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http://dx.doi.org/10.4490/algae.2017.32.11.29

Protective effect of gallic acid derivatives from the freshwater green alga Spirogyra sp. against ultraviolet B-induced apoptosis through reactive oxygen species clearance in human keratinocytes and zebrafish  

Wang, Lei (Department of Marine Life Sciences, Jeju National University)
Ryu, BoMi (Department of Marine Life Sciences, Jeju National University)
Kim, Won-Suk (Major in Pharaceutical Engineering Division of Bio-Industry, Silla University)
Kim, Gwang Hoon (Department of Biology, Kongju National University)
Jeon, You-Jin (Department of Marine Life Sciences, Jeju National University)
Publication Information
ALGAE / v.32, no.4, 2017 , pp. 379-388 More about this Journal
Abstract
In the present study, we enhanced the phenolic content of 70% ethanol extracts of Spirogyra sp. (SPE, $260.47{\pm}5.21$ gallic acid equivalent $[GAE]mg\;g^{-1}$), 2.97 times to $774.24{\pm}2.61GAE\;mg\;g^{-1}$ in the ethyl acetate fraction of SPE (SPEE). SPEE was evaluated for its antiradical activity in online high-performance liquid chromatography-ABTS analysis, and the peaks with the highest antiradical activities were identified as gallic acid derivatives containing gallic acid, methyl gallate, and ethyl gallate. Isolation of ethyl gallate from Spirogyra sp. was performed for the first time in this study. In ultraviolet B (UVB)-irradiated keratinocytes (HaCaT cells), SPEE improved cell viability by 8.22%, and 23.33% and reduced accumulation of cells in the sub-$G_1$ phase by 20.53%, and 32.11% at the concentrations of 50 and $100{\mu}g\;mL^{-1}$, respectively. Furthermore, SPEE (50 and $100{\mu}g\;mL^{-1}$) reduced reactive oxygen species generation in UVB-irradiated zebrafish by 66.67% and 77.78%. This study suggests a protective activity of gallic acid and its derivatives from Spirogyra sp. against UVB-induced stress responses in both in vitro and in vivo models, suggesting a potential use of SPEE in photoprotection.
Keywords
apoptosis; gallic acid derivatives; phenolic content; reactive oxygen species; Spirogyra sp.; ultraviolet B;
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Times Cited By KSCI : 8  (Citation Analysis)
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1 Eshaq, F. S., Ali, M. N. & Mohd, M. K. 2010. Spirogyra biomass a renewable source for biofuel (bioethanol) production. Int. J. Eng. Sci. Technol. 2:7045-7054.
2 Masaki, H. 2010. Role of antioxidants in the skin: anti-aging effects. J. Dermatol. Sci. 58:85-90.   DOI
3 Mohan, S. V., Ramanaiah, S. V., Rajkumar, B. & Sarma, P. N. 2007. Removal of fluoride from aqueous phase by biosorption onto algal biosorbent Spirogyra sp.-IO2: sorption mechanism elucidation. J. Hazard. Mater. 141:465-474.   DOI
4 Oh, J. -Y., Fernando, I. P. S. & Jeon, Y. -J. 2016. Potential applications of radioprotective phytochemicals from marine algae. Algae 31: 403-414.   DOI
5 Ramaraj, R., Unpaprom, Y., Whangchai, N. & Dussadee, N. 2015. Culture of macroalgae Spirogyra ellipsospora for long-term experiments, stock maintenance and biogas production. Emerg. Life Sci. Res. 1:38-45.
