Research Progress on Immune Regulation Activities of Marine Sulfate Polysaccharides

CHEN Qiuyu; ZHAO Ran; MENG Meishan; DOU Xinyu; CHEN Biyi; ZHAO Qiancheng; LI Ying

doi:10.13386/j.issn1002-0306.2024020170

Volume 46 Issue 1

Dec. 2024

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Science and Technology of Food Industry > 2025 > 46(1): 413-423. > DOI: 10.13386/j.issn1002-0306.2024020170

CHEN Qiuyu, ZHAO Ran, MENG Meishan, et al. Research Progress on Immune Regulation Activities of Marine Sulfate Polysaccharides[J]. Science and Technology of Food Industry, 2025, 46(1): 413−423. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2024020170.

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Research Progress on Immune Regulation Activities of Marine Sulfate Polysaccharides

1.
College of Food Science and Engineering, Dalian Ocean University, Dalian 116023, China
2.
Liaoning Provincial Marine Healthy Food Engineering Research Centre, Dalian 116023, China

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Received Date: February 20, 2024
Available Online: November 02, 2024

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Abstract

Abstract

With changes in modern lifestyles, weakened immunity becomes a health problem for an increasing number of people. The development of natural active products with immunomodulatory activity becomes a popular research topic. Marine sulfated polysaccharides are natural active products that are rich in sulfate groups and are extracted and isolated from marine organisms. They have a unique structure and multiple biological activities and have shown great potential with regard to having immune regulatory activity. To better understand the effects of marine sulfated polysaccharides on immune regulatory activity and the associated underlying mechanisms, this article was designed to analyse and summarize the current research literature on marine sulfated polysaccharides. The types of marine sulfated polysaccharides are summarized based on their structure and source, with a focus on functions involving regulating macrophages, natural killer cells, T/B lymphocytes, complement systems, and gut microbiota. The immune regulatory activity of marine sulfated polysaccharides and the underlying mechanisms are summarized. This article provides a theoretical basis for subsequent research on the immunomodulatory activity and structure-activity relationships of marine sulfated polysaccharides and provides novel ideas for the development of new marine sulfated polysaccharide immunoenhancers. In the future, functional foods or special medical foods based on marine sulfated polysaccharides designed to treat immune deficiency, tumours, and autoimmune diseases may be developed, and these foods will play a positive role in promoting the development of the food industry and human health.
- marine sulfate polysaccharide,
- immune regulation,
- mechanism,
- gut microbiota

