Anti-inflammatory activity of edible brown alga Eisenia bicyclis and its constituents fucosterol and phlorotannins in LPS-stimulated RAW264.7 macrophages

Food and Chemical Toxicology

Volumn 59, Issue , 2013, Pages 199-206

  Jung, Hyun Ah ^a   Jin, Seong Eun ^b   Ahn, Bo Ra ^b   Lee, Chan Mi ^b   Choi, Jae Sue ^b,c  

^a Chonbuk National University   (South Korea)

^b Pukyong National University   (South Korea)

^c Dong Eui University   (South Korea)

Author keywords

Anti inflammation; Eisenia bicyclis; Fucosterol; Phlorotannin; ROS

Indexed keywords

7 PHLOROECKOL; ACETIC ACID ETHYL ESTER; ANTIINFLAMMATORY AGENT; BUTANOL; CYCLOOXYGENASE 2; DICHLOROMETHANE; DIECKOL; DIOXINODEHYDROECKOL; ECKOL; EISENIA BICYCLIS EXTRACT; FUCOSTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; METHANOL; NITRIC OXIDE; PHLOROFUCOFUROECKOL A; PHLOROGLUCINOL; PLANT EXTRACT; REACTIVE OXYGEN METABOLITE; TANNIN DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BROWN ALGA; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG ISOLATION; DRUG MECHANISM; DRUG STRUCTURE; EISENIA BICYCLIS; ENZYME INHIBITION; NONHUMAN; PROTEIN EXPRESSION; SOLVENT EFFECT;

2′,7′-DICHLORODIHYDROFLUORESCEIN; 2′,7′-DICHLORODIHYDROFLUORESCEIN DIACETATE; 2′,7′-DICHLOROFLUORESCEIN; 2-AMINO-5,6-DIHYDRO-6-METHYL-4H-1,3-THIAZINE HYDROCHLORIDE; 3-[4,5-DIMETHYLTHIAZOL-2-YL]-2,5-DIPHENYL TETRAZOLIUM BROMIDE; 6-HYDROXY-2,5,7,8-TETRAMETHYLCHROMAN-2-CARBOXYLIC ACID; AMT; ANTI-INFLAMMATION; COX-2; CYCLOOXYGENASE-2; DCF; DCFH; DCFH-DA; DEUTERATED DIMETHYLSULFOXIDE; DMEM; DMSO-D(6); DULBECCO'S MODIFIED EAGLE'S MEDIUM; EISENIA BICYCLIS; FBS; FETAL BOVINE SERUM; FUCOSTEROL; HORSERADISH PEROXIDASE; HRP; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; LIPOPOLYSACCHARIDE; LPS; MTT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NO; NOS; PHLOROTANNIN; POLYVINYLIDENE FLUORIDE; PVDF; REACTIVE OXYGEN SPECIES; ROS; T-BHP; TERT-BUTYLHYDROPEROXIDE; THIN LAYER CHROMATOGRAPHY; TLC; TROLOX;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE, TRANSFORMED; CELL SURVIVAL; CYCLOOXYGENASE 2; DIOXANES; DOWN-REGULATION; FUNCTIONAL FOOD; KELP; MACROPHAGES; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OSMOLAR CONCENTRATION; OXIDATIVE STRESS; PHLOROGLUCINOL; PLANT EXTRACTS; PLANT LEAVES; REACTIVE OXYGEN SPECIES; REPUBLIC OF KOREA; SOLVENTS; STIGMASTEROL;

EID: 84880125851     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.05.061     Document Type: Article

References (60)

