Triterpene saponins from Salsola imbricata

Article abstract of DOI:10.1016/j.phytol.2011.07.010

Continuing our investigations on medicinal plants of the Egyptian desert, two new triterpene glycoside derivatives, along with three known compounds have been isolated from the roots of Salsola imbricata, a shrub widely growing in Egypt. Their structures have been established as 3-O-β-d-xylopyranosyl-(1 → 2)-O-β-d-glucuronopyranosyl-akebonic acid 28-O-β-d- glucopyranoside and 3-O-β-d-xylopyranosyl-(1 → 2)-O-β-d- glucuronopyranosyl-29-hydroxyoleanolic acid 28-O-β-d-glucopyranoside on the basis of spectroscopic methods including 1D- (¹H, ¹³C) and 2D-NMR (DQF-COSY, HSQC, HMBC) experiments as well as mass spectrometry analysis.

Full text of DOI:10.1016/j.phytol.2011.07.010

Phytochemistry Letters 4 (2011) 353–356
Contents lists available at ScienceDirect
Phytochemistry Letters
journal homepage: www.elsevier.com/locate/phytol
Triterpene saponins from Salsola imbricata
Arafa I. Hamed a, ,1, Milena Masullo b,1, Mohamed G. Sheded a, Usama A. Mahalel a, Moatz M. Tawfik a,
b,**
*
Angela Perrone b, Sonia Piacente
a Faculty of Science, South Valley University, Aswan 81528, Egypt
b
`
Dipartimento di Scienze Farmaceutiche e Biomediche, Universita degli Studi di Salerno, Via Ponte Don Melillo, I-84084 Fisciano, Salerno, Italy
A R T I C L E I N F O
A B S T R A C T
Article history:
Continuing our investigations on medicinal plants of the Egyptian desert, two new triterpene glycoside
Received 28 April 2011
Received in revised form 18 July 2011
Accepted 20 July 2011
derivatives, along with three known compounds have been isolated from the roots of Salsola imbricata, a
shrub widely growing in Egypt. Their structures have been established as 3-O-
(1 ! 2)-O- -glucuronopyranosyl-akebonic acid 28-O- -glucopyranoside and 3-O-
syl-(1 ! 2)-O- -glucuronopyranosyl-29-hydroxyoleanolic acid 28-O- -glucopyranoside on the
b
-
D-xylopyranosyl-
b
-D
b
-
D
b-D-xylopyrano-
Available online 3 August 2011
b
-
D
b-D
basis of spectroscopic methods including 1D- (1H, 13C) and 2D-NMR (DQF-COSY, HSQC, HMBC)
experiments as well as mass spectrometry analysis.
Keywords:
Salsola imbricata
ß 2011 Phytochemical Society of Europe. Published by Elsevier B.V. All rights reserved.
Triterpene glycosides
Noroleanene-type triterpenes
1. Introduction
and S. collina (Tundis et al., 2009; Zhao and Ding, 2004), flavonoids
and other phenolic compounds from S. kali, S. soda, S. oppositifolia
Plants belonging to the genus Salsola (Family: Chenopodiaceae)
are common in the arid and semiarid regions of our planet and
about 15 different Salsola species are found in Egypt (Boulos, 1999).
Typically, these plants grow on flat, often dry and/or somewhat
saline soils, with some species in salt marshes. Salsola imbricata
Forssk. subsp. imbricata (syns = Chenopodium baryosmum = Salsola
foetida = Caroxylon imbricata = Salsola baryosma) is a shrub widely
growing in Egypt, known with the Arabic name ‘‘Harm’’, and used
as a good camel food (Ta¨ckholm, 1974; Batanouny, 1999). The
aqueous extracts of Salsola species are used in traditional medicine
as an oral contraceptive by Bushmen women in Namibia and in the
Republic of South Africa (Swart et al., 2003). In the middle East,
Salsola baryosma is used against inflammations and as a diuretic
agent (Al-Saleh et al., 1993). It has also been reported to possess
antioxidant effects (Ahmad et al., 2008) and CNS depressant
activity (Woo et al., 1977).
and S. collina (Tundis et al., 2007; Xiang et al., 2007a, 2007b), and
fatty acid derivatives from S. tetrandra (Oueslati et al., 2006) have
been reported. Moreover, triterpenes with significant antioxidant
activity were isolated from S. baryosma (Ahmad et al., 2008). As a
part of our on going research on medicinal plants of the Egyptian
desert (Hamed et al., 2006; Perrone et al., 2007; Piacente et al.,
2009; Plaza et al., 2004, 2005), we carried out the phytochemical
investigation of S. imbricata.
