Three new coumarin glycosides from the stems of Hydrangea paniculata

Article abstract of DOI:10.1080/10286020.2017.1305958

Three new coumarin glycosides (1-3), together with three known compounds (4-6), have been obtained from the stems of Hydrangea paniculata Sieb. Their structures were elucidated based on spectroscopic data and chemical evidence. In addition, compounds 1-3

Full text of DOI:10.1080/10286020.2017.1305958

Journal of Asian Natural Products Research
ISSN: 1028-6020 (Print) 1477-2213 (Online) Journal homepage: http://www.tandfonline.com/loi/ganp20
Three new coumarin glycosides from the stems of
Hydrangea paniculata
Jie Ma, Chuang-Jun Li, Jing-Zhi Yang, Yan Li, Xiu-Qi Bao, Nai-Hong Chen &
Dong-Ming Zhang
To cite this article: Jie Ma, Chuang-Jun Li, Jing-Zhi Yang, Yan Li, Xiu-Qi Bao, Nai-Hong Chen &
Dong-Ming Zhang (2017) Three new coumarin glycosides from the stems of Hydrangea paniculata,
Journal of Asian Natural Products Research, 19:4, 320-326, DOI: 10.1080/10286020.2017.1305958
To link to this article: http://dx.doi.org/10.1080/10286020.2017.1305958
Published online: 02 Apr 2017.
Submit your article to this journal
View related articles
View Crossmark data
Full Terms & Conditions of access and use can be found at
http://www.tandfonline.com/action/journalInformation?journalCode=ganp20
Download by: [University of Exeter]
Date: 04 April 2017, At: 20:13

Journal of asian natural Products research, 2017
Vol. 19, no. 4, 320–326
http://dx.doi.org/10.1080/10286020.2017.1305958
Three new coumarin glycosides from the stems of Hydrangea
paniculata
Jie Ma, Chuang-Jun Li, Jing-Zhi Yang, Yan Li, Xiu-Qi Bao, Nai-Hong Chen and
Dong-Ming Zhang
state Key laboratory of Bioactive substance and function of natural Medicines, institute of Materia Medica,
chinese academy of Medical sciences and Peking union Medical college, Beijing 100050, china
ABSTRACT
ARTICLE HISTORY
received 27 december 2016
accepted 7 March 2017
Three new coumarin glycosides (1-3), together with three known
compounds (4-6), have been obtained from the stems of Hydrangea
paniculata Sieb. Their structures were elucidated based on
spectroscopic data and chemical evidence. In addition, compounds
1-3 were screened for their neuroprotective effects against serum
deprivation-induced PC12 cell damage, hepatoprotective activities
against DL-galactosamine-induced toxicity in HL-7702 cells and their
ability to inhibit LPS-induced nitric oxide production in the murine
microglia BV2 cell line, but they were inactive.
KEYWORDS
Hydrangea paniculata;
coumarin glycosides;
neuroprotective;
hepatoprotective; anti-
inflammatory
1. Introduction
Hydrangea paniculata Sieb, is a medicinal herb which is widely distributed in southern
area of China. It is documented that its stem has bioactivity against inflammation, malaria,
and fever [1]. Our previous studies have found that its effective fraction, containing high
concentration of coumarin glycosides, is used to make pharmaceutical constituents for the
prevention and/or treatment of renal insufficiency, hypertension, and diabetic nephropathy
[2,3]. Skimmin, the most abundant compound in the plant can slowdown the progression
of streptozocin-induced diabetic nephropathy [4] and BSA-induced membranous glomer-
ularitis [5]. Phytochemical investigations of this plant have led to a number of coumarin
glycosides, iridoid glucosides, and secoiridoids, which showed diverse biological activities,
such as neuroprotective, hepatoprotective, suppressive diabetic nephropathy, and anti-in-
flammatory activity [6,7]. We continued our investigation of the bioactive metabolites and
isolated three new coumarin glycosides (1-3) and three known analogues (4-6) (Figure 1)
from the stems of this plant. eir structures were determined on the basis of spectroscopic
and chemical methods. Reported herein are the isolation, structural elucidation and bio-
logical activity of 1-3.
CONTACT dong-Ming Zhang
zhangdm@imm.ac.cn
© 2017 informa uK limited, trading as taylor & francis Group

