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Received: 22 October 2018 Revised: 27 November 2018 Accepted: 3 January 2019 DOI: 10.1111/jfbc.12776
FULL ARTICLE
Phytochemical content, antioxidant activity, and enzyme inhibition effect of Salvia eriophora Boiss. & Kotschy against acetylcholinesterase, α‐amylase, butyrylcholinesterase, and α‐glycosidase enzymes Ercan Bursal1
| Abdulmelik Aras2 | Ömer Kılıç3 | Parham Taslimi4
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Ahmet C. Gören5 | İlhami Gülçin4 1
School of Health, Department of Nursing, Muş Alparslan University, Muş, Turkey 2
Faculty of Science and Arts, Department of Biochemistry, Iğdır University, Iğdır, Turkey 3
Department of Park and Garden Plants, Technical Vocational College, Bingöl University, Bingöl, Turkey 4
Faculty of Science, Department of Chemistry, Ataturk University, Erzurum, Turkey 5
Faculty of Pharmacy, Department of Basic Medicine, Bezmialem Vakif University, İstanbul, Turkey Correspondence Ercan Bursal, Department of Nursing, School of Health, Muş Alparslan University, Muş, Turkey. Emails:
[email protected];
[email protected]
Abstract Many taxa of Salvia genus have been used in herbal beverages, food flavoring, cos‐ metics, and pharmaceutical industry. In this paper, chemical compounds of Salvia eriophora (S. eriophora) leaves were determined by LC–MS/MS (Liquid Chromatography tandem Mass Spectrometry). Salvigenin (158.64 ± 10.8 mg/kg), fumaric acid (123.09 ± 8.54 mg/kg), and quercetagetin‐3.6‐dimethylether (37.85 ± 7.09 mg/kg) were detected as major compounds in the ethanol extract, whereas fumaric acid (555.96 ± 38.56 mg/kg), caffeic acid (103.62 ± 20.51 mg/kg), and epicatechin (83.19 ± 8.43 mg/kg) were detected as major compounds in the water extract. Furthermore, enzyme inhibition of S. eriophora against acetylcholinesterase (AChE), α‐amylase (AM), butyrylcholinesterase (BChE), and α‐glycosidase (AG) enzymes were detected. AChE, BChE, AG, and AM enzymes were very strongly inhibited by S. erio‐ phora water extract (WES) and S. eriophora methanol extract (MES). Additionally, an‐ tioxidant potential of S. eriophora was determined by in vitro analytical methods. IC50 values of WES and MES were performed for radicals.
Practical applications Metabolic enzymes have crucial functions on living systems due to inhibition or acti‐ vation of them mainly attributed with some health disorders. AChE, BChE, AM, and AG enzymes have important roles on carbohydrate metabolism or cholinergic path‐ ways. The relation between enzyme inhibition effect and phenolic compounds or antioxidant activity need to be confirmed. Thus, many studies tested to clarify this relation for pure samples or plant extracts. To the best of our knowledge, this is the first report about inhibition effects of Salvia eriophora extracts against AChE, BChE, AM, and AG enzymes as well as their phenolic contents and antioxidant activities. KEYWORDS
antioxidant, cholinesterase, enzyme inhibition, α‐amylase, α‐glycosidase
J Food Biochem. 2019;e12776. https://doi.org/10.1111/jfbc.12776
wileyonlinelibrary.com/journal/jfbc
© 2019 Wiley Periodicals, Inc. | 1 of 13
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1 | I NTRO D U C TI O N
anticholinergic, antiradical, and antioxidant properties of samples
Lamiaceae taxa has ethnobotanical, economic importance, chemical
the most convenient inhibitory activity of the S. eriophora extracts
constituents such as diterpenes, triterpenes, and phenolics (Wu et
against BChE, AChE, AG, and AM enzymes were investigated.
were determined using some bioanalytical techniques. Additionally,
al., 2012). The Salvia L. genus is one of the Lamiaceae members and it has more than 97 species in Turkey that more than half of them are endemic. Salvia is widely known as the largest genus in the mint family. Also, some species of Salvia were statemented to be used for memory‐enhancing property, as well as food flavoring, herbal tea,
2 | E X PE R I M E NTA L 2.1 | Plant material and extraction procedures
perfumery, cosmetics, and pharmaceutical industry (Orhan, Senol,
S. eriophora of endemic plant from Turkey was collected on June 26,
Ozturk, Akaydin, & Sener, 2012; Perry, Bollen, Perry, & Ballard,
2016, between Yenibektaşlı village and Gürün district (Sivas‐Turkey),
2003). Some of Salvia taxa secondary metabolites have aromatic
from southeast of Yenibektaşlı village, stony slopes (1750–1800 m).
character, antifungal, antimicrobial, and antioxidant properties
Dr. Omer Kilic identified the plant sample according to Flora of
(Alimpić et al., 2015; Dogan et al., 2010). Therefore, Salvia taxa have
Turkey and East Eagean Islands (Davis, 1982). The plants were de‐
been intensively studied in food preservation, medical, and pharma‐
posited in the Herbarium of the Park and Garden Plants Department,
cology fields (Gali‐Muhtasib & Affara, 2000).
