Inhibitory effect of fucosylated chondroitin sulfate from the sea cucumber Acaudina molpadioides on adipogenesis is dependent on Wnt/β-catenin pathway

Journal of Bioscience and Bioengineering

Volumn 119, Issue 1, 2015, Pages 85-91

  Xu, Hui ^a   Wang, Jingfeng ^a   Zhang, Xin ^a   Li, Zhaojie ^a   Wang, Yuming ^a   Xue, Changhu ^a  

^a OCEAN UNIVERSITY OF CHINA   (China)

Author keywords

Adipogenesis; CCAAT enhancer binding protein (C EBP ); Fucosylated chondroitin sulfate; Peroxisome proliferator activated receptor (PPAR ); Sterol regulatory element binding protein (SREBP 1c); Wnt catenin pathway

Indexed keywords

CYTOLOGY; PROTEINS; SULFUR COMPOUNDS;

ADIPOGENESIS; CCAAT/ENHANCER-BINDING PROTEINS; CHONDROITIN SULFATES; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; STEROL REGULATORY ELEMENT-BINDING PROTEINS;

POLYMERASE CHAIN REACTION;

BETA CATENIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; CHONDROITIN SULFATE; FRIZZLED PROTEIN; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; WNT PROTEIN; WNT10B PROTEIN; FAS LIGAND; FUCOSYLATED CHONDROITIN SULFATE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DEVELOPMENTAL STAGE; DOWN REGULATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEA CUCUMBER; WESTERN BLOTTING; 3T3 CELL LINE; ANIMAL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; WNT SIGNALING PATHWAY;

HOLOTHUROIDEA; MUS;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; BETA CATENIN; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CELL DIFFERENTIATION; CHONDROITIN SULFATES; DOWN-REGULATION; FAS LIGAND PROTEIN; MALE; MICE; MICE, INBRED C57BL; PPAR GAMMA; RNA, MESSENGER; SEA CUCUMBERS; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84927178737     PISSN: 13891723     EISSN: 13474421     Source Type: Journal    
DOI: 10.1016/j.jbiosc.2014.05.026     Document Type: Article

References (45)