In the present paper we describe the isolation of two new
triterpene glycosides (1 and 2) along with two known triterpene
glycosides pseudoginsenoside RT1 and silphioside G (Tanaka et al.,
1985), and one known nortriterpene glycoside boussingoside A2
(Espada et al., 1990). Their structures were elucidated by extensive
spectroscopic methods including 1D- (1H and 13C) and 2D-NMR
(DQF-COSY, HSQC, HMBC, and TOCSY) experiments as well as
ESIMS analysis.
At present, no pharmacological and phytochemical studies have
been reported for Salsola spp. growing in Egypt. Only few species
from the genus Salsola growing in other geographical areas have
been analyzed from a chemical point of view. In particular,
alkaloids from the aerial parts of S. oppositofolia, S. soda, S. tragus
2. Results and discussion
The roots of S. imbricata were extracted with 80% MeOH and the
crude extract was fractionated on RP-18 columns to yield two new
compounds (1 and 2) (Fig. 1).
The HRMALDITOF mass spectrum of 1 showed a major ion peak
at m/z 933.4065 [M+Na]+ ascribable to a molecular formula
* Corresponding author. Tel.: +20 972319811; fax: +20 3480450.
** Corresponding author. Tel.: +39 089 969763; fax: +39 089 969602.
E-mail addresses: arafahamed75@yahoo.com (A.I. Hamed), piacente@unisa.it
(S. Piacente).
C46H70O18 (calcd. for C46H70NaO18, 933.4060). The ESI-MS
spectrum showed the major ion peak at m/z 933 [M+Na]+ and
significant fragments in MS/MS analysis at m/z 625 [M+Na-132-
176]+ corresponding to the loss of one pentose and one uronic acid
1
Contributed equally to this work.
1874-3900/$ – see front matter ß 2011 Phytochemical Society of Europe. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.phytol.2011.07.010

354
A.I. Hamed et al. / Phytochemistry Letters 4 (2011) 353–356
Table 1
1H and 13C NMR data (J in Hz) of compounds 1 and 2 (600 MHz,
d ppm, in CD3OD).
Position
1
2
dC
dH (J in Hz)
dC
dH (J in Hz)
O
O
1
2
39.5
26.8
90.6
39.8
57.0
19.2
33.7
40.7
48.7
37.8
24.5
124.0
143.7
42.7
29.0
23.9
1.63, 1.03, m
2.03, 1.73, m
3.22, dd (11.5, 4.2)
–
39.6
26.8
90.4
40.1
56.8
19.1
33.7
40.5
48.8
37.6
24.3
123.8
144.6
42.5
28.7
23.7
1.62,1.02, m
2.03, 1.70, m
3
3.20, dd (11.4, 4.2)
4
–
OH
HOOC
5
0.81, m
0.79, m
O
O
O
6
1.57, 1.43, m
1.52, 1.35, m
–
1.56, 1.42, m
O
HO
HO
HO
HO
7
1.51, 1.33, m
8
–
OH
9
1.62, m
1.60, m
O
HO
10
11
12
13
14
15
16
–
–
HO
1
1.95 (2H), m
5.35, t (3.5)
–
1.92 (2H), t (3.5)
CH2OH
OH
5.29, t (3.5)
–
–
–
1.88 1.17, m
2.20, 1.88, m
1.83, 1.11, m
2.09, td (13.7, 3.0)
1.75, m
O
O
17
18
19
47.8
48.4
42.2
–
47.8
41.6
41.0
–
2.77, dd (13.3, 4.7)
2.59 t (13.3),
2.11, dd (13.3, 4.7)
–
2.91, dd (13.7, 3.3)
1.84, 1.13, m
OH
HOOC
O
O
20
21
22
23
24
25
26
27
28
29
30
149.3
30.8
38.4
28.1
16.4
15.6
17.6
26.4
177.8
107.2
–
36.7
29.1
32.3
28.0
16.3
15.8
17.4
26.2
177.5
74.1
19.3
–
O
O
HO
HO
HO
HO
2.26, 2.16, m
1.94, 1.58, m
1.08, s
1.53, 1.19, m
1.77, 1.68, m
1.07, s
OH
O
O
0.87, s
0.86, s
HO
HO
2
0.98, s
0.98, s
0.83, s
0.83, s
1.22, s
1.19, s
Fig. 1. Compounds 1 and 2 isolated from Salsola imbricata.