JOURNAL OF ASIAN NATURAL PRODUCTS RESEARCH
321
Api-1
HO
O
O
5
8
4
Glc'-6
6
3
2
O
OH
HO
HO
HO
O
O
O
O
HO
Glc'-1
O
HO
HO
Glc''-1
OH
1
Api-1
HO
O
O
5
4
Glc'-6
6
3
2
OH
HO
O
HO
HO
O
OH
2
O
O
O
HO
O
8
Glc'-1
HO
Glc''-1
OH
HO
HO
O
Glc''-1
O
HO
4
5
6
OH
3
2
O
HO
O
OCH3
O
HO
O
8
OH Glc'-1
3
Figure 1. structures and key hMBcs of compounds 1-3 from the stems of Hydrangea paniculata.
2. Results and discussion
Compound 1 was isolated as a white, amorphous solid and had a molecular formula of
C26H34O17 according to its HRESIMS (m/z 641.1688 [M + Na]+, calcd. for 641.1680). e
IR spectrum of 1 showed absorption bands at 3394, 1708, and 1617 cm−1 for hydroxyl, car-
bonyl, and aromatic groups, respectively. Its UV absorption spectrum revealed the presence
1
of coumarin moiety (203, 318 nm). e H NMR spectrum of 1 in DMSO-d6 exhibited
resonances including those ascribed to two olefinic protons at δH 6.32 (1H, d, J = 9.5 Hz)
and 7.99 (1H, d, J = 9.5 Hz), three aromatic protons at δH 7.63 (1H, d, J = 9.5 Hz), 7.06
(1H, br d, J = 9.5 Hz) and 7.07 (1H, s), and three anomeric proton signals at δH 5.15 (1H,
d, J = 7.5 Hz), 4.46 (1H, d, J = 8.0 Hz) and 4.80 (1H, d, J = 3.0 Hz) correlated in the HSQC
spectrum with three anomeric carbons at δH 98.9, 105.1 and 109.7 in the 13C NMR spectrum,
respectively (Table 1). e 13C NMR spectrum of 1 displayed 26 carbon signals, of which 17
carbon signals were assigned to the sugar moieties and the remaining nine carbon signals
were assigned to the aglycone. Comparison of the NMR spectroscopic data of 1 (Table
1) with those of umbelliferone 7-O-β-D-glucopyranosyl (1 → 3)-[β-D-apiofuranosyl (1
→ 6)]-β-D-glucopyranoside [7] demonstrated that two compounds were almost identical
except for C-1 (Glc″) of the terminal glucose connecting to C-2 (Glc′) of the inner glucose
through an oxygen atom, which was supported by the HMBC correlation (Figure 1) between
the proton at δH 4.46 (Glc″-H-1, d, J = 8.0 Hz) and the carbon at δC 83.1 (Glc′-C-2). e
HMBC correlation between the anomeric proton H-1′ with the carbon at δC 160.4 (C-7) sug-
gested the 7-O-glycosidation. Additional HMBC correlation of Api-H-1 and C′-6 revealed
Api-C-1 of the D-apiose unit was linked to C′-6 through an oxygen atom. From these facts,

