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Food Science and Biotechnology

, Volume 25, Issue 6, pp 1753–1760 | Cite as

Long-chain bases from Cucumaria frondosa inhibit adipogenesis and regulate lipid metabolism in 3T3-L1 adipocytes

  • Yingying Tian
  • Shiwei HuEmail author
  • Hui Xu
  • Jingfeng Wang
  • Changhu Xue
  • Yuming Wang
Article

Abstract

This study aims to investigate anti-adipogenic effects of long-chain bases from Cucumaria frondosa (Cf-LCBs) in vitro. Results showed that Cf-LCBs inhibited adipocyte differentiation and the expressions of CCAAT/enhancer binding proteins (C/EBPs) and peroxisome proliferators-activated receptor γ (PPARγ). Cf-LCBs increased β-catenin mRNA and nuclear translocation and increased its target genes, cyclin D1 and c-myc. Cf-LCBs enhanced fizzled and lipoprotein-receptor-related protein5/6 (LRP5/6) expressions, whereas wingless-type MMTV integration site10b (WNT10b) and glycogen syntheses kinase 3β (GSK3β) remained unchanged. Cf-LCBs also reduced adipogenesis and recovered WNT/β-catenin signaling in the cells suffering from 21H7, a β-catenin inhibitor. In addition, Cf-LCBs decreased triglyceride content and the expressions of lipogenesis genes. Cf-LCBs increased FFA levels and the expressions of lipidolytic factors. Cf-LCBs promoted the phosphorylation of adenosine-monophosphate-activated protein kinase (AMPK) and acetyl-CoA carboxylase. These findings indicate that Cf-LCBs inhibit adipogenesis through activation of WNT/β-catenin signaling and regulate lipid metabolism via activation of AMPK pathway.

