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Sea tangle (Saccharina japonica), an edible brown seaweed, improves serum lipid profiles and antioxidant status in rats fed high-fat and high-cholesterol diets

  • Hee Geun Jo
  • Min Ji Kim
  • Sun Hee CheongEmail author
Article

Abstract

In the present study, daily consumption of sea tangle (Saccharina japonica) was assessed for beneficial effects on blood lipid profiles and antioxidant status in rats fed high-fat and high-cholesterol diets (20% fat and 1% cholesterol, wt/wt) for 7 weeks. Thirty-six male Sprague-Dawley rats (average weight 170 g), 5-week old, were randomly divided into six groups: (1) a normal diet group (NOR), (2) a high-fat/high-cholesterol diet group (CON), and the high-fat/high-cholesterol diet combined with (3) 1% silk-shaped sea tangle powder (SST1), (4) 2% silk-shaped sea tangle powder (SST2), (5) 1% commercial sea tangle powder (CST1), and (6) 2% commercial sea tangle powder (wt/wt) (CST2) groups after a 2-week acclimation. The body weight gain and weight of adipose tissues in the CON group was increased compared with that of the NOR group, whereas those of the groups fed sea tangle decreased gradually. Serum triglyceride, total cholesterol, LDL-cholesterol levels, atherogenic index, and cardiac risk factors significantly and dose-dependently decreased in the sea tangle-fed groups when compared with the CON group, whereas serum HDL-cholesterol levels tended to increase in the sea tangle-fed groups. Moreover, serum and hepatic glutathione (GSH) levels and antioxidant enzyme activities such as superoxide dismutase (SOD) and catalase (CAT) were significantly improved in the sea tangle-fed groups compared with the CON group. In particular, serum LDL-cholesterol levels, GSH, SOD, and CAT activities were significantly and dose-dependently improved in the SST groups compared with the CST groups. Interestingly, sea tangle supplementation markedly reduced the hepatic lipid regulating enzyme activities including those of fatty acid synthase, HMG-CoA reductase, and acyl-coenzyme A: cholesterol acyltransferase. These results suggest that sea tangle, especially SST supplementation, may be potentially beneficial for preventing dyslipidemia-associated chronic diseases by improving blood lipid profiles and antioxidant properties due to its greater soluble alginate content and lower molecular weight.

Keywords

Silk-shaped sea tangle (Saccharina japonicaAlginate Molecular weight Serum biomarkers Blood lipid levels Antioxidant enzyme activities 

Notes

Funding information

This research was a part of the project titled “Development of the collecting treatment system and resources technology for Sagassum horneri,” funded by the Ministry of Oceans and Fisheries, Korea.

