In vitro Antioxidant, Lipoxygenase and Xanthine Oxidase Inhibitory Activities of Fractions from Cienfuegosia digitata Cav., Sida alba L. and Sida acuta Burn f. (Malvaceae)
In this study polyphenol content, antioxidant activity, lipoxygenase (LOX) and Xanthine Oxidase (XO) inhibitory effects of n-hexane, dichloromethane, ethyl acetate and n-butanol fractions of aqueous acetone extracts from S. alba L., S. acuta Burn f. and Cienfuegosia digitata Cav. were investigated. The total phenolics, flavonoids, flavonols and total tannins were determined by spectrophotometric methods using Folin-ciocalteu, AlCl3 reagents and tannic acid, respectively. The antioxidant potential was evaluated using three methods: inhibition of free radical 2,2-diphenyl-1-picrylhydramzyl (DPPH), ABTS radical cation decolorization assay and Iron (III) to iron (II) reduction activity (FRAP). For enzymatic activity, lipoxygenase and xanthine oxidase inhibitory activities were used. This study shows a relationship between polyphenol contents, antioxidant and enzymatic activities. Present results showed that ethyl acetate and dichloromethane fractions elicit the highest polyphenol content, antioxidant and enzymatic activities.
to cite this article:
K. Konate, A. Souza, A.Y. Coulibaly, N.T.R. Meda, M. Kiendrebeogo, A. Lamien-Meda, J. Millogo-Rasolodimby, M. Lamidi and O.G. Nacoulma, 2010. In vitro Antioxidant, Lipoxygenase and Xanthine Oxidase Inhibitory Activities of Fractions from Cienfuegosia digitata Cav., Sida alba L. and Sida acuta Burn f. (Malvaceae). Pakistan Journal of Biological Sciences, 13: 1092-1098.
Received: August 14, 2010;
Accepted: September 15, 2010;
Published: November 02, 2010
Traditional cures and plant-based remedies remain complementary and alternative
solution to health problems in many developing countries (Azaizeh
et al., 2003). The need to use folk medicine is explained by habit
and customs, the poverty of populations, the lack of medical facilities and
doctors and above all microbial resistance to some modern medicines (Adjanhoun
et al., 1985). In addition, many people in developed countries are
interested in having more autonomy over their medical care, so self-medication
is commonplace (Eisenberg et al., 1993). In this
fact, the present study concerned Sida alba L., S.acuta Burn f.
and Cienfuegosia digitata Cav. fractions; those Malvaceae species are
widely used in Africa particularly in Burkina Faso as a component of several
primitive medicinal remedies against human diseases. Ethnobotanical investigations
conducted in the central region of Burkina Faso have showed that those Malvaceae
species are used frequently and widely in traditional medicine for the treatment
of various kinds of diseases such as malaria, fever, gastrointestinal infections,
dermatitis, varicella, variola, anti-inflammatory and antibacterial properties,
particularly used to treat hepatitis B (Nacoulma, 1996).
The phytochemical screening on those Malvaceae species revealed the presence
of saponosides, cumarins, steroids, tannins, polyphenols and flavonoids (Nacoulma,
1996). It is well established that phenolic compounds are found to have
effect on oxidation damage (Ribeiro et al., 2008).
Antioxidants are compounds which reduce the action of reactive oxygen species
in tissue damage. The oxidation proceeds in lipids with polyunsaturated fatty
acids, generating reactive oxygen species such as hydroxyl radicals (Halliwell
and Gutteridge, 1984) and prevented many diseases as diabetes, hypertension
and combating oxidative stress (Cole et al., 2005).
Several studies have shown a link between polyhenol content and lipoxygenase
(Aquila et al., 2009). Then, it is know that
xanthine oxidase is an important biological source of oxygen-derived free radicals
that contribute to oxidative damage to living tissues involved in many pathological
processes such as inflammation, cancer (Sweeney et al.,
2001). In this fact, the objectives of this study were investigate the polyphenol
content, antioxidant activity, lipoxygenase and xanthine oxidase inhibitions
of fractions from those Malvaceae species. The choice of our investigated plants
is based on two criteria: First, in this domain there is no study in Burkina
Faso that deals with these plants and the second criterion is that these plants
have ethnopharmacological data indicating their traditional utilization in the
treatment of hepatitis B caused by an inflammation of the liver and due to a
lack of antioxidants.
