Fucoidan isolated from the popular edible brown seaweed Sargassum fusiforme suppresses lipopolysaccharide-induced inflammation by blocking NF-κB signal pathway

Abstract

The anti-inflammatory effect of a fucoidan with a molecular weight of 102.67 kDa isolated from an enzymatic digest of Sargassum fusiforme was investigated in lipopolysaccharide (LPS)-stimulated RAW 264.7 macrophages and zebrafish. The results indicated that the fucoidan significantly and dose-dependently inhibited the production of inflammatory molecules, including tumor necrosis factor-alpha (TNF-α), nitric oxide (NO), prostaglandin E2 (PGE2), interleukin-1 beta (IL-1β), and interleukin-6 (IL-6), as well as improved the viability of LPS-stimulated RAW 264.7 cells. Moreover, the fucoidan suppressed the expression of cyclooxygenase-2 (COX-2) and inducible nitric oxide synthase (iNOS) by regulating the nuclear factor kappa B (NF-κB) pathway in LPS-stimulated RAW 264.7 cells. Furthermore, in vivo test results suggested that the fucoidan remarkably reduced reactive oxygen species (ROS), cell death, and NO levels in LPS-stimulated zebrafish in a dose-dependent manner. Taken together, these results demonstrated that the fucoidan isolated from S. fusiforme possesses strong anti-inflammatory activities in vitro and in vivo, and could prove as an important candidate to be used to develop anti-inflammatory agents in pharmaceutical and cosmeceutical industries.

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References

  1. Cheong SH, Yang H-W, Ko E-Y, Ahn G, Lee W, Kim D, Jeon Y-J, Kim K-N (2016) Anti-inflammatory effects of trans-1,3-diphenyl-2,3-epoxypropane-1-one in zebrafish embryos in vivo model. Fish Shellfish Immunol 50:16–20

    CAS  Article  Google Scholar 

  2. Cui M, Wu J, Wang S, Shu H, Zhang M, Liu K, Liu K (2019) Characterization and anti-inflammatory effects of sulfated polysaccharide from the red seaweed Gelidium pacificum Okamura. Int J Biol Macromol 129:377–385

    CAS  Article  Google Scholar 

  3. Dong H, Zheng L, Yu P, Jiang Q, Wu Y, Huang C, Yin B (2020) Characterization and application of lignin–carbohydrate complexes from lignocellulosic materials as antioxidants for scavenging in vitro and in vivo reactive oxygen species. ACS Sustain Chem Eng 8:256–266

    CAS  Article  Google Scholar 

  4. Guevara M, Tejera E, Iturralde GA, Jaramillo-Vivanco T, Granda-Albuja MG, Granja-Albuja S, Santos-Buelga C, González-Paramás AM, Álvarez-Suarez JM (2019) Anti-inflammatory effect of the medicinal herbal mixture infusion, Horchata, from southern Ecuador against LPS-induced cytotoxic damage in RAW 264.7 macrophages. Food Chem Toxicol 131:110594

    CAS  Article  Google Scholar 

  5. Hwang D, Kang M-j, Jo JM, Seo BY, Park GN, Kim G-D (2019) Anti-inflammatory activity of β-thymosin peptide derived from Pacific oyster (Crassostrea gigas) on NO and PGE2 production by down-regulating NF-κB in LPS-induced RAW264.7 Macrophage Cells. Mar Drugs 17:129

    CAS  Article  Google Scholar 

  6. Kang S-M, Kim K-N, Lee S-H, Ahn G, Cha S-H, Kim A-D, Yang X-D, Kang M-C, Jeon Y-J (2011) Anti-inflammatory activity of polysaccharide purified from AMG-assistant extract of Ecklonia cava in LPS-stimulated RAW 264.7 macrophages. Carbohydr Polym 85:80–85

    CAS  Article  Google Scholar 

  7. Kim K-N, Ko Y-J, Yang H-M, Ham Y-M, Roh SW, Jeon Y-J, Ahn G, Kang M-C, Yoon W-J, Kim D, Oda T (2013) Anti-inflammatory effect of essential oil and its constituents from fingered citron (Citrus medica L. var. sarcodactylis) through blocking JNK, ERK and NF-κB signaling pathways in LPS-activated RAW 264.7 cells. Food Chem Toxicol 57:126–131

