Anti-Diabetic and Anti-Inflammatory Potential of the Edible Brown Alga Hizikia Fusiformis

Journal of Food Biochemistry

Volumn 39, Issue 4, 2015, Pages 417-428

  Han, Yu Ran ^a   Ali, Md Yousof ^a   Woo, Mi Hee ^b   Jung, Hyun Ah ^c   Choi, Jae Sue ^a  

^a Pukyong National University   (South Korea)

^b Catholic University of Daegu   (South Korea)

^c Chonbuk National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BLOOD PRESSURE; COLUMN CHROMATOGRAPHY; DISEASES; FREE RADICALS; NITRIC OXIDE;

ANTI-INFLAMMATORIES; ANTI-INFLAMMATORY ACTIVITY; DOSE-DEPENDENT MANNER; HIGH BLOOD PRESSURES; INDUCIBLE NITRIC OXIDE SYNTHASE (INOS); INHIBITORY ACTIVITY; T-BUTYL HYDROPEROXIDE; TYROSINE NITRATION;

CHLORINE COMPOUNDS;

HIZIKIA FUSIFORMIS; PHAEOPHYCEAE;

EID: 84937517170     PISSN: 01458884     EISSN: 17454514     Source Type: Journal    
DOI: 10.1111/jfbc.12138     Document Type: Article

References (79)