322
J. MA ET AL.
Table 1. 1h and 13c nMr spectroscopic data for compounds 1-3 in dMso-d6 (δ in ppm, J in hz).
1a
2b
3a
Position
δH
δC
δH
δC
δH
δC
2
3
4
5
6
7
8
9
10
Glc′
1
2
3
4
5
6
160.7
113.6
144.7
129.8
113.8
160.4
104.0
155.3
114.0
160.6
160.0
113.5
144.6
123.6
113.1
153.3
135.8
147.4
114.3
6.32 (1h, d, 9.5)
7.99 (1h, d, 9.5)
7.63 (1h, d, 9.5)
6.32 (1h, d, 9.6)
7.99 (1h, d, 9.6)
7.65 (1h, d, 8.4)
113.3 6.32 (1h, d, 9.5)
144.3 7.96 (1h, d, 9.5)
129.6 7.39 (1h, d, 9.0)
113.5 7.31 (1h, d, 9.0)
160.0
103.2
155.1
7.06 (1h, br. d, 9.5)
7.02 (1h, dd, 8.4, 2.4)
7.07 (1h, s)
7.05 (1h, d, 2.4)
113.5
5.15 (1h, d, 7.5)
3.50–3.52 (1h)c
3.50–3.52 (1h)c
3.19 (1h, m)
3.65 (1h, t, 7.0)
3.45 (1h, m)
98.9
83.1
76.1
69.8
75.7
67.8
5.10 (1h, d, 7.8)
3.31–3.33 (1h)c
3.44–3.46 (1h)c
3.44–3.46 (1h)c
3.79 (1h, m)
3.73 (1h, m)
3.89 (1h, m)
99.4 4.97 (1h, d, 7.5)
72.9 3.33 (1h, m)
74.7 3.29 (1h, m)
79.8 3.16(1h, m)
100.7
73.3
76.7
69.9
76.2
68.7
73.5 3.63–3.65 (1h, m)c
66.7 3.99 (1h, dd, 11.5, 1.5)
3.57 (1h, dd, 11.5, 7.0)
3.87 (1h, d, 11.5)
Glc″
1
2
3
4
5
6
4.46 (1h, d, 8.0)
2.97 (1h, dd, 9.0, 3.5)
3.18 (1h, m)
105.1
75.1
76.6
70.0
77.4
61.0
4.28 (1h, d, 7.8)
3.00 (1h, m)
3.20 (1h, m)
3.06 (1h, m)
3.23 (1h, m)
3.42 (1h, m)
3.71 (1h, m)
103.4 4.18 (1h, d, 8.0)
73.3 2.95 (1h, m)
76.4 3.07 (1h, m)
70.2 3.03 (1h, m)
76.7 3.00 (1h, m)
61.2 3.63–3.65 (1h, m)c
3.39 (1h, m)
103.5
73.7
77.0
70.2
76.8
61.1c
3.10 (1h, m)
3.12 (1h, m)
3.41–3.43 (2h, m)c
api
4.80 (1h, d, 3.0)
3.74 (1h, m)
109.7
76.4
79.2
73.8
4.87 (1h, d, 3.6)
3.75 (1h, dd, 6.6, 3.6)
109.5
76.0
78.6
73.4
3.88 (1h, d, 9.0)
3.59 (1h, d, 9.0)
3.35 (2h, m)
3.88 (1h, m)
3.55 (1h, m)
63.6
3.32–3.34 (2h, m)c
63.0
och3
3.86 (3h, s)
61.1c
a1h nMr data (δh) were measured at 500 Mhz, 13c nMr data (δc) were measured at 125 Mhz.
b1h nMr data (δh) were measured at 600 Mhz, 13c nMr data (δc) were measured at 150 Mhz.
coverlapping signals.
it was concluded that 1 is 7-substituted umbelliferone, containing two glucopyranosyl units
as well as one apiofuranosyl unit (Table 1).
Acid hydrolysis of 1 with 2 M HCl afforded D-glucose and D-apiose by GC analysis of
their trimethylsilyl L-cysteine derivatives, and the coupling constants (7.5 and 8.0 Hz) of the
anomeric protons of the glucopyranosyl units as well as the chemical shif (δC 109.7) of the
anomeric carbon of the apiofuranosyl indicated the β-configurations for the anomeric car-
bons [8,9]. us, the structure of 1 was elucidated as umbelliferone 7-O-β-D-glucopyranosyl
(1 → 2)-[β-D-apiofuranosyl (1 → 6)]-β-D-glucopyranoside.
Compound 2 was isolated as a white, amorphous solid. It was determined to have the
same molecular formula as 1 by the HRESIMS (641.1688 [M + Na]+, calcd. for 641.1688). Its
UV, IR, and NMR spectra were similar to those of 1, indicating that it is also a 7-substituted
coumarin with two glucopyranosyl units and an apiofuranosyl unit (Table 1), except that the
interglycosidic linkages of two glucopyranosyl units differed. Detailed comparison of the
NMR data of 2 and 1 indicated that Glc′-C-4 was deshielded by ΔδC 10.0 ppm and Glc′-C-2
was shielded by ΔδC 10.2 ppm, respectively. ese data suggested that the terminal glucose
(Glc″) was attached to Glc′-C-4, which was further confirmed by the HMBC correlation

