Anti-differentiation effect of B, D-seco limonoids of Swietenia mahogani
Heejung Yang1, Mina Choi2, Dong Young Lee2, Sang Hyun Sung2
1 College of Pharmacy, Kangwon National University, Chuncheon, Republic of Korea
2 College of Pharmacy and Research Institute of Pharmaceutical Science, Seoul National University, Seoul, Republic of Korea
|Date of Submission||20-Jan-2016|
|Date of Acceptance||10-Feb-2016|
|Date of Web Publication||18-Apr-2017|
Prof. Sang Hyun Sung
College of Pharmacy and Research, Institute of Pharmaceutical Science, Seoul National University, Seoul
Republic of Korea
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: Obesity is a pathological state caused by abnormal or excessive accumulation of fat. Swietenia mahogani JACQ., known as West Indian mahogany, is a medium-sized semi-evergreen tree belonging to Meliaceae. Their seeds are used in Indonesian folk medicine as a treatment for hypertension, diabetes, malaria, and it also has anti-feedant activities. The major components of S. mahogani are B, D-seco limonoids, a type of irregular triterpenes are well known. Objective: We tried to find the bioactive components, which have the inhibitory activity on adipocyte differentiation from the seeds of S. mahogani. Material and Methods: 3T3-L1 cells, derived from mouse preadipocyte, are widely used in studying adipogenesis process. In this study, we used 3T3-L1 cells to find natural products with the inhibitory activity on adipocyte differentiation. S. mahogani seeds were dried and extracted with 100% MeOH. Results: The methanolic extract was fractionated by bioassay-guided method to give nine B, D-seco limonoids (1-9) with slight structural modifications. Among nine compounds, compounds 4, 6 and 8 exhibited significant inhibitory effects of cell differentiation on 3T3-L1 cells. Those compounds have tigloyl residue at C-3 in common. Besides, compounds with no tigloyl residue at C-3 showed insignificant effect. Nevertheless, not all compounds with tigloyl residue at C-3 exerted significant inhibitory effect. Conclusion: These results suggested that tigloyl residue at C-3 may play a role in the anti-proliferative activity on a dipogenesis and the refined extract of S. mahogani may have a potential to be developed as a therapeutic agent to treat obesity.
Keywords: 3T3-L1, adipogenesis, obesity, seco-limonoid, structure and activity relationship, Swietenia mahogani
|How to cite this article:|
Yang H, Choi M, Lee DY, Sung SH. Anti-differentiation effect of B, D-seco limonoids of Swietenia mahogani. Phcog Mag 2017;13:293-9
|How to cite this URL:|
Yang H, Choi M, Lee DY, Sung SH. Anti-differentiation effect of B, D-seco limonoids of Swietenia mahogani. Phcog Mag [serial online] 2017 [cited 2021 Jul 23];13:293-9. Available from: http://www.phcog.com/text.asp?2017/13/50/293/204549
- Nine irregular seco-limonoids were isolated from Swietenia mahogani.
- Total extract and CHCl3 fraction of S. mahogani showed the significant inhibitory activities on 3T3-L1 cell differentiation.
- A tigloyl residue at C-3 in an aglycone may play a role in the anti-proliferative activity on adipogenesis.
| Introduction|| |
Obesity is a major cause of the risk factors for various metabolic and cardiovascular diseases such as fatty liver, diabetes, hypertension, and hyperlipidemia. Adipogenesis is a process where fibroblastic preadipocytes become mature adipocytes. It brings the abnormal accumulation by an increase in the sizes or numbers of adipocytes from precursor cells. Thus, the control of the differentiation of preadipocytesinto adipocytes is the crucial point for the prevention of obesity. However, many medicines available in the market for losing or controlling of weight are not successful in the long-term maintenance of over-weight patients. To find the anti-adipogenetic agents from natural products, 3T3-L1 cells were selected as in vitro screening tool. These cells are preadipocytes derived from mouse and sub-clones of swiss mouse embryo 3T3, and differentiate into adipocyte-like phenotype under the exposure of adipogenic inducers, such as fetal bovine serum, dexamethasone, isobutylmethylxanthine, and insulin. In the present study, we used 3T3-L1 cells to find natural products with the inhibitory activity on adipocyte differentiation, which are expected to lose or control body's over-weight.
