SEAWEED EXTRACTS AS A POTENTIAL TOOL FOR THE ATTENUATION OF OXIDATIVE DAMAGE IN OBESITY‐RELATED PATHOLOGIES1

Recent studies suggest that seaweed extracts are a significant source of bioactive compounds comparable to the dietary phytochemicals such as onion and tea extracts. The exploration of natural antioxidants that attenuate oxidative damage is important for developing strategies to treat obesity‐related pathologies. The objective of this study was to screen the effects of seaweed extracts of 49 species on adipocyte differentiation and reactive oxygen species (ROS) production during the adipogenesis in 3T3‐L1 adipocytes, and to investigate their total phenol contents and 2,2‐diphenyl‐1‐picrylhydrazyl (DPPH) radical scavenging activities. Our results show that high total phenol contents were observed in the extracts of Ecklonia cava (see Table 1 for taxonomic authors) (681.1 ± 16.0 μg gallic acid equivalents [GAE] · g^?1), Dictyopteris undulata (641.3 ± 70.7 μg GAE · g^?1), and Laurencia intermedia (560.9 ± 48.1 μg GAE · g^?1). In addition, DPPH radical scavenging activities were markedly higher in Sargassum macrocarpum (60.2%), Polysiphonia morrowii (55.0%), and Ishige okamurae (52.9%) than those of other seaweed extracts (P < 0.05). Moreover, treatment with several seaweed extracts including D. undulata, Sargassum micracanthum, Chondrus ocellatus, Gelidium amansii, Gracilaria verrucosa, and Grateloupia lanceolata significantly inhibited adipocyte differentiation and ROS production during differentiation of 3T3‐L1 preadipocytes. Furthermore, the production of ROS was positively correlated with lipid accumulation (R² = 0.8149). According to these preliminary results, some of the seaweed extracts can inhibit ROS generation, which may protect against oxidative stress that is linked to obesity. Further studies are required to determine the molecular mechanism between the verified seaweeds and ROS, and the resulting effects on obesity.

Table 1. List of Korean seaweed extracts of 49 species evaluated in this experiment.