References

  1. Adeneye AA, Adeyemi OO, Agbaje EO, Banjo AA (2010) Evaluation of the toxicity and reversibility profile of the aqueous seed extract of Hunteria umbellata (K. Schum.) f. in rodents. Afr J Tradit Complement Altern Med 7:350–369CrossRefGoogle Scholar
  2. Ahn IS, Do MS, Choi BH, Kong CS, Kim SO, Han MS, Park KY (2006) Reduced leptin secretion by fucoidan-added Kochujang and anti-adipogenic effect of fucoidan in mouse 3T3-L1 adipocytes. Korean J Food Sci Nutr 11:31–35Google Scholar
  3. Ahn SM, Hong YK, Kwon GS, Sohn HY (2010) Evaluation of in-vitro anticoagulation activity of 35 different seaweed extracts. J Life Sci 20:1640–1647CrossRefGoogle Scholar
  4. AOAC (2000) Official methods of analysis of the Association of Official Analytical Chemists (17th edn). Arlington, VA, USAGoogle Scholar
  5. Calvert R, Schneeman BO, Satchithanandam S, Cassidy MM, Vahouny GV (1985) Dietary fiber and intestinal adaptation: effects on intestinal and pancreatic digestive enzyme activities. Am J Clin Nutr 41:1249–1256CrossRefGoogle Scholar
  6. Carl MN, Lakshmanan MR, Porter WW (1975) Fatty acid synthase from rat liver. Methods Enzymol 35:37–44CrossRefGoogle Scholar
  7. Chen J, Zhao H, Ma X, Han X, Luo L, Wang L, Han J, Liu B, Wang W (2012) The effects of jiang-zhi-ning and its main components on cholesterol metabolism. Evid Based Complement Alternat Med 2012:928234Google Scholar
  8. Chobanian AV (1991) Single risk factor intervention may be inadequate to inhibit atherosclerosis progression when hypertension and hypercholesterolemia coexist. Hypertension 18:130–131CrossRefGoogle Scholar
  9. Chtourou Y, Slima AB, Makni M, Gdoura R, Fetoui H (2015) Naringenin protects cardiac hypercholesterolemia-induced oxidative stress and subsequent necroptosis in rats. Pharmacol Rep 67:1090–1097CrossRefGoogle Scholar
  10. Douglas G, Channon KM (2014) The pathogenesis of atherosclerosis. Medicine 42:480–484CrossRefGoogle Scholar
  11. Erickson SK, Schrewsbery MA, Brooks C, Meyer DJ (1980) Rat liver acyl-coenzyme A:cholesterol acyltransferase: its regulation in vivo and some of properties in vitro. J Lipid Res 21:930–941Google Scholar
  12. Ha AW, Kim WK (2013) The effect of fucoxanthin rich power on the lipid metabolism in rats with a high fat diet. Nutr Res Pract 7:287–293CrossRefGoogle Scholar
  13. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  14. Idota Y, Kogure Y, Kato T, Ogawa M, Kobayashi S, Kakinuma C, Yano K, Arakawa H, Miyajima C, Kasahara F, Ogihara T (2016) Cholesterol-lowering effect of calcium alginate in rats. Biol Pharm Bull 39:62–67CrossRefGoogle Scholar
  15. Jeon SM, Kim HJ, Woo MN, Lee MK, Shin YC, Park YB, Choi MS (2010) Fucoxanthin-rich seaweed extract suppresses body weight gain and improves lipid metabolism in high-fat-fed C57BL/6J mice. Biotechnol J 5:961–969CrossRefGoogle Scholar
  16. Kang YM, Lee BJ, Kim JI, Nam BH, Cha JY, Kim YM, Ahn CB, Choi JS, Choi IS, Je JY (2012) Antioxidant effects of fermented sea tangle (Laminaria japonica) by Lactobacillus brevis BJ20 in individuals with high level of γ-GT: a randomized, double-blind, and placebo-controlled clinical study. Food Chem Toxicol 50:1166–1169CrossRefGoogle Scholar
  17. Kang MC, Wijesinghe WA, Lee SH, Kang SM, Ko SC, Yang X, Kang N, Jeon BT, Kim J, Lee DH, Jeon YJ (2013) Dieckol isolated from brown seaweed Ecklonia cava attenuates type ІІ diabetes in db/db mouse model. Food Chem Toxicol 53:294–298CrossRefGoogle Scholar
  18. Kanthe PS, Patil BS, Bagali S, Deshpande A, Shaikh GB, Aithala M (2012) Atherogenic index as a predictor of cardiovascular risk among women with different grades of obesity. Int J Collab Res Intern Med Public Health 4:1767–1774Google Scholar
  19. Kimura Y, Watanabe K, Okuda H (1996) Effects of soluble sodium alginate on cholesterol excretion and glucose tolerance in rats. J Ethnopharmacol 54:47–54CrossRefGoogle Scholar
  20. Ku CS, Yang Y, Park Y, Lee J (2013) Health benefits of blue-green algae: prevention of cardiovascular disease and nonalcoholic fatty liver disease. J Med Food 16:103–111CrossRefGoogle Scholar
  21. Larsson SC (2013) Dietary fats and other nutrients on stroke. Curr Opin Lipidol 24:41–48CrossRefGoogle Scholar
  22. Lee BJ, Senevirathne M, Kim JS, Kim YM, Lee MS, Jeong MH, Kang YM, Kim JI, Nam BH, Ahn CB, Je JY (2010) Protective effect of fermented sea tangle against ethanol and carbon tetrachloride-induced hepatic damage in Sprague-Dawley rats. Food Chem Toxicol 48:1123–1128CrossRefGoogle Scholar