1. Shimada T., Nagai E., Harasawa Y., Watanabe M., Neigishi K., Akase T., Sai Y., Mivamoto K.-I., Aburada M. Salacia reticulate inhibits differentiation of 3T3-L1 adipocytes. J.Ethnopharmacol. 2011, 136:67-74.
2. Tsuda T. Regulation of adipocyte function by anthocyanins; possibility of preventing the metabolic syndrome. J.Agric. Food Chem. 2008, 56:642-646.
3. Lee I., Kim J., Ryoo I., Kim Y., Choo S., Yoo I., Min B., Na M., Hattori M., Bae K. Lanostane triterpenes from Ganoderma lucidum suppress the adipogenesis in 3T3-L1 cells through down-regulation of SREBP-1c. Bioorg. Med. Chem. Lett. 2010, 20:5577-5581.
4. Lee S., Yang W.K., Song J.H., Ra Y.M., Jeong J.-H., Choe W., Kang I., Kim S.-S., Ha J. Anti-obesity effects of 3-hydroxychromone derivative, a novel small-molecule inhibitor of glycogen synthase kinase-3. Biochem. Pharmacol. 2013, 85:965-976.
5. Siersbaek R., Nielsen R., Mandrup S. Transcriptional networks and chromatin remodeling controlling adipogenesis. Trends Endocrinol. Metab. 2012, 23:56-64.
6. Shimba S., Wada T., Hara S., Tezuka M. EPAS1 promotes adipose differentiation in 3T3-L1 cells. J.Biol. Chem. 2004, 279:40946-40953.
7. Ahn J., Lee H., Kim S., Ha T. Curcumin-induced suppression of adipogenic differentiation is accompanied by activation of Wnt/β-catenin signaling. Am. J. Physiol. Cell Physiol. 2010, 298:C1510-C1516.
8. Gustafson B., Smith U. Activation of canonical wingless-type MMTV integration site family (Wnt) signaling in mature adipocyte increases β-catenin levels and leads to cell dedifferentiation and insulin resistance. J.Biol. Chem. 2010, 285:14031-14041.
9. Okamura M., Kudo H., Wakabayashi K.-I., Tanaka T., Nonaka A., Uchida A., Tsutsumi S., Sakakibara I., Naito M., Osborne T.F., other 6 authors COUP-TFll acts downstream of Wnt/β-catenin signal to silence PPARγ gene expression and repress adipogenesis. Proc. Natl. Acad. Sci. USA 2009, 106:5819-5824.
10. Wang Y., Su W., Zhang C., Xue C., Chang Y., Wu X., Tang Q., Wang J. Protective effect of sea cucumber (Acaudina molpadioides) fucoidan against ethanol-induced gastric damage. Food Chem. 2012, 133:1414-1419.
11. Wu M., Huang R., Wen D., Gao N., He J., Li Z., Zhao J. Structure and effect of sulfated fucose branches on anticoagulant activity of the fucosylated chondroitin sulfate from sea cucumber Thelenata ananas. Carbohydr. Polym. 2012, 87:862-868.
12. Hu S., Chang Y., Wang J., Xue C., Shi D., Xu H., Wang Y. Fucosylated chondroitin sulfate from Acaudina molpadioides improves hyperglycemia via activation of PKB/GLUT4 signaling in skeletal muscle of insulin resistant mice. Food Funct. 2013, 4:1639-1646.
13. Chen S., Xue C., Yin L., Tang Q., Yu G., Chai W. Comparison of structures and anticoagulant activities of fucosylated chondroitin sulfates from different sea cucumbers. Carbohydr. Polym. 2011, 83:688-696.
14. Chen S., Hu Y., Ye X., Li G., Yu G., Xue C., Chai W. Sequence determination and anticoagulation and antithrombotic activity of a novel sulfated fucan isolated from the sea cucumber Isostichopus badionotus. Biochim. Biophys. Acta 2012, 1820:989-1000.
15. Chen S., Li G., Wu N., Guo X., Liao N., Ye X., Liu D., Xue C., Chai W. Sulfation pattern of the fucose branch is important for the anticoagulant and antithrombotic activities of fucosylated chondroitin sulfates. Biochim. Biophys. Acta 2013, 1830:3054-3066.
16. Hu S., Chang Y., Wang J., Xue C., Li Z., Wang Y. Fucosylated chondroitin sulfate from sea cucumber in combination with rosiglitazone improved glucose metabolism in the liver of the insulin-resistance mice. Biosci. Biotechnol. Biochem. 2013, 77:2263-2268.
17. Hsu H.-F., Tsou T.-C., Chao H.-R., Shy C.-G., Kuo Y.-T., Tsai F.-Y., Yeh S.-C., Ko Y.-C. Effects of arecoline on adipogenesis, lipolysis, and glucose uptake of adipocytes-A possible role of betel-quid chewing in metabolic syndrome. Toxicol. Appl. Pharm. 2010, 245:370-377.
18. Prestwich T.C., MacDougald O.A. Wnt/β-catenin signaling in adipogenesis and metabolism. Curr. Opin. Cell Biol. 2007, 19:612-617.
19. White U.A., Stephens J.M. Transcriptional factors that promote formation of white adipose tissue. Mol. Cell. Endocrinol. 2010, 318:10-14.
20. O'Neill H.M., Holloway G.P., Steinberg G.R. AMPK regulation of fatty acid metabolism and mitochondrial biogenesis: implication for obesity. Mol. Cell. Endocrinol. 2013, 366:135-151.
21. Farmer S.R. Transcriptional control of adipocyte formation. Cell Metab. 2006, 4:263-273.
