Home Anti-diabetic activity-guided isolation of α-amylase and α-glucosidase inhibitory terpenes from Capsella bursa-pastoris Linn.
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Anti-diabetic activity-guided isolation of α-amylase and α-glucosidase inhibitory terpenes from Capsella bursa-pastoris Linn.

  • Mohd Akbar Dar EMAIL logo , Nasir A. Siddiqui EMAIL logo , Showkat R. Mir , Seema Akbar , Ramzi A. Mothana and Mubashir H. Masoodi EMAIL logo
Published/Copyright: May 24, 2024
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Open Chemistry
From the journal Open Chemistry Volume 22 Issue 1

Abstract

The hypoglycaemic and hypolipidemic potential of ethanol extract of C. bursa-pastoris (ECbp) in streptozotocin (STZ)-provoked diabetic rats was evaluated, and compounds with their α-amylase and α-glucosidase inhibitory potential were isolated. Acute oral toxicity was evaluated in rats. Streptozotocin (STZ) (50 mg/kg body weight) was injected intraperitoneally into rats for diabetes induction. In diabetic rats, ECbp (0.2 g/kg b.w, p.o.) was administered orally for 21 days, and its outcome on blood glucose levels and body weight was observed on a weekly basis besides lipid profile. Compound isolation from ECbp was performed using column chromatography. Oral feeding of ECbp did not produce any toxic effects or death at a dose of 2,000 mg/kg body weight. A serum glucose reduction trend was observed in rats fed with glucose pre-treated with 200 mg/kg b.w. ECbp also appreciably (p < 0.001, p < 0.01, and p < 0.05) diminished raised blood glucose with decreased blood cholesterol levels and led to increased serum high-density lipoprotein levels in comparison to diabetic control rats. Body weight levels were considerably higher (p < 0.05) in diabetic rats treated with ECbp than in diabetic control rats. Isolation of two terpene derivatives (ECbp-1 and ECbp-2) was performed using ECbp, which exhibits significant α-amylase and α-glucosidase inhibition.

Graphical abstract

Keywords: Capsella bursa-pastoris ; terpenes; antidiabetic; α-amylase; streptozotocin; α-glucosidase

1 Introduction

Hyperglycaemia and altered lipids, carbohydrates, and protein metabolism are prominent symptoms of an endocrine metabolic disorder, i.e. diabetes mellitus, as well as increased risk of cardiovascular disease complications [1]. The basic differences between type-1 and type-2 diabetes are the basic processes of their progress and physiological features such as connection with overweight, age, and insulin. The common features of both types of diabetes are hyperglycemia and macrovascular and microvascular complications. Moreover, in both forms of diabetes, metabolic alterations in lipoproteins are responsible for cardiovascular disease pathogenesis in the same manner [2]. Impaired antioxidant defences in the body, which give rise to free radical generation, lead to oxidative stress, which may also lead to the advancement and development of diabetes and associated complications [3]. In type-2 diabetes mellitus, postprandial serum glucose reduction is one of the chief target therapeutic approaches for its treatment, and, at present, only a few drugs are available that are causing such an effect for postprandial hyperglycemia control. These drugs inhibit the hydrolysis of oligosaccharides and disaccharides to simple absorbable monosaccharides [4]. These drugs control postprandial hyperglycemia by selectively inhibiting enzymes (α-amylase and α-glucosidase) found in the small intestine (brush border cells), and control the formation of absorbable monosaccharides by breaking down oligosaccharides and disaccharides [5,6,7]. Enzyme inhibition is caused by drugs such as acarbose/voglibose, which delay carbohydrate digestion and extend the overall digestion time of carbohydrates, which reduces the glucose absorption rate and ultimately leads to a reduction in postprandial plasma glucose levels [8]. It has a significant effect on the health, life expectancy, lifestyle, and associated problems of people with diabetes. Oral hypoglycaemic agents and insulin are currently available drug options for their management, but these are not free from adverse effects. Since then, various medicinal plants and their preparations have been used traditionally as alternatives for the management of diabetes worldwide [9]. These medicinal plants possess anti-diabetic phytoconstituents that are controlled by multiple mechanisms and modes. Hence, medicinal herbs may be used as effective alternatives and valid therapeutic tools for the management and treatment of diabetes and associated complications [10].

Capsella bursa-pastoris L. (Brassicaceae) is a yearly or biennial plant commonly known as Shepherd’s purse, Shepherd’s bag, or Shepherd’s scrip, or Lady’s purse [11]. It has been found worldwide in Cyprus, Europe, Pakistan, Saudi Arabia, Turkey, Iraq, Azerbaijan, India, Iran, China, and other Asian countries. Capsella bursa-pastoris is also distributed in North Africa, Central America, and Eastern Europe [12,13,14]. In China and Japan, the plant has been used for many centuries because of its various therapeutic potentials, such as its ability to halt blood loss of lesions, intensify the formation of urine, and regulate body temperature [15]. The herb as a whole was consumed to treat inflammation caused by disorders in the kidneys, painful micturition, boils and haemorrhoids, severe menstruation, the occurrence of chyle in urine, and hypertension [16]. In some countries, the leaves and roots of this herb are consumed as raw or cooked vegetables [17,18]. Tea made from this herb has antiscorbutics, protein precipitation, diuretics, decreased blood pressure, stimulants, vasoconstrictors, and vulnerability. The pharmacological activities include antimicrobial and anticancer activities, smooth muscle stimulatory effects on guinea pig small intestine, very powerful contraction of guinea pig uterus, infertility effect, negative chronotropic and cardiac inotropic effects on guinea pigs and rabbits, reduction of penetrability in the blood vessel, hepatoprotective, sedative effects, and acetylcholinesterase inhibitor activity. The various phytoconstituents isolated are fatty acids, phytosterols, phenolics, flavonoids, organic acids, peptides, and amino acids [19].

Terpenes are bioactive compounds that occur both as hydrocarbons and terpenoids (oxygen-containing compounds), present naturally in many herbs, and are known to possess significant hypoglycaemic properties [20]. Terpenes show anti-diabetic potential by either of the mechanisms that include stimulation of insulin secretion [21,22,23,24], enhanced plasma BER (β-endorphin immunoreactivity) by activation of α1-ARs to improve the discharge of β-endorphin, which has the potential to excite opioid micro-receptors to diminish gluconeogenesis in the liver and boost glucose uptake in the soleus muscle [25,26], α-glucosidase inhibition [27,28,29], increasing glucose uptake and glycogen synthesis and blood insulin concentrations. It appears that the reason for this outcome was the facilitation of insulin secretagogue impact in β-cells of the pancreas [30] by appreciably augmenting the blood pyruvate concentration and liver glycogen level [31] by improving insulin discharge from β-cells of the pancreas, which is due to improved stimulation of β-cells and insulin synthesis [32,33,34], and by enhancing glucose utilization in striated muscles, which leads to lower plasma glucose levels and increases in insulin discharge from pancreatic β-cells [24,28,35,36]. This is actually a result of inhibiting glucose-6-phosphatase enzyme due to the formation of insulin despite the lack of glucose concentration, which is needed for stimulation [37].

2 Materials and methods

2.1 Plant material and extraction

C. bursa-pastoris was assembled in June–July 2013 from Narbal District Budgam of Jammu & Kashmir and was authenticated by Centre for Biodiversity and Taxonomy, University of Kashmir, under voucher specimen No. 2078/2013 KASH Herbarium, dated 10/07/2013. The plant material was cleaned, reduced to small fragments, and then shade-dried at 25–30°C for a month. The dried plant material was pulverized into a coarse powder. The powdered plant material was weighed (3.7 kg) and stored in labelled airtight bottles for further analysis. The powdered herb material was transferred to a 10 L glass percolator and then extracted by using absolute ethanol with occasional stirring and shaking. After 24 h, the extract was filtered using filter paper (Whatman No.1), and the filtrate was again extracted with equal volumes of solvent. After 48 and 72 h, the procedure was repeated. The pooled supernatants were dried under vacuum at 40°C using an IKA RV 10 (Rotary evaporator). The dried extract was weighed, poured into a labelled vial, and kept in a desiccator for future use.