Type	No.	Scientific name	Collection time	TP1 (μg GAE · g?1)
Brown macroalgae	SE‐1	Chondracanthus tenellus (Harv.) Hommers.	April 27, 2006	112.8 ± 15.1lm
	SE‐2	Colpomenia sinusa (F. C. Mertens ex Roth) Derbes et Solier in Castagne	May 11, 2006	44.0 ± 4.1opqrs
	SE‐3	Dictyopteris divaricata (Okamura) Okamura	April 6, 2006	41.5 ± 5.6pqrs
	SE‐4	Dictyopteris pacifica (Yendo) I. K. Hwang, H.‐S. Kim et W. J. Lee	April 27, 2006	80.9 ± 8.3mno
	SE‐5	Dictyopteris prolifera (Okamura) Okamura	November 26, 2007	48.4 ± 3.0nopqrs
	SE‐6	Dictyopteris undulata Holmes	July 28, 2007	641.3 ± 70.7b
	SE‐7	Dictyota asiatica I. K. Hwang	April 6, 2006	52.9 ± 7.6nonopqr
	SE‐8	Ecklonia cava Kjellm.	October 22, 2006	681.1 ± 16.0a
	SE‐9	Ecklonia stolonifera Okamura	November 26, 2007	36.5 ± 3.4pqrs
	SE‐10	Endarachne binghamiae J. Agardh	March 10, 2006	50.4 ± 2.6nopqrs
	SE‐11	Hizikia fusiformis (Harv.) Okamura	July 23, 2006	16.4 ± 1.2rs
	SE‐12	Hydroclathrus clathratus (C. Agardh) M. Howe	May 11, 2006	18.1 ± 0.9rs
	SE‐13	Ishige okamurae Yendo	May 26, 2006	237.4 ± 1.6h
	SE‐14	Lethesia difformis (L.) Aresch.	May 11, 2006	11.2 ± 1.9s
	SE‐15	Myelophycus simplex (Harv.) Papenf.	April 27, 2006	39.5 ± 3.2pqrs
	SE‐16	Padina arborescens Holmes	July 29, 2007	172.9 ± 23.1ij
	SE‐17	Sargassum fulvellum (Turner) C. Agardh	April 27, 2006	119.1 ± 5.6kl
	SE‐18	Sargassum micracanthum (Kütz.) Endl.	December 21, 2006	468.0 ± 22.7e
	SE‐19	Sargassum patens C. Agardh	January 21, 2007	41.5 ± 5.7pqrs
	SE‐20	Sargassum confusum C. Agardh f. validum Yendo	March 8, 2008	110.9 ± 3.5lm
	SE‐21	Sargassum horneri (Turner) C. Agardh	March 1, 2006	84.8 ± 9.4lmn
	SE‐22	Sargassum macrocarpum C. Agardh	January 21, 2007	353.9 ± 59.1g
	SE‐23	Sargassum muticum (Yendo) Fensolt	January 21, 2007	72.1 ± 14.9nop
	SE‐24	Sargassum nipponium Yendo	April 6, 2006	54.0 ± 3.5nopqr
	SE‐25	Sargassum sagamianum Yendo	March 8, 2008	41.0 ± 6.7pqrs
	SE‐26	Sargassum thunbergii (Mertens ex Roth) Kuntze	July 23, 2006	27.7 ± 0.8qrs
	SE‐27	Scytosiphon gracilis Kogame	May 26, 2006	30.2 ± 5.6qrs
	SE‐28	Scytosiphon lomentaria (Lyngb.) Link	May 11, 2006	66.5 ± 8.9nopq
Red macroalgae	SE‐29	Bonnemaisonia hamifera Har.	April 27, 2006	44.1 ± 2.3opqrs
	SE‐30	Callophyllis crispata Okamura	May 11, 2006	37.6 ± 12.6pqrs
	SE‐31	Chondria crassicaulis Harv.	May 11, 2006	45.4 ± 4.4opqrs
	SE‐32	Chondrus crispus Stackh.	May 26, 2006	40.7 ± 8.0pqrs
	SE‐33	Chondrus ocellatus Holmes	May 11, 2006	47.2 ± 1.7nopqrs
	SE‐34	Gelidium amansii (J. V. Lamour.) J. V. Lamour.	April 27, 2006	525.3 ± 35.9d
	SE‐35	Gloioperltis furcata (Postels et Rupr.) J. Agardh	May 26, 2006	147.7 ± 6.4jk
	SE‐36	Gloioperltis complanta (Harv.) Yamada	May 26, 2006	58.2 ± 6.4nopq
	SE‐37	Gracilaria verrucosa (Hudson) Papenf.	March 6, 2008	55.1 ± 7.5nopqr
	SE‐38	Grateloupia elliptica Holmes	May 26, 2006	154.4 ± 12.9j
	SE‐39	Grateloupia filicina (J. V. Lamour.) C. Agardh	May 11, 2006	38.2 ± 2.2pqrs
	SE‐40	Grateloupia lanceolata (Okamura) Kawag.	July 23, 2006	32.7 ± 3.0pqrs
	SE‐41	Laurencia intermedia J. V. Lamour.	May 11, 2006	560.9 ± 48.1c
	SE‐42	Laurencia intricata J. V. Lamour.	April 27, 2006	35.4 ± 4.0pqrs
	SE‐43	Laurencia okamurae Yamada	May 11, 2006	193.2 ± 41.9i
	SE‐44	Lomentaria hakodatensis Yendo	April 27, 2006	165.2 ± 15.1ij
	SE‐45	Polyopes affinis (Harv.) Kawag. et H.‐W. Wang	May 26, 2006	42.9 ± 2.3opqrs
	SE‐46	Polysiphonia morrowii Harv.	May 11, 2006	392.4 ± 40.3f
	SE‐47	Prionitis cornea (Okamura) E. Y. Dawson	October 22, 2006	47.9 ± 3.6nopqrs
Green macroalgae	SE‐48	Enteromorpha prolifera (O. F. Müll.) J. Agardh	March 26, 2006	42.0 ± 5.3pqrs
	SE‐49	Ulva pertusa Kjellm.	April 27, 2006	48.3 ± 3.8nopqrs

• GAE, gallic acid equivalents; SE, seaweed extracts.
• ¹TP, total phenol content is micrograms of total phenol contents per gram of seaweed extract based on gallic acid as standard. The values are means ± SD from three replications.
• ^a–sMeans in the same column not sharing a common letter are significantly different (P < 0.05) by Duncan’s multiple test.

