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Anti-diabetes and Anti-inflammatory Activities of Phenolic Glycosides from Liparis odorata

Hongdong Liu1,2, Bin Li1*, Piao Jiang1, Youquan Zhong1, Dongming Zhang3, Hua Liu1, Pingnan Wan1, Xuewen Lai1, Bo Liu1 and Jie Chen1

1Pharmacy College, Jiangxi University of Traditional Chinese Medicine, 818 Xinwan Road, Nanchang 330004, Jiangxi, PR China

2Technology Center, Jiangzhong Group, 618 Huoju Road, Nanchang 330096, Jiangxi, PR China

3Institute of Materia Medica, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100050, PR China

*Corresponding Author:
Bin Li
Pharmacy College, Jiangxi University of Traditional Chinese Medicine
818 Xinwan Road, Nanchang 330004, Jiangxi, PR China.
Tel: 8679187118827
Fax: 8679187118825
E-mail: [email protected]

Received Date: July 06, 2016; Accepted Date: July 14, 2016; Published Date: July 20, 2016

Citation: Liu H, Li B, Jiang P, Zhong Y, Zhang D, et al. (2016) Anti-diabetes and Anti-inflammatory Activities of Phenolic Glycosides from Liparis odorata. Med chem (Los Angeles) 6:500-505. doi:10.4172/2161-0444.1000390

Copyright: © 2016 Liu H, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Five new phenolic glycosides, liparisglycoside K-O (1-5) and one known compound, 4-allyl-2,6-dimethoxyphenol glucoside (6) were isolated from the whole plant of Liparis odorata. Compound 6 was isolated and identified from this genus for the first time. The structures of all compounds were elucidated through extensive spectroscopic methods including UV, IR, MS, 1D- and 2D-NMR. All compounds from Liparis odorata were evaluated for their ability to inhibit LPS-induced NO production on the BV2 microglial cell line in vitro, as well as their inhibitory effects on PTP1B and α-glucosidase enzyme assays.


Liparisodorata;Orchidaceae; Phenolic glycosides; Anti-inflammatory activity ;Anti-diabetes effect


Liparisodorata (Willd.)Lindl., belonging to the Orchid family [1], is an herbaceous plant widely distributed in southern China, and usually used to inhibit inflammation and reduce lipid in Jiangxi province folk medicine in China. Throughour continuous interest in the chemical and biologically active constituents of this plant [2-4], five new phenolic glycosides (Figure 1) were isolated and their structures elucidated through extensive spectroscopic analyses, as well as literature comparisons. In addition, one known compound was isolated and identified as 4-allyl-2,6-dimethoxyphenol glucoside [5]. To the best of our knowledge, obesity therapy using phenolic glycoside derivatives has not been studied yet, and we here reportthe anti-diabetes effects against protein tyrosine phosphatase 1B (PTP1B) and α-glucosidase enzymes forall the isolated compounds. PTP1B plays a critical role as a key negative regulator of the insulin and leptin signaling pathways, thereby regulating glucose homeostasis and body weight, respectively [6], while α-glucosidase inhibition is critical for the early treatment of diabetes mellitus [7]. Therefore, effective inhibition of both enzymesis a potential therapy for both type 2 diabetes mellitus and obesity.


Figure 1: Chemical structures of 1-5.

Materials and Methods

General experimental procedures

Ultraviolet (UV) spectra were recorded using a Shimadzu UV-300 spectrophotometer. IR spectra were recorded on a Nicolet 5700 FT-IR spectrometer by a transmission microscope method. HR-ESI-MS results were obtained using an Agilent 1100 series LC/MSD Trap SL mass spectrometer. Optical rotations were measured on a Perkin Elmer 241 automatic digital polarimeter. The 1D- and 2D-NMR spectra were recorded using INOVA 500 and Mercury-400 spectrometers in dimethyl sulfoxide-d6(DMSO-d6). GC was conducted on an Agilent Technologies 7890A instrument. Preparative highpressure liquid chromatography (HPLC) was carried out on a Shimadzu LC-6AD instrument with an SPD-20A detector, using a YMC-Pack ODS-A column (250×20mm, 5μm).Column chromatography (CC) was performed using silica gel (200-300 mesh, Qingdao Marine Chemical Inc.,Qingdao,China), ODS gel (50μm, YMC,Japan) and PRP-512A macroporous resin (100-200 mesh). Thin layer chromatography (TLC) was performed with glass pre-coated silica gel (GF254) plates. Spots were visualized by UV light (254nm) or spraying with 10% H2SO4 in ethanol (EtOH)followed by heating.

