Beneficial Health Potential of Algerian Polysaccharides
Beneficial Health Potential of Algerian Polysaccharides
Beneficial Health Potential of Algerian Polysaccharides
sciences
Article
Beneficial Health Potential of Algerian Polysaccharides
Extracted from Plantago ciliata Desf. (Septentrional Sahara)
Leaves and Seeds
Noura Addoun 1 , Zakaria Boual 1,2 , Cédric Delattre 3,4 , Toufik Chouana 1 , Christine Gardarin 3 ,
Pascal Dubessay 3 , Fatima Benaoun 1 , Seddik Addaoud 1 , Mohamed Didi Ould El Hadj 1 , Philippe Michaud 3
and Guillaume Pierre 3, *
1 Laboratoire de Protection des Ecosystèmes en Zones Arides et Semi-Arides, Université Kasdi Merbah,
Ouargla 30000, Algeria; nourabio14@gmail.com (N.A.); biozakaria1983@gmail.com (Z.B.);
chouanatoufik@yahoo.fr (T.C.); biodoctorante@gmail.com (F.B.); adseddik@gmail.com (S.A.);
mohameddidi@yahoo.fr (M.D.O.E.H.)
2 Laboratoire de Biologie Médicales IBN ROCHD, Rue Khemisti, 47000 Ghardaïa, Algeria
3 Université Clermont Auvergne, CNRS, SIGMA Clermont, Institut Pascal, 63000 Clermont-Ferrand, France;
cedric.delattre@uca.fr (C.D.); christine.gardarin@uca.fr (C.G.); pascal.dubessay@uca.fr (P.D.);
philippe.michaud@uca.fr (P.M.)
4 Institut Universitaire de France (IUF), 1 rue Descartes, 75005 Paris, France
* Correspondence: guillaume.pierre@uca.fr; Tel.: +33-(0)-473-407-222
Featured Application: This study substantially contributes to raising the understanding, safety,
Citation: Addoun, N.; Boual, Z.; and efficiency of ethnobotanical remedies from Plantago ciliata employed by traditional healers
Delattre, C.; Chouana, T.; Gardarin, in various Algerian health disorders.
C.; Dubessay, P.; Benaoun, F.;
Addaoud, S.; Ould El Hadj, M.D.; Abstract: Today, an ethnobotanical approach makes sense for identifying new active bioactive chemi-
Michaud, P.; et al. Beneficial Health
cals from uses of indigenous plants. Two water-soluble enriched polysaccharide fractions (L-PSPN
Potential of Algerian Polysaccharides
and S-PSPN) were extracted by hot water extraction from the leaves and seeds of Plantago ciliata Desf.
Extracted from Plantago ciliata Desf.
(1798), a Mzab indigenous herb currently used in Algeria by traditional healers. Primary investi-
(Septentrional Sahara) Leaves and
gation was performed for describing the main structural features of these polysaccharides (pectin-
Seeds. Appl. Sci. 2021, 11, 4299.
https://doi.org/10.3390/
and heteroxylan-like compositions) by using colorimetric assays, FTIR spectroscopy, HPAEC/PAD
app11094299 and GC/MS-EI analyses. Some biological activities were also monitored, such as anticomplement,
anti-inflammatory (phagocytic ability, NOX2 and MPO inhibitions) and anti-diabetic (α-amylase
Academic Editor: Ana M. L. Seca and α-glucosidase inhibitions). L-PSPC seems able to moderately modulate innate immune sys-
tem (IC50 around 100 µg/mL) and contribute to wound-healing processes (IC50 close to 217 vs.
Received: 12 April 2021 443 µg/mL for sodium heparin). S-PSPC shows some potential as an anti-hyperglycemic (IC50
Accepted: 30 April 2021 around 4.7 mg/mL) and anti-inflammatory (IC50 ranging from 111 to 203 µg/mL) agent, as well as
Published: 10 May 2021 other (fiber) psyllium-like polysaccharides extracted from Plantago species.
