Lipid-rich extracts were obtained from brown algae Saccharina cichorioides , Costaria costata , Chorda filum , Eularia fistulosa , Dictyopteris divaricata , Dictyosiphon chordaria , Silvetia babingtonii , and Fucus evanescens that were collected in Peter the Great Gulf of the Sea of Japan. The ability of algalextracts and glyceroglycolipids (GLs) monogalactosyldiacylglycerols (MGDG), digalactosyldiacylglycerols (DGDG), and sulfoquinovosyldiacylglycerols (SQDG) and carotenoid fucoxanthin to suppression of reactive oxygen species (ROS) in lipopolysaccharide (LPS)-stimulated RAW 264.7 macrophage cells, studied. The results showed that algae extracts could suppress ROS. However, extracts of D. divaricata , D. chordaria , C. filum , S. babingtonii , and F. evanescens had a higher degree of suppression of ROS. Extracts of S. cichorioides and D. divaricata showed the dependence of their activity from the month of collecting these algae. The GLs and fucoxanthin were isolated from extracts of using column chromatography with silica gel and their ROS-inhibitory activity was investigated too. The fatty acids (FAs) composition of lipids was determined byGC and GC/MS. It has been found that MGDG and DGDG stronger than SGDG inhibited the ROS and the degree of their activity depended on the species of algae, the month of collection, the amount of PUFA, the ratio of n - 3 and n - 6 PUFA in GLs. Fucoxanthin has shown a high degree of suppression of ROS. This preliminary study has shown the prospect of a deeper study of the suppression of ROS with the help of lipids from algae the Sea of Japan.
KeywordsAlgaeGlyceroglycolipidsFucoxanthinFatty AcidsReactive Oxygen Species (ROS)
Romay, C., Armesto, J., Remirez, D., González, R., Ledon, N. and García, I. (1998) Antioxidant and Anti-Inflammatory Properties of C-Phycocyanin from Blue-Green Algae. Inflammation Research, 47, 36-41. http://dx.doi.org/10.1007/s000110050256
Ruberto, G., Baratta, M.T., Biondi, D.M. and Amico, V. (2001) Antioxidant Activity of Extracts of the Marine Algal Genus Cystoseira in a Micellar Model System. Journal of Applied Phycology, 13, 403-407. http://dx.doi.org/10.1023/A:1011972230477
Tierney, M.S., Croft, A.K. and Hayes, M. (2010) A Review of Antihypertensive and Antioxidant Activities in Macroalgae. Botanica Marina, 53, 387-408. http://dx.doi.org/10.1515/bot.2010.044
Sachindra, N.M., Airanthi, M.K.W.A., Hosokawa, M, and Miyashita, K. (2010) Radical Scavenging and Singlet Oxygen Quenching Activity of Extracts from Indian Seaweeds. Journal Food Science Technollogy, 47, 94-99. http://dx.doi.org/10.1007/s13197-010-0022-4
Boonchum, W., Peerapornpisal, Y., Kanjanapothi, D., Pekkoh, J., Pumas, C., Jamjai, U., Amornlerdpison, D., Noiraksar, T. and Vacharapiyasophon, P. (2011) Antioxidant Activity of Some Seaweed from the Gulf of Thailand. International Journal Agriculture and Biology, 13, 95-99.