Plant material

L.odoratawas collected in the Jiangxi province of China in August 2012. The plant materials were identified by professor Lai Xuewen, Jiangxi University of Traditional Chinese Medicine in China, where a voucher specimen (No.002017) was deposited.

Extraction and isolation

The whole air-dried plant of L. odorata (30.0 kg) was extracted three times under reflux with 95% EtOH at ambienttemperature. After removing the organic solvent under reduced pressure, the 95% EtOH extract of L.odoratawas dissolved in 0.2MHCl. The HCl-soluble fraction was basified by NH3·H2O to pH 10.0 and then extracted three times in succession with chloroform, EtOAc and n-BuOH, respectively. The n-BuOH fraction (100.0 g) was subjected to macroporous resinCC (PRP-512A,Ø10 × 50 cm) and eluted with a gradient of EtOH in water (30-95% EtOH). The 70% EtOHeluate (1.8 g) was further subjected toreversed-phase chromatography using a C18silica gel column (Ø2.0 × 60 cm) with gradient mixtures of CH3OH-H2O (30:100-100:0) as eluents to yield five fractions (A-E). Fraction C (800.0 mg) was applied to a silica gel column (Ø2.0 × 60 cm) and eluted with CHCl3-MeOH (50:1, 25:1, 15:1, 10:1, 5:1, 2:1, 1:1, 0:1) to yield 8 subfractions (C1-C8) based on TLC analysis.

Subfraction C2 (50.0 mg) waschromatographed on a silica gel column (Ø1.2 × 50 cm) using CHCl3-MeOH (15:1) and purified by preparative HPLC with MeOH-H2O (45:55, 8.0 mL/min) to give compound 6 (11.0 mg). Subfraction C3 (150 mg) was chromatographed using aSephadex LH-20 column (Ø1.5 × 200 cm) eluting with MeOH, then further purified by preparative HPLC and eluted with MeOH-H2O (68:32, 8.0 mL/min) to yield compound 5 (105.0 mg) and compound 4 (6.0 mg). Subfraction C6 (62.0 mg) was purified with preparative HPLC eluting with MeOH-H2O (60:40, 8.0 mL/min) to yield compound 1 (21.0 mg), and subfraction C7 (79.0 mg) was purified by preparative HPLC with MeOH-H2O (60:40, 8.0 mL/min) to yield compound 3 (2.5 mg). Finally, subfraction C8 (82 mg) was subjected to a reversed-phase C18 silica gel column and eluted with MeOH-H2O (15:85, 30:70, 50:50, 75:25, 100:0). Then, the 75% eluate was further separated by repeated preparative HPLC with 55% MeOH at a flow rate of 8 mL/min to yield compound 2 (8.0 mg).

Liparisglycoside K (1): Colorless oil; [É]20 D:+23.6(c 1.0,MeOH); UV(MeOH) λmax (logε): 209(4.31), 242(3.97) nm; IR(KBr) νmax: 3376, 2973, 2916, 1681, 1426, 1378, 1190, 1042, 954 cm-1; 1H NMR (DMSO-d6, 500 MHz) and 13CNMR(DMSO-d6, 125 MHz) data (see Tables 1 and 2); HR-ESI-MS m/z 610.2632 [M]+(Calcd for C30H42O13, 610.2625).