MATERIALS AND METHODS
Chemicals: For evaluate phytochemical composition, antioxidant, lipoxygenase and xanthine oxidase inhibition activities we used solvents, enzymes and various classic reagents. All reagents and all other chemicals were of analytical grade. Folin-Ciocalteu reagent, carbonate de sodium (Na2CO3), gallic acid, quercetin, trichlorure dammonium (AlCl3), lipoxygenase, xanthine oxidase, linoleic acid, tannic acid, xanthine, phosphate borate (1/15 M, pH 7.5), phosphate buffer (1/15 M, pH 7.5) and phosphate buffer (0.2 M, pH 6.6) were purchased from Sigma-Aldrich chemie (Steinheim, Germany); ammonium ferric citrate (CAF), ammoniac, le potassium persulfate, DPPH (2, 2-diphenyl-1-picrylhydrazyl, Fluka), 2,2-azinobis (3-ethylbenzothiazoline-6-sulphonate) ABTS, acetone, methanol, ethanol hexane, dichloromethane (DCM), acetate of ethyl, n-butanol and trichloroacetic acid were supplied by Fluka chemie (Buchs, Switzerland); potassium hexacyanoferrate [K3Fe(CN)6] was sourced from Probalo (Paris, France); ascorbic acid, tannic acid and ion trichloride were supplied by labosi (Paris, France).
Plants material: Cienfuegosia digitata Cav., Sida alba L. and S. acuta Burn f. were collected in August 2008 in Gampela, 25 Km East of Ouagadougou, capital of Burkina Faso. The plants were botanically identified by Prof. Millogo-Rasolodimby from the plants Biology Department of the University of Ouagadougou. A voucher specimen was deposited at the Herbarium of the Laboratoire de Biologie et dEcologie Végétale, UFR/SVT of University of Ouagadougou.
Extraction and fractionation: Fifty grams (50 g) of powdered plant material were extracted with 80% aqueous acetone (500 mL) in 1/10 ratio (w/v) for 24 h under mechanic agitation (SM 25 shaker, Edmund BÜHLER, Germany) at room temperature. After filtration, acetone was removed under reduced pressure in a rotary evaporator (BÜCHI, Rotavopor R-200, Switzeland) at approximately 40°C. The aqueous extracts were subjected to sequential liquid-liquid extraction with n-hexane, dichloromethane, ethyl acetate and n-butanol. Each fraction was then collected and concentrated to dryness under reduced pressure to obtain n-hexane fraction (n-HF), dichloromethane fraction (DCMF), ethyl acetate fraction (EAF) and n-butanol fraction (n-BF). The different fractions were freeze-dried by Telstar Cryodos 50 freeze-dryer. The fraction residues were packed in waterproof plastic flasks and stored at 4°C until use.
Total phenolic content: Total polyphenols were determined by Folin-Ciocalteu
method as described by (Lamien-Meda et al., 2008).
Aliquots (125 μL) of solution from each fraction in methanol (10 mg/ml)
were mixed with 625 μL Folin-Ciocalteu reagent (0.2 N). After 5 min, 500
μL of aqueous Na2CO3 (75 g L-1) were added
and the mixture was vortexed. After 2 h of incubation in the dark at room temperature,
the absorbencies were measured at 760 nm against a blank (0.5 mL Folin-Ciocalteu
reagent +1 mL Na2CO3) on a UV/visible light spectrophotometer
(CECIL CE 2041, CECIL Instruments, England). The experiments were carried out
in triplicate. A standard calibration curve was plotted using gallic acid (Y
= 0.0289x-0.0036; R2 = 0.9998). The results were expressed as mg
of gallic acid equivalents (GAE)/100 mg of fractions.
Total flavonoid content: The total flavonoids were estimated according
to the Dowd method as adapted by (Lamien-Meda et al.,
2008). The 0.5 mL of methanolic AlCl3 (2%, w/v) were mixed with
0.5 mL of methanolic fraction solution (0.1 mg mL-1) of each plant.