1. Ahmad, F., Lonsidane, R.V., Bauer, T.L., Ohannesian, J.P., Marco, C.C. and Goldstein, B. 1997. Improved sensitivity to insulin in obese subjects following weight loss is accompanied by reduced protein-tyrosine phosphatases in adipose tissue. Metabolism 46, 1140-1145.
2. Arasaki, S. and Arasaki, T. 1983. Vegetables from the Sea, pp. 6-96, Japan Publications Inc., Tokyo, Japan.
3. Arroyo, P.L., Hatch-Pigott, V., Mower, H.F. and Cooney, R.V. 1992. Mutagenicity of nitric oxide and its inhibition by antioxidants. Mutat. Res. 281, 193-202.
4. Aulak, K.S., Miyagi, M., Yan, L., West, K.A., Massillon, D., Crabb, J.W. and Stuehr, D.J. 2001. Proteomic method identifies proteins nitrated during inflammatory challenge. Proc. Natl. Acad. Sci. U.S.A. 98, 12056-12061.
5. Beckman, J.S. and Koppenol, W.H. 1996. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am. J. Physiol. 271, 1424-1437.
6. Beckman, J.S., Beckman, T.W. and Chen, J. 1990. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U S A 87, 1620-1624.
7. Betteridge, D.J. 2000. What is oxidative stress? Metabolism 49, 3-8.
8. Bonizzi, G. and Karine, M. 2004. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25, 280-288.
9. Brownlee, M. 2001. Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813-820.
10. Cabrita, M.T., Vale, C. and Rauter, A.P. 2010. Halogenated compounds from marine algae. Mar. Drugs 8, 2301-2317.
11. Ceriello, A., Mercuri, F., Quagliaro, L., Assaloni, R., Motz, E., Tonutti, L. and Tabaga, C. 2001. Detection of nitrotyrosine in the diabetic plasma: Evidence of oxidative stress. Diabetologia 44, 834-838.
12. Chaturvedi, N. 2007. The burden of diabetes and its complications: Trends and implications. Diabetes Res. Clin. Pract. 76, 3-12.
13. Conforti, F., Sosa, S., Marrelli, M., Menichini, F., Statti, G.A., Uznnov, D.H., Tubaro, A. and Menichini, F. 2009. The protective ability of Mediterranean dietary plant against the oxidative damage: The role of radical oxygen species on inflammation and the polyphenol, flavonoid and sterol content. Food Chem. 112, 587-594.
14. Cosentino, F., Hishikawa, K., Katusic, Z.S. and Luscher, T.F. 1997. High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96, 25-28.
15. Cui, L., Na, M., Oh, H., Bae, E.Y., Jeong, D.G., Ryu, S.E., Kim, S., Kim, B.Y., Oh, W.K. and Ahn, J.S. 2006. Protein tyrosine phosphatase 1B inhibitors from Morus root bark. Bioorg. Med. Chem. Lett. 16, 1426-1429.
16. Dhargalkar, V.K. and Pereira, N. 2005. Seaweed: Promising plant of the millennium. Sci. Cult. 4, 60-66.
17. Ding, Y., Vaziri, N.D. and Coulson, R. 2000. Effect of simulated hyperglycemia, insulin, and glucagons on endothelial nitric oxide synthase expression. Am. J. Physiol. Endocrinol. Metab. 279, 11-17.
18. Dobashi, K., Nishino, T., Fujihara, M. and Nagumo, T. 1989. Isolation and preliminary characterization of fucose-containing sulfated polysaccharides with blood-anticoagulant activity from the brown seaweed Hizikia fusiforme. Carbohydr. Res. 194, 315-320.
19. Fisher, E.H., Charbonneau, H. and Tonks, N.K. 1991. Protein tyrosine phosphatases: A diverse family of intracellular and transmembrane enzymes. Science 253, 401-406.
20. Ganesan, P., Kumar, C.S. and Bhaskar, N. 2008. Antioxidant properties of methanol extract and its solvent fractions obtained from selected Indian red seaweeds. Bioresour. Technol. 99, 2717-2723.
21. Garrido, G., Gonzalez, D., Delporte, C., Backhouse, N., Quintaro, G., Nunez-Selles, A.J. and Morales, M.A. 2001. Analgesic and anti-inflammatory effects of Mangifera indica L. extract (Vimang). Phytother. Res. 15, 18-21.
22. Gryglewski, R.J., Palmer, R.M. and Moncada, S. 1986. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320, 454-456.