University of Bingol, Turkey (Voucher No: Kilic 2574 for S. eriophora).
Biological activities and enzyme inhibition effects of some Salvia species were investigated in many reports (Bahadori et al., 2017;
The S. eriophora leaves were dried in air and then powdered to small pieces before use.
Bahadori, Dinparast, Valizadeh, Farimani, & Ebrahimi, 2016; Zengin,
The leaves of S. eriophora were dried at room condition. For the
Llorent‐Martínez et al., 2018). Endemic plant species like S. erio‐
preparation of WES and MES, 20 g of leaves were powdered and
phora, grows naturally only in a single and narrow geographic area.
mixed with 200 ml of distilled water or methanol (1/10:w/v). The mix‐
However, there is insufficient information about S. eriophora in the
tures were homogenized by a magnetic mixer about 12 hr, at room
literature. In several work clearly stated that noteworthy part of
conditions. The homogeneous mixtures were filtered with filter pa‐
green plants, vegetables, and fruits are found to be primary and nat‐
pers. The filtrate samples were lyophilized in a lyophilizer (Labconco,
ural sources of antioxidants. Consuming of the antioxidant sources
Freezone 1 L) at 5 mm Hg at −50°C for water extract and evaporated
is a reasonable way to reduce risk of many disease (Aras, Bursal,
with a rotary evaporator (Heidolph 94200, Bioblock Scientific) for
& Dogru, 2016; Silinsin & Bursal, 2018). Secondary metabolites of
methanol extract. They were stored at −30°C until used.
plants might have correlation with antioxidant activity (Kandemir et al., 2017; Koeduka et al., 2014). These compounds have protective effects against oxidative reactions such as reducing activity, a hydro‐
2.2 | Chemicals
gen donor functions, and metal chelating activity which are proper‐
Standards of LC–MS/MS analysis: luteolin‐7‐O‐glu (99%) from
ties of antioxidants (Limmongkon et al., 2017).
AppliChem and isorhamnetin (98%, ExtraSynthese) from Genay‐
AChE is relevant with the development of cells and assists the re‐
France and all other standards from Sigma‐Aldrich were supplied
generation of nerves and maturation of neurons (Zhang, Chen, & Liu,
(Table 1). Stock solutions were prepared as 10 mg/L in methanol
2016). Inhibition of this enzyme cause to the constant and extreme
(Merck), which were prepared as 0.1 mg/L and 5 mg/L respectively,
acetylcholine accumulation in nerve synapses. The AChE activities
in the same solvent. Calibration solutions were prepared in metha‐
have been used as biomarkers of organophosphorus and carbamate
nol in a linear range (Table 1). Using glass volumetric flasks (A class)
insecticides. AChE, primarily spreads in the nervous tissue, swiftly
and automatic pipettes dilutions were performed, stored at −20°C
interferes in the catalyzation of the hydrolysis of the neurotrans‐
in glass containers. Approximately 100 mg/L curcumin solution was
mitter acetylcholine, and causes the cancellation of transmission of
freshly prepared, from which 50 μl was used as an Internal Standard
nerve impulse, thus ensures the physiological function of the body
(IS) in all experiments.
normally. For nervous system AChE is a significant member, so any negative effects on AChE efficiency may cause to neurotoxicity (Mrdaković et al., 2016). BChE related in many physiological factors, the most exclusive is the hydrolysis of both choline and noncho‐ line esters, such as aspirin, cocaine, and succinylcholine; therefore,
2.3 | Antioxidant activity 2.3.1 | DPPH• scavenging assay
it has a significant role in neurotransmission and anesthesia. Some
The free radical scavenging capacities were evaluated using DPPH
of AChE and BChE enzymes inhibitor compounds have detected as
(1,1‐diphenyl‐2‐picryl‐hydrazyl)
drugs developed for the treatment of Alzheimer's disease and myas‐
(Gülçin, Beydemir, Şat, & Küfrevioğlu, 2005). This technique is based
thenia gravis (Taslimi et al., 2018).