Swietenia mahogani JACQ., known as West Indian mahogany, is a medium-sized semi-evergreen tree belonging to Meliaceae. It is native to West Indies and cultivated in tropical countries. Its seeds are used as a treatment for hypertension, diabetes and malariain Indonesian folk medicine. Decoction of its bark has been used as febrifuge or anti-malarial drug. Furthermore, some studies reported that it acts as a blood platelet aggregation inhibitor. The well known constituents are mainly limonoids, especially B, D-seco limonoids, which are derivatives of limonoids oxidized rings B and D of limonoid. To the best of our knowledge, the study of the extract or compounds of S. mahogani on anti-adipogenesis has not been reported. As a result, we isolated B, D-seco limonoids (1-9) from the seeds of S. mahogani and elucidated their anti-adipogenesis against 3T3-L1 cells.
| Material and Methods|| |
First grade solvent for extraction, fractionation and isolation were purchased from Dae Jung Pure chemical Eng. Co. Ltd. (Ansan, Korea), and HPLC grade solvents from Fisher Scientific (Pittsburgh, PA, USA). Dulbecco's modified Eagle's media (DMEM), penicillin/streptomycin, trypsin, PBS for cultures of 3T3-L1 cells were purchased from Sigma Chemical Co. (St. Louis, MO, USA). MTT, IBMX, dexamethasone, insulin, EGCG, Nonidet P-40, isopropyl alcohol, and reagents for ORO were also obtained from Sigma Chemical Co. (St. Louis, MO, USA). FBS, CS were obtained from Hyclone Co. (Logan, UT, USA), Gibco Co. (Grand Island, NY, USA), respectively. Multi-well culture plate and cell culture dishes were purchased from Corning (New York, NY, USA).
The Seeds of S. mahogani were collected at Jakarta, Indonesia in August 2012 and air-dried. These seeds were identified by Prof. Sang Hyun Sung, one of the authors in the present study; (SNUPH-0830) has been stored in the Herbarium of the Medicinal Plant Garden, Seoul National University.
Isolation of compounds 1-9 from the seeds of S. mahogani
Dried seeds (1.2 kg) of S. mahogani were extracted with 100% MeOH (4L × 3) in an ultrasonic apparatus. After removal of the solvent in vacuo, the 100% MeOH extract (444.6 g) was suspended in H2O and successively partitioned into n-hexane fraction (1.2 g), CHCl3 fraction (110.9 g), EtOAc fraction (0.4 g), and n-BuOH fraction (6.7 g), respectively. Among these fractions, CHCl3 fraction showing significant anti-differentiation effect on 3T3-L1 cells was subjected to repeated column chromatography and HPLC to give compounds 1-9.
The CHCl3 fraction was subjected to silica gel column chromatography (CC) and eluted with mixtures of n-hexane-EtOAc = 10:1, 3:1, 1:1, CHCl3-MeOH= 10:1, to yield twelve fractions (C1 ~ C12) and compound 1 (1401 mg). C6 was subjected to ODS silica gel HPLC with MeCN-H2O (6:4, 6 ml/min) to give compound 4 (81 mg). C8 was subjected to silica gel CC and eluted with mixtures of CHCl3-MeOH = 100:1, 50:1, 10:1, 1:1 to give compounds 6 (143 mg) and 8 (247 mg). Compound 3 (895 mg) was isolated from C10 by recrystallization (MeOH). C11 was subjected to silica gel MPLC gradient eluting with mixtures of n-hexane-EtOAc (62:38, 0:100) to give thirteen fractions (C11-1 ~ C11-13) and compound 7 (117 mg). C11-12 was further separated into six fractions (C11-12-1 ~ C11-12-6) by ODS silica gel HPLC with MeCN-H2O (5:5, 6 ml/min). C11-12-2 was subjected to ODS silica gel HPLC with MeCN-H2O (7:3, 6 ml/min) again to give compound 2 (42mg). C11-12-6 was subjected to ODS silica gel HPLC in same condition to give compounds 5 (22 mg) and 9 (209 mg).
