Hindawi

BioMed Research International

Volume 2018, Article ID 1824790, 6 pages
https://doi.org/10.1155/2018/1824790

Research Article
In Vitro Antidiabetic Effects and Antioxidant Potential of
Cassia nemophila Pods

Gauhar Rehman,1 Muhammad Hamayun,2 Amjad Iqbal ,3 Saif Ul Islam,1 Saba Arshad,1
Khair Zaman,4 Ayaz Ahmad,5 Adeeb Shehzad,6 Anwar Hussain,2 and InJung Lee 7
1
Department of Zoology, Abdul Wali Khan University Mardan, Mardan, Pakistan
2
Department of Botany, Abdul Wali Khan University Mardan, Mardan, Pakistan
3
Department of Agriculture, Abdul Wali Khan University Mardan, Mardan, Pakistan
4
Department of Chemistry, Abdul Wali Khan University Mardan, Mardan, Pakistan
5
Department of Biotechnology, Abdul Wali Khan University Mardan, Mardan, Pakistan
6
Department of Biomedical Engineering and Sciences, SMME, National University of Science and Technology (NUST),
H 12, Islamabad, Pakistan
7
Division of Plant Biosciences, School of Applied Biosciences, College of Agriculture & Life Science, Kyungpook National University,
Daegu, Republic of Korea

Correspondence should be addressed to Amjad Iqbal; amjadiqbal147@yahoo.com and InJung Lee; ijlee@knu.ac.kr

Received 16 October 2017; Revised 8 December 2017; Accepted 19 December 2017; Published 23 January 2018

Academic Editor: Kazim Husain

Copyright © 2018 Gauhar Rehman et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

The antidiabetic and antioxidant potential of ethanolic extract of Cassia nemophila pod (EECNP) was evaluated by three in vitro
assays, including yeast glucose uptake assay, glucose adsorption assay, and DPPH radical scavenging activity. The result revealed
that the extracts have enhanced the uptake of glucose through the plasma membrane of yeast cells. A linear increase in glucose
uptake by yeast cells was noticed with gradual increase in the concentration of the test samples. Moreover, the adsorption capacity
of the EECNP was directly proportional to the molar concentration of glucose. Also, the DPPH radical scavenging capacity of the
extract was increased to a maximum value of 43.3% at 80 𝜇g/ml, which was then decreased to 41.9% at 100 𝜇g/ml. From the results,
it was concluded that EECNP possess good antidiabetic and antioxidant properties as shown by in vitro assays.

1. Introduction 8 per 20 died persons were of old age (≥79 years of age).
In the technologically advanced countries, huge amount of
Diabetes mellitus is the collective name of metabolic abnor- sum is spent on the prevention and treatment of diabetes as
malities, primarily caused by the defect in secretion of insulin well as on the discovery of new synthetic or natural drugs. In
hormone by the pancreatic islets. It is chiefly manifested in 2014, the global health management expenditures on diabetes
the form of elevated levels of blood glucose (hyperglycemia). reached USD 612 billion, which represented 11% of total
The reduced action of insulin on target tissues leads to worldwide healthcare expenditures [3]. Certainly, a large
a group of abnormalities, affecting the biochemistry and number of synthetic drugs have been discovered in the past,
physiology of carbohydrate, fat, and protein [1, 2]. According but these drugs were found to have side effects. Therefore,
to the reports of International Diabetes Foundation 2014, the researchers were focusing to develop new drugs from natural
estimated global prevalence of diabetes among adults is 8.3% sources that are safe without having any side effects. One
(387 million), which will reach an estimated value of 53% of the recent developments in the field of natural products
(592 million) by the year 2035. Diabetes mellitus stands 5th is the exploration of a potent plant species, such as Cassia
among the diseases that can lead to death around the world. nemophila. The species also known as Senna nemophila,
Approximately, 4.9 million deaths were recorded in 2014, and silver Cassia, or desert Cassia is an evergreen shrub of about
2 BioMed Research International