Kelman, D., Posner, E.K., McDermid, K.J., Tabandera, N.K., Wright, P.R. and Wright, A.D. (2012) Antioxidant Activity of Hawaiian Marine Algae. Marine Drugs, 10, 403-416. http://dx.doi.org/10.3390/md10020403
Siqueira, R.C.L., da Silva, M.S.J., de Alencar, D.B., Pires, A.F., de Alencar, N.M.N., Pereira, M.G., Cavada, B.S., Sampaio, A.H., Farias, W.R.L. and Assreuy, A.M.S. (2011) In vivo Anti-inflammatory Effect of a Sulfated Polysaccharide Isolated from the Marine Brown Algae Lobophoravariegata. Pharmaceutical Biology, 49, 167-174. http://dx.doi.org/10.3109/13880209.2010.505605
Vo, T.S., Ngo, D.H. and Kim, S.K. (2012) Potential Targets for Anti-Inflammatory and Anti-Allergic Activities of Marine Algae: an Overview. Inflammation Allergy Drug Targets, 11, 90-101. http://dx.doi.org/10.2174/187152812800392797
Dore, C.M.P.G., Alves, M.G.C.F., Costa, T.G., Sabry, D.A., Rego, L.A.S., Accado, C.M., Rocha, H.A.O., Filgueira, L.G.A. and Leite, E.L. (2013) A Sulfated Polysaccharide, Fucan, Isolated from Brown Algae Sargassum vulgare with Anticoagulant, Antithrombotic, Antioxidant and Anti-Inflammatory Effects. Carbohydrate Polymers, 91, 467-475. http://dx.doi.org/10.1016/j.carbpol.2012.07.075
Samarakoon, K. and Jeon, Y.J. (2012) Bio-Functionalities of Proteins Derived from Marine Algae: A Review. Food Research International, 48, 948-960. http://dx.doi.org/10.1016/j.foodres.2012.03.013
Vo, T.S., Ngo, D.H. and Kim, S.K. (2012) Marine Algae as a Potential Pharmaceutical Source for Anti-Allergic Therapeutics. Process Biochemistry, 47, 386-394. http://dx.doi.org/10.1016/j.procbio.2011.12.014
Pangestuti, R. and Kim, S.K. (2011) Neuroprotective Effects of Marine Algae. Marine Drugs, 9, 803-818. http://dx.doi.org/10.3390/md9050803
Waris, G. and Ahsan, H. (2006) Reactive Oxygen Species: Role in the Development of Cancer and Various Chronic Conditions. Journal of Carcinogenesis, 5, 14. http://dx.doi.org/10.1186/1477-3163-5-14
Beaglehole, R.S., Reddy, E.S., Voute, J. and Leeder, S. (2007) Prevention of Chronic Diseases: A Call to Action. The Lancet, 370, 2152-2157. http://dx.doi.org/10.1016/S0140-6736(07)61700-0
Abad, M.J., Bedoya, L.M. and Bermejo, P. (2008) Natural Marine Anti-Inflammatory Products. Medicinal Chemistry, 8, 740-754. http://dx.doi.org/10.2174/138955708784912148
Wang, W., Wang, S.X. and Guan, H.S. (2012) The Antiviral Activities and Mechanisms of Marine Polysaccharides: An Overview. Marine Drugs, 10, 2795-2816. http://dx.doi.org/10.3390/md10122795
D’Orazio, N., Gammone, M.A., Gemello, E., De Girolamo, M., Cusenza, S. and Riccioni, G. (2012) Marine Bioactives: Pharmacological Properties and Potential Applications against Inflammatory Diseases. Marine Drugs, 10, 812-833. http://dx.doi.org/10.3390/md10040812
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. Archives of Pharmacal Research, 27, 194-198. http://dx.doi.org/10.1007/BF02980106
Kim, Y.A., Kong, C.S., Um, Y.R., Lee, J.I., Nam, T.J. and Seo, Y.W. (2008) Antioxidant Efficacy of Extracts from a Variety of Seaweeds in a Cellular System. Ocean Science Journal, 43, 31-37. http://dx.doi.org/10.1007/BF03022429
Badrinathan, S., Suneeva, S.C., Shiju, T.M., Girish Kumar, C.P. and Pragasam, V. (2011) Exploration of a Novel Hydroxyl Radical Scavenger from Sargassum myriocystum. Journal of Medical Plants Research, 5, 1997-2005.