Swietenolide (1): white amorphous powder; C27H34O8;[α]25D: -140.1000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 3496, 1721, 876; HRMS (positive mode): m/z 487.2332 [M+H]+(calc. mass: 487.2336); 1H NMR (CDCl3, 500 MHz): see [Table 1]; 13C NMR (CDCl3, 125 MHz): see [Table 2].
3-O-acetylswietenolide (2): white amorphous powder; C29H36O9; [α]25D: -90.1000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 3495, 1732, 876; HRMS (positive mode): m/z 529.2438 [M+H]+(calc. mass: 529.2438); 1H NMR (CDCl3, 400 MHz): see [Table 1]; 13C NMR (CDCl3, 100 MHz): see [Table 2].
3,6-O,O-diacetylswietenolide (3): white amorphous powder; C31H38O10; [α]25D: -206.7000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 1737, 876; HRMS (positive mode): m/z 571.2543 [M+H]+(calc. mass: 571.2543); 1H NMR (CDCl3, 500 MHz): see [Table 1]; 13C NMR (CDCl3, 125 MHz): see [Table 2].
khayasin T (4): white amorphous powder; C32H40O8; [α]25D: -121.7000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 1728, 876; HRMS (positive mode): m/z 553.2801 [M+H]+(calc. mass: 553.2801); 1H NMR (CDCl3, 400 MHz): see [Table 1]; 13C NMR (CDCl3, 100 MHz): see [Table 2].
3-O-tigloylswietenolide (4): white amorphous powder; C32H40O9; [α]25D: -120.4000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 3489, 1719, 876; HRMS (positive mode): m/z 569.2751 [M+H]+(calc. mass: 569.2744); 1H NMR (CDCl3, 500 MHz): see [Table 1]; 13C NMR (CDCl3, 125 MHz): see [Table 2].
Febrifugin (6): white amorphous powder; C32H40O8; [α]25D: -100.6000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 1727, 876; HRMS (positive mode): m/z 553.2808 [M+H]+(calc. mass: 553.2808); 1H NMR (CDCl3, 500 MHz): see [Table 1]; 13C NMR (CDCl3, 125 MHz): see [Table 2].
Swietenine (7): white amorphous powder; C32H40O9; [α]25D: -76.0000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 3470, 1725, 876; HRMS (positive mode): m/z 569.2751 [M+H]+(calc. mass: 569.2748); 1H NMR (CDCl3, 600 MHz): see [Table 1]; 13C NMR (CDCl3, 150 MHz): see [Table 2].
Swietenine acetate (8): white amorphous powder; C34H42O10; [α]25D: -139.3000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 1728, 876; HRMS (positive mode): m/z 611.2857 [M+H]+(calc. mass: 611.2856); 1H NMR (CDCl3, 500 MHz): see [Table 1]; 13C NMR (CDCl3, 125 MHz): see [Table 2].
Swietemahonin E (9): white amorphous powder; C32H40O10; [α]25D: -100.7000 (c=0.1, chloroform); IR vmax (KBr) (cm-1): 3495, 1729, 876; HRMS (positive mode): m/z 585.2717 [M+H]+(calc. mass: 585.2700); 1H NMR (CDCl3, 500 MHz): see [Table 1]; 13C NMR (CDCl3, 125 MHz): see [Table 2].