upon the removal of stable DPPH free radicals by reaction with
free
radical
scavenging
assay
On the present study, LC–MS/MS method was used for de‐
antioxidants. According to this assay, concentration of extracts
termination of phenolic contents of S. eriophora extracts. Also,
(10–30 µg/ml) and standards were prepared and adjusted to 3 ml
Quercetagetin‐3,6‐di‐ methylether
Rosmarinic acid
Luteolin‐7‐O‐Glucoside
Luteolin‐5‐O‐Glucoside
Kaempferol‐3‐O‐ Rutinoside
Rutin
Curcumin*
20
21
22
23
24
25
26
*Used as internal standard
Isorhamnetin
19
193
t‐Ferulic acid
Luteolin
17
18
125
Fumaric acid
Pyrogallol
15
369.3
609
593
447
447
359.2
345.1
315
285
115
329
287
301
353
16
Ellagic acid
12
Kaempferol
Chlorogenic acid
11
179
269
Salvigenin
Caffeic acid
10
13
Apigenin
9
175
289
611.5
449
289
305
168.6
471.9
Parent ion
14
Catechin
Ascorbic acid
Cyanidin chloride
6
7
Cyanidin‐3‐O‐Glu
5
8
Epigallocatechin
Epicatechin
3
4
Quercitrin
Gallic acid
1
2
Compounds
176.9
301
284.4
289.5
284.5
160.5
329.5
300
132
133
80
71
295.8
152.3
150.5
191
135
151
114.6
245
287
287
245
125
124
309.9
Daughter ion
20
16
18
20
14
15
16
15
30
15
16
8
15
30
10
14
10
22
12
15
28
16
14
18
13
16
Coll. energy (V)
TA B L E 1 LC–MS/MS validation and uncertainty parameters of compounds
y = 0.0232x+0.0008
y = 0.1080x+0.0135
y = 0.2300x+0.0413
y = 0.1350x+0.0246
y = 0.1960x+0.0043
y = 0.0181x+0.0202
y = 0.0739x+0.5100
y = 0.2120x+0.0699
y = 0.0655x+0.0266
y = 0.0438x+0.0073
y = 0.0569x+0.0177
y = 0.0355x+0.8620
y = 0.0230x+0.0116
y = 0.0244x+0.0048
y = 0.2620x+0.0674
y = 0.3300x+0.0036
y = 0.1780x+0.0850
y = 0.4892x+0.0090
y = 0.9045x+0.0061
y = 0.2613x+0.0035
y = 0.3840x+0.0809
y = 0.1594x+0.0205
y = 0.0227x+0.0191
y = 0.0569x+0.0177
y = 0.0290x+0.0058
Linear regression equation
0.9969
0.9977
0.9926
0.9957
0.9982
0.9924
0.9608
0.9937
0.9925
0.9803
0.9912
0.9912
0.9841
0.9951
0.998
0.9924
0.9961
0.9788
0.9099
0.9059
0.9762
0.9581
0.9566
0.9912
0.9918
R2
0.01
0.014
0.01
0.022
0.022
0.022
0.088
0.062
0.047
0.001
0.003
0.036
0.002
0.02
0.445
0.028
0.15
0.199
0.008
0.006
0.019
0.002
0.211
0.002
0.001
LOD (mg/L)
0.034
0.045
0.034
0.072
0.072
0.074
0.294
0.207
0.158
0.002
0.01
0.119
0.008
0.068
1.483
0.093
0.501
0.665
0.027
0.021
0.064
0.007
0.704
0.008
0.002
LOQ (mg/L)
7.9
8.15
1.12
8.56
3.73
0.1
3.67
0.16
5.21
5.47
5.44
5.21
5.47
0.11
5.45
8.04
4.01
9.42
0.3
6.39
6.57
4.78
0.21
4.85
4.28
RSD (%)
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with ethanol. To each sample; 0.1 mM and 1 ml of DPPH was added. The mixtures were left in the dark at room temperature for 30 min. Absorption spectra were calculated at 517 nm via (Shimadzu, UV‐1800, Japan). The scavenging capabilities of samples on DPPH free radicals were measured by comparing with controls. Also, IC50 values of samples and standard compounds were determined.
2.3.2 | ABTS
•+
ing agent for determination of the antioxidant capability of polyphe‐ nols for this method. First, (1 ml, 7.5 × 10−3 M) neocuproine solution, CuCl2 solution (1 ml, 0.01 M), and (1 ml, 1 M) CH3COONH4 buffer were added to those tubes. The volumes were completed to 4 ml with distilled water. The samples were left at room temperature for 30 min
Free radical scavenging potentials were evaluated by ABTS (2,2′‐ acid)
cation
radi‐
cal scavenging technique (Guelcin, Oktay, Koeksal, Serbetci, & Beydemir, 2008). First of all, the ABTS radicals were produced by reaction of 2 mM ABTS in pure water with potassium persulphate (2.45 mM) solution during 12 hr at room temperature. The ABTS cation with a characteristic absorption at 734 nm has a dark blue‐ green color. The solution of ABTS cation was diluted with phosphate buffer concentration (0.1 M, pH 7.4) to get absorbance of 0.9 ± 0.1 at 734 nm. 1 ml of ABTS•+ solution was added to 3 ml of extract so‐ lution at (10–30 mg/ml) concentrations in methanol and standard compounds separately. The samples were vortexed and left in the dark for 30 min. Then absorbances at 734 nm were measured. The decrease in sample absorption shows the activity of ABTS•+ radical scavenging.
2.3.3 | DMPD scavenging assay The DMPD (N,N‐Dimethyl‐p‐phenylenediamine) cation radical scavenging capacity of S. eriophora was detected by a previously re‐ ported technique by Gülçin (2008). For this purpose, a dark‐colored solution of radical cation (DMPD ∙+) was first obtained. Then, 1 ml of DMPD solution and 0.2 ml of 0.05 M FeCl3 were added to 100 ml of acetate buffer (pH 5.3; 100 mM). The absorbance of the control solution at 505 nm was adjusted to 0.900 ± 0.100 nm using phos‐ phate buffer (0.1 M and pH 5.3). The concentrations of the extracts and standards were ranged from 10 µg/ml to 30 µg/ml. The volume was brought to 0.5 ml using pure water for each tube. One milliliter of DMPD•+ solution was added and absorbance was measured at 505 nm after incubation for 50 min. The buffer solution was used for blank.