2.2 Chemicals, reagents, and instruments

Solvents were purchased from Merck Mumbai and Rankem (New Delhi, India). The analytical grade reagents, chemicals, and solvents were used in the study and obtained from Himedia (A-516, Mumbai 400086, India). Biochemical parameters were assessed using commercially accessible diagnostic kits obtained from Primal Healthcare Limited (Mumbai, India). Melting points were established by using a melting apparatus (Perfit); Bruker spectrospin (400 MHz) was used for recording 1H NMR spectra employing CDCl3 and dimethyl sulphoxide (DMSO)-d 6 solvents and tetramethylsilane (TMS) as an internal standard. δ (ppm) was used to denote the chemical shift with TMS and coupling constant (J, in Hz). For spin-coupled patterns, the notations used throughout are as follows: s = singlet, d = doublet, dd = double doublet, ddd = double-double doublet, qd = quaternary doublet, t = triplet, m = multiplet, and br = unresolved broad signal. 13CNMR spectra were recorded on Advance DRY 300, Bruker spectrospin 100 MHz in 5 mm spinning tubes at 27°C, and mass spectra (MS) were examined using Electron Impact ionization at 70 eV on a UPLC system coupled to a Q-TOF Synapt mass spectrometer (Waters, USA) fitted with direct inlet probe system.

2.3 In vitro α-amylase inhibition test

The α-amylase repressive potential was measured using the technique described by Dong et al. [38], with some modifications. In this assay, a solution of the sample (40 µL) with DMSO or acarbose (in a mixture of sodium phosphate buffer [20 mM], pH 6.9 and 0.006 M sodium chloride) was mixed with α-amylase (1 U/mL in phosphate buffer, pH 6.9; 200 µL solution) and incubated for 30 min at room temperature. To each tube, 400 µL of 0.25% starch solution in phosphate buffer (pH 6.9) was added to initiate the reaction. The reaction was carried out at 37°C for 5 min. The reaction was terminated by adding 1.0 mL of the DNS reagent (12% sodium potassium tartrate in 0.4 M sodium hydroxide and 1% 3,5-dinitrosalicylic acid). The tubes containing the above contents were then kept in a water bath (boiling) for 10 min and then cooled to 25°C. The volume was made to 10 mL in each test tube by distilled water and absorbance (A) was recorded at λ max of 540 nm. The control test tube incubation, representing 100% enzyme activity, was performed in the same manner by replacing the extract with a buffer solution. To measure the absorbance of the test samples, only the blank absorbance of the buffer solution (blank incubation) was determined. The α-amylase repressive action was defined as % inhibition and was estimated using the following formula:

% Inhibition = A c − ( A t − A b ) A c × 100 ,

where A c is absorbance of 100% enzyme activity, A t is the absorbance of the test sample with enzyme, and A b is the absorbance of the test sample without enzyme. The sample potency is expressed by IC50, which is the amount of extract required to inhibit 50% of enzyme activity.

2.4 α-Glucosidase inhibition assay

Dong et al.'s [38] method with slight modifications was used for evaluating α-glucosidase inhibition efficacy. In this assay, the test sample in DMSO (60 µL) or acarbose in DMSO and 50 µL of α-glucosidase mixture (0.2 U/mL in 0.1 M phosphate buffer, pH 6.8) was mixed and maintained at 37°C for 20 min in 96-well plate. About 50 µL of 5 mM p-nitrophenyl-α-d-glucopyranoside in 0.1 M phosphate buffer solution (pH 6.8) was added to each well, followed by 20 min incubation at 37°C. To each well, 160 µL of 0.2 M sodium carbonate was added to halt the reaction. A microplate reader was used to record the absorbance (A) at 405 nm, which was matched with the control (60 µL of buffer instead of the test sample). The blank contained only the buffer, and the absorbance was measured. Percent inhibition, which indicated α-glucosidase inhibitory potential, was expressed as

% Inhibition = A c − ( A t − A b ) A c × 100 ,

where A c is the absorbance of 100% enzyme activity, A t is the absorbance of the test sample with enzyme, and A b is the absorbance of the test sample deprived of the enzyme. The sample efficacy is given by the IC50, which is the amount necessary to stop 50% of the enzyme action.

2.5 Experimental animals

Male and female Wistar albino rats (150–200 g) were obtained from the Indian Institute of Integrative Medicine Jammu, J&K, and housed under restricted conditions (12-h light/12-h darkcycle), temperature of 22°C ± 2°C and humidity of 45% ± 5%). The experimental rats were adapted to the environment before and during the experiment. Rats were fed rat feed (Ashirwad Industries, Mohali, Punjab, India), and water was provided ad libitum. The approval for this experimental study was granted under approval (No. F-IAEC (Pharm. Sc.) APPROVAL/2013/20, dated 19-09-2013), Institutional Animal Ethics Committee (IAEC), Department of Pharmaceutical Sciences, University of Kashmir, Hazratbal, Srinagar, India. The ethanol extract of C. bursa-pastoris (ECbp) and the standard drug were orally administered.

2.6 Acute toxicity testing

Oral acute toxicity assessment was conducted in compliance with the Organization for Economic Cooperation and Development Guidelines 423 (acute toxicity classic method) [39]. Rats were scrutinized separately at least once within the first half an hour after oral administration of ECbp (2,000 mg/kg), regularly in the initial 24 h, with particular care provided during the initial 4 h, and daily afterwards for 14 days to determine toxicity.

2.7 Glucose tolerance test

Fasting overnight Wistar albino rats (150–200 g) were chosen for the evaluation of glucose tolerance. The rats were divided arbitrarily into IV groups, with six rats (n = 6 per group). Group I was marked as the normal control, which was fed 1 mL/kg b.w. of vehicle (0.5% CMC in distilled water as a suspending agent). Group II served as the glucose-challenged control that received glucose (2 g/kg b.w.). Group III was fed glibenclamide (Glib) (5 mg/kg b.w.) as a standard drug [40]. Group IV was given 0.2 g/kg b.w. of ECbp. Experimental groups III and IV were given glucose after 20 min of administration of Glib and ECbp, respectively. Blood was collected from the tail vein for glucose estimation at time intervals of 0, 30, 60, and 120 min after glucose administration [41]. A one-touch glucometer (MyLife Pura, Switzerland) was used to measure the blood glucose levels. Blood glucose concentrations and the area under the curve (AUC) were calculated. The trapezoidal method was used to calculate AUC [42].

AUC was calculated using the following formula:

AUC ( mM / L / h ) = BG 0 + BG 30 2 × 0.5 + BG 30 + BG 60 2 × 0.5 + BG 60 + BG 120 2 × 1 ,

where BG represents the blood glucose concentration recorded at 0, 30, 60, and 120-min time intervals.

2.8 Experimental design for in vivo anti-diabetic activity

Streptozotocin (50 mg/kg), freshly prepared in cold citrate buffer 0.1 M (pH 4.5), was administered by intraperitoneal injection to rats fasted overnight [43,44]. To avoid streptozotocin (STZ) provoked deadly hypoglycaemia, for the next 24 h, a 5% dextrose solution was given to rats after 6 h of streptozotocin (STZ) injection. STZ causes fatal hypoglycaemia due to huge pancreatic insulin discharge [45]. About 72 h after the injection of STZ, diabetes in rats was established by determining plasma glucose via the tail vein with a digital glucometer (MyLife Pura, Switzerland) by glucose oxidase-peroxidase method using the strip method. To stabilize plasma glucose levels, diabetic rats were maintained under optimal laboratory conditions for 2 weeks [43]. After 2 weeks of diabetes induction, plasma glucose level was once more ascertained, and rats with equal or more than 200 mg/dL blood glucose levels were chosen for further study. The rats in this study were arbitrarily divided into four groups, with six rats in each group (n = 6).

