Received: 21 August 2017
|
Revised: 17 December 2017
|
Accepted: 19 December 2017
DOI: 10.1111/jfbc.12497
FULL ARTICLE
Anticholinesterase activity and phenolic profile of two medicinal
plants (Quassia undulata and Senecio abyssinicus) used in
managing cognitive dysfunction in Nigeria
Veronica O. Odubanjo1,2
|
Ganiyu Oboh2 | Sunday I. Oyeleye2,3
|
Stephen A. Adefegha2
1
Department of Biochemistry, Adekunle
Ajasin University, P.M.B 001, Akungba
Akoko, Ondo State, Nigeria
2
Functional Foods and Nutraceuticals,
Department of Biochemistry, Federal
University of Technology, P.M.B 704, Akure,
Ondo State, Nigeria
3
Biomedical Department, Federal University
of Technology, P.M.B 704, Akure, Ondo
State, Nigeria
Abstract
Quassia undulata (QU) and Senecio abyssinicus (SA) leaves are known in folklore in the management
of cognitive disorder in Nigeria. However, there is dearth of information about their mechanism of
actions. In this study, the effect of QU and SA aqueous extracts on acetylcholinesterase (AChE)
and butrylcholinesteras (BChE) activities were determined as well as their antioxidant capacity and
phenolic constituents. The result showed that both extracts inhibited AChE and BChE activities
and also exhibited antioxidant effect, however, extract from SA had the highest effect compared
to that of QU. HPLC analysis revealed the presence of gallic, ellagic, caffeic, quercetin, rutin, and
catechin. The inhibition of AChE and BChE activities, and antioxidant capacity of QU and SA could
Correspondence
Veronica O. Odubanjo, Department of
Biochemistry, Adekunle Ajasin University,
P.M.B 001, Akungba Akoko, Ondo State,
Nigeria.
Emails: goboh2001@yahoo.com;
oluwatoyin.odubanjo@aaua.edu.ng
be among the mechanism of actions regarding their use in folklore for the management of cognitive dysfunction. These could therefore be linked to their richness in phenolic compounds, as SA
extract exhibited higher effects.
Practical applications
Many plants have been used traditionally in the treatment of various disorders owing to their bioactivity. The outcome of this research provides biochemical information to the folkloric use of
Quassia undulate and Senecio abyssinicus in the management of neurodegenerative disorder, and
also to the pharmacologist with an option to synthesize drugs with little or no side effects.
KEYWORDS
anticholinesterase, antioxidant, medicinal plants, neurodegeneration, Quassia undulata, Senecio
abyssinicus
1 | INTRODUCTION
Yorubas in Nigeria has been use locally to improve cognitive function
and alertness (Cyril-Olutayo, Adekunle, & Taiwo, 2012; Orilogbon &
The research on herbal plants are on the increase, focusing on the prepa-
Adewole, 2011). It is an annual herb of about 50 cm high, commonly
ration of alternative pharmaceutical ingredients for the management of
found in lowlands and mountain elevations in Northern and Southern
several human ailments (Ceylan et al., 2016; Hirasa & Takemasa, 1998).
parts of Nigeria. The plant is considered by Nigerians to be stomachic
The interest in finding natural cholinesterases (ChEs) inhibitors for the
and a blood-purifier, while the crushed leaves and the juice are applied
management of cognitive/mental disorders is on the increase as studies
topically to painful areas of rheumatism, and to bruises and cuts
have shown that polyphenolic compounds such as quercetin, rutin among
(Adebayo & Krettli, 2011). Quassia undulata (Guill. & Perr.) D.Dietr
others could of health benefits (Ademosun, Oboh, Bello, & Ayeni, 2015;
(Family: Simaroubaceae), known as Bitter ash and locally called “Oriji”
s-Vilaplana et al., 2012; Khan et al., 2009; Nwanna et al., 2016).