2.3.4 | FRAP assay The FRAP (Ferric Reducing Antioxidant Power) assay is based upon measuring of reduction Fe3+ions by antioxidants to the Fe2+ ions using TPTZ (tripyridyltriazine) under proper acidic conditions. TPTZ solution (2.25 ml, 10 mM TPTZ in 40 mM HCl) was freshly prepared and transferred to FeCl3 (2.25 ml, 20 mM) and acetate buffer (25 ml, 0.3 M, pH 3.6) solution. Then, (10–30 µg/ml) extracts and reference standard were dissolved in buffer solvent (5 ml), vortexed and incu‐ bated for 30 min at 37°C. The measurement was done at 593 nm (Aksu et al., 2016).
Reactive copper (II) neocuproine was used as a chromogenic oxidiz‐
were added to each tube. 10–30 µg/ml concentrations of extracts
scavenging assay
Azino‐bis‐3‐ethylbenzothiazoline‐6‐sulfonic
2.3.5 | Cu2+ reducing assay
to fully reveal their reducing capacity. Finally, absorbance calculation was done at 450 nm. Absorbance increase was evaluated as an in‐ crease of reducing capacity (Aras, Silinsin, Bingol, & Bursal, 2017).
2.3.6 | Fe3+ reducing assay Fe3+ to Fe2+ reduction method was chosen for specification Fe3+ re‐ ducing the capability of S. eriophora (Bursal & Boğa, 2018). Briefly, 10–30 μg/mL S. eriophora concentrations in 0.75 ml of deionized H2O were added to 1.25 ml of potassium ferricyanide [K3Fe(CN)6] (1%) and 1.25 ml of phosphate buffer (0.2 M, pH 6.6). After solu‐ tion was incubated at 50°C for 20 min trichloroacetic acid (1.25 ml, 10%) and FeCl3 (0.5 ml, 0.1%) was added to this mixture. Absorbance value was measured at 700 nm in a spectrophotometer. As seen from the results obtained, parallel to reduction capacity, absorbance values increases.
2.4 | Enzyme inhibition 2.4.1 | Evaluation of α‐Glycosidase (AG) and α‐Amylase (AM) inhibitons The inhibitory efficacy of S. eriophora against AG and AM was ap‐ plied using p nitrophenyl‐D‐glucopyranoside (p‐NPG), as the sub‐ strate (Tao, Zhang, Cheng, & Wang, 2013). To prepare the sample, 10 mg in 10 ml (EtOH: H2O) was dissolved. First, sample (10–100 µl) and enzyme solution (20 µl) were mixed in 100 µl of phosphate buffer (0.15 U/ml, pH 7.4). To get best enzyme inhibition multiple solutions were prepared in phosphate buffer. Then, to the initiation of the reaction p‐NPG was added and incubated at 35°C for 12 min. After this step p‐NPG (50 µl) in phosphate buffer (5 mM, pH 7.4) was added and incubation repeated at 37°C. Absorbances were calcu‐ lated at 405 nm. The value of the EC50 was measured from plant con‐ centration plots. For calculation of the Vmax, Ki and other inhibition parameters Lineweaver Burk graphs were used. One unit of AM or AG is the number of enzymes that catalyze the hydrolysis of 1.0 mol substrate per minute (pH 7.4).
2.4.2 | Determination of AChE and BChE inhibitions S. eriophora extracts inhibitory activities on AChE and BChE was de‐ termined. Acetylthiocholine iodide (AChI) and butyrylcholine iodide (BChI) were used as substrates for activity studies of enzymes (Işık
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BURSAL et al.
et al., 2015). BChE or AChE activities were defined using 5,5′‐dithio‐
LOD and LOQ values were calculated to be 0.5–50 mg/L for the
bis (2‐nitrobenzoic) acid (DTNB). 50–200‐µl concentration of water
compounds (Table 1). Each analyte concentration within the linear
solutions and buffer solution (100 µl, pH 8.0, Tris‐HCl, 1.0 M) were
range and of the method concentration was acquired from the cal‐
added to 50 µl of BChE and AChE solutions (5.32 × 10 −3 EU). Then,
ibration curve. For evaluation of sources and quantification of the
the prepared mixture was incubated for 10 min at 20°C. After all
uncertainty of LC–MS/MS process EURACHEM/CITAC guide was
these processes, 50 µl of DTNB (0.5 mM and 25 ml) and BChI/AChI
referred.
(50 µl) were added to the mixtures. Also, by the addition of 50 µl of BChI/AChI reaction was initiated. Efficacy of both enzymes were measured at 412 nm. One unit of AChE hydrolyzes 1.0 mol of AChI to choline and acetate as well as one BChE unit states the amount of enzyme that hydrolyzes 1.0 mol of BChI to choline and butyrate for
3 | R E S U LT S A N D D I S CU S S I O N 3.1 | Phenolic compounds
per minute at 37°C (pH 8.0). The enzymes were provided from Sigma
Flavonoids are phenolic compounds that synthesized by plants
(AG and AM from Saccharomyces cerevisiae, AChE from electric eel
and are effective against microbial infections. They are abundantly
Electrophorus electricus, BChE from equine serum).
found in almost all part of plants and widely consumed for diet. These hydroxylated phenolic compounds have many effects like an‐
2.5 | Determination of phenolics using LC–MS/MS 2.5.1 | Preparation of samples
timutagenic, antiviral, and antioxidant (Aras, Dogru, & Bursal, 2016). Antioxidants are thought to be reason for preventing or lowering cardiovascular diseases, cancer risk, brain dysfunction, and cata‐ racts (Bursal, 2013; Köksal et al., 2017).