Group I: Normal control (1 mL/kg. b.w., 0.5% carboxymethyl cellulose in water, orally)

Group II: STZ (Toxic control given 50 mg/kg, b.w. orally)

Group III: streptozotocin (STZ) + Glib (5 mg/kg, b.w. orally) [46]

Group IV: streptozotocin (STZ) + ECbp (200 mg/kg, b.w. orally)

Glib, ECbp extract, and blank vehicle were fed orally to their respective rat groups for 21 days at 10.00 a.m. daily. Initially and every week (0, 7, 14, and 21 days), fasting plasma glucose levels and any change in the body weight of rats were estimated. At the termination of the third week, that is on 21st day, vehicle, ECbp, and Glib were given to the night-long fasted rats, and 1-h after treatment, all rats were anaesthetized with chloroform. Plasma samples were drawn through retro-orbital plexus penetration for biochemical analyses.

2.9 Biochemical studies

Serum glucose levels were estimated using a glucometer. Commercially available diagnostic kits were used to estimate serum lipid profiles, including triglyceride (TG), high-density lipoprotein (HDL), and total cholesterol (TC). Friedewald’s formula was used to determine the serum very low-density lipoprotein (VLDL) and low-density lipoprotein (LDL) concentrations as follows:

V -LDL = Triglycerides / 5 ,

LDL = TC − ( HDL + VLDL ) .

A semi-autoanalyzer (Photometer 5010V5+, Germany) was used to determine all the biochemical parameters.

2.10 Isolation of compounds

ECbp (135 g) was subjected to column chromatography (52″:2.5″) over a silica gel (200–400 mesh, 200 g) bed using hexane as the eluent with increasing amounts of ethyl acetate. Individual 100 mL fractions were collected, and similar fractions were pooled after monitoring the TLC by using anisaldehyde-sulphuric acid reagent as a visualizing agent, which was prepared by adding 0.5 mL of anisaldehyde and 10 mL of glacial acetic acid to 85 mL of methanol and 5 ml of concentrated sulphuric acid, in that order. The development and elution of the column were performed with successive sequences of solvents in many combinations, hexane–ethyl acetate ([95:05] three fractions each of 100 mL, 95:05 [7 frs.], 95:05 [6 frs.], 90:10 [6 frs.] v/v), which yielded 22 fractions (Frs. A-V). The first three fractions (A-C) were pooled after monitoring by TLC, which showed a prominent single spot and was labelled as compound ECbp-1. Similarly, on the basis of TLC, fractions Q–V were pooled and showed similar single spot and was labelled as ECbp-2.

2.11 Statistical assessment

The data were expressed as mean ± SD, and were assessed by one-way analysis of variance. For multiple comparisons, Dunnett’s test was applied using Graphpad Prism version 5.0, and p values < 0.05 were considered statistically significant.

3 Results and discussion

The percentage yield of ECbp extract was 9.4% (348.6 g). ECbp and acarbose were tested in the concentration range of 0.15–5 mg/mL for in vitro inhibition assay of α-amylase and α-glucosidase. The IC50 values, which represent the concentration required to inhibit 50% of enzyme activity for α-amylase and α-glucosidase in acarbose were 0.46 ± 0.02 and 1.98 ± 0.08, respectively. For ECbp, they were 4.28 ± 0.81 and 2.57 ± 0.89 for α-amylase and α-glucosidase, respectively (Table 1 and Figure 1).

Table 1

α-Amylase and α-glucosidase % inhibition by standard acarbose and ECbp

Conc. (mg/mL) Acarbose ECbp
α-Amylase α-Glucosidase α-Amylase α-Glucosidase
0.150 31.29 ± 4.35 16.81 ± 2.76 7.20 ± 1 9.72 ± 1.92
0.310 46.74 ± 4.18 28.94 ± 2.67 11.31 ± 2.1 14.97 ± 1.99
0.620 54.51 ± 2.61 39.44 ± 3.35 14.35 ± 1.34 21.55 ± 5.01
1.250 61.64 ± 4.21 51.24 ± 2.49 26.44 ± 4.87 35.44 ± 6.22
2.500 74.27 ± 3.02 63.82 ± 5.88 32.96 ± 6.4 49.32 ± 3.42
5.000 81.33 ± 2.31 76.82 ± 4.49 56.02 ± 4.52 62.92 ± 6.51
IC50 0.46 ± 0.02 1.98 ± 0.08 4.28 ± 0.81 2.57 ± 0.89
Figure 1 α-Amylase and α-glucosidase enzyme inhibition ability of acarbose and ECbp.
Figure 1

α-Amylase and α-glucosidase enzyme inhibition ability of acarbose and ECbp.

3.1 Acute toxicity study

ECbp at a dose of 2,000 mg/kg in rats after oral administration did not produce any signs of toxicity, and no fatality was observed for up to 14 days. The results of this toxicity test revealed that up to an oral dose of 2,000 mg/kg b.w. ECbp was nontoxic. Therefore, 1/10th of 2,000 mg/kg b.w., which is equal to 200 mg/kg b.w. dose was selected for determining the activity.

3.2 Effect of ECbp on plasma glucose of glucose-challenged rats

A significant (p < 0.001) increase in blood glucose levels was observed after STZ administration in rats compared with that in normal control rats. ECbp at a dose of 200 mg/kg b.w. and Glib (5 mg/kg b.w.) via oral treatment led to a significant decrease in blood glucose level (p < 0.001) in the diabetic rats compared to those in the diabetic control group rats (Figure 2).

Figure 2 Effect of ECbp extract on blood glucose levels in glucose-challenged rats. Data represented as mean ± SD, n = 6; BGL: blood glucose level; NC: normal control; GlC: glucose control; Glib: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris.
Figure 2

Effect of ECbp extract on blood glucose levels in glucose-challenged rats. Data represented as mean ± SD, n = 6; BGL: blood glucose level; NC: normal control; GlC: glucose control; Glib: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris.

At a dose of 200 mg/kg b.w., ECbp extract treatment exhibited a reduction trend in the plasma glucose levels from 83, 105.4, 100.5, 96.8, and 91.03 mg/dL at 0, 30, 60, 90, and 120 min, respectively, while as standard Glib (5 mg/kg, b.w.) exhibited a significant reduction trend in plasma glucose levels from 85.9, 112.5, 110,104.8, and 100.6 mg/dL after 0, 30, 60, 90, and 120 min, respectively. The toxic group showed 90.6, 127.8, 122.7, 116.2, and 109.4 mg/dL after 0, 30, 60, 90, and 120 min, respectively (Figure 2).

The percentage reduction in AUC by ECbp (200 mg/kg, b.w) in glucose-fed rats was found to be 9.76% compared to the standard Glib (32.73%). ECbp leads to decreases in AUC and was comparable to that of Glib (Figure 3).

Figure 3 Effect of ECbp on AUC of blood glucose levels of glucose-challenged diabetic rats. Data represented as mean ± SD; NC: normal control; GlC; glucose control; Acar: acarbose; Glbn: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris. aGlucose-challenged control GlC vs normal control; btreated group vs glucose-challenged control; *p < 0.05, **p < 0.01.
Figure 3

Effect of ECbp on AUC of blood glucose levels of glucose-challenged diabetic rats. Data represented as mean ± SD; NC: normal control; GlC; glucose control; Acar: acarbose; Glbn: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris. aGlucose-challenged control GlC vs normal control; btreated group vs glucose-challenged control; *p < 0.05, **p < 0.01.

3.3 Effect on plasma glucose levels and body weight

The effect of 21 days of ECbp treatment on fasting blood glucose (FBG) in diabetic rats was studied (Table 2, Figure 4). STZ (50 mg/kg, b.w., i.p.) successfully induced diabetes and significantly (p < 0.01) increased fasting blood glucose (FBG) compared with normal control rats. Treatment with ECbp (200 mg/kg, b.w., p.o) showed a significant (p < 0.05) decrease in the FBG levels on the 21st day compared to that in diabetic control rats (Figure 4). The decrease in FBG was significantly (p < 0.01) enhanced by ECbp (42.74%) after 21 days treatment compared to the toxic control (STZ), while Glib (5 mg/kg, b.w) showed 53.91% reduction in FBG compared to toxic control after 21 days treatment.