H 1a 2a    3a 4b 5a
2/6 7.54 s 7.55 s 7.55 s 7.55 s 7.55 s
7/12 3.45 m 3.43 m 3.46 d (7.5) 3.48 m 3.49 m
8/13 5.24 t (8.5) 5.22 t (7.0) 5.26 t (7.5) 5.24 m 5.24 t (7.5)
10/15 1.68 s 1.68 s 1.69 s 1.68 s 1.69 s
11/16 1.71 s 1.71 s 1.71 s 1.71 s 1.72 s
  Ara Gluc Ara Gluc Ara
1´ 4.72 d (6.0) 4.69 d (7.5) 4.81d (6.0) 4.62d (7.6) 4.50 d (7.5)
2´ 3.95 m 3.43 m 3.94 m 3.33 m 3.66 m
3´ 373 m 3.49 m 3.81 m 3.24 m 3.40 m
4´ 3.73 m 3.43 m 4.16 m 3.19 m 3.64 m


3.77 m
3.36 m

3.55 m

3.61 m
3.94 m

3.45 m

3.16 m
3.69 m



4.25 overlapped
4.25 overlapped


4.05 m
4.15 m


CH3CO- - 1.89 s 2.08 s 1.89 s  
  Gluc Gluc Gluc    
1 " 4.46 d (7.5) 4.25 d (6.5) 4.53d (8.0)    
2 " 3.18 m 3.13 m 3.09 m    
3 " 3.05 m 2.96 m 3.04 m    
4 " 3.05 m 3.03 m 3.09 m    
5 " 3.33 m 3.22 m 3.17 m    
6 " 3.93 m
4.15 m
3.70 m
3.39 m
3.41 m
3.52 m
CH3CO- 1.62 s - -    

Table 1: 1H NMR Spectroscopic Data of Compounds 1-5.1

Position Compound 1 Compound 2 Compound 3 Compound 4 Compound 5
1 126.5 126.9 126.7 126.8 126.6
2/6 128.5 128.5 128.5 128.5 128.6
3/5 135.2 135.5 135.3 135.4 135.4
4 156.6 156.0 156.2 156.0 156.3
7/12 28.1 27.9 28.2 27.8 28.1
8/13 122.7 122.8 122.7 122.8 122.8
9/14 132.2 132.2 132.1 132.2 132.2
10/15 17.9 17.8 17.8 17.8 17.9
11/16 25.7 25.6 25.6 25.6 25.6
17 167.2 167.1 167.1 167.2 167.2
  Ara Gluc Ara Gluc Ara
1´ 102.8 104.0 102.6 104.4 105.5
2´ 80.5 80.4 79.8 73.4 71.2
3´ 71.2 74.5 70.1 76.1 72.6
4´ 66.5 73.8 69.8 69.8 67.8


64.9 71.6 62.4 74.0 66.5
6´   63.0   63.4  
CH3CO   20.5 21.0 20.5  
CH3CO   170.0 170.0 170.2  
  Gluc Gluc Gluc    
104.8 103.3 104.2    
76.2 76.5 76.5    
74.5 73.3 74.5    
70.1 70.1 70.1    
73.9 77.0 77.0    
63.9 61.1 61.2    
CH3CO 20.0        
CH3CO 170.2        

Table 2: 13C NMR data for compounds 1-5 a.

Liparisglycoside L (2): White amorphous power; [É]20 D:+10.2(c 1.10,MeOH); UV(MeOH) λmax(logε): 208(4.34), 241(3.79) nm; IR(KBr) νmax: 3370, 2969, 2928, 1714, 1601, 1553, 1424, 1250, 1095, 961 cm-1; 1H (DMSO-d6, 500 MHz) and 13C NMR (DMSO-d6, 125 MHz) data (see Tables 1 and 2); HR-ESI-MS m/z 640.2729 [M]+(Calcd. for C31H44O14, 640.2731).

Liparisglycoside M (3): Colorless oil; [É]20 D:+23.6(c 1.0, MeOH); UV(MeOH) λmax (logε): 209(4.31), 242(3.97) nm; IR(KBr) νmax 3359, 2969, 2926, 1679, 1424ï¼1378, 1250, 1135, 1080, 936 cm-1; 1H NMR (DMSO-d6, 500 MHz) and 13C NMR (DMSO-d6, 125 MHz) data (see Tables 1 and 2); HR-ESI-MS m/z 610.2630 [M]+(Calcd. for C30H42O13,610.2625).