Jung, H.A., Jin, S.E., Ahn, B.R., Lee, C.M. and Choi, J.S. (2013) Anti-inflammatory Activity of Edible Brown Alga Eiseniabicyclis and Its Constituents Fucosterol and Phlorotannins in LPS-stimulated RAW264.7 Macrophages. Food and Chemistry Toxicology, 59, 199-206. http://dx.doi.org/10.1016/j.fct.2013.05.061
Islam, M.N., Ishita, I.J., Jin, S.E., Choi, R.J., Lee, C.M., Kim, Y.S., Jung, H.A. and Choi, J.S. (2013) Anti-Inflammatory Activity of Edible Brown Alga Saccharina japonica and Its Constituents Pheophorbide a and Pheophytin a in LPS-Stimulated RAW 264.7 Macrophage Cells. Food and Chemistry Toxicology, 55, 541-548. http://dx.doi.org/10.1016/j.fct.2013.01.054
McCauley, J.I., Meyer, B.J., Winberg, P.C., Ranson, M. and Skropeta, D. (2015) Selecting Australian Marine Macroalgae Based on the Fatty Acid Composition and Anti-Inflammatory Activity. Journal of Applied Phycology, 27, 2111-2121. http://dx.doi.org/10.1007/s10811-014-0465-5
Júnior, S.Q., Carneiro, V.H.A., Fontenelle, T.P.C., Chaves, L.D.S., Mesquita, J.X., de Brito, T.V., Siva Prudêncio, R., de Oliveira, J.S., Medeiros, J.-V.R., Arag?o, K.S., Ribeiro, R.D.A., Barbosa, A.L.D.R. and Freitas, A.L.P. (2015) Antioxidant and Anti-Inflammatory Activities of Methanol Extractand Its Fractions from the Brown Seaweed Spatoglossum schroederi. Journal of Applied Phycology, 27, 2367-2376. http://dx.doi.org/10.1007/s10811-014-0497-x
Kim, M.M. and Kim, S.K. (2010) Effect of Phloroglucinol on Oxidative Stress and Inflammation. Food and Chemistry Toxicology, 48, 2925-2933. http://dx.doi.org/10.1016/j.fct.2010.07.029
Kim, S.K. and Himaya, S.W. (2011) Medicinal Effects of Phlorotannins from Marine Brown Algae. Advances in Food Nutrition Research, 64, 97-109. http://dx.doi.org/10.1016/B978-0-12-387669-0.00008-9
Kim, S.J., Kim, E.A., Kang, M.C., Lee, J.H., Yang, H.W., Lee, J.S., Lim, T.I. and Jeon, Y.J. (2014) Polyphenol-Rich Fraction from Ecklonia cava (a Brown Alga) Processing By-Product Reduces LPS-Induced Inflammation in Vitro and in Vivo in a Zebrafish Model. Algae, 29, 165-174. http://dx.doi.org/10.4490/algae.2014.29.2.165
Shiratori, K., Ohgami. K., Ilieva, 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. Experimental Eye Research, 81, 422-428. http://dx.doi.org/10.1016/j.exer.2005.03.002
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. and Jeon, Y.J. (2010) Evaluation of Anti-Inflammatory Effect of Fucoxanthin Isolated from Brown Algae in Lipopolysaccharide- Stimulated RAW 264.7 Macrophages. Food and Chemistry Toxicology, 48, 2045-2051. http://dx.doi.org/10.1016/j.fct.2010.05.003
Zou, Y., Li, Y., Kim, M.-M., Lee, S.-H. and Kim, S.-K. (2009) Ishigoside, a New Glyceroglycolipid Isolated from the Brown Alga Ishige okamurae. Biotechnology and Bioprocess Engineering, 14, 20-26. http://dx.doi.org/10.1007/s12257-008-0131-3
Banskota, A.H., Stefanova, R., Sperker, S., Lall, S.P., Craigie, J.S. and Hafting, J.T. (2014a) Lipids Isolated from the Red Alga Chondrus crispus Inhibit Nitric Oxide Production. Journal of Applied Phycology, 26, 1565-1571. http://dx.doi.org/10.1007/s10811-013-0174-5
Banskota, A.H., Stefanova, R., Sperker, S., Lall, S.P., Craigie, J.S., Hafting, J.T. and Critchley, A.T. (2014b) Polar Lipids from the Marine Macroalga Palmaria palmate Inhibit Lipopolysaccharide-Induced Nitric Oxide Production in RAW 264.7 Macrophage Cells. Phytochemistry, 101, 101-108. http://dx.doi.org/10.1016/j.phytochem.2014.02.004
Lopes, G., Daletos, G., Proksch, P., Andrade, P.B. and Valent?o, P. (2014) Anti-Inflammatory Potential of Monogalactosyl Diacylglycerols and a Monoacylglycerol from the Edible Brown Seaweed Fucus spiralis Linnaeus. Marine Drugs, 12, 1406-1418. http://dx.doi.org/10.3390/md12031406
Robertson, R.C., Guiheneuf, F., Bahar, B., Schmid, M., Stengel, D.B., Fitzgerald, G.F., Ross, R.P. and Stanton, C. (2015) The Anti-Inflammatory Effect of Algae-Derived Lipid Extracts on Lipopolysaccharide (LPS)-Stimulated Human THP-1 Macrophages. Marine Drugs, 13, 5402-5424. http://dx.doi.org/10.3390/md13085402
Gerasimenko, N.I., Martyyas, E.A. and Busarova, N.G. (2012) Composition of Lipids and Biological Activity of Lipids and Photosynthetic Pigments from Algae of the Families Laminariaceae and Alariaceae. Chemistry of Natural Compounds, 48, 737-741. http://dx.doi.org/10.1007/s10600-012-0371-5
Gerasimenko, N.I., Busarova, N.G. and Martyyas, E.A. (2012) Composition of Lipids from Fucusevanescens (Sea of Okhotsk and Japan) and Biological Activity of Lipids and Photosynthetic Pigments. Chemistry of Natural Compounds, 48, 742-747. http://dx.doi.org/10.1007/s10600-012-0372-4
Martyyas, E.A., Gerasimenko, N.I., Busarova, N.G., Yurchenko, E.A., Skriptsova, A.V. and Anisimov, M.M. (2013) Seasonal Changes in Biological Activity of Lipids and Photosynthetic Pigments of Saccharinacichorioides (Miyabe) (Laminariaceae Family). Russian Journal of Bioorganic Chemistry, 39, 720-727. http://dx.doi.org/10.1134/S106816201307008X
Pollet, S., Ermidou, S., Le Saux, F., Monge, M. and Baumnn, N. (1978) Microanalysis of Brain Lipids: Multiple Two-Dimensional Thin-Layer Chromatography. Journal of Lipid Research, 19, 916-921.
