Journal of the East Asian Society of Dietary Life (동아시아식생활학회지)

The East Asian Society of Dietary Life (동아시아식생활학회)
권호 표지
DOI QR코드

DOI QR Code

Anti-inflammatory Effects of Fermented Laminaria japonica and Hizikia fusiforme Water Extracts with Probiotics in LPS-stimulated RAW264.7 Macrophage Cell Line

RAW 264.7 대식세포에서 유산균으로 발효한 다시마와 톳의 항염증 효과

  • Hwang, Yeon-ji (Dept. of Food Science and Nutrition, Jeju National University) ;
  • Chae, Insook (Dept. of Food Science and Nutrition, Jeju National University) ;
  • Lee, Yunkyoung (Dept. of Food Science and Nutrition, Jeju National University)
  • 황연지 (제주대학교 식품영양학과) ;
  • 채인숙 (제주대학교 식품영양학과) ;
  • 이윤경 (제주대학교 식품영양학과)
  • Received : 2016.08.18
  • Accepted : 2017.02.17
  • Published : 2017.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

This study was conducted to investigate alterations of seaweed composition upon Lactobacillus rhamnosus GG (LGG) fermentation as well as potential anti-inflammatory effects and mechanism (s) of water extracts and fermented water extracts of Laminaria japonica (LJ) and Hizikia fusiforme (HF) in lipopolysaccharide (LPS)-stimulated RAW264.7 macrophages. Total polyphenol, total sugar, and reducing sugar contents were measured in LJ and HF water extracts before and after fermentation by LGG. Alterations of inflammatory cytokine levels in cell culture media were measured by ELISA, and levels of phosphorylation of c-jun NH2-terminalkinase (JNK) and extra cellular signal regulated kinase (ERK) were examined by Western blot analysis. LGG fermentation of LJ and HF altered total polyphenol and sugar contents in water extracts of LJ and HF. LPS-induced production of pro-inflammatory cytokines such as IL-6 and $TNF-{\alpha}$ was significantly reduced by HF-f compared to control in RAW264.7 cells. Consistent with reduction of anti-inflammatory cytokine, interleukin (IL)-6, and tumor necrosis factor $(TNF)-{\alpha}$ levels by HF-f, HF-f also significantly reduced phosphorylation of ERK and JNK in LPS-stimulated RAW264.7 cells. In addition, LJ-f and HF also significantly reduced phosphorylation of JNK and ERK induced by LPS in RAW264.7 cells. Overall, our result suggests that HF-f among the four tested seaweed extracts is the most potent anti-inflammatory agent, and its mechanism of action is partially mediated by reduction of JNK and ERK phosphorylation as well as IL-6 and $TNF-{\alpha}$ production in LPS-stimulated RAW264.7 cells.