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• Kas?m Cemal Güven, Burak Coban, Osman Özdemir, Pharmacology of Marine Macroalgae, Encyclopedia of Marine Biotechnology, 10.1002/9781119143802, (585-615), (2020). Wiley Online Library
• Giovanna Bermano, Teodora Stoyanova, Franck Hennequart, Cherry L. Wainwright, Seaweed-derived bioactives as potential energy regulators in obesity and type 2 diabetes, , 10.1016/bs.apha.2019.10.002, (2019). Crossref
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• M. Lynn Cornish, Alan T. Critchley, Ole G. Mouritsen, A role for dietary macroalgae in the amelioration of certain risk factors associated with cardiovascular disease, Phycologia, 10.2216/15-77.1, 54 , 6, (649-666), (2019). Crossref
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• Noelia Flórez‐Fernández, María P Casas, María Jesús González‐Muñoz, Herminia Domínguez, Microwave hydrogravity pretreatment of Sargassum muticum before solvent extraction of antioxidant and antiobesity compounds, Journal of Chemical Technology & Biotechnology, 10.1002/jctb.5771, 94 , 1, (256-264), (2018). Wiley Online Library
• Yannick Lerat, M. L. Cornish, Alan T. Critchley, Stéphane La Barre, Stephen S. Bates, Applications of Algal Biomass in Global Food and Feed Markets: From Traditional Usage to the Potential for Functional Products, Blue Biotechnology, 10.1002/9783527801718, (143-189), (2018). Wiley Online Library
• Gabriele Andressa Zatelli, Ana Cláudia Philippus, Miriam Falkenberg, An overview of odoriferous marine seaweeds of the Dictyopteris genus: insights into their chemical diversity, biological potential and ecological roles, Revista Brasileira de Farmacognosia, 10.1016/j.bjp.2018.01.005, 28 , 2, (243-260), (2018). Crossref
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• Fook Yee Chye, Birdie Scott Padam, Seah Young Ng, Innovation and Sustainable Utilization of Seaweeds as Health Foods, Sustainability Challenges in the Agrofood Sector, 10.1002/9781119072737, (390-434), (2017). Wiley Online Library
• Gaurav Rajauria, Lynn Cornish, Francesco Ometto, Flower E. Msuya, Raffaella Villa, Identification and selection of algae for food, feed, and fuel applications, Seaweed Sustainability, 10.1016/B978-0-12-418697-2.00012-X, (315-345), (2015). Crossref
• Jatinder Sangha, Owen Wally, Arjun Banskota, Roumiana Stefanova, Jeff Hafting, Alan Critchley, Balakrishnan Prithiviraj, A Cultivated Form of a Red Seaweed (Chondrus crispus), Suppresses β-Amyloid-Induced Paralysis in Caenorhabditis elegans, Marine Drugs, 10.3390/md13106407, 13 , 10, (6407-6424), (2015). Crossref
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• Georgia M. Hart, Tamara Ticktin, Dovi Kelman, Anthony D. Wright, Nicole Tabandera, Contemporary Gathering Practice and Antioxidant Benefit of Wild Seaweeds in Hawai’i, Economic Botany, 10.1007/s12231-014-9258-7, 68 , 1, (30-43), (2014). Crossref
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• Min‐Jung Seo, Hyeon‐Son Choi, Ok‐Hwan Lee, Boo‐Yong Lee, Grateloupia lanceolata (Okamura) Kawaguchi, the Edible Red Seaweed, Inhibits Lipid Accumulation and Reactive Oxygen Species Production During Differentiation in 3T3‐L1 Cells, Phytotherapy Research, 10.1002/ptr.4765, 27 , 5, (655-663), (2012). Wiley Online Library
• Mi‐Seon Woo, Hyeon‐Son Choi, Ok‐Hwan Lee, Boo‐Yong Lee, The Edible red Alga, Gracilaria verrucosa, Inhibits Lipid Accumulation and ROS Production, but Improves Glucose Uptake in 3T3‐L1 Cells, Phytotherapy Research, 10.1002/ptr.4813, 27 , 7, (1102-1105), (2012). Wiley Online Library
• Young-Jun Lee, Bo-Ra Yoon, Hyeon-Son Choi, Boo-Yong Lee, Ok-Hwan Lee, Effect of Sargassum micracanthum extract on Lipid Accumulation and Reactive Oxygen Species (ROS) Production during Differentiation of 3T3-L1 Preadipocytes, Korean Journal of Food Preservation, 10.11002/kjfp.2012.19.3.455, 19 , 3, (455-461), (2012). Crossref
• Mei Piao, Yu Hyun, Suk Cho, Hee Kang, Eun Yoo, Young Koh, Nam Lee, Mi Ko, Jin Hyun, An Ethanol Extract Derived from Bonnemaisonia hamifera Scavenges Ultraviolet B (UVB) Radiation-Induced Reactive Oxygen Species and Attenuates UVB-Induced Cell Damage in Human Keratinocytes, Marine Drugs, 10.3390/md10122826, 10 , 12, (2826-2845), (2012). Crossref

Volume 47 , Issue 3 June 2011

Pages 548-556