Response of spring wheat to NPK and S fertilization. The content and uptake of macronutrients and the value of ionic ratios
  96. The Effect of Macroalgal Extracts and Near Infrared Radiation on Germination of Soybean Seedlings: Preliminary Research Results
  97. Content of Zn, Cd and Pb in purple moor-grass in soils heavily contaminated with heavy metals around a zinc and lead ore tailing landfill
  98. Topical Issue on Research for Natural Bioactive Products
  99. Synthesis of (±)-3,4-dimethoxybenzyl-4-methyloctanoate as a novel internal standard for capsinoid determination by HPLC-ESI-MS/MS(QTOF)
  100. Repellent activity of monoterpenoid esters with neurotransmitter amino acids against yellow fever mosquito, Aedes aegypti
  101. Effect of Flammulina velutipes (golden needle mushroom, eno-kitake) polysaccharides on constipation
  102. Bioassay-directed fractionation of a blood coagulation factor Xa inhibitor, betulinic acid from Lycopus lucidus
  103. Antifungal and repellent activities of the essential oils from three aromatic herbs from western Himalaya
  104. Chemical composition and microbiological evaluation of essential oil from Hyssopus officinalis L. with white and pink flowers
  105. Bioassay-guided isolation and identification of Aedes aegypti larvicidal and biting deterrent compounds from Veratrum lobelianum
  106. α-Terpineol, a natural monoterpene: A review of its biological properties
  107. Utility of essential oils for development of host-based lures for Xyleborus glabratus (Coleoptera: Curculionidae: Scolytinae), vector of laurel wilt
  108. Phenolic composition and antioxidant potential of different organs of Kazakh Crataegus almaatensis Pojark: A comparison with the European Crataegus oxyacantha L. flowers
  109. Isolation of eudesmane type sesquiterpene ketone from Prangos heyniae H.Duman & M.F.Watson essential oil and mosquitocidal activity of the essential oils
  110. Comparative analysis of the polyphenols profiles and the antioxidant and cytotoxicity properties of various blue honeysuckle varieties
  111. Special Issue on ICCESEN 2017
  112. Modelling world energy security data from multinomial distribution by generalized linear model under different cumulative link functions
  113. Pine Cone and Boron Compounds Effect as Reinforcement on Mechanical and Flammability Properties of Polyester Composites
  114. Artificial Neural Network Modelling for Prediction of SNR Effected by Probe Properties on Ultrasonic Inspection of Austenitic Stainless Steel Weldments
  115. Calculation and 3D analyses of ERR in the band crack front contained in a rectangular plate made of multilayered material
  116. Improvement of fuel properties of biodiesel with bioadditive ethyl levulinate
  117. Properties of AlSi9Cu3 metal matrix micro and nano composites produced via stir casting
  118. Investigation of Antibacterial Properties of Ag Doped TiO2 Nanofibers Prepared by Electrospinning Process
  119. Modeling of Total Phenolic contents in Various Tea samples by Experimental Design Methods
  120. Nickel doping effect on the structural and optical properties of indium sulfide thin films by SILAR
  121. The effect mechanism of Ginnalin A as a homeopathic agent on various cancer cell lines
  122. Excitation functions of proton induced reactions of some radioisotopes used in medicine
  123. Oxide ionic conductivity and microstructures of Pr and Sm co-doped CeO2-based systems
  124. Rapid Synthesis of Metallic Reinforced in Situ Intermetallic Composites in Ti-Al-Nb System via Resistive Sintering
  125. Oxidation Behavior of NiCr/YSZ Thermal Barrier Coatings (TBCs)
  126. Clustering Analysis of Normal Strength Concretes Produced with Different Aggregate Types
  127. Magnetic Nano-Sized Solid Acid Catalyst Bearing Sulfonic Acid Groups for Biodiesel Synthesis
  128. The biological activities of Arabis alpina L. subsp. brevifolia (DC.) Cullen against food pathogens
  129. Humidity properties of Schiff base polymers
  130. Free Vibration Analysis of Fiber Metal Laminated Straight Beam
  131. Comparative study of in vitro antioxidant, acetylcholinesterase and butyrylcholinesterase activity of alfalfa (Medicago sativa L.) collected during different growth stages
  132. Isothermal Oxidation Behavior of Gadolinium Zirconate (Gd2Zr2O7) Thermal Barrier Coatings (TBCs) produced by Electron Beam Physical Vapor Deposition (EB-PVD) technique
  133. Optimization of Adsorption Parameters for Ultra-Fine Calcite Using a Box-Behnken Experimental Design
  134. The Microstructural Investigation of Vermiculite-Infiltrated Electron Beam Physical Vapor Deposition Thermal Barrier Coatings
  135. Modelling Porosity Permeability of Ceramic Tiles using Fuzzy Taguchi Method
  136. Experimental and theoretical study of a novel naphthoquinone Schiff base
  137. Physicochemical properties of heat treated sille stone for ceramic industry
  138. Sand Dune Characterization for Preparing Metallurgical Grade Silicon
  139. Catalytic Applications of Large Pore Sulfonic Acid-Functionalized SBA-15 Mesoporous Silica for Esterification
  140. One-photon Absorption Characterizations, Dipole Polarizabilities and Second Hyperpolarizabilities of Chlorophyll a and Crocin
  141. The Optical and Crystallite Characterization of Bilayer TiO2 Films Coated on Different ITO layers
  142. Topical Issue on Bond Activation
  143. Metal-mediated reactions towards the synthesis of a novel deaminolysed bisurea, dicarbamolyamine
  144. The structure of ortho-(trifluoromethyl)phenol in comparison to its homologues – A combined experimental and theoretical study
  145. Heterogeneous catalysis with encapsulated haem and other synthetic porphyrins: Harnessing the power of porphyrins for oxidation reactions
  146. Recent Advances on Mechanistic Studies on C–H Activation Catalyzed by Base Metals
  147. Reactions of the organoplatinum complex [Pt(cod) (neoSi)Cl] (neoSi = trimethylsilylmethyl) with the non-coordinating anions SbF6– and BPh4–
  148. Erratum
  149. Investigation on Two Compounds of O, O’-dithiophosphate Derivatives as Corrosion Inhibitors for Q235 Steel in Hydrochloric Acid Solution
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Heruntergeladen am 7.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/chem-2018-0072/html
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