Keywords

Cusumaria frondosa long-chain bases adipocyte differentiation lipid metabolism 

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References

  1. 1.
    Kopelman PG. Obesity as a medical problem. Nature 404: 635–643 (2000)Google Scholar
  2. 2.
    Kang SI, Shin HS, Kim SJ. Sinensetin enhances adipogenesis and lipolysis by increasing cyclic adenosine monophosphate levels in 3T3-L1 adipocytes. Biol. Pharm. Bull. 38: 552–558 (2015)CrossRefGoogle Scholar
  3. 3.
    Kowalska K, Olejnik A, Rychlik J, Grajek W. Cranberries (Oxycoccus quadripetalus) inhibit adipogenesis and lipogenesis in 3T3-L1 cells. Food Chem. 148: 246–252 (2014)CrossRefGoogle Scholar
  4. 4.
    Choi K, Ghaddar B, Moya C, Shi H, Sridharan GV, Lee K, Jayaraman A. Analysis of transcription factor network underlying 3T3-L1 adipocyte differentiation. PLoS ONE 9: e100177 (2014)CrossRefGoogle Scholar
  5. 5.
    Lim H, Yeo E, Song E, Chang YH, Han BK, Choi HJ, Hwang J. Bioconversion of Citrus unshiu pell extracts with cytolase suppresses adipogenic activity in 3T3-L1 cells. Nutr. Res. Pract. 9: 599–605 (2015)CrossRefGoogle Scholar
  6. 6.
    Vanella L, Sodhi K, Kim DH, Puri N, Maheshwari M, Hinds TD, Bellner L, Goldstein D, Peterson SJ, Shapiro JI, Abraham NG. Increased heme-oxygenase 1 expression in mesenchymal stem cell-derived adipocytes decreases differentiation and lipid accumulation via upregulation of the canonical Wnt signaling cascade. Stem Cell Res. Ther. 4, 28 (2013)CrossRefGoogle Scholar
  7. 7.
    He H, Chen K, Wang F, Zhao L, Wan X, Wang L, Mo Z. miR-204-5p promotes the adipogenic differentiation of human adipose derived mesenchymal stem cells by modulating DVL3 expression and suppressing Wnt/β-catenin signaling. Int. J. Mol. Med. 35: 1587–1595 (2015)Google Scholar
  8. 8.
    Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A. Adipogenesis and WNT signaling. Trends Endocrin. Met. 20: 16–24 (2009)CrossRefGoogle Scholar
  9. 9.
    Lee H, Bae S, Kim K, Kim W, Chung S, Yoon Y. Beta-Catenin mediates the antiadipogenic effect of baicalin. Biochem. Bioph. Res. Co. 398: 741–746 (2010)CrossRefGoogle Scholar
  10. 10.
    Kowalska K, Olejnik A, Rychlik J, Grajek W. Cranberries (Oxycoccus quadripetalus) inhibit lipid metabolism and modulate leptin and adiponectin secretion in 3T3-L1 adipocytes. Food Chem. 185: 383–388 (2015)CrossRefGoogle Scholar
  11. 11.
    Kim SK, Kong CS. Anti-adipogenic effect of dioxinodehydroeckol via AMPK activation in 3T3-L1 adipocytes. Chem.-Biol. Interact. 186: 24–29 (2010)CrossRefGoogle Scholar
  12. 12.
    Samovski D, Sun J, Pietka T, Gross RW, Eckel RH, Su X, Stahi PD, Abumrad NA. Regulation of AMPK activation by CD36 links fatty acid uptake to β-oxidation. Diabetes 64: 353–359 (2015)CrossRefGoogle Scholar
  13. 13.
    Shimajiri J, Shiota M, Hosokawa M, Miyashita K. Synergistic antioxidant activity of milk sphingomyeline and its sphingoid base with α-tocopherol on fish oil triacylglycerol. J. Agr. Food Chem. 61: 7969–7975 (2013)CrossRefGoogle Scholar
  14. 14.
    Rozema E, Binder M, Bulusu M, Bochkov V, Krupitza G, Kopp B. Effects on inflammatory responses by the sphingoid base 4:8-sphingadienine. Int. J. Mol. Med. 30: 703–707 (2012)Google Scholar
  15. 15.
    Alden KP. Dhondt-Cordelier S, McDonald KL, Reape TJ, Ng CK, McCabe PF, Leaver CJ. Sphingolipid long chain base phosphates can regulate apoptoticlike programmed cell death in plants. Biochem. Bioph. Res. Co. 410: 574–580 (2011)CrossRefGoogle Scholar
  16. 16.
    Wei N, Pan J, Pop-Busui R, Othman A, Alecu I, Hornemann T, Eichler FS. Altered sphingoid base profiles in type 1 compared to type 2 diabetes. Lipids Health Dis. 13, 161 (2014)CrossRefGoogle Scholar
  17. 17.
    Sigruener A, Tarabin V, Paragh G, Liebisch G, Koehler T, Farwick M, Schmitz G. Effects of sphingoid bases on the sphingolipidome in early keratinocyte differentiation. Exp. Dermatol. 22: 677–679 (2013)CrossRefGoogle Scholar
  18. 18.
    Bordbar S, Anwar F, Saari N. High-value components and bioactives from sea cucumbers for functional foods—A review. Mar. Drugs. 9: 1761–1805 (2011)CrossRefGoogle Scholar
  19. 19.
    Hossain Z, Sugawara T, Hirata T. Sphingoid bases from sea cucumber induce apoptosis in human hepatoma HepG2 cells through p-AKT and DR5. Oncol. Rep. 29: 1201–1207 (2013)Google Scholar
  20. 20.
