Manniosides B-F, five new triterpenoid saponins from the leaves of Schefflera mannii (Hook.f.) Harms

Article abstract of DOI:10.1016/j.carres.2021.108279

Fifteen triterpenoid saponins including five new compounds (Mannioside B: 3β-[(β-D-glucopyranosyl)oxy]urs-12-en-28-oic acid α-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-glucopyranosyl ester (1), mannioside C: 3β-[(β-D-glucopyranosyl)23-dioxy

Full text of DOI:10.1016/j.carres.2021.108279

Carbohydrate Research 502 (2021) 108279
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Carbohydrate Research
journal homepage: www.elsevier.com/locate/carres
Manniosides B-F, five new triterpenoid saponins from the leaves of
Schefflera mannii (Hook.f.) Harms
a
,
b
,
*
b
a
a
Beaudelaire K. Ponou
Tomofumi Miyamoto
, Chiaki Tanaka , R ´e my B. Teponno , Azefack L. Tapondjou ,
b,**
a
Research Unit of Environmental and Applied Chemistry, Department of Chemistry, Faculty of Science, University of Dschang, Box 183, Dschang, Cameroon
Department of Natural Products Chemistry, Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka, 812-8582, Japan
b
A R T I C L E I N F O
A B S T R A C T
Keywords:
Fifteen triterpenoid saponins including five new compounds (Mannioside B: 3β-[(β-D-glucopyranosyl)oxy]urs-12-
Araliaceae
en-28-oic acid
side C: 3β-[(β-D-glucopyranosyl)23-dioxy]urs-12-en-28-oic acid
anosyl-(1 6)-β-D-glucopyranosyl ester (2), mannioside D: 3β,23-dihydroxyurs-12-en-28-oic acid β-D-
glucopyranosyl-(1 → 6)- β-D-glucopyranosyl ester (3), mannioside E: 3β-hydroxy-23-oxolup-20(29)-en-28-oic
acid
-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-glucopyranosyl ester (4) and mannioside F:
22S)-27β-[(β-D-glucopyranosyl)oxy]-22-hydroxyprotosta-12,24-dien-3β-yl β-D-glucopyranoside (5)) were iso-
α
-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-glucopyranosyl ester (1), mannio-
Schefflera mannii
Triterpenoid saponins
Manniosides
α
-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyr-
→
α
(
lated from the leaves of Schefflera mannii (Hook.f.) Harms. Their structures were established on the basis of 1D
and 2D NMR data, mass spectrometry and chemical methods. The major isolated compounds were tested for their
antiproliferative activity on human malignant epithelial (HeLa) cells but were not efficient at the concentration
of 33 mM.
1
. Introduction
The Araliaceae family is known as one of the most medically
As part of our continuous effort to isolate bioactive saponins from
Cameroonian medicinal plants [7,14–20], we have examined the
methanol extract from the leaves of S. mannii. In the present paper, we
describe the isolation and structure elucidation of five new triterpenoid
saponins (1–5) along with ten known compounds (6–15). Although
compound 14 was previously identified [21], its NMR data are herein
reported for the first time. Furthermore, the major isolated compounds
were tested for their antiproliferative activity on human malignant
epithelial cells (HeLa).
important plant families [1]. Several chemical and pharmacological
studies revealed triterpenoid saponins to be the main bioactive com-
ponents present in Araliaceae species [2–7]. Saponins isolated from
Araliaceae are reported to exhibit various pharmacological activities
including anti-inflammatory, antiproliferative, antifungal, antioxidant,
hepatoprotective, neuroprotective, wound healing and cancer prevent-
ing effects [8]. The genus Schefflera (Araliaceae) comprises about 600
described species found in the tropics and subtropics [9] where they are
used as folk medicine for the treatment of inflammation, rheumatism,
fever, pain, and as a general tonic [1,10,11]. They are also known as a
rich source of pentacyclic triterpenoids and their glycoside derivatives,
mainly with oleanane, ursane, and lupane type skeletons [1,4,10,12].
Schefflera mannii (Hook.f.) Harms is found in Cameroon, Equatorial
Guinea, Nigeria, and S ˜a o Tom ´e and Príncipe [13]. No previous phyto-
chemical studies on this plant have been reported.
2. Experimental
2.1. General experimental procedures
Optical rotations were measured on a JASCO DIP-370 Digital
1
13
Polarimeter. H and C NMR were performed in C
5 5 2
D N/D O (20 : 1) on
1
a Varian INOVA-600 NMR Spectrometer (600 MHz for H, 150 MHz for
1
3
C). All chemical shifts (δ) are given in ppm with reference to
*
Corresponding author. Research Unit of Environmental and Applied Chemistry, Department of Chemistry, Faculty of Science, University of Dschang, Box 183,
Dschang, Cameroon.
* Corresponding author.
E-mail addresses: beaudelaireponou@yahoo.fr (B.K. Ponou), miyamoto@phar.kyushu-u.ac.jp (T. Miyamoto).
*
https://doi.org/10.1016/j.carres.2021.108279
Received 18 December 2020; Received in revised form 25 February 2021; Accepted 25 February 2021
Available online 1 March 2021
0
008-6215/© 2021 Elsevier Ltd. All rights reserved.

B.K. Ponou et al.
