A new sesquiterpenoid glycoside from Saussurea involucrata

Article abstract of DOI:10.1080/14786419.2018.1543683

Saussurea involucrata, known for the abundant bioactive components, is a precious traditional Chinese medicine. In this study, a novel guaiane sesquiterpenoid glycoside named (1R, 5R, 6R, 7R, 8S, 11S)-11, 13-dihydrodehydrocostuslactone-8-O-6'-2''(E)-butenoyl-β-D-glucopyranoside (1), together with seven known compounds (2–8) were isolated from the dried aerial part of S. involucrata. Their structures were elucidated by spectroscopic and physico-chemical analyses. The antioxidant and anti-inflammatory activities of compound 1 were investigated. And compound 1 showed weak radical scavenging activity and low inhibitory activity on nitric oxide (NO) production.

Full text of DOI:10.1080/14786419.2018.1543683

Natural Product Research
Formerly Natural Product Letters
ISSN: 1478-6419 (Print) 1478-6427 (Online) Journal homepage: https://www.tandfonline.com/loi/gnpl20
A new sesquiterpenoid glycoside from Saussurea
involucrata
Shizhou Qi, Yiren Yang, Xiaoyan Xian, Xianzhe Li & Huiyuan Gao
To cite this article: Shizhou Qi, Yiren Yang, Xiaoyan Xian, Xianzhe Li & Huiyuan Gao (2019):
A new sesquiterpenoid glycoside from Saussureaꢀinvolucrata, Natural Product Research, DOI:
10.1080/14786419.2018.1543683
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NATURAL PRODUCT RESEARCH
https://doi.org/10.1080/14786419.2018.1543683
A new sesquiterpenoid glycoside from Saussurea
involucrata
Shizhou Qi, Yiren Yang, Xiaoyan Xian, Xianzhe Li and Huiyuan Gao
School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University, Shenyang,
People’s Republic of China
ABSTRACT
ARTICLE HISTORY
Received 10 September 2018
Accepted 29 October 2018
Saussurea involucrata, known for the abundant bioactive compo-
nents, is a precious traditional Chinese medicine. In this study, a
novel guaiane sesquiterpenoid glycoside named (1R, 5R, 6R, 7R,
8S, 11S)-11, 13-dihydrodehydrocostuslactone-8-O-6’-2’’(E)-bute-
noyl-b-D-glucopyranoside (1), together with seven known com-
pounds (2–8) were isolated from the dried aerial part of S.
involucrata. Their structures were elucidated by spectroscopic and
physico-chemical analyses. The antioxidant and anti-inflammatory
activities of compound 1 were investigated. And compound 1
showed weak radical scavenging activity and low inhibitory activ-
ity on nitric oxide (NO) production.
KEYWORDS
antioxidant; anti-
inflammatory; Saussurea
involucrata; sesquiterpe-
noid glycoside
1. Introduction
Saussurea involucrata (Kar. et Kir.) Sch. -Bip (Asteraceae), named ‘Tianshan Snow Lotus’,
‘Xinjiang Xuelian’ or ‘Xuelian Hua’ in China, is a rare, slow growth and very precious
Chinese medicinal herb (Flora of China Editorial Committee 1999). As a medicine
which was recorded in Pharmacopoeia of People’s Republic of China, S. involucrata
was used to treat rheumatoid arthritis (Li et al. 1980), cough (Chik et al. 2015), dys-
menorrhea (National Institutes for Food and Drug Control 1984), altitude sickness and
CONTACT Huiyuan Gao
sypugaohy@163.com
Supplemental data for this article can be accessed at https://doi.org/10.1080/14786419.2018.1543683.
ß 2019 Informa UK Limited, trading as Taylor & Francis Group

