Pterocephanoside A, a new iridoid from a traditional Tibetan medicine, Pterocephalus hookeri

Article abstract of DOI:10.1080/10286020.2020.1860951

This work obtained and identified pterocephanoside A (1), one new iridoid glucoside derivative with rare structure of three iridoid glycosides linked to cyclopenta[c]pyran-3(1H)-one, and 10 known iridoids (2–11) from Pterocephalus hookeri through silica gel column chromatography and semi-preparative HPLC. The structure of the new compound was confirmed by 1D and 2D NMR and HRMS data analysis. Compounds 1 and 2 were isolated from this plant for the first time. The iridoids mostly possessed seco-iridoid subtype and iridoid subtype skeletons from P. hookeri. Compounds 1, 3, 4, and 6–11 showed weak anti-inflammatory activity.

Full text of DOI:10.1080/10286020.2020.1860951

Journal of Asian Natural Products Research
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Pterocephanoside A, a new iridoid from a
traditional Tibetan medicine, Pterocephalus hookeri
Wen-Xiang Wang, Shi-Ying Luo, Yi Wang, Li Xiang, Xiu-Hua Liu, Ce Tang & Yi
Zhang
To cite this article: Wen-Xiang Wang, Shi-Ying Luo, Yi Wang, Li Xiang, Xiu-Hua Liu, Ce
Tang & Yi Zhang (2020): Pterocephanoside A, a new iridoid from a traditional Tibetan
medicine, Pterocephalusꢀhookeri, Journal of Asian Natural Products Research, DOI:
10.1080/10286020.2020.1860951
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JOURNAL OF ASIAN NATURAL PRODUCTS RESEARCH
https://doi.org/10.1080/10286020.2020.1860951
Pterocephanoside A, a new iridoid from a traditional
Tibetan medicine, Pterocephalus hookeri
a
ꢀ
b
ꢀ
c
b
d
b
Wen-Xiang Wang , Shi-Ying Luo , Yi Wang , Li Xiang , Xiu-Hua Liu , Ce Tang
and Yi Zhang
c
a
Department of Traditional Chinese Medicine Chemistry, School of Pharmacy, Chengdu University of
b
Traditional Chinese Medicine, Chengdu 611137, China; Innovative Institute of Chinese Medicine and
Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu 611137, China; Ethnic
c
Medicine Academic Heritage Innovation Research Center, Chengdu University of Traditional Chinese
d
Medicine, Chengdu 611137, China; Department of Internal Classics, School of Basic Medical
Sciences, Chengdu University of Traditional Chinese Medicine, Chengdu 611137, China
ABSTRACT
ARTICLE HISTORY
This work obtained and identified pterocephanoside A (1), one
new iridoid glucoside derivative with rare structure of three iri-
doid glycosides linked to cyclopenta[c]pyran-3(1H)-one, and 10
known iridoids (2–11) from Pterocephalus hookeri through silica
gel column chromatography and semi-preparative HPLC. The
structure of the new compound was confirmed by 1D and 2D
NMR and HRMS data analysis. Compounds 1 and 2 were isolated
from this plant for the first time. The iridoids mostly possessed
seco-iridoid subtype and iridoid subtype skeletons from P. hookeri.
Compounds 1, 3, 4, and 6–11 showed weak anti-inflamma-
tory activity.
Received 10 August 2020
Accepted 3 December 2020
KEYWORDS
Dispsacaceae;
pterocephanoside A;
traditional Tibetan
medicine; Pterocephalus
hookeri; iridoid glycoside;
anti-inflammatory activity
1. Introduction
Pterocephalus genus (Dipsacaceae) is distributed largely in Europe and Asia and com-
prises approximately 25 species. Among them, Pterocephalus hookeri and P. bretsch-
neideri are traditional Tibetan medicine mainly distributed in Tibetan of China [1].
As the most commonly used Tibetan medicine, P. hookeri has been extensively pre-
scribed for treating common diseases such as flu, cold, enteritis, and rheumatoid
CONTACT Xiu-Hua Liu
Chengdu University of Traditional Chinese Medicine, No. 1166 liutai avenue, Chengdu, Sichuan 611137, China; Ce Tang
09014182@qq.com Innovative Institute of Chinese Medicine and Pharmacy, Chengdu University of
2447049718@qq.com
Department of Internal Classics, School of Basic Medical Sciences,
4
Traditional Chinese Medicine, Chengdu 611137, China
ꢀ
These authors contributed equally to this work.
ß 2020 Informa UK Limited, trading as Taylor & Francis Group

