Divergent immunomodulatory and gut microbiota-modulating effects of Sargassum polysaccharides and oligosaccharides in delayed-type hypersensitivity mice

Yang-Ching Chen , Shih-Yuan Fang , Chien-Li Chen , Ming-Chih Fang , Yu-Ying Yang , Meng-Chou Lee , Chung-Hsiung Huang

Bioresources and Bioprocessing ›› 2025, Vol. 12 ›› Issue (1) : 108

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Bioresources and Bioprocessing ›› 2025, Vol. 12 ›› Issue (1) :108 DOI: 10.1186/s40643-025-00948-8
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Divergent immunomodulatory and gut microbiota-modulating effects of Sargassum polysaccharides and oligosaccharides in delayed-type hypersensitivity mice

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Abstract

Recent research has indicated that polysaccharides extracted from Sargassum (SP) possess promising activity in alleviating type I hypersensitivity reactions. However, effects of SP and Sargassum oligosaccharides (SO) on immune regulation and gut microbiota in type IV hypersensitivity remain unexplored. In this study, SP and SO were prepared and structurally characterized. SP contained high-molecular-weight fractions (866 kDa and 276 kDa), whereas SO was composed of low-molecular-weight components (3.74 kDa and 126 Da), lacked sulfate groups, and exhibited higher reducing sugar contents. The influence of SP and SO on immune regulation and the structure of gut microbial communities was examined using a mouse model of ovalbumin (OVA)-induced delayed-type hypersensitivity (DTH). Administration of SP and SO (25 or 250 mg/kg per day for 10 days) significantly attenuated DTH responses, evidenced by a decrease in footpad edema and a lower degree of cell infiltration. While both SP and SO had limited effects on serum IgG1 levels and splenic TGF-β production, treatment with SO at 250 mg/kg significantly reduced serum total IgG, OVA-specific IgG, and splenic IL-2 levels, while increasing IL-10 production. Notably, SO exerted the most pronounced effect in lowering IgG2a and IFN-γ levels. Additionally, SO treatment led to distinct shifts in gut microbial profile, marked by elevated levels of Muribaculaceae, Lactobacillus, and Bacteroides. These microbial changes were accompanied by elevated concentrations of short-chain fatty acids (SCFAs). Collectively, these results indicate that SO holds potential as a functional dietary component for the alleviation of type IV hypersensitivity responses, through modulation of gut microbiota and immunomodulation.

Keywords

Delayed-type hypersensitivity / Gut microbiota / Oligosaccharides / Polysaccharides / Sargassum

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Yang-Ching Chen, Shih-Yuan Fang, Chien-Li Chen, Ming-Chih Fang, Yu-Ying Yang, Meng-Chou Lee, Chung-Hsiung Huang. Divergent immunomodulatory and gut microbiota-modulating effects of Sargassum polysaccharides and oligosaccharides in delayed-type hypersensitivity mice. Bioresources and Bioprocessing, 2025, 12(1): 108 DOI:10.1186/s40643-025-00948-8

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References

[1]

AllenIC. Delayed-type hypersensitivity models in mice. Methods Mol Biol, 2013, 1031: 101-107.

[2]

AnyanjiVU, MustaphaNM, LimS-L, MohamedS. Seaweed (Eucheuma cottonii) reduced inflammation, mucin synthesis, eosinophil infiltration and MMP-9 expressions in asthma-induced rats compared to Loratadine. J Funct Foods, 2015, 19: 710-722.

[3]

BlackCA. Delayed type hypersensitivity: current theories with a historic perspective. Dermatol Online J, 1999, 57.

[4]

BurrelloC, GaravagliaF, CribiùFM, ErcoliG, LopezG, TroisiJ, ColucciA, GugliettaS, CarloniS, GuglielmettiS. Therapeutic faecal microbiota transplantation controls intestinal inflammation through IL10 secretion by immune cells. Nat Commun, 2018, 95184.

[5]

ByunE-H. Comparison study of Immunomodulatory activity of polysaccharide and ethanol extracted from sargassum fulvellum. J Korean Soc Food Sci Nutr, 2015, 44: 1621-1628.

[6]

CaoJ, WangJ, WangS, XuX. Porphyra species: a mini-review of its Pharmacological and nutritional properties. J Med Food, 2016, 19: 111-119.

[7]

CoffmanRL, LebmanDA, RothmanP. Mechanism and regulation of Immunoglobulin isotype switching. Adv Immunol, 1993, 54: 229-270.