6 Raut, S., Bhadoriya, S. S., Uplanchiwar, V., Mishra, V., Gahane, A. & Jain, S. K. 2012. Lecithin organogel: a unique micellar system for the delivery of bioactive agents in the treatment of skin aging. Acta Pharm. Sin. B 2:8-15.   DOI
7 Rezvani, H. R., Mazurier, F., Cario-Andre, M., Pain, C., Ged, C., Taieb, A. & de Verneuil, H. 2006. Protective effects of catalase overexpression on UVB-induced apoptosis in normal human keratinocytes. J. Biol. Chem. 281:17999-18007.   DOI
8 Farooqi, A. A., Li, R. -N., Huang, H. -W., Ismail, M., Yuan, S. -S. F., Wang, H. -M. D., Liu, J. -R., Tang, J. -Y. & Chang, H. -W. 2015. Natural products mediated regulation of oxidative stress and DNA damage in ultraviolet exposed skin cells. Curr. Pharm. Biotechnol. 16:1078-1084.   DOI
9 Fernando, I. P. S., Kim, H. -S., Sanjeewa, K. K. A., Oh, J. -Y., Jeon, Y. -J. & Lee, W. W. 2017a. Inhibition of inflammatory responses elicited by urban fine dust particles in keratinocytes and macrophages by diphlorethohydroxycarmalol isolated from a brown alga Ishige okamurae. Algae 32:261-273.   DOI
10 Fernando, I. P. S., Sanjeewa, K. K. A., Samarakoon, K. W., Lee, W. W., Kim, H. -S., Kim, E. -A., Gunasekara, U. K. D. S. S., Abeytunga, D. T. U., Nanayakkara, C., de Silva, E. D., Lee, H. -S. & Jeon, Y. -J. 2017b. FTIR characterization and antioxidant activity of water soluble crude polysaccharides of Sri Lankan marine algae. Algae 32:75-86.   DOI
11 Gill, S. S. & Tuteja, N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48:909-930.   DOI
12 Gupta, V. K. & Rastogi, A. 2008. Biosorption of lead from aqueous solutions by green algae Spirogyra species: kinetics and equilibrium studies. J. Hazard. Mater. 152:407-414.   DOI
13 Gupta, V. K., Rastogi, A., Saini, V. K. & Jain, N. 2006. Biosorption of copper (II) from aqueous solutions by Spirogyra species. J. Colloid Interface Sci. 296:59-63.   DOI
14 Gupta, V. K., Shrivastava, A. K. & Jain, N. 2001. Biosorption of chromium (VI) from aqueous solutions by green algae Spirogyra species. Water Res. 35:4079-4085.   DOI
15 Heo, S. -J., Ko, S. -C., Cha, S. -H., Kang, D. -H., Park, H. -S., Choi, Y. -U., Kim, D., Jung, W. -K. & Jeon, Y. -J. 2009. Effect of phlorotannins isolated from Ecklonia cava on melanogenesis and their protective effect against photo-oxidative stress induced by UV-B radiation. Toxicol in Vitro 23:1123-1130.   DOI
16 Ryu, B., Ahn, B. -N., Kang, K. -H., Kim, Y. -S., Li, Y. -X., Kong, C. -S., Kim, S. -K. & Kim, D. G. 2015. Dioxinodehydroeckol protects human keratinocyte cells from UVB-induced apoptosis modulated by related genes Bax/Bcl-2 and caspase pathway. J. Photochem. Photobiol. B Biol. 153:352-357.   DOI
17 Samarakoon, K. W., Cha, S. -H., Lee, J. -H. & Jeon, Y. -J. 2013. The growth, innate immunity and protection against $H_2O_2$-induced oxidative damage of a chitosan-coated diet in the olive flounder Paralichthys olivaceus. Fish. Aquat. Sci. 16:149-158.
18 Sanjeewa, K. K. A., Fernando, I. P. S., Samarakoon, K. W., Lakmal, H. H. C., Kim, E. -A., Kwon, O. -N., Dilshara, M. G., Lee, J. -B. & Jeon, Y. -J. 2016. Anti-inflammatory and anticancer activities of sterol rich fraction of cultured marine microalga Nannochloropsis oculata. Algae 31:277-287.   DOI
19 Wijesinghe, W. A. J. P., Jeon, Y. J., Ramasamy, P., Wahid, M. E. A. & Vairappan, C. S. 2013. Anticancer activity and mediation of apoptosis in human HL-60 leukaemia cells by edible sea cucumber (Holothuria edulis) extract. Food Chem. 139:326-331.   DOI
20 Yang, H. -M., Ham, Y. -M., Yoon, W. -J., Roh, S. W., Jeon, Y. -J., Oda, T., Kang, S. -M., Kang, M. -C., Kim, E. -A., Kim, D. & Kim, K. -N. 2012. Quercitrin protects against ultraviolet B-induced cell death in vitro and in an in vivo zebrafish model. J. Photochem. Photobiol. B Biol. 114:126-131.   DOI
21 Heo, S. -J., Ko, S. -C., Kang, S. -M., Cha, S. -H., Lee, S. -H., Kang, D. -H., Jung, W. -K., Affan, A., Oh, C. & Jeon, Y. -J. 2010. Inhibitory effect of diphlorethohydroxycarmalol on melanogenesis and its protective effect against UV-B radiation-induced cell damage. Food Chem. Toxicol. 48:1355-1361.   DOI
22 Hwang, J. -H., Kim, K. -J., Ryu, S. -J. & Lee, B. -Y. 2016. Caffeine prevents LPS-induced inflammatory responses in RAW264.7 cells and zebrafish. Chem. Biol. Interact. 248:1-7.   DOI
23 Kammeyer, A. & Luiten, R. M. 2015. Oxidation events and skin aging. Ageing Res. Rev. 21:16-29.   DOI
24 Kang, M. -C., Kim, S. Y., Kim, Y. T., Kim, E. -A., Lee, S. -H., Ko, S. -C., Wijesinghe, W. A. J. P., Samarakoon, K. W., Kim, Y. -S., Cho, J. H., Jang, H. -S. & Jeon, Y. -J. 2014. In vitro and in vivo antioxidant activities of polysaccharide purified from aloe vera (Aloe barbadensis) gel. Carbohydr. Polym. 99:365-371.   DOI
25 Kang, N., Lee, J. -H., Lee, W., Ko, J. -Y., Kim, E. -A., Kim, J. -S., Heu, M. -S., Kim, G. H. & Jeon, Y. -J. 2015. Gallic acid isolated from Spirogyra sp. improves cardiovascular disease through a vasorelaxant and antihypertensive effect. Environ. Toxicol. Pharmacol. 39:764-772.   DOI
26 Kim, H. -S., Zhang, C., Lee, J. -H., Ko, J. -Y., Kim, E. -A., Kang, N. & Jeon, Y. -J. 2014. Evaluation of the biological activities of marine bacteria collected from Jeju Island, Korea, and isolation of active compounds from their secondary metabolites. Fish Aquat. Sci. 17:215-222.