Liparisglycoside N (4): White amorphous power; [É]20 D: -20.8 (c 1.0, MeOH); UV(MeOH) λmax (logε): 208(4.24), 240(3.81) nm; IR(KBr) νmax: 3362, 2971, 2927, 1715, 1601, 1428, 1380, 1271, 1190, 910 cm-1; 1H NMR (DMSO-d6, 400 MHz) and 13C NMR(DMSO-d6, 100 MHz) data (see Tables 1 and 2); HR-ESI-MS m/z 478.2202 [M]+(Calcd for C25H34O9, 478.2203).

Liparisglycoside O (5): White amorphous power; [É]20 D: +63.8(c 0.95, MeOH); UV(MeOH) λmax(logε): 208(4.39), 242(3.87) nm; IR(KBr) νmax: 3358, 2974, 2924, 1691, 1545, 1424, 1382, 1189, 1150, 953 cm-1; 1H NMR (DMSO-d6, 500 MHz) and 13C NMR (DMSO-d6, 125 MHz) data (see Tables 1 and 2); HR-ESI-MS m/z 406.1993 [M]+ (calcd for C22H30O7, 406.1992).

Anti-diabetes and anti-inflammatory assays: As previous studies showed that phenolic glycosides compounds from Liparisodoratapossessed anti-inflammatory activities [3], so, these new phenolic glycosides in this paper were also evaluated activities to inhibit inflammation. Also because of new compounds, widespread screening on activities were looked forward to, thus evaluation of these compounds for their protein tyrosine phosphatase 1B inhibition and α-glucosidase inhibition activities were untaken in our experiments, seeking new potential drugs for the clinic.

Protein tyrosine phosphatase 1B inhibition: The assay was carried out as previouslydescribed [8]. Briefly, all samples were dissolved in 100% DMSO. p-Nitrophenyl phosphate(p-NPP, 2 mM) and PTP1B (0.05-0.1 μg) were added to a buffer containing 50mM citrate (pH 6.0), 1mMEDTA, 0.1MNaCl, and 1mM dithiothreitol, with or without test sample. Following incubation at 37°C for 30min, the reaction was terminated by adding 10M NaOH (10 μL). The amount of released produced p-nitrophenol (p-NP) was estimated by measuring the absorbance at 405 nm. The measured values were corrected for non-enzymatic hydrolysis of 2mMp-NP by measuring the increase in absorbance at 405 nm in the absence of the PTP1B enzyme.

α-Glucosidase inhibition:α-Glucosidase inhibitory activity was determined according to a previously reported method [9]. Briefly, for each compound, the extract was premixed with p-nitrophenylglucopyranoside (p-NPG) (2 mM) as a substrate in 2 mL 0.1 M phosphate buffer (pH=6.86). Then, α-glucosidase (0.05 units) was added to the mixture to start the reaction. The reaction was incubated at 37±0.5â for 15 min and stopped with 4 mL of 0.1 M Na2CO3. The α-glucosidase inhibitory activity was determined by measuring the absorbance at 400 nm as an indication forp-NP produced from p-NPG.

3Anti-inflammatory activity: The murine microglial BV2 cell lines were purchased from the Cell Culture Centre at the Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences. LPS (from Escherichia coli 055: B5), were obtained from Sigma-Aldrich. The inhibitory activity of extracted compounds on LPS-stimulated NO production in BV2 cells was measured as described previously [3].

Results and Discussion

Liparisodoratais was widely used as a folk medicine to inhibit inflammation and reduce lipid inChina, through our continuous interests in the bioactive constituents of this plant [2-4], on the basis of pharmacological action tracking method, systematically studies on the chemical compositions andbioactivities of Liparisodoratawere carried out, looking for new biological compounds.