[8]

FanS, ZhangJ, NieW, ZhouW, JinL, ChenX, LuJ. Antitumor effects of polysaccharide from sargassum fusiforme against human hepatocellular carcinoma HepG2 cells. Food Chem Toxicol, 2017, 102: 53-62.

[9]

HanEJ, KimH-S, SanjeewaKKA, JungK, JeeY, JeonY-J, FernandoIPS, AhnG. Sargassum Horneri as a functional food ameliorated IgE/BSA-induced mast cell activation and passive cutaneous anaphylaxis in mice. Mar Drugs, 2020, 18594.

[10]

HanEJ, FernandoIPS, KimH-S, JeonY-J, MadusankaDMD, DiasMKHM, JeeY, AhnG. Oral administration of sargassum Horneri improves the HDM/DNCB-induced atopic dermatitis in NC/Nga mice. Nutrients, 2020, 122482.

[11]

HiippalaK, JouhtenH, RonkainenA, HartikainenA, KainulainenV, JalankaJ, SatokariR. The potential of gut commensals in reinforcing intestinal barrier function and alleviating inflammation. Nutrients, 2018, 10988.

[12]

HuangL, ZengQ, ZhangY, YinQ, ZhuX, ZhangP, WangC, LiuJ. Effects of fucoidans and alginates from sargassum graminifolium on allergic symptoms and intestinal microbiota in mice with OVA-induced food allergy. Food Funct, 2022, 13: 6702-6715.

[13]

IshiharaK, OyamadaC, MatsushimaR, MurataM, MuraokaT. Inhibitory effect of porphyran, prepared from dried Nori, on contact hypersensitivity in mice. Biosci Biotechnol Biochem, 2005, 69: 1824-1830.

[14]

KazłowskiB, ChiuY-H, KazłowskaK, PanC-L, WuC-J. Prevention of Japanese encephalitis virus infections by low-degree-polymerisation sulfated saccharides from gracilaria sp. and monostroma nitidum. Food Chem, 2012, 133: 866-874.

[15]

KimHI, KimD-S, JungY, SungN-Y, KimM, HanI-J, NhoEY, HongJH, LeeJ-K, BooM. Immune-enhancing effect of sargassum Horneri on cyclophosphamide-induced immunosuppression in BALB/c mice and primary cultured splenocytes. Molecules, 2022, 278253.

[16]

KobayashiK, KanedaK, KasamaT. Immunopathogenesis of delayed-type hypersensitivity. Microsc Res Tech, 2001, 53: 241-245.

[17]

KohA, De VadderF, Kovatcheva-DatcharyP, BäckhedF. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell, 2016, 165: 1332-1345.

[18]

LeeP-T, TranHTQ, HuangH-T, NanF-H, LeeM-C. Sargassum Horneri extracts stimulate innate immunity, enhance growth performance, and upregulate immune genes in the white shrimp Litopenaeus vannamei. Fish Shellfish Immunol, 2020, 102: 276-285.

[19]

LiyanageNM, KimY-S, NagahawattaDP, JinH, YangH-W, JayawardhanaHHACK, JayawardenaTU, JeonY-J. Sargassum Horneri as a prebiotic dietary supplement for immunity development in Streptococcus parauberis infected zebrafish model. Front Mar Sci, 2022, 9901676.

[20]

MitraIMC, VasquezRD, SalongaRB, CorpuzMJ-A. Physicochemical characterization of sargassum polcystum C. Agardh and its activity against dinitrofluorobenzene-induced allergic contact dermatitis in mice. J Ilm Farm Farmasyifa, 2020, 16: 19-30.

[21]

MorrisHJ, CarrilloO, AlmaralesA, BermúdezRC, LebequeY, FontaineR, LlauradóG, BeltránY. Immunostimulant activity of an enzymatic protein hydrolysate from green microalga chlorella vulgaris on undernourished mice. Enzyme Microb Technol, 2007, 40: 456-460.

[22]

OuJY, WeiYJ, LiuFL, HuangCH. Anti-allergic effects of Ulva-derived polysaccharides, oligosaccharides and residues in a murine model of food allergy. Heliyon, 2023, 9e22840.

[23]

OuJY, LiuFL, ChenCL, FangMC, HuangCH. Immunomodulatory effects of Ulva-derived polysaccharides, oligosaccharides, and residues in a murine model of delayed-type hypersensitivity. Biosci Microbiota Food Health, 2024, 43: 128-134.

[24]

PalomaresO, Martin-FontechaM, LauenerR, Traidl-HoffmannC, CavkaytarO, AkdisM, AkdisC. Regulatory T cells and immune regulation of allergic diseases: roles of IL-10 and TGF-β. Genes Immun, 2014, 15: 511-520.