2
W.-X. WANG ET AL.
arthritis [2]. Several triterpenoid saponins [3,4], iridoids [5], monoterpenoids [4],
pyridine alkaloids [6], tetrahydrofuranoid lignans [7], and bis-iridoids [6,7] have been
identified in this plant by previous chemical investigations.
Total glycosides from P. hookeri display potent antiarthritic effect that can be
attributed to its anti-inflammatory activity [8]. In this study, 11 iridoid glycosides
including 1 novel tetramer containing seco-iridoid and iridoid subtype skeletons (1)
were obtained from the water extract of P. hookeri whole grass. The content of iri-
doids (55 mg/g) was noticeably higher than that of triterpenoids (12 mg/g) in P. hook-
eri traditional Tibetan medicine [9]. The new compound 1 displayed secoiridoid/
iridoid subtype skeletons consisting of secologanic acid condensed to the 7-OH of
loganin iridoids. Nitric oxide production inhibition test was employed to gauge the
anti-inflammatory activity of these compounds. Compounds 1, 3–4, and 6–11 showed
weak anti-inflammatory activity.
2. Result and discussion
25
The new compound 1 was observed as pale yellow powder with ½aꢁ –86.5 (c 0.022,
D
MeOH). Its molecular formula was C H O as indicated by the HR-ESI-MS
5
8
78 30
–
(
2
(
3
Supplementary Figure S7) at m/z 1253.4513 [M–H] . The maximum absorption at
38 nm was displayed in UV spectrum (Supplementary Figure S8). The IR spectrum
Supplementary Figure S13) of 1 showed absorption bands of the hydroxy group at
ꢂ1
ꢂ1
412 cm
and the carbonyl groups at 1694 and 1634 cm , respectively. Acid
hydrolysis of 1 generated D-glucose identified by GC analysis. The relevant signals of
were in accordance with three b-glucopyranose moieties (Table 1) as suggested by
1
the three typical protons acting as doublets at d 4.68 (1H, d, J ¼ 7.9 Hz, H-1’A), 4.67
H
(
1H, d, J ¼ 7.9 Hz, H-1’B), and 4.66 (1H, d, J ¼ 7.9 Hz, H-1’D), respectively [10]. The
1
3
C NMR spectrum (Supplementary Figure S2) showed three glucopyranoside units
(dC 100.1, 99.5, 100.4, 74.4, 74.7, 74.8, 77.7, 78.0, 78.2, 71.5, 71.5, 71.6, 78.3, 78.3,
78.4, 62.6, 62.8, and 62.9) and 58 carbon resonance signals (Table 2) ascribed to 3
methyls, 10 methylenes, 37 methines, and 8 quaternary carbons.
In the 1D NMR spectra, three singlets at dH 7.54 (1H, s, H-3A), 7.48 (1H, s, H-
3
B), and 7.45 (1H, s, H-3D) together with d 154.1, 151.9, 153.2, 111.0, 109.8, and
C
1
12.6 and three carbonyl signals at d 168.2, 168.3, and 169.4 indicated the presence
C
of three olefinic protons of the enols [7,11]. Moreover, protons signals at dH 5.57
1H, d, J ¼ 4.6 Hz, H-1A), 5.48 (1H, d, J ¼ 4.6 Hz, H-1B), and 5.19 (1H, d, J ¼ 5.8 Hz,
H-1C) and the carbons at dC 97.8, 97.2, and 98.3 based on 1D NMR data
(
(
[
Supplementary Figure S9) established the existence of three protons on hemiacetal
5]. In addition, signals at dH 9.31 (1H, s, H-7B) and d 197.1 were ascribed to an
C
aldehyde, and signals at dH 6.76 (1H, t, J ¼ 7.0 Hz, H-7A) and d 135.3 and 156.1
C
revealed a trisubstituted olefin. These findings indicated the rationality of a, b-unsat-
1
urated aldehyde based on NMR spectra. Its H NMR spectrum (Supplementary
Figure S1) uncovered two sets of terminal olefin proton signals at dH 5.30 (1H, d,
J ¼ 10.5 Hz, H-10aA), 5.38 (1H, d, J ¼ 17.2 Hz, H-10bA), 5.75–5.77 (1H, m, H-8A),
5
.02 (1H, d, J ¼ 10.5 Hz, H-10aB), 5.06 (1H, d, J ¼ 17.2 Hz, H-10bB), and 5.63–5.65
(1H, m, H-8B) and three sets of b-glucopyranosyl units signals d 3.21–3.92,
H