–
–
4.64 (2H), s
–
3.21 (2H), s
0.95, s
at m/z 463 [M+Na-132-176-162]+ attributable to the subsequent
b
-
D
-GlcA (at C-3)
b-D-GlcA (at C-3)
,
1
2
3
4
5
6
105.1
83.2
77.7
73.4
76.2
176.8
4.46, d (7.5)
3.51, dd (7.5, 9.0)
3.62, dd (9.0, 9.0)
3.49, dd (9.0, 9.0)
3.57, m
105.0
83.1
77.6
73.3
76.4
176.5
4.45, d (7.5)
3.51, dd (7.5, 9.0)
3.62, dd (9.0, 9.0)
3.49, dd (9.0, 9.0)
3.57, m
loss of one hexose unit.
The 1H NMR spectrum of the aglycone portion of 1 displayed
signals for five tertiary methyl groups at
d 0.83, 0.87, 0.98, 1.08, and
1.22, two exo-methylene protons at 4.64, an olefinic proton at
d
d
–
–
5.35 (1H, t, J = 3.5 Hz), and for a proton at
d 3.22 (1H, dd, J = 11.5,
b-
D
-Xyl (at C-2GlcA
)
b-
D
-Xyl (at C-2GlcA
)
4.2) assigned to H-3 (Table 1). The 13C NMR spectrum of 1 showed
1
2
3
4
5
106.2
76.2
77.4
70.9
66.8
4.55, d (7.5)
3.25, dd (9.2, 7.5)
3.34, t (9.2)
106.1
75.8
77.8
70.9
67.2
4.55, d (7.5)
3.25, dd (9.2, 7.5)
3.34, t (9.2)
for the aglycone 29 carbon signals which suggested a noroleanane
skeleton (Table 1). Two olefinic carbons at
143.7 (C-13) indicated
typical D12 pentacyclic triterpene
derivative (De Tommasi et al., 1998). In the HMBC spectrum of
1, the 20(29)-exo-methylene proton signal at 4.64 correlated
with two methylene carbons at 42.2 (C-19) and 30.8 (C-21) which
d 124.0 (C-12) and d
3.47, m
3.49, m
a
3.82, dd (11.7, 5.2)
3.16, t (11.7)
3.84, dd (11.7, 5.2)
3.17, t (11.7)
d
b-
D
-Glc (at C-28)
b-D-Glc (at C-28)
d
1
2
3
4
5
6
95.4
73.7
78.3
70.7
77.9
62.1
5.40, d (7.8)
95.4
73.6
78.1
70.9
78.1
62.3
5.42, d (7.8)
3.35, dd (7.8, 9.0)
3.38, dd (9.0, 9.0)
3.38, t (9.0)
3.36, dd (7.8, 9.0)
3.38, dd (9.0, 9.0)
3.39, t (9.0)
confirmed a noroleanene-type skeleton. A detailed analysis of NMR
data allowed us to determine the aglycone as the akebonic acid
(Ikuta and Itokawa, 1989).
3.44, m
3.45, m
The 1H NMR spectrum displayed in the sugar region signals
3.84, dd (2.5, 12.0)
3.71, dd (4.5, 12.0)
3.84, dd (2.5, 12.0)
3.70, dd (4.5, 12.0)
corresponding to three anomeric protons at
d 5.40 (d, J = 7.8 Hz),
4.55 (d, J = 7.5 Hz), and 4.46 (d, J = 7.5 Hz), whose carbon
resonances were assigned unambiguously by HSQC experiments
to be at
d 95.4, 106.2, and 105.1, respectively (Table 1).