Carbohydrate Research 502 (2021) 108279
tetramethylsilane (TMS) as internal standard and coupling constants (J)
are in Hz. ESI-TOF-MS were recorded on a Bruker Micro TOF II LC/MS
Spectrometer. Centrifugation was done on Mini Centrifuge model
NG002B. Column chromatography was performed using Sephadex LH-
(52.4 mg), C2 (8.9 mg), C3 (23.7 mg), C4 (3.4 mg), C5 (34 mg) and C6
(34.5 mg). HPLC purifications of the combined C3, C4 and C5 on 10 mm
× 250 mm column eluted with MeOH/H
isolation of 9 (t 75.1 min, 1.2 mg), 7 (t 55.7 min, 5.4 mg), 15 (t
min, 1.5 mg), and 10 (t 101.8 min, 1.1 mg). Given the relative small
2
O (75 : 25) allowed the
R
R
R
60.4
2
0 (eluted with MeOH) and silica gel 60 (0.040–0.063 mm, Merck)
eluted with CHCl /MeOH/H O (60 : 37: 7, 70 : 30: 0.5, 80 : 20: 0.5, 90 :
0: 5)). MPLC was done with a KISO Power Tool E5305T pump and an
R
(
3
2
amount of subfraction B34 which showed compounds not yet isolated
from the previous fractions, and the complexity to separate its constit-
1
Advantec SF-160 fraction collector. TLC were carried out on precoated
Kieselgel 60 F254 (Merck) plates developed with CHCl /MeOH/H O (60
37: 7, 70 : 30: 1, 80 : 20: 1, 90 : 10: 5) and on Kieselgel 60 RP-8 F254S
Merck KGaA 64271 Darmstadt, Germany) developed with MeOH/H
CN/H O mixtures. They were visualised by spraying with 5%
methanolic H SO followed by heating. Preparative HPLC was per-
2
uents using MeOH/H O mixtures as mobile phase, we have repeated the
3
2
experiments in similar conditions starting with 1.2 g of the MeOH
extract. The second round of the experiments allowed to obtain several
fractions including one, namely Br33 (24.1 mg) comparable to B34 on
TLC profiles. Both Br33 and B34, were combined and the resulting
fraction was submitted to HPLC on 4.6 mm × 250 mm column eluted
:
(
2
O
and CH
3
2
2
4
formed with a JASCO PU-2080 Plus Intelligent HPLC pump connected to
a 5C18-AR-II column (Nacalai Tesque Inc., Japan) and JASCO UV-2075
with CH
3
CN/H
2
O (35 : 65) giving 4 (t
R
17.8 min, 1.7 mg), 5 (t
R
9.1 min,
1.7 mg) in addition to 8 (t
R
11.0 min, 1.8 mg) and 3 (t 15.4 min, 3.5 mg)
R
Inteligent UV/VIS detector, λmax 210 nm. 300
solution were injected each time with flow rates of 2.5 mL/min (on 20
mm × 250 mm), 1.5 mL/min (on 10 mm × 250 mm) and 1 mL/min (on
μ
L, 40
μ
L and 20
μ
L of
initially isolated.
2.3.1. Mannioside B (1)
4
.6 mm × 250 mm) column, respectively. GC-MS was performed with
White amorphous powder; [
α
]24
D
= +1.66◦ (c = 0.0006 g/mL,
1
13
GCMS-QP2010SE (Shimadzu, Japan) with Inert Cap 5MS/Sil i.d. 0.25 ×
5 5 2 5 5
MeOH); H NMR (C D N: D O (20 : 1), 600 MHz) and C NMR (C D N:
◦
3
0 m (GL Sciences Inc., Japan) [Column temperature: 100–280 C, rate
2
D O (20 : 1), 150 MHz) data: see Table 1; HRESIMS: m/z 1111.5371
◦
+
of temperature increase: 10 C/min]. The following sugar samples were
commercially obtained: D-glucose, L-rhamnose, L-glucose (Aldrich Chem.
Co., Japan), D-rhamnose (Carbosynth Ltd., United Kingdom), L-cysteine
methyl ester hydrochloride (Kanto Chemical Co., Inc., Japan), N-tri-
methylsilylimidazole (TMS-imidazole) (Tokyo Kasei Kogyo Co., Ltd.,
Japan). Fetal bovine serum (FBS) was purchased from Nichirei Biosci-
[M+Na] (calcd for C54
88
H O22Na, 1111.5665).
2.3.2. Mannioside C (2)
White amorphous powder; [
α
]23
O (20 : 1), 600 MHz) and C NMR (C
2
O (20 : 1), 150 MHz) data: see Table 1; HRESIMS: m/z 1127.5289
D
= ꢀ 13.94 (c = 0.0038 g/mL,
1
13
MeOH); H NMR (C
5
D
5
N: D
2
5 5
D N:
D
◦
+
ence Inc. (Tokyo, Japan) and heat-inactivated at 56 C for 30 min for cell
[M+Na] (calcd for C54
88
H O23Na, 1127.5614).
culture.
2
.3.3. Mannioside D (3)
]24
O (20 : 1), 600 MHz) and C NMR (C
2
D O (20 : 1), 150 MHz) data: see Table 1; HRESIMS: m/z 819.4386
= +9.13 (c = 0.0023 g/mL,
2
.2. Plant material
White amorphous powder; [
α
D
1
13
MeOH); H NMR (C
5
D
5
N: D
2
5 5
D N:
The leaves of S. mannii were collected in November 2017 in Dschang
◦
′
′′
◦
′
′′
+
(
5 27 0 N et 10 4 0 E), West Region of Cameroon, and identified at the
[M+Na] (calcd for C42
68
H O14Na, 819.4507).
Cameroon National Herbarium in Yaound ´e by Mr. NANA Victor in com-
◦
parison with a voucher specimen deposited under the reference N
2.3.4. Mannioside E (4)
White amorphous powder; [
α
]24
5 5
O (20 : 1), 600 MHz) and C NMR (C D N:
D
= ꢀ 8.07 (c = 0.0026 g/mL,
13
3
5063/HNC.
1
MeOH); H NMR (C
5
D
5
N: D
2
2
.3. Extraction and isolation
2
D O (20 : 1), 150 MHz) data: see Table 2; HRESIMS: m/z 963.4726
[
M+Na]+ (calcd for C48
76
H O18Na, 963.4929).
