Skip to main content
SpringerLink
Log in

Dietary Supplementation with Sea Cucumber Saponins and Exercise Can Significantly Suppress Adipose Accumulation in Mice Fed with High-Fat Diet

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

Dietary supplementation with sea cucumber saponins (SCS) and exercise have been confirmed to be effective in preventing the development of obesity and its related diseases. However, the combined effectiveness of these interventions has not been explored. Here, we studied whether the beneficial influences of exercise could be further enhanced by dietary supplementation with SCS in high-fat diet-fed KM (Kunming) mice. Mice were randomly divided into four groups, including the high-fat diet group (HF), the SCS group (HF-S), the exercise group (HF-E), and the combination of dietary SCS and exercise group (HF-S + E). There were eight mice in every group. The results demonstrated that the combination of dietary SCS and exercise could synergistically reduce fat accumulation. In particular, white adipose tissue decreased by 63% in the HF-S + E group compared with that in the HF group. SCS supplementation with exercise also improved peripheral markers, such as serum parameters and hepatic TG levels. Further mechanical testing indicated that the combined effects of dietary SCS and exercise on inhibiting fat accumulation might be attributed to the inhibition of lipid synthesis in the liver and the activation of lipolysis in white adipose tissue to increase energy consumption.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ACC1 :

1-aminocyclopropane-1-carboxylate 1

ACOX1 :

acyl-coenzyme A oxidase 1

ATGL :

adipose triglyceride lipase

ACAA1 :

acetyl-coenzyme A acyltransferase 1

CPT1a :

carnitine palmitoyl transferase 1a

CPT2 :

carnitine palmitoyl transferase 2

EA:

echinoside A

FAS :

fatty acid synthase

FABP4 :

fatty acid binding protein 4

FFA:

free fatty acid

G6PDH :

glucose-6-phosphate dehydrogenase

GC:

gas chromatography

HA:

holothurin A

HDL-C:

density lipoprotein cholesterol

HF:

high-fat diet group

HF-S:

sea cucumber saponins group

HF-E:

exercise group

HF-S + E:

sea cucumber saponins and exercise group

HSL :

hormone-sensitive lipase

LPL :

lipoprotein lipase

LDL-C:

low-density lipoprotein-cholesterol

ME :

malic enzyme

PPARα :

peroxisome proliferator activated receptor alpha

PPARγ :

peroxisome proliferator-activated receptor γ

SCS:

sea cucumber saponins

SCD1 :

stearoyl-coenzyme A desaturase 1

SREBP-1c :

sterol regulatory element binding transcription factor 1

TC:

cholesterol

TG:

triacylglycerol

References

  • Adegboye, A. R. A., and Linne, Y. M., 2013. Diet or exercise, or both, for weight reduction in women after childbirth. Cochrane Database of Systematic Reviews, 7: CD005627.

    Google Scholar 

  • Bhattacharya, A., Rahman, M. M., Sun, D., Lawrence, R., Mejia, W., McCarter, R., O’shea, M., and Fernandes, G., 2005. The combination of dietary conjugated linoleic acid and treadmill exercise lowers gain in body fat mass and enhances lean body mass in high fat-fed male balb/c mice. The Journal of Nutrition, 135(5): 1124–1130.

    Article  Google Scholar 

  • Brunani, A., Caumo, A., Graci, S., Castagna, G., Viberti, G., and Liuzzi, A., 2008. Rosiglitazone is more effective than metformin in improving fasting indexes of glucose metabolism in severely obese, non-diabetic patients. Diabetes, Obesity and Metabolism, 10(6): 460–467.

    Article  Google Scholar 

  • Carlson, C., and Winder, W., 1999. Liver AMP-activated protein kinase and acetyl-CoA carboxylase during and after exercise. Journal of Applied Physiology, 86(2): 669–674.

    Article  Google Scholar 

  • Chen, G., Liang, G., Ou, J., Goldstein, J. L., and Brown, M. S., 2004. Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proceedings of the National Academy of Sciences, 101(31): 11245–11250.

    Article  Google Scholar 

  • Cho, A. S., Jeon, S. M., Kim, M. J., Yeo, J., Seo, K. I., Choi, M. S., and Lee, M. K., 2010. Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice. Food and Chemical Toxicology, 48(3): 937–943.

    Article  Google Scholar 

  • Davitt, P. M., Arent, S. M., Tuazon, M. A., Golem, D. L., and Henderson, G. C., 2013. Postprandial triglyceride and free fatty acid metabolism in obese women after either endurance or resistance exercise. Journal of Applied Physiology, 114(12): 1743–1754.

    Article  Google Scholar 

  • Dyck, D. J., and Bonen, A., 1998. Muscle contraction increases palmitate esterification and oxidation and triacylglycerol oxidation. American Journal of Physiology-Endocrinology and Metabolism, 275(5): E888–E896.

    Article  Google Scholar 

  • Eaton, S., 2002. Control of mitochondrial β-oxidation flux. Progress in Lipid Research, 41(3): 197–239.