JOURNAL OF ASIAN NATURAL PRODUCTS RESEARCH
3
1
Table 1. H NMR (700 MHz) spectral data of 1 in CD OD.
3
Unit A
5.57 d (4.6)
Unit B
Unit C
Unit D
5.19 d (5.8)
1
2
3
4
5
6
7
8
9
1
5.48 d (4.6)
4.20/4.40 dd (4.1, 11.6)
7.54, s
7.48, s
7.45, s
2.74–2.76, m
2.88–2.90, m
1.49–1.51/2.15–2.17, m
5.24–5.26, m
2.06–2.08, m
2.22–2.24, m
1.06 d (6.8)
3.01–3.03, m
2.36–2.38/3.16–3.18, m
6.76 t (7.0)
5.75–5.77, m
2.79–2.81, m
5.30/5.38 d
4.09 d (4.6)
3.01–3.03, m
1.61–1.63/2.15–2.17, m
5.15 t (5.2)
2.13–2.15, m
1.97–1.99, m
1.01 d (6.8)
9.31, s
5.63–5.65, m
2.87–2.59, m
5.02/5.06 d
(10.5, 17.2)
0
1
(
10.5, 17.2)
1
1
1
2
3
4
5
6
6
1-OMe
3.71, s
0
4.68 d (7.9)
4.67 d (7.9)
4.66 d (7.9)
3.22 brt (8.6)
3.21–3.41, m
3.21–3.41, m
3.21–3.41, m
3.64–3.70, m
3.88–3.92, m
0
0
0
0
0
0
3.22 brt (8.6)
3.21–3.41, m
3.21–3.41, m
3.21–3.41, m
3.64–3.70, m
3.88–3.92, m
3.22 brt (8.6)
3.21–3.41, m
3.21–3.41, m
3.21–3.41, m
3.64–3.70, m
3.88–3.92, m
1
3
Table 2. C NMR (150 MHz) spectral data of 1 in CD OD.
3
unit A
97.8
unit B
97.2
unit C
69.8
unit D
98.3
1
2
3
4
5
6
7
8
9
1
1
1
1
2
3
4
5
6
154.1
111.0
33.5
151.9
109.8
30.7
143.6
197.1
135.6
46.6
176.5
35.1
34.1
40.0
80.2
40.4
46.9
13.6
153.2
112.6
33.5
40.2
77.8
41.1
46.9
14.3
169.4
51.8
100.4
74.8
78.2
71.6
78.4
62.9
29.6
156.1
135.3
45.3
120.6
168.2
0
1
119.4
168.3
1-OMe
0
100.1
74.4
77.7
71.5
78.3
62.6
99.5
74.7
78.0
71.5
78.3
62.8
0
0
0
0
0
illustrating the existence of three iridoid glucoside units in compound 1. One methyl
1
group in H-NMR spectrum at dH 1.01 (3H, d, J ¼ 6.8 Hz, H-10D) and two olefinic
signals at dH 7.45 (1H, s, H-3D) were identified as an iridoid of loganic-type. NMR
spectroscopic data for compound 1 revealed four distinct parts (Figure S10) displayed
as units A, B, C, and D. Among them, units A, B, and D in 1 were extremely consist-
ent with those in strychoside B in literature [12]. Except for the relative signal of
units A, B, and D, one methoxy, three methylene, and four methine protons signals
were found in the remaining signals at d 4.20/4.40 (2H, dd, J ¼ 4.1, 11.6 Hz, H-1C),
H
2
6
.74–2.76 (1H, m, H-4C), 2.88–2.90 (1H, m, H-5C), 1.49-1.51/2.15–2.17 (2H, m, H -
C), 5.24–5.26 (1H, m, H-7C), 2.06–2.08 (1H, m, H-8C), 2.22–2.24 (1H, m, H-9C),
2
and 1.06 (3H, d, J ¼ 6.8 Hz, H -10C). In addition, one ester carbonyl group was found
3