Table 2

Effect of 21 days treatment of ECbp (200 mg/kg b.w.) on plasma glucose levels in diabetic rats

Treatment groups Fasting plasma glucose level (mg/dL) % Increase in FBG vs NC % Reduction in FBG vs toxic
0 day 7 day 14 day 21 day
NC 89.4 ± 3.64 91.6 ± 3.78 92.0 ± 4.84 91.4± 3.13 100 —
DC (STZ) 217 ± 4.52a** 221.8 ± 5.1a** 219.8 ± 6.18a** 217.6 ± 9.02a** 138.07 100
STZ + Glbn 211.4 ± 5.94 179.2 ± 2.27b* 146.2 ± 4.54b** 100.3 ± 3.16b** 9.74 53.91
STZ + ECbp 212.6 ± 6 188.2 ± 6.48b* 159.1 ± 3.55b* 124.6 ± 3.56b** 36.32 42.74

Data as presented as mean ± SD, n = 6; FPG: fasting plasma glucose: STZ: streptozotocin; Glbn: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris; aDiabetic control versus normal control, bTreated group versus diabetic control, * p < 0.05, ** p < 0.01.

Figure 4 Effect of 21 days treatment with ECbp (200 mg/kg b.w.) on plasma glucose in STZ-induced diabetic rats. C. bursa-pastoris (ECbp) ethanol extract at 0.2 g/kg, b.w, dose for 3 weeks in rats prevented the weight loss of rats (p < 0.05) compared to that in diabetic control. A notable (p < 0.001) reduction in the average body weight with feeding STZ was noticed in diabetic rats compared to that in normal control rats (Figure 5). In diabetic rats, treatment with ECbp and Glib significantly (p < 0.01 and p < 0.01) increased body weight compared to diabetic control rats.
Figure 4

Effect of 21 days treatment with ECbp (200 mg/kg b.w.) on plasma glucose in STZ-induced diabetic rats. C. bursa-pastoris (ECbp) ethanol extract at 0.2 g/kg, b.w, dose for 3 weeks in rats prevented the weight loss of rats (p < 0.05) compared to that in diabetic control. A notable (p < 0.001) reduction in the average body weight with feeding STZ was noticed in diabetic rats compared to that in normal control rats (Figure 5). In diabetic rats, treatment with ECbp and Glib significantly (p < 0.01 and p < 0.01) increased body weight compared to diabetic control rats.

Figure 5 Effect of ECbp on average body weight of diabetic rats. Data are presented as mean ± SD, n = 6, NC: normal control (1 mL/kg b.w. of 0.5% CMC in distilled water); DC: diabetic control (STZ, 50 mg/kg, b.w., i.p.); Glbn: glibenclamide (5 mg/kg, b.w); ECbp: ethanol extract of C. bursa-pastoris; *p < 0.05.
Figure 5

Effect of ECbp on average body weight of diabetic rats. Data are presented as mean ± SD, n = 6, NC: normal control (1 mL/kg b.w. of 0.5% CMC in distilled water); DC: diabetic control (STZ, 50 mg/kg, b.w., i.p.); Glbn: glibenclamide (5 mg/kg, b.w); ECbp: ethanol extract of C. bursa-pastoris; *p < 0.05.

3.4 Effect on serum lipid profile

Treatment with the ECbp extract for 21 days at a dose of 0.2 g/kg, b.w. notably reduced the elevated levels of all cholesterols, viz., TC, LDL-C, VLDL-C, and TGs, significantly (p < 0.05) compared to diabetic control. However, the HDL-cholesterol levels were significantly (p < 0.01) increased compared to diabetic control rats. In the Glib-treated rat group, significantly (p < 0.01) reduced elevated levels of all these cholesterol levels were observed (Figure 6). Additionally, a significant reduction in atherogenic index was also found (p < 0.01) in the ECbp treatment group and produced a pronounced normalization of lipid profile significantly (p < 0.05) compared to the diabetic control. Also, the HDL-cholesterol levels were significantly increased (p < 0.01) compared to the diabetic control, besides improvement in the atherogenic index (Figure 7).

Figure 6 Effect of 3 weeks treatment of ECbp (0.2 g/kg b.w) on the lipid profile of diabetic rats. Data are presented as mean ± SD, n = 6. NC: normal control; DC: diabetic control; Glbn: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris. aDiabetic control vs Blank control, btreated group vs diabetic control, ns p > 0.05, * p < 0.05, ** p < 0.01.
Figure 6

Effect of 3 weeks treatment of ECbp (0.2 g/kg b.w) on the lipid profile of diabetic rats. Data are presented as mean ± SD, n = 6. NC: normal control; DC: diabetic control; Glbn: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris. aDiabetic control vs Blank control, btreated group vs diabetic control, ns p > 0.05, * p < 0.05, ** p < 0.01.

Figure 7 Effect of 3 weeks treatment of ECbp (0.2 g/kg b.w) on the atherogenic index. Data are expressed as mean ± SD, n = 6. NC: normal control; DC: diabetic control; Glbn: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris.
Figure 7

Effect of 3 weeks treatment of ECbp (0.2 g/kg b.w) on the atherogenic index. Data are expressed as mean ± SD, n = 6. NC: normal control; DC: diabetic control; Glbn: glibenclamide; ECbp: ethanol extract of C. bursa-pastoris.

3.5 Isolated compounds from ECbp

ECbp-1 (109 mg) was obtained as a white crystalline mass, melting point 192 ± 5°C from hexane–ethyl acetate (95:5 v/v) eluent.

1H NMR: (CDCl3, 300 MHz): δ H 5.68 (1H, dd, J = 11.2, 3.9 Hz, H = 11), 5.33 (1H, d, J = 4.8, H-12), 4.15 (2H, d, J = 7.2 Hz, H-28), 4.08 (2H, d, J = 6.9 H-21), 3.45 (1H, s, OH), 2.82 (1H, dd, J = 4.8, 11.1 Hz, H-7), 1.27 (3H, s, H-29), 1.18 (3H, s, H-19), 0.97 (3H, s, H-18), 0.87 (3H, d, J = 6.6 Hz, H-27), 0.83 (3H, d, J = 6.6 Hz, H-26)

13C NMR: (CDCl3, 75 MHz): δ C 33.9 (C-1), 29.6 (C-2), 34.0 (C-3), 40.5 (C-4), 50.3 (C-5), 22.5 (C-6), 68.8 (C-7), 26.8 (C-8), 41.2 (C-9), 34.2 (C-10), 130.0 (C-11), 127.6 (C-12), 34.4 (C-13), 36.0 (C-14), 20.7 (C-15), 22.4 (C-16), 34.5 (C-17), 11.2 (C-18), 18.5 (C-19), 33.7 (C-20), 60.2 (C-21), 31.4 (C-22), 29.3 (C-23), 29.2 (C-24), 28.9 (C-25),13.9 (C-26), 14.0 (C-27), 62.0 (C-28), 20.7 (C-29), 170.9 (C-30)

+ve ESI-MS m/z (rel. int.): 490 [M]+ C30H50O5 (29), 489 [M-H]+ (100), 445 [M-CO2]+ (3)

Compound ECbp-2 (73 mg) was obtained as an orange-coloured shining waxy mass with a melting point 171 ± 5°C from the ethanol fraction using hexane:ethylacetate (85:15 v/v) as an eluent. On the basis of 13C NMR and MS, the molecular mass of ECbp-2 was established at m/z 332. Its ESI-MS spectrum displayed a pseudomolecular ion peak at m/z 333, corresponding to the molecular formula C20H29O4 [M + H]+ of a diterpenoic acid. The formula indicated the presence of seven double bond equivalents, four of which were attributed to four vinylic linkages, two to a bicyclic carbon framework of a clerodane moiety, and the remaining one to a carboxylic group.

1H NMR: (CDCl3, 300 MHz): δ H 6.20 (1H, d, J = 6.5 Hz, H-11), 5.41 (4H, brm, H-3, H-6, H-7, H-12), 3.63 (1H, dt, J = 6.0, 6.9 Hz, H-2), 4.14 (2H, brs, H-20), 2.80 (1H, m, H-13), 1.63 (2H, m, H-1), 1.33 (6H, s, H-17, H-19), 1.03 (2H, m, H-14), 1.25 (3H, s, H-18), 0.87 (3H, t, J = 6.5 Hz, H-15).