The air dried and pulverized plant material (3 kg) was extracted at
◦
room temperature (24 C) three times (each time for 24 h) with 15 L of
MeOH (95%). The filtrate obtained was concentrated under reduced
2.3.5. Mannioside F (5)
White amorphous powder; [
α
]23
O (20 : 1), 600 MHz) and C NMR (C
2
D O (20 : 1), 150 MHz) data: see Table 2; HRESIMS: m/z 805.4671
D
= ꢀ 7.00 (c = 0.0010 g/mL,
◦
1
13
pressure at 40 C to give 405 g of crude extract using rotator evaporator
MeOH); H NMR (C
5
D
5
N: D
2
5 5
D N:
(
yield 13.5%). Part of the extract (1 g) was dissolved in MeOH, centri-
+
fuged to eliminate non soluble particles (9.1 mg) and the MeOH soluble
portion was subjected to Sephadex column to afford five fractions A
[M+Na] (calcd for C42
70
H O13Na, 805.4714).
(
158.3 mg), B (377.7 mg), C (154.7 mg), D (151.5 mg) and E (66.9 mg).
MPLC of fraction B on normal phase silica gel column using CHCl
MeOH/H O (70 : 30: 0.5) as eluent gave seven subfractions B1 (46.5
mg), B2 (18.3 mg), B3 (112.1 mg), B4 (60.6 mg), B5 (19.5 mg), B6 (29.6
mg) and B7 (43.2 mg). HPLC of subfraction B3 eluted with MeOH–H
80 : 20) on 20 mm × 250 mm column gave compound 12 (t 44.0 min,
1.2 mg), subfractions B32 (48.7 mg), B33 (9.0 mg) and B34 (5.3 mg).
Further HPLC purifications of B32 on a cholester 4.6 mm × 250 mm
column eluted with MeOH/H O (65 : 35) afforded 8 (t 25.0 min, 25.2
mg), and 13 (t 28.6 min, 9.2 mg). When the same conditions applied to
B33, compounds 3 (t 20.6 min, 3.5 mg) and 14 (t 24.1 min, 1.7 mg)
were isolated. Subfraction B6 was submitted to HPLC on 20 mm × 250
mm column eluted with MeOH/H O (80 : 20) to give 1 (t 42.5 min, 1.2
mg) while in the same conditions, B7 led to the isolation of 11 (t 28.2
min, 6.3 mg), 2 (t 30.2 min, 7.7 mg), and 6 (t 34.8 min, 8.0 mg). Based
2.3.6. Echinocystic acid 28
α
-L-rhamnopyranosyl-(1 → 4)-β-D-
3
/
glucopyranosyl-(1 → 6)-β-D-glucopyranosyl ester (14)
2
4
White amorphous powder; [
α
]
D
= ꢀ 5.00 (c = 0.0010 g/mL,
13
2
1
MeOH); H NMR (C
5 5 2 5 5
D N: D O (20 : 1), 600 MHz) and C NMR (C D N:
2
O
D
2
O (20 : 1), 150 MHz) data: see Table 2. HRESIMS: m/z 965.4944
+
(
R
[M+Na] (calcd for C48
78
H O18Na, 965.5986).
1
2.4. Acid hydrolysis and GC analysis
2
R
◦
R
Each saponin (ca. 0.5 mg) was heated in 1 M HCl (0.1 mL) at 90 C for
3 h. The reaction mixture was dried in vacuo and dissolved in pyridine
R
R
(0.2 mL). TMS-imidazole (50
μ
L) was added to the part of solution (0.1
◦
2
R
mL) then heated at 50 C for 30 min. The reaction mixture was diluted
R
2
with H O (0.2 mL) and extracted with hexane (0.1 mL) then analysed by
R
R
GC-MS by comparison with standard samples derivated in the same
on the similarities observed on TLC profiles of subfraction B2 and frac-
tion C, they were combined and the resulting fraction was subjected to
conditions. L-Cysteine methyl ester hydrochloride (ca. 1.0 mg) was
◦
added to the remaining pyridine solution (0.1 mL) and heated at 60 C
MPLC on normal phase silica gel using CHCl
3
/MeOH/H
2
O (90 : 10: 5
for 1 h then the TMS derivative was prepared the same manner
then 70 : 30: 0.5) as elution systems to obtain six subfractions named C1
R
mentioned above and analysed by GC-MS. D-glucose (t 19.51 min) and
2

B.K. Ponou et al.
Carbohydrate Research 502 (2021) 108279
Table 1
1
13
H and C NMR data of compounds 1–3 (C
5 5
D
N: D
2
O (20 : 1), 600 MHz, 150 MHz).