Fifty milligrams of the extracts were dissolved and reflux in 5 ml of
In current work, the phenolic content of S. eriophora was deter‐
ethanol–water (50:50 v/v) in a volumetric flask for 1 hr, then from
mined using LC–MS/MS. Some standard phenolic acid chromato‐
which 1 ml was added to a 5 ml of another flask. After, 50 µl of cur‐
grams are shown in Figure 1. Identification peaks were depending
cumin was added and diluted to the volume with methanol. From the
on retention time, parent and fragment ions of the standards.
final solution, 1 ml was added to the capped autosampler vial and
The most intensive phenolics in methanol extract were de‐
10 µl of the sample was injected to LC. The samples in autosampler
termined as salvigenin and fumaric acid, as well as fumaric acid
were kept at 15°C during the experiment.
and caffeic acid, were determined for water extracts as shown in Table 2. The correlation between the intensive phenolic content of
2.5.2 | Chromatographic conditions
S. eriophora (salvigenin, fumaric acid, and caffeic acid) and some of diseases treatment has been detected by many researchers. Some
Evaluations were carried out on an HPLC integrated with Tandem
of them; salvigenin has affection on growth inhibition of MCF‐7
Gold Triple quadrupole (Zivak®, Istanbul, Turkey). Chromatographic
(a breast cancer cell line isolated) (Noori, Hassan, Yaghmaei, &
separations were done in Synergy Max C18 column (250 × 2 mm
Dolatkhah, 2013) causes vasorelaxation in rat aortic rings (Uydeş‐
i.d., 5‐µm particle diameter). Solvent A was water (0.1% formic acid)
Doğan et al., 2005), as a neuroprotective flavone inhibits apoptosis
and solvent B was methanol (0.1% formic acid) the gradient at 30°C
and oxidative stress with diverse size in the cortex and hippocam‐
was as follows: 0–1 min, 55% A and 45% B, 1–20 min 100% B and
pus of beta‐amyloid‐injected rats (Esfandabadi, Khodagholi, &
20–23 min 55% A and 45% B at the flow rate of 0.25 ml/min. and the
Sanati, 2013), for vasorelaxation and malaria disease salvigenin
injection volume was 10 µl.
effects have been determined (Rafatian, Khodagholi, Farimani,
Triple quadrupole integrated mass spectrometry is frequently
Abraki, & Gardaneh, 2012).
used because of its fragmented ion stability. Therefore, this sys‐
Due to inhibition of tyrosinase and its crucial role in pigment
tem was decided to use for defining the phenolic composition of
production, fumaric acid is a potential natural anti pigmentation
S. eriophora. The ESI source optimum parameters were as follows:
agent (Gou et al., 2017), accessed as a food additive for its an‐
2.40‐mTorr CID gas pressure, 600‐V ESI shield voltage, 5,000‐V ESI
timicrobial and antioxidant effects. Fumaric acid is also used as
needle voltage, 50‐C API housing temperature, 300‐C drying gas
an acidity regulator (E297) (Wu, Cravotto, Adrians, Ondruschka,
temperature, 40‐psi drying gas pressure, and 55‐psi Nebulizer gas
& Li, 2015) and also has highest inhibitory activity against
pressure.
Staphylococcus aureus and Streptococcus (He, Fu, Shen, Jiang, &
For each compound, reported method linearity was detected
Wei, 2011). Caffeic acid is one of the major hydroxycinnamic acids
by analyzing standard solution. The linearity ranges were given in
found in plants. In particular, it is one of the intensive phenolic
Table 1. The correlation coefficients (r2) were detected as ≥0.99.
acids found in potatoes, coffee, and wine, its derivatives have
Equations for linear decline of the compounds are also shown in
very good electron donating abilities (Urbaniak, Kujawski, Czaja, &
Table 1, where x is the concentration and y is the peak area.
Szelag, 2017), different caffeic acid derivatives have been stated
Determining method sensitivity was done by measure of concen‐
as strong and selective matrix metalloproteinase‐9 (MMP‐9) in‐
trations repeating 3 times for each compound. High sensitivity was
hibitors for the therapeutic treatment of cancer (Singh, Grewal,
detected, and the results were applied to the uncertainty budget.
Pandita, & Lather, 2018).