    Article  Google Scholar 

  • Folch, J., Lees, M., and Stanley, G. S., 1957. A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry, 226(1): 497–509.

    Article  Google Scholar 

  • Galani, C., and Schneider, H., 2007. Prevention and treatment of obesity with lifestyle interventions: Review and meta-analysis. International Journal of Public Health, 52(6): 348–359.

    Article  Google Scholar 

  • Guo, L., Gao, Z., Zhang, L., Guo, F., Chen, Y., Li, Y., and Huang, C., 2016. Saponin-enriched sea cucumber extracts exhibit an antiobesity effect through inhibition of pancreatic lipase activity and upregulation of LXR-β signaling. Pharmaceutical Biology, 54(8): 1312–1325.

    Article  Google Scholar 

  • Hu, X. Q., Wang, Y. M., Wang, J. F., Xue, Y., Li, Z. J., Nagao, K., Yanagita, T., and Xue, C. H., 2010. Dietary saponins of sea cucumber alleviate orotic acid-induced fatty liver in rats via PPARα and SREBP-1c signaling. Lipids in Health and Disease, 9(1): 25.

    Article  Google Scholar 

  • Karbowska, J., and Kochan, Z., 2012. Fat-reducing effects of dehydroepiandrosterone involve upregulation of ATGL and HSL expression, and stimulation of lipolysis in adipose tissue. Steroids, 77(13): 1359–1365.

    Article  Google Scholar 

  • Kushner, R. F., 2014. Weight loss strategies for treatment of obesity. Progress in Cardiovascular Diseases, 56(4): 465–472.

    Article  Google Scholar 

  • Lavoie, J. M., and Gauthier, M. S., 2006. Regulation of fat metabolism in the liver: Link to non-alcoholic hepatic steatosis and impact of physical exercise. Cellular and Molecular Life Sciences CMLS, 63(12): 1393–1409.

    Article  Google Scholar 

  • Liu, R., Zheng, Y., Cai, Z., and Xu, B., 2017. Saponins and flavonoids from adzuki bean (Vigna angularis L.) ameliorate high-fat diet-induced obesity in ICR mice. Frontiers in Pharmacology, 8: 687.

    Article  Google Scholar 

  • Liu, X., Cui, J., Leng, K., Xue, C., Li, Z., Xue, Y., and Wang, Y., 2016. Docosahexaenoic acid-enriched phospholipids exhibit superior effects on obesity-related metabolic disorders to egg yolk phospholipids and soybean phospholipids in mice. European Journal of Lipid Science and Technology, 118(11): 1712–1721.

    Article  Google Scholar 

  • Liu, X., Cui, J., Li, Z., Xu, J., Wang, J., Xue, C., and Wang, Y., 2014. Comparative study of DHA-enriched phospholipids and EPA-enriched phospholipids on metabolic disorders in diet-induced-obese C57BL/6J mice. European Journal of Lipid Science and Technology, 116(3): 255–265.

    Article  Google Scholar 

  • Marques, C., Motta, V., Torres, T., Aguila, M., and Mandarimde-Lacerda, C., 2010. Beneficial effects of exercise training (treadmill) on insulin resistance and nonalcoholic fatty liver disease in high-fat fed C57BL/6 mice. Brazilian Journal of Medical and Biological Research, 43(5): 467–475.

    Article  Google Scholar 

  • Meng, J., Hu, X., Zhang, T., Dong, P., Li, Z., Xue, C., Chang, Y., and Wang, Y., 2018. Saponin from sea cucumber exhibited more significant effects than ginsenoside on ameliorating high fat diet-induced obesity in C57BL/6 mice. MedChemComm, 9(4): 725–734.

    Article  Google Scholar 

  • Ohyama, K., Nogusa, Y., Suzuki, K., Shinoda, K., Kajimura, S., and Bannai, M., 2014. A combination of exercise and capsinoid supplementation additively suppresses diet-induced obesity by increasing energy expenditure in mice. American Journal of Physiology-Endocrinology and Metabolism, 308(4): E315–E323.

    Article  Google Scholar 

  • Oktay, A. A., Lavie, C. J., Kokkinos, P. F., Parto, P., Pandey, A., and Ventura, H. O., 2017. The interaction of cardiorespiratory fitness with obesity and the obesity paradox in cardiovascular disease. Progress in Vardiovascular Diseases, 60(1): 30–44.

    Article  Google Scholar 

  • Pillitteri, J. L., Shiffman, S., Rohay, J. M., Harkins, A. M., Burton, S. L., and Wadden, T. A., 2008. Use of dietary supplements for weight loss in the United States: Results of a national survey. Obesity, 16(4): 790–796.

    Article  Google Scholar 

  • Schweiger, M., Schreiber, R., Haemmerle, G., Lass, A., Fledelius, C., Jacobsen, P., Tornqvist, H., Zechner, R., and Zimmermann, R., 2006. Adipose triglyceride lipase and hormonesensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism. Journal of Biological Chemistry, 281(52): 40236–40241.