  8. Kim E-A, Lee S-H, C-i K, Cha S-H, Kang M-C, Kang S-M, Ko S-C, Lee W-W, Ko J-Y, Lee J-H, Kang N, Oh J-Y, Ahn G, Jee YH, Jeon Y-J (2014) Protective effect of fucoidan against AAPH-induced oxidative stress in zebrafish model. Carbohydr Polym 102:185–191

    CAS  Article  Google Scholar 

  9. Ko S-C, Jeon Y-J (2015) Anti-inflammatory effect of enzymatic hydrolysates from Styela clava flesh tissue in lipopolysaccharide-stimulated RAW 264.7 macrophages and in vivo zebrafish model. Nutr Res Pract 9:219–226

    CAS  Article  Google Scholar 

  10. Lee S-H, Ko C-I, Jee Y, Jeong Y, Kim M, Kim J-S, Jeon Y-J (2013) Anti-inflammatory effect of fucoidan extracted from Ecklonia cava in zebrafish model. Carbohydr Polym 92:84–89

    CAS  Article  Google Scholar 

  11. Lee J-H, Ko J-Y, Kim E-A, Hwang E-K, Park CS, Lee J-S, Kim C-Y, Lee H-S, Kang H-K, Cha S-H, Jeon Y-J (2017) Identification and large isolation of an anti-inflammatory compound from an edible brown seaweed, Undariopsis peterseniana, and evaluation on its anti-inflammatory effect in in vitro and in vivo zebrafish. J Appl Phycol 29:1587–1596

    CAS  Article  Google Scholar 

  12. Li Y, Fu X, Duan D, Xu J, Gao X (2018) Comparison study of bioactive substances and nutritional components of brown algae Sargassum fusiforme strains with different vesicle shapes. J Appl Phycol 30:3271–3283

    CAS  Article  Google Scholar 

  13. Sanjeewa KKA, Jayawardena Thilina U, Kim H-S, Kim S-Y, Shanura FIP, Wang L, Abetunga DTU, Kim W-S, Lee D-S, Jeon Y-J (2019) Fucoidan isolated from Padina commersonii inhibit LPS-induced inflammation in macrophages blocking TLR/NF-κB signal pathway. Carbohydr Polym 224:115195

    Article  Google Scholar 

  14. Wan P, Xie M, Chen G, Dai Z, Hu B, Zeng X, Sun Y (2019) Anti-inflammatory effects of dicaffeoylquinic acids from Ilex kudingcha on lipopolysaccharide-treated RAW264.7 macrophages and potential mechanisms. Food Chem Toxicol 126:332–342

    CAS  Article  Google Scholar 

  15. Wang L, Lee W, Oh YJ, Cui RY, Ryu B, Jeon Y-J (2018a) Protective effect of sulfated polysaccharides from celluclast-assisted extract of Hizikia fusiforme against ultraviolet B-induced skin damage by regulating NF-κB, AP-1, and MAPKs signaling pathways in vitro in human dermal fibroblasts. Mar Drugs 16:239–246

    Article  Google Scholar 

  16. Wang L, Oh JY, Kim HS, Lee W, Cui Y, Lee HG, Kim Y-T, Ko JY, Jeon Y-J (2018b) Protective effect of polysaccharides from Celluclast-assisted extract of Hizikia fusiforme against hydrogen peroxide-induced oxidative stress in vitro in Vero cells and in vivo in zebrafish. Int J Biol Macromol 112:483–489

    CAS  Article  Google Scholar 

  17. Wang L, Park Y-J, Jeon Y-J, Ryu B (2018c) Bioactivities of the edible brown seaweed, Undaria pinnatifida: a review. Aquaculture 495:873–880

    CAS  Article  Google Scholar 

  18. Wang L, Cui YR, Yang H-W, Lee HG, Ko J-Y, Jeon Y-J (2019a) A mixture of seaweed extracts and glycosaminoglycans from sea squirts inhibits α-MSH-induced melanogenesis in B16F10 melanoma cells. Fish Aquat Sci 22:11

