Skip to main content
Log in

Anti-inflammatory activity of phlorotannin-rich fermented Ecklonia cava processing by-product extract in lipopolysaccharide-stimulated RAW 264.7 macrophages

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

In this study, fermentation was employed as a tool to further increase the bioactive potential of processing by-product from a brown seaweed, Ecklonia cava, which can be obtained from food and cosmetic industries after its polyphenol extraction. The fermentation process was done for 24 h using an industrially important microorganism Candida utilis prior to being extracted with 80 % ethanol. The anti-inflammatory potential of the fermented E. cava processing by-product extract (FEPBE) was evaluated in vitro. The phlorotannin-rich FEPBE dose-dependently inhibited the nitric oxide production, prostaglandin-E2 production and suppressed the inducible nitric oxide synthase and cyclooxygenase-2 expressions in lipopolysaccharide-stimulated RAW 264.7 cells. The release of pro-inflammatory cytokines, interleukin-1β and interleukin-6, was significantly suppressed by the extract in a dose-dependent manner. Due to the profound anti-inflammatory activity, FEPBE appears as a value-added biomass fraction that can be exploited in numerous industrial applications as a source of functional ingredients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahmed N, Chen LC, Gordon MA, Laskin JD, Laskin DL (2002) Regulation of cyclooxygenase-2 by nitric oxide in activated hepatic macrophages during acute endotoxemia. J Leukocyte Biol 71:1005–1011

    Google Scholar 

  • Ahn GN, Kim KN, Cha SH, Son CB, Lee J, Heo MS, Yeo IK, Lee NH, Jee YH, Kim JS, Heu MS, Jeon YJ (2007) Antioxidant activities of phlorotannins purified from Ecklonia cava on free radical scavenging using ESR and H2O2-mediated DNA damage. Eur Food Res Technol 226:71–79

    Article  CAS  Google Scholar 

  • Araujo JR, Goncalves P, Martel F (2011) Chemopreventive effect of dietary polyphenols in colorectal cancer cell line. Nutr Res 31:77–87

    Article  PubMed  CAS  Google Scholar 

  • Chang YC, Li PC, Chen BC, Chang MS, Wang JL, Chiu WT, Lin CH (2006) Lipoteichoic acid-induced nitric oxide synthase expression in RAW 264.7 macrophages is mediated by cyclooxygenase-2, prostaglandin E2, protein kinase A, p38 MAPK, and nuclear factor-κ B pathways. Cell Signal 18:1235–1243

    Article  PubMed  CAS  Google Scholar 

  • Cho JY, Baik KU, Jung JH, Park MH (2000) In vitro anti-inflammatory effects of cynaropicrin, a sesquiterpene lactone, from Saussurea lappa. Eur J Pharmacol 398:399–407

    Article  PubMed  CAS  Google Scholar 

  • Diaz RTA, Chabrillon M, Cabello-Pasini AC, Gomez-Pinchetti JL, Figueroa FL (2011) Characterization of polysaccharides from Hypnea spinella (Gigartinales) and Halopithys incurva (Ceramiales) and their effect on RAW 264.7 macrophage activity. J Appl Phycol 23:523–528

    Article  Google Scholar 

  • Dordevic TM, Marinkovic SSS, Brankovic SID (2010) Effect of fermentation on antioxidant properties of some cereals and pseudo cereals. Food Chem 119:957–963

    Article  CAS  Google Scholar 

  • Garrote G, Cruz JM, Moure A, Dominguez H, Parajo JC (2004) Antioxidant activity of byproducts from the hydrolytic processing of selected lignocellulosic materials. Trends Food Sci Technol 15:191–200

    Article  CAS  Google Scholar 

  • Heo SJ, Ko SC, Cha SH, Kang DH, Park HS, Choi YU, Kim D, Jung WK, Jeon YJ (2009) Effect of phlorotannins isolated from Ecklonia cava on melanogenesis and their protective effect against photo-oxidative stress induced by UV-B radiation. Toxicol In Vitro 23:1123–1130

    Article  PubMed  CAS  Google Scholar 

  • Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    Article  CAS  Google Scholar 

  • Ibanoglu S, Ibanoglu E (2001) Modelling of natural fermentation in cowpea using response surface methodology. J Food Eng 48:277–281

    Article  Google Scholar 

  • Jasna SD, Brunet C, Cetkovic G (2009) By-products of fruits processing as a source of phytochemicalas. Chem Ind Chem Eng Q 15:191–202