1
2
3
1
3
1
13
1
13
1
Position
C
H (multiplicity, J in Hz)
C
H (multiplicity, J in Hz)
C
H (multiplicity, J in Hz)
1
2
3
4
5
6
7
8
9
38.8
26.2
88.8
39.8
55.6
18.2
32.9
39.2
47.8
36.6
23.8
125.8
138.2
42.2
28.5
24.3
48.1
53.0
38.7
39.1
30.5
36.0
28.0
16.8
15.5
17.2
23.5
176.1
16.8
21.1
0.86 (m), 1.44 (m)
1.85 (m), 2.27 (m)
3.42 dd (11.7, 4.5)
–
38.8
25.8
82.2
43.0
47.2
17.9
32.9
39.8
47.6
36.6
23.6
125.9
138.5
42.3
28.5
24.0
48.2
53.0
39.1
38.7
30.5
36.4
64.1
13.4
16.5
17.5
23.5
176.4
16.5
21.8
0.94 (m), 1.50 (m)
38.7
27.1
73.0
42.5
48.2
18.3
32.9
39.9
47.8
36.8
23.5
125.8
138.1
42.3
28.5
24.3
48.2
53.0
38.9
38.7
30.5
36.5
67.2
12.8
16.0
17.6
23.5
176.3
17.1
21.0
1.00 (m), 1.57 (m)
1.96 (m), 2.34 (m)
1.94 (m)
4.25, (o)
4.19 (o)
–
–
0.78 (br d)
1.27 (m), 1.44 (m)
1.35 (m), 1.49 (m)
–
1.63 (br d)
1.32 (m), 1.65 (m)
1.35 (m), 1.71 (m)
–
1.49 (br d)
1.37 (m), 1.60 (m)
1.36 (m), 1.66 (m)
–
1.54 (m)
1.65 (m)
–
1.67 (m)
1
1
1
1
1
1
1
1
1
1
2
2
2
2
2
2
2
2
2
2
3
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
–
–
1.92 (m)
1.92 (m)
5.46 (br s)
–
1.95 (m)
5.46 (br s)
–
5.47
–
–
–
–
1.20 (m)
1.14 (m)
2.04 (m)
–
1.15 (m), 2.39 (m)
2.04 (m)
2.00 (m)
–
–
2.51 (d, 11.4)
1.42 (m)
2.49 (d, 11.1)
1.39 (m)
0.88 (m)
1.23 (m), 1.37 (m)
1.76 (m), 1.91 (m)
3.68 (d, 10.9), 4.31(o)
0.95 (s)
2.51 (d, 11.3)
1.38 (m)
0.91 (m)
0.85 (m)
1.28 (m), 1.38 (m)
1.77 (m), 1.92 (m)
1.31 (s)
1.23 (m), 1.36 (m)
1.79 (m), 1.93 (m)
3.68 (d, 10.9), 4.14 (o)
1.03 (s)
1.01 (s)
0.86 (s)
0.94 (s)
1.00 (s)
1.12 (s)
1.14 (s)
1.17 (s)
1.21 (s)
1.16 (s)
1.13 (s)
–
–
–
0.97 (d, 6.4)
0.93 (d, 6.2)
0.94 (d, 5.9)
0.89 (d, 5.6)
0.92 (d, 6.4)
0.86 (d, 5.6)
1
1
1
1
’
106.5
4.94 (d, 7.8)
4.06 (o)
105.4
75.3
78.1
71.2
77.8
62.3
95.3
73.4
78.0
70.3
77.5
69.0
104.3
74.7
76.1
78.1
76.7
60.9
102.3
72.0
72.1
73.3
70.0
18.2
5.15 (d, 7.8)
4.06 (o)
7
7
7
7
6
5.2
8.2
1.5
6.1
2.5
4.33 (o)
4.24 (o)
4.20 (o)
4.20 (o)
4.12 (o)
3.95 (o)
4.37 (o), 4.59 (dd, 11.8, 2.3)
6.16 (d, 8.2)
4.14 (o)
4.35 (o), 4.59 (dd, 11.8; 2.3)
6.14 (d, 8.2)
4.14 (o)
’’
95.1
95.3
73.3
78.0
70.4
77.5
69.0
104.7
74.7
77.8
71.1
78.0
62.2
6.17 (d, 8.2)
4.16 (o)
7
7
7
7
6
3.4
8.0
0.3
7.5
8.7
4.26 (o)
4.26 (o)
4.26 (o)
4.32 (o)
4.32 (o)
4.32 (o)
4.09 (o)
4.09 (o)
4.10 (m)
4.31 (o), 4.65 (o)
4.97 (d, 7.6)
3.96 (dd, 9.0; 8.0)
4.13 (o)
4.31 (o), 4.65 (o)
4.97 (d, 7.6)
3.95 (dd, 9.0; 8.0)
4.12 (o)
4.31 (o), 4.71 (dd, 11.2, 1.8)
5.01 (d, 7.1)
4.01 (dd, 8.8, 8.0)
4.18 (o)
′′′
104.3
7
7
7
7
6
4.7
6.1
8.1
6.5
0.7
4.32 (o)
4.32 (o)
4.15 (o)
3.64 (m)
3.63 (m)
3.90 (m)
4.06 (o), 4.20 (o)
5.79 (br s)
4.67 (o)
4.06 (o), 4.19 (o)
5.77 (br s)
4.67 (o)
4.31 (o), 4.47 (dd, 11.9; 2.3)
′′′’
102.3
7
7
7
7
1
2.0
2.1
3.4
0.8
8.2
4.54 (dd, 9.3; 3.4)
4.34 (o)
4.54 (dd, 9.3; 3.4)
4.34 (o)
4.88 (m)
4.88 (m)
1.68 (d, 6.2)
1.68 (d, 6.0)
L-rhamnose (t
4 while only D-glucose was present in 3 and 5.
Standard TMS-Sugars (t , min).
TMS-glucose, t
= 14.27; TMS-rhamnose, t
Standard TMS-Thiazolidine Derivatives (t , min).
D -glucose, t = 19.64; L-rhamnose, t
= 19.51; L-glucose, t
D-rhamnose, t
= 18.43.
R
18.28 min) were characterized for compounds 1, 2, 4 and
2
containing 5% CO . FBS was purchased from Nichirei Bioscience Inc.
1
(Tokyo, Japan). Cell viability was determined by a Cell-Titer 96 Aqueous
Non-Radioactive Cell Proliferation (MTS) Assay (Promega, WI, U.S.A.)
R
4
R
R
= 11.20.
according to the manufacturer’s protocol. HeLa cells (1 × 10 cells/well)
R
were seeded in 96 well plates and incubated for 24 h, subsequently
grown with compounds for additional 48 h, and then cell proliferation
assay was performed [16]. Cells were counted after 24h then, after 48h.
Cisplatin was used as a reference drug.
R
R
R
= 18.29;
R
2
.5. Antiproliferative assay
3
. Results and discussion
Human malignant epithelial cells (HeLa) were cultured in Eagle’s
The crude methanol extract of the leaves of S. mannii was repeatedly
minimum essential medium (EMEM) supplemented with 10% fetal
subjected to column chromatography to afford fifteen compounds
bovine serum (FBS) kept in an incubator at 37 ◦C in a humidified air
3

B.K. Ponou et al.