Complete assignments of the resonances of each sugar unit
were achieved by extensive 1D-(1H, 13C, TOCSY) and 2D-(HSQC,
HMBC) NMR analyzes. All these data showed the presence of one
Therefore, compound 1 was identified as the new 3-O-
xylopyranosyl-(1 ! 2)-O- -glucuronopyranosyl akebonic acid
28-O- -glucopyranoside.
b-D-
b
-D
b
-D
b
-glucopyranosyl unit (
d
5.40), one
b
-xylopyranosyl unit (
d
4.55),
To the best of our knowledge, this is the first report of
compounds characterized by a C-30 noroleanane skeleton with a
C20–C29 double bond in the Salsola genus.
The HRMALDITOF mass spectrum of 2 showed a major ion peak
at m/z 965.4728 [M+Na]+ ascribable to the molecular formula
and one -glucuronic acid unit (
b
d
4.46). The configuration of
D
xylose, glucose and glucuronic acid units were established after
hydrolysis of 1 with 1 N HCl, trimethylsilation and determination
of the retention times by GC (De Marino et al., 2003).
Glycosidation shifts were observed for C-2glcA
90.6) and C-28 ( 177.8). All connectivities within 1 were
confirmed by the HMBC spectrum, which showed a long-range
correlation between H-1xyl 4.55) and C-2glcA 83.1), H-1glcA
4.46) and C-3 ( 90.6), and between H-1glc 5.40) and C-28 (
177.8), confirming the bidesmosidic character of 1.
(
d
83.1), C-3 (
d
C47H74O19 (calcd. for C47H74NaO19, 965.4722). The ESI-MS
d
spectrum showed the major ion peak at m/z 965 [M+Na]+ and
significant fragments in MS/MS analysis at m/z 657 [M+Na-132-
176]+ ascribable to the loss of one pentose and one uronic acid, and
at m/z 495 [M+Na-132-176-162]+ due to the subsequent loss of one
hexose unit. The 1H NMR spectrum of the aglycone portion of 2
(
d
(
d
(d
d
(
d
d

A.I. Hamed et al. / Phytochemistry Letters 4 (2011) 353–356
355
displayed signals attributable to six tertiary methyl groups at
0.83, 0.86, 0.95, 0.98, 1.07, and 1.19, a primary alcoholic function
at 3.21 (2H, s), and an olefinic proton at 5.29 (1H, t,
3.20 (1H, dd, J = 11.4, 4.2) was assigned
d
3.2. Plant material
d
d
The roots of S. imbricata Forssk. subsp. imbricata were collected
at Edfu-Marsa Alam road, South-Eastern Desert (Aswan, Egypt) in
February 2009 and identified by Prof. M.G. Sheded according to
Ta¨ckholm (1974) and Boulos (1999). The voucher specimen (No.
11373) was deposited at the Botany Department Herbarium,
Faculty of Science of Aswan, Egypt.
J = 3.5 Hz). A signal at
d
to H-3 (Table 1).
The 13C NMR spectrum of 2 showed for the aglycone portion 30
carbon signals. Two olefinic carbons at
d 123.8 (C-12) and d 144.6
(C-13) indicated a typical D12 pentacyclic triterpene derivative
(Table 1). In the HMBC spectrum of 2, the correlations of the
primary alcoholic proton signal at
d
3.21 with the methyl carbon at
41.0 (C-19)
3.3. Extraction and isolation
d
19.3 (C-30) and with the two methylene carbons at
d
and 29.1 (C-21) confirmed the location of the secondary alcoholic
group at C-29. Thus, the aglycone of 2 was identified as 29-
hydroxyoleanolic acid (mesembryanthemoidigenic acid), which
was confirmed by comparison with literature data (Wenjuan et al.,
1986).