23. Güven, K.C., Percot, A. and Sezik, E. 2010. Alkaloids in marine algae. Mar. Drugs 8, 269-284.
24. Harris, R.C., McKanna, J.A., Akai, Y., Jacobson, H.R., Dubois, R.N. and Breyer, M.D. 1994. Cyclooxygenase-2 is associated with the macula densa of rat kidney and increases with salt restriction. J. Clin. Invest. 94, 2504-2510.
25. Heo, S.J., Hwang, J.Y., Choi, J.I., Ham, J.S., Kim, H.J. and Jeon, Y.J. 2009. Diphlorethohydroxycarmalol isolated from Ishige okamurae, brown algae, a potent α-glucosidase and α-amylase inhibitor, alleviates postprandial hyperglycemia in diabetic mice. Eur. J. Pharmacol. 615, 252-256.
26. Huang, G.J., Bhaskar Reddy, M.V., Kuo, P.C., Huang, C.H., Shih, H.C., Lee, E.J., Yang, M.L., Leu, Y.L. and Wu, T.S. 2012. A concise synthesis of viscolin, and its anti-inflammatory effects through the suppression of iNOS, COX-2, ERK phosphorylation and proinflammatory cytokines expressions. Eur. J. Med. Chem. 48, 371-378.
27. Ischiropoulos, H. 1998. Biological tyrosine nitration: A pathophysiological function of nitric oxide and reactive oxygen species. Arch. Biochem. Biophys. 356, 1-11.
28. Joubert, P.H., Venter, H.L. and Foukaridis, G.N. 1990. The effect of miglitol and acarbose after an oral glucose load: A novel hypoglycaemic mechanism. Br. J. Clin. Pharmacol. 30, 391-396.
29. Jung, B.M., Ahn, C.B., Kang, S.J., Park, J.H. and Chung, D.H. 2001. Effect of Hizikia fusiformis extracts on lipid metabolism and liver anti-oxidative enzyme activities in triton-induced hyperlipidemic rats. J. Korean Soc. Food Sci. Nutr. 30, 1184-1189.
30. Jung, H.A., Islam, M.N., Lee, C.M., Oh, S.H., Lee, S.H., Jung, J.H. and Choi, J.S. 2013a. Kinetics and molecular docking studies of an anti-diabetic complication inhibitor fucosterol from edible brown algae Eisenia bicyclis and Ecklonia stolonifera. Chem. Biol. Interact. 206, 55-62.
31. Jung, H.A., Jin, S.E., Ahn, B.R., Lee, C.M. and Choi, J.S. 2013b. Anti-inflammatory activity of edible brown alga Eisenia bicyclis and its constituents fucosterol and phlorotannins in LPS-stimulated RAW 264.7 macrophages. Food Chem. Toxicol. 59, 199-206.
32. Kang, H.S., Chung, H.Y., Kim, J.Y., Son, B.W., Jung, H.A. and Choi, J.S. 2004. Inhibitory phlorotannins from the edible brown alga Ecklonia stolonifera on total reactive oxygen species (ROS) generation. Arch. Pharm. Res. 27, 194-198.
33. Kargman, S., Charleson, S., Cartwright, M., Frank, J., Riendeau, D., Mancini, J., Evans, J. and O'Neill, G. 1996. Characterization of prostaglandin G/H synthase 1 and 2 in rat, dog, monkey, and human gastrointestinal tracts. Gastroenterology 111, 445-454.
34. Kim, S.A., Kim, J., Woo, M.K., Kwak, C.S. and Lee, M.S. 2005. Antimutagenic and cytotoxic effects of ethanol extracts from five kinds of seaweeds. J. Korean Soc. Food Sci. Nutr. 34, 451-459.
35. Kim, S.H., Lim, S.B., Ko, Y.H., Oh, C.K., Oh, M.C. and Park, C.S. 1994. Extraction yields of Hizikia fusiforme by solvents and their antimicrobial effects. Bull. Korean Fish. Soc. 27, 462-468.
36. Kim, S.M., Shang, Y.F. and Um, B.H. 2011. A preparative method for isolation of fucoxanthin from Eisenia bicyclis by centrifugal partition chromatography. Phytochem. Anal. 22, 322-329.
37. Koo, J.G., Choi, Y.S. and Kwak, J.K. 2001. Blood-anticoagulant activity of fucoidans from sporophylls of Undaria pinnatifida, Laminaria religiosa, Hizikia fusiforme and Sargassum fulvellum in Korea. J. Korean Fish. Soc. 34, 515-520.
38. Kooy, N.W., Royall, J.A., Ischiropoulos, H. and Beckman, J.S. 1994. Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radic. Biol. Med. 2, 149-156.
39. Koren, S. and Fantus, I.G. 2007. Inhibition of the protein tyrosine phosphatase PTP1B: Potential therapy for obesity, insulin resistance and type-2 diabetes mellitus. Best Pract. Res. Clin. Endocrinol. Metab. 21, 621-640.
