Browse > Article
http://dx.doi.org/10.4014/jmb.1910.10068

Neuroprotective Effects of Phlorotannin-Rich Extract from Brown Seaweed Ecklonia cava on Neuronal PC-12 and SH-SY5Y Cells with Oxidative Stress  

Nho, Jin Ah (Department of Food Science and Biotechnology, Kyung Hee University)
Shin, Yong Sub (Graduate School of Biotechnology, Kyung Hee University)
Jeong, Ha-Ram (Graduate School of Biotechnology, Kyung Hee University)
Cho, Suengmok (Department of Food Science and Technology, Pukyong National University)
Heo, Ho Jin (Division of Applied Life Science (BK21 Plus), Institute of Agricultural and Life Science, Gyeongsang National University)
Kim, Gun Hee (Department of Foods and Nutrition, Duksung Women's University)
Kim, Dae-Ok (Department of Food Science and Biotechnology, Kyung Hee University)
Publication Information
Journal of Microbiology and Biotechnology / v.30, no.3, 2020 , pp. 359-367 More about this Journal
Abstract
Neurodegenerative disorders in the elderly are characterized by gradual loss of memory and cognitive function. Oxidative stress caused by reactive oxygen species is associated with progressive neuronal cell damage and death in Alzheimer's disease, one of the most common neurodegenerative disorders. An edible brown seaweed, Ecklonia cava, contains a variety of biologically active compounds such as phlorotannins. In this study, we comparatively evaluated the total phenolic content, antioxidant capacity, and neuroprotective effects of the phlorotannin-rich extract from E. cava (PEEC). The total phenolic content of PEEC and dieckol was 810.8 mg gallic acid equivalents (GAE)/g and 996.6 mg GAE/g, respectively. Antioxidant capacity of PEEC was 1,233.8 mg vitamin C equivalents (VCE)/g and 392.1 mg VCE/g determined using ABTS and DPPH assays, respectively, while those of dieckol were 2,238.4 mg VCE/g and 817.7 mg VCE/g. High-performance liquid chromatography results revealed 48.08 ± 0.67 mg dieckol/g of PEEC. PEEC had neuroprotective effects in pheochromocytoma (PC-12) and human neuroblastoma (SH-SY5Y) cells against H2O2- and AAPH-induced oxidative damage, partly due to reduced intracellular oxidative stress. PEEC treatment inhibited acetylcholinesterase and butyrylcholinesterase in a dose-dependent manner. Taken together, these findings suggest that PEEC is a good source of antioxidants and neuroprotective materials.
Keywords
Cholinesterase; dieckol; neuron; neuroprotection; vitamin C equivalent antioxidant capacity;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Alghazwi M, Kan YQ, Zhang W, Gai WP, Garson MJ, Smid S. 2016. Neuroprotective activities of natural products from marine macroalgae during 1999-2015. J. Appl. Phycol. 28: 3599-3616.   DOI
2 Pangestuti R, Kim S-K. 2011. Neuroprotective effects of marine algae. Mar. Drugs 9: 803-818.   DOI
3 Kim J, Um M, Yang H, Kim I, Lee C, Kim Y, et al. 2016. Method development and validation fordieckol in the standardization of phlorotannin preparations. Fish. Aquat. Sci. 19: 3.   DOI