Carbohydrate Research 502 (2021) 108279
Table 2
1
13
H and C NMR data of compounds 4, 5 and 14 (C
5
5 2
D N: D O (20 : 1), 600 MHz, 150 MHz).
4
5
14
1
3
1
13
1
13
1
Position
C
H (multiplicity, J in Hz)
C
H (multiplicity, J in Hz)
C
H (multiplicity, J in Hz)
1
2
3
4
5
6
7
8
9
38.5
26.8
71.5
56.2
47.5
20.9
33.6
41.3
50.5
36.9
21.0
25.8
38.1
42.6
29.8
32.0
56.7
49.5
47.2
150.7
30.6
36.5
207.7
9.2
1.02 (m), 1.64 (m)
36.6
26.5
89.1
39.3
50.8
18.0
29.5
33.7
50.0
35.4
23.9
118.3
145.8
43.6
30.0
26.2
49.5
21.4
12.9
48.6
12.2
72.8
29.7
128.9
133.2
21.7
67.6
27.4
15.6
27.2
1.03 (m), 1.54 (m)
40.3
24.7
79.3
40.5
57.1
19.6
34.7
41.3
48.5
37.1
25.1
124.0
145.6
42.5
37.1
75.3
50.4
42.5
48.5
32.0
33.2
29.0
29.9
17.7
16.9
18.8
28.4
177.4
34.3
25.9
0.96 (m), 1.52 (m)
1.92 (m), 1.99 (m)
1.86 (m), 2.35 (m)
1.96 (o)
4.12 (o)
3.49 (dd, 11.7; 3.9)
4.17
–
–
–
0.78
1.38 (o)
1.38 (o)
0.94 (m), 1.33 (m)
1.47 (m)
1.44
1.20 (m), 1.36 (m)
2.43 (m)
1.34, 1.51
–
–
–
1.74
1.42 (dd, 9.1, 3.6)
1.38 (o)
1
1
1
1
1
1
1
1
1
1
2
2
2
2
2
2
2
2
2
2
3
0
1
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
–
–
–
1.15 (m), 1.47 (m)
1.15 (m), 1.86 (m)
2.62 (m)
2.10 (m)
5.30 (br s)
–
1.95 (o)
5.56 (br s)
–
–
–
–
1.18 (m), 1.97 (m)
1.52 (m), 2.66 (m)
–
2.44 (m)
1.85 (m)
3.60 (br s)
0.92 (s)
1.76 (o), 2.45 (br d)
5.26 (brs)
–
1.74 (m)
3.44 (dd, 14.4; 4.2)
1.29 (o), 2.71 (m)
–
2.06 (m), 2.35 (m)
1.82 (m)
1.14 (s)
3.38 (td, 11.0, 5.0)
–
1.43 (m), 2.16 (m)
1.51 (m), 2.23 (m)
9.63 (s)
0.74 (s)
2.21 (m)
1.22 (d, 6.7)
4.07 (m)
2.44 (m), 2.58 (m)
5.88 (t, 7.3)
–
1.34 (s)
0.97 (s)
16.1
16.2
14.6
174.9
109.7
19.2
1.10 (s)
0.89 (s)
0.82 (s)
2.01 (s)
1.08 (s)
1.03 (s)
4.66 (d, 11.6), 4.75 (d, 11.6)
1.30 (s)
1.73 (s)
–
–
4.77 (br s), 4.89 (br s)
1.76 (s)
1.12 (s)
0.91 (s)
1.07 (s)
0.98 (s)
1
1
1
1
’
106.4
4.98 (d, 7.8)
4.08 (o)
7
7
7
7
6
4.3
7.9
1.2
7.9
2.0
4.28 (o)
4.21 (o)
3.95 (m)
4.39 (o), 4.56 (o)
4.92 (d, 7.8)
4.08 (o)
’’
94.9
6.32 (d, 8.2)
4.11 (o)
103.0
74.3
77.9
71.2
77.9
62.0
96.9
74.9
79.2
71.6
79.6
70.2
105.4
76.2
77.5
79.4
78.1
62.3
103.8
73.5
73.6
74.8
71.5
19.6
6.15 (d, 8.3)
4.01 (o)
7
7
7
7
6
3.6
8.2
0.2
7.9
8.9
4.29 (o)
4.29 (o)
4.18 (o)
4.34 (o)
4.22 (o)
4.23 (o)
4.10 (o)
4.03 (m)
4.17 (o)
4.30 (o), 4.67 (o)
4.95 (d, 7.9)
3.93 (dd, 9.0; 8.0)
4.11 (o)
4.39 (o), 4.56 (o)
4.25 (o), 4.59 (o)
4.91 (d, 7.9)
3.87 (dd, 9.0; 8.0)
4.06 (o)
′′′
104.4
7
7
7
7
6
4.7
6.0
7.9
6.6
0.9
4.10 (o)
4.25 (o)
3.61 (m)
3.56 (m)
4.06 (dd, 12.2; 3.7), 4.18 (o)
5.77 (brs)
4.00 (o), 4.12
5.72 (brs)
′′′’
102.4
7
7
7
7
1
2.0
2.1
3.3
0.1
8.2
4.67 (o)
4.61 (o)
4.54 (dd, 9.3; 3.3)
4.33 (o)
4.48 (dd, 9.3; 3.4)
4.27 (o)
4.87 (m)
4.83 (m)
1.68 (d, 6.2)
1.62 (d, 6.2)
including five new triterpenoid saponins, mannioside B (1), mannioside
C (2), mannioside D (3), mannioside E (4), mannioside F (5), and ten
3.1. Structure elucidation
known compounds, scheffursoside
yurs-12-en-28-oic acid β-D-glucopyranosyl ester (7) [22], 3β,23-dihy-
droxyurs-12-en-28-oic acid -L-rhamnopyranosyl-(1
)-β-D-glucopyranosyl-(1 6)-β-D-glucopyranosyl ester (8) [23],
bafouoside B (9) [3], bafouoside A (10) [3], cirenshenoside S (11) [24],
pulsatilloside C (12) [25], cussonoside A (13) [2], echinocystic acid
C
(6) [10], 3β,23-dihydrox-
Compound 1 was isolated as a white amorphous powder. The mo-
lecular formula C54
H
88
O
22 was deduced from its HRESIMS spectrum
+
α
→
which showed a pseudo molecular ion peak at m/z 1111.5371 [M+Na]
1 13
4
→
(calcd for C54
H
88
O
22Na, 1111.5665). On the basis of the H and
C
NMR spectral data (Table 1), compound 1 was identified as an urs-12-
ene type pentacyclic triterpene saponin, and this was further
confirmed by comparison of its NMR data with those of known urs-12-
ene derivatives [27].
