Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of Ecklonia cava Extract on Neuronal Damage and Apoptosis in PC-12 Cells against Oxidative Stress

  • Shin, Yong Sub (Graduate School of Biotechnology, Kyung Hee University) ;
  • Kim, Kwan Joong (Graduate School of Biotechnology, Kyung Hee University) ;
  • Park, Hyein (Department of Applied Biotechnology, Ajou University) ;
  • Lee, Mi-Gi (Bio-Center, Gyeonggido Business and Science Accelerator) ;
  • Cho, Sueungmok (Department of Food Science and Technology, Pukyong National University) ;
  • Choi, Soo-Im (Department of Foods and Nutrition, Duksung Women's University) ;
  • Heo, Ho Jin (Division of Applied Life Science (BK21), Institute of Agriculture and Life Science, Gyeongsang National University) ;
  • Kim, Dae-Ok (Graduate School of Biotechnology, Kyung Hee University) ;
  • Kim, Gun-Hee (Department of Foods and Nutrition, Duksung Women's University)
  • Received : 2020.12.07
  • Accepted : 2021.03.24
  • Published : 2021.04.28
Download PDF
⟨ Previous Next ⟩

Abstract

Marine algae (seaweed) encompass numerous groups of multicellular organisms with various shapes, sizes, and colors, and serve as important sources of natural bioactive substances. The brown alga Ecklonia cava Kjellman, an edible seaweed, contains many bioactives such as phlorotannins and fucoidans. Here, we evaluated the antioxidative, neuroprotective, and anti-apoptotic effects of E. cava extract (ECE), E. cava phlorotannin-rich extract (ECPE), and the phlorotannin dieckol on neuronal PC-12 cells. The antioxidant capacities of ECPE and ECE were 1,711.5 and 1,050.4 mg vitamin C equivalents/g in the ABTS assay and 704.0 and 474.6 mg vitamin C equivalents/g in the DPPH assay, respectively. The dieckol content of ECPE (58.99 mg/g) was approximately 60% higher than that of ECE (36.97 mg/g). Treatment of PC-12 cells with ECPE and ECE increased cell viability in a dose-dependent manner. Intracellular oxidative stress in PC-12 cells due to ECPE and ECE decreased dose-independently by up to 63% and 47%, respectively, compared with the stress control (323%). ECPE reduced the production of the pro-apoptotic proteins Bax and caspase-3 more effectively than ECE. Early and late apoptosis in PC-12 cells were more effectively decreased by ECPE than ECE treatments. From the results obtained in this study, we concluded that ECPE, which is rich in phlorotannins, including the marker compound dieckol, may be applied to the development of functional materials for improving cognition and memory.