4 Singleton VL, Rossi JA, Jr. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16: 144-158.
5 Kim D-O, Lee CY. 2004. Comprehensive study of vitamin C equivalent antioxidant capacity (VCEAC) of various polyphenolics in scavenging a free radical and its structural relationship. Crit. Rev. Food Sci. Nutr. 44: 253-273.   DOI
6 Brand-Williams W, Cuvelier ME, Berset C. 1995. Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci. Technol. 28: 25-30.   DOI
7 Heo H-J, Cho H-Y, Hong B, Kim H-K, Kim E-K, Kim B-G, et al. 2001. Protective effect of 4',5-dihydroxy-3',6,7-trimethoxyflavone from Artemisia asiatica against $A{\beta}$-induced oxidative stress in PC12 cells. Amyloid-J. Protein Fold. Disord. 8: 194-201.   DOI
8 Wolfe KL, Liu RH. 2007. Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements. J. Agric. Food Chem. 55: 8896-8907.   DOI
9 Heo S-J, Park E-J, Lee K-W, Jeon Y-J. 2005. Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresour. Technol. 96: 1613-1623.   DOI
10 Ellman GL, Courtney KD, Andres V, Jr., Featherstone RM. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7: 88-95.   DOI
11 Senevirathne M, Kim S-H, Siriwardhana N, Ha J-H, Lee K-W, Jeon Y-J. 2006. Antioxidant potential of Ecklonia cava on reactive oxygen species scavenging, metal chelating, reducing power and lipid peroxidation inhibition. Food Sci. Technol. Int. 12: 27-38.   DOI
12 Li Y, Qian Z-J, Ryu B, Lee S-H, Kim M-M, Kim S-K. 2009. Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg. Med. Chem. 17: 1963-1973.   DOI
13 Shin D-B, Han E-H, Park S-S. 2014. Cytoprotective effects of Phaeophyta extracts from the coast of Jeju island in HT-22 mouse neuronal cells. J. Korean Soc. Food Sci. Nutr. 43: 224-230.   DOI
14 Kim D-O, Lee KW, Lee HJ, Lee CY. 2002. Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J. Agric. Food Chem. 50: 3713-3717.   DOI
15 Yoo KM, Kim D-O, Lee CY. 2007. Evaluation of different methods of antioxidant measurement. Food Sci. Biotechnol. 16: 177-182.
16 Kang HS, Chung HY, Jung JH, Son BW, Choi JS. 2003. A new phlorotannin from the brown alga Ecklonia stolonifera. Chem. Pharm. Bull. 51: 1012-1014.   DOI
17 Kim HS, Lee K, Kang KA, Lee NH, Hyun JW, Kim H-S. 2012. Phloroglucinol exerts protective effects against oxidative stress-induced cell damage in SH-SY5Y cells. J. Pharmacol. Sci. 119: 186-192.   DOI
18 Shibata T, Ishimaru K, Kawaguchi S, Yoshikawa H, Hama Y. 2008. Antioxidant activities of phlorotannins isolated from Japanese Laminariaceae. J. Appl. Phycol. 20: 705-711.   DOI
19 Kang I-J, Jeon YE, Yin XF, Nam J-S, You SG, Hong MS, et al. 2011. Butanol extract of Ecklonia cava prevents production and aggregation of beta-amyloid, and reduces beta-amyloid mediated neuronal death. Food Chem. Toxicol. 49: 2252-2259.   DOI
20 Kang IJ, Jang BG, In S, Choi B, Kim M, Kim MJ. 2013. Phlorotannin-rich Ecklonia cava reduces the production of beta-amyloid by modulating alpha- and gamma-secretase expression and activity. NeuroToxicology 34: 16-24.   DOI
21 Lee J-H, Kim G-H. 2015. Evaluation of antioxidant activity of marine algae-extracts from Korea. J. Aquat. Food Prod. Technol. 24: 227-240.   DOI
22 Othman SB, Yabe T. 2015. Use of hydrogen peroxide and peroxyl radicals to induce oxidative stress in neuronal cells. Rev. Agric. Sci. 3: 40-45.   DOI
23 Kang S-M, Cha S-H, Ko J-Y, Kang M-C, Kim D, Heo S-J, et al. 2012. Neuroprotective effects of phlorotannins isolated from a brown alga, Ecklonia cava, against $H_2O_2$-induced oxidative stress in murine hippocampal HT22 cells. Environ. Toxicol. Pharmacol. 34: 96-105.   DOI
24 Yoon NY, Chung HY, Kim HR, Choi JS. 2008. Acetyl- and butyrylcholinesterase inhibitory activities of sterols and phlorotannins from Ecklonia stolonifera. Fish. Sci. 74: 200-207.   DOI
25 Myung C-S, Shin H-C, Bao HY, Yeo SJ, Lee BH, Kang JS. 2005. Improvement of memory by dieckol and phlorofucofuroeckol in ethanol-treated mice: possible involvement of the inhibition of acetylcholinesterase. Arch. Pharm. Res. 28: 691-698.   DOI
26 World Health Organization. 2017. Dementia: a public health priority. Available from https://www.who.int/en/newsroom/fact-sheets/detail/dementia. Accessed on October 9th, 2019.