13C NMR: (CDCl3, 125 MHz): δ C 39.8 (C-1), 62.3 (C-2), 127.1 (C-3), 131.9 (C-4), 39.3 (C-5), 130.2 (C-6), 128.3 (C-7), 128.2 (C-8), 145.2 (C-9), 37.3 (C-10), 127.7 (C-11), 127.1 (C-12), 50.6 (C-13) 23.1 (C-14), 14.1 (C-15), 179.0 (C-16), 20.5 (C-17), 22.6 (C-18), 19.4 (C-19), 65.0 (C-20).

ESI-MS m/z (rel. int.): 333 [M + H]+ C20H29O4(10), 275(8) 7,21,28-trihydroxy-lanosta-11-en-30-oic acid 2,20-dihydroxy-cleroda-3, 6, 8, 11-tetraen-16-oic acid.

3.6 α-Amylase and α-glucosidase inhibition assays

In vitro α-amylase and α-glucosidase inhibition assays were carried out on ECbp-1, ECbp-2, and acarbose in the concentration range of 0.15 to 5 mg/mL. The compounds showed strong inhibition of both the carbohydrate-digesting enzymes in a concentration-dependent manner (Figure 8).

Figure 8 α-Amylase and α-glucosidase inhibition ability of acarbose, ECbp-1, and ECbp-2.
Figure 8

α-Amylase and α-glucosidase inhibition ability of acarbose, ECbp-1, and ECbp-2.

The use of herbal remedies by humans has been well documented for thousands of years. Two ethnic systems of alternative medicine, i.e. Ayurveda and Unani, document various crude drug formulations for the management of numerous ailments. These remedies contain a variety of extracts from different herbs [43], and various herbs have been part of traditional remedies in several cultures as a remedial choice against diabetes mellitus worldwide [47]. Although several oral and systemic anti-diabetic treatment options are available in the market, the need for natural anti-diabetic drug options is increasing [48,49]. The main action of α-amylase and α-glucosidase is the hydrolysis of carbohydrates into monosaccharide glucose. α-Amylase controls the hydrolysis of polysaccharide-starch, which leads to glucose prior to systemic entry [50]. Inhibition of α-amylase can cause a decline in postprandial high glucose levels. The presence of α-glucosidase in the small intestine is responsible for the production of glucose via disaccharide hydrolysis. Numerous phytoconstituents exist in the plant kingdom and possess α-glucosidase inhibition potential [37]. ECbp is a generous example with both α-amylase and α-glucosidase inhibitory potential, which leads to the minimum absorption of monosaccharide-glucose. The inhibition of both of these enzymes avoids the abrupt upsurge in postprandial hyperglycaemia and plays a dominant role in the management of DM; thus, targeting α-glucosidase and α-amylase inhibition may be a challenging goal to control the sudden rise in hyperglycaemia [51]. The results obtained in this study agree with those of a number of other studies [52,53]. Numerous medicinal plants and their different parts can reduce the plasma glucose concentration. This ability is due to the tannins, terpenoids, and flavonoids present in these herbs, which have been evaluated for their potential to inhibit α-amylase and α-glucosidase [54]. The α-amylase and α-glucosidase inhibitory actions of terpenoids, tannins, and flavonoids from plants have also been well documented. The α-amylase suppressing capacity of tannins was attributed to their ability to combine with carbohydrates and proteins [55]. Some examples of terpenes possessing action against DM are stevioside and its aglucon Steviol from Stevia rebaudiana, bassic acid, from Bumelia sartorum, trans-dehydrocrotonin from Croton cajucara, D-limonene from citrus fruits, rebaudioside from Stevia rebaudiana lupeol from mango, alpha-amyrin from Ficus bengalensis, Betulin from Euclea undulata, tinosporaside from Tinospora cordifolia, lactucain A from Lactuca indica, urosolic acid from Rosmarinus officinalis, and palbinone from Moutan cortex [30].

In this study, inhibition of both enzymes was concentration-dependent by both ECbp and acarbose (Table 1). This was also evidenced by comparing their IC50 values (Figure 1). ECbp inhibited α-glucosidase (IC50 = 2.57 ± 0.89) more effectively than α-amylase (IC50 = 4.28 ± 0.81) as compared to the standard drug acarbose with α-amylase (IC50 = 0.46 ± 0.02) and α-glucosidase (IC50 = 1.98 ± 0.08). The research proposes that rats treated with streptozotocin target damage to insulin-secreting β-cells of the pancreas, thereby producing a diabetic condition. Insufficient levels of insulin further result in the inability of cells to use glucose, resulting in the formation of reactive oxygen species [56]. Additionally, these experimental rats demonstrate various diabetic malfunctions, such as cardiomyopathy, retinopathy, and nephropathy, which mainly develop through oxidative stress-induced mechanisms [3]. Body weight drop due to the disproportion of metabolic pathways is normally linked to DM [57]. In the current study, diabetic rats treated with ECbp gained significant weight, most likely due to repealing glycogenolysis and gluconeogenesis, thereby helping to restore normal metabolic pathways [58]. ECbp at a dose of 0.2 g/kg, b.w for 21 days in rats prevented the weight loss (p < 0.05) compared to the diabetic control. In this study, a significant (p < 0.001) reduction in body weight was observed in diabetic rats (STZ) compared with that in normal control rats (Figure 5). In diabetic rats, ECbp treatment and Glib significantly (p < 0.01 and p < 0.01) showed increased body weight compared to the diabetic control rats. In contrast, an abnormal lipid profile was observed in diabetic rats compared to the normal group. This may be due to an imbalance in the various metabolic and regulatory pathways that have developed, which is mainly due to the deficiency of insulin [59]. Treatment with the ECbp at 0.2 g/kg, b.w. decreased the elevated levels of all cholesterols (TC, LDL-C, and VLDL-C) and TGs significantly (p < 0.05), whereas the HDL-cholesterol levels were significantly (p < 0.01) increased compared to diabetic control. On the other hand, Glib treatment also significantly (p < 0.01) reduced elevated levels of all TC, LDL-C, and VLDL-C and TGs (Figure 6). An improvement in the atherogenic index was also observed after treatment with ECbp (Figure 7).

Based on 13C NMR and MS details, the molecular weight of ECbp-1 was found to be m/z 490, consistent with the molecular formula C30H50O5. It showed the presence of six double-bond equivalents, four of which were present in the tetracyclic carbon framework of lanostane and one each in a carboxylic group and vinylic linkage. The 1H NMR band of ECbp-1 exhibited two downfield signals at δ values of 5.68 (dd, J = 11.2, 3.9 Hz) and 5.33 (d, J = 4.8 Hz) ascribed to H-11 and H-12 vinylic protons, respectively. Two doublets at δ 4.15 (J = 7.2 Hz) and 4.08 (J = 6.9 Hz), each assimilating for two protons, were attributed to H-26 and H-21 hydroxymethyl protons, respectively. A double doublet at δ 2.82 (J = 4.8, 11.1 Hz) was assigned to the H-7 carbinol proton. The methyl protons appearing at δ 1.27 (s, H-29), 1.23 (s, H-28), 1.18 (s, H-19), 0.97 (s, H-18), and 0.87 (d, J = 6.6 Hz, H-27) supported the presence of lanostane nucleus. This was further confirmed by the presence of 30 signals in the 13C NMR spectrum. Prominent signals appeared for carboxylic carbon at δ 170.9 (C-30); vinylic carbon at δ 130.0 (C-11) and 127.6 (C-12); hydroxymethyl carbons at δ 60.2 (C-21) and 62.0 (C-26); and carbinol carbon at δ 68.8 (C-7). The NMR data were compared to those in earlier reports [60]. On the basis of the above discussion, the structure of ECbp-1 was elucidated as 7,21,28-trihydroxy-lanosta-11-en-30-oic acid (Figure 9).

Figure 9 Structures of ECbp-1 and ECbp-2.
Figure 9

Structures of ECbp-1 and ECbp-2.

