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Protective effect of a freshwater alga, Spirogyra sp., against lipid peroxidation in vivo zebrafish and purification of antioxidative compounds using preparative centrifugal partition chromatography

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Abstract

A freshwater alga, Spirogyra sp., collected in shallow ponds in South Korea, was evaluated for its antilipid peroxidative effect against 2,2′-azobis (2-amidinopropane) dihydrochloride (AAPH)-induced in vivo zebrafish, and antioxidative compounds from the alga were efficiently identified using 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS+) online high-performance liquid chromatography (HPLC) and preparative centrifugal partition chromatography. The ethyl acetate fraction of Spirogyra sp. (SPE) in each fraction showed the strongest 2,2-diphenyl-1-picrylhydrazyl scavenging activity and significantly scavenged 2′,7′-dichlorodihydrofluorescein diacetate and diphenyl-1-pyrenylphosphine fluorescence, respectively, in AAPH-induced zebrafish embryo without any cytotoxicity in the concentrations between 25 and 50 μg mL−1. The two main antioxidative compounds in SPE were confirmed by ABTS+ online HPLC and were identified as gallic acid and methyl gallate, respectively, by HPLC–diode array detection (DAD)–electrospray ionization (ESI)/mass spectrometry (MS), 1H- and 13C-NMR. We conclude therefore that Spirogyra sp. is rich in gallic acid and methyl gallate, and it might be useful as a strong antilipid peroxidation material.

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References

  • Ames BN (1998) Micronutrients prevent cancer and delay aging. Toxicol Lett 102–103:5–18

    Article  PubMed  Google Scholar 

  • Bozidar LM, Sonja MD, Jasna MCB (1998) Antioxidative activity of phenolic compounds on the metal-ion breakdown of lipid peroxidation system. Food Chem 61:443–447

    Article  Google Scholar 

  • Cannell RJP, Farmer P, Walker JM (1988) Purification and characterization of pentagalloylglucose, and α-glucosidase inhibitor/antibiotic from the freshwater green alga Spirogyra varians. Biochem J 255:937–941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi MW, Kim JI (2013) Anti-inflammatory effect of ethyl acetate fraction isolated from Undaria pinnatifida on lipopolysaccharides-stimulated RAW 264.7 cells. Kor J Fish Aquat Sci 46:384–392

    CAS  Google Scholar 

  • Cholbi MR, Paya M, Alcaraz MJ (1991) Inhibitory effects of phenolic compounds on CCl4-induced microsomal lipid peroxidation. Experientia 47:195–199

    Article  CAS  PubMed  Google Scholar 

  • Cox DA, Cohen ML (1996) Effects of oxidized low-density lipoprotein on vascular contraction and relaxation: clinical and pharmacological implications in atherosclerosis. Pharmacol Rev 48:3–19

    CAS  PubMed  Google Scholar 

  • Dodoa K, Minatoa Suganumac TNYM, Hashimotoa Y (2008) Antiproliferative and apoptosis-inducing activities of alkyl gallate and gallamide derivatives related to (−)-epigallocatechin gallate. Bioorg Med Chem 16:7975–7982

    Article  Google Scholar 

  • Eisen JS (1996) Zebrafish make a big splash. Cell 87:969–977

    Article  CAS  PubMed  Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    Article  CAS  PubMed  Google Scholar 

  • Fishman MC (1999) Zebrafish genetics: the enigma of arrival. Proc Natl Acad Sci U S A 96:10554–10556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han SS, Lo SC, Choi YW, Kim JH, Baek SH (2004) Antioxidant activity of crude extract and pure compounds of Acer ginnala Max. B Korean Chem Soc 25:389–391

    Article  CAS  Google Scholar 

  • Han JW, Yoon M, Kupper FD, Klochkova TA, Oh JS, Rho JR, Kim GH (2012) Accumulation of galloyl dericatives in a green alga, Spirogyra varians, in response to cold stress. J Appl Phycol 24:1279–1286

    Article  CAS  Google Scholar 

  • Hansi PD, Stanely MPP (2009) Cardioprotective effect of gallic acid on cardiac troponin-T, cardiac marker enzymes, lipid peroxidation products and antioxidants in experimentally induced myocardial infarction in Wistar rats. Chem Biol Interact 179:118–124

    Article  Google Scholar 

  • Harman D (1994) Aging: prospects for further increases in the functional life span. Age 17:119–146

    Article  CAS  Google Scholar 

  • Hiramoto K, Johkoh H, Sako K, Kikugawa K (1993) DNA breaking activity of the carbon-centered radical generated from 2,2-azobis (2-amidinopropane) hydrochloride (AAPH). Free Radical Res Com 19:323–332

    Article  CAS  Google Scholar 

  • Hsieh TJ, Liu TZ, Chia YC, Chern CL, Lu FJ, Chuang MC (2004) Protective effect of methyl gallate from Toona sinensis (Meliaceae) against hydrogen peroxide-induced oxidative stress and DNA damage in MDCK cells. Food Chem Toxicol 42:843–850

    Article  CAS  PubMed  Google Scholar 

  • Ivanova A, Khotimchenko S, Toneva A, Marinova E, Dimitroba-Konaklieva S, Stefanov K (2002) Lipid composition and antioxidative effectivity of different Spirogyra species. Bulg Acad Sci 55:47–50

    CAS  Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dynam 203:253–310

    Article  CAS  Google Scholar 

  • Ko JY, Lee JH, Samarakoon K, Kim JS, Jeon YJ (2013) Purification and determination of two novel antioxidant peptides from flounder fish (Paralichthys olivaceus) using digestive proteases. Food Chem Toxicol 52:113–120