Girone
in Nigeria, has been reportedly use in the treatment of malaria
Senecio abyssinicus Sch. Bip (Family: Asteraceae) commonly known
(Ajaiyeoba, Abalogu, Krebs, & Oduola, 1999), menstrual pain (Borokini,
as senecio or ragwort in English and locally called “amunimuye” by
Ighere, Clement, Ajiboye, & Alowonle, 2013), and memory disorder
J Food Biochem. 2018;e12497.
https://doi.org/10.1111/jfbc.12497
wileyonlinelibrary.com/journal/jfbc
C 2018 Wiley Periodicals, Inc.
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(Cyril-Olutayo et al., 2012). It is a perennial shrub, distributed mostly on
re-dissolved into 100 mL of distilled water and kept at 48C for subse-
open grassland or wooded grassland in tropical and subtropical Africa,
quent assays. The freeze-dried extracts were used for HPLC analysis
Asia, Australia, and America (Odubanjo, Ibukun, & Oboh, 2017). The
leaves can be consumed by cooking as soup, and for the management
of memory loss and aging (Adebayo & Krettli, 2011). It also has antibac-
2.2 | Chemicals and reagents
teria and antifungi properties (Ajaiyeoba & Krebs, 2003). However, till
Methanol and acetic acid, gallic acid, ellagic acid, and p-coumaric acid
date, no intense research has been done to elucidate the possible
were purchased from Merck (Darmstadt, Germany). Catechin and rutin
mechanism of actions of these herbs toward the management of cogni-
were acquired from Sigma Chemical Co. (St. Louis, MO). Butrylthiocho-
tive dysfunction and other neurodegerative diseases.
line and acetylthiocholine iodide, 5,5ʹ-dithiobio-(2-nitrobenzoic acid)
In the control of cognitive functions, cholinergic system is the
were product of Sigma Aldrich. Except otherwise stated all other rea-
most crucial neurotransmitter involved (Adefegha et al., 2017). Reports
gent were analytical grade and water used was glass distilled. JENWAY
have shown that reduced/decreased acetylcholine (ACh) level in the
UV-visible spectrophotometer was used to measure absorbance. High
cerebro-spinal fluid of Alzheimer’s disease (AD) victims correlated with
performance liquid chromatography (HPLC-DAD) was performed with
€ gren, Blennow, &
the severity of dementia (Rawicki, 2013; Wallin, Sjo
a Shimadzu Prominence Auto Sampler (SIL-20A) HPLC system
Davidsson, 2003). Today, administration of selective acetylcholinester-
(Shimadzu, Kyoto, Japan), equipped with Shimadzu LC-20AT recipro-
ase (AChE) inhibitors is the most common treatment of AD (Akinyemi,
cating pumps connected to a DGU 20A5 degasser with a CBM 20A
Oboh, Oyeleye, & Ogunsuyi, 2017). However, butyrylcholinesterase
integrator, SPD-M20A diode array detector and LC solution 1.22 SP1
(BChE) enzyme is also known to act simultaneously with AChE in the
software.
hydrolysis of ACh (Chaiyana & Okonogi, 2012). Moreover, these synthetic inhibitors adversely exhibited ill-effect such as nausea, hepatotoxicity among others, and low therapeutic effect toward memory
2.3 | AChE and BChE inhibition assay
improvement in mild dementia and cannot stop the process of neuro-
Inhibition of AChE (EC 3.1.1.7) and BChE (EC 3.1.1.8) activities by the
degeneration (Akinyemi et al., 2017; Chaiyana & Okonogi, 2012; de
extracts was assessed by the colorimetric method of Oboh, Ademiluyi,
Paula et al., 2009; Schneider, 2004). Therefore, co-inhibitors of AChE
et al. (2017) and Oboh, Ogunruku, et al. (2017). The mixture containing
and BChE activities for holistic and effective treatment/management
200 mL of AChE enzyme solution in 0.1 M phosphate buffer (pH 8.0),
of AD is desirable, and compound from natural sources including phe-
100 mL of 5,50 -dithio-bis(2-nitrobenzoic) acid (DTNB, 3.3 mM in 0.1 M
nolic compound, with ability to prevent oxidative stress, another culprit
phosphate-buffer, pH 7.0 containing NaHCO3 6 mM), extracts/prostig-
in the pathophysiology of AD have been proved effective (Ademosun
mine (standard inhibitor [30–90 lg/mL]) and 500 mL of phosphate
et al., 2015; Oboh et al., 2016). In view of the aforementioned, this
buffer (pH 8.0) were incubated for 20 min at 258C. Thereafter, 100 mL
study sought to investigate and compare the AChE and BChE inhibi-
of the enzyme substrate (acetylthiocholine iodide [0.05 mM]) solution
tory, and antioxidative capacity of Senecio abyssinicus (SA) and Quassia
was added, and AChE activity was measured by monitoring changes in
undulata (QU). It also sought to characterize the phenolic constituents
absorbance at 412 nm for 3 min. BChE activity was determined by
present in the plants using high performance liquid chromatography
using butyrylthiocholine iodide (100 mL) as substrate, while all other
coupled with diode array detector (HPLC-DAD).