1. Ahmed E., Nawaz S.A., Malik A., Choudhary I. Isolation and cholinesterase-inhibition studies of sterol from Haloxylon recuvum. Bioorg. Med. Chem. Lett. 2006, 16:573-580.
2. Ali A.E.G. Biological importance of marine algae. Saudi Pharm. J. 2010, 18:1-25.
3. Bang M.H., Kim H.H., Lee D.Y., Han M.W., Baek Y.S., Chung D.K., Baek N.I. Anti-osteoporotic activities of fucosterol from sea mustard (Undaria pinnatifida). Food Sci. Biotechnol. 2011, 20:343-347.
4. Barbosa J.P., Pereira R.C., Abrantes J.L., dos Santos C.C.C., Rebello M.A., Frugulhetti I.C.P.P., Teixeira V.L. In vitro antiviral diterpenes from the Brazilian brown alga Dictyota pfaffii. Planta Med. 2004, 70:856-860.
5. Chao W.W., Kuo Y.H., Lin B.F. Anti-inflammatory activity of new compounds from Andrographis paniculata by NF-κB transactivation inhibition. J. Agric. Food Chem. 2010, 58:2505-2512.
6. Conner E.M., Grisham M.B. Inflammation, free radicals and antioxidants. Nutrition 1996, 12:274-277.
7. Dembitsky V.M., Maoka T. Allenic and cumulenic lipids. Prog. Lipid Res. 2007, 46:328-375.
8. Elliott S.J., Eskin S.G., Schilling W.P. Effect of t-butyl-hydroperoxide on bradykinin-stimulated changes in cytosolic calcium in vascular endothelial cells. J. Biol. Chem. 1989, 264:3806-3810.
9. Fukuyama Y., Kodama M., Miura J., Kinzyo Z., Mori H., Nakayama Y., Takahashi M. Structure of an anti-plasmin inhibitor, eckol, isolated from the brown alga Ecklonia kurome Okamura and inhibitory activities of its derivatives on plasma plasmin inhibitors. Chem. Pharm. Bull. 1989, 37:349-353.
10. Ganchevakamenarska Z., Dimitrovadimitrova-konaklieva S., Stefanov K.L., Popov S.S. A comparative study on the sterol composition of some brown algae from the Black Sea. J. Ser. Chem. Soc. 2003, 68:269-275.
11. Guardia S.D., Valls R., Mesguiche V., Brunei J.M., Gulioli G. Enantioselective synthesis of (-)-bifuracadiol: a natural antitumor marine product. Tetrahedron Lett. 1999, 40:8359-8360.
12. Heo S.J., Yoon W.J., Kim K.N., Ahn G.N., Kang S.M., Kang D.H., Affan A., Oh C., Jung W.K., Jeon Y.J. Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide-stimulated RAW 264.7 macrophages. Food Chem. Toxicol. 2010, 48:2045-2051.
13. Iwai K. Antidiabetic and antioxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-Ay mice. Plant Foods Hum. Nutr. 2008, 63:163-169.
14. Jeong G.S., Li B., Lee D.S., Kim K.H., Lee I.K., Lee K.R., Kim Y.C. Cytoprotective and anti-inflammatory effects of spinasterol via the induction of heme oxygenase-1 in murine hippocampal and microglial cell lines. Int. Immunopharmacol. 2010, 10:1587-1594.
15. Joe M.J., Kim S.N., Choi H.Y., Shin W.S., Park G.M., Kang D.W., Kim Y.K. The inhibitory effects of eckol and dieckol from Ecklonia stolonifera on the expression of matrix metalloproteinase-I in human dermal fibroblasts. Biol. Pharm. Bull. 2006, 29:1735-1739.
16. Jung H.A., Hyun S.K., Kim H.R., Choi J.S. Angiotensin-converting enzyme I inhibitory activity of phlorotannins from Ecklonia stolonifera. Fish. Sci. 2006, 72:1292-1299.
17. Jung H.A., Oh S.H., Choi J.S. Molecular docking studies of phlorotannins from Eisenia bicyclis with BACE1 inhibitory activity. Bioorg. Med. Chem. Lett. 2010, 20:3211-3215.
18. Jung H.A., Yoon N.Y., Woo M.H., Choi J.S. Inhibitory activities of extracts from several kinds of seaweeds and phlorotannins from the brown alga Ecklonia stolonifera on glucose-mediated protein damage and rat lens aldose reductase. Fish. Sci. 2008, 74:1363-1365.
19. Kabe Y., Ando K., Hirao S., Yoshida M., Handa H. Redox regulation of inflammatory processes. Mem. Inst. Oswaldo Cruz. 2005, 100:5-9.
20. Kang H.S., Chung H.Y., Jung J.H., Son B.W., Choi J.S. A new phlorotannin from the brown alga Ecklonia stolonifera. Chem. Pharm. Bull. 2003, 51:1012-1014.
21. Kang H.S., Chung H.Y., Kim J.Y., Son B.W., Jung H.A., Choi J.S. Inhibitory phlorotannins from the edible brown alga Ecklonia stolonifera on total reactive oxygen species (ROS) generation. Arch. Pharm. Res. 2004, 27:194-198.