    Gao Z, Zhou X, Hu X, Xue C, Xu J, Wang Y. Effects of sea cucumber cerebroside and its long-chain base on lipid and glucose metabolism in obese mice. Zhejiang Da Xue Xue Bao Yi Xue Ban 41: 60–64 (2012) (in Chinese)Google Scholar
  21. 21.
    Sugawara T, Zaima N, Yamamoto A, Sakai S, Noguchi R, Hirata T. Isolation of sphingoid bases of sea cucumber cerebrosides and their cytotoxicity against human colon cancer cells. Biosci. Biotech. Bioch. 70: 2906–2912 (2006)CrossRefGoogle Scholar
  22. 22.
    Siersbaek R, Nielsen R, Mandrup S. PPARgamma in adipocyte differentiation and metabolism—novel insights from genome-wide studies. FEBS Lett. 584: 3242–3249 (2010)CrossRefGoogle Scholar
  23. 23.
    Kim JH, Park KW, Lee EW, Jang WS, Seo J, Shin S, Hwang KA, Song J. Suppression of PPARγ through MKRN1-mediated ubiquitination and degradation prevents adipocyte differentiation. Cell Death Differ. 21: 594–603 (2014)CrossRefGoogle Scholar
  24. 24.
    Yang J, Croniger CM, Lekstrom-Himes J, Zhang P, Fenyus M, Tenen DG, Darlington GJ, Hanson RW. Metabolic response of mice to a postnatal ablation of CCAAT/enhancer-binding protein alpha. J. Biol. Chem. 280: 38689–38699 (2005)CrossRefGoogle Scholar
  25. 25.
    Yao Y, Zhu Y, Gao Y, Shi Z, Hu Y, Ren G. Suppressive effects of saponin-enriched extracts from quinoa on 3T3-L1 adipocyte differentiation. Food Funct. 6: 3282–3290 (2015)CrossRefGoogle Scholar
  26. 26.
    Madsen MS, Siersbaek R, Boergesen M, Nielsen R, Mandrup S. Peroxisome proliferator-activated receptor γ and C/EBPα synergistically activate key metabolic adipocyte genes by assisted loading. Mol. Cell. Biol. 34: 939–954 (2014)CrossRefGoogle Scholar
  27. 27.
    Chen C, Peng Y, Peng Y, Peng J, Jiang S. m iR-135a-5p i nhibits 3 T3-L1 adipogenesis through activation of canonical Wnt/β-catenin signaling. J. Mol. Endocrinol. 52: 311–320 (2014)CrossRefGoogle Scholar
  28. 28.
    Lee H, Bae S, Yoon Y. Anti-adipogenic effects of 1:25-dihydroxyvitamin D3 are mediated by the maintenance of the wingless-type MMTV integration site/β-catenin pathway. Int. J. Mol. Med. 30: 1219–1224 (2012)Google Scholar
  29. 29.
    Park YK, Park B, Lee S, Choi K, Moon Y, Park H. Hypoxia-inducible factor-2α-dependent hypoxic induction of Wnt10b expression in adipogenic cells. J. Biol. Chem. 288: 26311–26322 (2013)CrossRefGoogle Scholar
  30. 30.
    Xu H, Wang F, Wang J, Xu J, Wang Y, Xue C. The WNT/â-catenin pathway is involved in the anti-adipogenic activity of cerebrosides from the sea cucumber Cucumaria frondosa. Food Funct. 6: 2396–2404 (2015)CrossRefGoogle Scholar
  31. 31.
    Cho YM, Kim DH, Kwak SN, Jeong SW, Kwon OJ. X-box binding protein 1 enhances adipogenic differentiation of 3T3-L1 cells through the downregulation of Wnt10b expression. FEBS Lett. 587: 1644–1649 (2013)CrossRefGoogle Scholar
  32. 32.
    Xu H, Wang J, Zhang X, Li Z, Wang Y, Xue C. Inhibitory effect of fucosylated chondroitin sulfate from the sea cucumber Acaudina molpadioides on adipogenesis is dependent on Wnt/β-catenin pathway. J. Biosci. Bioeng. 119: 85–91 (2015)CrossRefGoogle Scholar
  33. 33.
    Ferrante MC, Amero P, Santoro A, Monnolo A, Simeoli R, Di Guida F, Mattace Raso G, Meli R. Polychlorinated biphenyls (PCB 101: PCB 153 and PCB 180) alter leptin signaling and lipid metabolism in differentiated 3T3-L1 adipocytes. Toxicol. Appl. Pharm. 279: 401–408 (2014)CrossRefGoogle Scholar
  34. 34.
    Chang JJ, Hsu MJ, Huang HP, Chung DJ, Chang YC, Wang CJ. Mulberry anthocyanins inhibit oleic acid induced lipid accumulation by reduction of lipogenesis and promotion of hepatic lipid clearance. J. Agr. Food Chem. 61: 6069–6076 (2013)CrossRefGoogle Scholar
  35. 35.
    Zheng G, Lin L, Zhong S, Zhang Q, Li D. Effects of puerarin on lipid accumulation and metabolism in high-fat diet-fed mice. PLoS ONE 10: e0122925 (2015)CrossRefGoogle Scholar

Copyright information

© The Korean Society of Food Science and Technology and Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Yingying Tian
    • 1
    • 2
  • Shiwei Hu
    • 1
    • 2
    Email author
  • Hui Xu
    • 2
  • Jingfeng Wang
    • 2
  • Changhu Xue
    • 2
  • Yuming Wang
    • 2
  1. 1.Innovation Application InstituteZhejiang Ocean UniversityZhoushan, ZhejiangChina
  2. 2.College of Food Science and EngineeringOcean University of ChinaQingdao, ShandongChina

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