2
S. QI ET AL.
stomachache (Yi et al. 2010). Previous phytochemical and biological investigations
revealed that Saussurea genus has numerous bioactive compounds such as coumarins
(Jia et al. 1983), lignan, flavonoids (Xu et al. 2009), sesquiterpene lactones (Cao et al.
2016; Ren et al. 2007), steroids as well as phenylpropanoids (Seilgazy et al. 2017).
Recent pharmacological studies demonstrated that some compounds of S. involucrata
possessed a wide range of biological activities including anti-inflammatory, analgesic
(Zhai et al. 2010), anti-fatigue (Jia and Wu 2008), anti-aging, anti-oxidative, anti-hyp-
oxia, and hormonal-related gynecological disorders (Chik et al. 2015). In our previous
in vivo study, the dried aerial parts of S. involucrata showed significant anti-arthritic
effect (Han et al. 2016). And this result further stimulated us to explore the bioactive
constituents of S. involucrata. Herein, we report the isolation and structural elucidation
of a novel guaiane sesquiterpene glycoside, along with seven known compounds.
New compound was evaluated for its antioxidant and anti-inflammatory activities. In
addition, compound 3 was isolated from this genus for the first time, and compounds
7 and 8 were isolated from this plant for the first time.
2. Results and discussion
Compound 1, obtained as colorless needles, gave a molecular formula of C25H34O9
according to an [M þ Na]þ ion at m/z 501.2173 (calcd for C25H34O9Na, 501.2101) in its
HR-ESI-MS spectrum. The IR (KBr) spectrum showed absorptions attributable to
hydroxyl (3427 cmꢀ1), carbonyl (1742 cmꢀ1) groups and olefinic bond (1654 cmꢀ1). The
1H-NMR spectrum showed six olefinic protons at dH 6.88 (1H, m), 5.86 (1H, dd,
J ¼ 15.5, 1.8 Hz), 5.02 (1H, br s), 4.95 (1H, br s), 4.86 (1H, br s) and 4.78 (1H, br s), two
methyl groups at dH 1.82 (3H, d, J ¼ 7.2 Hz) and 1.28 (3H, d, J ¼ 7.2 Hz), two oxyme-
thine groups at 3.91 (1H, t, J ¼ 9.6 Hz) and 3.65 (1H, td, J ¼ 9.0, 5.4 Hz), a sugar moiety
at dH 4.10 (1H, dd, J ¼ 11.4, 7.8 Hz), 4.38 (1H, dd, J ¼ 12.0, 1.8 Hz), 4.35 (1H, d,
J ¼ 8.4 Hz), 3.40 (1H, t, J ¼ 8.4 Hz), 3.17 (1H, t, J ¼ 8.4 Hz), 3.06 (1H, t, J ¼ 9.0 Hz) and
2.99 (1H, m), and three protons of hydroxyl groups in sugar unit at dH 5.21 (1H, d,
J ¼ 5.4 Hz), 5.09 (1H, s), 5.05 (1H, d, J ¼ 6.0 Hz). And the d at dH 4.35 was assigned to
an anomeric proton signal of the sugar moiety. The 13C-NMR of 1 displayed twenty-
five carbon signals. With the aid of HSQC spectrum, these carbon signals were classi-
fied as two ester carbonyl carbons at dC 178.8, 165.4, three pair of olefinic carbons at
dC 145.3 and 113.6; 152.2 and 108.6; and 145.4 and 122.2, two oxymethine carbons at
dC 83.2, 79.3, a sugar unit at dC 103.7, 76.8, 73.7, 73.6, 70.3, 63.5, and two methyl car-
bons at dC 17.7, 16.1. All these data indicated that compound 1 possessed the skel-
eton of sesquiterpene glycoside. And the structure could also be confirmed by
comparing with NMR data of compound 2. However, the 1 D and 2 D data of 1 were
close to 2 except for the extra signals of an ester carbonyl signal (dC 165.4), a pair of
olefinic signals (dH 6.88, dC 145.3; dH 5.86, dC 122.2) and a methyl signal (dH 1.82; dC
17.7). Furthermore, the downfield chemical shifts of C-5’ and C-6’ of 1 which appeared
at dC 73.6 and 63.6 were also be observed. Combined with the key HMBC correlations
of H-2’’ (dH 5.86) to C-1’’ (dC 165.4), C-4’’ (dC 17.7), of H-6’ (dH 4.10, 4.38) to C-1’’ (dC
165.4), and of H-4’’ (dH 1.82) to C-2’’ (dC 122.2), C-3’’ (dC 145.3), the side chain which
located at the C-6’ was established. The sugar moiety attached to C-8 was deduced by

