Abstract
A sulfated galactofucan designated as UpG was obtained from the brown algae Undaria pinnatifida by calcium chloride extraction. Chemical analyses showed that UpG is composed of galactose and fucose at a high sulfation level. Low-molecular weight UpGP-0.5 was prepared from UpG through acid hydrolysis for structure characterization. The backbones of UpG are determined to be α-(1,3)-Fuc, α-(1,4)-Gal, α-(1,3)-Gal, and α-(1,6)-Gal by GC-MS, FT-IR, NMR, and LC-MS analyses. Sulfate groups are modified at C2 and/or C4 of fucose and C3 and/or C4 of galactose. UpG could partially lower blood sugar and serum lipid levels in type 2 diabetic mice. Moreover, UpG treatment regulates the abundance of some specific gut microbiota, such as enriching the abundance of Muribaculum and Christensenellaceae, and reducing that of Bilophila, Tannerellaceae, Candidatus Saccharimonas and Anaerotruncus. The findings characterized the detailed structure of a sulfated galactofucan and investigated its potential for the treatment of type 2 diabetes mellitus.
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The data that support the finding of this study are available from the corresponding author.
References
Anastyuk S D, Imbs T I, Shevchenko N M et al. 2012. ESIMS analysis of fucoidan preparations from Costaria costata, extracted from alga at different life-stages. Carbohydrate Polymers, 90(2): 993–1002.
Arata P X, Quintana I, Canelón D J et al. 2015. Chemical structure and anticoagulant activity of highly pyruvylated sulfated galactans from tropical green seaweeds of the order Bryopsidales. Carbohydrate Polymers, 122: 376–386.
Chen P L, Lei S Z, Chen Y Y et al. 2020. Structural characterization of a novel galactoglucan from Fortunella margarita and its molecular structural change following simulated digestion in vitro. Journal of Functional Foods, 71: 104024.
Chen X Y, Ji H Y, Xu X M et al. 2019. Optimization of polysaccharide extraction process from Grifola frondosa and its antioxidant and anti-tumor research. Journal of Food Measurement and Characterization, 13(1): 144–153.
Chizhov A O, Dell A, Morris H R et al. 1999. A study of fucoidan from the brown seaweed Chorda filum. Carbohydrate Research, 320(1–2): 108–119.
Choi J I, Lee S G, Han S J et al. 2014. Effect of gamma irradiation on the structure of fucoidan. Radiation Physics and Chemistry, 100: 54–58.
DeFronzo R A, Ferrannini E, Groop L et al. 2015. Type 2 diabetes mellitus. Nature Reviews Disease Primers, 1(1): 15019.
Deore U V, Mahajan H S. 2021. Isolation and structural characterization of mucilaginous polysaccharides obtained from the seeds of Cassia uniflora for industrial application. Food Chemistry, 351: 129262.
Diamant M, Blaak E E, de Vos W M. 2011. Do nutrient-gutmicrobiota interactions play a role in human obesity, insulin resistance and type 2 diabetes?. Obesity Reviews, 12(4): 272–281.
Dodgson K S, Price R G. 1962. A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochemical Journal, 84(1): 106–110.
Frost F, Kacprowski T, Rühlemann M et al. 2021. Long-term instability of the intestinal microbiome is associated with metabolic liver disease, low microbiota diversity, diabetes mellitus and impaired exocrine pancreatic function. Gut, 70(3): 522–530.
Geng L H, Zhang Q B, Wang J et al. 2018. Glucofucogalactan, a heterogeneous low-sulfated polysaccharide from Saccharina japonica and its bioactivity. International Journal of Biological Macromolecules, 113: 90–97.
Hakomori S I. 1964. A rapid permethylation of glycolipid, and polysaccharide catalyzed by methylsulfinyl carbanion in dimethyl sulfoxide. The Journal of Biochemistry, 55(2): 205–208.
Hemmingson J A, Falshaw R, Furneaux R H et al. 2006. Structure and antiviral activity of the galactofucan sulfates extracted from Undaria pinnatifida (Phaeophyta). Journal of Applied Phycology, 18(2): 185–193.
