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.
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Williams CS, Mann M, DuBois RN (1999) The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18:7908–7916
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
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
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
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).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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 33, 1845–1852 (2021). https://doi.org/10.1007/s10811-021-02390-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-021-02390-7