After 10 min, the absorbencies were measured at 415 nm against a blank (mixture
of 0.5 mL methanolic fractions solution and 0.5 mL methanol) on a UV/visible
light spectrophotometer (CECIL CE 2041, CECIL Instruments, England) and compared
to a quercetin calibration curve (Y= 0.0289x-0.0036; R2 = 0.9998).
The data obtained were the means of three determinations. The amounts of flavonoids
in plant fractions were expressed as mg of quercetin equivalents (QE)/100 mg
Total flavonols content: The contents of flavonols were determined as
described by Abarca et al. (2007) method. Aliquots
were prepared by mixing of 750 μL ethanolic fractions solution (0.1 mg
mL-1) of each plant and 750 μL aqueous AlCl3 (20%,
w/v). The absorptions were read at 425 nm after 10 min incubation against a
blank (mixture of 750 μL ethanolic fraction solution of each plant and
750 μL ethanol) on a UV/visible light spectrophotometer (CECIL CE 2041,
CECIL Instruments, England). All determinations were carried out in triplicate.
A standard calibration curve was plotted using quercetin (0-50 μg mL-1).
The results were expressed as mg of quercetin equivalents (QE)/100 mg of fractions.
Determination of tannins contents: Total tannins contents were determined as described by European community in 2004, using tannic acid as a standard. In test tube, 200 μL aqueous fraction of each fraction, 1 mL distilled water, 200 μL ammonium ferric citrate (3.5 g L-1) and 200 μL ammoniac (20%) were mixed. After 10 min, the absorbencies of samples were measured at 525 nm against a blank (200 μL aqueous fraction of each plant +1.2 mL distilled water) on a UV/visible light spectrophotometer (CECIL CE 2041, CECIL Instruments, England). The data obtained was the mean of three determinations. The results were expressed as mg of tannic acid equivalents (TAE) per 100 mg of fraction (mg TAE/100 mg fractions).
Antioxidant activity determination
DPPH radical scavenging: Radical scavenging activity of plant fractions
against stable DPPH (2, 2-diphenyl-1-picrylhydrazyl, Fluka) was determined
with a UV/visible light spectrophotometer (CECIL CE 2041, CECIL Instruments,
England) at 517 nm as described by Lamien-Meda et al.
(2008). Fraction solutions were prepared by dissolving 10 mg of dry extract
in 10 mL of methanol. The samples were homogenized in an ultrasonic bath. 0.5
mL of aliquots which were prepared at different concentrations from each sample
of fraction was mixed with 1 mL of methanolic DPPH solution (20 mg mL). After
15 min in the dark at room temperature, the decrease in absorption was measured.
All experiments were performed in triplicate and expressed in mmol Ascorbic
Acid Equivalent per gram of fraction (Y = -16.815x+6.8373; R2 = 0.9976).
Quercetin was used as positive control.
ABTS radical cation decolorization assay: For ABTS radical cation decolorization
assay, the procedure followed the method of Lamien-Meda
et al. (2008). ABTS was dissolved in water to a 7 mM concentration.
ABTS radical cation (ABTS•+) was produced by reacting ABTS
stock solution with 2.45 mM potassium persulfate (final concentration) and allowing
the mixture to stand in the dark at room temperature for 12 h before use. This
mixture was diluted with ethanol to give an absorbency of 0.7±0.02 units
at 734 nm using a UV/visible light spectrophotometer (CECIL CE 2041, CECIL Instruments,
England). For present study, we used 10 μL of the diluted sample (1 mg
mL-1 in methanol) which was allowed to react with 990 μL of
fresh ABTS•+ solution and the absorbance was taken 6 min exactly
after initial mixing. Ascorbic acid was used as standard (Y = -0.0342x+0.634;
R2 = 0.9996) and the capacity of free radical scavenging was expressed
as mmol Ascorbic Acid Equivalent per g of fraction. Quercetin, a reference compound
was used as positive control.
Iron (III) to iron (II) reduction activity (FRAP): The FRAP assay was
performed according to Hinneburg et al. (2006).