α
-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-gluco-
pyranosyl ester (14) [21] and 3β,23-dihydroxyolean-12-en-28-oic acid
β-D-glucopyranosyl ester (15) [26]. Their structures were determined
The aglycone of 1 was identified as 3β-hydroxyurs-12-en-28-oic acid
1
1
1
13
using MS, 1D and 2D NMR experiments ( H, H COSY, TOCSY, ROESY,
and all the H and C NMR spectral data were in good agreement with
HSQC, HMBC) and chemical methods.
literature values [28]. Signals of four anomeric protons at δ 4.94 (d, J =
′
′′
′′′
7
.8, H-1 ), 6.16 (d, J = 8.2, H-1 ), 4.97 (d, J = 7.6, H-1 ) and 5.79 (brs,
4

B.K. Ponou et al.
′′
Carbohydrate Research 502 (2021) 108279
′
H-1 ’) were also observed, giving HSQC correlations with four anomeric
carbons at δ 106.5, 95.1, 104.3 and 102.3, respectively. The identifica-
tion of protons belonging to each sugar unit was achieved via TOCSY
experiment and their assignment to the respective carbon atoms was
saponins from Araliaceae species showed that, the sugar chains are
preferably attached at C-3 and C-28 [4,6,7,28–30]. In the case of tri-
terpenoid saponins having betulinic, oleanolic or ursolic acid as agly-
cone, C-3 of the aglycone resonates at about 88.8 ppm [28,31,32]. The
downfield shift observed for C-3 (δ 88.8) and the upfield shift for C-28 (δ
176.2) (Table 1) reflected the bidesmosidic nature of compound 1.
Furthermore, the HMBC correlations observed between the anomeric
1
1
deduced from H, H COSY and HSQC experiments starting from
anomeric protons. The analysis of the chemical shifts of the sugar part
allowed the identification of three glucopyranosyl (Glc) and one rham-
nopyranosyl (Rha) units. The β anomeric configuration of the gluco-
pyranosyl units was deduced from their coupling constants ranged
′
′′
protons at δ 4.94 (H-1 ) and 6.16 (H-1 ) and carbons at δ 88.8 (C-3) and
176.2 (C-28), respectively evidenced the linkage positions of the sugar
chains. The interglycosidic linkage sites of the sugar chain at C-28 were
deduced from additional HMBC correlations observed between the
between 7 and 8 Hz, while the
α
configuration was assigned to the
rhamnopyranosyl unit because its anomeric proton appeared as a broad
singlet. Extensive survey of bidesmosidic pentacyclic triterpenoid
′
′′
′′′
anomeric protons at δ 4.97 (H-1 ) and 5.79 (H-1 ’), and carbons at δ
Fig. 1. Structures of compounds 1–15.
5

B.K. Ponou et al.
Carbohydrate Research 502 (2021) 108279
′
′
′′′
6
8.7 (C-6 ) and δ 78.1 (C-4 ), respectively. This sugar chain is
commonly found in triterpenoid saponins from Araliaceae species [23,
8,33]. The remaining glucopyranosyl unit was then attached to C-3 of
2
the aglycone. The absolute configuration was determined to be D for
glucose and L for rhamnose by GC analysis (see experimental). Thus, the
structure of compound 1 was elucidated as 3β-[(β-D-glucopyranosyl)
oxy]urs-12-en-28-oic acid
α-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyr-
anosyl-(1 → 6)-β-D-glucopyranosyl ester, a new triterpenoid saponin
trivially named mannioside B.
Compound 2 was obtained as a white amorphous powder. Its HRE-
+
SIMS showed the ion cluster at m/z 1127.5289 [M+Na] (calcd for
54 88
C H O23Na, 1127.5614). Compared to 1, compound 2 has an addi-
1
13
tional oxygen atom. Both H and C NMR data (Table 1) revealed
compound 2 to be an oxidized form of 1 in which one of the methyl
groups was converted to a hydroxymethylene. The upfield shift observed
for C-3 (δ 82.2) in 2 with respect to 1 (δ 88.8) in addition to the HMBC
3
cross peak correlation observed between H C-24 (δ 0.95, s) and the
hydroxymethylene group signal at δ 64.1 as well as the C-3 (δ 82.2)
chemical shift confirmed the hypothesis and ascertained the position of
the hydroxymethylene at C-23. Thus the structure of compound 2 was
established as 3β-[(β-D-glucopyranosyl)23-dioxy]urs-12-en-28-oic acid
Fig. 2. Important ROESY correlations of the aglycones of 4 and 5.
[
35] and Acanthopanax koreanum [37]. Important ROESY correlations of
the aglycone of 4 are shown in Fig. 2.
α
-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-gluco-
Compound 5 was isolated as a white amorphous powder. Its molecular
pyranosyl ester, a new triterpenoid saponin trivially named mannioside
C. Compound 2 is an ursane-type isomer of tanguticoside A (oleanane-
type) previously isolated from Clematis tangutica (Ranunculaceae) [34].