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References

[1]	李俊慧, 李珊, 胡亚芹, 等. 食源性海洋硫酸多糖的神经保护构效机理研究进展[J]. 中国食品学报,2017,17(4):155−164. [LI Junhui, LI Shan, HU Yaqin, et al. Research progress on the neuroprotective structure-activity mechanism of foodborne marine sulfate polysaccharides[J]. Journal of Chinese Institute of Food Science and Technology,2017,17(4):155−164.] LI Junhui, LI Shan, HU Yaqin, et al. Research progress on the neuroprotective structure-activity mechanism of foodborne marine sulfate polysaccharides[J]. Journal of Chinese Institute of Food Science and Technology, 2017, 17（4）: 155−164.
[2]	LI Y, QIN J, CHENG Y, et al. Marine sulfated polysaccharides:Preventive and therapeutic effects on metabolic syndrome:A review[J]. Marine Drugs,2021,19(11):608. doi: 10.3390/md19110608
[3]	MUTHUKUMAR J, CHIDAMBARAM R, SUKUMARAN S. Sulfated polysaccharides and its commercial applications in food industries—A review[J]. Journal of Food Science Technology,2021,58(7):2453−2466. doi: 10.1007/s13197-020-04837-0
[4]	FERREIRA S S, PASSOS C P, MADUREIRA P, et al. Structure-function relationships of immunostimulatory polysaccharides:A review[J]. Carbohydrate Polymers,2015,132:378−396. doi: 10.1016/j.carbpol.2015.05.079
[5]	谷福蝶, 周钰, 陈慧莹, 等. “蓝色食物”来源多糖的免疫调节活性研究进展[J]. 食品科学,2023,44(13):272−280. [GU Fudie, ZHOU Yu, CHEN Huiying, et al. Research progress on the immunomodulatory activity of polysaccharides derived from "blue food"[J]. Food Science,2023,44(13):272−280.] doi: 10.7506/spkx1002-6630-20220730-343 GU Fudie, ZHOU Yu, CHEN Huiying, et al. Research progress on the immunomodulatory activity of polysaccharides derived from "blue food"[J]. Food Science, 2023, 44（13）: 272−280. doi: 10.7506/spkx1002-6630-20220730-343
[6]	HUANG L, SHEN M, MORRIS G A, et al. Sulfated polysaccharides:Immunomodulation and signaling mechanisms[J]. Trends in Food Science & Technology,2019,92:1−11.
[7]	JIANG J L, ZHANG W Z, NI W X, et al. Insight on structure-property relationships of carrageenan from marine red algal:A review[J]. Carbohydrate Polymers,2021,257:117642. doi: 10.1016/j.carbpol.2021.117642
[8]	YU L, XUE C, CHANG Y, et al. Structure and rheological characteristics of fucoidan from sea cucumber Apostichopus japonicus[J]. Food Chemistry,2015,180:71−76. doi: 10.1016/j.foodchem.2015.02.034
[9]	ZHU Z, DONG X, YAN C, et al. Structural features and digestive behavior of fucosylated chondroitin sulfate from sea cucumbers Stichopus japonicus[J]. Journal of Agricultural Food Chemistry,2019,67(37):10534−10542. doi: 10.1021/acs.jafc.9b04996
[10]	KHOTIMCHENKO M, TIASTO V, KALITNIK A, et al. Antitumor potential of carrageenans from marine red algae[J]. Carbohydrate Polymers,2020,246:116568. doi: 10.1016/j.carbpol.2020.116568
[11]	CAO S, YANG Y, LIU S, et al. Immunomodulatory activity in vitro and in vivo of a sulfated polysaccharide with novel structure from the green alga ulva Conglobata kjellman[J]. Marine Drugs,2022,20(7):447. doi: 10.3390/md20070447
[12]	WANG T, ZHANG S, REN S, et al. Structural characterization and proliferation activity of chondroitin sulfate from the sturgeon, Acipenser schrenckii[J]. International Journal of Biological Macromolecules,2020,164:3005−3011. doi: 10.1016/j.ijbiomac.2020.08.110
[13]	SHANG Q, LI Q, ZHANG M, et al. Dietary keratan sulfate from shark cartilage modulates gut microbiota and increases the abundance of Lactobacillus spp[J]. Marine Drugs,2016,14(12):224. doi: 10.3390/md14120224
[14]	王莹莹, 张振坤, 李亚, 等. 岩藻多糖在肿瘤治疗中的作用[J]. 郑州大学学报(医学版),2021,56(1):47−52. [WANG Yingying, ZHANG Zhenkun, LI Ya, et al. The role of fucoidan in tumor treatment[J]. Journal of Zhengzhou University (Medical Edition),2021,56(1):47−52.] WANG Yingying, ZHANG Zhenkun, LI Ya, et al. The role of fucoidan in tumor treatment[J]. Journal of Zhengzhou University （Medical Edition）, 2021, 56（1）: 47−52.