JOURNAL OF ASIAN NATURAL PRODUCTS RESEARCH
323
of Glc″-H-1/Glc′-C-4 (Figure 1). e other connectivity for the sugar residues was further
confirmed from the following HMBC correlations: Api-H-1 (δH 4.87)/Glc′-6 (δC 66.7) and
Glc′-H-1 (δH 5.10)/aglycone-C-7 (δC 160.0) (Figure 1 and Table 1). Afer acid hydrolysis of
1, D-glucose and D-apiose were detected from the hydrolysate by GC analysis. erefore,
the structure of compound 2 was established as umbelliferone 7-O-β-D-glucopyranosyl (1
→ 4)-[β-D-apiofuranosyl (1 → 6)]-β-D-glucopyranoside.
The molecular formula of 3, C22H28O14, was indicated from the HRESIMS peak at
m/z 539.1379 [M + Na]+. The NMR data (Table 1) indicated that 3 contained the same
aglycone and sugar chain as umbelliferone 7-O-β-D-glucopyranosyl (1 → 6)-β-D-glu-
copyranoside (4), which has been reported previously [10]. The only difference between
them is an additional signal [δH 3.86 (3H, s); δC 61.1] assignable to one methoxyl
1
group in the NMR spectrum of 3. Two AB-type protons at δH 7.39 and 7.31 in its H
NMR spectrum and the HMBC correlation of δH 3.86 (3H, s)/δC 135.8 verified that
the OCH3 group was attached to C-8. The anometric carbons of the two glucoses were
3
determined as β-configured because of the large JH-1, H-2 coupling constants (7.5 and
8.0 Hz). Acid hydrolysis of 3 afforded D-glucose as determined through GC analysis.
Therefore, 3 was characterized as 8-methoxyl umbelliferone 7-O-β-D-glucopyranosyl
(1 → 6)-β-D-glucopyranoside.
Known compounds, umbelliferone 7-O-β-D-glucopyranosyl (1→6)-β-D-glucopyrano-
side (4) [10], skimmin (5) [11]and apiosylskimmin (6) [12] were also elucidated on the
basis of their spectroscopic profiles (NMR, UV, and MS) and comparison to published data
in the literatures.
Compounds 1-3 were tested for their anti-inflammatory [13], neuroprotective [14], and
hepatoprotective activities [15], however, none of them were active.
3. Experimental
3.1. General experimental procedures
Optical rotations were determined using a JASCO P2000 automatic digital polarim-
eter (JASCO, Tokyo, Japan). UV spectra were recorded in MeOH on a JASCO V-650
spectrophotometer (JASCO). IR spectra were measured on a Nicolet 5700 spectrometer
using an FTIR microscope transmission method (ermo Electron, Madison, WI, USA).
NMR spectra were collected on Bruker AV500-III and AVIIIHD 600 in DMSO-d6 with
solvent peaks as references (Bruker, Billerica, Massachusetts, USA). HR-ESI-MS data
were measured on an Agilent 1100 series LC/MSD Trap SL mass spectrometer (Agilent,
Waldbronn, Germany). e MPLC system included two C-605 pumps, a C-660 fraction
collector, a C-635 UV detector (Buchi, Flawil, Switzerland), and an ODS column (YMC,
6 × 45 cm, 50 μm, 800 g, Kyoto, Japan). Reversed-phase HPLC was carried out on a
Shimadzu LC-6AD instrument using an SPD-10A detector (Shimadzu, Kyoto, Japan).
A reversed-phase C18 column (YMC-Pack ODS-A 2 × 25 cm, 5 μm) was used. Column
chromatography was conducted on silica gel (100–160, 200–300 mesh, Qingdao Marine
Chemistry Company, Qingdao, China) and Sephadex LH-20 (Pharmacia Biotech AB,
Uppsala, Sweden). TLC was performed on precoated silica gel GF254 plates. Spots were
visualized under UV light (254 or 365 nm) or by spraying with 10% H2SO4 in 90% EtOH
followed by heating.

