Abstract
Eucheuma denticulatum is a red edible seaweed that grows in the East Malaysia coastal region. The objective of this study was to investigate the α-amylase, antioxidant and anti-inflammatory activities of E. denticulatum ethanol extract and its three fractions (n-hexane, ethyl acetate and acetone). α-Amylase activity was assessed by dinitrosalicylic acid (DNS) assay, while the antioxidant property was determined by oxygen radical absorbance capacity (ORAC) analysis. The anti-inflammatory effects of the seaweed samples were evaluated by nitric oxide (NO), interleukin-6 (IL-6), interleukin-1 (IL-1), tumor necrosis factor-alpha (TNF-α), and monocyte chemoattractant protein-1 (MCP-1) activities on the interferon-gamma/lipopolysaccharide (IFN-γ/LPS)-stimulated murine macrophage cell line (RAW 264.7) using Griess reaction and immunoassays, respectively. At 10 mg mL−1, E. denticulatum ethanol extract and three fractions inhibited α-amylase activities at variable levels. The highest (67 %) inhibition of α-amylase enzyme was by the ethanol crude extract. The three fractions showed inhibition with a mean of 42 %. Crude ethanol extracts also exhibited higher antioxidant capacity (36,400 ± 23.5 mol Trolox equivalent (TE) (100 g)−1) when compared to the fractions. Crude extract and fractions (1–100 μg mL−1), also exhibited anti-inflammatory activity without showing any cytotoxic effect to RAW 264.7 cells. The present study suggests that E. denticulatum has the potential to be a promising source of effective functional metabolite. An extensive research on the edible varieties would contribute to a better understanding of their importance as functional food.
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References
Ask EI, Azanza RV (2002) Advances in cultivation technology of commercial eucheumatoid species: a review with suggestions for future research. Aquaculture 206:257–277
Balasubramaniam V, Mustar S, Khalid NM, Rashed AA, Noh MFM, Wilcox MD, Chater PI, Brownlee IA, Pearson JP (2013) Inhibitory activities of three Malaysian edible seaweeds on lipase and alpha-amylase. J Appl Phycol 25:1405–1412
Chen H (2006) Cellular inflammatory responses: novel insights for obesity and insulin resistance. Pharmacol Res 53:469–477
Chensue SW, Warmington KS, Ruth JH, Sanghi PS, Lincoln P, Kunkel SL (1996) Role of monocyte chemoattractant protein-1 (MCP-1) in Th1 (mycobacterial) and Th2 (schistosomal) antigen-induced granuloma formation: relationship to local inflammation, Th cell expression, and IL-12 production. J Immunol 157:4602–4608
Chin YX, Lim PE, Maggs CA, Phang SM, Sharifuddin Y, Green BD (2014) Anti-diabetic potential of selected Malaysian seaweeds. J Appl Phycol. doi:10.1007/s10811-014-0462-8:1-12
Colombo ML, RisÈ P, Giavarini F, Angelis L, Galli C, Bolis CL (2006) Marine macroalgae as sources of polyunsaturated fatty acids. Plant Foods Hum Nutr 61:64–69
D’Orazio N, Gammone MA, Gemello E, De Girolamo M, Cusenza S, Riccioni G (2012) Marine bioactives: pharmacological properties and potential applications against inflammatory diseases. Mar Drugs 10:812–833
Fasshauer M, Kralisch S, Klier M, Lossner U, Bluher M, Klein J, Paschke R (2003a) Adiponectin gene expression and secretion is inhibited by interleukin-6 in 3T3–L1 adipocytes. Biochem Biophys Res Commun 301:1045–1050
Fasshauer M, Klein J, Lossner U, Paschke R (2003b) Interleukin-6 mRNA expression is stimulated by insulin, isoproterenol, tumor necrosis factor alpha, growth hormone, and IL-6 in 3T3–L1 adipocytes. Horm Metab Res 35:147–152
Glombitza KW, Knoss W (1992) Sulphated phlorotannins from the brown alga Pleurophycus gardneri. Phytochem 31:279–281
Godbout A, Chiasson JL (2007) Who should benefit from the use of alpha-glucosidase inhibitors? Curr Diab Rep 7:333–339
Han S, Sung KH, Yim D, Lee S, Cho K, Lee CK, Ha NJ, Kim K (2002) Activation of murine macrophage cell line RAW 264.7 by Korean propolis. Arch Pharm Res 25:895–902