NATURAL PRODUCT RESEARCH
3
the key HMBC correlation of H-1’ (dH 4.35) to C-8 (dC 83.2). The b-configuration of
anomeric carbon of sugar moiety can be deduced on the basis of coupling constant
of the anomeric proton (J ¼ 7.8 Hz). And acid hydrolysis of 1 provided a D-glucose
moiety using HPLC method (tR: 18.5) (Tanaka et al. 2007).
Moreover, the NOESY correlations between H-1 (dH 2.88) and H-7 (dH 2.19); H-8 (dH
3.65), H-6 (dH 3.91) and H-11 (dH 2.67); and H-7 (dH 2.19), H-1 (dH 2.88), H-5 (dH 2.77)
and H-9 (dH 2.18, 2.75), suggested that H-1, H-5 and H-7 exhibited a orientation, and
H-6, H-8 and H-11 exhibited b orientation. The absolute configuration of 1a could be
gained by the comparison of the experimental and calculated electronic circular
dichroism (ECD) spectra (Xiao et al. 2011). The experimental ECD spectrum of 1a which
possess the positive Cotton effect at 237 nm was consistent with the theoretical ECD
spectrum of 1a. Therefore, compound 1 was determined as (1R, 5R, 6R, 7R, 8S, 11S)-11,
13-dihydrodehydrocostuslactone-8-O-6’-2’’(E)-butenoyl-b-D-glucopyranoside.
The known compounds were determined to be 11b,13-dihydrodehydrocostuslactone-
8a-O-b-D-glucopyranoside (2) (Wang et al. 2007), flazine (3) (Su et al. 2002), involucratolac-
tone (4) (Li and Jia 1989), 11a, 13-dihydrozaluzanin C (5) (Strapasson et al. 2012), dehydro-
costuslactone (6) (Julianti et al. 2011), zaluzanin D (7) (Julianti et al. 2011), cinnamic acid
(8) (Ferreira et al. 2005) by comparing their NMR data with literatures.
The new compound 1 was tested for its antioxidant avtivity through DPPH, ABTS
free radical scavenging and FRAP assay. The anti-inflammatory activity of 1 was also
evaluated in RAW 264.7 cells which stimulated by LPS. Compound 1 did not show sig-
nificant radical scavenging activity or obvious inhibitory activity on nitric oxide (NO)
production. This study provides a potentially contribution for the search of antioxidant
and anti-inflammatory drugs.
3. Experimental
3.1. General experimental procedures
NMR spectra were obtained by Bruker AV-400 and AV-600 spectrometers (Bruker,
Billerica, MA, USA) using tetramethyl silane as an internal standard. HR-ESI-MS spectra
were obtained using a Bruker micro-TOF-Q mass spectrometer, IR spectra were
obtained with a Bruker IFS-55 Fourier transform infrared (FT-IR) spectrometer (Bruker).
CD spectrum was recorded with a Jasco CD-2095-plus circular dichroismdetector
(JASCO Corporation, Tokyo, Japan). Open-column chromatography was performed
using silica gel (200–300 mesh, Qingdao Marine Chemical Co., Ltd.), macroporous
adsorption resin D101 (Langfang Nanda resin Co., Ltd.), and Sephadex LH-20
(Pharmacia Biotech, USA). TLC was performed with precoated silica gel GF254 glass
plates (Qingdao Marine Chemical Co., Ltd). Preparative RP-HPLC was conducted on an
Agela P1050 pump and Agela UV1000D UV spectrophotometric detector at 210 nm
using a Mightysil RP-18 GP 250-20 column (5 lm, 20 ꢁ 250 mm).
3.2. Plant materials
The dried aerial parts of S. involucrata were purchased in February 2014 from Yuan
Long Trade Co., Ltd. (Urumqi, Xinjiang, China), and identified by Associate Prof. Jincai