Publisher’s Note: MDPI stays neutral Keywords: Plantago ciliata; polysaccharides; characterization; biological activities; Africa
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
1. Introduction
Herbal medicines have attracted considerable interest as alternative anti-inflammatory
remedies due to their large therapeutic properties, low toxicity and costs [1]. Today,
Copyright: © 2021 by the authors.
involved mechanisms of anti-inflammatory remain unclear [2] and potentiating innate
Licensee MDPI, Basel, Switzerland.
immune system has been recognized as a possible way for inhibiting inflammation growth
This article is an open access article
without harming the host [3].
distributed under the terms and
Polysaccharides from various traditional medicinal herbs have been shown to be im-
conditions of the Creative Commons
Attribution (CC BY) license (https://
munopotentiating, in vitro as well as in vivo [4]. Many reports on the biological activities
creativecommons.org/licenses/by/
of polysaccharides from Plantago highlighted that species belonging to this genus showed
4.0/). anti-inflammatory effects and immune enhancements through specific and non-specific
dichloromethane. This procedure was applied for standards including Ara (Arabinose),
Glc, Gal (Galactose), GalA (Galacturonic acid), Rha (Rhamnose), Xyl (Xylose). GC/MS-
EI system was an Agilent 6890 GC / 5973 Network Mass Selective Detector, equipped
with an OPTIMA-1MS Accent column (Macherey-Nagel; 30 m, 0.32 mm, 0.25 µm), using
the following parameters, for instance, target ion: 40–800 m/z, injector line temperature:
250 ◦ C, trap temperature: 150 ◦ C, split ratio: 50:1, helium pressure: 8.8 psi; helium flow
rate: 2.3 mL/min, ionization: 70 eV, rise in temperature: starting at 100 ◦ C during 3 min,
8 ◦ C/min up to 200 ◦ C for 1 min and then 5 ◦ C/min up to 215 ◦ C. Data were analyzed
with MestReNova 7.1. software (Mestrelab Research, USA).
of α-glucosidase activity was estimated using the methods of Christudas et al., Bisht et al.
and Qian et al., which were also slightly modified [25,26]. Briefly, 500 µL in dry tubes of
α-glucosidase solution (2 UI/L) was introduced with 100 µL of each dilution of S-PSPC or
S-PSPCh , acarbose (positive control) or ultrapure water (negative control). S-PSPCh was
a hydrolyzed version of S-PSPC (H2 SO4 , 50 ◦ C, 30 min) for preliminary investigations of
molar mass effects (data not shown). The mixture was pre-incubated for 15 min at 37 ◦ C.
Then, 100 µL of p-NPG (p-nitrophenyl-α-D-glucopyranoside) solution (4 mM) were added.
The tubes were shaken and incubated for 20 min at 37 ◦ C. One mL of Na2 CO3 (0.2M) was
added to stop the reaction, and the absorbances were measured at λ = 405 nm. Inhibition
activity results were expressed regarding Equation (4) [27]. All the experiments were done
in triplicate.
Inhibition (%) = ((A(control) − A(sample) )/A(control) ) × 100 (4)
L-PSPC and S-PSPC are mainly composed of carbohydrates (66.6% and 86.5% w/w,
respectively) (Table 1). Water-soluble polysaccharides extracted from Plantago ciliata leaves
contained more uronic acids (24.0% w/w) than those extracted from seeds (7.96% w/w).
Note that L-PSPC and S-PSPC are clearly enriched-polysaccharide fractions since both are
poorly contaminated by proteins (2.30% and 0.35% w/w) and phenol compounds (close
to 0% w/w). Three polysaccharide fractions from Plantago asiatica seeds (PLP-1, -2, -3)
with high levels of total carbohydrates varying between 79.2% and 87% (w/w), and very
low protein contents (around 1% w/w) [32]. PSPN, a heteroxylan extracted from Plantago
notata seeds, was composed of 85.6% of carbohydrates including 78% of neutral sugars [29].
279 both are poorly contaminated by proteins (2.30% and 0.35% w/w) and phenol compounds
280 (close to 0% w/w). Three polysaccharide fractions from Plantago asiatica seeds (PLP-1, -2, -
281 3) with high levels of total carbohydrates varying between 79.2% and 87% (w/w), and very
282 Appl. Sci. 2021, 11, 4299 low protein contents (around 1% w/w) [32]. PSPN, a heteroxylan extracted from Plantago 7 of 15
283 notata seeds, was composed of 85.6% of carbohydrates including 78% of neutral sugars
284 [29]. Craeyveld et al. also described few amounts of uronic acids (< 5% w/w) in a seed
285 husk arabinoxylan extracted from Plantago ovata Forsk [33]. A branched rhamnogalac-
286 Craeyveld
turonan with et al.side
alsochains
described few amounts ofwas
of arabinogalactan, uronic acids (<
extracted in5% w/w)conditions
similar in a seed husk
from
287 arabinoxylan extracted from Plantago ovata Forsk [33]. A branched rhamnogalacturonan
Plantago major leaves and mainly contained uronic acids (59.3% w/w) followed by neutral
288 with
sugarsside chains
(39.1% w/w) of arabinogalactan,
[34]. Homogeneous was extracted
acidic protein-bound conditions from Plantago
in similarheteropolysaccharides com-
289 major leaves and mainly contained uronic acids (59.3%
posed of carbohydrates (89–92% w/w), proteins (3–7% w/w) and uronicw/w) followed by neutral sugars
acids (10–20%
290 (39.1%
w/w) werew/w)extracted
[34]. Homogeneous
from seedsacidic protein-bound
of Plantago depressa heteropolysaccharides composed
[35]. Thus, pectic substances and
291
of carbohydrates (89–92% w/w), proteins (3–7% w/w) and uronic acids (10–20%
mainly heteroxylan are usually identified, respectively, from Plantago leaves or seeds by w/w)
292
were
usingextracted from seeds
water extraction of Plantago
bioprocesses depressa [35]. Thus, pectic substances and mainly
[6,36].