Vaskovsky, V.E., Kostetsky, E.Y. and Vasendin, I.M. (1975) A Universal Reagent for Phospholipid Analysis. Journal of Chromatography, 114, 129-141. http://dx.doi.org/10.1016/S0021-9673(00)85249-8
Radwan, S.S. (1978) Coupling of Two-Dimensional Thin Layer Chromatography with Gas Chromatography for Quantitative Analysis of Lipid Classes and Their Constituent Fatty Acid. Journal Chromatographic Science, 16, 538-542. http://dx.doi.org/10.1093/chromsci/16.11.538
Whitlle, S.J. and Casselton, P.J. (1975) The Chloroplast Pigments of the Algal Classes Eustigmatophyceae and Xanthophyceae. I. Eustigmatophyceae. British Phycological Journal, 10, 179-191. http://dx.doi.org/10.1080/00071617500650171
Lichtenthaler, H.K. (1987) Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods in Enzymology, 148, 350-382. http://dx.doi.org/10.1016/0076-6879(87)48036-1
Hashimoto, T., Ozaki, Y., Taminato, M., Das, S.K., Mizimo, M., Yoshimura, K., Maoka, T. and Kanozawa, K. (2009) The Distribution and Accumulation of Fucoxanthin and Its Metabolites after Oral Administration in Mice. British Journal Nutrition, 102, 242-248. http://dx.doi.org/10.1017/S0007114508199007
Prevot, A.F. and Mordret, F.X. (1976) Utilisation des Colonnes Capillaries de Verre Pour l’Analyse des Corps Gras par Chromatographie en Phase Gazeuse. Revue Francaise des Corps Gras, 23, 409-423.
Strànsky, K., Jursík, T. and Vitek, A. (1997) Standard Equivalent Chain Length Values of Monoenic and Polyenic (Methylene Interrupted) Fatty Acids. Journal of High Resolution Chromatography, 20, 143-158. http://dx.doi.org/10.1002/jhrc.1240200305
Rasoarahona, J.R.E. and Ramanoelina, P.A.R. (2008) Muscle Lipids and Fatty Acid Profiles of the Sea Catfish (Arius madagascariensis) in Madagascar Inland Waters. Journal of the American Oil Chemists Society, 85, 435-440. http://dx.doi.org/10.1007/s11746-008-1211-4
Tada, H., Shiho, O., Kuroshima, K., Koyama, M. and Tsukamoto, K. (1986) An Improved Colorimetric Assay for Interleukin 2. Journal of Immunological Methods, 93, 157-165. http://dx.doi.org/10.1016/0022-1759(86)90183-3
Kicha, A.A., Kalinovsky, A.I., Malyarenko, T.V., Ivanchina, N.V., Dmitrenok, P.S., Menchinskaya, E.S., Yurchenko, E.A., Pislyagin, E.A., Aminin, D.L., Huong, T.T., Long, P.Q. and Stonik, V.A. (2015) Cyclic Steroid Glycosides from the Starfish Echinaster luzonicus: Structures and Immunomodulatory Activities. Journal of Natural Products, 78, 1397-1405. http://dx.doi.org/10.1021/acs.jnatprod.5b00332
Khotimchenko, S.V. (2002) Distribution of Glyceroglycolipids in Marine Algae and Grasses. Chemistry of Natural Compounds, 38, 223-229. http://dx.doi.org/10.1023/A:1020471709232
Guschina, I.A. and Harwood, J.L. (2009) Algal Lipids and Effect of the Environment on Their Biochemistry. In: Arts, M.T., Brett, M.T., and Kainz, M., Eds., Lipids in Aquatic Ecosystems, Springer Science, Business Media LLC, 1-24. http://dx.doi.org/10.1007/978-0-387-89366-2_1