Hasnain SZ, Borg DJ, Harcourt BE, Tong H, Sheng YH, Ng CP, Das I, Wang R, Chen AC et al (2014) Glycemic control in diabetes is restored by therapeutic manipulation of cytokines that regulate beta cell stress. Nat Med 20:417–1426
Heo SJ, Yoon WJ, Kim KN, Ahn GN, Kang SM, Kang DH et al (2010) Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide stimulated RAW 264.7 macrophages. Food Chem Toxicol 48:2045–2051
Kern PA, Ranganathan S, Li C, Wood L, Ranganatha G (2001) Adipose tissue necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280:745–751
Kim HK, Cheon BS, Kim SY, Kim HP (1999) Effects of naturally occuring flavonoids on nitric oxide production in the macrophage cell line RAW264.7 and their structure-activity relationship. Biochem Pharmacol 58:759–765
Kim KY, Nguyen TH, Kurihara H, Kim SM (2010) Alpha-glucosidase inhibitory activity of bromophenol purified from the red alga Polyopes lancifolia. J Food Sci 75:145–150
Kumar SA, Brown L (2013) Seaweeds as potential therapeutic interventions for the metabolic syndrome. Rev Endocr Metab Disord 14:299–308
Lee SH, Li Y, Karadeniz F, Kim MM, Kim SK (2009) α-Glucosidase and α-amylase inhibitory activities of phloroglucinal derivatives from edible marine brown alga, Ecklonia cava. J Sci Food Agric 89:1552–1558
Lee HJ, Hyun EA, Yoon WJ, Kim BH, Rhee MH, Kang HK, Cho JY, Yoo ES (2006) In- vitro anti-inflammatory and anti-oxidative effects of Cinnamomum camphora extracts. J Ethnopharmacol 103:208–216
Lee YH, Pratley RE (2005) The evolving role of inflammation in obesity and the metabolic syndrome. Curr Diabetes Rep 5:70–75
Liu H, Gu L (2012) Phlorotannins from brown algae (Fucus vesiculosus) inhibited the formation of advanced glycation endproducts by scavenging reactive carbonyls. J Agric Food Chem 60:1326–1334
Lordan S, Ross RP, Stanton C (2011) Marine bioactives as functional food ingredients: Potential to reduce the incidence of chronic diseases. Marine Drugs 9:1056–1100
Lordan S, Smyth TJ, Soler-Vila A, Stanton C, Ross RP (2013) The α-amylase and α-glucosidase inhibitory effects of Irish seaweed extracts. Food Chem 141:2170–2176
Maeda H, Tsukui T, Sashima T, Hosokawa M, Miyashita K (2008) Seaweed carotenoid, fucoxanthin, as a multi-functional nutrient. Asia Pac J Clin Nutr 17:196–199
Maeda H, Hosokawa M, Sashima T, Miyashita K (2007) Dietary combination of fucoxanthin and fish oil attenuates the weight gain of white adipose tissues and decreases blood glucose in obese/diabetic KK-A mice. J Agric Food Chem 55:7701–7706
Marcovecchio M, Mohn A, Chiarelli F (2005) Type 2 diabetes mellitus in children and adolescents. J Endocrinol Invest 28:853–863
Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Ming CH (2008) Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. J Appl Phycol 20:367–373
McCauley JI, Meyer BJ, Winberg PC, Ranson M, Skropeta D (2015) Selecting Australian marine macroalgae based on the fatty acid composition and anti-inflammatory activity. J Appl Phycol. doi:10.1007/s10811-014-0465-5:1-11
Miyashita K (2009) Function of marine carotenoids. Forum Nutr 61:136–146
Mohamed F, Namitha KK, Chidambara MKN, Mahadeva SM, Sarada R, Salma K, Subbarao PV, Ravishankar GA (2005) Chemical composition, iron bioavailability, and antioxidant activity of Kappaphycus alvarezzi (Doty). J Agric Food Chem 53:792–797
Motshakeri M, Ebrahimi M, Goh YM, Matanjun P, Mohamed S (2013) Sargassum polycystum reduces hyperglycaemia, dyslipidaemia and oxidative stress via increasing insulin sensitivity in a rat model of type 2 diabetes. J Sci Food Agr 93:1772–1778
Munro MHG, Blunt JW (2005) MarinLit, a marine chemical literature database. Available from: University of Canterbury, Christchurch, New Zealand, http://www.chem.canterbury.ac.nz/marinlit/marinlit.shtmL, accessed December 2014