27 Kulms, D. & Schwarz, T. 2002. Mechanisms of UV‐induced signal transduction. J. Dermatol. 29:189-196.   DOI
28 Kim, J. -K., Kim, Y., Na, K. -M., Surh, Y. -J. & Kim, T. -Y. 2007. [6]-Gingerol prevents UVB-induced ROS production and COX-2 expression in vitro and in vivo. Free Radic. Res. 41:603-614.   DOI
29 Ko, S. -C., Cha, S. -H., Heo, S. -J., Lee, S. -H., Kang, S. -M. & Jeon, Y. -J. 2011. Protective effect of Ecklonia cava on UVB-induced oxidative stress: in vitro and in vivo zebrafish model. J. Appl. Phycol. 23:697-708.   DOI
30 Kong, S. -Z., Chen, H. -M., Yu, X. -T., Zhang, X., Feng, X. -X., Kang, X. -H., Li, W. -J., Huang, N., Luo, H. & Su, Z. -R. 2015. The protective effect of 18${\beta}$-glycyrrhetinic acid against UV irradiation induced photoaging in mice. Exp. Gerontol. 61:147-155.   DOI
31 Lee, J. -H., Han, J. W., Ko, J. -Y., Lee, W., Ahn, G., Kim, C. -Y., Kim, G. H. & Jeon, Y. -J. 2015a. 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. Physiol. 28:181-189.
32 Lee, J. -H., Ko, J. -Y., Oh, J. -Y., Kim, E. -A., Kim, C. -Y. & Jeon, Y. -J. 2015b. Evaluation of phlorofucofuroeckol-A isolated from Ecklonia cava (Phaeophyta) on anti-lipid peroxidation in vitro and in vivo. Algae 30:313-323.   DOI
33 Lee, J. -H., Zhang, C., Ko, J. -Y., Lee, J. -S. & Jeon, Y. -J. 2015c. Evaluation on anticancer effect against HL-60 cells and toxicity in vitro and in vivo of the phenethyl acetate isolated from a marine bacterium Streptomyces griseus. Fish. Aquat. Sci. 18:35-44.
34 Dong, Q., Svoboda, K., Tiersch, T. R. & Monroe, W. T. 2007. Photobiological effects of UVA and UVB light in zebrafish embryos: evidence for a competent photorepair system. J. Photochem. Photobiol. B Biol. 88:137-146.   DOI
35 Alves, G. d. A. D., de Souza, R. O., Rogez, H., Masaki, H. & Fonseca, M. J. V. 2016. Cecropia obtusa, an Amazonian ethanolic extract, exhibits photochemoprotective effect in vitro and balances the redox cellular state in response to UV radiation. Ind. Crops Prod. 94:893-902.   DOI
36 Bishnoi, N. R., Bajaj, M. & Sanatomba, K. 2005. Biosorption of zinc (II) using Spirogyra species from electroplating effluent. J. Environ. Biol. 26:661-664.
37 Chandler, S. F. & Dodds, J. H. 1983. The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of Solanum laciniatum. Plant Cell Rep. 2:205-208.   DOI
38 Liu, M., Li, X., Liu, Y., Shi, Y. & Ma, X. 2015. Analysis of differentially expressed genes under UV-B radiation in the desert plant Reaumuria soongorica. Gene 574:265-272.   DOI
39 Lee, S. -H., Kang, S. -M., Sok, C. H., Hong, J. T., Oh, J. -Y. & Jeon, Y. -J. 2015d. Cellular activities and docking studies of eckol isolated from Ecklonia cava (Laminariales, Phaeophyceae) as potential tyrosinase inhibitor. Algae 30:163-170.