4
S. QI ET AL.
Lu of Shenyang Pharmaceutical University. A voucher specimen (ZB-14-XS012A) was
deposited in the School of Traditional Chinese Medicine, Shenyang Pharmaceutical
University, Shenyang, China.
3.3. Extraction and isolation
The dried aerial parts of S. involucrata (5.5 kg) were pulverized and extracted with
CHCl3 (44L ꢁ 2h ꢁ 3) to give 196.2 g crude extract. Then the S. involucrata was further
extracted with 70% EtOH (44L ꢁ 2h ꢁ 3). The crude extract (2.4 kg) was suspended in
H2O and partitioned with EtOAc and n-BuOH to yield an EtOAc (128.6 g), n-BuOH
(295.1 g) and aqueous (1.75 kg) fractions. The EtOAc part (120 g) was subjected to silica
gel CC eluted with a gradient of CH2Cl2-CH3OH (from 1: 0 to 0: 1) to obtain 10 frac-
tions. Fraction 8 (2.6 g) was was chromatographed over a silica gel column using a
gradient of CH2Cl2-MeOH (from 50: 1 to 0: 1), and was separated into 9 fractions
(Fr.8.1–Fr.8.9). Furthermore, Fr.8.7 (102 mg) was purified by Spehadex LH-20 CC, and
then separated by HPLC, using an gradient solvent system 40%-45% MeOH in H2O
over 60 min yielded compounds 1 (5.2 mg, tR ¼ 46.2 min), 2 (13.3 mg, tR ¼ 49.4 min).
Fr.8.4 (800 mg) was subjected to the RP-18 column and eluted with MeOH-H2O (3:10
to 10:0) to afford 8 fractions (Fr.8.4.1–Fr.8.4.8). Fr.8.4.4 (75.1 mg) was separated by
HPLC, using an gradient solvent system 50%-70% MeOH in H2O over 70 min yielded
compounds 7 (8.2 mg, tR ¼ 35.1 min), 4 (10.9 mg, tR ¼ 54.7 min) and 5 (15.2 mg, tR ¼
56.4 min). Fr.8.4.6 (118.7 mg) was purified via preparative HPLC using an isocratic solv-
ent system of 65% MeOH in H2O over 60 min yielded compounds 6 (8.1 mg, tR
41.2 min), 3 (10.9 mg, tR ¼ 48.1 min) and 8 (21.2 mg, tR ¼ 55.8 min).
¼
Compound 1: (1R, 5R, 6R, 7R, 8S, 11S)-11, 13-dihydrodehydrocostuslactone-8-O-6’-
20
2’’(E)-butenoyl-b-D-glucopyranoside, colorless needles; ½aꢂD þ 82.9 (c 0.09, CH3OH); IR
1
(KBr) ꢀmax 3427, 2921, 1742, 1717, 1653, 1381, 1073, 974, 899 cmꢀ1; H-NMR (DMSO-d6,
600 MHz) d 6.88 (1H, m, H-3’’), 5.86 (1H, dd, J ¼ 15.5, 1.7 Hz, H-2’’), 5.21 (1H, d,
J ¼ 5.4 Hz, OH), 5.09 (1H, s, OH), 5.05 (1H, d, J ¼ 6.0 Hz, OH), 5.02, 4.95 (2H, br s, H-15),
4.86 (1H, br s, H-14), 4.78 (1H, br s, H-14), 4.36 (1H, m, H-6’), 4.30 (1H, d, J ¼ 7.8 Hz, H-
1’), 4.10 (1H, dd, J ¼ 11.7, 7.5 Hz, H-6’), 3.91 (1H, t, J ¼ 9.6 Hz, H-6), 3.65 (1H, m, J ¼ 9.6,
5.2 Hz, H-8), 3.40 (1H, m, H-3’), 3.17 (1H, m, H-2’), 3.06 (1H, m, H-4’), 2.99 (1H, m, H-5’),
2.88 (1H, q, J ¼ 7.8 Hz, H-1), 2.77 (1H, br t, J ¼ 9.6 Hz, H-5), 2.75 (1H, dd, J ¼ 13.2, 9.6 Hz,
H-9), 2.67 (1H, dd, J ¼ 10.2, 7.2 Hz, H-11), 2.44, 2.38 (2H, m, H-2), 2.19 (1H, q, J ¼ 9.6 Hz,
H-7), 2.18 (1H, dd, J ¼ 13.2, 5.2 Hz, H-9), 1.82 (1H, dd, J ¼ 7.2, 1.6 Hz, H-4’’), 1.82, 1.74
(2H, m, H-3), 1.28 (3H, d, J ¼ 7.2 Hz, H-13); 13C-NMR (DMSO-d6, 150 MHz) d 178.8 (C-12),
165.4 (C-1’’), 152.2 (C-4), 145.4 (C-10), 145.3 (C-3’’), 122.2 (C-2’’), 113.6 (C-14), 108.6 (C-
15), 103.7 (C-1’), 83.3 (C-8), 79.3 (C-6), 76.8 (C-2’), 73.7 (C-5’), 73.6 (C-3’), 70.3 (C-4’), 63.5
(C-6’), 53.0 (C-7), 52.2 (C-5), 46.5 (C-1), 44.1 (C-9), 40.2 (C-11), 31.9 (C-2), 29.4 (C-3), 17.7
(C-4’’), 16.1 (C-13); HR-ESI-MS: m/z 501.2173 [M þ Na]þ (calcd for C25H34O9, 478.2203).
3.4. Acid hydrolysis of compound 1
Compound 1 (5 mg) dissolved in MeOH was mixed with 10% HCl (1.0 mL) and refluxed
for 4 h. The cold hydrolysate was diluted 2-fold with H2O, and extracted with EtOAc. 2