22. Kim C.K., Kim M., Oh S.D., Lee S.-M., Sun B., Choi G.S., Kim S.-K., Bae H., Kang C., Min B.-I. Effects of Atractylodes macrocephala Koidzumi rhizome on 3T3-L1 adipogenesis and animal model of obesity. J.Ethnopharmacol. 2011, 137:396-402.
23. Kim K.-J., Lee O.-H., Lee B.-Y. Fucoidan, a sulfated polysaccharide, inhibits adipogenesis through the mitogen-activated protein kinase pathway in 3T3-L1 preadipocytes. Life Sci. 2010, 86:791-797.
24. Kim M.-J., Chang U.-J., Lee J.-S. Inhibitory effects of fucoidan in 3T3-L1 adipocyte differentiation. Mar. Biotechnol. 2009, 11:557-562.
25. Lee H., Bae S., Kim Y.S., Yoon Y. Wnt/β-catenin pathway mediates the anti-adipogenic effect of platycodin D, a natural compound found in Platycodon grandiflorum. Life Sci. 2011, 89:388-394.
26. Christodoulides C., Lagathu C., Sethi J.K., Vidal-Puig A. Adipogenesis and WNT signaling. Trends Endocrinol. Metab. 2008, 20:16-24.
27. Lee, H., Bae, S., and Yoon, Y.: The anti-adipogenic effects of (-) epigallacatechin gallate are dependent on the Wnt/β-catenin pathway, 24, 1232-1240 (2013).
28. Longo K.A., Wright W.S., Kang S., Gerin I., Chiang S.-H., Lucas P.C., Opp M.R., MacDougald O.A. Wnt10b inhibits development of white and brown adipose tissues. J.Biol. Chem. 2004, 279:35503-35509.
29. Gustafson B., Smith U. Cytokines promote Wnt signaling and inflammation and impair the normal differentiation and lipid accumulation in 3T3-L1 preadipocytes. J.Biol. Chem. 2006, 281:9507-9516.
30. Longo K.A., Kennell J.A., Ochocinska M.J., Ross S.E., Wright W.S., MacDougald O.A. J.Biol. Chem. 2002, 277:38239-38244.
31. Bennett C.N., Ross S.E., Longo K.A., Bajnok L., Hemati N., Johnson K.W., Harrison S.D., MacDougald O.A. Regulation of Wnt signaling during adipogenesis. J.Biol. Chem. 2002, 277:30998-31004.
32. Lee H., Bae S., Yoon Y. The Wnt/β-catenin pathway mediates the anti-adipogenic mechanism of SH21B, a traditional herbal medicine for the treatment of obesity. J.Ethnopharmacol. 2011, 133:788-795.
33. Lee H., Bae S., Kim K., Kim W., Chung S.-I., Yoon Y. β-Catenin mediates the anti-adipogenic effect of baicalin. Biochem. Biophys. Res. Commun. 2010, 398:741-746.
34. Kennell J.A., MacDougald O.A. Wnt signaling inhibits adipogenesis through β-catenin-dependent and -independent mechanisms. J.Biol. Chem. 2005, 280:24004-24010.
35. Tilgner K., Wojciechowicz K., Jahoda C., Hutchison C., Markiewicz E. Dynamic complexes of A-type lamins and emerin influence adipogenic capacity of the cell via nucleocytoplasmic distribution of β-catenin. J.Cell Sci. 2008, 122:401-413.
36. Lowe C.E., O'Rahilly S., Rochford J.J. Adipogenesis at a glance. J.Cell Sci. 2011, 124:2681-2686.
37. Mandrup S., Lane M.D. Regulating adipogenesis. J.Biol. Chem. 1997, 272:5367-5370.
38. Rosen E.D., Walkey C.J., Puigserver P., Spiegelman B.M. Transcriptional regulation of adipogenesis. Genes Dev. 2013, 14:1293-1307.
39. Christodoulides C., Vidal-Puig A. PPARs and adipocyte function. Mol. Cell. Endocrinol. 2010, 318:61-68.
40. Jeon B.-N., Kim Y.-S., Choi W.-I., Koh D.-I., Kim M.-K., Yoon J.-H., Kim M.-Y., Hur B., Paik P.D.-H., Hur M.-W. Kr-pok increases FASN expression by modulating the DNA binding of SREBP-1c and Sp1 at the proximal promoter. J.Lipid Res. 2012, 53:755-766.
41. Lauressergues E., Martin F., Helleboid A., Bouchaert E., Cussac D., Bordet R., Hum D., Luc G., Majd Z., Staels B., Duriez P. Overweight induced by chronic risperidone exposure is correlated with overexpression of the SREBP-1c and FAS genes in mouse liver. Naunyn-Schmied. Arch. Pharmacol. 2011, 383:423-436.
42. Kim S., Jin Y., Choi Y., Park T. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulating of adipogenic and inflammatory processes in mice. Biochem. Pharmacol. 2011, 81:1343-1351.
43. Sim J.-S., Jun G., Toida T., Cho S.Y., Choi D.W. Quantitative analysis of chondroitin sulfate in raw materials, ophthalmic solutions, soft capsules and liquid preparations. J.Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2005, 818:133-139.
44. Cho S.Y., Sim J.-S., Jeong C.S., Chang S.Y., Choi D.W., Toida T., Kim Y.S. Effects of low molecular weight chondroitin sulfate in type II collagen-induced arthritis in DBA/1J mice. Biol. Pharm. Bull. 2004, 27:47-51.
45. Jin M., Satsu H., Yamada K., Hisada N., Totsuka M., Shimizu M. Permeation of disaccharides derived from chondroitin sulfate through human intestinal Caco-2 cell monolayers via the paracellular pathway. Biosci. Biotechnol. Biochem. 2010, 74:1243-1249.