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F I G U R E 1 The chromatograms of standard secondary metabolites by LC–MS/MS (5 mg/L)
3.2 | Antioxidant activity
radicals to colored DPPH‐H complex. Table 3 and Figure 2a define an important decrement (p Trolox ≈ WES > BHA > BHT
antioxidants prevent oxidative stress. The reduction capability of
> α‐tocopherol. The lower IC50 means the higher radical scavenging
a compound may relate to its possible antioxidant capacity. These
activity for both DPPH and ABTS•+. According to the results, metha‐
compounds have the capability to transfer electrons into reactive
nol extract of S. eriophora has effective DPPH radical scavenging ac‐
radicals, thus reduce them into more stable and unreactive spe‐
tivity. Likewise, water extracts of S. eriophora showed effective free
cies. They have been investigated broadly because of having many
radicals scavenging activity. It was monitored that the free radical
positive effects on health (Parhiz, Roohbakhsh, Soltani, Rezaee, &
scavenging potential of the standards and plant extracts increased
Iranshahi, 2015). Many plants have the potential to stabilize or pre‐
with increasing their concentration (Figure 2a).
vent radical chain reactions due to certain specific reducing agents
As demonstrated in Figure 2b and Table 3, S. eriophora ex‐
in their structure (Jindal & Kumar, 2012). We measured the antioxi‐
tracts had an effect on ABTS•+ radical scavenging. The IC50 values,
dant potential of S. eriophora (water and methanol extracts) by var‐
6.58 ± 0.003 µg/ml for WES and 6.03 ± 0.008 µg/ml for MES. It
ious in vitro spectrophotometric technique including DPPH, ABTS,
is understood that ABTS•+ concentration (p Trolox ≈ WES > BHT > B
compared. S. eriophora content has the capability to reduce DPPH
HA > α‐tocopherol.
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BURSAL et al.
TA B L E 2 Amount of secondary metabolites in extracts mg/kg concentration
Compounds
S. eriophora‐Methanol
S. eriophora‐Water
1
Quercitrin
18.73 ± 2.49
–
2
Gallic acid
1.2 ± 0.08
2.59 ± 0.18
3
Epigallocatechin
–
–
4
Epicatechin
3.62 ± 0.37
83.19 ± 8.43
5
Cyanidin‐3‐O‐Glu
–
–
6
Cyanidin chloride
–
–
7
Catechin
–
53.85 ± 3.63
8
Ascorbic acid
–
–
9
Apigenin
–
0.36 ± 0.03
10
Caffeic acid
–
103.62 ± 20.51
11
Chlorogenic acid
4.13 ± 0.57
6.47 ± 0.90
12
Ellagic acid
–
–
13
Kaempferol
–
–
14
Salvigenin
158.64 ± 10.80
22.48 ± 1.53
15
Fumaric acid
123.09 ± 8.54
555.96 ± 38.56
16
Pyrogallol
–
15.23 ± 1.01
17
t‐Ferulic acid
11.3 ± 0.79
49.79 ± 3.48
18
Luteolin
–
2.74 ± 0.70
19
Isorhamnetin
10.03 ± 0.88
–
20
Quercetagetin‐3.6‐di‐ methylether
37.85 ± 7.09
–
21
Rosmarinic acid
–
9.82 ± 0.75
22
Luteolin‐7‐O‐Glucoside
–
–
23
Luteolin‐5‐O‐Glucoside
2.41 ± 0.16
–
24
Kaempferol‐3‐O‐ Rutinoside
–
–
25
Rutin
–
–
TA B L E 3 The IC50 values of S. eriophora and standards for scavenging DPPH·, ABTS•+ and DMPD ·+ radicals Antioxidant Compounds
DPPH scavenging
R2
ABTS•+ scavenging
R2
DMPD•+ scavenging
R2
BHA
10.66 ± 0.012
0.9508
8.07 ± 0.006
0.9720
28.17 ± 0.016
0.9618
BHT
11.01 ± 0.005
0.9810
7.16 ± 0.004
0.9955
33.81 ± 0.014
0.9082
α‐Tocopherol
15.37 ± 0.009
0.9684
10.12 ± 0.010
0.9429
40.62 ± 0.020
0.9593
Trolox
9.83 ± 0.006
0.9927
6.28 ± 0.007
0.9112
31.18 ± 0.009
0.9887
S. eriophora (Water)
9.94 ± 0.015
0.9401
6.58 ± 0.003
0.9649
38.10 ± 0.015
0.9266
S. eriophora (Methanol)
9.21 ± 0.011
0.9793
6.03 ± 0.008
0.9911
36.82 ± 0.008
0.9521
As demonstrated in Figure 2c and Table 3, S. eriophora extracts
to evaluate the total reducing power of antioxidants. Because of
had effective DMPD•+ radical scavenging. The IC50 values for WES
its colored complex with TPTZ, Fe2+ can be defined spectrophoto‐
and MES were 38.10 ± 0.008 µg/ml for WES and 36.82 ± 0.015 µg/
metrically. The blue‐colored complex (Fe2+‐TPTZ) has a maximum
ml for MES. The scavenging efficacy of S. eriophora extracts and ref‐
absorbance at 593 nm (Köse et al., 2015). Fe3+ reducing capacities
erence standards on the DMPD
•+
decreased as: BHA > Trolox > BH
T > MES > WES > α‐tocopherol.
of extracts and standards at the same concentration (30 µg/ml) were increased as follows: WES, MES, α‐tocopherol, Trolox, BHA,
Reduction of both ferric (Fe3+) and cupric (Cu2+) ions are gen‐
and BHT (Figure 3a, Table 4). FRAP assay has been often used for a
erally utilized as an electron donor and it is significant for phenolic
fast definition of the total antioxidant capacity of many foods, me‐
compounds action mechanism. The FRAP assay frequently used
dicinal, and pharmaceutical plants. Also, it has been implemented
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F I G U R E 2 Radical scavenging activities of different concentrations (10–30 µg/ml) of Salvia eriophora extracts and reference antioxidants by some in vitro methods: (a) DPPH, (b) ABTS, (c) DMPD
for the measure of in vitro antioxidant ability of flavonoids, phenolics, and polyphenols (Cavalli et al., 2008).Cu
2+
reducing
powers of S. eriophora extracts and standards were graphed on
(Fe3+) ions reducing capacity and also had remarkable electron‐ releasing properties to neutralize free radicals by forming steady compounds.