Cell culture and adipocyte differentiation
Mouse embryo fibroblasts 3T3-L1 cells were obtained from the American Type Culture Collection (Manassas, VA, U.S.A.) and incubated in DMEM supplemented with 10% bovine calf serum until confluence. Two days after confluence (designated day 0), preadipocytes were stimulated to differentiate with differentiation medium (DM, DMEM with 10% FBS, 0.5 mM 3-isobutyl-1-methyl-xanthine, 10 µg/mL insulin and 1 µM dexamethasone) for 2 days (day 2). Cells were then maintained in DM (DMEM 10% FBS and 10 µg/mL insulin) for other 2 days (day 4), followed by culturing with DM (DMEM with 10% FBS) for additional 4 days (day 8). All media contained 100 IU/mL penicillin and 100 mg/mL streptomycin. The cells were maintained at 37°C in a humidified atmosphere of 95% air - 5% CO2. Test compounds were dissolved in DMSO (final concentration of 0.1% in media). The cultures were treated with test samples for the whole culture period (day 0-8).
Oil red o staining
Lipid droplets in cells were stained with Oil Red O (ORO) on day 8. Briefly, culture dishes were washed three times with PBS and fixed with 10% formalin for 1 hour at room temperature. After fixation, cells were washed once with PBS and stained with a filtered ORO solution (6 parts of saturated 0.6% ORO in isopropyl alcohol and 4 parts of water) for 15 minutes at room temperature. Cells were washed twice with water for 15 minutes and visualized. To quantify the intracellular lipids, spectrophotometrical quantification of the stain was performed by dissolving the stained lipid droplets with 4% Nonidet P-40 in isopropyl alcohol for 5 minutes. The absorbance was measured at 544 nm. Lipid contents (% of control) =A540nm (sample-undifferentiated control)/A540nm (differentiated control-undifferentiated control) × 100.
Statistical analysis was performed using Student's t test. Data were expressed as the means ± standard deviation (SD). Statistical significance was represented with an asterisk for p values < 0.05, two asterisks for p values < 0.01 and three asterisks for p values < 0.001.
| Results|| |
Identification of chemical structure of compounds from the seeds of S. mahogani
Nine B, D-seco limonoids (1-9) were isolated from the seeds of S. mahogani using series of column chromatographies and elucidated as swietenolide (1), 3-O-acetylswietenolide (2), 3, 6-OO-diacetylswietenolide (3), khayasin T (4), 3-O-tigloylswietenolide (5), febrifugin (6), swietenine (7), swietenine acetate (8) and swietemahonin E (9) by the various spectroscopic techniques [Figure 1].
Compound 1 exhibited molecular ion peak at m/z 487.2332 [M+H]+ indicating C27H34O8 as its molecular formula in the positive HRMS analysis. The IR spectrum showed the presence of hydroxyl (3496 cm-1), carbonyl (1721 cm-1) and furan ring (876cm-1) as the functional groups. The 1H, 13C NMR and HMQC spectral data demonstrated the presence of one ketone at δC 219.7 (C-1), two carboxyl groups at δC 175.8 (C-7) and 171.3 (C-16), two hydroxyl groups at δH/δC3.54 (1H, J = 9.7 and 3.4 Hz, H-3)/78.5 (C-3) and 4.50 (1H, s, H-6)/73.6 (C-6), and four methyl groups at δH/δC0.95 (3H, s, H-18)/17.9 (C-18), 1.37 (3H, s, H-19)/17.9 (C-19) and 0.96 (3H, s, H-28)/23.2 (C-28), 0.83 (3H, s, H-29)/23.6 (C-29). In addition, furan ring was present at δH/δC 120.8 (C-20) and 7.44 (1H, s, H-21)/141.0 (C-21), and 6.37 (1H, s, H-22)/109.8 (C-22) and 7.38 (1H, s, H-23)/142.9 (C-23). On the basis of above information, compound 1 was estimated to be a B, D-seco limonoid found in Meliaceae plants. The HMBC correlations from δH5.44 (1H, s, H-17) to δC120.8 (C-20), 141.0 (C-21) and 109.8 (C-22) indicated