Compound 3 was isolated as a white amorphous powder. Its HRE-
formula C42
H
70
O
13 was deduced from its HRESIMS spectrum which
+
exhibited a pseudo molecular ion peak at m/z 805.4671 [M+Na] (calcd
70
for C42H O
13Na, 805.4714). On the basis of 1H and C NMR spectral
13
+
data (Table 2), compound 5 was identified as a protostane type-
SIMS showed the pseudomolecular ion at m/z 819.4386 [M+Na]
1
triterpenoid. Its H NMR spectrum showed six tertiary methyl groups at
(
68
calcd for C42H O14Na, 819.4507). The difference of 308.0903 a.m.u
observed between 2 and 3 suggested the loss of two sugars units,
including one hexose and one deoxyhexose from 2. The above sugges-
′
1
13
tion was further confirmed by H and C NMR spectral data, showing
compounds 2 and 3 to have the same aglycone. Nevertheless, the main
difference appeared in the sugar parts where compound 3 displayed
′
signals of only two anomeric protons at δ 6.17 (d, J = 8.2, H-1 ) and 5.01
′
′
(
d, J = 7.8, H-1 ) giving HSQC correlations with two anomeric carbons
at 95.3 and 104.7, respectively. Full inspection of the sugar part allowed
to identify two β-glucopyranosyl units. The HMBC correlations observed
′
′′
from the anomeric protons at δ 6.17 (H-1 ) and 5.01 (H-1 ), to carbons at
′
δ 176.3 (C-28) and 69.0 (C-6 ) allowed to attach the sugar chain as
shown in Fig. 1. The structure of compound 3 was then established as
3
β,23-dihydroxyurs-12-en-28-oic acid β-D-glucopyranosyl-(1 → 6)- β-D-
glucopyranosyl ester, a new monodesmosidic triterpenoid saponin
trivially named mannioside D.
Compound 4 was obtained as a white powder and its HRESIMS
+
exhibited a pseudomolecular ion peak at m/z 963.4726 [M+Na] , cor-
responding to the molecular formula
48 76
C H O18Na (calcd for
1
13
C
48
H
76
O18Na, 963.4929). Taken together the H and C NMR data
1.22) to C-22 (δ 72.8). The C-3, C-8 and C-14 configurations were evi-
(
Table 2), compound 4 was deduced to be a lupane-type triterpenoid
denced by the ROESY spectrum in which correlations were observed
glycoside [1,25,29,35]. Based on the 1D and 2D NMR data, the aglycone
of 4 was identified as 3β-hydroxy-23-oxolup-20(29)-en-28-oic acid [35].
The β orientation of the hydroxy group at C-3 was firstly suggested by
the upfield shifts observed for C-3 (δ 71.5) and C-24 (δ 9.2) with respect
between Me-19 (δ 0.74) which is biogenetically β oriented and Me-30 (δ
1
.07), H-5 (
at C-22 was determined via the ROESY correlation depicted between
H-17, Me-21 (which are biogenetically oriented) and H-22. From the
above information, the aglycone was recognized to be (22S)-protosta-12,
4-diene-3β,22,27-triol. The ring proton of each monosaccharide residue
was assigned starting from the readily identifiable anomeric protons using
α
oriented) with H-3 and Me-18 (Fig. 2). The stereochemistry
α
to the
5.0 [35,36], respectively. The above suggestion was further confirmed
by the ROESY spectrum through the cross peak correlation observed
between H-3 and H-5, since H-5 is biogenetically oriented in penta-
cyclic triterpenoids (Fig. 2). The sugar sequence was established as
α orientation in which C-3 and C-24 resonates at about δ 73.0 and
1
2
α
1
1
1
1
H, H COSY, HSQC and TOCSY spectra. Extensive analysis of H, H
coupling constants as well as 2D experiments followed by comparison of
α
-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-gluco-
1
13
H and C NMR data (Table 2) with those reported in the literature
pyranosyl, commonly found in triterpenoid saponins from Araliaceae
revealed the presence of β-glucopyranosyl moieties. The absolute
configuration was determined to be D by GC analysis. The linkage sites of
the sugars were determined by HMBC correlations observed between the
species [23,28,33] and its location at C-28 of the aglycone was deduced
′
from the HMBC correlation between H-1 and C-28. The structure of 4
was then determined as 3β-hydroxy-23-oxolup-20(29)-en-28-oic acid
′
′′
anomeric protons at δ 4.98 (H-1 ), 4.92 (H-1 ) and at δ 89.1 (C-3), 67.6
α
-L-rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-gluco-
(C-27), respectively. Thus, the structure of
5 was elucidated as
pyranosyl ester, a new monodesmosidic triterpenoid saponin trivially
named mannioside E. However, an epimer of 4 at C-3 trivially named
wujiapioside A was previously reported from Acanthopanax gracilistylus
(22S)-27β-[(β-D-glucopyranosyl)oxy]-22-hydroxyprotosta-12,24-dien-3β-
yl β-D-glucopyranoside, a new bidesmosidic triterpenoid saponin trivially
6

B.K. Ponou et al.
Carbohydrate Research 502 (2021) 108279
named mannioside F.
[8] S.G. Sparg, M.E. Light, J.V. Staden, Biological activities and distribution of plant
saponins, J. Ethnopharmacol. 94 (2004) 219–243, https://doi.org/10.1016/j.
jep.2004.05.016.
The isolation of triterpenoid saponins from this plant is in good
agreement with results previously obtained from Schefflera species with
[
9] G.M. Plunkett, P.P. Lowry II, D.G. Frodin, J. Wen, Phylogeny and geography of
Schefflera: pervasive polyphyly in the largest genus of araliaceae, Ann. Mo. Bot.
Gard. 92 (2005) 202–204. https://www.jstor.org/stable/3298514.
the prevalence of triterpenoid saponins having the sugar sequence -L-
α
rhamnopyranosyl-(1 → 4)-β-D-glucopyranosyl-(1 → 6)-β-D-glucopyr-
anosyl at C-28 [4,10,12]. Protostane type triterpenoids were isolated
from plants belonging to the genera Alisma (Alismataceae) [39–42] and
Garcinia (Guttiferae) [38]. To the best of our knowledge, this is the first
report on the isolation of a protostane type triterpenoid from a plant of
the Araliaceae family. However, their stereoisomers (Dammarane) were
previously isolated from Panax species (Araliaceae) [43–45].
