Abstract
Chronic exposure of the skin to ultraviolet B (UVB) radiation induces oxidative stress, which plays a crucial role in the induction of skin aging. In this study, potential protective effect of extracts of six species of brown seaweeds on UVB radiation-induced cell damage was assessed via cell viability in HaCaT cells. The Ecklonia cava extract showed a profound protective effect against UVB radiation-induced cell damage, compared to that exhibited by other brown seaweed extracts. Thus, E. cava was selected for use in further experiments and was extracted with different solvents. The protection effect was evaluated via DCFH-DA, MTT, and morphological changes in HaCaT cells. Profound protective effect against UVB radiation-induced cell damage was detected in the 100% methanol extract. Partitioning of the 100% methanol extract with different organic solvents revealed a pronounced protective effect in the ethyl acetate fraction. The isolated active compounds were phlorotannins, especially dieckol, as identified using ultra-performance liquid chromatography-tandem mass spectrometry. Among the phlorotannins, dieckol showed a higher protective effect on UVB-induced cell damage in HaCaT cells than the other phlorotannins. Therefore, UVB protection of dieckol was evaluated via DCFH-DA, DAF-FM DA, acridine orange, and morphological changes in zebrafish model. Reactive oxygen species, nitric oxide, and cell death in live zebrafish induced by UVB radiation were reduced by the addition of dieckol. These results indicated that dieckol has potential protective effects on UVB-induced skin damage, which might be useful in pharmaceutical and cosmetic formulations.
References
Afaq F, Adhami VM, Mukhtar H (2005) Photochemoprevention of ultraviolet B signaling and photocarcinogenesis. Mutat Res 571:153–173
Afaq F, Syed DN, Malik A, Hadi N, Sarfaraz S, Kweon MH, Khan N, Zaid MA, Mukhtar H (2007) Delphinidin, an anthocyanidin in pigmented fruits and vegetables, protects human HaCaT keratinocytes and mouse skin against UVB-mediated oxidative stress and apoptosis. J Invest Dermatol 127:222–232
Ahn GN, Kim KN, Cha SH, Song CB, Lee JH, Heo MS, Yeo IK, Lee NH, Jee YH, Kim JS, Heu MS, Jeon YJ (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
Athukorala Y, Jeon YJ (2005) Screening for angiotensin I-converting enzyme inhibitory activity of Ecklonia cava. J Food Sci Nutr 10:134–139
Balogh A, Paragh JG, Juhasz A, Kobling T, Torocsik D, Miko E, Varga V, Emri Z, Horkay I, Scholtz B, Remenyik E (2008) Reference genes for quantitative real time PCR in UVB irradiated keratinocytes. J Photochem Photobiol B Biol 93:133–139
Bowden GT (2004) Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signaling. Nat Rev Cancer 4:23–35
Carini M, Aldini G, Bombardelli E, Morazzoni P, Maffei FR (2000) UVB-induced hemolysis of rat erythrocytes: protective effect of procyanidins from grape seeds. Life Sci 67:1799–1814
Choi TY, Kim JH, Ko DH, Kim CH, Hwang JS, Ahn S, Kim SY, Kim CD, Lee JH, Yoon TJ (2007) Zebrafish as a new model for phenotyoe-based screening of melanogenic regulatory compounds. Pigment Cell Res 20:120–127
Cimino F, Cristani M, Saija A, Bonina FP, Virgili F (2008) Protective effects of a red orange extract on UVB-induced damage in human keratinocytes. Biofactors 30:129–138
Dapkevicius A, Venakutonis R, van Beek TA, Linssen JPH (1998) Antioxidant activity of extracts obtained by different isolation procedures from some aromatic herbs grown in Lithuania. J Sci Food Agric 77:140–146
Eisen JS (1996) Zebrafish make a big splash. Cell 87:969–977
F'guyer S, Afaq F, Mukhtar H (2003) Photochemoprevention of skin cancer by botanical agents. Photodermatol Photoimmunol Photomed 19:56–72