324
J. MA ET AL.
3.2. Plant material
e stems of Hydrangea paniculata were collected from the county of Jinxiu, Guangxi
Zhuang Autonomous Region, China, in May 2009, and identified by Mr. Guangri Long
(Liuzhou Forestry Bureau of Guangxi). Its voucher specimen (ID-S-4645) is deposited at
the Institute of Materia Medica, Chinese Academy of Medical Sciences.
3.3. Extraction and isolation
e air-dried stems of H. paniculata (20 kg) were extracted with water (2 × 90 L) at reflux, each
for 3 h. e combined H2O extract was passed through a HPD100 macroporous resin (30 L)
column eluted with H2O (90 L) and 17% ethanol (150 L) successively. e ethanolic portion was
dried with a rotary vacuum evaporator and the residue was refluxed with 95% ethanol. Afer
removing the solvent, the ethanol-soluble portion (400 g) was fractionated via a macroporous
resin column (HP2MGL, 12L) eluted with water and 20% EtOH. e latter portion (200 g, A)
was separated by silica gel CC (200–300 mesh, 10 × 100 cm, 2.8 kg) using CHCl3-MeOH-H2O
gradient mixtures (80:20:2–70:30:5, v/v/v) to give 13 fractions (A1–A13) on the basis of TLC
analysis. Fraction A11 (26 g) was further purified by recrystallization from 50% MeOH to yield
compound 5 (10 g). e lef mother liquors of Fraction A11 was separated by reversed-phase
HPLC with CH3OH-H2O (15:85, v/v) as mobile phase to yield compound 6 (56 mg). Fraction
A13 (27 g) was further subjected to a Sephadex LH-20 column chromatography (5 × 130 cm,
600 g) using 50% EtOH as a mobile phase to afford five subfractions (A13a-–A13e). Subfraction
A13b (9.5 g) was chromatographed by reversed-phase silica MPLC with 10–40% aqueous MeOH
(25 ml/min, 6 h) to get 40 parts (A13b1–40). Fraction A13b19 (319 mg) was further purified on
HPLC (YMC-ODS-A 5 μm, 2 × 25 cm, detection at 210 nm) to afford compound 4(7 mg) using
12% MeOH-H2O (12:88, v/v, 7 ml/min). Fraction A13b26 (110 mg) was separated by repeated
reversed-phase HPLC with CH3CN-H2O (10:90, v/v) as mobile phase to give compound 1
(16 mg). Fraction A13b31 was followed by repeated preparative HPLC (YMC-ODS-A 5 μm,
2 × 25 cm, detection at 210 nm) using CH3OH-H2O (14:86, v/v, 7 ml/min) as mobile phase to
yield compound 2 (30 mg). e A13b22 fraction (350 mg) was purified by repeated semi-pre-
parative HPLC (YMC-ODS-A, 5 μm, 1 × 25 cm, detection at 210 nm) using CH3OH-H2O (11:
89, v/v, 3 ml/min) as mobile phase to get compound 3 (22 mg).
3.3.1. Umbelliferone 7-O-β-D-glucopyranosyl (1 → 2)-[β-D-apiofuranosyl
(1 → 6)]-O-β-D-glucopyranoside (1)
White amorphous solid. [ꢀ]2D0 −50.0 (c 0.19, MeOH). UV (MeOH) λmax (log ε): 203 (4.57),
290 (4.05), and 318 (4.20) nm; IR (microscope) νmax 3394, 2920, 1708, 1617, 1076, and
1025 cm−1. 1H NMR (DMSO-d6, 500 MHz) and 13C NMR (DMSO-d6, 125 MHz), spectral
data see Table 1. HRESIMS: m/z 641.1680 [M + Na]+ (calcd for C26H34O17Na, 641.1688).
3.3.2. Umbelliferone 7-O-β-D-glucopyranosyl(1→4)-[β-D-apiofuranosyl
(1→6)]-β-D-glucopyranoside (2)
White amorphous solid. [ꢀ]2D0 −87.9 (c 0.22, MeOH). UV (MeOH) λmax (log ε): 203 (4.59),
291 (4.13), and 318 (4.27) nm; IR (microscope) νmax 3360, 2918, 1708, 1618, 1073, and
1026 cm−1. 1H NMR (DMSO-d6, 600 MHz) and 13C NMR (DMSO-d6, 150 MHz) spectral
data see Table 1. HRESIMS: m/z 641.1688 [M + Na]+ (calcd for C26H34O17Na, 641.1688).