6–8 feet high [4]. It belongs to the family Caesalpiniaceae a rotary evaporator, where ethanol was evaporated under
and is native to Australia, which is domesticated to Khyber reduced pressure at 48∘ C. The crude extract (180 gm) was
Pakhtunkhwa, Pakistan, some 20 years ago. It has bright collected as a black dense paste. The paste was kept at
green needle-like leaves and bearing large number of bright 4∘ C and was used in various experiments to test it for
yellow flowers in the early spring. Brown papery seedpods bioactivity.
follow the flowering stage, which remain on the plant till
harvest. The pods can be removed by hand or by shearing, 2.4. Determination of Glucose Uptake Capacity by Yeast
but shearing is preferred [5]. Various Cassia species have been Cells. This assay was performed according to the well-
known to possess a good amount of medicinal properties. defined method of Cirillo [13]. Commercial baker’s yeast was
Traditionally, Cassia species were used as a medicine against dissolved in distilled water to prepare 1% suspension. The
ringworm infections, scabies, as a laxative, purgative, in the suspension was kept overnight at room temperature (25∘ C).
treatment of leprosy and syphilis. Additionally, the species On the next days, yeast cells suspension was centrifuged
have been noticed to possess antimutagenic, antitumor, anti- at 4200 rpm (Microfuge 16 Centrifuge, FX241.5P Rotor,
inflammatory, hepatoprotective, antimicrobial, and antioxi- 50/60 Hz and 220–240 V) for 5 minutes. The process was
dant properties [6]. repeated by the addition of distilled water to the pallet until
As mentioned earlier, diabetes mellitus has a close asso- a clear supernatant was obtained. Exactly 10 parts of the clear
ciation with other metabolic abnormalities; one of the core supernatant fluids were mixed with 90 parts of distilled water
abnormalities is oxidative stress. Biochemical studies have to get a 10% v/v suspension of the yeast cells.
revealed an increased generation of Reactive Oxygen Species About 1–5 mg w/v of plant extract was mixed with
(ROS) in the cells and tissues of diabetic patients [3]. To tackle dimethyl sulfoxide (DMSO) till dissolution. The mixture was
the ROS, the presence of potent antioxidant in the body of a then supplemented with various concentrations (5, 10, and
patient is necessary because an antioxidant has the capacity 25 Mm) of 1 mL of glucose solution and incubated for 10 min
of retarding or completely inhibiting the oxidation of other at 37∘ C. To initiate the reaction, 100 𝜇L of yeast suspension
substances. In this regard, DPPH radical scavenging assay is was poured in the mixture of glucose and extract, vortexed,
one of the popular antioxidant assays, originally introduced and incubated for another 60 minutes at 37∘ C. After incuba-
by Marsden Blois of Stanford University in 1958. Several tion, the tubes were centrifuged for 5 minutes at 3800 rpm
workers have used this method to investigate the antioxidant and glucose was estimated by using a spectrophotometer (UV
potential of synthetic drugs and natural products. Brand- 5100B) at 520 nm. Absorbance for the respective control was
Williams and his colleagues have introduced a modified also recorded on the same wavelength. The percent increase
version of Blois method in 1995, which is used as a reference in uptake was calculated by the formula:
by various group of researchers in recent days [7]. Similarly,
indicators of the possible antidiabetic potential of a drug can % increase in glucose uptake
be assessed through several in vitro assays, providing clues (1)
for its in vivo antidiabetic potential. Beside the antioxidant (Abs. of control − Abs. of sample)
= × 100,
assays [8], several other indicator assays include (i) potential Abs. of control
of glucose uptake across cell membrane such as that of yeast where control is the solution having all reagents except
cells [9], adipose cells [10], or muscle cells [11]; (ii) capability the test sample. Metronidazole was used as standard
of glucose adsorption [9]; (iii) inhibition of alpha amylase and drug.
alpha glucosidase enzymes [12].
2.5. Glucose Adsorption Assay. The glucose adsorption capac-
2. Materials and Methods ity of the extract was determined by the method of Ou et al.
[14]. Approximately, 1 gram of extract was added to 100 mL of
2.1. Plant Material. The pods of Cassia nemophila from vari- glucose solution of five different concentrations (5, 10, 15, 20,
ous parts of Khyber Pakhtunkhwa, Pakistan, were collected in and 30 mM). Each of these mixtures was mixed well, stirred,
the months of March till May. The specimens were kept in the and incubated in a shaker water bath at 37∘ C for 6 hours,
herbarium at Abdul Wali Khan University, Mardan, before respectively. After incubation, the mixture was centrifuged
further processing. at 4800 rpm for 20 minutes and finally the glucose content
was determined in the supernatant by using glucose oxidase
2.2. Chemicals. Commercial baker’s yeast, metronidazole, peroxidase diagnostic kit. The amount of bound glucose was
dimethyl sulfoxide (DMSO), solid DPPH, and ascorbic acid determined by the given formula:
were purchased from Sigma Aldrich. Ethanol and methanol
were purchased from Merck. 𝐺1 − 𝐺6
Glucose bound =
weight of sample (2)
2.3. Preparation of Plant Extracts. The seeds (1 kg) from the × volume of sample.
pods of C. nemophila were washed, dried in the shade, and
ground into a coarse powder. Ethanol was used as solvent Here, 𝐺1 represents the glucose concentration of the original
for 8 h to obtain an ethanol soluble fraction, using a Soxhlet solution, while 𝐺6 represents the glucose concentration after
apparatus. The extract containing solvent was transferred to 6 hours.
BioMed Research International 3