    Article  Google Scholar 

  • Kang KA, Lee KH, Park JW, Lee NH, Na HK, Surh YJ, You HJ, Chung MH, Hyun JW (2007) Triphlorethol-A induces heme oxygenase-1 via activation of ERK and NF-E2 related factor 2 transcription factor. FEBS Lett 581:2000–2008

    Article  PubMed  CAS  Google Scholar 

  • Kassim M, Achoui M, Mustafa MR, Mohd MA, Yusoff KM (2010) Ellagic acid, phenolic acids, and flavonoids in Malaysian honey extracts demonstrate in vitro anti-inflammatory activity. Nutr Res 30:650–659

    Article  PubMed  CAS  Google Scholar 

  • Kim HK, Cheon BS, Kim YH, Kim SY, Kim HP (1999) Effects of naturally occurring flavonoids on nitric oxide production in the macrophage cell line RAW 264.7 and their structure-activity relationship. Biochem Pharmacol 58:759–765

    Article  PubMed  CAS  Google Scholar 

  • Kim KN, Heo SJ, Song CB, Lee J, Heo MS, Yeo IK, Kang KA, Hyun JW, Jeon YJ (2006) Protective effect of Ecklonia cava enzymatic extracts on hydrogen peroxide-induced cell damage. Process Biochem 41:2393–2401

    Article  CAS  Google Scholar 

  • Kong CS, Kim JA, Yoon NY, Kim SK (2009) Induction of apoptosis by phloroglucinol derivative from Ecklonia cava in MCF-7 human breast cancer cells. Food Chem Toxicol 47:1653–1658

    Article  PubMed  CAS  Google Scholar 

  • Le QT, Li Y, Qian ZJ, Kim MM, Kim SK (2009) Inhibitory effects of polyphenols isolated from marine algae Ecklonia cava on histamine release. Process Biochem 44:168–176

    Article  CAS  Google Scholar 

  • Lee MH, Lee JM, Jun SH, Lee SH, Kim NW, Lee JH, Ko NY, Mun SH, Kim BK, Lim BO, Choi DK, Choi WS (2007) The anti-inflammatory effects of Pyrolae herba extract through the inhibition of the expression of inducible nitric oxide synthase (iNOS) and NO production. J Ethnopharmacol 112:49–54

    Article  PubMed  Google Scholar 

  • Lee SH, Han JS, Heo SJ, Hwang JY, Jeon YJ (2010) Protective effects of dieckol isolated from Ecklonia cava against high glucose-induced oxidative stress in human umbilical vein endothelial cells. Toxicol In Vitro 24:375–381

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Qian ZJ, Ryu B, Lee SH, Kim MM, Kim SK (2009) Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg Med Chem 17:1963–1973

    Article  PubMed  CAS  Google Scholar 

  • Lucas AD, Rodriguez L, Villasenor J, Fernandez FJ (2007) Fermentation of agro-food wastewaters by activated sludge. Water Res 41:1635–1644

    Article  PubMed  Google Scholar 

  • Ma Q, Kinneer K, Ye J, Chen BJ (2003) Inhibition of nuclear factor κB by phenolic antioxidants: interplay between antioxidant signaling and inflammatory cytokine expression. Mol Pharmacol 64:211–219

    Article  PubMed  CAS  Google Scholar 

  • Moure A, Cruz JM, Franco D, Dominguez JM, Sineiro J, Dominguez H, Nunez MJ, Nunez MJ, Parajo JC (2001) Natural antioxidants from residual sources. Food Chem 72:145–171

    Article  CAS  Google Scholar 

  • Nakagawa T (2011) Roles of prostaglandin E2 in the cochlea. Hearing Res 276:27–33

    Article  CAS  Google Scholar 

  • Park E, Ahn G, Yun JS, Kim MJ, Bing SJ, Kim DS, Lee J, Lee NH, Park JW, Jee Y (2010) Dieckol rescues mice from lethal irradiation by accelerating hemopoiesis and curtailing immunosuppression. Int J Radiat Biol 86:848–859

    PubMed  CAS  Google Scholar 

  • Park YG, Kang SK, Kim WJ, Lee YC, Kim CH (2004) Effect of TGF-β, IL-β and IL-6 alone or in combination, and tyrosine kinase inhibitor on cyclooxygenase expression, prostaglandin E2 production and bone resorption in mouse calvarial bone cells. Int J Biochem Cell Biol 36:2270–2280