4
W.-X. WANG ET AL.
at d 176.5. The above deduction indicated the existence of a 7-methylcyclopenta[c]-
C
pyran-3(1H)-one moiety. Complete structure assignments and further information
1
1
were obtained from the exhaustive analysis of HSQC, H- HCOSY, and HMBC data
Supplementary Figure S3–S5). d 2.36-2.38/3.16-3.18 (2H, m, H -6A) was correlated
(
H
2
1
1
with dH 6.76 (1H, t, J ¼ 7.0 Hz, H-7A) and dH 3.01-3.03 (1H, m, H-5A) in H- H
COSY spectrum (Figure S11). The signals at dH 6.76 (1H, t, J ¼ 7.0 Hz, H-7A) dis-
played long-range correlations with the carbons at d 30.7 (C-5B) and 197.1 (C-7B)
C
in the HMBC spectrum (Supplementary Figure S11), indicating the linkage location
of units A and B. In addition, long-range correlations were observed between the sig-
nals at dH 5.15 (1H, t, J ¼ 5.2 Hz, H-7D) and the carbon at d 168.3 (C-11B) and
C
between the signal of proton at d 5.24-5.26 and the carbon at d 168.2 (C-11A) in
H
C
HMBC spectrum. These findings indicated the linkage location of units A and C,
units B and D, respectively. The three anomeric protons signals as doublets at d 4.68,
4
.67, and 4.66 exhibited long range correlations with d 97.8 (C-1A), 97.2 (C-1B),
C
and 98.3 (C-1D) could help to correctly determine the linkage location of three gluco-
ses. This location was also supported by long-range heteronuclear correlations of H-
1A/C-1’A, H-1B/C-1’B, and H-1D/C-1’D in the HMBC spectrum.
The relative configuration of 1 was ultimately defined by coupling constants and
NOESY experiments (Supplementary Figure S6). A J value of 4.0 Hz between H-1b
and H-9b implied their trans-relationship [13,14]. With the assumption that B-1 had
b-configuration, stereochemistries for all positions in unit B were assigned.
The published compounds possess b-configuration at C-1 of the loganin [15,16].
Units A, B, and D were determined as loganin moieties according to NMR data
[
5
6,17]. NOESY correlations (Supplementary Figure S12) clearly observed between H-
a and H-9a uncovered their b-orientation in the iridoid skeleton. This orientation
was also observed for H-5B and H-9B. Thus, the structure of 1 was determined as
shown in Figure 1 and named as pterocephanoside A.
The known compounds 2–11 were identified as triplostoside A (2) [18], dipaspero-
side A (3) [19], dipsanoside A (4) [5], dipsanoside B (5) [5], cantleyoside (6) [20],
0
6
-O-b-apiofuranosylsweroside (7) [21], loganin (8) [22], loganic acid (9) [23], sylves-
troside I (10) [15], and sweroside (11) [24] according to their NMR data. Previous
studies on P. hookeri promoted the investigation of its chemical constituents and
anti-inflammatory activity. Eleven compounds (1–11) have been extracted from
P. hookeri, and their anti-inflammatory activity was evaluated. Compounds 1, 3, 4,
and 6–11 displayed weak anti-inflammatory activity (Table 3). In particular, the new
compound (1) had the weakest inhibitory effect with IC50 value of 93.58 lM. This
work mainly focused on chemical constituents and their anti-inflammatory activity.
Iridoids with anti-inflammatory activity are considered as chemotaxonomic markers
of P. hookeri and thus require further investigation.
3. Experiment
3.1. General experimental procedures
Shimadzu 210 A spectrophotometer was employed to detect UV spectrum (Shimadzu
Co., LTD., Shanghai, China). Horiba SEPA-300 digital polarimeter was used to

JOURNAL OF ASIAN NATURAL PRODUCTS RESEARCH
5
Figure 1. The structure of compound 1 isolated from Pterocephalus hookeri.
Table 3. Inhibitory effect of compounds 1 2 11 on LPS induced NO production in RAW
64.7 cells.
2
Compound
IC50 (lM)
Compound
IC50 (lM)
1
2
3
4
5
6
a
93.58 ± 0.36
—
57.65 ± 0.43
98.25 ± 0.29
—
7
8
9
46.33 ± 0.38
45.76 ± 0.53
55.28 ± 0.34
101.42 ± 0.48
27.66 ± 0.43
19.36 ± 0.35
10
11
L-NMMA
a
89.48 ± 0.45
Positive control. “—” is stand for the inhibitory rate <50% at a dose of 100 lM.
measure specific rotations (Horiba Co., LTD., Shanghai, China). Bruker DRX-700
spectrometer was applied to survey NMR data with TMS as the solvent peak (Bruker
Technologies Co., LTD., Beijing, China). APIQSTAR time-of-flight mass spectrometer
was utilized to acquire mass spectra (Agilent Technologies Inc, Beijing, China). Silica
gel column chromatography (200–300 mesh) and GF254TLC silica gel plates were
employed for isolation as supported by Qingdao Haiyang Chemical Co., Ltd, China.