Keywords

References

  1. Kumar A, Singh A. 2015. A review on Alzheimer's disease pathophysiology and its management: an update. Pharmacol. Rep. 67: 195-203. https://doi.org/10.1016/j.pharep.2014.09.004
  2. Akagi M, Matsui N, Akae H, Hirashima N, Fukuishi N, Fukuyama Y, et al. 2015. Nonpeptide neurotrophic agents useful in the treatment of neurodegenerative diseases such as Alzheimer's disease. J. Pharmacol. Sci. 127: 155-163. https://doi.org/10.1016/j.jphs.2014.12.015
  3. Xu Q, He C, Xiao C, Chen X. 2016. Reactive oxygen species (ROS) responsive polymers for biomedical applications. Macromol. Biosci. 16: 635-646. https://doi.org/10.1002/mabi.201500440
  4. Watts ME, Pocock R, Claudianos C. 2018. Brain energy and oxygen metabolism: emerging role in normal function and disease. Front. Mol. Neurosci. 11: 216. https://doi.org/10.3389/fnmol.2018.00216
  5. Magistretti PJ, Allaman I. 2015. A cellular perspective on brain energy mtabolism and functional imaging. Neuron 86: 883-901. https://doi.org/10.1016/j.neuron.2015.03.035
  6. Patel AB, Lai JCK, Chowdhury GMI, Hyder F, Rothman DL, Shulman RG, et al. 2014. Direct evidence for activity-dependent glucose phosphorylation in neurons with implications for the astrocyte-to-neuron lactate shuttle. Proc. Natl. Acad. Sci. USA 111: 5385-5390. https://doi.org/10.1073/pnas.1403576111
  7. Turrens JF. 2003. Mitochondrial formation of reactive oxygen species. J. Physiol. 552(Pt 2): 335-344. https://doi.org/10.1113/jphysiol.2003.049478
  8. Polster BM, Basanez G, Young M, Suzuki M, Fiskum G. 2003. Inhibition of Bax-induced cytochrome c release from neural cell and brain mitochondria by dibucaine and propranolol. J. Neurosci. 23: 2735-2743. https://doi.org/10.1523/jneurosci.23-07-02735.2003
  9. Mecocci P, MacGarvey U, Beal MF. 1994. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 36: 747-751. https://doi.org/10.1002/ana.410360510
  10. Rosa GP, Tavares WR, Sousa PMC, Pages AK, Seca AML, Pinto DCGA. 2020. Seaweed secondary metabolites with beneficial health effects: an overview of successes in in vivo studies and clinical trials. Mar. Drugs 18: 8.
  11. Olasehinde TA, Olaniran AO, Okoh AI. 2019. Macroalgae as a valuable source of naturally occurring bioactive compounds for the treatment of Alzheimer's disease. Mar. Drugs 17: 609. https://doi.org/10.3390/md17110609
  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. Biotech. 28: 40-49. https://doi.org/10.4014/jmb.1710.10043
  13. Nho JA, Shin YS, Jeong H-R, Cho S, Heo HJ, Kim GH, et al. 2020. Neuroprotective effects of phlorotannin-rich extract from brown seaweed Ecklonia cava on neuronal PC-12 and SH-SY5Y cells with oxidative stress. J. Microbiol. Biotech. 30: 359-367. https://doi.org/10.4014/jmb.1910.10068
  14. Park SK, Kang JY, Kim JM, Yoo SK, Hye Ju Han, Chung DH, et al. 2019. Fucoidan-rich substances from Ecklonia cava improve trimethyltin-induced cognitive dysfunction via down-regulation of amyloid production/tau hyperphosphorylation. Mar. Drugs 17: 591. https://doi.org/10.3390/md17100591
  15. Plaza M, Cifuentes A, Ibanez E. 2008. In the search of new functional food ingredients from algae. Trends Food Sci. Technol. 19: 31-39. https://doi.org/10.1016/j.tifs.2007.07.012
  16. Sanjeewa KKA, Jeon Y-J. 2018. Edible brown seaweeds: a review. J. Food Bioact. 2: 37-50.
  17. Wijesekara I, Yoon NY, Kim S-K. 2010. Phlorotannins from Ecklonia cava (Phaeophyceae): biological activities and potential health benefits. Biofactors 36: 408-414. https://doi.org/10.1002/biof.114
  18. Ahn G-N, Kim K-N, Cha S-H, Song C-B, Lee J, Heo M-S, et al. 2007. Antioxidant activities of phlorotannins purified from Ecklonia cava on free radical scavenging using ESR and H2O2-mediated DNA damage. Eur. Food Res. Technol. 226: 71-79. https://doi.org/10.1007/s00217-006-0510-y
  19. Lee SH, 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. https://doi.org/10.1002/jsfa.3623
  20. 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
  21. Jeong H-R, Cho H-S, Cho Y-S, Kim D-O. 2020. Changes in phenolics, soluble solids, vitamin C, and antioxidant capacity of various cultivars of hardy kiwifruits during cold storage. Food Sci. Biotechnol. 29: 1763-1770. https://doi.org/10.1007/s10068-020-00822-7
  22. 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 Aβ-induced oxidative stress in PC12 cells. Amyloid-J. Protein Fold. Disord. 8: 194-201. https://doi.org/10.3109/13506120109007362
  23. 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
  24. Piao MJ, Kang KA, Zhang R, Ko DO, Wang ZH, You HJ, et al. 2008. Hyperoside prevents oxidative damage induced by hydrogen peroxide in lung fibroblast cells via an antioxidant effect. BBA-Gen. Subjects 1780: 1448-1457. https://doi.org/10.1016/j.bbagen.2008.07.012
  25. 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 H2O2-induced oxidative stress in murine hippocampal HT22 cells. Environ. Toxicol. Pharmacol. 34: 96-105. https://doi.org/10.1016/j.etap.2012.03.006
  26. Segawa K, Nagata S. 2015. An apoptotic 'eat me' signal: phosphatidylserine exposure. Trends Cell Biol. 25: 639-650. https://doi.org/10.1016/j.tcb.2015.08.003
  27. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A. 2002. Selective cytotoxicity of intracellular amyloid β peptide1-42 through p53 and Bax in cultured primary human neurons. J. Cell Biol. 156: 519-529. https://doi.org/10.1083/jcb.200110119
  28. Okouchi M, Ekshyyan O, Maracine M, Aw TY. 2007. Neuronal apoptosis in neurodegeneration. Antioxid. Redox. Signal. 9: 1059-1096. https://doi.org/10.1089/ars.2007.1511
  29. Youle RJ, Strasser A. 2008. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9: 47-59. https://doi.org/10.1038/nrm2308
  30. Salakou S, Kardamakis D, Tsamandas AC, Zolota V, Apostolakis E, Tzelepi V, et al. 2007. Increased Bax/Bcl-2 ratio up-regulates caspase-3 and increases apoptosis in the thymus of patients with myasthenia gravis. In Vivo 21: 123-132.