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Yoon M, Sung NY, Choi JI (2012) Spirogyra varians mutant generated by high dose gamma-irradiation shows increased antioxidant properties. Radiat Phys Chem 81:1017–1019

    Article  CAS  Google Scholar 

  • Lee JH, Ko JY, Samarakoon K, Oh JY, Heo SJ, Kim CY, Nah JW, Jang MK, Lee JS, Jeon YJ (2013a) Preparative isolation of sargachromanol E from Sargassum siliquastrum by centrifugal partition chromatography and its anti-inflammatory activity. Food Chem Toxicol 62:54–60

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Kang MC, Moon SH, Jeon BT, Jeon YJ (2013b) Potential use of ultrasound in antioxidant extraction from Ecklonia cava. Algae 28:371–378

    Article  CAS  Google Scholar 

  • Lee JH, Ko JY, Oh JY, Kim CY, Lee HJ, Kim J, Jeon YJ (2014) Preparative isolation and purification of phlorotannins from Ecklonia cava using centrifugal partition chromatography by one-step. Food Chem 158:433–437

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Qian ZJ, Ryu BM, Lee SH, Kim MM, Kim SK (2009) Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg Med Chem 17:1963–1973

    Article  CAS  PubMed  Google Scholar 

  • Lin E, Calvano SE, Lowry SF (2000) Inflammatory cytokines and cell response in surgery. Surgery 127:117–126

    Article  CAS  PubMed  Google Scholar 

  • Lu Z, Nie G, Belton PS, Tang H, Zhao B (2006) Structure–activity relationship analysis of antioxidant ability and neuroprotective effect of gallic acid derivatives. Neurochem Int 48:263–274

    Article  CAS  PubMed  Google Scholar 

  • Masuoka N, Nihei KI, Kubo I (2006) Xanthine oxidase inhibitory activity of alkyl gallates. Mol Nutr Food Res 50:725–731

    Article  CAS  PubMed  Google Scholar 

  • Mayo JC, Tan DX, Saing RM, Lopez-Burilli S, Reiter RJ (2003) Oxidative damage to catalase induced by peroxyl radicals: functional protection by melatonin and other and other antioxidants. Free Radical Res 37:543–553

    Article  CAS  Google Scholar 

  • Nakai S, Inoue Y, Hosomi M, Murakami A (2000) Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Res 34:3026–3032

    Article  CAS  Google Scholar 

  • Nakayama T, Niimi T, Osawa T, Kawakishi S (1992) The protective role of polyphenols in cytotoxicity of hydrogen peroxide. Animal Cell Technol: Basic Appl Asp 4:571–576

    Google Scholar 

  • Nanjo F, Goto K, Seto R, Suzuki M, Sakai M, Hara Y (1996) Scavenging effects of tea catechins and their derivatives on 1,1-diphenyl-2-picrylydrazyl radical. Free Radical Biol Med 21:895–902

    Article  CAS  Google Scholar 

  • Niki E (1990) Free radical initiators as source of water- or lipid-soluble peroxyl radicals. Meth Enzymol 186:100–108

    Article  CAS  PubMed  Google Scholar 

  • Pichler FB, Laurenson S, Williams LC, Dodd A, Copp BR, Love DR (2003) Chemical discovery and global gene expression analysis in zebrafish. Nat Biotechnol 21:879–883

    Article  CAS  PubMed  Google Scholar 

  • Roedig-Penman A, Gordon MH (1997) Antioxidant properties of catechins and green tea extracts in model food emulsions. J Agr Food Chem 45:4267–4270

    Article  CAS  Google Scholar 

  • Shahidi F, Janitha PK, Wanasundara PD (1992) Phenolic antioxidants. Crit Rev Food Sci 32:67–103

    Article  CAS  Google Scholar 

  • Thumvijit T, Thuschana W, Amornlerdpison D, Peerapornpisal Y, Wongpoomchai R (2013) Evaluation of hepatic antioxidant capacities of Spirogyra neglecta (Hassall) Kützing in rats. Interdiscip Toxicol 6:152–156

    Article  PubMed  PubMed Central  Google Scholar 

  • Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266:37–56

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Feinstein SI, Fisher AB (2008) Peroxiredoxin 6 as an antioxidant enzyme: protection of lung alveolar epithelial type II cells from H2O2-induced oxidative stress. J Cell Biochem 104:1274–1285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu WJ, Chang CC, Kuo TF, Tsai TC, Chang SJ (2012) Toona sinensis Roem leaf extracts improve antioxidant activity in the liver of rats under oxidative stress. Food Chem Toxicol 50:1860–1865

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Ministry of Agriculture, Food and Rural Affairs (MAFRA), Ministry of Oceans and Fisheries (MOF), Rural Development Administration (RDA), and Korea Forest Service (KFS) (213004-04-2-SB930)

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Correspondence to Gwang Hoon Kim or You-Jin Jeon.

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Ji-Hyeok Lee, Jong Won Han, Gwang Hoon Kim and You-Jin Jeon contributed equally to this work.

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Lee, JH., Han, J.W., Ko, JY. et al. Protective effect of a freshwater alga, Spirogyra sp., against lipid peroxidation in vivo zebrafish and purification of antioxidative compounds using preparative centrifugal partition chromatography. J Appl Phycol 28, 181–189 (2016). https://doi.org/10.1007/s10811-015-0548-y

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  • DOI: https://doi.org/10.1007/s10811-015-0548-y

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