[15]	SENTHILKUMAR K, MANIVASAGAN P, VENKATESAN J, et al. Brown seaweed fucoidan:Biological activity and apoptosis, growth signaling mechanism in cancer[J]. International Journal of Biological Macromolecules,2013,60:366−374. doi: 10.1016/j.ijbiomac.2013.06.030
[16]	YUGUCHI Y, TRAN V T T, BUI L M, et al. Primary structure, conformation in aqueous solution, and intestinal immunomodulating activity of fucoidan from two brown seaweed species Sargassum crassifolium and Padina australis[J]. Carbohydrate Polymers,2016,147:69−78. doi: 10.1016/j.carbpol.2016.03.101
[17]	安子哲, 张朝辉, 刘梦阳, 等. 海参硫酸多糖化学组成与结构的研究进展[J]. 食品科学,2022,43(7):289−297. [AN Zizhe, ZHANG Chaohui, LIU Mengyang, et al. Research progress on the chemical composition and structure of sulfated polysaccharides from sea cucumber[J]. Food Science,2022,43(7):289−297.] doi: 10.7506/spkx1002-6630-20210315-189 AN Zizhe, ZHANG Chaohui, LIU Mengyang, et al. Research progress on the chemical composition and structure of sulfated polysaccharides from sea cucumber[J]. Food Science, 2022, 43（7）: 289−297. doi: 10.7506/spkx1002-6630-20210315-189
[18]	KARIYA Y, MULLOY B, IMAI K, et al. Isolation and partial characterization of fucan sulfates from the body wall of sea cucumber Stichopus japonicus and their ability to inhibit osteoclastogenesis[J]. Carbohydrate Research,2004,339(7):1339−1346. doi: 10.1016/j.carres.2004.02.025
[19]	YANG W, CAI Y, YIN R, et al. Structural analysis and anticoagulant activities of two sulfated polysaccharides from the sea cucumber Holothuria coluber[J]. International Journal of Biological Macromolecules,2018,115:1055−1062. doi: 10.1016/j.ijbiomac.2018.04.175
[20]	徐元庆, 王哲奇, 张静, 等. 岩藻多糖的抗氧化功能研究进展[J]. 天然产物研究与开发,2020,32(10):1782−1793. [XU Yuanqing, WANG Zheqi, ZHANG Jing, et al. Research progress on the antioxidant function of fucoidan[J]. Research and Development of Natural Products,2020,32(10):1782−1793.] XU Yuanqing, WANG Zheqi, ZHANG Jing, et al. Research progress on the antioxidant function of fucoidan[J]. Research and Development of Natural Products, 2020, 32（10）: 1782−1793.
[21]	BARBOSA A I, COUTINHO A J, COSTA LIMA S A, et al. Marine polysaccharides in pharmaceutical applications:Fucoidan and chitosan as key players in the drug delivery match field[J]. Marine Drugs,2019,17(12):654. doi: 10.3390/md17120654
[22]	PRADHAN B, KI J S. Biological activity of algal derived carrageenan:A comprehensive review in light of human health and disease[J]. International Journal of Biological Macromolecules,2023,238:124085. doi: 10.1016/j.ijbiomac.2023.124085
[23]	沈伟. 低分子量κ-卡拉胶烷氧基化衍生物合成及生物活性的研究[D]. 汕头:汕头大学, 2008. [SHEN Wei. Low molecular weight κ- Study on the synthesis and biological activity of alkoxylated derivatives of carrageenan[D]. Shantou:Shantou University, 2008.] SHEN Wei. Low molecular weight κ- Study on the synthesis and biological activity of alkoxylated derivatives of carrageenan[D]. Shantou: Shantou University, 2008.
[24]	田秀芳. 低分子量κ-卡拉胶O-琥珀酰基化衍生物的合成、表征及生物活性的研究[D]. 汕头:汕头大学, 2006. [TIAN Xiufang. Low molecular weight κ- Synthesis, characterization, and biological activity of O-succinylated derivatives of carrageenan[D]. Shantou:Shantou University, 2006.] TIAN Xiufang. Low molecular weight κ- Synthesis, characterization, and biological activity of O-succinylated derivatives of carrageenan[D]. Shantou: Shantou University, 2006.
[25]	CHEN H, WU D, MA W, et al. Strong fish gelatin hydrogels enhanced by carrageenan and potassium sulfate[J]. Food Hydrocolloids,2021,119:106841. doi: 10.1016/j.foodhyd.2021.106841
[26]	SINTHUSAMRAN S, BENJAKUL S, SWEDLUND P J, et al. Physical and rheological properties of fish gelatin gel as influenced by κ-carrageenan[J]. Food Bioscience,2017,20:88−95. doi: 10.1016/j.fbio.2017.09.001