The 1H NMR band of ECbp-2 showed two downfield signals at δ 6.20 (1H, d, J = 6.5 Hz, H-11) and 5.41 (4H, m, H-3, H-6, H-7, H-12) for vinylic protons. A double-triplet at δ 3.63 (J = 6.0, 6.9 Hz) was assigned to the H-2 carbinol proton. A two-proton broad singlet at δ 4.14 was assigned to hydroxymethyl protons (H-20). Two singlets at δ 1.33 (6H), 1.25 (3H), and a triplet at δ 0.87 (3H), attributable to H-17, H-19, H-18, and H-15 methyl protons, supported the presence of clerodane moiety. Further evidence supporting the proposed structure is derived from the 13C NMR spectrum. ECbp-2 13C NMR band exhibited signals for carboxylic carbon at δ 179.0 (C-16); vinylic carbons at δ 127.1–131.9; and hydroxylated carbons at δ 62.3 (C-2) and 65.0 (C-20). The positions of the vinylic linkages, hydroxyl groups, and carboxylic function were established on the basis of the HMBC experiment. It displays key interactions between C-16 and H-13/H-15; C-3 and H-2/H-19; and C-8 and H-17/H-12. The NMR data of ECbp-2 were compared with the reported data for clerodane derivatives and found to be in good agreement [61]. Based on this analysis, the most likely structure of ECbp-2 was confirmed to be 2,20-dihydroxy-cleroda-3,6,8,11-tetraen-16-oic acid (Figure 9).

4 Conclusions

As indicated by the WHO, more than 176 million individuals worldwide experience diabetes, and this number is rising very fast; it is estimated that by the year 2030, this number will be twofold. Traditionally used herbs should be thoroughly studied because of the lack of side effects, as suggested by the WHO Expert Committee on Diabetes. Our study on C. bursa-pastoris ethanol extract showed promising results in improving serum glucose and lipid levels in STZ-induced diabetic rats, in addition to significant in vitro inhibition of carbohydrate digesting enzymes (α-amylase and α-glucosidase) responsible for postprandial hyperglycaemia in diabetic rats. Also, two potent compounds, a triterpene 7,21,28-trihydroxy-lanosta-11-en-30-oic acid (ECbp-1) and a diterpene 2,20-dihydroxy-cleroda-3,6,8,11-tetraen-16-oic acid (ECbp-2), showing promising inhibitory potential towards a-amylase and a-glucosidase enzymes were isolated from ECbp. Hence, it may be concluded that ECbp-1 and ECbp-2 are responsible for the anti-diabetic effect of the ECbp. In the future, an in vivo study will be conducted to prove and support the in vitro results of the isolated ECbp-1 and ECbp-2 terpenes.

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Acknowledgements

The authors are highly thankful to the “Researchers Supporting Project” number (RSPD2024R981), King Saud University, Riyadh, Saudi Arabia, for supporting this study and funding the research work. Besides authors are highly thankful to the University Grants Commission for providing “Basic Scientific Research (BSR) fellowship” to Mohd Akbar Dar.

  1. Funding information: The authors are highly thankful to the “Researchers Supporting Project” number (RSPD2024R981), King Saud University, Riyadh, Saudi Arabia, for supporting this study and funding the research work.

  2. Author contributions: Conceptualization: M.A.D. and M.H.M.; methodology: M.A.D, M.H.M., and S.A.; software: M.A.D. and M.H.M.; validation: M.A.D., M.H.M., S.A.M., and S.A.; formal analysis: M.A.D. and S.A.M.; investigation: M.A.D., M.H.M., and S.A.M.; resources: M.A.D.; data curation: M.A.D., M.H.M., and S.A.M.; writing–original draft preparation: M.A.D., N.A.S., and M.H.M.; writing–review and editing: M.D.D., N.A.S., and M.H.M.; funding acquisition: N.A.S. and R.A.M. All authors have read and agreed to the published version of the manuscript.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Ethical approval: Under approval (No. F-IAEC (Pharm. Sc.) APPROVAL/2013/20), Institutional Animal Ethics Committee (IAEC), Department of Pharmaceutical Sciences, University of Kashmir, Hazratbal, Srinagar, India granted approval for this experimental study.

  5. Data availability statement: The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Received: 2024-03-05
Revised: 2024-04-02
Accepted: 2024-04-06
Published Online: 2024-05-24

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Articles in the same Issue

  1. Regular Articles
  2. Porous silicon nanostructures: Synthesis, characterization, and their antifungal activity
  3. Biochar from de-oiled Chlorella vulgaris and its adsorption on antibiotics
  4. Phytochemicals profiling, in vitro and in vivo antidiabetic activity, and in silico studies on Ajuga iva (L.) Schreb.: A comprehensive approach
  5. Synthesis, characterization, in silico and in vitro studies of novel glycoconjugates as potential antibacterial, antifungal, and antileishmanial agents
  6. Sonochemical synthesis of gold nanoparticles mediated by potato starch: Its performance in the treatment of esophageal cancer
  7. Computational study of ADME-Tox prediction of selected phytochemicals from Punica granatum peels
  8. Phytochemical analysis, in vitro antioxidant and antifungal activities of extracts and essential oil derived from Artemisia herba-alba Asso
  9. Two triazole-based coordination polymers: Synthesis and crystal structure characterization
  10. Phytochemical and physicochemical studies of different apple varieties grown in Morocco
  11. Synthesis of multi-template molecularly imprinted polymers (MT-MIPs) for isolating ethyl para-methoxycinnamate and ethyl cinnamate from Kaempferia galanga L., extract with methacrylic acid as functional monomer
  12. Nutraceutical potential of Mesembryanthemum forsskaolii Hochst. ex Bioss.: Insights into its nutritional composition, phytochemical contents, and antioxidant activity
  13. Evaluation of influence of Butea monosperma floral extract on inflammatory biomarkers
  14. Cannabis sativa L. essential oil: Chemical composition, anti-oxidant, anti-microbial properties, and acute toxicity: In vitro, in vivo, and in silico study
  15. The effect of gamma radiation on 5-hydroxymethylfurfural conversion in water and dimethyl sulfoxide
  16. Hollow mushroom nanomaterials for potentiometric sensing of Pb2+ ions in water via the intercalation of iodide ions into the polypyrrole matrix
  17. Determination of essential oil and chemical composition of St. John’s Wort
  18. Computational design and in vitro assay of lantadene-based novel inhibitors of NS3 protease of dengue virus
  19. Anti-parasitic activity and computational studies on a novel labdane diterpene from the roots of Vachellia nilotica
  20. Microbial dynamics and dehydrogenase activity in tomato (Lycopersicon esculentum Mill.) rhizospheres: Impacts on growth and soil health across different soil types
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  27. pH-based colorimetric detection of monofunctional aldehydes in liquid and gas phases
  28. Investigating the effect of resveratrol on apoptosis and regulation of gene expression of Caco-2 cells: Unravelling potential implications for colorectal cancer treatment
  29. Metformin inhibits knee osteoarthritis induced by type 2 diabetes mellitus in rats: S100A8/9 and S100A12 as players and therapeutic targets
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https://doi.org/10.1515/chem-2024-0025
Keywords for this article
Capsella bursa-pastoris; terpenes; antidiabetic; α-amylase; streptozotocin; α-glucosidase
Creative Commons
BY 4.0