  23. McKenney JM, Davidson MH, Jacobson TA, Guyton JR (2006) Final conclusions and recommendations of the National Lipid Association Statin Safety Assessment Task Force. Am J Cardiol 97:89C–94CCrossRefGoogle Scholar
  24. Miettinen TA, Puska P, Gylling H, Vanhanen H, Vartiainen E (1995) Reduction of serum cholesterol with sitostanol-ester margarine in a mildly hypercholesterolemic population. N Engl J Med Overseas Ed 333:1308–1312CrossRefGoogle Scholar
  25. Nishide E, Tsukayarna K, Uchida N, Nisizawa K (1984) Isolation of water-soluble alginate from brown algae. Hydrobiologia 116:557–562CrossRefGoogle Scholar
  26. Okai Y, Higashi-Okai K, Nakamura S (1993) Identification of heterogenous antimutagenic activities in the extract of edible brown seaweeds, Laminaria japonica (Makonbu) and Undaria pinnatifida (Wakame) by the umu gene expression system in Salmonella typhimurium (TA1535/pSK1002). Mutat Res 303:63–70CrossRefGoogle Scholar
  27. Park PJ, Kim EK, Lee SJ, Park SY, Kang DS, Jung BM, Kim KS, Je JY, Ahn CB (2009) Protective effects against H2O2-induced damage by enzymatic hydrolysates of an edible brown seaweed, sea tangle (Laminaria japonica). J Med Food 12:159–166CrossRefGoogle Scholar
  28. Pinto MC, Mata AM, Lopez-Barea J (1984) Reversible inactivation of Saccharomyces cerevisiae glutathione reductase under reducing conditions. Arch Biochem Biophys 228:1–12CrossRefGoogle Scholar
  29. Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, Eckel RH (2006) Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on obesity and heart disease from the obesity committee of the council on nutrition, physical activity, and metabolism. Circulation 14:898–918CrossRefGoogle Scholar
  30. Renn DW (1990) Seaweeds and biotechnology-inseparable companions. Hydrobiologia 204-205:7–13CrossRefGoogle Scholar
  31. Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354CrossRefGoogle Scholar
  32. Schröder H (2007) Protective mechanisms of the Mediterranean diet in obesity and type 2 diabetes. J Nutr Biochem 18:149–160CrossRefGoogle Scholar
  33. Shapiro DJ, Nordstrom JL, Mitschelen JJ, Rodwell VW, Schimke RT (1974) Micro assay for 3-hydroxy-3-methylglutaryl-CoA reductase in rat liver and in L-cell fibroblasts. Biochim Biophys Acta 370:369–377CrossRefGoogle Scholar
  34. Song Y, Wang Q, He Y, Ren D, Kow F, Li J, Liu S, Cong H (2017) The positive effects of fucoidans extracted from the brown seaweed Saccharina japonica on protection against CCl4-induced liver injury. J Appl Phycol 29:2077–2087CrossRefGoogle Scholar
  35. Stone NJ (1996) Lipid management: current diet and drug treatment options. Am J Med 101:40S–49SCrossRefGoogle Scholar
  36. Welker TL, Congleton JL (2003) Relationship between dietary lipid source, oxidative stress, and the physiological response to stress in sub-yearling Chinook salmon (Oncorhynchus tshawytscha). Fish Physiol Biochem 29:225–235CrossRefGoogle Scholar
  37. Woo MN, Jeon SM, Kim HJ, Lee MK, Shin SK, Shin YC, Park YB, Choi MS (2010) Fucoxanthin supplementation improves plasma and hepatic lipid metabolism and blood glucose concentration in high-fat fed C57BL/6N mice. Chem Biol Interact 186:316–322CrossRefGoogle Scholar
  38. Yang Y, Kim B, Park YK, Lee JY (2014) Effects of long-term supplementation of blue-green algae on lipid metabolism in C57BL/6J mice. J Nutrit Health Food Sci 1:6Google Scholar
  39. Yeo AR, Lee J, Tae IH, Park SR, Cho YH, Lee BH, Shin HC, Kim SH, Yoo YC (2012) Anti-hyperlipidemic effect of polyphenol extract (Seapolynol(™)) and dieckol isolated from Ecklonia cava in in vivo and in vitro models. Prev Nutr Food Sci 17:1–7CrossRefGoogle Scholar
  40. Yokota T, Nomura K, Nagashima M, Kamimura N (2016) Fucoidan alleviates high-fat diet-induced dyslipidemia and atherosclerosis in ApoE (shl) mice deficient in apolipoprotein E expression. J Nutr Biochem 32:46–54CrossRefGoogle Scholar
  41. You JS, Sung MJ, Chang KJ (2009) Evaluation of 8-week body weight control program including sea tangle (Laminaria japonica) supplementation in Korean female college students. Nutr Res Pract 3:307–314CrossRefGoogle Scholar
  42. Yuan YV, Walsh NA (2006) Antioxidant and antiproliferative activities of extracts from a variety of edible seaweeds. Food Chem Toxicol 44:1144–1150CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Marine Bio Food Science, College of Fisheries and Ocean ScienceChonnam National UniversityYeosuRepublic of Korea

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