The 0.5 mL of each fraction (1 mg mL-1) was mixed with 1.25 mL of
phosphate buffer (0.2 M, pH 6.6) and 1.25 mL of aqueous potassium hexacyanoferrate
[K3Fe (CN)6] solution (1%). After 30 min incubation at
50°C, 1.25 mL of trichloroacetic acid (10%) was added and the mixture was
centrifuged at 2000xg for 10 min. Then, the upper layer solution (0.625 mL)
was mixed with distilled water (0.625 mL) and a freshly prepared FeCl3
solution (0.125 mL, 0.1%). Absorbencies were read at 700 nm on a UV/visible
light spectrophotometer (CECIL CE 2041, CECIL Instruments, England) and Ascorbic
acid was used to produce the calibration curve (Y = 0.008x-0.0081; R2 =
0.9999). The iron (III) reducing activity determination was performed in triplicate
and expressed in mmol Ascorbic Acid Equivalent per gram of fractions. Troloc,
a reference compound was used as positive control.
In vitro lipoxygenase inhibitory assay: Lipoxygenase inhibiting
activity of plant fractions with linoneic acid as a substrate was measured with
a UV/visible light spectrophotometer (CECIL CE 2041, CECIL Instruments, England)
as described by Malterud and Rydland (2000) with some
modifications. Fractions were screened for lipoxygenase inhibitory activity
at a final concentration of 50 μg mL. The mixture assay consisted of 150
μL phosphate borate (1/15 M, pH 7.5), 50 μL of each fraction solution
and 50 μL enzyme solution (0.28 U mL-1 in phosphate borate).
The reaction was initiated by adding 250 μL of substrate solution (0.15
mM in water). Enzymatic kinetic was recorded at 234 nm for 2 min. Negative control
was prepared and contained 1% methanol solution without fraction solution. All
experiments were performed in triplicate. Lipoxygenase inhibitory activity was
expressed as the percentage inhibition of lipoxygenase, calculated as (%) inhibition
following Eq. 1:
where, A is the change in absorbance of the assay without the fraction extracts (Δabs. with enzyme -Δabs. without enzyme) and B is the change in absorbance of the assay with the fraction extracts (Δabs. with enzyme -Δabs. without enzyme).
In vitro xanthine oxidase inhibition assay: Xanthine oxidase
inhibition activity of our plants fractions and the xanthine was measured by
a spectrophotometer (CECIL CE 2041, CECIL Instruments, England) as described
by Filha et al. (2006) with some modifications.
Extracts were directly dissolved in phosphate buffer-MeOH (1%) and screened
for xanthine oxidase inhibitory activity at a final concentration of 50 μg
mL-1. The mixture assay consisted of 150 μL phosphate buffer
(1/15 M, pH 7.5), 50 μL fraction solution and 50 μL enzyme solution
(0.28 U mL-1 in phosphate buffer). The reaction was initiated by
adding 250 μL of substrate solution (0.15 mM in water). Enzymatic kinetic
was recorded at 295 nm for 2 min. The negative control was prepared and contained
1% methanol solution without extract solution. Allopurinol a well known inhibitor
of xantine oxidase was used as a positive control at a final concentration of
50 μg mL-1 prepared. All experiments were performed in triplicate.
Xanthine oxidase inhibitory activity was expressed as the percentage inhibition
of xantine oxidase, calculated as (%) inhibition following Eq.
Statistical analysis: The data were expressed as Mean±Standard Deviation (SD) of three determinations. Statistical analysis (ANOVA with a statistical significance level set at p<0.05 and linear regression) was carried out with XLSTAT 7.1.
RESULTS AND DISCUSSION
Polyphenols contents: The amount of total phenolics content varied in different fractions and ranged from 23.60±0.03 mg GAE to 61.23±0.12 mg GAE for Cienfuegosia digitata followed by 17.37±0.02 mg GAE to 35.16±0.04 mg GAE for Sida alba and 15.77±0.60 mg GAE to 33.98±0.20 mg GAE for S. acuta. The highest total phenolics levels have been detected in EAF and the lowest in n-HF.
The total flavonoids content per 100 mg of Cienfuegosia digitata, Sida alba and S. acuta fractions ranged from 3.83±0.07 mg QE to 10.83±0.02 mg QE for Cienfuegosia digitata followed by 3.25±0.04 mg QE to 5.79±0.01 mg QE for Sida alba and 3.08±0.07 mg QE to 6.22±0.07 mg QE for S. acuta. The highest content was detected in EAF and the lowest in n-HF.