Jia R B, Wu J, Li Z R et al. 2020. Comparison of physicochemical properties and antidiabetic effects of polysaccharides extracted from three seaweed species. International Journal of Biological Macromolecules, 149: 81–92.
Jiang P R, Zheng W Y, Sun X N et al. 2021. Sulfated polysaccharides from Undaria pinnatifida improved high fat diet-induced metabolic syndrome, gut microbiota dysbiosis and inflammation in BALB/c mice. International Journal of Biological Macromolecules, 167: 1587–1597.
Jin W H, Jiang D, Zhang W J et al. 2020. Interactions of fibroblast growth factors with sulfated galactofucan from Saccharina japonica. International Journal of Biological Macromolecules, 160: 26–34.
Koh H S A, Lu J, Zhou W B. 2019. Structure characterization and antioxidant activity of fucoidan isolated from Undaria pinnatifida grown in New Zealand. Carbohydrate Polymers, 212: 178–185.
Lee J B, Hayashi K, Hashimoto M et al. 2004. Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chemical and Pharmaceutical Bulletin, 52(9): 1091–1094.
Lee J, Lee S, Synytsya A et al. 2018. Low molecular weight mannogalactofucans derived from Undaria pinnatifida induce apoptotic death of human prostate cancer cells in vitro and in vivo. Marine Biotechnology, 20(6): 813–828.
Li L L, Wang Y T, Zhu L M et al. 2020. Inulin with different degrees of polymerization protects against diet-induced endotoxemia and inflammation in association with gut microbiota regulation in mice. Scientific Reports, 10(1): 978.
Li N, Mao W J, Yan M X et al. 2015. Structural characterization and anticoagulant activity of a sulfated polysaccharide from the green alga Codium divaricatum. Carbohydrate Polymers, 121: 175–182.
Lin F D, Yang D D, Huang Y Y et al. 2019. The potential of neoagaro-oligosaccharides as a treatment of type II diabetes in mice. Marine Drugs, 17(10): 541.
Lin F M, Pomeranz Y. 1968. Effect of borate on colorimetric determinations of carbohydrates by the phenol-sulfuric acid method. Analytical Biochemistry, 24(1): 128–131.
Liu X, Xi X Y, Jia A R et al. 2021. A fucoidan from Sargassum fusiforme with novel structure and its regulatory effects on intestinal microbiota in high-fat diet-fed mice. Food Chemistry, 358: 129908.
Marchetti P. 2016. Islet inflammation in type 2 diabetes. Diabetologia, 59(4): 668–672.
Nagasawa K, Inoue Y, Kamata T. 1977. Solvolytic desulfation of glycosaminoglycuronan sulfates with dimethyl sulfoxide containing water or methanol. Carbohydrate Research, 58(1): 47–55.
Natividad J M, Lamas B, Pham H P et al. 2018. Bilophila wadsworthia aggravates high fat diet induced metabolic dysfunctions in mice. Nature Communications, 9(1): 2802.
Raguraman V, L S A, J J et al. 2019. Sulfated polysaccharide from Sargassum tenerrimum attenuates oxidative stress induced reactive oxygen species production in in vitro and in zebrafish model. Carbohydrate Polymers, 203: 441–449.
Song Y J, Shen H T, Liu T T et al. 2021. Effects of three different mannans on obesity and gut microbiota in high-fat diet-fed C57BL/6J mice. Food & Function, 12(10): 4606–4620.
Sun W L, Zhang B W, Yu X X et al. 2018a. Oroxin A from Oroxylum indicum prevents the progression from prediabetes to diabetes in streptozotocin and high-fat diet induced mice. Phytomedicine, 38: 24–34.
Sun Y H, Chen X L, Liu S et al. 2018b. Preparation of low molecular weight Sargassum fusiforme polysaccharide and its anticoagulant activity. Journal of Oceanology and Limnology, 36(3): 882–891.
Usoltseva R V, Anastyuk S D, Surits V V et al. 2019. Comparison of structure and in vitro anticancer activity of native and modified fucoidans from Sargassum feldmannii and S. duplicatum. International Journal of Biological Macromolecules, 124: 220–228.