    Article  Google Scholar 

  19. Wang L, Kim HS, Oh JY, Je JG, Jeon Y-J, Ryu B (2019b) Protective effect of diphlorethohydroxycarmalol isolated from Ishige okamurae against UVB-induced damage in vitro in human dermal fibroblasts and in vivo in zebrafish. Food Chem Toxicol 110963

  20. Wang L, Lee W, Cui YR, Ahn G, Jeon Y-J (2019c) Protective effect of green tea catechin against urban fine dust particle-induced skin aging by regulation of NF-κB, AP-1, and MAPKs signaling pathways. Environ Pollut 252:1318–1324

    CAS  Article  Google Scholar 

  21. Wang L, Oh JY, Yang H-W, Kim HS, Jeon Y-J (2019d) Protective effect of sulfated polysaccharides from a celluclast-assisted extract of Hizikia fusiforme against ultraviolet B-induced photoaging in vitro in human keratinocytes and in vivo in zebrafish. Mar Life Sci Tech 1:104–111

    Article  Google Scholar 

  22. Wang L, Jayawardena TU, Yang H-W, Lee HG, Kang M-C, Sanjeewa KKA, Oh JY, Jeon Y-J (2020a) Isolation, characterization, and antioxidant activity evaluation of a fucoidan from an enzymatic digest of the edible seaweed, Hizikia fusiforme. Antioxidants 9:363

    CAS  Article  Google Scholar 

  23. Wang L, Oh JY, Jayawardena TU, Jeon Y-J, Ryu B (2020b) Anti-inflammatory and anti-melanogenesis activities of sulfated polysaccharides isolated from Hizikia fusiforme: short communication. Int J Biol Macromol 142:545–550

    CAS  Article  Google Scholar 

  24. Wang L, Oh JY, Kim Y-S, Lee H-G, Lee J-S, Jeon Y-J, Ryu B (2020c) Anti-photoaging and anti-melanogenesis effects of fucoidan isolated from Hizikia fusiforme and its underlying mechanisms. Mar Drugs 18:427

    CAS  Article  Google Scholar 

  25. Welsh P, Grassia G, Botha S, Sattar N, Maffia P (2017) Targeting inflammation to reduce cardiovascular disease risk: a realistic clinical prospect? Br J Pharmacol 174:3898–3913

    CAS  Article  Google Scholar 

  26. Wijesinghe WAJP, Kim E-A, Kang M-C, Lee W-W, Lee H-S, Vairappan CS, Jeon Y-J (2014) Assessment of anti-inflammatory effect of 5β-hydroxypalisadin B isolated from red seaweed Laurencia snackeyi in zebrafish embryo in vivo model. Environ Toxicol Pharmacol 37:110–117

    CAS  Article  Google Scholar 

  27. Williams CS, Mann M, DuBois RN (1999) The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18:7908–7916

    CAS  Article  Google Scholar 

  28. Wu G-J, Shiu S-M, Hsieh M-C, Tsai G-J (2016) Anti-inflammatory activity of a sulfated polysaccharide from the brown alga Sargassum cristaefolium. Food Hydrocoll 53:16–23

    CAS  Article  Google Scholar 

  29. Yang Y, Chen J, Lei L, Li F, Tang Y, Yuan Y, Zhang Y, Wu S, Yin R, Ming J (2019) Acetylation of polysaccharide from Morchella angusticeps peck enhances its immune activation and anti-inflammatory activities in macrophage RAW264.7 cells. Food Chem Toxicol 125:38–45

    CAS  Article  Google Scholar 

  30. Zeng X, Chen X, Qin H, Han Y, Chen X, Han Z, Zhao W (2020) Preventive effects of a natural anti-inflammatory agent salvianolic acid a on acute kidney injury in mice. Food Chem Toxicol 135:110901

    CAS  Article  Google Scholar 

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Funding

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1A6A1A03033553).

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Correspondence to Jae-Il Kim or You-Jin Jeon.

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Wang, L., Oh, JY., Yang, HW. et al. Fucoidan isolated from the popular edible brown seaweed Sargassum fusiforme suppresses lipopolysaccharide-induced inflammation by blocking NF-κB signal pathway. J Appl Phycol (2021). https://doi.org/10.1007/s10811-021-02390-7

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Keywords

  • Sargassum fusiforme
  • Fucoidan
  • Anti-inflammatory effect
  • NF-κB pathway
  • Zebrafish