reagents and conditions remain the same. The AChE and BChE inhibition by the extracts were calculated and expressed as percentage inhi-
2 | MATERIALS AND METHODS
bition as follow:
% Inhibition 5
2.1 | Sample collection and preparation
SA and QU leaves were freshly harvested from Adekunle Ajasin Uni-
AbsControl – AbsSamples =AbsControl 3 100
(1)
where Abscontrol is the absorbance without the extract and Abssample is
the absorbance with extract.
versity Akungba Akoko botanical garden, and authenticated by A.A.
Shorungbe, and deposited at the Biology Department, Federal University of Technology, Akure Nigeria. Herbarium with voucher number
BIO/FUTA/152 and BIO/FUTA/150 for SA and QU, respectively. The
2.4 | Antioxidant assay (radicals scavenging
and Fe21 chelating abilities)
leaves were thoroughly washed and allowed to drain. Thereafter, with
The scavenging ability of the extracts against DPPH (1,1-diphenyl–2
the aid of table knife, the leaves were chopped into pieces; air dried at
picrylhydrazyl) radical was evaluated as described by Akomolafe et al.
room temperature and pulverized. Ten gram of the pulverized leaves
(2016). The method of Oboh, Ademiluyi, et al. (2017) was used to
was soaked in 100 mL of distilled water and vigorously shaked using
determine the ability of the extract to scavenge hydroxyl radical pro-
orbital shaker for 6 hr. Thereafter, the extracts were filtered through
duced from the decomposition of deoxyribose induced by Fe21/H2O2
Whatman filter paper (No. 1) and the filtrates were freeze-dried into
mixture. The Fe21 chelating ability was determined using the method
powdery form with the aid of freeze-drier, giving a percentage yield of
described by Dada et al. (2017). The radicals scavenging and Fe21 che-
11.50% (SA) and 15.80% (QU). Each dried extract (100 mg) was
lating abilities were subsequently calculated as in Equation 1.
ODUBANJO
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2.5 | Determination of total phenolic (phenol and
flavonoid) content
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0.030–0.500 mg/mL. The peaks were confirmed by comparing its
retention time with those of reference standards and by DAD spectra
(200–600 nm). All chromatography operations were carried out at
The total phenolic content were determined according to the method of
Oboh, Ademiluyi, et al. (2017) Gallic acid was used as standard and total
phenol content was subsequently calculated as gallic acid equivalent
(GAE), while total flavonoid content was determined using quercetin as
standard and subsequently calculated as quercetin equivalent (QE).
2.6 | Phenolics quantification by HPLC-DAD
ambient temperature and in triplicate. Calibration curve for catechin:
Y 5 12,785x 1 1,309.4 (r 5 0.9999); chlorogenic acid: Y 5 13,492x 1
1,187.6 (r 5 0.9999); caffeic acid: Y 5 11,983x 1 1,296.5 (r 5 0.9998);
ellagic acid: Y 5 11,763x 1 1,184.7 (r 5 0.9998); p-coumaric acid:
Y 5 11,695x 1 1,358.1 (r 5 0.9996); gallic acid: Y 5 12,683x 1 1,267.4
(r 5 0.9997); rutin: Y 5 13,548x 1 1,272.9 (r 5 0.9999); and quercetin:
Y 5 13,492x 1 1,347.1 (r 5 0.9995).