The total flavonols content per 100 mg of Cienfuegosia digitata, Sida alba and S.acuta fractions ranged from 1.79±0.16 mg QE to 5.71±0.11 mg QE. The highest content of total flavonols was detected in EAF and the lowest in n-HF.
The amount of total tannin content ranged from 10.08±0.21 mg TAE to
53.62±0.03 mg TAE. The highest content was detected in EAF and
the lowest in n-HF. It has been noted that amount of total phenolic
compounds in EAF is higher following by DCMF; the results are reported in the
(Table 1). This fact could be explained by the fact that these
compounds are more extractible by dichloromethane and ethyl acetate. Also, we
could add that, dichloromethane fraction abundantly alkaloids and certain flavonoids;
on the other side, ethyl acetate fraction abundantly especially phenolic compounds
(Nacoulma, 1996). Moreover, the presence of these metabolites
in some Malvaceae species particularly Sida acuta has been already reported
by Damintoti et al. (2005). The abundance of
the two fractions in polyphenol content should also explained antioxidant activity
results. It is well known that, total phenolics constitute one of the major
groups of compounds antioxidants (Cakir et al., 2003).
The results of the present study confirmed these reports. However, the abundance
of polyphenols could justify the use of our plants in traditional medicine because
polyphenols show protective effects on brain degenerative processes (Conte
et al., 2003) and anti-inflammatory (Subbaramaiah
et al., 1998). We could note that many medicinal plants contain large
amounts of polyphenols which can play an important role in adsorbing and neutralizing
free radicals, quenching singlet and triplet oxygen, or decomposing peroxides.
Many of these phytochemicals possess significant antioxidant capacities that
are associated with lower occurrence and lower mortality rates of several human
diseases (Djeridane et al., 2006). The presence
of the phenolic compounds in DCMF and EAF would be certainly justifying the
popular use of these three Malvaceae species in traditional medicine in Burkina
Antioxidant activities: For the antioxidants properties, we have tested
three methods because a recent study demonstrates that there are differences
between the test systems for the determination of the antioxidants properties
(Nsimba et al., 2008). Results are consigned
in the Table 2; the reduction capacity of DPPH radicals was
determined by the decrease of the absorbance induced by antioxidant at 517 nm,
which is induced by antioxidant. The values of different concentrations of fractions
varied respectively from 5.00±0.09 mmol AAE/g fraction to 12.90±0.04
mmol AAE/g fractions. Among the different fractions, the strongest DPPH activity
was obtained by EAF and the lowest activities were obtained by n-hexane fraction
Control compound gave 13.76±0.26 mmol AAE/g fraction for Quercetin.
For FRAP assay, the following values were varied respectively from 1.93±0.10
mmol AAE/g fraction to 5.38±0.07 mmol AAE/g fractions. The strongest
FRAP activity was obtained by EAF and the lowest activities were obtained n-hexane
|| Polyphenols contents of Cienfuegosia digitata, Sida
alba and S. acuta fractions
|mg GAE/100 mg fraction: mg equivalent Gallic acid for 100
mg dried fraction. mg QE/100 mg fraction: mg equivalent Quercetin for 100
mg dried fraction mg TAE/100 mg fraction: mg equivalent Tanic acid for 100
mg dried fraction. n-HF: n-hexane fraction; DCMF: Dichloromethane fraction;
EAF: Ethyl acetate fraction; n-BF: n-butanol fraction. Values are Mean±SD
(n = 3). Different letters in the same column indicate significant difference
(p<0.05) for our different fractions
|| Antioxidant Properties of Cienfuegosia digitata, Sida
alba and S.acuta fractions
|mmol AAE/g fraction: mmol equivalent Ascorbic Acid for 1g
dried fraction. n-HF: n-hexane fraction; DCMF: Dichloromethane fraction;
EAF: Ethyl acetate fraction; n-BF: n-butanol fraction. Values are Mean±D
(n = 3). Different letters in the same column indicate significant difference
(p<0.05) for our different fractions
Control compound gave 7.46±3.38 mmol AAE/g fractions for Trolox. We
remark also that, the fractions from Cienfuegosia digitata have exerted
a best antioxidant activity by FRAP method.