the existence of the furan ring at C-17. A double bond existing between C-8 (δC 129.03) and C-14 (δC 130.78) was located in C-ring by the HMBC signals from δH3.15 (1H, dd, J = 14.4 and 2.3 Hz, H-30a) and 1.99 (1H, m, H-30b) to δC 129.0 (C-8) and 130.8 (C-14). With above data, the structure of compound 1 was established as swietenolide. Compound 2 exhibiting the molecular ion peak at m/z 529.2438 [M+H]+ has the molecular formula for C29H36O9. The 1H, 13C NMR and HMQC spectrum demonstrated similar patterns with compound 1 except for the presence of an acetyl group at δC170.28 (C-1') and δH/δC 2.12 (3H, s, H-2')/21.1 (C-2') instead of the hydroxyl group at C-3 in compound 1. The location of the acetyl group was determined by the HMBC correlations from δH4.79 (1H, d, J = 9.9 Hz, H-3) to δC170.3 (C-1').On the basis of the above data, the structure of compound 2 was established as 3-O-acetylswietenolide. Compound 3 with C31H38O10 determined by the molecular ion peak at m/z 571.2543 [M+H]+ showed the similar structure with compounds 1 and 2 by the 1H, 13C NMR and HMQC spectra. The HMBC analysis indicated that two acetyl groups were located at C-3 and C-6, respectively, by the signals at δH/δC4.85 (1H, d, J = 10.0 Hz, H-3)/170.3 (C-1') and 5.44 (1H, s, H-6)/169.7 (C-2''). Consequently, compound 3 was established as 3, 6-O,O-diacetyl swietenolide. Compound 4 has C32H40O8 as its molecular formula determined by the molecular ion peak at m/z 553.2801 [M+H]+. Similar to compound 1 and 2, it had the tigloylmoiety at C-3 by the signals at δC167.4 (C-1'), 128.9 (C-2') and δH/δC 6.93 (1H, m, C-3')/139.3 (C-3'), 1.86 (3H, s, CH3at C-2')/12.3 (CH3 at C-2'), 1.81 (3H, m, CH3 at H-3')/14.6 (CH3 at C-3') by the 1D and 2D NMR spectroscopic data. Also the HMBC correlations of δH/δC4.82 (1H, d, J=9.7 Hz, H-3)/176.4 (C-1') indicated that the tigloyl group existed at C-3. With above data, the structure of compound 4 was determined as khayasin T. Compound 5 with the molecular ion peak at m/z 569.2751 [M+H]+ with C32H40O9 indicated the similar structure with compound 4. According to the HMBC correlations, compound 5 had a tigloyl moiety at C-3 by the characteristic values from δH4.67 (1H, d, J = 9.8 Hz, H-3) to δC167.2 (C-1'), from δH 1.88 (3H, m, CH3at C-2') to δC 129.0 (C-2') and from δH 1.80 (3H, m, CH3at C-3') to δC 139.0 (C-3'). A hydroxyl moiety was located at C-6 by the signals at δH/δC3.34 (1H, s, H-6)/73.3 (C-6). Therefore, compound 5 was identified as 3-O-tigloyl swietenolide. Compound 6 with C32H40O8 by the molecular ion peak at m/z 553.2808 [M+H]+. Compound 6 was significantly similar to those of compound 4 by 1D and 2D NMR spectroscopic data except for the signals responding to the double bond at δH/δC138.5 (C-8) and 5.30 (1H, d, J = 7.1 Hz, H-30)/123.0 (C-30). Thus, compound 6 was established as febrifugin. Compounds 7 (C32H40O9, m/z 569.2751 [M+H]+) and 8 (m/z 611.2857 [M+H]+, C34H42O10) had same backbones with compound 6 except for the derivatives attached at C-6 in 1D and 2D NMR spectra data. Compounds 7 and 8 has a hydroxyl moiety indicated by δC72.7 (C-6 in 7) and acetyl moiety by δC169.7 (COCH3 in 8) and 21.0 (COCH3 in 8) instead of a hydrogen bond, respectively. Therefore, they were identified as swietenine (7) and swietenine acetate (8), respectively. Compound 9 (C32H40O10, m/z 585.2717 [M+H]+) had one more oxygen molecule by the comparison to compound 7. Two oxygenated signals at δC60.3 (C-8) and 63.0 (C-30) existed instead of those of a double bond. Their up-fielded signals indicated the presence of an epoxide moiety. Consequently, the structure of compound 9 was established as swietemahonin E.
