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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)
  • Received : 2019.10.31
  • Accepted : 2019.11.21
  • Published : 2020.03.28

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

References

  1. Scarpini E, Cogiamanian F. 2003. Alzheimer's disease: from molecular pathogenesis to innovative therapies. Expert Rev. Neurother. 3: 619-630. https://doi.org/10.1586/14737175.3.5.619
  2. Kovacs GG. 2014. Current concepts of neurodegenerative diseases. EMJ Neurol. 1: 78-86.
  3. 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.
  4. 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.
  5. 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. https://doi.org/10.3390/antiox7010013
  6. 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. https://doi.org/10.1074/jbc.C500238200
  7. Halliwell B. 2012. Free radicals and antioxidants: updating a personal view. Nutr. Rev. 70: 257-265. https://doi.org/10.1111/j.1753-4887.2012.00476.x
  8. 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. https://doi.org/10.1002/jcb.26536
  9. Soreq H, Seidman S. 2001. Acetylcholinesterase - new roles for an old actor. Nat. Rev. Neurosci. 2: 294-302. https://doi.org/10.1038/35067589
  10. Darvesh S, Hopkins DA, Geula C. 2003. Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci. 4: 131-138. https://doi.org/10.1038/nrn1035
  11. 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. https://doi.org/10.1080/13880209.2017.1397179
  12. 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. https://doi.org/10.4014/jmb.1710.10043
  13. 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.
  14. Singh IP, Bharate SB. 2006. Phloroglucinol compounds of natural origin. Nat. Prod. Rep. 23: 558-591. https://doi.org/10.1039/b600518g
  15. 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. https://doi.org/10.3109/09637486.2011.619965
  16. 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. https://doi.org/10.1016/j.procbio.2008.10.002
  17. 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. https://doi.org/10.1002/jsfa.3623
  18. 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. https://doi.org/10.1016/j.foodchem.2011.08.040
  19. 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. https://doi.org/10.1007/s10811-016-0908-2
  20. Pangestuti R, Kim S-K. 2011. Neuroprotective effects of marine algae. Mar. Drugs 9: 803-818. https://doi.org/10.3390/md9050803
  21. 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. https://doi.org/10.1186/s41240-016-0003-2
  22. Singleton VL, Rossi JA, Jr. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16: 144-158.
  23. 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. https://doi.org/10.1080/10408690490464960
  24. 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. https://doi.org/10.1016/S0023-6438(95)80008-5
  25. 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. https://doi.org/10.3109/13506120109007362
  26. Wolfe KL, Liu RH. 2007. Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements. J. Agric. Food Chem. 55: 8896-8907. https://doi.org/10.1021/jf0715166
  27. Ellman GL, Courtney KD, Andres V, Jr., Featherstone RM. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7: 88-95. https://doi.org/10.1016/0006-2952(61)90145-9
  28. 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. https://doi.org/10.1016/j.biortech.2004.07.013
  29. 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. https://doi.org/10.1177/1082013206062422
  30. 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. https://doi.org/10.1080/10498850.2013.770809
  31. 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. https://doi.org/10.3746/jkfn.2014.43.2.224
  32. 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. https://doi.org/10.1021/jf020071c
  33. Yoo KM, Kim D-O, Lee CY. 2007. Evaluation of different methods of antioxidant measurement. Food Sci. Biotechnol. 16: 177-182.
  34. 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. https://doi.org/10.1016/j.bmc.2009.01.031
  35. 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. https://doi.org/10.1248/cpb.51.1012
  36. 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. https://doi.org/10.1007/s10811-007-9254-8
  37. 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. https://doi.org/10.1016/j.fct.2011.06.023
  38. 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. https://doi.org/10.1016/j.neuro.2012.09.013
  39. 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. https://doi.org/10.1254/jphs.12056FP
  40. 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. https://doi.org/10.1371/journal.pone.0163433
  41. 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. https://doi.org/10.1039/C6RA21697H
  42. 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. https://doi.org/10.7831/ras.3.40
  43. 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. https://doi.org/10.1016/j.etap.2012.03.006
  44. 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. https://doi.org/10.1111/j.1444-2906.2007.01511.x
  45. 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. https://doi.org/10.1007/BF02969360

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