For ABTS radical cation decolorization assay, the different values were varied
respectively from 1.97±0.16 mmol AAE/g fraction to 6.23±0.20 mmol
AAE/g fraction. The strongest ABTS activity was obtained by EAF and the lowest
activities were obtained n-hexane fraction. The reference compound is Quercetin
7.81±0.21 mmol AAE/g fraction. We also note that, the fractions from
Cienfuegosia digitata have exerted a best antioxidant activity. This
good relationship between the results from total phenols analysis and the antioxidant
activity has been previously reported by some studies in past (Zheng
and Wang, 2001). Phenolic compounds are known as powerful chain breaking
antioxidants (Shahidi et al., 1992) and may contribute
directly to antioxidative action (Duh et al., 1999).
But, comparatively to the reference compounds used and the results of research
works reported by Damintoti et al. (2005), the
antioxidant assay by ABTS method in this present study, is not interesting.
However, the aqueous acetone extracts of Sida acuta showed a good relation
between phenolic compounds contents and the antioxidant activities (R2
= 0.91 with ABTS method) (Damintoti et al., 2005).The
result may be due to the variety of the plant materials or the nature of the
soil (Coulidiati et al., 2009). These results
show the interest of our plants in the treatment of hepatitis B which is an
immune deficiency disease, because natural antioxidants such as phenolic compounds
possess the ability to reduce the oxidative damage associated with many diseases
such as immune deficiency diseases (Pietta et al.,
1998; Lee et al., 2000; Malterud
and Rydland, 2000).
Enzymatic activities: Enzymatic activity was evaluated through the percentage of lipoxygenase inhibition and xantine oxidase inhibition. Results are consigned in the (Table 3), the amount of lipoxygenase inhibition varied from 19.68±0.57 to 93.17±0.02%. The strongest inhibition was obtained by EAF and the lowest activities were obtained n-hexane fraction.
||Lipoxygenase and xanthine oxidase inhibition activities of
Cienfuegosia digitata, Sida alba and S.acuta fractions
|n-HF: n-hexane fraction; DCMF: dichloromethane fraction; EAF:
ethyl acetate fraction; n-BF: n-butanol fraction. Values are Mean±SD
(n = 3). Different letters in the same column indicate significant difference
(p<0.05) for our different fractions
Xanthine oxidase inhibition ranged from 17.43±1.95 to 67.22±0.04%. The strongest inhibition was obtained by EAF and the lowest activities were obtained n-hexane fraction.
We remark that DCMF and EAF have a best lipoxygenase and xanthine oxidase inhibitory
activities comparatively to the other fractions. The results of these three
fractions could explain by the abundance of the two fractions in polyphenol
content. This good relationship between polyphenol content and lipoxygenase
inhibitory activity has been reported by Aquila et al.
(2009). We evaluated xanthine oxidase because, it is an important biological
source of oxygen-derived free radicals that contribute to oxidative damage to
living tissues that are involved in many pathological processes such as inflammation,
cancer (Sweeney et al., 2001). We also notice
the present study, a good relationship between polyphenolic compounds and xanthine
oxidase particularly flavonoids. Many research works reported that flavonoids
are a group of polyphenolic compounds, which have been reported to possess xanthine
oxidase inhibitory activity (Meda et al., 2010).
In this fact, lipoxygenase and xanthine oxidase inhibitory activities would
be probably due to the phenolic compounds. Inhibition of these two liver enzymes
by the fractions from three plants, particularly DCMF and EAF of Cienfuegosia
digitata could explain the reasons of it most utilization in hepatitis B
In conclusion, the fractions of Cienfuegosia digitata have the best
results in polyphenol contents, antioxidants properties and enzymatic activities
than Sida alba and S. acuta fractions. Moreover, DCMF and EAF
have the best results. The results of this study show that those Malvaceae species
particularly Cienfuegosia digitata can be used as easily accessible source
of natural antioxidants, natural lipoxygenase and xanthine oxidase inhibitories.
However, the components responsible for the antioxidant potential, lipoxygenase
and xanthine oxidase inhibitory activities are currently unclear. Therefore,
it is suggested that further works should be performed on the isolation and
identification of the news bioactive components in DCMF and EAF to better manage
hepatitis B in Burkina Faso.
The authors are grateful to the France Embassy in Burkina Faso/EGIDE-France for the mobility scholarship. The authors thank Dr G. Walters for her kind help and suggestions regarding the English revision of the manuscript.
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