22. Kang H.S., Kim H.R., Byun D.S., Son B.W., Nam T.J., Choi J.S. Tyrosinase inhibitors isolated from the edible brown alga Ecklonia stolonifera. Arch. Pharm. Res. 2004, 27:1226-1232.
23. Kim A.R., Lee M.S., Shin T.S., Hua H., Jang B.C., Choi J.S., Byun D.S., Utsuki T., Ingram D., Kim H.R. Phlorofucofuroeckol A inhibits the LPS-stimulated iNOS and COX-2 expressions in macrophages via inhibition of NF-κB, Akt, and p38 MAPK. Toxicol. in Vitro 2011, 25:1789-1795.
24. Kim A.R., Shin T.S., Lee M.S., Park J.Y., Park K.E., Yoon N.Y., Kim J.S., Choi J.S., Jang B.C., Byun D.S., Park N.K., Kim H.R. Isolation and identification of phlorotannins from Ecklonia stolonifera with antioxidant and anti-inflammatory properties. J. Agric. Food Chem. 2009, 57:3483-3489.
25. Kim K.N., Heo S.J., Yoon W.J., Kang S.M., Ahn G., Yi T.H., Jeon Y.J. Fucoxanthin inhibits the inflammatory response by suppressing the activation of NF-κB and MAPKs in lipopolysaccharide-induced RAW 264.7 macrophages. Eur. J. Pharmacol. 2010, 15(649):369-375.
26. Kim M.M., Ta Q.V., Mendis E., Rajapakse N., Jung W.K., Byun H.K., Jeon Y.J., Kim S.K. Phlorotannins in Ecklonia cava extract inhibit matrix metalloproteinase activity. Life Sci. 2006, 79:1436-1443.
27. Kim S.M., Shang Y.F., Um B.H. A preparative method for isolation of fucoxanthin from Eisenia bicyclis by centrifugal partition chromatography. Phytochem. Anal. 2011, 22:322-329.
28. Kim Y.C., An R.B., Yoon N.Y., Nam T.J., Choi J.S. Hepatoprotective constituents of the edible brown alga Ecklonia stolonifera on tacrine-induced cytotoxicity in hep G2 cells. Arch. Pharm. Res. 2005, 28:1376-1380.
29. Kumar S.S., Kumar Y., Khan M.S.Y., Gupta V. New antifungal steroids from Turbinaria conoides (J. Agardh) Kutzing. Nat. Prod. Res. 2010, 24:1481-1487.
30. Lebel C.P., Bondy S.C. Sensitive and rapid quantitation of oxygen reactive species formation in rat synaptosomes. Neurochem. Int. 1990, 17:435-440.
31. Lee G., Na H.J., Namkoong S., Kwon H.J., Han S., Ha K.S., Kwon Y.G., Kim Y.M. 4-O-methylgallic acid down-regulates endothelial adhesion molecule expression by inhibiting NF-κB-DNA-binding activity. Eur. J. Pharmacol. 2006, 551:143-151.
32. Lee J.H., Park J.C., Choi J.S. The antioxidant activity of Ecklonia stolonifera. Arch. Pharm. Res. 1996, 19:223-227.
33. Lee S.H., Heo S.J., Hwang J.Y., Han J.S., Jeon Y.J. Protective effects of enzymatic digest from Ecklonia cava against high glucose-induced oxidative stress in human umbilical vein endothelial cells. J. Sci. Food Agric. 2010, 90:349-356.
34. Lee S.H., Lee Y.S., Jung S.H., Kang S.S., Shin K.H. Anti-oxidant activities of fucosterol from the marine algae Pelvetia siliquosa. Arch. Pharm. Res. 2003, 26:719-722.
35. Lee S.H., Li Y., Karadeniz F., Kim M.M., Kim S.K. α-Glucosidase and α-amylase inhibitory activities of phloroglucinal derivatives from edible marine brown alga, Ecklonia cava. J. Sci. Food Agric. 2009, 89:1552-1558.
36. Lee S.H., Park M.H., Heo S.J., Kang S.M., Ko S.C., Han J.S., Jeon Y.J. Dieckol isolated from Ecklonia cava inhibits α-glucosidase and α-amylase in vitro and alleviates postprandial hyperglycemia in streptozotocin-induced diabetic mice. Food Chem. Toxicol. 2010, 48:2633-2637.
37. Lee S.J., Bai S.K., Lee K.S., Namkoong S., Na H.J., Ha K.S., Han J.A., Yim S.V., Chang K., Kwon Y.G., Lee S.K., Kim Y.M. Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing IκB kinase dependent NF-κB activation. Mol. Cells 2003, 16:97-105.
38. Lee Y.S., Shin K.H., Kim B.K., Lee S. Anti-diabetic activities of fucosterol from Pelvetia siliquosa. Arch. Pharm. Res. 2004, 27:1120-1122.
39. Li Y., Qian Z.J., Ryu B., Lee S.H., Kim M.M., Kim S.K. Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg. Med. Chem. 2009, 17:1963-1973.
40. MacMicking J., Xie Q.W., Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 1997, 15:323-350.
41. Mossman T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assays. J. Immunol. Methods 1983, 65:55-63.