Reverse phase chromatographic analyses was employed under gradient
conditions (C18 column [4.6 3 150 mm] packed with 5 lm diameter
2.7 | Statistical analysis
particles) for the characterization of the phenolic compounds in the
studied samples. The mobile phase was the mixture of solvent A
(water: acetic acid [98:2, vol/vol]) and solvent B (methanol). The gradient program was started with 95% of A and 5% of B for 2 min and
changed to obtain 25, 40, 50, 60, 70, and 80% B at 10, 20, 30, 40, 50,
The data shown are mean values (n 5 3). All data were subjected to
analysis of variance (ANOVA) and a Multiple Range Test (Tukey’s test),
accepted at p < .05. IC50 (extract concentration causing 50% effectiveness) was calculated with GraphPad Prism version 5.00 for Windows.
and 80 min, respectively (Adefegha et al., 2017). The volume injected
was 40 mL at the flow rate of 0.6 mL/min. Prior to use, extracts and
3 | RESULTS AND DISCUSSION
mobile phase were filtered with 0.45 lm membrane filter (Millipore)
and degassed by ultrasonic bath. Standards stock solutions were
Inhibitory effects of the extracts/prostigmine on AChE and BChE activ-
prepared in the HPLC mobile phase at a concentration range of
ities were presented in Figure 1a,b, respectively. From the IC50 values
F I G U R E 1 (a) AChE and (b) BChE inhibition by Quassia undulata (QU) and Senecio abyssinicus (SA) extracts. Values represent means 6 SD of
triplicate readings
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TA BL E 1 IC50 values of AChE and BChE inhibition, radicals (DPPH*, OH*) scavenging and Ferric reducing antioxidant abilities of Quassia
undulata (QU) and Senecio abyssinicus (SA) extracts
Samples
AChE
BChE
DPPH radical
Hydroxyl radical
Fe21 chelation
QU*
0.20 6 0.04b
0.24 6 0.03b
0.69 6 0.02b
0.62 6 0.03b
0.80 6 0.02b
SA*
0.136 0.01b
0.166 0.02c
0.43 6 0.02c
0.35 6 0.02c
0.46 6 0.01c
Prostigmine**
36.936 0.01a
37.756 0.02a
–
–
–
Vitamin C**
–
a
0.30 6 0.02
–
–
–
a
Gallic acid**
–
–
–
0.34 6 0.03
–
EDTA**
–
–
–
–
0.76 6 0.02a
Mean (n 5 3) in the same column followed by different letters are significantly different at p < .05. *mg/mL, **mg/mL.
higher AChE
lower than that of the synthetic inhibitors, such as galantamine (IC50
(IC50 5 0.13 mg/mL) and BChE (IC50 5 0.16 mg/mL) inhibitory abilities
for AChE 5 0.14 lg/mL) or huperzine A (IC50 5 1024 lM) (Mukherjee,
compared to that of QU (AChE, IC50 5 0.20 mg/mL; BChE,
Kumar, Mal, & Houghton, 2007; Wszelaki, Kuciun, & Kiss, 2010), but
IC50 5 0.24 mg/mL). Although, prostigmine exhibited higher cholines-
the adverse effects exhibited by these synthetic drugs/inhibitors may
terases inhibitory effects compared to the studied extracts, still the
not be experience using plants or plant-based inhibitors such as the
interest in searching for natural cholinesterases inhibitors is on the
plants in use (Ademosun et al., 2016; Chaiyana & Okonogi, 2012; de
increase. This is because several synthetic inhibitors adversely exhib-
Paula et al., 2009)
listed in Table 1, extract from SA exhibited
ited monotherapeutic and ill-effects (Akinyemi et al., 2017; Chaiyana &
The DPPH and hydroxyl radicals scavenging abilities of the
Okonogi, 2012; de Paula et al., 2009; Schneider, 2004). The in vitro
extracts and standards (Vitamin C, gallic acid, and EDTA) are presented
inhibition of AChE and BChE activities by the studied plant could be
in Figure 2a–c, respectively, and their IC50 values listed in Table 1.