Compound 1, a colorless solid, was assigned a molecular formula of C30H42O13 determined byhigh-resolution electrospray ionization mass spectrometry (HR-ESI-MS) of its quasi-molecular ion peak at m/z 610.2632 [M]+ (calcd. for 610.2625). The 1H NMR spectrum (Table1) displays the signals attributable to two aromatic protons at δH 7.54 (s, H-2, 6), two olefinic protons at δH 5.24 (t, J=8.5 Hz, H-8/13), two methylene protons at δH 3.45 (m, H-7/12), and four methyl protons at δH 1.68 (s, H-10/15) and 1.71 (s, H-11/16). The 13C NMR (Table 2) and HSQC spectra exhibited signals for two aromatic methenyl carbons at δC 128.5 (C-2, 6), and four quaternary carbons at δC 156.6 (C-4), δC 135.2 (C-3/5) and δC 126.5 (C-1), all indicating a meta-tetrasubstituted benzene ring. HMBC spectroscopy correlationswere observed from H-2/6 (δH 7.54) with carbonyl carbon (δC 167.2,C-17), suggesting that the carbonyl group was attached to C-1 (δ 126.5). The HMBC spectrum exhibited long-range correlations of H-7/12 (δH 3.45) with C-2/6 (δ 128.5), C-3/5 (δ 135.2), C-9/14 (δ 132.2) and C-4 (δ 156.6), indicating that there were two prenyl groups attached to the benzene ring at C-3 and C-5 [2-3]. The 2D-NMR spectra (Figure 2) showed the presence of an acetyl group at δH 1.62 (3H, s),δC 170.2 and δC20.0, this group was assigned to C-6'' (δC 63.9)from the HMBC cross-peak of H-6'' (δH 4.15 and δH 3.93) with the acetyl group (δC 170.2). Next, the proton resonances of the sugar units were observed, and their hydrolyzed productswere identified as α-L-arabinose and β-D-glucose by gas chromatography. In the HMBC spectrum, long-range correlations were observed of Ara H-1' (δ 4.72) with C-4 (δ 156.6), and Glc H-1'' (δ 4.46) with Ara C-2' (δ 80.5), indicating that the sugar moiety was located at C-4 of the aglycone unit. The spectral data were similar to the known compound methyl-3,5-bis(3-methyl-2-butenyl)-4-O-[β-D-glucopyranosyl-(1→2)-α-L-arabinopyranosyl] benzoate [10], except for the major difference in the presence of an additional acetyl group assigned to C-6''. Consequently, the structure of compound 1 was confirmed as 4-O-[a-L-arabinopyranosyl-(1→2)-6''-O-acetyl-β-D-glucopyranosyl]-3,5-bis(3-methyl-2-butenyl) benzoic acid(Figure1) and named liparisglycoside K(1).


Figure 2: HMBC and key correlations of compounds 1 and 2.

Compound 2 was obtained as a white amorphous powder. Its molecular formula was deduced as C31H44NaO14 from HR-ESI-MS at m/z 663.2622 [M + Na]+ (calcd. for C31H44NaO14, 633.2518). The 1H (Table 1) and 13C NMR date (Table 2) of 2 showed a close structural similarity to the aglycone moiety of compound 1, indicating that the major differences werein their sugar moieties. Aided by 2D-NMR analysis (Figure 2) of 2, one acetyl and two glucopyranosylgroups were confirmed. In HMBC data, long-range correlations were observed from Gluc H-1' (δH 4.69) with C-4(δC 156.0), and Gluc H-1'' (δH 4.25) with Gluc C-2' (δC 80.4), and the carbonyl carbons of the acetyl δC 170.0 with Gluc H-6'' (δH4.25), indicating that the acetyl unit was located at C-6' of the first Glc unit. The sugar residues were identified as two β-D-glucopyranosylgroups by GC of the hydrolyzed product. Thus, structure 2 was determined to be 4-O-[6'-O-acetyl-β-D-glucopyranosyl-(1→2)-β-D-glucopyranosyl]-3,5-bis(3-methyl-2-butenyl) benzoic acid, and the compound was named liparisglycoside L(2).

Compound 3 was isolated as colorless oil. Its molecular formula was established as C30H42O13 by analysis of the HR-ESI-MS spectrum at m/z 633.2522 [M+Na]+ (calcd. for C30H42O13,633.2518). The 1H (Table 1) and 13C NMR data (Table 2) of 3 were comparable to those of 1 and 2, showing that the main differences were in the sugar part and the location of the acetoxy (OAc) group. Connectivity of the OAc group was established from the HMBC spectrum, which showed a correlation between Ara H-4' (δH 4.16) and the carboxyl carbon of the acetyl unit (δC 170.0).Hence, the OAc group was located at C-4' of the Ara. Moreover, the sugar residues were identified as α-L-arabinose and β-D-glucose by GC of the hydrolyzed product. So the structure of 3 was established as 4-O-[4'-O-acetyl-α-L-arabinopyranosyl-(1→2)-β-D-glucopyranosyl]-3,5-bis(3-methyl-2-butenyl) benzoic acid, which was namedliparisglycoside M(3).