JOURNAL OF ASIAN NATURAL PRODUCTS RESEARCH
325
3.3.3. 8-Methoxyl umbelliferone 7-O-β-D-glucopyranosyl
(1 → 6)-O-β-D-glucopyranoside (3)
White amorphous solid; [ꢀ]2D0 −33.8 (c 0.21, MeOH). UV (MeOH) λmax (log ε): 205 (4.59),
252 (3.68), and 309 (4.17) nm; IR (microscope) νmax 3358, 2920, 1716, 1608, and 1074 cm−1.
1H NMR (DMSO-d6, 500 MHz) and 13C NMR (DMSO-d6, 125 MHz) spectral data, see Table
1. HRESIMS: m/z 539.1379 [M + Na]+ (calcd. for C22H28O14Na, 539.1371).
3.3.4. Determination of absolute configurations of the sugar moiety in 1–3
Each compound (2 mg) was dissolved in 2 ml 2 M HCl and refluxed at 80 °C for 5 h. e
reaction mixture was extracted with EtOAc (1 ml × 3), and the aqueous layer was evapo-
rated to give a mixture of monosaccharides. e residue was further dissolved in anhydrous
pyridine (1 ml), followed by addition of 2 mg L-cysteine methyl ester hydrochloride (J&K
Scientific Ltd, Beijing, China; 99%). Afer heating at 60 °C for 2 h, the solvent was eliminated
under N2 and 0.2 ml trimethylsilylimidazole (J&K Scientific Ltd, Beijing, China; 99%) was
added. en, the mixture was heated at 60 °C for another 2 h and partitioned with n-hexane
and water (2 ml each). e organic layer was analyzed by GC. e authentic samples were
treated with the same method, and D-glucose and D-apiose were detected from 1-3 [8].
Acknowlegments
e authors thank the National Natural Science Foundation of China (NNSFC 81630094) and the
Beijing Municipal Science and Technology Project (No. Z161100001816047). e authors are grateful
to Department of Instrumental Analysis, Institute of Materia Medica, Chinese Academy of Medical
Sciences and Peking Union Medical College for the spectroscopic data measurements. We also thank
Prof. J.B. Li for ESI-MS measurements, Prof. Y.H. Yuan, X.Y. Song for the neuroprotective activity
assay, Prof. H. Chen for the hepatoprotective effects test, L. Wang for anti-inflammatory activity assay,
and Prof. D.W. Lai for revising the manuscript.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
is work was supported by the National Natural Science Foundation of China [grant number 81630094];
and the Beijing Municipal Science and Technology Project [grant number Z161100001816047].
References
[1] Chinese Herbal Medicine Company. Chinese Traditional Medicine Resource Records. (Science
Publishing House, Beijing, 1994), p. 480.
[2] D.M. Zhang, X.G. Chen, J.Z. Yang, Y. Li, and X.G. Zheng, Chinese Patent CN1690069A (2005).
[3] D.M. Zhang, X.G. Chen, J.Z. Yang, and Y. Li, Chinese Patent CN 1605343A (2005).
[4] S. Zhang, J.Z. Yang, H.Y. Li, Y. Li, Y. Liu, D.M. Zhang, F.R. Zhang, W.Q. Zhou, and X.G. Chen,
Eur. J. Pharmacol. 692, 78 (2012).
[5] S. Zhang, H.Q. Xin, Y. Li, D.M. Zhang, J. Shi, J.Z. Yang, and X.G. Chen, Evidence-based
Complemen. Alter. Med: eCAM. Article ID 819296 (2013).
[6] J. Shi, C.J. Li, J.Z. Yang, J. Ma, C. Wang, J. Tang, Y. Li, H. Chen, and D.M. Zhang, Fitoterapia.
96, 138 (2014).

326
J. MA ET AL.
[7] J. Shi, C.J. Li, J.Z. Yang, Y.H. Yuan, N.H. Chen, and D.M. Zhang, Planta Med. 78, 1844 (2012).
[8] D.M. Zhang, I. Miyase, M. Kuroyanagi, K. Umehara, and A. Ueno, Chem. Pharm. Bull. 44, 810
(1996).
[9] I. Kitagawa, M. Sakagami, F. Hashiuchi, J.L. Zhou, M. Yoshikawa, and J. Ren, Chem. Pharm.
Bull. 37, 551 (1989).
[10] W. Li, K. Koike, Y. Asada, T. Yoshikawa, and T. Nikaido, Tetrahedron Lett. 43, 5633 (2002).
[11] Y.M. Liu, G.Y. Liang, and B.X. Xu, Nat. Prod. Res. Dev. 15, 15 (2003).
[12] P. Satyanarayana, P. Subrahmanyam, R. Kasai, and O. Tanaka, Phytochemistry 24, 1862 (1985).
[13] H.M. Xia, C.J. Li, J.Z. Yang, L. Li, D. Zhang, and D.M. Zhang, J. Asian Nat. Prod. Res. 16, 971
(2014).
[14] C.J. Li, J.Z. Yang, and S.S. Yu, N.H. Chen, W. Xue, J.F. Hu, and D.M. Zhang, Planta Med. 74,
133 (2008).
[15] J. Kang, T. Zhang, L. Li, H. Sun, D.D. Wang, and R.Y. Chen, J. Asian Nat. Prod. Res. 18, 504 (2016).