Figure 3b. The positive correlation was determined for different concentration of S. eriophora extracts and Cu2+ reducing power. It was defined that Cu2+ reducing capacity of S. eriophora depends
3.3 | Enzyme inhibition
on concentration. Cu2+ reducing capabilities of S. eriophora ex‐
In the present study, AChE, BChE, α‐amylase, and α‐glycosidase
tracts and standards at the same concentration (30 µg/ml) were
enzymes were efficiently inhibited by S. eriophora plant (Table 5).
increased as follows: Trolox, α‐tocopherol, WES, MES, BHA, and
TAC (9‐amino‐1,2,3,4‐tetrahydroacridine) is a reversible inhibitor of
BHT (Table 4). The highest reducing power was found as BHT
BChE and AChE and the first drug to be authorized for the placa‐
for both (Fe3+) and (Cu2+) ions reducing power methods.The Fe3+
tive treatment of AD. IC50 values for WES and MES on metabolic
(CN−) 6 reduction technique, measure the molecule antioxidant ef‐
enzymes were obtained 15.06 ± 0.015 9.91 ± 0.058 µg/ml for
fects by measuring reducing capacity in the reaction. S. eriophora
AChE and 10.82 ± 0.010, 5.17 ± 0.043 µg/ml for BChE, respec‐
extracts had the most efficient reducing capacity using Fe3+ (CN−) 6
tively. In addition, tacrine (TAC) was used as positive standard BChE
reduction and Cu2+ ions reducing capability when compared with
and AChE inhibitor it had IC50 values 0.101 ± 0.016 µmol/L and
the positive controls. As shown in Figure 3c and Table 4, reducing
0.124 ± 0.015 µmol/L, respectively. In a previous study, the inhibi‐
capacity of 30 µg/ml concentration of extracts and standard were
tion percentages of the EtOAc and MeOH extracts of S. eriophora
increased as follows: WES, α‐tocopherol, MES, Trolox, BHT, and
against BChE and AChE enzymes were reported to be low‐level
BHA. The results showed that S. eriophora extracts had excellent
inhibitions (Orhan et al., 2012). Also, another study reported to
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F I G U R E 3 Reducing abilities of different concentrations (10–30 µg/ml) of Salvia eriophora extracts and reference antioxidants by some in vitro methods: (a) Fe3+ −TPTZ−Fe2+ −TPTZ, (b) Cu2+ reducing, (c) Fe3+ reducing
TA B L E 4 Detection of reducing power of S. eriophora and standard compounds by FRAP methods, Fe3+ and Cu2+ ions reducing methods Fe3+–Fe2+reducing
Cu2+–Cu+ reducing
Fe3+–TPTZ reducing
Antioxidants
λ 700
R2
λ 450
R2
λ593
R2
BHA
2.404 ± 0.013
0.9622
2.398 ± 0.020
0.9588
2.733 ± 0.017
0.9629
BHT
2.307 ± 0.009
0.9902
2.568 ± 0.011
0.9362
2.809 ± 0.012
0.9788
α‐Tocopherol
1.644 ± 0.017
0.9118
1.371 ± 0.009
0.9277
2.327 ± 0.001
0.9998
Trolox
2.177 ± 0.007
0.9736
1.282 ± 0.008
0.9811
2.432 ± 0.015
0.9611
S. eriophora (Water)
1.533 ± 0.009
0.9815
1.514 ± 0.002
0.9507
1.814 ± 0.006
0.9698
S. eriophora (Methanol)
1.662 ± 0.002
0.9424
1.606 ± 0.006
0.9816
1.944 ± 0.005
0.9862
S. eriophora ethanol extract inhibited 29.26 ± 2.9% of BChE activity.
systems of medicine and are presently accepted as an alternative for
However, it did not exhibit any inhibition against AChE (Topcu et al.,
diabetic therapy. Also, for many plant extracts, there is clear under‐
2013).
standing of the mechanism of action. AChE and BChE have been de‐
There is raising interest to report documents about the safety
fined in amyloid plaques and neurofibrillary tangles (Li et al., 2018).