42. Myung C.S., Shin H.C., Bao H.Y., Yeo S.J., Lee B.H., Kang J.S. Improvement of memory by dieckol and phlorofucofuroeckol in ethanol-treated mice: possible involvement of the inhibition of acetylcholinesterase. Arch. Pharm. Res. 2005, 28:691-698.
43. Nagayama K., Shibata T., Fujimoto K., Honjo H., Nakamura T. Algicidal effect of phlorotannins from the brown alga Ecklonia kurome on red tide microalgae. Aquaculture 2003, 218:601-611.
44. Nisizawa K., Noda H., Kikuchi R., Watanabe T. The main seaweed foods in Japan. Hydrobiology 1987, 151(152):5-29.
45. Noda H., Amano H., Arashima K., Hashimoto S., Nisizawa K. Studies on the antitumor activity of marine algae. Nippon Suisan Gakk. 1989, 55:1259-1264.
46. Okada Y., Ishimaru A., Suzuki R., Okuyama T. A new phloroglucinol derivative from the brown alga Eisenia bicyclis: potential for the effective treatment of diabetic complications. J. Nat. Prod. 2004, 67:103-105.
47. Perry N.B., Bluent J.W., Munro M.H.G. A cytotoxic and antifungal l,4-naphthoquinone and related compounds from A New Zealand brown alga Landsburgia Quercifolia. J. Nat. Prod. 1991, 54:978-985.
48. Ryu B., Li Y., Qian Z.J., Kim M.M., Kim S.K. 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. 2009, 179:192-201.
49. Sánchez-Machado D.I., López-Hernández J., Paseiro-Losada P., López-Cervantes J. An HPLC method for the quantification of sterols in edible seaweeds. Biomed. Chromatogr. 2004, 18:183-190.
50. Sharif O., Bolshakov V.N., Raines S., Newham P., Perkins N.D. Transcriptional profiling of the LPS induced NF-κB response in macrophages. BMC Immunol. 2007, 8:1-17.
51. Sheu J.H., Wang G.H., Sung P.J., Chiu Y.H., Duh C.Y. Cytotoxic sterols from the formosan brown alga Turbinaria ornata. Planta Med. 1997, 63:571-572.
52. Shibata T., Nagayama K., Tanaka R., Yamaguchi K., Nakamura T. Inhibitory effects of brown algal phlorotannins on secretory phospholipase A2s, lipoxygenases and cyclooxygenases. J. Appl. Phycol. 2003, 15:61-66.
53. Shin E.M., Zhou H.Y., Guo L.Y., Kim J.A., Lee S.H., Merfort I., Kang S.S., Kim H.S., Kim S., Kim Y.S. Anti-inflammatory effects of glycyrol isolated from Glycyrrhiza uralensis in LPS-stimulated RAW 264.7 macrophages. Int. Immunopharmacol. 2008, 8:1524-1532.
54. Shiratori K., Ohgami K., Ilieva I., Jin X.H., Koyama Y., Miyashita K., Yoshida K., Kase S., Ohno S. Effects of fucoxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Exp. Eye Res. 2005, 81422-81428.
55. Sugiura Y., Matsuda K., Yamada Y., Nishikawa M., Shioya K., Katsuzaki H., Imai K., Amano H. Isolation of a new antiallergic phlorotannin, phlorofucofuroeckol-B, from an edible brown alga, Eisenia arborea. Biosci. Biotechnol. Biochem. 2006, 70:2807-2811.
56. Terasaki M., Hirose A., Narayan B., Baba Y., Kawagoe C., Yasui H., Saga N., Hosokawa M., Miyashita K. Evaluation of recoverable functional lipid components with special reference to fucoxanthin and fucosterol contents of several brown seaweeds of Japan. J. Phycol. 2009, 45:974-980.
57. Valerio M., Liu H.B., Heffner R., Zivadinov R., Ramanathan M., Weinstock-Guttman B., Awad A.B. Phytosterols ameliorate clinical manifestations and inflammation in experimental autoimmune encephalomyelitis. Inflamm. Res. 2011, 60:457-465.
58. Yoo M.S., Shin J.S., Choi H.E., Cho Y.W., Bang M.H., Baek N.I., Lee K.T. Fucosterol isolated from Undaria pinnatifida inhibits lipopolysaccharide-induced production of nitric oxide and pro-inflammatory cytokines via the inactivation of nuclear factor-κB and p38 mitogen-activated protein kinase in RAW264.7 macrophages. Food Chem. 2012, 135:967-975.
59. Yoon N.Y., Chung H.Y., Kim H.R., Choi J.S. Acetyl- and butyrylcholinesterase inhibitory activities of sterols and phlorotannins from Ecklonia stolonifera. Fish. Sci. 2008, 74:200-207.
60. Yoon N.Y., Kim H.R., Chung H.Y., Choi J.S. Anti-hyperlipidemic effect of an edible brown algae, Ecklonia stolonifera, and its constituents on poloxamer 407-induced hyperlipidemic and cholesterol-fed rats. Arch. Pharm. Res. 2008, 31:1564-1571.