The roots of S. imbricata Forssk. subsp. imbricata (1.4 kg) were
powdered and exhaustively extracted with 80% MeOH (3 Lꢀ 1.5 L)
for 20 days by maceration at room temperature. The crude extract
was concentrated under reduced pressure to a syrupy consistency
(200 g). Part of the extract (2.5 g) was fractionated on an RP-18
column (LiChroprep_ RP-18, 25-40 lm, Merck, 10 cm ꢀ 25 cm)
using H2O: MeOH as the mobile phase. Six fractions (1000 mL)
were collected 100% H2O (550 mg), 20% MeOH (624 mg), 40%
MeOH (226 mg), 60% MeOH (349 mg), 80% MeOH (333 mg), and
100% MeOH (1.411 g), respectively. Fraction obtained with 80%
MeOH contained saponins. 100 mg of this fraction from 80% was
fractioned on RP-18 column (50 ꢀ 2) eluted with 60–70% MeOH as
mobile phase to yield compounds 1 (5 mg), 2 (4.8 mg), boussingo-
side A2 (8.2 mg), pseudoginsenoside RT1 (9.2 mg), and silphioside
G (10.2 mg), respectively.
The 1H NMR spectrum displayed in the sugar region signals
corresponding to three anomeric protons at
4.55 (d, J = 7.5 Hz), and 4.45 (d, J = 7.5 Hz) (Table 1), corresponding
to one -glucopyranosyl unit, one -xylopyranosyl unit, and one
-glucuronic acid unit, respectively. The 1H NMR and 13C chemical
shifts of the sugar moiety were superimposable on those of 1. In the
HMBC spectrum long-range correlations between H-1xyl 4.55)
and C-2glcA 83.1), H-1glcA 4.45) and C-3 ( 90.4), and H-1glc
5.42) and C-28 ( 177.5) were observed. Therefore, compound 2
was identified as the new 3-O-
-xylopyranosyl-(1 ! 2)-O-
glucuronopyranosyl-29-hydroxyoleanolic acid 28-O- -gluco-
d 5.42 (d, J = 7.8 Hz),
b
b
b
(
d
(d
(
d
d
(d
d
b
-D
b-D-
b
-D
pyranoside. 29-Hydroxyoleanene glycosides, salsolins A and B,
have been also isolated from another Salsola species, S. baryosma
and have been reported to possess a significant antioxidant activity
(Ahmad et al., 2008).
Pseudoginsenoside RT, silphioside G and boussingoside A2
were identified by comparison of their 1H and 13C NMR data
with those reported in the literature (Tanaka et al., 1985; Espada
et al., 1990). Boussingoside A2 is a C-30 noroleanane derivative
with a C20–C29 double bond and, therefore, together with
compound 1 represent the first report of this kind of compounds
in a Salsola species, thus being potentially useful as chemotaxo-
nomic markers to differentiate S. imbricata in the frame of
Salsola genus.
3.4. 3-O-
b
-
D
-xylopyranosyl-(1 ! 2)-O-
b-D-glucuronopyranosyl-
-glucopyranoside (1)
akebonic acid 28-O-
b
-D
Amorphous powder; ½a D25
ꢁ
þ 45:2 (c 0.3, MeOH); 1H NMR
(CD3OD, 600 MHz) and 13C NMR (CD3OD, 150 MHz) data, see
Table 1; ESIMS m/z 933 [M+Na]+; ESIMS/MS m/z 625 [M+Na-132-
176]+, 463 [M+Na-132-176-162]+; HRMALDITOFMS m/z 933.4065
[M+Na]+ (calcd. for C46H70NaO18, 933.4060).
3.5. 3-O-
b
-D
-xylopyranosyl-(1!2)-O-
b-D-glucuronopyranosyl-29-
-glucopyranoside (2)
hydroxyoleanolic acid-28-O-
b-D
Amorphous powder; ½a D25
ꢁ
þ 31 (c 0.3, MeOH); 1H NMR (CD3OD,
600 MHz) and 13C NMR (CD3OD, 150 MHz) data, see Table 1; ESIMS
m/z 965 [M+Na]+; ESIMS/MS m/z 657 [M+Na-132-176]+, 495
[M+Na-132-176-162]+; HRMALDITOFMS m/z 965.4728 [M+Na]+
(calcd. for C47H74NaO19, 965.4722).