[27]	高鑫, 山珊, 曾德永, 等. 石莼属绿藻多糖的生物活性研究进展[J]. 食品工业科技, 2021, 42(2):364−369. [GAO Xin, SHAN Shan, ZENG Deyong, et al. Research progress on the biological activity of polysaccharides from Ulva genus green algae[J]. Food Industry Technology 2021, 42 (2):364−369.] GAO Xin, SHAN Shan, ZENG Deyong, et al. Research progress on the biological activity of polysaccharides from Ulva genus green algae[J]. Food Industry Technology 2021, 42 （2）: 364−369.
[28]	TZIVELEKA L A, IOANNOU E, ROUSSIS V. Ulvan, a bioactive marine sulphated polysaccharide as a key constituent of hybrid biomaterials:A review[J]. Carbohydrate Polymers,2019,218:355−370. doi: 10.1016/j.carbpol.2019.04.074
[29]	MOU J, LI Q, QI X, et al. Structural comparison, antioxidant and anti-inflammatory properties of fucosylated chondroitin sulfate of three edible sea cucumbers[J]. Carbohydrate Polymers,2018,185:41−47. doi: 10.1016/j.carbpol.2018.01.017
[30]	LI Q, HU F, ZHU B, et al. Insights into ulvan lyase:Review of source, biochemical characteristics, structure and catalytic mechanism[J]. Critical Reviews in Biotechnology,2020,40(3):432−441. doi: 10.1080/07388551.2020.1723486
[31]	WANG H, CAO Z, YAO L, et al. Insights into the edible and biodegradable ulvan-based films and coatings for food packaging[J]. Foods,2023,12(8):1622. doi: 10.3390/foods12081622
[32]	王宏玲, 罗盛, 杨劲松. 硫酸软骨素二糖重复片段的合成[J]. 华西药学杂志,2022,37(1):15−18. [WANG Hongling, LUO Sheng, YANG Jinsong. Synthesis of chondroitin sulfate disaccharide repeat fragments[J]. Huaxi Pharmaceutical Journal,2022,37(1):15−18.] WANG Hongling, LUO Sheng, YANG Jinsong. Synthesis of chondroitin sulfate disaccharide repeat fragments[J]. Huaxi Pharmaceutical Journal, 2022, 37（1）: 15−18.
[33]	YANG J, SHEN M, WEN H, et al. Recent advance in delivery system and tissue engineering applications of chondroitin sulfate[J]. Carbohydrate Polymers,2020,230:115650. doi: 10.1016/j.carbpol.2019.115650
[34]	左格格, 钟赛意, 陈菁, 等. 罗非鱼加工副产物不同部位硫酸软骨素的制备、理化性质及结构表征[J]. 食品科学,2022,43(24):67−73. [ZUO Gege, ZHONG Saiyi, CHEN Jing, et al. Preparation, physicochemical properties, and structural characterization of chondroitin sulfate from different parts of tilapia processing by-products[J]. Food Science,2022,43(24):67−73.] doi: 10.7506/spkx1002-6630-20211013-119 ZUO Gege, ZHONG Saiyi, CHEN Jing, et al. Preparation, physicochemical properties, and structural characterization of chondroitin sulfate from different parts of tilapia processing by-products[J]. Food Science, 2022, 43（24）: 67−73. doi: 10.7506/spkx1002-6630-20211013-119
[35]	REGINSTER J Y, VERONESE N. Highly purified chondroitin sulfate:A literature review on clinical efficacy and pharmacoeconomic aspects in osteoarthritis treatment[J]. Aging Clinical and Experimental Research,2021,33(1):37−47. doi: 10.1007/s40520-020-01643-8
[36]	高洁, 赵玲, 马丽曼, 等. 鱼源硫酸软骨素的研究进展[J]. 食品安全质量检测学报,2020,11(22):8166−8172. [GAO Jie, ZHAO Ling, MA Liman, et al. Research progress on fish derived chondroitin sulfate[J]. Journal of Food Safety and Quality Testing,2020,11(22):8166−8172.] GAO Jie, ZHAO Ling, MA Liman, et al. Research progress on fish derived chondroitin sulfate[J]. Journal of Food Safety and Quality Testing, 2020, 11（22）: 8166−8172.
[37]	白雪, 高昕, 赵雪, 等. 鲟鱼软骨硫酸软骨素的制备及结构分析[J]. 中国海洋药物,2022,41(2):28−36. [BAI Xue, GAO Xin, ZHAO Xue, et al. Preparation and structural analysis of chondroitin sulfate from sturgeon cartilage[J]. China Marine Medicine,2022,41(2):28−36.] BAI Xue, GAO Xin, ZHAO Xue, et al. Preparation and structural analysis of chondroitin sulfate from sturgeon cartilage[J]. China Marine Medicine, 2022, 41（2）: 28−36.
[38]	GONG P X, LI Q Y, WU Y C, et al. Structural elucidation and antidiabetic activity of fucosylated chondroitin sulfate from sea cucumber Stichopus japonicas[J]. Carbohydrate Polymers,2021,262:117969. doi: 10.1016/j.carbpol.2021.117969