among the mechanism of actions for their therapeutic use in folklore
Aqueous
medicine for the management of cognitive dysfunction. From the IC50
(IC50 5 0.43 mg/mL) and hydroxyl (IC50 5 0.35 mg/mL) radicals scav-
values listed in Table 1, SA displayed higher inhibitory effect against
enging abilities, as well as Fe21 chelating (IC50 5 0.46 mg/mL) ability
extract
from
SA
leaves
exhibited
higher
DPPH
both cholinesterases than QU. The flavonoid content of SA and the
compared to that from QU leaves (DPPH radical [IC50 5 0.69 mg/mL]
presence of quercetin in conjunction with chlorogenic and caffeic acids,
and hydroxyl radical [IC50 5 0.62 mg/mL] scavenging abilities; Fe21
which have been demonstrated to be potent inhibitor of cholinester-
chelating ability [IC50 5 0.80 mg/mL]), but not up to the standards used
ases (Ademosun et al., 2015; Oboh, Agunloye, Akinyemi, Ademiluyi, &
(Table 1). Studies have shown that neuronal cells are highly susceptible
Adefegha, 2013; Sriraksa et al., 2011), could have (but not completely)
to oxidative stress due to their rich-lipid contents and high consump-
responsible for this effects. Although, this effect could be considered
tion of metabolic oxygen (Ademosun et al., 2015; Oboh et al., 2016).
(a) DPPH and (b) Hydroxyl radical scavenging, and C-Fe21 chelating abilities of Quassia undulata (QU) and Senecio abyssinicus
(SA) extracts. Values represent means 6 SD of triplicate readings
FIGURE 2
ODUBANJO
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ET AL.
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extract from SA exhibited higher radicals scavenging and metal chelat-
The total phenol and flavonoid contents of Quassia
undulata (QU) and Senecio abyssinicus (SA) aqueous extracts
TA BL E 2
ing activities. These activities could be linked to its richness in phenolic
compounds, most especially flavonoid content. Phenolic compounds
Parameter (unit)
QU
SA
Total phenol (mg GAE/g)
12.51 6 0.32a
25.42 6 0.71b
Total flavonoid (mg QE/g)
7.62 6 0.12a
11.82 6 0.07b
(phenolic acid and flavonoid) have been reported to be potent radicals
scavenger and metals chelator (Ademosun et al., 2015; Masuoka, Matsuda, & Kubo, 2012).
The result of the total phenol and flavonoid contents are pre-
Mean (n 5 3) in the same row followed by different letters are
significantly different at p < .05.
sented in Table 2. The extract from SA contained higher total phenol
(25.14 mg GAE/g) and total flavonoid (11.82 mg QE/g) than QU
Oxidative stress damage the neuronal cells, impair communication flow
(total phenol 5 12.51 mg GAE/g; total flavonoid 5 7.62 mg QE/g).