27 Kim J-J, Kang Y-J, Shin S-A, Bak D-H, Lee JW, Lee KB, et al. 2016. Phlorofucofuroeckol improves glutamate-induced neurotoxicity through modulation of oxidative stress-mediated mitochondrial dysfunction in PC12 cells. PLoS One 11: e0163433.   DOI
28 Cha S-H, Heo S-J, Jeon Y-J, Park SM. 2016. Dieckol, an edible seaweed polyphenol, retards rotenone-induced neurotoxicity and ${\alpha}$-synuclein aggregation in human dopaminergic neuronal cells. RSC Adv. 6: 110040-110046.   DOI
29 Scarpini E, Cogiamanian F. 2003. Alzheimer's disease: from molecular pathogenesis to innovative therapies. Expert Rev. Neurother. 3: 619-630.   DOI
30 Kovacs GG. 2014. Current concepts of neurodegenerative diseases. EMJ Neurol. 1: 78-86.
31 Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, et al. 2017. Oxidative stress: harms and benefits for human health. Oxid. Med. Cell. Longev. 2017: 8416763.
32 Jezek J, Cooper K, Strich R. 2018. Reactive oxygen species and mitochondrial dynamics: the yin and yang of mitochondrial dysfunction and cancer progression. Antioxidants 7: 13.   DOI
33 Tabner BJ, El-Agnaf OMA, Turnbull S, German MJ, Paleologou KE, Hayashi Y, et al. 2005. Hydrogen peroxide is generated during the very early stages of aggregation of the amyloid peptides implicated in Alzheimer disease and familial British dementia. J. Biol. Chem. 280: 35789-35792.   DOI
34 Halliwell B. 2012. Free radicals and antioxidants: updating a personal view. Nutr. Rev. 70: 257-265.   DOI
35 Panahi Y, Rajaee SM, Johnston TP, Sahebkar A. 2019. Neuroprotective effects of antioxidants in the management of neurodegenerative disorders: a literature review. J. Cell. Biochem. 120: 2742-2748.   DOI
36 Soreq H, Seidman S. 2001. Acetylcholinesterase - new roles for an old actor. Nat. Rev. Neurosci. 2: 294-302.   DOI
37 Darvesh S, Hopkins DA, Geula C. 2003. Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci. 4: 131-138.   DOI
38 Lee J-w, Seok JK, Boo YC. 2018. Ecklonia cava extract and dieckol attenuate cellular lipid peroxidation in keratinocytes exposed to PM10. Evid.-Based Compl. Alt. Med. 2018: 8248323.
39 Lee S, Lee D, Baek J, Jung EB, Baek JY, Lee IK, et al. 2017. In vitro assessment of selected Korean plants for antioxidant and antiacetylcholinesterase activities. Pharm. Biol. 55: 2205-2210.   DOI
40 Park SK, Kang JY, Kim JM, Park SH, Kwon BS, Kim G-H, et al. 2018. Protective effect of fucoidan extract from Ecklonia cava on hydrogen peroxide-induced neurotoxicity. J. Microbiol. Biotechnol. 28: 40-49.   DOI
41 Singh IP, Bharate SB. 2006. Phloroglucinol compounds of natural origin. Nat. Prod. Rep. 23: 558-591.   DOI
42 Wijesinghe WAJP, Jeon Y-J. 2011. Exploiting biological activities of brown seaweed Ecklonia cava for potential industrial applications: a review. Int. J. Food Sci. Nutr. 63: 225-235.   DOI
43 Le Q-T, Li Y, Qian Z-J, Kim M-M, Kim S-K. 2009. Inhibitory effects of polyphenols isolated from marine alga Ecklonia cava on histamine release. Process Biochem. 44: 168-176.   DOI
44 Lee SH, Li Y, Karadeniz F, Kim M-M, Kim S-K. 2009. ${\alpha}$-Glucosidase and ${\alpha}$-amylase inhibitory activities of phloroglucinal derivatives from edible marine brown alga, Ecklonia cava. J. Sci. Food. Agric. 89: 1552-1558.   DOI
45 Cho S, Yang H, Jeon Y-J, Lee CJ, Jin Y-H, Baek N-I, et al. 2012. Phlorotannins of the edible brown seaweed Ecklonia cava Kjellman induce sleep via positive allosteric modulation of gamma-aminobutyric acid type A-benzodiazepine receptor: a novel neurological activity of seaweed polyphenols. Food Chem. 132: 1133-1142.   DOI