    Article  Google Scholar 

  • Sjögren, P., Sierra-Johnson, J., Gertow, K., Rosell, M., Vessby, B., De Faire, U., Hamsten, A., Hellenius, M. L., and Fisher, R., 2008. Fatty acid desaturases in human adipose tissue: Relationships between gene expression, desaturation indexes and insulin resistance. Diabetologia, 51(2): 328–335.

    Article  Google Scholar 

  • Sullivan, D. R., Kruijswijk, Z., West, C. E., Kohlmeier, M., and Katan, M. B., 1985. Determination of serum triglycerides by an accurate enzymatic method not affected by free glycero. Clinical Chemistry, 31(7): 1227–1228.

    Article  Google Scholar 

  • Swift, D. L., McGee, J. E., Earnest, C. P., Carlisle, E., Nygard, M., and Johannsen, N. M., 2018. The effects of exercise and physical activity on weight loss and maintenance. Progress in Cardiovascular Diseases, 61(2): 206–213.

    Article  Google Scholar 

  • Sylow, L., Kleinert, M., Richter, E. A., and Jensen, T. E., 2017. Exercise-stimulated glucose uptake-regulation and implications for glycaemic control. Nature Reviews Endocrinology, 13(3): 133–148.

    Article  Google Scholar 

  • Takeuchi, Y., Yahagi, N., Izumida, Y., Nishi, M., Kubota, M., Teraoka, Y., Yamamoto, T., Matsuzaka, T., Nakagawa, Y., and Sekiya, M., 2010. Polyunsaturated fatty acids selectively suppress sterol regulatory element-binding protein-1 through proteolytic processing and autoloop regulatory circuit. Journal of Biological Chemistry, 285(15): 11681–11691.

    Article  Google Scholar 

  • Uemura, T., Goto, T., Kang, M. S., Mizoguchi, N., Hirai, S., Lee, J. Y., Nakano, Y., Shono, J., Hoshino, S., and Taketani, K., 2011. Diosgenin, the main aglycon of fenugreek, inhibits LXRα activity in HepG2 cells and decreases plasma and hepatic triglycerides in obese diabetic mice. The Journal of Nutrition, 141(1): 17–23.

    Article  Google Scholar 

  • Wang, T., Xue, C., Zhang, T., and Wang, Y., 2018. The improvements of functional ingredients from marine foods in lipid metabolism. Trends in Food Science & Technology, 81: 74–89.

    Article  Google Scholar 

  • Wang, Y., Wang, J., Yanagita, R. C., Liu, C., Hu, X., Dong, P., Xue, C., and Xue, Y., 2014. Effects of two sulfated triterpene saponins echinoside A and holothurin A on the inhibition of dietary fat absorption and obesity reduction. Bioscience, Biotechnology, and Biochemistry, 78(1): 139–146.

    Article  Google Scholar 

  • Wu, T., Qi, X., Liu, Y., Guo, J., Zhu, R., Chen, W., Zheng, X., and Yu, T., 2013. Dietary supplementation with purified mulberry (Morus australis Poir) anthocyanins suppresses body weight gain in high-fat diet fed C57BL/6 mice. Food Chemistry, 141(1): 482–487.

    Article  Google Scholar 

  • Ye, S. Y., and Liu, J., 2016. Chinese adults’ physical exercise, static behaviors, trends and influencing factors. Journal of Capital University of Physical Education and Sports, 28: 365–369.

    Google Scholar 

  • Zhang, J., Zhao, Y., Xu, C., Hong, Y., Lu, H., Wu, J., and Chen, Y., 2014. Association between serum free fatty acid levels and nonalcoholic fatty liver disease: A cross-sectional study. Scientific Reports, 4: 5832.

    Article  Google Scholar 

  • Zhao, Y. C., Xue, C. H., Zhang, T. T., and Wang, Y. M., 2018. Saponins from sea cucumber and their biological activities. Journal of Agricultural and Food Chemistry, 66(28): 7222–7237.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key R&D Program of China (No. 2018YFD0901103) and the National Natural Science Foundation of China (Nos. 31901688 and 31571771).

Author information

Authors and Affiliations

  1. College of Food Science and Engineering, Ocean University of China, Qingdao, 266003, China

    Rong Li, Jing Meng, Haohao Shi, Chengcheng Wang, Zhaojie Li, Changhu Xue, Yuming Wang & Tiantian Zhang

  2. Laboratory for Marine Drugs and Bioproducts, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Changhu Xue & Yuming Wang

  3. Jining Center for Food and Drug Control, Jining, 272025, China

    Jing Meng

Authors
  1. Rong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jing Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haohao Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chengcheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhaojie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Changhu Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tiantian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yuming Wang or Tiantian Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, R., Meng, J., Shi, H. et al. Dietary Supplementation with Sea Cucumber Saponins and Exercise Can Significantly Suppress Adipose Accumulation in Mice Fed with High-Fat Diet. J. Ocean Univ. China 20, 629–640 (2021). https://doi.org/10.1007/s11802-021-4577-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-021-4577-7

Key words

Search

Navigation