heteroxylan are usually identified, respectively, from Plantago leaves or seeds by using
293 water
Table extraction
1. Biochemicalbioprocesses
composition[6,36].
of L-PSPC (leaves) and S-PCPC (seeds).
Carbohydrate
Table 1. Biochemical composition (w/w
of L-PSPC %) and S-PCPC
(leaves) Proteins
(seeds). Phenols Ash
Fractions
Total Neutral Uronic acids (w/w %) (w/w %) (w/w %)
Carbohydrate (w/w %) Proteins Phenols Ash
L-PSPC
Fractions 66.6 ± 1.42 42.6 ± 1.37 24.0 ± 1.12 2.30 ± 0.09 0.6 ± 0.03 3.65 ± 0.08
Total Neutral Uronic Acids (w/w %) (w/w %) (w/w %)
S-PSPC 86.5 ± 4.32 63.3 ± 3.17 7.96 ± 0.39 0.35 ± 0.02 0 5.12 ± 0.24
L-PSPC 66.6 ± 1.42 42.6 ± 1.37 24.0 ± 1.12 2.30 ± 0.09 0.6 ± 0.03 3.65 ± 0.08
294 S-PSPC
3.1.2. 86.5 ± 4.32
FTIR spectroscopy 63.3 ± 3.17 7.96 ± 0.39 0.35 ± 0.02 0 5.12 ± 0.24
295 FTIR spectra of both (a) L-PSPC and (b) S-PSPC are shown in Figure 2. The peaks at
296
3.1.2. FTIR Spectroscopy
3300–3400 cm-1 were attributed to O-H stretching vibration of both water and carbohy-
297 dratesFTIR spectra
[29]. of both
Aliphatic (a) L-PSPC
bending groupsand (b) S-PSPC
(C-H) are observed
were also shown in close
Figureto2.2900
The cmpeaks at
-1 [37].
3300–3400 − 1
cm were attributed to O-H stretching vibration of both water and carbohy-
298 The characteristic absorption peaks around 1620 cm -1 were attributed to the vibration of
drates [29]. Aliphatic bending groups (C-H) were also observed close to 2900 cm −1 [37].
299 carboxylate groups whereas the ones close to 1416 cm could correspond to ester carbonyl
-1
305
306 Figure2.2.FTIR
Figure FTIRfootprints
footprintsof
of(a)
(a)L-PSPC
L-PSPC(leaves)
(leaves)and
and(b)
(b)S-PCPC
S-PCPC(seeds).
(seeds).
Figure 3. Monosaccharide compositions of (a) L-PSPC (leaves) and (b) S-PCPC (seeds). White and black bars, respectively
correspond to the results obtained from HPAEC-PAD or GC/MS-EI experiments.
• Composition of L-PCPC
L-PSPC is composed of six main monosaccharides, highlighting its complexity, i.e.,
GalA (22.4–31.8%), Gal (18.4–20.7%), Glc (20.6–15.9%), Rha (8.93–14.4%), Xyl (13.4–9.58%)
and Ara (14.9–7.6%). Accordingly, the composition is similar to some kinds of pectin.
Significant differences of monosaccharide compositions were described in the litera-
ture, depending on the extraction/purification methodologies, analytical procedures but
also species of Plantaginaceae and obviously plant parts. Polysaccharides from Plantago
major leaves, are often composed of GalA, Gal, Ara and Rha in addition to small amounts of
Glc and Xyl [34,39]. Samuelsen et al. showed that water-soluble polysaccharides extracted
from Plantago major leaves contained two subfractions (PMIa and PMIb). The first one
was composed of Ara (38%), Gal (49%), Rha (6%) and GalA (7%) whereas the second one
consisted of Ara (31%), Gal (32%), Xyl (18%), Glc (7%), Rha (5%) and GalA (8%) [6]. A
water soluble heteroxylan extracted from Plantago notata leaves was composed of Gal (44%),
Rha (20%), Glc (11%), Ara (10%) and GalA (13%) [40]. Neutral rhamnoarabinogalactan
were also extracted from Plantago lanceolata, which were rich in Gal (54%), Ara (35%) and
Rha (11%) [10]. Other water-soluble polysaccharides extracted from Plantago palmata leaves
were composed of Gal (39%), Ara/Xyl (27%), Man (Mannose) (5%), Rha (10%), Glc (5%)
and GalA (14%) [9]. As stated before, these differences may be related to species, cultivation
regions, extraction procedures, analysis methods, and samplings [41].