Compound 4 was obtained as a white amorphous powder. Its molecular formula was determined to be C25H34O9 by HR-ESI-MS at m/z 501.2094 [M+Na]+ (calcd. for C25H34NaO9, 501.2095). The 1H (Table 1) and 13C NMR data (Table 2) revealed that compound 4 was structurally very similar to compound 1, butthe molecular weight of compound 4 was 132 less than compound 1 due to the absence of an arabinose. The acetyl group [δH 1.89 (3H, s); δC 170.2, 20.5] was located at C-6',determined by the HMBC correlation of H-6' (δH 4.15, 4.05) with C=O (δC 170.2) (Figure 2), while the sugar residue was identified as β-D-glucopyranose by GC of the hydrolyzed product. Therefore compound4 was established as 4-O-(6'-O-acetyl-β-D-glucopyranosyl)-3,5-bis(3-methyl-2-butenyl) benzoic acid, named liparisglycoside N(4).

Compound 5, obtained as a white amorphous power, was assigned the molecular formula of C22H30O7 via HR-ESI-MS atm/z 429.1885 [M+Na]+ (calcd. for C22H30O7,429.1884). Analysis of the 1H (Table 1) and 13C-NMR spectra (Table 2) indicated that compound 5 also possessed a structure similar to compound 1 and that the major differences between them were the absence of the acetyl group and glucose. The sugar residue was identified as α-L-arabinose by GC of the hydrolyzed product. Therefore, the structure of compound 5 was determined to be 4-O-(a-L-arabinopyranosyl)-3,5-bis(3-methyl-2-butenyl) benzoic acid, named liparisglycoside O (5).

The biological activity of the above compounds 1-6, isolated from Liparisodorata, was tested by individual evaluationoftheirin vitrohypolipidemic activity against α-glucosidase and PTP1B enzymes. The results are summarized in Table 3. Only compound 3 showed inhibitory activity (9.7% of PTP1B and 6.1% of α-glucosidase), other compounds didn’t have significant effects. As the structure of compound 3 is different from other compounds by the existence of an acetoxy (OAc) group linking to the C-4 of Arabinose, and maybe it was the reason to have such bioactivities. In addition, the compounds were evaluatedin vitrofor their inhibition (%) oflipopolysaccharide (LPS)-stimulated nitric oxide (NO) production in BV2 microglial cells using the Griess reagent.As shown in Table 4, all compounds were found to possess weak inhibitory activity.

Compounda Concentration (µM) Inhibition (%) of PTP1B

Inhibition(%) of

1 10 0.2


2 10 2.5


3 10 9.7


4 10 3.2


5 10 -0.2


6 10 9.5


Table 3: Inhibitory effects of isolated compounds 1-6 on PTP1B enzyme and a-Glucosidase.


Compounds Concentration (Mol/L) Inhibition (%)
1 10-5 20.43
2 10-5 1.11
3 10-5 20.30
4 10-5 15.05
5 10-5 19.89
6 10-5 19.56
Curcumina 10-5 62.16

Table 4: Inhibitory activities on LPS-induced NO production in BV2 of compounds 1-6.


In summary, five new phenolic glycosides (1-5), along with one known compounds (6) were isolated from L. odorata. We found only compound 3 showed weak inhibitory activityagainst α-glucosidase and PTP1B enzymesand all the compounds possessed anti-inflammatory effects by inhibition the NO production in LPS-activatedBV2 microglial cells. Further studies on the action mechanismof phenolic glycosides compounds of Liparisodorata were taken in our laboratory, it was better to expand the usage of this ancient and effective folk medicine.

Conflict of Interest

The authors confirm that this article content has no conflictof interest.


The authors are grateful to the National Natural Science Foundation of China (No.81260629), the Jiangxi province young scientist training fund (Jing gang star item, 2008-222), the Jiangxi province major fund of Education Ministry (GJJ12515), and the Jiangxi province fund of Medical Ministry (2009A056).


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