Fiers W, Bevaert R, Declercq W, Vandenabeele P (1999) More than one way to die: apoptosis and necrosis and reactive oxygen species. Oncogene 18:7719–7730
Fishman MC (1999) Zebrafish genetics: the enigma if arrival. Proc Natl Acad Sci 96:10554–10556
Gonzalez AG, Darias V, Estevez E (1982) Chemotherapeutic activity of polyhalogenated terpenes from Spanish algae. Planta Med 44:44–46
Halliday GM (2005) Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat Res 571:107–120
Handa O, Kokura S, Adachi S, Takagi T, Naito Y, Tanigawa T, Yoshida N, Yoshikawa T (2006) Methylparaben potentiates UV-induced damage of skin keratinocytes. Toxicology 227:62–72
Henry TR, Spitsbergen JM, Hornung MW, Abnet CC, Peterson RE (1997) Early life stage toxicity of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in zebrafish (Danio rerio). Toxicol Appl Pharmacol 142:56–58
Heo SJ, Jeon YJ (2008) Radical scavenging capacity and cytoprotective effect of enzymatic digests of Ishige okamurae. J Appl Phycol 20:1087–1095
Heo SJ, Jeon YJ (2009) Evaluation of diphlorethohydroxycarmalol isolated from Ishige okamurae for radical scavenging activity and its protective effect against H2O2-induced cell damage. Process Biochem 44:412–418
Heo SJ, Park EJ, Lee KW, Jeon YJ (2005) Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresour Technol 96:1613–1623
Hill AJ, Teraoka H, Heideman W, Peterson RE (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86:6–19
Ishida T, Sakaguchi I (2008) Protection of human keratinocytes from UVB-induced inflammation using root extract of Lithospermum erythrorhizon. Biol Pharm Bull 30:928–934
Jung WK, Choi I, Oh S, Park SG, Seo SK, Lee SW, Lee DS, Heo SJ, Jeon YJ, Je JY, Ahn CB, Kim JS, Oh KS, Kim YM, Moon C, Choi IW (2009) Anti-asthmatic effect of marine red alga (Laurencia undulata) polyphenolic extracts in a murine model of asthma. Food Chem Toxicol 47:293–297
Kang KA, Lee KH, Chae S, Zhang R, Jung MS, Lee Y, Kim SY, Kim HS, Joo HG, Park JW, Hyun JW (2005) Eckol isolated from Ecklonia cava attenuates oxidative stress induced cell damage in lung fibroblast cells. FEBS Lett 579:6295–6304
Kang KA, Zhang R, Lee KH, Chae S, Kim BS, Kwak YS, Park JW, Lee NH, Hyun JW (2006) Protective effect of triphlorethol-A from Ecklonia cava against ionizing radiation in vitro. J Radiat Res 47:61–68
Kashiwagi M, Mynderse JS, Moore RE, Norton TR (1980) Antineoplastic evaluation of pacific basin marine algae. J Pharm Sci 69:735–738
Kim EM, Yang HS, Kang SW, Ho JN, Lee SB, Um HD (2008) Amplification of the γ--irradiation-induced cell death pathway by reactive oxygen species in human U937 cells. Cell Signal 20:916–924
Kim YG, Maho S, Masahiro S, Yoshiyuki K (2009) Effects of ginseng saponins isolated from red ginseng on ultraviolet B-induced skin aging in hairless mice. Eur J Pharmacol 602:148–156
Konstantin T, Park HB, Kim YM, Chung JI, Shin SC, Shim HJ, Lee WS, Seo HG, Lee JH, Chang KC (2008) Protective effect of anthocyanins from black soybean seed coats on UVB-induced apoptotic cell death in vitro and in vivo. J Agric Food Chem 56:10600–10605
Kosovel V, Avanzini A, Scarcia V, Furlani A (1988) Algae as possible sources of antitumoral agents. Preliminary evaluation of the in vitro cytostatic activity of crude extracts. Pharmacol Res Commun 20:27–31
Kotake-Nara E, Asai A, Nago A (2005) Neoxanthin and fucoxanthin induce apoptosis in PC-3 human prostate cancer cells. Cancer Lett 220:75–84
Langheinrich U, Hennen E, Stott G, Vacun G (2002) Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr Biol 12:2023–2028
Lee SH, Athukorala Y, Lee JS, Jeon YJ (2008) Simple separation of anticoagulant sulfated galactan from marine red algae. J Appl Phycol 20:1053–1059