• Composition of S-PCPC
S-PSPC is easily identified as an arabinoxylan mainly composed of Xyl (85–78% ± 3–
3.75), Ara (11–18% ± 3.45–2.1), Rha (2–3% ± 0.45–0.75) and GalA (1–1% ± 0.47–0.21). With
a Xyl:Ara molar ratio close to 4:1, results are in accordance with the literature concerning the
identification of arabinoxylan or heteroxylan from Plantago seeds. Polysaccharide fractions
(PLP-2 and PLP-3) isolated from Plantago asiatica were defined as arabinoxylan containing,
respectively Xyl (61 and 56%) and Ara (32.2 and 39.6%) residues [32]. An arabinoxylan
extracted from the pericarp of Plantago ovata Forssk. seeds was mainly composed of Xyl
(75%) and Ara (23%) with a Xyl: Ara molar ratio close to 3: 1 [42,43]. Seeds from other
Plantago species could contain heteroxylan as reported for an acidic one from Plantago
Appl. Sci. 2021, 11, 4299 9 of 15
major L., composed of Xyl (40%), Ara (13%), Glc (10%), Gal (3%), Rha (2%), GalA (17%) and
GlcA (16%) [44]. Benaoun et al. identified a neutral heteroxylan Plantago notata Lagasca
seeds. This polysaccharide was mainly composed of Xyl (77%), Rha (9%), Ara (8%), Gal
(3%), Glc (1%) and GalA (2%) [29]. Note that further structural characterization has been
published for S-PSPC [45].
370
371
Figure 4. 4.Biological
Figure Biologicaleffects
effectsof
ofL-PSPC
L-PSPC on
on (a)
(a) phagocytosis activity of
phagocytosis activity ofpolymorphonuclear
polymorphonuclearleukocytes
leukocytesbybythe
theuptake
uptakeof of
op-
372 opsonized
sonized C.C.albicans
albicansand
and(b)
(b)complement
complementfixation.
fixation.
Figure 4b showed that L-PSPC had a significant in vitro human complement fixing
activity. IC50 for sodium heparin was around 443 µg/mL, as reported for other works
with values ranging from 420 to 750 µg/mL for sodium heparin [46]. Pure heparin gave
better results with IC50 values between 16 to 36 µg/mL [47] and up to 150 µg/mL [48].
IC50 for L-PSPC was 216.7 µg/mL which was lower than for other pectic-like polysac-
charides extracted from Plantago species. Samuelsen et al. reported IC50 between 35
and 60 µg/mL [6]. Accordingly, pectin usually show decent to strong anti-complement
activities below 100 µg/mL due to their anionic character [10]. Heteroxylan from Plantago
seeds (major and asiatica), consisting of a 1,3- and 1,4-linked β-D-Xylp backbone with short
side chains, also showed potent complement activity, as reported with values ranging from
200 to 350 µg/mL [44].
Further experiments could also be done on S-PSPC to check this behavior. It is
noteworthy that polysaccharide fractions with IC50 values higher than 200–400 µg/mL
(sodium heparin) have no chance to emerge as new anti-complement drugs on the market.
These results explained the uses of Plantago ciliatia leaves as remedies for treating wounds
and specific inflammation by traditional healers.
In this study, PLPC was a heteroxylan of 3870 kDa. Histological observations high-
lighted a significant reduction in the length of colitis in the group treated with DSS com-
pared to the control group, i.e., 64.3 ± 4.1 mm and 85.6 ± 4.5 mm, respectively. Type 2
diabetes is a progressive disease that benefits from a complex therapeutic arsenal. Synthetic
drugs prescribed for diabetics are increasingly numerous and more and more effective,
e.g., hypoglycemic sulfonamides, acarbose, metformin, etc. These products can cause
undesirable effects on human health such as the risk of hypoglycemia, weight gain or
digestive disorders [55,56].
• Antihyperglymic potential of S-PCPC
Today, alternative approaches are currently being targeted as the use of plant mu-
cilages and/or gums with antihyperglycemic potential [57]. One of the regulatory pathways
is to inhibit the functioning of α-amylase and α-glucosidase, thus preventing the cleavage
of carbohydrates into oligosaccharides and their conversion to simple monosaccharides.