[39]	MOU J, LI Q, SHI W, et al. Chain conformation, physicochemical properties of fucosylated chondroitin sulfate from sea cucumber Stichopus chloronotus and its in vitro fermentation by human gut microbiota[J]. Carbohydrate Polymers,2020,228:115359. doi: 10.1016/j.carbpol.2019.115359
[40]	USTYUZHANINA N E, BILAN M I, DMITRENOK A S, et al. Fucosylated chondroitin sulfates from the sea cucumbers Paracaudina chilensis and Holothuria hilla:Structures and anticoagulant activity[J]. Marine Drugs,2020,18(11):540. doi: 10.3390/md18110540
[41]	UCHIMURA K. Keratan sulfate:Biosynthesis, structures, and biological functions[J]. Methods in Molecular Biology,2015,1229:389−400.
[42]	MELROSE J. Keratan sulfate (KS)-proteoglycans and neuronal regulation in health and disease:The importance of KS-glycodynamics and interactive capability with neuroregulatory ligands[J]. Journal of Neurochemistry,2019,149(2):170−194. doi: 10.1111/jnc.14652
[43]	国家药典委员会. 中华人民共和国药典[M]. 第二部. 北京:中国医药科技出版社, 2015. [National Pharmacopoeia Committee. Pharmacopoeia of the People's Republic of China[M]. Part II. Beijing:China Medical Science & Technology Press, 2015.] National Pharmacopoeia Committee. Pharmacopoeia of the People's Republic of China[M]. Part II. Beijing: China Medical Science & Technology Press, 2015.
[44]	SONG S, PENG H, WANG Q, et al. Inhibitory activities of marine sulfated polysaccharides against SARS-CoV-2[J]. Food Function,2020,11(9):7415−7420. doi: 10.1039/D0FO02017F
[45]	KOLLINIATI O, IERONYMAKI E, VERGADI E, et al. Metabolic regulation of macrophage activation[J]. Journal of Innate Immunity,2022,14(1):48−64.
[46]	张祺, 李学敏, 李兆杰, 等. 海参岩藻聚糖硫酸酯对巨噬细胞的调节作用及信号通路研究[J]. 中国药理学通报,2015,31(1):87−92. [ZHANG Qi, LI Xuemin, LI Zhaojie, et al. The regulatory effect and signaling pathway of sea cucumber fucoidan sulfate on macrophages[J]. Chinese Pharmacological Bulletin,2015,31(1):87−92.] doi: 10.3969/j.issn.1001-1978.2015.01.019 ZHANG Qi, LI Xuemin, LI Zhaojie, et al. The regulatory effect and signaling pathway of sea cucumber fucoidan sulfate on macrophages[J]. Chinese Pharmacological Bulletin, 2015, 31（1）: 87−92. doi: 10.3969/j.issn.1001-1978.2015.01.019
[47]	KIDGELL J T, GLASSON C R, Magnusson M, et al. The molecular weight of ulvan affects the in vitro inflammatory response of a murine macrophage[J]. International Journal of Biological Macromolecules,2020,150:839−848. doi: 10.1016/j.ijbiomac.2020.02.071
[48]	JIANG S, YIN H, QI X, et al. Immunomodulatory effects of fucosylated chondroitin sulfate from Stichopus chloronotus on RAW 264.7 cells[J]. Carbohydrate Polymers,2021,251:117088. doi: 10.1016/j.carbpol.2020.117088
[49]	萨仁娜. 海带岩藻聚糖分级纯化及对肉仔鸡巨噬细胞免疫调节的研究[D]. 北京:中国农业科学院, 2008. [SA Renna. Classification and purification of kelp fucoidan and its effect on immune regulation of broiler macrophages[D]. Beijing:Chinese Academy of Agricultural Sciences, 2008.] SA Renna. Classification and purification of kelp fucoidan and its effect on immune regulation of broiler macrophages[D]. Beijing: Chinese Academy of Agricultural Sciences, 2008.
[50]	JAYAWARDENA T U, SANJEEWA K A, Nagahawatta D, et al. Anti-Inflammatory effects of sulfated polysaccharide from Sargassum swartzii in macrophages via blocking TLR/NF-Kb signal transduction[J]. Marine Drugs,2020,18(12):601. doi: 10.3390/md18120601
[51]	XU H P, HITOSHI K, TOMOMI I, et al. The keratan sulfate disaccharide gal(6S03)β 1, 4-GlcNAc(6S03) modulates interleukin 12 production by macrophages in murine Thy-1 type autoimmune disease[J]. The Journal of Biological Chemistry,2005(21):280−284.