3. Experimental
3.1. General
Optical rotations were measured on a JASCO DIP 1000
polarimeter. NMR experiments were performed on a Bruker
3.6. Acid hydrolysis
DRX-600 spectrometer equipped with
a
Bruker 5 mm TCI
The configuration of sugar units were established after
CryoProbe at 300 K. All 2D-NMR spectra were acquired in CD3OD
(99.95%, Sigma Aldrich) and standard pulse sequences and phase
cycling were used for DQF-COSY, HSQC, HMBC and ROESY spectra.
Exact masses were measured by a Voyager DE mass spectrometer.
Samples were analyzed by matrix-assisted laser desorption
ionization time-off light (MALDITOF) mass spectrometry. A
hydrolysis of 1 and 2 with 1 N HCl, trimethylsilation and
determination of the retention times by GC operating in the
experimental conditions previously reported by De Marino et al.
(2003).
The peaks of the hydrolysate of 1 and 2 were detected at 10.99
and 12.02 (D-xylose), at 14.73 min (D-glucose) and at 15.83 min (D-
mixture of analyte solution and
a
-cyano-4-hydroxycinnamic
glucuronic acid). Retention times for authentic samples after being
treated in the same manner with 1-(trimethylsilyl)-imidazole in
acid (Sigma) was applied to the metallic sample plate and dried.
Mass calibration was performed with the ions from ACTH
(fragment 18–39) at 2465.1989 Da and angiotensin III at
931.5154 Da as internal standards. ESIMS analyses were per-
formed using a ThermoFinnigan LCQ Deca XP Max ion-trap mass
spectrometer equipped with Xcalibur software. Column chroma-
tography was performed over RP-18 (LiChroprep_ RP-18, 40–
63 lm, Merck, 2 cm ꢀ 50 cm). GC apparatus using a l-Chirasil-Val
column (0.32 mm ꢀ 25 m). TLC was performed on both silica gel
F254 (Merck) and RP-18 F254s plates, and visualized with
Liebermann–Burchard reagent.
pyridine were detected at 10.98 and 12.00 min (
D-xylose), and
14.71 min ( -glucose), 15.81 min ( -glucuronic acid).
D
D
Acknowledgments and funding
This work has been performed in the frame of the bilateral
project Italy-Egypt ‘‘Chemical-biological study of medicinal plants
growing in south-eastern desert of Egypt’’, granted by the Italian
Ministery of Foreign Affairs (MAE). The authors thank the MAE

356
A.I. Hamed et al. / Phytochemistry Letters 4 (2011) 353–356
Piacente, S., Masullo, M., De Neve, N., Dewelle, J., Hamed, A., Kiss, R., Mijatovic, T.,
2009. Cardenolides from Pergularia tomentosa display cytotoxic activity result-
ing from their potent inhibition of Na+/K+-ATPase. J. Nat. Prod. 72, 1087–1091.
Plaza, A., Piacente, S., Perrone, A., Hamed, A., Pizza, C., Bifulco, G., 2004. Stemmosides
C and D, two novel unusual pregnane glycosides from Solenostemma argel:
structural elucidation and configurational study by a combined NMR-quantum
mechanical strategy. Tetrahedron 60, 12201–12209.
Plaza, A., Perrone, A., Balestrieri, M.L., Felice, F., Balestrieri, C., Hamed, A.I., Pizza, C.,
Piacente, S., 2005. New unusual pregnane glycosides with antiproliferative
activity from Solenostemma argel. Steroids 70, 594–603.
General Management for the Cultural Promotion and Cooperation,
for its support.
References
Ahmad, Z., Mehmood, S., Fatima, I., Malik, A., Ifzal, R., Afza, N., Iqbal, L., Latif, M.,
Nizami, T.A., 2008. Structural determination of salsolins A and B, new antioxi-
dant polyoxygenated triterpenes from Salsola baryosma by 1D and 2D NMR
spectroscopy. Magn. Reson. Chem. 46, 94–98.
Swart, P., Swart, A.C., Louw, A., van der Merwe, K.J., 2003. Biological activities of the
shrub Salsola tuberculatiformis Botsch.: contraceptive or stress alleviator?
Bioessays 25, 612–619.
Ta¨ckholm, V., 1974. Students’ Flora of Egypt, 2nd ed. Cairo University, Egypt.