Keywords

References

  1. Anisowicz A, Messineo M, Lee SW, Sager R (1991) An NF-Kappa B-like transcription factor mediates IL-1/TNF-alpha induction of Gro in human fibroblasts. J Immunol 147: 520-527.
  2. Bae H, Kim Y (2010) Improvement of the functional qualities of sea tangle extract through fermentation by Aspergillus oryzae. Fisheries Aquatic Scis 13: 12-17. https://doi.org/10.5657/fas.2010.13.1.012
  3. Baker RG, Hayden MS, Ghosh S (2011) NF-${\kappa}B$, inflammation, and metabolic disease. Cell Met 13: 11-22. https://doi.org/10.1016/j.cmet.2010.12.008
  4. Chandini SK, Ganesan P, Bhaskar N (2008) In vitro antioxidant activities of three selected brown seaweeds of India. Food Chem 107: 707-713. https://doi.org/10.1016/j.foodchem.2007.08.081
  5. Chen I, Ng C, Wang C, Chang T (2009) Lactic fermentation and antioxidant activity of Zingiberaceae plants in Taiwan. Int J Food Sci Nutr 60: 57-66. https://doi.org/10.1080/09637480802375531
  6. Deville C, Damas J, Forget P, Dandrifosse G, Peulen O (2004) Laminarin in the dietary fibre concept. J Sci Food Agric 84: 1030-1038. https://doi.org/10.1002/jsfa.1754
  7. Dogne J, Hanson J, Supuran C, Pratico D (2006) Coxibs and cardiovascular side-effects: From light to shadow. Curr Pharm Des 12: 971-975. https://doi.org/10.2174/138161206776055949
  8. Eom S, Kang Y, Park J, Yu D, Jeong E, Lee M, Kim Y (2011) Enhancement of polyphenol content and antioxidant activity of brown alga Eisenia bicyclis extract by microbial fermentation. Fisheries Aquatic Sci 14: 192-197. https://doi.org/10.5657/FAS.2011.0192
  9. Eom S, Lee B, Kim Y (2010) Effect of yeast fermentation on the antioxidant and anti-inflammatory activity of sea tangle water extract. Korean J Fisheries Aquatic Sci 43: 117-124. https://doi.org/10.5657/kfas.2010.43.2.117
  10. Folin O, Denis, W (1912) On phosphotungstic-phosphomolybdic compounds as color reagents. J Biol Chem 12(2): 239-243.
  11. Gomes AM, Malcata FX (1999) Bifidobacterium spp. and Lactobacillus acidophilus: Biological, biochemical, technological and therapeutical properties relevant for use as probiotics. Trends Food Sci Technol 10: 139-157. https://doi.org/10.1016/S0924-2244(99)00033-3
  12. Gomez-Ordonez E, Jimenez-Escrig A, Ruperez P (2010) Dietary fibre and physicochemical properties of several edible seaweeds from the northwestern Spanish coast. Food Res Int 43: 2289-2294. https://doi.org/10.1016/j.foodres.2010.08.005
  13. Hwang YJ (2016) Anti-inflammatory effect and its mechanism (s) of Laminaria japonica and Hizikia fusiforme fermented extracts by Lactobacillus rhamnosus GG. MS Thesis, Jeju National University. Jeju. pp 19-20.
  14. Ishihara K, Hirano T (2002) IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 13: 357-368. https://doi.org/10.1016/S1359-6101(02)00027-8
  15. Jimenez-Escrig A, Sanchez-Muniz F (2000) Dietary fibre from edible seaweeds: Chemical structure, physicochemical properties and effects on cholesterol metabolism. Nutr Res 20: 585-598. https://doi.org/10.1016/S0271-5317(00)00149-4
  16. Kang B, Kim K, Kim M, Bark S, Pak W, Kim B, Ahn N, Choi Y, Ahn D (2014) Anti-inflammatory activity of an ethanol extract of Laminaria japonica root on lipopolysaccharideinduced inflammatory responses in RAW 264.7 cells. Korean J Food Sci Tech 46: 729-733. https://doi.org/10.9721/KJFST.2014.46.6.729
  17. Kim Y, Shin D, Jeong M, Oh H, Kang T (1993) Changes in quality characteristics of traditional Kochujang during fermentation. Korean J Food Sci Tech 25: 724-729.
  18. Kown MS, Mun OJ, Bae MJ, Lee SG, Kim M, Lee SH, Yu KH, Kim YY, Kong CS (2015) Anti-inflammatory activity of ethanol extracts from Hizikia fusiformis fermented with lactic acid bacteria in LPS-stimulated RAW264.7 macrophages. J Korean Soc Food Sci Nutr 44:1450-1457. https://doi.org/10.3746/jkfn.2015.44.10.1450