[52]	BAE S, YIM J, LEE H, et al. Activation of murine peritoneal macrophages by sulfated exopolysaccharide from marine microalga Gyrodinium impudicum (strain KG03):Involvement of the NF-κB and JNK pathway[J]. International Immunopharmacology,2021,99:107981. doi: 10.1016/j.intimp.2021.107981
[53]	KIM J K, CHO M L, KARNJANAPRATUM S, et al. In vitro and in vivo immunomodulatory activity of sulfated polysaccharides from Enteromorpha prolifera[J]. International Journal of Biological Macromolecules,2011,49(5):1051−1058. doi: 10.1016/j.ijbiomac.2011.08.032
[54]	TAN L H. Sulfation of a polysaccharide obtained from Phellinus ribis and potential biological activities of the sulfated derivatives[J]. Carbohydrate Polymers:Scientific and Technological Aspects of Industrially Important Polysaccharides,2009,77(2):370−375.
[55]	DI T, CHEN G, SUN Y, et al. Antioxidant and immunostimulating activities in vitro of sulfated polysaccharides isolated from Gracilaria rubra[J]. Journal of Functional Foods,2017,28:64−75. doi: 10.1016/j.jff.2016.11.005
[56]	CRABTREE G R, CLIPSTONE N A. Signal transmission between the plasma membrane and nucleus of T lymphocytes[J]. Annual Review of Biochemistry,1994,63:1045−1083. doi: 10.1146/annurev.bi.63.070194.005145
[57]	HAN S B, PARK S K, AHN H J, et al. Characterization of B cell membrane receptors of polysaccharide isolated from the root of Acanthopanax koreanum[J]. International Immunopharmacology,2003,3(5):683−691. doi: 10.1016/S1567-5769(03)00056-0
[58]	AHN G, BING S J, KANG S-M, et al. The JNK/NFκB pathway is required to activate murine lymphocytes induced by a sulfated polysaccharide from Ecklonia cava[J]. Biochimica et Biophysica Acta-General Subjects,2013,1830(3):2820−2829. doi: 10.1016/j.bbagen.2012.12.008
[59]	JANG J Y, MOON S Y, JOO H G. Differential effects of fucoidans with low and high molecular weight on the viability and function of spleen cells[J]. Food and Chemical Toxicology:An International Journal Published for the British Industrial Biological Research Association,2014,68:234−238. doi: 10.1016/j.fct.2014.03.024
[60]	MOREIRA A S P, GASPAR D, FERREIRA S S, et al. Water-soluble Saccharina latissima polysaccharides and relation of their structural characteristics with in vitro immunostimulatory and hypocholesterolemic activities[J]. Marine Drugs,2023,21(3):183. doi: 10.3390/md21030183
[61]	ZHAO X, JIAO G, YANG Y, et al. Structure and immunomodulatory activity of a sulfated agarose with pyruvate and xylose substitutes from Polysiphonia senticulosa Harvey[J]. Carbohydrate Polymers,2017,176:29−37. doi: 10.1016/j.carbpol.2017.08.065
[62]	PARK H B, HWANG J, ZHANG W, et al. Polysaccharide from Codium fragile induces anti-cancer immunity by activating natural killer cells[J]. Marine Drugs,2020,18(12):626. doi: 10.3390/md18120626
[63]	SURAYOT U, LEE S, YOU S. Effects of sulfated fucan from the sea cucumber Stichopus japonicus on natural killer cell activation and cytotoxicity[J]. International Journal of Biological Macromoleculesm,2018,108:177−184. doi: 10.1016/j.ijbiomac.2017.11.102
[64]	BRUSILOVSKY M, CORDOBA M, ROSENTAL B, et al. Genome-wide siRNA screen reveals a new cellular partner of NK cell receptor KIR2DL4:Heparan sulfate directly modulates KIR2DL4-mediated responses[J]. Journal of Immunology,2013,191(10):5256−5267. doi: 10.4049/jimmunol.1302079
[65]	ZHANG W, AN E K, PARK H B, et al. Ecklonia cava fucoidan has potential to stimulate natural killer cells in vivo[J]. International Journal of Biological Macromolecules,2021,185:111−121. doi: 10.1016/j.ijbiomac.2021.06.045
[66]	MERLE N S, CHURCH S E, FREMEAUX-BACCHI V, et al. Complement system part I - molecular mechanisms of activation and regulation[J]. Frontiers in Immunology,2015,6:262.
