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Heliyon
2024 Aug 15;1017:e36943. doi: 10.1016/j.heliyon.2024.e36943.
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Identification of novel anti-obesity saponins from the ovary of sea cucumber (Stichopus japonicus).
Seo HD
,
Lee JY
,
Park SH
,
Lee E
,
Hahm JH
,
Ahn J
,
Jang AR
,
An SH
,
Ha JH
,
No KT
,
Jung CH
.
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The potential anti-obesity effects of sea cucumber extract have been reported. However, the individual saponins responsible for these effects are yet to be isolated and characterized. This study aimed to identify the most effective sea cucumber body part for inhibiting lipid accumulation in adipocytes and to elucidate the compounds responsible for this effect using nuclear magnetic resonance (NMR) techniques. Sea cucumber ovary 80 % ethanol extract (SCOE) demonstrated remarkable efficacy in inhibiting adipocyte differentiation compared to other sea cucumber body parts with 50 % or 80 % ethanol extracts. SCOE anti-obesity effect was evaluated in C57BL/6 mice fed a high-fat diet, which revealed significant reductions in body weight, serum lipids, adipose tissue, and liver weight. Using column chromatography, eight saponins were isolated from the SCOE, four of which exhibited potent inhibitory effects on adipocyte differentiation. Of these, three active saponins, holotoxins A, B, and D1, were newly identified. These findings highlight the potential of SCOE and its saponins as effective anti-obesity agents.
Fig. 1. Anti-adipogenic effects of ethanol extracts from different sea cucumber parts. (A) 3T3-L1 cells were treated with ethanol extracts from different sea cucumber body parts and cell viability was measured using MTT assay kit. (B) Oil Red O (ORO) staining images and (C) intensity of differentiated 3T3-L1 cells treated with the different ethanol extracts. (D) Protein levels of FAS, PPARγ, FABP4, and C/EBPα in 3T3-L1 cells treated with the ethanol extracts (non-adjusted images are provided in Supplementary Fig. 1). The derived data and significant differences compared to the veh group were as follows: mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001.
Fig. 2. SCOE significantly reduces body weight gain in obese mice fed a high-fat diet. (A) Body weight changes and (B) measurement of body weight gain in mice observed after inclusion of 0.05, 0.1, and 0.2 % SCOE in the HFD group for eight weeks. (C) Measurement of changes in blood glucose levels using oral glucose tolerance test and (D) quantification of data from the area under the curve. (E) Serum insulin, adiponectin, and leptin levels. (F) Quantification of serum cholesterol and triglyceride concentrations. Derived data and significant differences compared to the HFD + veh group were as follows: mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001. SCOE, sea cucumber ovary extract; LFD, low-fat diet; HFD, high-fat diet.
Fig. 3. SCOE reduces the weight of adipose tissues in obese mice. (A) Weight measurement of WAT. (B) Histological analysis of the size of eWAT and (C) measurement of lipid droplet size and frequency in eWAT. (D) Measurement of mRNA expression levels of target genes related to adipogenesis compared to GAPDH in eWAT. The derived data and significant differences compared to the HFD + veh group were as follows: mean ± SEM, *p < 0.05, **p < 0.01. WAT, white adipose tissue; scWAT, subcutaneous WAT; rWAT, retroperitoneal WAT; eWAT, epididymal WAT; SCOE, sea cucumber ovary extract; LFD, low-fat diet; HFD, high-fat diet.
Fig. 4. SCOE improves fatty liver in obese mice. (A) Weights of the liver of mice in the HFD + veh and SCOE-intake groups. (B) Measurement of triglycerides, total cholesterol, and lipid levels in liver. (C) Liver morphology and histological analysis. (D) Measurement of mRNA expression levels of target genes related to lipogenesis compared to GAPDH in eWAT. Derived data and significant differences compared to the HFD + veh group were as follows: mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001. SCOE, sea cucumber ovary extract; LFD, low-fat diet; HFD, high-fat diet; TG, triglycerides; TC, total cholesterol.
Fig. 5. Flow diagram for the separation and purification of saponins from SCOE. RPCC: reverse-phase column chromatography. NPCC: normal phase column chromatography.
Fig. 6. Inhibitory effect of adipogenesis of saponins isolated from SCOE. (A) ORO staining and (B) intensity of differentiated 3T3-L1 cells. (C) Cell viability. (D) Protein levels of FAS, PPARγ, FABP4, and C/EBPα in 3T3-L1 cells (non-adjusted images are provided in Supplementary Figs. 2–4). *p < 0.05, **p < 0.01, ***p < 0.001.
Fig. 7. Putative structures of saponins with anti-adipogenesis effect. (A) Holotoxin D1, (B) Holotoxin B, and (C) Holotoxin A.