Vishchuk O S, Ermakova S P, Zvyagintseva T N. 2013. The fucoidans from brown algae of Far-Eastern seas: antitumor activity and structure-function relationship. Food Chemistry, 141(2): 1211–1217.
Wang H Y, Guo L X, Hu W H et al. 2019. Polysaccharide from tuberous roots of Ophiopogon japonicus regulates gut microbiota and its metabolites during alleviation of high-fat diet-induced type-2 diabetes in mice. Journal of Functional Foods, 63: 103593.
Wang J J, Zhu G N, Sun C et al. 2020. TAK-242 ameliorates DSS-induced colitis by regulating the gut microbiota and the JAK2/STAT3 signaling pathway. Microbial Cell Factories, 19(1): 158.
Wang J, Zhang Q B, Zhang Z S et al. 2010. Structural studies on a novel fucogalactan sulfate extracted from the brown seaweed Laminaria japonica. International Journal of Biological Macromolecules, 47(2): 126–131.
Wang L, Park Y J, Jeon Y J et al. 2018. Bioactivities of the edible brown seaweed, Undaria pinnatifida: a review. Aquaculture, 495: 873–880.
Wei B, Zhong Q W, Ke S Z et al. 2020. Sargassum fusiforme polysaccharides prevent high-fat diet-induced early fasting hypoglycemia and regulate the gut microbiota composition. Marine Drugs, 18(9): 444.
Wei X Q, Cai L Q, Liu H L et al. 2019. Chain conformation and biological activities of hyperbranched fucoidan derived from brown algae and its desulfated derivative. Carbohydrate Polymers, 208: 86–96.
Yang Y J, Hu T, Li J J et al. 2021. Structural characterization and effect on leukopenia of fucoidan from Durvillaea antarctica. Carbohydrate Polymers, 256: 117529.
Zhang J J, Zhang Q B, Wang J et al. 2009. Analysis of the monosaccharide composition of fucoidan by precolumn derivation HPLC. Chinese Journal of Oceanology and Limnology, 27(3): 578–582.
Zhao Y, Feng Y Y, Jing X et al. 2021. Structural characterization of an alkali-soluble polysaccharide from Angelica sinensis and its antitumor activity in vivo. Chemistry & Biodiversity, 18(6): e2100089.
Zhong Q W, Wei B, Wang S J et al. 2019. The antioxidant activity of polysaccharides derived from marine organisms: an overview. Marine Drugs, 17(12): 674.
Zhong Q W, Zhou T S, Qiu W H et al. 2021. Characterization and hypoglycemic effects of sulfated polysaccharides derived from brown seaweed Undaria pinnatifida. Food Chemistry, 341: 128148.
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Songze KE and Bo ZHANG analyzed the data and drafted the manuscript. Yanlei YU and Sijia WANG helped with the biological experiments. Weihua JIN and Huawei ZHANG provided valuable intellectual input. Jianwei CHEN and Jian WU provided polysaccharide sample. Hong WANG and Bin WEI designed the experiment and revised the manuscript.
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Supported by the National Key Research and Development Program (Nos. 2018YFC0311003, 2017YFE0103100), the National Natural Science Foundation of China (Nos. 81903534, 81773628, 81741165), and the High-Level Talent Special Support Plan of Zhejiang Province (No. 2019R52009)
Supporting Information
The 2D spectra 1H-1H COSY, 1H-1H TOCSY and HMBC of UpGP-0.5 (Supplementary Fig. S1). Negative-ion mode ESI- MS spectra of the oligosaccharide fractions U1, U2, U3, U4, U5 and U6 (Supplementary Fig.S2).
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Ke, S., Zhang, B., Yu, Y. et al. Structural characterization of sulfated galactofucan from Undaria pinnatifida and its effect on type 2 diabetic mice. J. Ocean. Limnol. 41, 300–313 (2023). https://doi.org/10.1007/s00343-021-1307-3
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DOI: https://doi.org/10.1007/s00343-021-1307-3