and effect of natural dietary supplements and specific herbs that
AChE detected as predominates enzyme in the normal brain, BChE
have been used for treating diabetes in traditional medicine. Indeed,
is thought to be related with a secondary role in the brain for regula‐
plenty of the currently accessible drugs have been indirectly or
tion of acetylcholine levels (Chen et al., 2017; Gulçin et al., 2017). A
directly derived from plants. Plant methanol extracts have long
significant increase in the AChE activity is monitored in Alzheimer’s
been utilized for the ethnomedical treatment of diabetes in diverse
disease early stage but the activity of BChE increasingly progresses
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TA B L E 5 The results of S. eriophora enzyme inhibition (IC50 values) against AG, AM, AChE, and BChE enzymes S. eriophora (Water)(µg/ml)
S. eriophora (Methanol) (µg/ml)
Standards (µM)
Enzymes
IC50
r2
IC50
r2
IC50
r2
α‐Glycosidase*
5.54 ± 0.050
0.9937
2.94 ± 0.035
0.9915
22.80 ± 0.032
0.9922
α‐Amylase*
1.41 ± 0.013
0.9795
8.88 ± 0.075
0.9936
10.01 ± 0.022
0.9424
Acetylcholinesterase**
15.06 ± 0.015
0.9621
9.91 ± 0.058
0.9862
0.124 ± 0.015
0.9804
Butyrylcholinesterase**
10.82 ± 0.010
0.9581
5.17 ± 0.043
0.9938
0.101 ± 0.016
0.9698
*
For α‐glycosidase and α‐amylase enzymes acarbose was used as standard reference **For acetylcholinesterase and butyrylcholinesterase enzymes tacrine was used as standard reference.
F I G U R E 4 The enzyme inhibition of Salvia eriophora water extract against α‐Glycosidase (AG), α‐Amylase (AM), acetylcholinesterase (AChE), and butyrylcholinesterase (BchE) enzymes
in Alzheimer’s later stages. For this reason, both AChE and BChE are
According to the result of our study, IC 50 values for WES
substantial therapeutic targets for the recovery of the cholinergic
and MES on metabolic enzymes were obtained 1.41 ± 0.013,
deficit and thought to be the Alzheimer’s disease hallmark (Zengin,
8.88 ± 0.075 µg/ml
Senkardes et al., 2018). Alzheimer’s disease is initiated with short‐
2.94 ± 0.035 µg/ml for α‐glycosidase, respectively. A previous
for
α‐amylase
and
5.54 ± 0.050,
term memory loss and worsening more with impaired communica‐
study reported that the inhibition effect of dichloromethane ex‐
tion, disorientation, behavior changes, swallowing, speaking, and
tract of Salvia officinalis was lower than hot water extract of S.
walking difficulties (Garibov et al., 2016).
officinalis against on both α‐glucosidase and amylase enzymes
By the consumption of carbohydrates, AM breaks down polysac‐
(Paddy, Tonder, & Steenkamp, 2015). Similar to our study, the en‐
charides to the oligosaccharides form which will be further cleaves
zyme inhibitory (cholinesterase, tyrosinase, amylase, glucosidase,
by AG to produce glucose and this leads to an increase in the level of
lipase, and elastase) effects of three extracts (dichloromethane,
glycemic. This carbohydrate hydrolyzing enzyme inhibition has been
methanol, and water) from three Salvia species (S. blepharoch‐
determined by many researchers as one of the most substantial ther‐
laena, S. euphratica var. leiocalycina, and S. verticillata subsp. ama‐
apeutic ways to control type II diabetes.
sica) were assessed (Zengin, Senkardes et al., 2018). Also, a similar
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F I G U R E 5 The enzyme inhibition of Salvia eriophora methanol extract against α‐Glycosidase (AG), α‐Amylase (AM), acetylcholinesterase (AChE), and butyrylcholinesterase (BchE) enzymes
study investigated the antioxidant and enzyme inhibitory activity
plant and it is biological activity will inspire for drug designers in the
of Salvia cadmica Boiss against five enzymes (α‐amylase, α‐glucosi‐
treatment of many diseases such as diabetes mellitus, Alzheimer, and
dase, AChE, BChE, and tyrosinase). According to the results of that
dementia symptoms.
report, the plant extract showed only α‐amylase and α‐glucosidase inhibition (Kocak et al., 2016). Some researcher reported that Salvia taxa improves memory and has anticholinesterase activity (Çulhaoğlu, Yapar, Dirmenci, & Topçu, 2013). Furthermore, Salvia taxa have been searched to measure for Alzheimer’s disease treatment via anticholinesterase effect (Orhan et
C O N FL I C T O F I N T E R E S T The authors declared that they have no conflict of interest. ORCID
al., 2007). Because of these reasons; the evaluation of effects of S. erio‐
Ercan Bursal
phora on AChE, BChE, AG, and AM was the important purpose of this
Parham Taslimi
work. AChE, BchE, AG, and AM were very strongly inhibited by S. erio‐
İlhami Gülçin
https://orcid.org/0000-0001-7289-4507 https://orcid.org/0000-0002-3171-0633 https://orcid.org/0000-0001-5993-1668
phora water and methanol extracts as shown in Table 5, Figures 4 and 5. REFERENCES
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How to cite this article: Bursal E, Aras A, Kılıç Ö, Taslimi P, Gören AC, Gülçin İ. Phytochemical content, antioxidant activity, and enzyme inhibition effect of Salvia eriophora Boiss. & Kotschy against acetylcholinesterase, α‐amylase, butyrylcholinesterase, and α‐glycosidase enzymes. J Food Biochem. 2019;e12776. https://doi.org/10.1111/jfbc.12776