[67]	REID K B, TURNER M W. Mammalian lectins in activation and clearance mechanisms involving the complement system; Proceedings of the Springer seminars in immunopathology[J]. Springer Seminars in Immunopathology,1994,15:307−26. doi: 10.1007/BF01837363
[68]	ZVYAGINTSEVA T N, SHEVCHENKO N M, NAZAROVA I V, et al. Inhibition of complement activation by water-soluble polysaccharides of some far-eastern brown seaweeds[J]. Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology,2000,126(3):209−215.
[69]	BLONDIN C, FISCHER E, BOISSON-VIDAL C, et al. Inhibition of complement activation by natural sulfated polysaccharides (fucans) from brown seaweed[J]. Molecular Immunology,1994,31(4):247−253. doi: 10.1016/0161-5890(94)90121-X
[70]	TISSOT B, MONTDARGENT B, CHEVOLOT L, et al. Interaction of fucoidan with the proteins of the complement classical pathway[J]. Acta Biochimica Et Biophysica Sinica,2003,1651(1-2):5−16. doi: 10.1016/S1570-9639(03)00230-9
[71]	COFRANCSCO E, RADAELLI F, POGLIANIA E, et al. Correlation of sulfate content and degree of carboxylation of heparin and related glycosaminoglycans with anticomplement activity. Relationships to the anticoagulant and platelet-aggregating activities[J]. Thrombosis Research,1979,14(1):179−187. doi: 10.1016/0049-3848(79)90036-7
[72]	SHARATH M D, MERCHANT Z M, KIM Y S, et al. Small heparin fragments regulate the amplification pathway of complement[J]. Immunopharmacology,1985,9(2):73−80. doi: 10.1016/0162-3109(85)90002-5
[73]	LI L, LI Y, IJAZ M, et al. Review on complement analysis method and the roles of glycosaminoglycans in the complement system[J]. Carbohydrate Polymers,2015,134:590−597. doi: 10.1016/j.carbpol.2015.08.028
[74]	TISSOT B, DANIEL R, PLACE C. Interaction of the C1 complex of complement with sulfated polysaccharide and DNA probed by single molecule fluorescence microscopy[J]. European Journal of Biochemistry,2003,270(23):4714−4720. doi: 10.1046/j.1432-1033.2003.03870.x
[75]	LI Y, LIU S, DING Y, et al. Structure, in vitro digestive characteristics and effect on gut microbiota of sea cucumber polysaccharide fermented by Bacillus subtilis Natto[J]. Food Research International,2023,169:112872. doi: 10.1016/j.foodres.2023.112872
[76]	QIN J, LI R, RAES J, et al. A human gut microbial gene catalogue established by metagenomic sequencing[J]. Nature,2010,464(7285):59−65. doi: 10.1038/nature08821
[77]	ZHU Z, HAN Y, DING Y, et al. Health effects of dietary sulfated polysaccharides from seafoods and their interaction with gut microbiota[J]. Comprehensive Reviews in Food Science and Food Safety,2021,20(3):2882−2913. doi: 10.1111/1541-4337.12754
[78]	LIU X, ZHANG Y, LI W, et al. Fucoidan ameliorated dextran sulfate sodium-induced ulcerative colitis by modulating gut microbiota and bile acid metabolism[J]. Journal of Agricultural and Food Chemistry,2022,70(47):14864−14876. doi: 10.1021/acs.jafc.2c06417
[79]	ZHU Z, ZHU B, SUN Y, et al. Sulfated polysaccharide from sea cucumber modulates the gut microbiota and its metabolites in normal mice[J]. International Journal of Biological Macromolecules, 2018, 120(Pt A):502−512.
[80]	HU S, WANG J, XU Y, et al. Anti-inflammation effects of fucosylated chondroitin sulphate from Acaudina molpadioides by altering gut microbiota in obese mice[J]. Food Function,2019,10(3):1736−1746. doi: 10.1039/C8FO02364F
[81]	BISSON-BOUTELLIEZ C, MASSIN F, DUMAS D, et al. Desulfovibrio spp. survive within KB cells and modulate inflammatory responses[J]. Molecular Oral Microbiology,2010,25(3):226−235. doi: 10.1111/j.2041-1014.2009.00550.x
[82]	ZHU Z, ZHU B, SUN Y, et al. Sulfated polysaccharide from sea cucumber and its depolymerized derivative prevent obesity in association with modification of gut microbiota in high-fat diet-fed mice[J]. Molecular Nutrition & Food Research,2018,62(23):1800446.

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