Núñez Miguel R, Wong J, Westoll JF et al (2007) A dimer of the toll-like receptor 4 cytoplasmic domain provides a specific scaffold for the recruitment of signalling adaptor proteins. PLoS ONE 2(8), e788
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
Othman AR, Abdullah N, Ahmad S, Ismail IS, Zakaria MP (2015) Elucidation of in-vitro anti-inflammatory bioactive compounds isolated from Jatropha curcas L. plant root. BMC Complement Altern Med 15:11
Pangestuti R, Kim SK (2011) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 3:255–266
Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286:327–334
Rengasamy KR, Aderogba M, Amoo S, Stirk W, Van Staden J (2014) Macrocystis angustifolia is a potential source of enzyme inhibitors linked to type 2 diabetes and dementia. J Appl Phycol 26:1557–1563
Rodriguez-Bernaldo de Quiros A, Lage-Yusty MA, Lopez-Hernandez J (2010) Determination of phenolic compounds in macroalgae for human consumption. Food Chem 121:634–638
Rosiak M, Grzeszczak S, Kosior DA, Postuła M (2014) Emerging treatments in type 2 diabetes: focus on canagliflozin. Ther Clin Risk Manag 10:683–689
Saisho Y (2014) Glycemic variability and oxidative stress: a link between diabetes and cardiovascular disease? Int J Mol Sci 15:18381–18406
Sharma BR, Rhyu DY (2014) Anti-diabetic effects of Caulerpa lentillifera: stimulation of insulin secretion in pancreatic β-cells and enhancement of glucose uptake in adipocytes. Asian Pac J Trop Biomed 4:575–580
Shiratori K, Ohgami K, Ilieva I, Jin XH, Koyama Y, Miyashita K et al (2005) Effects of fucoxanthin on lipopolysaccharide-induced inflammation in-vitro and in-vivo. Exp Eye Res 81:422–428
Sokolova EV, Barabanova AO, Bogdanovich RN, Khomenko VA, Solov’eva TF, Yermak IM (2011) In-vitro antioxidant properties of red algal polysaccharides. Biomed Prev Nutr 1:161–167
Van de Laar FA (2008) Alpha-glucosidase inhibitors in the early treatment of type 2 diabetes. Vasc Health Risk Manag 4:1189–1195
Van de Laar FA, Lucassen PL, Akkermans RP, Van de Lisdonk EH, Rutten GE, Van Weel C (2005) Alpha-glucosidase inhibitors for patients with type 2 diabetes: results from a Cochrane systematic review and meta-analysis. Diabetes Care 28:154–163
Wang T, Jonsdottir R, Liu H, Gu L, Kristinsson HG, Raghavan S, Olafsdottir G (2012) Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. J Agric Food Chem 60:5874–5883
Woo MN, Jeon SM, Kim HJ, Lee MK, Shin SK, Shin YC et al (2010) Fucoxanthin supplementation improves plasma and hepatic lipid metabolism and blood glucose concentration in high-fat fed C57BL/6N mice. Chem Biol Interact 186:316–322
Yudkin JS, Kumari M, Humphries SE, Mohamed-Ali V (2000) Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link? Atherosclerosis 148:209–214
Zhao Y, Joshi-Barve S, Barve S, Chen LH (2004) Eicosapentaenoic acid prevents LPS-induced TNF-α expression by preventing NF-κB activation. J Am Coll Nutr 23:71–78
Acknowledgments
The authors thank the Director General of Health Malaysia and the Director of Institute for Medical Research (IMR) for giving the permission to publish this article. We also thank the staff of the Nutrition Unit, Institute for Medical Research for their continuous support. We sincerely thank the Department of Fisheries Sabah, Malaysia, for their help and support to obtain the seaweed samples. Special thanks to Ms. Ang Jo-Lyn for her invaluable assistance for this project. This project was funded by the National Institutes of Health (NIH), Ministry of Health Malaysia (No. 12–011).
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Balasubramaniam, V., Lee, J.C., Noh, M.F.M. et al. Alpha-amylase, antioxidant, and anti-inflammatory activities of Eucheuma denticulatum (N.L. Burman) F.S. Collins and Hervey. J Appl Phycol 28, 1965–1974 (2016). https://doi.org/10.1007/s10811-015-0690-6
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DOI: https://doi.org/10.1007/s10811-015-0690-6