Yeast glucose uptake assay with 5 mM glucose concentration Yeast glucose uptake assay with 10 mM glucose concentration
100 80
90 e 70
cd e
bc bc bc cd de
80 b bc bcd bc
60 c c bc
ab

Glucose uptake (%)

Glucose uptake (%)

70 a
a ab
50 a
60
50 40
40 30
30
20
20
10
10
0 0
1 mg 2 mg 3 mg 4 mg 5 mg 1 mg 2 mg 3 mg 4 mg 5 mg
Concentration of extract (mg/mL) Concentration of extract (mg/mL)

EECNP EECNP
Metronidazole Metronidazole

Figure 1: Glucose uptake by yeast cells at 5 mM initial concentration of Figure 2: Glucose uptake by yeast cells at 10 mM initial concentration
glucose in the presence of EECNP. EECNP: ethanolic extract of Cassia of glucose in the presence of EECNP. EECNP: ethanolic extract of
nemophila pods. The error bars represent ± SE of triplicate data. The Cassia nemophila pods. The error bars represent ± SE of triplicate
bars having different letters are significantly different at 𝑃 = 0.05. data. The bars having different letters are significantly different at 𝑃
= 0.05.

2.6. Antioxidant Activity DPPH Radical Scavenging Assay. Yeast glucose uptake assay with 25 mM glucose concentration
The free radical scavenging ability of the EECN extract 40
e
was determined using DPPH according to the method of 35 cde
cde
Burits and Bucar [15]. Freshly prepared 1 ml DPPH solution
30 bcd cd
(0.004% w/v in 99% ethanol) was added to a 3 ml of sample c
Glucose uptake (%)

(100 𝜇g/ml ethanol). The mixture was incubated at room 25

b
bc
temperature in the dark for 20 mins. After incubation, the b
mixture was vortexed and the absorbance was read at 517 nm 20
a
using a spectrophotometer. Ascorbic acid was used as a 15
reference and 99% ethanol was used as blank. The DPPH free
10
radical scavenging activity was measured using the following
formula: 5

DPPH radical scavenging activity (%) 0

1 mg 2 mg 3 mg 4 mg 5 mg
𝐵−𝑆 (3) Concentration of extract (mg/mL)
= × 100,
𝐵
EECNP
where 𝐵 is the absorbance of the blank; 𝑆 is the absorbance of Metronidazole
the sample extracts or standard.
Figure 3: Glucose uptake by yeast cells at 25 mM initial concentration
of glucose in the presence of EECNP. EECNP: ethanolic extract of
2.7. Statistical Analysis. All the experiments were carried Cassia nemophila pods. The error bars represent ± SE of triplicate
out in triplicate and the data was analyzed by 𝑡-test using data. The bars having different letters are significantly different at 𝑃
Microsoft Excel 2010. = 0.05.

3. Results
Moreover, the glucose uptake capacity at 1 mg/mL EECNP
3.1. Effect of EECNP on Glucose Uptake Capacity by Yeast Cells. was >60% that has reached almost 80% when 5 mg/mL of
The ethanolic extract of Cassia nemophila pod promoted EECNP was used (Figure 1). This means that by increasing
the uptake of glucose across the plasma membrane of yeast the concentration of EECNP will increase the capability of
cells (Figures 1, 2, and 3). The glucose uptake at an initial yeast cells to uptake more glucose from the environment.
concentration of 5 mM and 10 mM by the EECNP was Similarly, Figures 2 and 3 revealed a linear increase in the
comparable to that of known drug metronidazole (Figures uptake of glucose by yeast cells with a gradual increase in
1 and 2). However, the effect of metronidazole on glucose the concentration of the test sample. On the other hand, an
uptake by the yeast cells at 25 mM glucose concentration inverse relationship to the molar concentration of glucose was
was a bit higher as compared to that of EECNP (Figure 3). observed, when glucose uptake by yeast cells was compared
4 BioMed Research International