Tanaka, O., Morita, T., Kasai, R., Kinouchi, J., Sanada, S., Ida, Y., Shoji, J., 1985. Study on
saponins of rhizomes of Panax pseudo-ginseng subsp. himalaicus collected at
Tzatogang and Pari-la, Bhutan-Himalaya. Chem. Pharm. Bull. 33, 2323–2330.
Tundis, R., Loizzo, M.R., Statti, G.A., Menichini, F., 2007. Inhibitory effects on the
digestive enzyme alpha-amylase of three Salsola species (Chenopodiaceae) in
vitro. Pharmazie 62, 473–475.
Al-Saleh, F.S., Ali, H., Mirza, M., 1993. Chemical constituents of some medicinal
plants growing in Bahrain. Fitoterapia 64, 251–256.
Batanouny, K.H., 1999. Wild Medicinal Plants in Egypt (An Inventory to Support
Conservation and Sustainable Use). The Palm Press, Cairo, Egypt.
Boulos, L., 1999. Flora of Egypt (Azollaceae-Oxalidaceae). Al-Hadara Publishing,
Cairo, Egypt.
De Marino, S., Borbone, N., Iorizzi, M., Esposito, G., McClintock, J.B., Zollo, F., 2003.
Bioactive asterosaponins from the starfish Luidia quinaria and Psilaster cassiope.
Isolation and structure characterization by two-dimensional NMR spectrosco-
py. J. Nat. Prod. 66, 515–519.
Tundis, R., Menichini, F., Confort, F., Loizzo, M.R., Bonesi, M., Statti, G., Menichini, F.,
2009. A potential role of alkaloid extracts from Salsola species (Chenopodiaceae)
in the treatment of Alzheimer’s disease. J. Enzyme Inhib. Med. Chem. 24, 818–
824.
Wenjuan, Q., Xiue, W., Junjie, Z., Fukuyama, Y., Yamada, T., Nakagawa, K., 1986.
Triterpenoid glycosides from leaves of Ilex cornuta. Phytochemistry 25, 913–
916.
Woo, W.S., Lee, E.B., Chi, H.J., 1977. Biological evaluation of some Saudi Arabian
plants. J. Pharm. Sci. Korea 21, 141–145.
Xiang, Y., Li, Y.B., Zhang, J., Li, P., Yao, Y.Z., 2007a. Studies on chemical constituents of
Salsola collina. Zhongguo Zhong Yao Za Zhi 32, 409–413.
De Tommasi, N., Piacente, S., Gacs-Baitz, E., De Simone, F., Pizza, C., Aquino, R., 1998.
Triterpenoid saponins from Spergularia ramosa. J. Nat. Prod. 61, 323–327.
Espada, A., Rodriguez, J., Villaverde, M.C., Riguera, R., 1990. Hypoglucemic triter-
penoid saponins from Boussingaultia baselloides. Can. J. Chem. 68, 2039–2044.
Hamed, A.I., Plaza, A., Balestrieri, M.L., Mahalel, U.A., Springuel, I.V., Oleszek, W.,
Pizza, C., Piacente, S., 2006. Cardenolide glycosides from Pergularia tomentosa
and their proapoptotic activity in Kaposi’s sarcoma cells. J. Nat. Prod. 69, 1319–
1322.
Ikuta, A., Itokawa, H., 1989. The triterpenes from Stauntonia hexaphylla callus tissues
and their biosynthetic significance. J. Nat. Prod. 52, 623–628.
Oueslati, M.H., Ben, J.H., Mighri, Z., Chriaa, J., Abreu, P.M., 2006. Phytochemical
constituents from Salsola tetrandra. J. Nat. Prod. 69, 1366–1369.
Perrone, A., Masullo, M., Bassarello, C., Hamed, A.I., Belisario, M.A., Pizza, C.,
Piacente, S., 2007. Sulfated triterpene derivatives from Fagonia arabica. J. Nat.
Prod. 70, 584–588.
Xiang, Y., Li, Y.B., Zhang, J., Li, P., Yao, Y.Z., 2007b. A new alkaloid from Salsola collina.
Yao Xue Xue Bao 42, 618–620.
Zhao, Y.X., Ding, X.B., 2004. Studies on the alkaloids from Salsola collina Pall. Yao Xue
Xue Bao 39, 598–600.