Chemical fingerprint of S. mahogani seeds using ESI-QTOF-MS
The CHCl3 fraction of the seeds of S. mahogani was analyzed to monitor the chemical profile by UPLC-ESI-QTOF-MS [Figure 2]. Nine compounds isolated from CHCl3 fraction were detected and identified by the comparison of the retention times and m/z valuesin CHCl3 fraction compared with those of compounds 1-9 [Table 3].
|Figure 2: The chromatogram of CHCl3fraction from S. mahogani analyzed by UPLC-QTOF-MS.|
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|Table 3: Spectral and chromatographic data of compounds 1-9 detected in CHCl 3 fraction of S. mahogani seeds.|
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Anti-differentiation activities of total extract, fractions and the compounds from the seeds of S. mahogani against 3T3-L1 cells
Inhibitory effect on adipocyte differentiation in 3T3-L1 cells was investigated with total extract, CHCl3 and BuOH fraction, and aqueous residue [Figure 3]A. After inducing of the differentiation of 3T3-L1 cells, total extract and CHCl3 fraction showed significant inhibitory activities on 3T3-L1 cell differentiation compared to the other fractions, BuOH fraction and aqueous residue.
|Figure 3: Inhibitory effect of total extract and fractions (A) and compounds 1-9 (B) of S. mahogani seeds on 3T3-L1 differentiation|
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Compounds 1-9 isolated from CHCl3 fraction were treated on 3T3-L1 cells [Figure 3]B. Among them, compounds 4, 6 and 8 showed significant anti-differentiation activities in dose-dependent manner at the concentrations of 50 and 100 μM against 3T3-L1 cells.
| Discussion|| |
S. mahogani produces active secondary metabolites, limonoids, which have been known to possess a wide range of biological activities. We isolated nine B, D-seco limonoids derivatives with slight modifications, such as hydroxylation, acetylation and tigloylation, from the seeds of S. mahogani and evaluated their anti-differentiation activities against 3T3-L1 cells. Blocking adipogenesis (adipocyte differentiation) has been considered as an effective prevention strategy for obesity. 3T3-L1 cells are being used as a useful tool to investigate biological factors affecting adipogenesis. We performed in vitro study for the evaluation of the inhibitory effect on adipocyte differentiation in 3T3-L1 cells by total extract, sub-fractions, and B, D-seco limonoids (1-9) isolated from CHCl3 fraction. Compounds 1-9 were highly substituted with hydroxyl, acetyl or tigloyl moieties and showed different inhibitory activities against 3T3-L1 cells. Compounds 4, 6 and 8 showing the significant anti-differentiation activities had a tigloyl moiety at C-3 in common. But it is in appropriate to make an assumption that it is essential for leading to inhibitory effect on adipocyte differentiation because compounds 5, 7 and 9 having a tigloyl moiety showed weak inhibitory activities. It was estimated that a tigloyl residue may not be an essential factor for anti-differentiation of 3T3-L1 cells, but give an effect on anti-differentiation.
| Conclusion|| |
Limonoids are known to have a wide range of activities including anti-malarial, anti-cancer, anti-HIV, and anti-feedant on insects. We reported B, D-seco limonoids have an anti-differentiation against 3T3-L1 cells. It might need the structure and activity relationship study against the 3T3-L1 cells differentiation according to the types of backbone or functional groups in the further study.
This research was supported by a grant of the Korea Health Technology R and D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health and Welfare, Republic of Korea (No. HI15C0075) and 2015 Research Grant from Kangwon National University (No. 520150296)
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]