and cognitive function (Adefegha et al., 2017; Ademosun et al., 2015;
The HPLC analysis of the phenolic constituents of the studied plants
Nwanna et al., 2016). Hence, consumption of phenolic-rich compound
are presented in Table 3, with their chromatograms in Figure 3. The
could augment body’s antioxidant status, via scavenging of radical and
analysis revealed the presence of five phenolics in each sample. Rutin
metal chelation, which could be a strategic means of attenuating oxida-
(3.52 mg/g), catechin (3.05 mg/g), ellagic (2.49 mg/g), p-coumaric
~ oz, & Argu
€elles,
tive stress in neurodegenerative conditions (Ayala, Mun
(0.81 mg/g), and gallic (0.76 mg/g) acids were found in QU extract
2014; Odubanjo, Olasehinde, Oyeleye, Oboh, & Boligon, 2017). The
while caffeic acid (2.17 mg/g), ellagic acid (2.13 mg/g), quercetin
extracts from QU and SA scavenged DPPH and hydroxyl radicals, and
(1.65 mg/g), gallic (1.62 mg/g), and chlorogenic (0.59 mg/g) acids
also chelate Fe21 in a dose-dependent manner. However, aqueous
were found in SA. Research on phenolic compounds is gaining much
interest and could be due to their pharmacological actions such as
Phenolic constituents of Quassia undulata (QU) and
Senecio abyssinicus (SA) leave (mg/g dry weight)
TA BL E 3
Component
QU
antioxidant and nootropic properties. Clinical trials have revealed
that polyphenols from plant materials possess neuroprotective
potentials, exhibit anticholinesterases properties, protect neurons
SA
a
a
against oxidative and metabolic assault, improve memory and learn-
Gallic acid
0.76 6 0.01
Catechin
3.05 6 0.03b
ND
Chlorogenic acid
ND
0.59 6 0.01b
Kumar & Khanum, 2012; Nile & Park, 2014; Oboh et al., 2013; Ren-
Caffeic acid
ND
2.17 6 0.01c
deiro, Guerreiro, Williams, & Spencer, 2012). These abilities could be
c
as result of the synergistic effects of the redox properties of the
c
1.62 6 0.02
2.13 6 0.03
ing abilities, and neuronal functions (Adefegha, Oyeleye, & Oboh,
2015; Ademosun et al., 2015; Gomez-Pinilla & Nguyen-Trang, 2012;
Ellagic acid
2.49 6 0.02
p-Coumaric acid
0.81 6 0.01a
ND
Rutin
3.52 6 0.01d
ND
Our findings suggest that the phenolic constituents of the samples in
Quercetin
ND
1.65 6 0.04a
this study could be responsible for the inhibition of AChE and BChE
Results are expressed as mean 6 standard deviations (SD) of three determinations. Averages followed by different letters differ by Tukey test at
p < .05. ND 5 not detected.
hydroxyl groups presents in their moiety (Adefegha, Oboh, Ejakpovi,
€ lçin, Huyut, Elmastaş, & Aboul-Enein, 2010).
& Oyeleye, 2015; Gu
activities and antioxidant properties. However, the differences in the
observed biological activities of the extracts could be linked to the
individual and/or synergistic effect of phenolics detected.
F I G U R E 3 Representative reverse-phase HPLC analysis of Quassia undulata (QU) and Senecio abyssinicus (SA) leaves. Using standard and
spectral analysis, peaks a, b, c, d, and e represent gallic acid, catechin, ellagic acid, p-coumaric acid, and rutin in QU, and gallic acid, chlorogenic acid, caffeic acid, ellagic acid, and quercetin, respectively, in SA. The detected wavelengths were 254, 280, 325, 366 nm for gallic
acid, ellagic acid, catechin; p-coumaric; chlorogenic and caffeic acids; rutin and quercetin, respectively
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ODUBANJO
4 | CONCLUSION
The aqueous extracts from the leaves of QU and SA inhibited AChE
and BChE activities, and also exhibited antioxidative potentials in vitro.
These effects could be attributed to the detected polyphenolic compounds. This study suggests at least in part, some of the possible mechanisms by which these leaves elicit their neuroprotective effects and
provides a scientific basis for their use in folkloric medicine in the management of cognitive dysfunction. However, toxicology and in vivo
studies of these plants should be carried out to verify these claims.
AC KNOWLEDG MENT S
This work was supported by Adekunle Ajasin University, Akungba,
Akoko.
CONFLIC T OF I NTE R ES T
The authors declare that they have no conflict of interest.
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How to cite this article: Odubanjo VO, Oboh G, Oyeleye SI,
Odubanjo, V. O., Olasehinde, T. A., Oyeleye, S. I., Oboh, G., & Boligon, A.
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