40. Kuda, T., Tsunekawa, M., Goto, H. and Araki, Y. 2005. Antioxidant properties of four edible algae harvested in the Noto Peninsula, Japan. J. Food Compos. Anal. 18, 625-633.
41. Kusari, J., Kenner, K.A., Shu, K.I., Hill, D.E. and Henry, R.R. 1994. Skeletal muscle protein tyrosine phosphatase activity and tyrosine phosphatase 1B protein content are associated with insulin action and resistance. J. Clin. Invest. 93, 1156-1162.
42. Lebel, C.P. and Bondy, S.C. 1990. Sensitive and rapid quantification of oxygen reactive species formation in rat synaptosome. Neurochem. Int. 17, 435-440.
43. Lebovitz, H.E. 1997. Alpha-glucosidase inhibitors. Endocrinol. Metab. Clin. North Am. 26, 539-551.
44. Lee, J.R., Kim, J.K., Lee, S.J. and Kim, K.P. 2009. Role of protein tyrosine nitration in neurodegenerative disease and atherosclerosis. Arch. Pharm. Res. 32, 1109-1118.
45. Lee, Y.S., Shin, K.H., Kim, B.K. and Lee, S. 2004. Anti-diabetic activities of fucosterol from Pelvetia siliquosa. Arch. Pharm. Res. 27, 1120-1122.
46. Li, B., Wei, X.J., Sun, J.L. and Xu, S.Y. 2006. Structural investigation of a fucoidan containing a fucose-free core from the brown seaweed, Hizikia fusiforme. Carbohydr. Res. 341, 1135-1146.
47. Li, T., Zhang, X.D., Song, Y.W. and Liu, J.W. 2005. A microplate based screening method for alpha glucosidase inhibitors. Chin. J. Clin. Pharmacol. Ther. 10, 1128-1134.
48. Li, Y.X., Wijesekara, I., Li, Y. and Kim, S.K. 2011. Phlorotannins as bioactive agents from brown algae. Process. Biochem. 46, 2219-2224.
49. Liao, J.C., Deng, J.S., Lin, Y.C., Lee, C.Y., Lee, M.M., Hou, W.C., Huang, S.S. and Huang, G.J. 2012. Antioxidant, antinociceptive, and anti-inflammatory activities from Actinidia callosa var. callosa in vitro and in vivo. Evid. Based Complement. Alternat. Med. 1, 0-14.
50. Maeda, H., Hosokawa, M., Sashima, T., Takahasi, N., Kawada, T. and Miyashitam, K. 2006. Fucoxanthin and its metabolite, fucoxanthinol, suppress adipocyte differentiation in 3T3-L1 cells. Int. J. Mol. Med. 18, 147-152.
51. Maeda, H., Hosokawa, M., Sashima, T. and Miyashita, K. 2007. Dietary combination of fucoxanthin and fish oil attenuates the weight gain of white adipose tissue and decreases blood glucose in obese/diabetic KK-Ay mice. J. Agric. Food Chem. 55, 7701-7706.
52. Maeda, H., Hosokawa, M., Sashima, T., Murakami-Funayama, K. and Miyashitam, K. 2011. Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol. Med. Rep. 2, 897-902.
53. Manish, D., Uzma, S., Amit, K., Mohammad, I.S., Akhilesh, K.T., Arvind, K.S. and Atul, G. 2008. Synthesis, molecular docking and PTP1B inhibitory activity of functionalized 4, 5-dihydronaphthofurans and dibenzofurans. Med. Chem. 4, 18-24.
54. Melagraki, G., Afantitis, A., Igglessi-Markopoulos, O., Detsi, A., Koufaki, M., Kontogiorgis, S. and Hadjipavuou-Nitina, D.J. 2009. Synthesis and evaluation of the antioxidant and anti-inflammatory activity of novelcoumarin-3-aminoamides and their alpha-lipoic acid adducts. Eur. J. Med. Chem. 44, 3023-3026.
55. Miwa, M., Stuehr, D.J., Marletta, M.A., Wishnok, J.S. and Tannenbaum, S.R. 1987. Nitrosation of amines by stimulated macrophages. Carcinogenesis 8, 955-958.
56. Miyashita, K., Maeda, H., Okada, T., Abe, M. and Hosokawa, M. 2010. Anti-obesity and anti-diabetic effects of allenic carotenoid, fucoxanthin. Agro Food Ind. Hi Tec. 21, 24-27.
57. Moldoveanu, B., Otmishi, P., Jani, P., Walker, J., Sarmiento, X., Guardiola, J., Saad, M. and Yu, J. 2009. Inflammatory mechanisms in the lung. J. Inflamm. Res. 2, 1-11.
58. Mossman, T. 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