Lisbeth A, Pacheco P, Giuliana N, Lal H, Stephen TT, Susanne U, Mertens T (2008) Protective effects of standardized pomegranate (Punica granatum L.) polyphenolic extract in ultraviolet-irradiated human skin fibroblasts. J Agric Food Chem 56:8434–8441
Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192:1–15
Mayer AMS, Hamann MT (2004) Marine pharmacology in 2000: marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiplatelet, antiprotozoal, anti-tuberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems and other miscellaneous mechanisms of action. Mar Biotechnol 6:37–52
Moriwaki S, Takahashi Y (2007) Photoaging and DNA repair. J Dermatol Sci 50:169–176
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to roliferation and cytotoxicity assays. J Immunol Meth 65:55–63
Nagayama K, Iwamura Y, Shibata T, Hirayama I, Nakamura T (2002) Bactericidal activity of phlorotannins from the brown alga Ecklonia kurome. J Antimicrob Chemother 50:889–893
Naito Y, Handa O, Takagi T, Ishikawa T, Imamoto E, Nakagawa S, Yamaguchi T, Yoshida N, Matsui H, Yoshikawa T (2002) Ubiquitin-proteasome inhibitor enhances tumor necrosis factor-alpha-induced apoptosis in rat gastric epithelial cells. Aliment Pharmacol Ther 16(suppl 2):59–66
Podda M, Traber MG, Weber C, Lan LJ, Packer L (1992) UV-irradiation depletes antioxidants and cause oxidative damage in a model of human skin. Photochem Photobiol 56:357–363
Ramachandran S, Rajendra PN (2008) Effect of ursolic acid, a triterpenoid antioxidant, on ultraviolet-B radiation-induced cytotoxicity, lipid peroxidation and DNA damage in human lymphocytes. Chem Biol Interact 176:99–107
Scholz E, Rimpler H (1989) Proanthocyanidins from Krameria triandra root. Planta Med 55:379–384
Schwarz A, Maeda A, Gan D, Mammone T, Matsui MS, Schwarz T (2008a) Green tea phenol extracts reduce UVB-induced DNA damage in human cells via interleukin-12. Photochem Photobiol 84:350–355
Schwarz M, Rodriguez MC, Martinez C, Bosquet V, Guillen D, Barroso CG (2008b) Antioxidant activity of Brandy de Jerez and other aged distillates, and correlation with their polyphenolic content. Food Chem 116:29–33
Tomaino A, Cristani M, Cimino F, Speciale A, Trombetta D, Bonina F, Saija A (2006) In vitro protective effect of a Jacquez grapes wine extract on UVB-induced skin damage. Toxicol In Vitro 20:1395–1402
Torres MA, Barros MP, Campos SC, Pinto E, Rajamani S, Sayre RT, Colepicolo P (2008) Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol Environ Saf 71:1–15
Vayalil PK, Elments CA, Katiyar SK (2003) Treatment of green tea polyphenols in hydrophilic cream prevents UVB-induced oxidation of lipids and proteins, depletion of antioxidant enzymes and phosphorylation of MAPK proteins in SKH-1 hairless mouse skin. Carcinogenesis 24:927–936
Veerman EC, Nazmi K, Hof WV, Bolscher JG, Hertog ALD, Amerongen AVN (2004) Reactive oxygen species play no role in the candidacidal activity of the salivary antimicrobial peptide histatin 5. Biochem J 381:447–452
Wang Y, Biswas G, Prabu SK, Avadhani NG (2006) Modulation of mitochondrial metabolic function by phorbol 12-myristate 13-acetate through increased mitochondrial translocation of protein kinase Cα in C2C12 myocytes. Biochem Pharmacol 72:881–892
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This research was supported by a grant from the Marine Bioprocess Research Center of the Marine Bio 21 Center, funded by the Ministry of Marine Affairs and Fisheries, Republic of Korea.
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Ko, SC., Cha, SH., Heo, SJ. et al. Protective effect of Ecklonia cava on UVB-induced oxidative stress: in vitro and in vivo zebrafish model. J Appl Phycol 23, 697–708 (2011). https://doi.org/10.1007/s10811-010-9565-z
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DOI: https://doi.org/10.1007/s10811-010-9565-z