Articles in the same Issue

  1. Regular Articles
  2. Porous silicon nanostructures: Synthesis, characterization, and their antifungal activity
  3. Biochar from de-oiled Chlorella vulgaris and its adsorption on antibiotics
  4. Phytochemicals profiling, in vitro and in vivo antidiabetic activity, and in silico studies on Ajuga iva (L.) Schreb.: A comprehensive approach
  5. Synthesis, characterization, in silico and in vitro studies of novel glycoconjugates as potential antibacterial, antifungal, and antileishmanial agents
  6. Sonochemical synthesis of gold nanoparticles mediated by potato starch: Its performance in the treatment of esophageal cancer
  7. Computational study of ADME-Tox prediction of selected phytochemicals from Punica granatum peels
  8. Phytochemical analysis, in vitro antioxidant and antifungal activities of extracts and essential oil derived from Artemisia herba-alba Asso
  9. Two triazole-based coordination polymers: Synthesis and crystal structure characterization
  10. Phytochemical and physicochemical studies of different apple varieties grown in Morocco
  11. Synthesis of multi-template molecularly imprinted polymers (MT-MIPs) for isolating ethyl para-methoxycinnamate and ethyl cinnamate from Kaempferia galanga L., extract with methacrylic acid as functional monomer
  12. Nutraceutical potential of Mesembryanthemum forsskaolii Hochst. ex Bioss.: Insights into its nutritional composition, phytochemical contents, and antioxidant activity
  13. Evaluation of influence of Butea monosperma floral extract on inflammatory biomarkers
  14. Cannabis sativa L. essential oil: Chemical composition, anti-oxidant, anti-microbial properties, and acute toxicity: In vitro, in vivo, and in silico study
  15. The effect of gamma radiation on 5-hydroxymethylfurfural conversion in water and dimethyl sulfoxide
  16. Hollow mushroom nanomaterials for potentiometric sensing of Pb2+ ions in water via the intercalation of iodide ions into the polypyrrole matrix
  17. Determination of essential oil and chemical composition of St. John’s Wort
  18. Computational design and in vitro assay of lantadene-based novel inhibitors of NS3 protease of dengue virus
  19. Anti-parasitic activity and computational studies on a novel labdane diterpene from the roots of Vachellia nilotica
  20. Microbial dynamics and dehydrogenase activity in tomato (Lycopersicon esculentum Mill.) rhizospheres: Impacts on growth and soil health across different soil types
  21. Correlation between in vitro anti-urease activity and in silico molecular modeling approach of novel imidazopyridine–oxadiazole hybrids derivatives
  22. Spatial mapping of indoor air quality in a light metro system using the geographic information system method
  23. Iron indices and hemogram in renal anemia and the improvement with Tribulus terrestris green-formulated silver nanoparticles applied on rat model
  24. Integrated track of nano-informatics coupling with the enrichment concept in developing a novel nanoparticle targeting ERK protein in Naegleria fowleri
  25. Cytotoxic and phytochemical screening of Solanum lycopersicum–Daucus carota hydro-ethanolic extract and in silico evaluation of its lycopene content as anticancer agent
  26. Protective activities of silver nanoparticles containing Panax japonicus on apoptotic, inflammatory, and oxidative alterations in isoproterenol-induced cardiotoxicity
  27. pH-based colorimetric detection of monofunctional aldehydes in liquid and gas phases
  28. Investigating the effect of resveratrol on apoptosis and regulation of gene expression of Caco-2 cells: Unravelling potential implications for colorectal cancer treatment
  29. Metformin inhibits knee osteoarthritis induced by type 2 diabetes mellitus in rats: S100A8/9 and S100A12 as players and therapeutic targets
  30. Effect of silver nanoparticles formulated by Silybum marianum on menopausal urinary incontinence in ovariectomized rats
  31. Synthesis of new analogs of N-substituted(benzoylamino)-1,2,3,6-tetrahydropyridines
  32. Response of yield and quality of Japonica rice to different gradients of moisture deficit at grain-filling stage in cold regions
  33. Preparation of an inclusion complex of nickel-based β-cyclodextrin: Characterization and accelerating the osteoarthritis articular cartilage repair
  34. Empagliflozin-loaded nanomicelles responsive to reactive oxygen species for renal ischemia/reperfusion injury protection
  35. Preparation and pharmacodynamic evaluation of sodium aescinate solid lipid nanoparticles
  36. Assessment of potentially toxic elements and health risks of agricultural soil in Southwest Riyadh, Saudi Arabia
  37. Theoretical investigation of hydrogen-rich fuel production through ammonia decomposition
  38. Biosynthesis and screening of cobalt nanoparticles using citrus species for antimicrobial activity
  39. Investigating the interplay of genetic variations, MCP-1 polymorphism, and docking with phytochemical inhibitors for combatting dengue virus pathogenicity through in silico analysis
  40. Ultrasound induced biosynthesis of silver nanoparticles embedded into chitosan polymers: Investigation of its anti-cutaneous squamous cell carcinoma effects
  41. Copper oxide nanoparticles-mediated Heliotropium bacciferum leaf extract: Antifungal activity and molecular docking assays against strawberry pathogens
  42. Sprouted wheat flour for improving physical, chemical, rheological, microbial load, and quality properties of fino bread
  43. Comparative toxicity assessment of fisetin-aided artificial intelligence-assisted drug design targeting epibulbar dermoid through phytochemicals
  44. Acute toxicity and anti-inflammatory activity of bis-thiourea derivatives
  45. Anti-diabetic activity-guided isolation of α-amylase and α-glucosidase inhibitory terpenes from Capsella bursa-pastoris Linn.
  46. GC–MS analysis of Lactobacillus plantarum YW11 metabolites and its computational analysis on familial pulmonary fibrosis hub genes
  47. Green formulation of copper nanoparticles by Pistacia khinjuk leaf aqueous extract: Introducing a novel chemotherapeutic drug for the treatment of prostate cancer
  48. Improved photocatalytic properties of WO3 nanoparticles for Malachite green dye degradation under visible light irradiation: An effect of La doping
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  50. Groundwater quality and health risk assessment of nitrate and fluoride in Al Qaseem area, Saudi Arabia
  51. A comparative study of the antifungal efficacy and phytochemical composition of date palm leaflet extracts
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  71. Identification and in silico screening of natural phloroglucinols as potential PI3Kα inhibitors: A computational approach for drug discovery
  72. Exploring the phytochemical profile and antioxidant evaluation: Molecular docking and ADMET analysis of main compounds from three Solanum species in Saudi Arabia
  73. Unveiling the molecular composition and biological properties of essential oil derived from the leaves of wild Mentha aquatica L.: A comprehensive in vitro and in silico exploration
  74. Analysis of bioactive compounds present in Boerhavia elegans seeds by GC-MS
  75. Homology modeling and molecular docking study of corticotrophin-releasing hormone: An approach to treat stress-related diseases
  76. LncRNA MIR17HG alleviates heart failure via targeting MIR17HG/miR-153-3p/SIRT1 axis in in vitro model
  77. Development and validation of a stability indicating UPLC-DAD method coupled with MS-TQD for ramipril and thymoquinone in bioactive SNEDDS with in silico toxicity analysis of ramipril degradation products
  78. Biosynthesis of Ag/Cu nanocomposite mediated by Curcuma longa: Evaluation of its antibacterial properties against oral pathogens
  79. Development of AMBER-compliant transferable force field parameters for polytetrafluoroethylene
  80. Treatment of gestational diabetes by Acroptilon repens leaf aqueous extract green-formulated iron nanoparticles in rats
  81. Development and characterization of new ecological adsorbents based on cardoon wastes: Application to brilliant green adsorption
  82. A fast, sensitive, greener, and stability-indicating HPLC method for the standardization and quantitative determination of chlorhexidine acetate in commercial products
  83. Assessment of Se, As, Cd, Cr, Hg, and Pb content status in Ankang tea plantations of China
  84. Effect of transition metal chloride (ZnCl2) on low-temperature pyrolysis of high ash bituminous coal
  85. Evaluating polyphenol and ascorbic acid contents, tannin removal ability, and physical properties during hydrolysis and convective hot-air drying of cashew apple powder
  86. Development and characterization of functional low-fat frozen dairy dessert enhanced with dried lemongrass powder
  87. Scrutinizing the effect of additive and synergistic antibiotics against carbapenem-resistant Pseudomonas aeruginosa
  88. Preparation, characterization, and determination of the therapeutic effects of copper nanoparticles green-formulated by Pistacia atlantica in diabetes-induced cardiac dysfunction in rat
  89. Antioxidant and antidiabetic potentials of methoxy-substituted Schiff bases using in vitro, in vivo, and molecular simulation approaches