59. Nakagawa, T. and Yokozawa, T. 2002. Direct scavenging of nitric oxide and superoxide by green tea. Food Chem. Toxicol. 40, 1745-1750.
60. Nishino, H., Tokuda, H., Murakoshi, M., Satomoni, Y., Masuda, M., Onozuka, M., Yamaguchi, S., Takayasu, J., Tsuruta, J., Okada, M. etal. 2000. Cancer prevention by natural carotenoids. Biofactors 13, 89-94.
61. Ohshima, H. and Bartsch, H. 1994. Chronic infections and inflammatory processes as cancer risk factors: Possible role of nitric oxide in carcinogenesis. Mutat. Res. 305, 253-264.
62. Ong, C.K.S., Lirk, P., Tan, C.H. and Seymour, R.A. 2007. An evidence-based update on nonsteroidal anti-inflammatory drugs. Clin. Med. Res. 5, 19-34.
63. Paniagua-Michel, J., Capa-Robels, W., Olmos-Soto, J. and Gutierrez-Millan, L.E. 2009. The carotenogenesis pathway via the isoprenoid-beta-carotene interference approach in a new strain of Dunaliella salina isolated from Baja California Mexico. Mar. Drugs 7, 45-56.
64. Park, K.E., Jang, M.S., Lim, C.W., Kim, Y.K., Seo, Y.G. and Park, H.Y. 2005. Antioxidant activity on ethanol extract from boiled-water of Hizikia fusiformis. J. Korean Soc. Appl. Biol. Chem. 48, 435-439.
65. Rhabasa-Lhoret, R. and Chiasson, J.L. 2004. α-Glucosidase inhibitors. In International Textbook of Diabetes Mellitus, Vol 1, 3rd Ed. (R.A. Defronzo, E. Ferrannini, H. Keen and P. Zimmet, eds) pp. 901-914, John Wiley & Sons Ltd., Chichester, U.K.
66. Saltiel, A.R. and Kahn, C.R. 2001. Insulin signaling and the regulation of glucose and lipid metabolism. Nature 414, 799-806.
67. Salvemini, D., Wang, Z.Q., Stern, M.K., Currie, M.G. and Misko, T.P. 1998. Peroxynitrite decomposition catalysts: Therapeutics for peroxynitrite mediated pathology. Proc. Natl. Acad. Sci. U.S.A. 95, 2659-2663.
68. Sautebin, L. 2000. Prostaglandins and nitric oxide as molecular targets for anti-inflammatory therapy. Fitoterapia 71, 48-57.
69. 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. and Kim, Y.S. 2008. Anti-inflammatory effects of glycyrol isolated from Glycyrrhiza uralensis in LPS-stimulated RAW 264.7 macrophages. Int. J. Immunopharmacol. 8, 1524-1532.
70. Shiratori, K., Ohgami, K., Ilivea, I., Jin, X.H., Koyama, Y., Miyashita, K., Yoshida, K., Kase, S. and Ohno, S. 2005. Effects of fucoxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Exp. Eye Res. 81, 422-428.
71. Squadrito, G.L. and Pryor, W.A. 1995. The formation of peroxynitrite in vivo from nitric oxide and superoxide. Chem. Biol. Interact. 96, 203-206.
72. Stadtman, E.R. and Berlett, B.S. 1998. Reactive oxygen-mediated protein oxidation in aging and disease. Drug Metab. Rev. 30, 225-243.
73. Tonks, N.K. 2003. PTP1B: From the sidelines to the front lines! FEBS Lett. 546, 140-148.
74. Trachtman, H., Futterweit, S. and Crimmins, D.L. 1997. High glucose inhibits nitric oxide production in cultured rat mesangial cells. J. Am. Soc. Nephrol. 8, 1276-1282.
75. Vane, J.R. 1971. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nature 231, 232-235.
76. Walsh, N.C., Crotti, T.N., Goldring, S.R. and Gravallese, E.M. 2005. Rheumatic disease: The effects of inflammation on bone. Immunol. Res. 208, 228-251.
77. Wink, D.A., Kasprzak, K.S., Maragos, C.M., Elespuru, R.K., Misrs, M., Dunams, T.M., Cebula, T.A., Koch, W.H., Andrews, A.W. and Allen, J.S. 1991. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254, 1001-1003.
78. Yagihashi, N., Nishida, N. and Seo, H.G. 1996. Expression of nitric oxide synthase in macula densa in streptozotocin diabetic rats. Diabetologia 39, 793-799.
79. Yoo, M.S., Shin, J.S., Choi, H.E., Cho, Y.W., Bang, M.H., Baek, N.I. and Lee, K.T. 2012. 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 RAW 264.7 macrophages. Food Chem. 3, 967-975.