30 60
c
% glucose adsorption (mg/dL)

25
c

DPPH activity (%)

20 bc 40

15
ab
10 20
a
5

0 0
5 10 15 20 30 10 20 40 60 80 100
Glucose conc. (mM) Concentration (g/ml)

Figure 4: Glucose adsorption capacity by EECNP. EECNP: ethanolic EECNP

extract of Cassia nemophila pods. The error bars represent ± SE AA
of triplicate data. The bars having different letters are significantly
different at 𝑃 = 0.05. Figure 5: Antioxidant activity of EECNP. EECNP: ethanolic extract
of Cassia nemophila pod (test sample); AA: ascorbic acid (standard).

among 5 mM, 10 mM, and 25 mM for the same amount of

EECNP (Figures 1, 2, and 3). From the results it is concluded eugenol, caryophyllene, 𝛽-copaene, azulene, dodecatetrae-
that the lower the concentration of glucose in the solution, namide, and phenethylamine [18, 19]. Therefore, the presence
the higher the uptake by yeast cells. of one of these compounds in the extract of EECNP might
help in the uptake of glucose in the present study. On a general
3.2. Effect of EECNP on Glucose Adsorption. The effect of basis, the uptake of glucose by skeletal muscles is due to the
EECNP on in vitro glucose adsorption has been shown in accumulation of functional glucose transporting molecules in
Figure 4. The results of the present study indicated that the the cell membrane. The glucose transporting molecules are
extract possessed a significant glucose adsorption capacity regulated by leptocytes and/or myocytes in response to high
at all tested concentrations. Moreover, the adsorption of secretion of insulin in blood, resulting in hypoglycemic effect
glucose by the test sample was directly proportional to the [11]. On the contrary, the studies concerning the effect of
concentration of glucose, provided that the weight of the drugs on reduction of postprandial hyperglycemia have been
sample was kept constant. Hence the minimum adsorption one of the important aspects in the management of diabetes
was recorded at 5 mM glucose concentration and maximum mellitus, which is a well-focused therapeutic approach till
at 30 mM. Likewise, it was proved that the test extract is date.
capable of binding the glucose even at lower concentrations. Furthermore, glucose uptake by yeast cells may be dif-
ferent from that of other eukaryotic or human body cells.
3.3. Antioxidant Capacity of the EECNP. To assess the antiox- Transport of glucose across yeast membrane may involve
idant effect of EECP, 1,1-diphenyl-2-picrylhydrazyl (DPPH) facilitated diffusion rather mediation of a phosphotransferase
assay was performed in vitro. As shown in Figure 5, the enzyme system or any other unknown process. The glucose
dose-response curve of DPPH confirms the free radical uptake by the yeast cells may be affected by several variables,
scavenging activity of the EECP. At a concentration of such as glucose concentration inside the cells or the subse-
25 𝜇g/ml, EECP showed maximum scavenging activity. The quent metabolism of glucose. If most of the internal sugar is
effect of antioxidants on DPPH is thought to be due to converted readily into other metabolites, the internal glucose
their hydrogen donating ability. Though, the DPPH radical concentration will get low and high uptake of glucose into the
scavenging potential of the extract was less than those of cell will be favored. Likewise, there are possibilities that the
ascorbic acid (100%). The study showed that the extract has glucose uptake by yeast cells in the presence of EECNP extract
an average proton-donating ability and could serve as free is due to both facilitated diffusion and elevated glucose
radical inhibitors. metabolism. Certainly, it will be quite interesting to explore
the activity of natural extract (including EECNP) in vivo,
4. Discussion which might help in the enhanced glucose uptake by muscle
cells and adipose tissues of the body. The extract could bind
The antidiabetic and antioxidant properties of ethanolic glucose effectively and transport it across the cell membrane
extract from the pods of Cassia nemophila may be attributed for further metabolism.
to the presence of bioactive compounds that might be present In the present study, the glucose adsorption capacity of
in Cassia genus [16, 17]. The previously identified bioac- the sample was also found to have a directly proportional
tive compounds in Cassia genus include oxacyclododecan- relationship with the molar concentration of glucose. The
2-one, imidazole, amentoflavone, bioflavonoids, roseanone, adsorption property of the EECNP extract may be due to the
BioMed Research International 5

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The authors declare that there are no conflicts of interest
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