6
W.-X. WANG ET AL.
3.2. Plant material
The whole grass of Pterocephalus hookeri was gathered in September 2018 in Tibetan
areas, and voucher samples (No. PH20181108–201A) were deposited in Ethnic
Medicine Academic Heritage Innovation Research Center of Chengdu University of
Traditional Chinese Medicine.
3
.3. Extraction and isolation
The whole grass of P. hookeri (5 kg) was extracted three times using purified water at
metal container. The aqueous extract was evaporated and then extracted sequentially
with petroleum ester, ethyl acetate, and n-butanol. The n-butanol extract (513 g) was
eluted with a gradient of ethanol/water (from 0:1 to 1:0, v/v) and chromatographed
over D101 macroporous resin to gain five fractions (Frs. A–E). Subsequently, seven
sub-fractions (Frs. B1–B7) were obtained from fraction B (60 g) through column
chromatography (CH Cl -CH OH, 1:0-0:1, v/v), and compounds 1 (21 mg) and 3
2
2
3
(
3
4 mg) were isolated from fraction B3 through pre-HPLC (CH OH/H O, 39:61,
mlꢃmin , 237 nm). Fraction B4 was isolated by preparative TLC with the develop-
3 2
ꢂ1
ing solvent of dichloromethane-methanol-water (8:1:0.2, v/v) and preparative HPLC
(
(
B5b of Fr. B5 through preparative HPLC (CH OH–H O, 36:64, 3 mlꢃmin , 237 nm).
ꢂ1
CH OH–H O, 36:64, 3 mlꢃmin , 237 nm) to gain 2 (2.9 mg), 5 (3.8 mg), and 6
3
2
5.2 mg). Compounds 4 (3 mg) and 7 (1.8 mg) were separated from Fr. B5a and Fr.
ꢂ1
3
2
3
.3.1. Compound 1
2
D
5
Yellowish powder (CH OH), ½aꢁ ꢂ86.5 (c 0.022, MeOH); UV (MeOH) k
(log e):
3
max
1
ꢂ1
13
238 (4.25) nm; IR (KBr) v
3412, 2923, 2358, 1694, 1291, 1076 cm ; H and
C
max
1
13
NMR spectral data (CD OD, 700 MHz for H and 175 MHz for C) see Tables 1 and
3
–
2
. HR-ESI-MS: m/z 1253.4513 [M–H] (calcd for C H O , 1253.4500).
58 77 30
3
.5. Measurement of anti-inflammatory activity in vitro
Nitric oxide production inhibition test was employed to gauge the anti-inflammatory
activity of these P. hookeri compounds on macrophages. The Cell Bank of the
Chinese Academy of Sciences (Shanghai, China) provided the RAW 264.7 cell line for
the cellular experiment. The inhibition activity of NO production was evaluated based
on a previous method. The RAW264.7 cells were cultured using Dulbecco’s modifica-
tion of Eagle’s medium (DMEM) containing 10% FBS, 100 units/ml penicillin, and
5
1
00 lg/ml streptomycin and seeded in 96-well cell culture plates (1.5 ꢄ 10 cells/well).
The cells were treated with serial dilutions of the compounds with a maximum con-
centration of 100 lM, followed by stimulation with LPS (1 lg/ml) for 18 h. Griess
reagent (reagent A and reagent B, Sigma) was employed to evaluate the NO produc-
tion of the supernatant. Microplate reader (Thermo, Waltham, MA) was used to
gauge the absorbance at 570 nm. Nitric oxide synthase (NOS) inhibitor NG-Methyl-
L-arginine acetate salt was applied as the positive control (L-NMMA, Sigma) [25].

JOURNAL OF ASIAN NATURAL PRODUCTS RESEARCH
7
3.6. Acid hydrolysis
Pterocephanoside A (2 mg) was processed in 4 ml of 1,4-dioxane/10% HCl (1:1) at
ꢅ
8
0 C for 4 h. The mixture was neutralized with 1 M NaOH in MeOH after cooling,
the solution was extracted with EtOAc (5 ml ꢄ 3) after adding 5 ml of water, and the
residue of water layer after evaporating was silylated with pyridine: HMDS: TMCS
(9:3:1). Finally, GC was used to determine sugar content by comparing it with the
retention time of the standards at 13.15 min.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the National Natural Science Foundation of China [grant number
8
2
1903922]; National Key Research and Development Program of China [grant number
017YFC1703900]; Xinglin Scholars Research Promotion Project of Chengdu University of
Traditional Chinese Medicine (BSH2019002).
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[
[
[
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