  90. Anti-melanoma cancer activity and chemical profile of the essential oil of Seseli yunnanense Franch
  91. Molecular docking analysis of subtilisin-like alkaline serine protease (SLASP) and laccase with natural biopolymers
  92. Overcoming methicillin resistance by methicillin-resistant Staphylococcus aureus: Computational evaluation of napthyridine and oxadiazoles compounds for potential dual inhibition of PBP-2a and FemA proteins
  93. Exploring novel antitubercular agents: Innovative design of 2,3-diaryl-quinoxalines targeting DprE1 for effective tuberculosis treatment
  94. Drimia maritima flowers as a source of biologically potent components: Optimization of bioactive compound extractions, isolation, UPLC–ESI–MS/MS, and pharmacological properties
  95. Estimating molecular properties, drug-likeness, cardiotoxic risk, liability profile, and molecular docking study to characterize binding process of key phyto-compounds against serotonin 5-HT2A receptor
  96. Fabrication of β-cyclodextrin-based microgels for enhancing solubility of Terbinafine: An in-vitro and in-vivo toxicological evaluation
  97. Phyto-mediated synthesis of ZnO nanoparticles and their sunlight-driven photocatalytic degradation of cationic and anionic dyes
  98. Monosodium glutamate induces hypothalamic–pituitary–adrenal axis hyperactivation, glucocorticoid receptors down-regulation, and systemic inflammatory response in young male rats: Impact on miR-155 and miR-218
  99. Quality control analyses of selected honey samples from Serbia based on their mineral and flavonoid profiles, and the invertase activity
  100. Eco-friendly synthesis of silver nanoparticles using Phyllanthus niruri leaf extract: Assessment of antimicrobial activity, effectiveness on tropical neglected mosquito vector control, and biocompatibility using a fibroblast cell line model
  101. Green synthesis of silver nanoparticles containing Cichorium intybus to treat the sepsis-induced DNA damage in the liver of Wistar albino rats
  102. Quality changes of durian pulp (Durio ziberhinus Murr.) in cold storage
  103. Study on recrystallization process of nitroguanidine by directly adding cold water to control temperature
  104. Determination of heavy metals and health risk assessment in drinking water in Bukayriyah City, Saudi Arabia
  105. Larvicidal properties of essential oils of three Artemisia species against the chemically insecticide-resistant Nile fever vector Culex pipiens (L.) (Diptera: Culicidae): In vitro and in silico studies
  106. Design, synthesis, characterization, and theoretical calculations, along with in silico and in vitro antimicrobial proprieties of new isoxazole-amide conjugates
  107. The impact of drying and extraction methods on total lipid, fatty acid profile, and cytotoxicity of Tenebrio molitor larvae
  108. A zinc oxide–tin oxide–nerolidol hybrid nanomaterial: Efficacy against esophageal squamous cell carcinoma
  109. Research on technological process for production of muskmelon juice (Cucumis melo L.)
  110. Physicochemical components, antioxidant activity, and predictive models for quality of soursop tea (Annona muricata L.) during heat pump drying
  111. Characterization and application of Fe1−xCoxFe2O4 nanoparticles in Direct Red 79 adsorption
  112. Torilis arvensis ethanolic extract: Phytochemical analysis, antifungal efficacy, and cytotoxicity properties
  113. Magnetite–poly-1H pyrrole dendritic nanocomposite seeded on poly-1H pyrrole: A promising photocathode for green hydrogen generation from sanitation water without using external sacrificing agent
  114. HPLC and GC–MS analyses of phytochemical compounds in Haloxylon salicornicum extract: Antibacterial and antifungal activity assessment of phytopathogens
  115. Efficient and stable to coking catalysts of ethanol steam reforming comprised of Ni + Ru loaded on MgAl2O4 + LnFe0.7Ni0.3O3 (Ln = La, Pr) nanocomposites prepared via cost-effective procedure with Pluronic P123 copolymer
  116. Nitrogen and boron co-doped carbon dots probe for selectively detecting Hg2+ in water samples and the detection mechanism
  117. Heavy metals in road dust from typical old industrial areas of Wuhan: Seasonal distribution and bioaccessibility-based health risk assessment
  118. Phytochemical profiling and bioactivity evaluation of CBD- and THC-enriched Cannabis sativa extracts: In vitro and in silico investigation of antioxidant and anti-inflammatory effects
  119. Investigating dye adsorption: The role of surface-modified montmorillonite nanoclay in kinetics, isotherms, and thermodynamics
  120. Antimicrobial activity, induction of ROS generation in HepG2 liver cancer cells, and chemical composition of Pterospermum heterophyllum
  121. Study on the performance of nanoparticle-modified PVDF membrane in delaying membrane aging
  122. Impact of cholesterol in encapsulated vitamin E acetate within cocoliposomes
  123. Review Articles
  124. Structural aspects of Pt(η3-X1N1X2)(PL) (X1,2 = O, C, or Se) and Pt(η3-N1N2X1)(PL) (X1 = C, S, or Se) derivatives
  125. Biosurfactants in biocorrosion and corrosion mitigation of metals: An overview
  126. Stimulus-responsive MOF–hydrogel composites: Classification, preparation, characterization, and their advancement in medical treatments
  127. Electrochemical dissolution of titanium under alternating current polarization to obtain its dioxide
  128. Special Issue on Recent Trends in Green Chemistry
  129. Phytochemical screening and antioxidant activity of Vitex agnus-castus L.
  130. Phytochemical study, antioxidant activity, and dermoprotective activity of Chenopodium ambrosioides (L.)
  131. Exploitation of mangliculous marine fungi, Amarenographium solium, for the green synthesis of silver nanoparticles and their activity against multiple drug-resistant bacteria
  132. Study of the phytotoxicity of margines on Pistia stratiotes L.
  133. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part III
  134. Impact of biogenic zinc oxide nanoparticles on growth, development, and antioxidant system of high protein content crop (Lablab purpureus L.) sweet
  135. Green synthesis, characterization, and application of iron and molybdenum nanoparticles and their composites for enhancing the growth of Solanum lycopersicum
  136. Green synthesis of silver nanoparticles from Olea europaea L. extracted polysaccharides, characterization, and its assessment as an antimicrobial agent against multiple pathogenic microbes
  137. Photocatalytic treatment of organic dyes using metal oxides and nanocomposites: A quantitative study
  138. Antifungal, antioxidant, and photocatalytic activities of greenly synthesized iron oxide nanoparticles
  139. Special Issue on Phytochemical and Pharmacological Scrutinization of Medicinal Plants
  140. Hepatoprotective effects of safranal on acetaminophen-induced hepatotoxicity in rats
  141. Chemical composition and biological properties of Thymus capitatus plants from Algerian high plains: A comparative and analytical study
  142. Chemical composition and bioactivities of the methanol root extracts of Saussurea costus
  143. In vivo protective effects of vitamin C against cyto-genotoxicity induced by Dysphania ambrosioides aqueous extract
  144. Insights about the deleterious impact of a carbamate pesticide on some metabolic immune and antioxidant functions and a focus on the protective ability of a Saharan shrub and its anti-edematous property
  145. A comprehensive review uncovering the anticancerous potential of genkwanin (plant-derived compound) in several human carcinomas
  146. A study to investigate the anticancer potential of carvacrol via targeting Notch signaling in breast cancer
  147. Assessment of anti-diabetic properties of Ziziphus oenopolia (L.) wild edible fruit extract: In vitro and in silico investigations through molecular docking analysis
  148. Optimization of polyphenol extraction, phenolic profile by LC-ESI-MS/MS, antioxidant, anti-enzymatic, and cytotoxic activities of Physalis acutifolia
  149. Phytochemical screening, antioxidant properties, and photo-protective activities of Salvia balansae de Noé ex Coss
  150. Antihyperglycemic, antiglycation, anti-hypercholesteremic, and toxicity evaluation with gas chromatography mass spectrometry profiling for Aloe armatissima leaves
  151. Phyto-fabrication and characterization of gold nanoparticles by using Timur (Zanthoxylum armatum DC) and their effect on wound healing
  152. Does Erodium trifolium (Cav.) Guitt exhibit medicinal properties? Response elements from phytochemical profiling, enzyme-inhibiting, and antioxidant and antimicrobial activities
  153. Integrative in silico evaluation of the antiviral potential of terpenoids and its metal complexes derived from Homalomena aromatica based on main protease of SARS-CoV-2
  154. 6-Methoxyflavone improves anxiety, depression, and memory by increasing monoamines in mice brain: HPLC analysis and in silico studies
  155. Simultaneous extraction and quantification of hydrophilic and lipophilic antioxidants in Solanum lycopersicum L. varieties marketed in Saudi Arabia
  156. Biological evaluation of CH3OH and C2H5OH of Berberis vulgaris for in vivo antileishmanial potential against Leishmania tropica in murine models
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