[
10] C. Maeda, K. Ohtani, R. Kasai, K. Yamasaki, M.N. Due, T.N. Nhamt, Q.K.N. Cu,
Oleanane and ursane glycosides from Schefflera octophylla, Phytochemistry 37
(1994) 1131–1137, https://doi.org/10.1016/S0031-9422(00)89543-6.
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[
[
12] C. Wu, Y.-H. Duan, M.-M. Li, W. Tang, X. Wu, G.-C. Wang, W.-C. Ye, G.-X. Zhou, Y.-
L. Li, Triterpenoid saponins from the stem barks of Schefflera heptaphylla, Planta
Med. 79 (2013) 1348–1355, https://doi.org/10.1055/s-0033-1350674.
13] M. Cheek, Schefflera mannii. The IUCN red list of threatened species, e.
T45425A10997220, https://www.iucnredlist.org/species/45425/10997220,
[
2
004. (Accessed 17 July 2020).
3
.2. Biological activity
[14] L.A. Tapondjou, L.B.T. Nyaa, P. Tane, M. Ricciutelli, L. Quassinti, M. Bramucci,
G. Lupidi, B.K. Ponou, L. Barboni, A.-C. Parkioside, Cytotoxic and antioxidant
triterpene saponins from Butyrospermum parkii (Sapotaceae), Carbohydr. Res. 346
Given the fact that saponins from Araliaceae species have been
(
2011) 2699–2704, https://doi.org/10.1016/j.carres.2011.09.014.
shown to be antiproliferative against human malignant epithelial cells
HeLa) [46,47], the major isolated compounds were tested for their
[
15] R.T. Fouedjou, R.B. Teponno, L. Quassinti, M. Bramucci, D. Petrelli, L.A. Vitali,
D. Fiorini, L.A. Tapondjou, L. Barboni, Steroidal saponins from the leaves of
Cordyline fruticosa (L.) A. Chev. and their cytotoxic and antimicrobial activity,
Phytochem. Lett. 7 (2014) 62–68, https://doi.org/10.1016/j.phytol.2013.10.001.
16] R.B. Teponno, C. Tanaka, B. Jie, L.A. Tapondjou, T. Miyamoto, A.-
J. Trifasciatosides, Steroidal saponins from Sansevieria trifasciata, Chem. Pharm.
Bull. 64 (2016) 1347–1355, https://doi.org/10.1248/cpb.c16-00337.
(
antiproliferative activity on HeLa cells. All the compounds were not
efficient at the concentration of 33 mM. These observations are in good
agreement with other screening results for anti-inflammatory, cytotoxic,
antimicrobial and molluscicidal activities of triterpenoid derivatives
which established that the presence of sugar(s) bound to the 28-COOH
group considerably decreases their activity [48–51] when sugar chains
attached at C-3 and having at least three sugar units increase the anti-
proliferative activity of saponins [52].
[
[
17] R.B. Teponno, J.P. Dzoyem, N.N. Raymond, U. Kauhl, L.P. Sandjo, L.A. Tapondjou,
U. Bakowsky, T. Opatz, Cytotoxicity of secondary metabolites from Dracaena
viridiflora Engl & Krause and their semisynthetic analogues, Record Nat. Prod. 11
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[
[
18] B.K. Ponou, L. Barboni, R.B. Teponno, M. Mbiantcha, T.B. Nguelefack, H.-J. Park,
K.T. Lee, L.A. Tapondjou, Polyhydroxyoleanane-type triterpenoids from Combretum
molle and their anti-inflammatory activity, Phytochem. Lett. 1 (2008) 183–187,
https://doi.org/10.1016/j.phytol.2008.09.002.
19] B.K. Ponou, R.B. Teponno, M. Ricciutelli, L. Quassinti, M. Bramucci, G. Lupidi,
L. Barboni, L.A. Tapondjou, Dimeric antioxidant and cytotoxic triterpenoid
saponins from Terminalia ivorensis, A. Chev. Phytochemistry 71 (2010) 2108–2115,
https://doi.org/10.1016/j.phytochem.2010.08.020.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
[20] B.K. Ponou, R.B. Teponno, L.A. Tapondjou, M.-A. Lacaille-Dubois, L. Quassinti,
M. Bramucci, L. Barboni, Steroidal saponins from the aerial parts of Cordyline
fruticosa L. var. strawberries, Fitoterapia 134 (2019) 454–458, https://doi.org/
1
0.1016/j.fitote.2019.03.019.
[
21] Y.-G. Xia, G.-Y. Li, J. Liang, C.A. Ortori, B.-Y. Yang, H.-X. Kuang, D.A. Barrett,
A strategy for characterization of triterpene saponins in Caulophyllum robustum
hairy roots by liquid chromatography with electrospray ionization quadrupole
time-of-flight mass spectrometry, J. Pharmaceut. Biomed. 100 (2014) 109–122,
https://doi.org/10.1016/j.jpba.2014.07.024.
Acknowledgements
Dr. B. K. Ponou is grateful to The Matsumae International Founda-
tion (MIF) for financing a postdoctoral research stay (6 months) at the
Graduate School of Pharmaceutical Sciences, Kyushu University, Japan.
[
[
22] H. Yang, E.J. Jeong, J. Kim, S.H. Sung, Y.C. Kim, Antiproliferative triterpenes from
the leaves and twigs of Juglans sinensis on HSC-T6 cells, J. Nat. Prod. 74 (2011)
7
51–756, https://doi.org/10.1021/np1008202.
23] I.I. Dovgii, V.I. Grishkovets, V.V. Kachala, A.S. Shashkov, Tripterpene glycosides A,
Appendix A. Supplementary data
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