[25]

ParkJ, KimM, KangSG, JannaschAH, CooperB, PattersonJ, KimCH. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR–S6K pathway. Mucosal Immunol, 2015, 8: 80-93.

[26]

RossignoloJA, DuranAJFP, BuenoC, Martinelli FilhoJE, JuniorHS, ToninFG. Algae application in civil construction: A review with focus on the potential uses of the pelagic sargassum spp. Biomass. J Environ Manage, 2022, 303114258.

[27]

RushdiMI, Abdel-RahmanIA, SaberH, AttiaEZ, AbdelraheemWM, MadkourHA, HassanHM, ElmaidomyAH, AbdelmohsenUR. Pharmacological and natural products diversity of the brown algae genus sargassum. RSC Adv, 2020, 10: 24951-24972.

[28]

SönmezAY, Bi̇lenS, TaştanY, SeragKJB, ToringCC, RomeroJB, KenanoğluON, TerziE. Oral administration of sargassum polycystum extracts stimulates immune response and increases survival against Aeromonas hydrophila infection in Oncorhynchus Mykiss. Fish Shellfish Immunol, 2021, 117: 291-298.

[29]

SunM, WuW, LiuZ, CongY. Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. J Gastroenterol, 2017, 52: 1-8.

[30]

SunY, ChenX, LiuS, YuH, LiR, WangX, QinY, LiP. Preparation of low molecular weight sargassum fusiforme polysaccharide and its anticoagulant activity. J Oceanol Limnol, 2018, 36: 882-891.

[31]

TanJ, McKenzieC, PotamitisM, ThorburnAN, MackayCR, MaciaL. The role of short-chain fatty acids in health and disease. Adv Immunol, 2014, 121: 91-119.

[32]

TominagaA, OkuyamaH, FukuokaS, TaguchiT, KusumotoY, ShimizuK, OnoS. Effects of edible algae polysaccharides on allergic, inflammatory, and anti-tumor responses through toll-like receptor 4. Antiinflamm Antiallergy Agents Med Chem, 2010, 9: 238-250.

[33]

TroyEB, KasperDL. Beneficial effects of bacteroides fragilis polysaccharides on the immune system. Front Biosci (Landmark Ed), 2010, 1525.

[34]

Victoriano-BlanciaPL, MamelocoEJG, CadizRE, TraifalgarRFM. Sargassum polycystum polysaccharide extract improved immunological responses and enhanced resistance of Penaeus monodon against vibrio harveyi infection. Int Aquat Res, 2022, 14: 181-192.

[35]

WeiY-J, FangR-E, OuJ-Y, PanC-L, HuangC-H. Modulatory effects of Porphyra-derived polysaccharides, oligosaccharides and their mixture on antigen-specific immune responses in ovalbumin-sensitized mice. J Funct Foods, 2022, 96105209.

[36]

WenZ-S, XiangX-W, JinH-X, GuoX-Y, LiuL-J, HuangY-N, OuYangX-K, QuY-L. Composition and anti-inflammatory effect of polysaccharides from sargassum Horneri in RAW264. 7 macrophages. Int J Biol Macromol, 2016, 88: 403-413.

[37]

WooG-E, HwangH-J, ParkA-Y, SimJ-Y, WooS-Y, KimM-J, JeongS-M, SungN-Y, KimD-S, AhnD-H. Anti-atopic activities of sargassum Horneri hot water extracts in 2, 4-dinitrochlorobezene-induced mouse models. J Microbiol Biotechnol, 2023, 33363.

[38]

YangC-f, LaiS-s, ChenY-h, LiuD, LiuB, AiC, WanX-z, GaoL-y, ChenX-h, ZhaoC. Anti-diabetic effect of oligosaccharides from seaweed sargassum confusum via JNK-IRS1/PI3K signalling pathways and regulation of gut microbiota. Food Chem Toxicol, 2019, 131110562.

[39]

ZhangD, JianY-P, ZhangY-N, LiY, GuL-T, SunH-H, LiuM-D, ZhouH-L, WangY-S, XuZ-X. Short-chain fatty acids in diseases. Cell Commun Signal, 2023, 21212.

[40]

ZhouR, ShiX, GaoY, CaiN, JiangZ, XuX. Anti-inflammatory activity of guluronate oligosaccharides obtained by oxidative degradation from alginate in lipopolysaccharide-activated murine macrophage RAW 264.7 cells. J Agric Food Chem, 2015, 63: 160-168.

Funding

National Science and Technology Council(NSTC 113-2320-B019-004-MY3)

University System of Taipei Joint Research Program(USTP-NTOU-TMU-112-05)

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