Thus, it delays digestion process and prolongs their stay in the jejunum [58]. In vitro anti-
hyperglycemic effects of S-PSPC using acarbose as positive control are reported in Figure 5
c, d. Acarbose showed better IC50 values (0.30 and 0.32 mg/mL) against α-amylase and α-
glucosidase than S-PSPC (3.60 and 10 mg/mL), respectively (p < 0.05). The results observed
Appl. Sci. 2021, 11, 4299 12 of 15
for the positive control were consistent with the literature with values ranging from 0.05
to 0.60 mg/mL [59]. As reported by Chen et al., inhibition of α-glucosidase activity was
inversely proportional to molar mass and S-PSPCh showed an IC50 of 4.71 mg/mL [60].
Note that S-PSPC had a molar mass of 700 kDa [45]. A heteroxylan extracted from Plantago
notata seeds also showed a moderate inhibitory potential at 10 mg/mL (58%) [29]. Varia-
tions in monosaccharide compositions are also classically involved in these differences [61].
Inhibitory capacity of heteroxylan and arabinoxylan are due to Xyl:Ara ratio and degree of
substitution, highly substituted ones presenting the best IC50 values. Arabinoxylan also
uncompetitively inhibit α-glucosidase [62]. Treating diabetic rats with an arabinoxylan
(PLP) isolated from Plantago asiatica seeds leaded to a reduction in blood glucose levels [63].
PLP significantly inhibited α-amylase activity and diffusion of glucose, in vitro. At 2.5
mg/mL, PLP reduced α-amylase activity by 10% compared to the negative control, which
was lower than for S-PSPC at the same concentration (36%). Inhibition of α-amylase could
be due to the number of free carboxylic groups [64]. Note that S-PSPC contained few
uronic acids (8% w/w). Adsorption of polysaccharides to starch remains the most reported
hypothesis, which would prevent the hydrolytic activity of enzymes such as α-amylase [65].
Consuming Plantago ovata fibers (rich in arabinoxylan) improved postprandial glycemic
index and insulin sensitivity in rats [43,66]. Dietary fibers from Plantago ovata may also
reduce blood glucose levels in patients with type II diabetes [67]. Bisht et al. tested in vitro
antihyperglycemic potency of Acacia tortilis polysaccharide (AG), showing its potential as
an effective remedy for treating diabetes mellitus. IC50 of AG was around 0.7 mg/mL for α-
glucosidases extracted from rats and 0.5 mg/mL for those extracted from yeast [25]. More
recently, an arabinan-rich polysaccharide exhibited significant α-glucosidase inhibitory
activities [60,68]. These observations are consistent with traditional uses of Plantago ciliata
seeds in medicine for reducing blood sugar levels [11].
Finally, all these preliminary results assessed the biological potential of both L-PSPC
(pectin-like) and S-PSPC (arabinoxylan-like), giving an understanding as to why Plantago
ciliata leaves and seeds are widely used in Algerian ethnobotany approach to treat diabetes
and diseases often associated with inflammation. Further experiments should be needed in
the future, as instance, the analysis of the antiproliferative and in vitro digestion activities
of both fractions to better comprehend their biological potentials in Nutraceutics and
Inflammation processes. In vivo (cells, animals and clinical) experiments should complete
these results to assess their uses as new healthy drugs (or based-drug compounds).
Author Contributions: Conceptualization, G.P., N.A., Z.B.; methodology, C.D., G.P., N.A., P.D.;
validation, C.D., G.P., N.A., P.D.; formal analysis, C.G., F.B., G.P., N.A., S.A., T.C., Z.B.; investigation,
C.D., F.B., N.A., P.D., S.A., T.C., Z.B.; writing—original draft preparation, G.P., N.A., Z.B.; writing—
review and editing, G.P., Z.B.; supervision, G.P., M.D.O.E.H., P.M., Z.B.; project administration,
M.D.O.E.H., P.M.; funding acquisition, M.D.O.E.H., P.M. All authors have read and agreed to the
published version of the manuscript.
Funding: This work has been sponsored by Campus France and the Hubert Curien Tassili program—
Phase II (15MDU933).
Institutional Review Board Statement: The study was conducted according to the guidelines of the
Declaration of Helsinki, and approved by Ethics Research Committee of Laboratoire de Biologie
Médicales IBN ROCHD (Ghardaïa, Algeria), number 1154/He/Ce/Z/11/LSPSPC, 23 August 2017.
Conflicts of Interest: The authors declare no conflict of interest.
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