  19. Lawrence T, Gilroy DW (2007) Chronic inflammation: A failure of resolution? Int J Exp Pathol 88: 85-94.
  20. Lee NY (2013) Antioxidant effect and tyrosinase inhibition activity of seaweeds ethanol extracts. J Korean Soc Food Sci Nutr 42: 1893-1898. https://doi.org/10.3746/jkfn.2013.42.12.1893
  21. Lee W, Oh JY, Kim E, Kang N, Kim K, Ahn G, Jeon Y (2016) A prebiotic role of Ecklonia cava improves the mortality of edwardsiellatarda-infected zebrafish models via regulating the growth of lactic acid bacteria and pathogen bacteria. Fish Shellfish Immunol 54: 620-628. https://doi.org/10.1016/j.fsi.2016.05.018
  22. Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K (2007) Effect of medium-chain triacylglycerols on antiobesity effect of fucoxanthin. J Oleo Sci 56: 615-621. https://doi.org/10.5650/jos.56.615
  23. Makins R, Ballinger A (2003) Gastrointestinal side effects of drugs. Exp Opin Drug Safety 2: 421-429. https://doi.org/10.1517/14740338.2.4.421
  24. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31: 426-428. https://doi.org/10.1021/ac60147a030
  25. Miyata M, Koyama T, Kamitani T, Toda T, Yazawa K (2009) Anti-obesity effect on rodents of the traditional Japanese food, tororokombu, shaved Laminaria. Biosci Biotechnol Biochem 73: 2326-2328. https://doi.org/10.1271/bbb.90344
  26. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63. https://doi.org/10.1016/0022-1759(83)90303-4
  27. Nwosu F, Morris J, Lund VA, Stewart D, Ross HA, McDougall GJ (2011) Anti-proliferative and potential anti-diabetic effects of phenolic-rich extracts from edible marine algae. Food Chem 126: 1006-1012. https://doi.org/10.1016/j.foodchem.2010.11.111
  28. O'Sullivan L, Murphy B, McLoughlin P, Duggan P, Lawlor PG, Hughes H, Gardiner GE (2010) Prebiotics from marine macroalgae for human and animal health applications. Marine Drugs 8: 2038-2064. https://doi.org/10.3390/md8072038
  29. Oh J, Lee Y (2015) Effects of water and ethanol extracts from four types of domestic seaweeds on cell differentiation in 3T3-L1 cell lin. J East Asian Soc Dietary Life 25: 990-998. https://doi.org/10.17495/easdl.2015.12.25.6.990
  30. Oh J, Kim J, Lee Y (2016) Anti-inflammatory and anti-diabetic effects of brown seaweeds in high-fat diet-induced obese mice. Nutr Res Prac 10: 42-48. https://doi.org/10.4162/nrp.2016.10.1.42
  31. Park HY, Han MH, Park C, Jin C, Kim G, Choi I, Kim ND, Nam T, Kwon TK, Choi YH (2011) Anti-inflammatory effects of fucoidan through inhibition of NF-${\kappa}B$, MAPK and Akt activation in lipopolysaccharide-induced BV2 microglia cells. Food Chem Tox 49: 1745-1752. https://doi.org/10.1016/j.fct.2011.04.020
  32. Ren K, Torres R (2009) Role of interleukin-$1{\beta}$ during pain and inflammation. Brain Res Rev 60: 57-64. https://doi.org/10.1016/j.brainresrev.2008.12.020
  33. Shah N (2000) Probiotic bacteria: Selective enumeration and survival in dairy foods. J Dairy Sci 83: 894-907. https://doi.org/10.3168/jds.S0022-0302(00)74953-8
  34. Shon JH, Kang DY, Oh HC, Jung BM, Kim MH, Shin MO, Bae SJ (2006) The effects on antimicrobial and cytotoxicity of Hijikia Fusiformis fraction. Korean J Nutr 39: 444-450.
  35. Wada T, Penninger JM (2004) Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23: 2838-2849. https://doi.org/10.1038/sj.onc.1207556
  36. Wolfrom ML, BeMiller JN (1963) Methods in Carbohydrate Chemistry: Reactions of Carbohydrates. Academic Press.
  37. Zhang G, Ghosh S (2000) Molecular mechanisms of NF-kappaB activation induced by bacterial lipopolysaccharide through toll-like receptors. J Endotoxin Res 6: 453-457. https://doi.org/10.1177/09680519000060060701

Cited by

  1. 흰 쥐에서 복합 유산균과 다시마가 항비만 및 장내 미생물에 미치는 영향 vol.27, pp.12, 2017, https://doi.org/10.5352/jls.2017.27.12.1421
  2. 다시마 물 추출액과 발효액의 항산화 및 항염증 활성 vol.29, pp.5, 2017, https://doi.org/10.5352/jls.2019.29.5.596