Miyashita, K., Nishikawa, S., Beppu, F., Tsukui, T., Abea, M. and Hosokawa, M. (2011) The Allenic Carotenoid Fucoxanthin, a Novel Marine Nutraceutical from Brown Seaweeds. Journal of the Science of Food and Agriculture, 91, 1166-1174. http://dx.doi.org/10.1002/jsfa.4353
Funga, A., Hamida, N. and Lua, J. (2013) Fucoxanthin Content and Antioxidant Properties of Undaria pinnatifida. Food Chemistry, 136, 1055-1062. http://dx.doi.org/10.1016/j.foodchem.2012.09.024
Mikami, K. and Hosokawa, M. (2013) Biosynthetic Pathway and Health Benefits of Fucoxanthin, an Algae-Specific Xanthophyll in Brown Seaweeds. International Journal of Molecular Science, 14, 13763-13781. http://dx.doi.org/10.3390/ijms140713763
Kanda, H., Kamo, Y., Machmudah, S., Goto, W. and Goto, M. (2014) Extraction of Fucoxanthin from Raw Macroalgae Excluding Drying and Cell Wall Disruption by Liquefied Dimethyl Ether. Marine Drugs, 12, 2383-2396. http://dx.doi.org/10.3390/md12052383
Bruno, A., Rossi, C., Marcolongo, G., Di Lena, A., Venzo, A., Berrie, C.P. and Corda, D. (2005) Selective in Vivo Anti-Inflammatory Action of the Galactolipid Monogalactosyldiacylglycerol. European Journal of Pharmacology, 524, 159-168. http://dx.doi.org/10.1016/j.ejphar.2005.09.023
Simopoulos, A.P. (2002) Omega-3 Fatty Acids in Inflammation and Autoimmune Diseases. The Journal of the American Colllege of Nutrrition, 21, 495-505. http://dx.doi.org/10.1080/07315724.2002.10719248
Simopoulos, A.P. (2008) The Importance of the Omega-6/Omega-3 Fatty Acid Ratio in Cardiovascular Disease and Other Chronic Diseases. Experimental Biology and Medicine, 233, 674-688. http://dx.doi.org/10.3181/0711-MR-311
Khan, M.N.A., Cho, J.Y., Lee, M.C., Kang, J.Y., Park, N.G., Fujii, H. and Hong, Y.K. (2007) Isolation of Two Anti-Inflammatory and One Pro-Inflammatory Polyunsaturated Fatty Acids from the Brown Seaweed Undaria pinnatifida. Journal of Agricultural and Food Chemistry, 55, 6984-6988. http://dx.doi.org/10.1021/jf071791s
Calder, P.C. (2011) Fatty Acids and Inflammation: The Cutting Edge between Food and Pharma. European Journal of Pharmacology, 668, S50-S58. http://dx.doi.org/10.1016/j.ejphar.2011.05.085
Glick, N.R. and Fisher, M.H. (2013) The Role of Essential Fatty Acids in Human Health. Journal of Evidence-Based Complementary and Alternative Medicine, 18, 268-289. http://dx.doi.org/10.1177/2156587213488788
Banskota, A.H., Stefanova, R., Gallant, P. and McGinn, P.J. (2013a) Mono- and Digalactosyl Diacylglycerols: Potent Nitric Oxide Inhibitors from the Marine Microalga Nannochloropsis granulate. Journal of Applied Phycology, 25, 349- 357. http://dx.doi.org/10.1007/s10811-012-9869-2
Banskota, A.H., Gallant, P., Stefanova, R., Melanson, R. and O’Leary, S.J.B. (2013) Monogalactosyldiacylglycerols, Potent Nitric Oxide Inhibitors from the Marine Microalga Tetraselmis chui. Natural Products Research, 27, 1084- 1090. http://dx.doi.org/10.1080/14786419.2012.717285