    Article  PubMed  CAS  Google Scholar 

  • Peschel W, Rabaneda FS, Diekmann W, Plescher A, Gartzia I, Jimenez D, Raventos RL, Buxaderas S, Codina C (2006) An industrial approach in the search of natural antioxidants from vegetable and fruit wastes. Food Chem 97:137–150

    Article  CAS  Google Scholar 

  • Rioux LE, Turgeon SL, Beaulieu M (2009) Effect of season on the composition of bioactive polysaccharides from the brown seaweed Saccharina longicruris. Phytochemistry 70:1069–1075

    Article  PubMed  CAS  Google Scholar 

  • Ryu BM, Qian ZJ, Kim MM, Kim SK (2009) Differentiation of human osteosarcoma cells by isolated phlorotannins is subtly linked to COX-2, iNOS, MMPs, and MAPK signaling: implication for chronic articular disease. Chem Biol Interact 179:192–201

    Article  PubMed  CAS  Google Scholar 

  • Savonenko A, Munoz P, Melnikova T, Wang Q, Liang X, Breyer RM, Montine TJ, Kirkwood A, Andreasson K (2009) Impaired cognition, sensorimotor gating, and hippocampal long-term depression in mice lacking the prostaglandin E2 EP2 receptor. Exp Neurol 217:63–73

    Article  PubMed  CAS  Google Scholar 

  • Shim SY, To LQ, Lee SH, Kim SK (2009) Ecklonia cava extract suppresses the high-affinity IgE receptor, FcRIε expression. Food Chem Toxicol 47:555–560

    Article  PubMed  CAS  Google Scholar 

  • Smith JA, Das A, Ray SK, Banik NL (2012) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull 87:10–20

    Article  PubMed  CAS  Google Scholar 

  • Suh GH, Youn YK, Song HG, Rhee JE, Jung SE (2003) The effect of glutamine on inducible nitric oxide synthase gene expression in intestinal ischemia-reperfusion. Nutr Res 23:131–140

    Article  CAS  Google Scholar 

  • Vishchuk OS, Ermakova SP, Zvyagintseva TN (2011) Sulfated polysaccharides from brown seaweeds Sachcarina japonica and Undaria pinnatifida: isolation, structural characteristics, and antitumor activity. Carbohydr Res 346:2769–2776

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and Taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide 15:351–358

    Article  PubMed  CAS  Google Scholar 

  • Wijesinghe WAJP, Athukorala Y, Jeon YJ (2011) Effect of anticoagulative polysaccharide purified from enzyme-assistant extract of a brown seaweed Ecklonia cava on Wistar rats. Carbohydr Polym 86:917–921

    Article  CAS  Google Scholar 

  • Wijesinghe WAJP, Jeon YJ (2012) Exploiting biological activities of brown seaweed Ecklonia cava for potential industrial applications. Int JFood Sci Nutr 63:225–235

    Article  CAS  Google Scholar 

  • Wijesinghe WAJP, Won-Woo L, Young-Mog K, Young-Tae K, Se-Kwon K, Byong-Tae J, Jin-Soo K, Min-Soo H, Won-Kyo J, Ahn G, Lee KW, Jeon YJ (2012) Value-added fermentation of Ecklonia cava processing by-product and its antioxidant effect. J Appl Phycol 24:201–209

    Article  CAS  Google Scholar 

  • You Z, Luo C, Zhang W, Chen Y, He J, Zhao Q, Zuo R, Wu Y (2011) Pro- and anti-inflammatory cytokines expression in rat’s brain and spleen exposed to chronic mild stress: involvement in depression. Behav Brain Res 225:135–141

    Article  PubMed  CAS  Google Scholar 

  • Zhen HZ, Hwang IW, Chung SK (2009) Enhancing polyphenol extraction from unripe apples by carbohydrate-hydrolysing enzymes. J Zhejiang Univ Sci B 10:912–919

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by a grant from the Marine Bioprocess Research Center of the Marine Biotechnology Program funded by the Ministry of Land, Transport, and Maritime, Republic of Korea.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to You-Jin Jeon.

Additional information

W. A. J. P. Wijesinghe and Ginnae Ahn equally contributed to the work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wijesinghe, W.A.J.P., Ahn, G., Lee, WW. et al. Anti-inflammatory activity of phlorotannin-rich fermented Ecklonia cava processing by-product extract in lipopolysaccharide-stimulated RAW 264.7 macrophages. J Appl Phycol 25, 1207–1213 (2013). https://doi.org/10.1007/s10811-012-9939-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-012-9939-5

Keywords

Navigation