NATURAL PRODUCT RESEARCH
5
Figure 1. The structures of compounds 1–8.
M ammonium hydroxide was used to neutralize the aqueous layer and a residue was
obtained in vacuo. Then residue was analyzed by TLC over silica gel and by compari-
son with authentic samples. The residue was further analyzed by dissolving in pyridine
(0.4 mL) which contain -cysteine methyl ester hydrochloride (2mg) and kept at 60 ꢃC
L
for 2 h. Next, O-Toylisothiocyanate (2 mL) was added and the mixture was heated at
60 ꢃC for 1 h. The reaction mixture was analyzed by HPLC and a C18 HPLC column
(4.6 ꢁ 250 mm, 10 mm particle size) was used [flow: 0.8 mL/min; mobile phase: CH3CN-
H2O (25:75) containing 50 mM H3PO4]. Compared with the retention times of L-glucose
(tR ¼ 18.7 min), L-glucose (tR ¼ 17.1 min), the structure of L-glucose of 1 was deduced
by the retention times of 18.5 min.
3.5. Anti-inflammatory activity assay
2ꢀ
NO production was determined by evaluating the level of NO2 using Griess reaction.
Briefly, RAW264.7 cells were plated in a 96 well plate at a density of 5 ꢁ 104 cells/well.
After cells were treated with different concentrations of compound 1, then were
incubated and stimulated with LPS (100 ng/mL) for 24 h. And Griess reagent was
added to simple to determine NO production. The absorbance was gained at 540 nm
by a Varioskan flash instrument. NO production was calculated using the NaNO2
standard curve and minocycline was used as a positive control.
3.6. Antioxidant activity assay
Antioxidant activity was evaluated by DPPH, ABTS free radical scavenging and FRAP
assay. And trolox was used to be the positive control. DPPH, ABTS free radical scav-
enging assays were carried out according to the previous method (Peng et al. 2016).
The free radical scavenging capability was calculated by the equation: RSA % ¼ [(OD
control - OD sample)/(OD control - OD blank)] ꢁ 100%. FRAP assay was determined by
the published method (Wang et al. 2007). A calibration curve was established by

6
S. QI ET AL.
different concentrations of FeSO4 at 0.15 to 5.00 mM and results were expressed as
mmol of Fe2þ equivalents per gram.
4. Conclusion
Based on the result that the dried aerial parts of S. involucrata showed significant anti-
arthritic effect in Wistar rats, eight bioactive compounds (1–8) including a novel ses-
quiterpene glycoside of were isolated from the dried aerial part of S. involucrata. And
the structure of a 2-butenoic acid methyl ester group linked with sugar unit of 1 is
rare. Except for the novelty of 1, compound 3 was first isolated from the this genus
and 7 and 8 were first isolated from S. involucrata. In addition, the antioxidant and
anti-inflammatory activities of 1 were evaluated and 1 didn’t show any signifi-
cant activity.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the Liaoning Province University Students Innovation and
Entrepreneurship Training Program (201610163), Youth Teacher Development Support scheme
of Shenyang Pharmaceutical University (2014) and the Project of Key Laboratory of Structure-
Based Drug Design & Discovery of Ministry of Education of Shenyang Pharmaceutical University.
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