Ethyl acetate fraction of Sargassum pallidum extract attenuates particulate matter-induced oxidative stress and inflammation in keratinocytes and zebrafish

Wook Chul Kim , Ji-Won Park , Bohyun Yun , Won Woo Lee , Kyung-Min Choi , Seung-Hong Lee

Asian Pacific Journal of Tropical Biomedicine ›› 2024, Vol. 14 ›› Issue (4) : 137 -146.

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Asian Pacific Journal of Tropical Biomedicine ›› 2024, Vol. 14 ›› Issue (4) :137 -146. DOI: 10.4103/apjtb.apjtb_921_23
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Ethyl acetate fraction of Sargassum pallidum extract attenuates particulate matter-induced oxidative stress and inflammation in keratinocytes and zebrafish
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Abstract

Objective: To evaluate the effect of the ethyl acetate fraction derived from Sargassum pallidum extract against particulate matter (PM)-induced oxidative stress and inflammation in HaCaT cells and zebrafish. Methods: HaCaT cells and zebrafish were used to evaluate the protective effects of the ethyl acetate fraction of Sargassum pallidum extract against PM-induced oxidative stress and inflammation. The production of nitric oxide (NO), intracellular ROS, prostaglandin E2 (PGE2), and pro-inflammatory cytokines, and the expression levels of COX-2, iNOS, and NF-κB were evaluated in PM-induced HaCaT cells. Furthermore, the levels of ROS, NO, and lipid peroxidation were assessed in the PM-exposed zebrafish model. Results: The ethyl acetate fraction of Sargassum pallidum extract significantly decreased the production of NO, intracellular ROS, and PGE2 in PM-induced HaCaT cells. In addition, the fraction markedly suppressed the levels of pro-inflammatory cytokines and inhibited the expression levels of COX-2, iNOS, and NF-κB. Furthermore, it displayed remarkable protective effects against PM-induced inflammatory response and oxidative stress, represented by the reduction of NO, ROS, and lipid peroxidation in zebrafish. Conclusions: The ethyl acetate fraction of Sargassum pallidum extract exhibits a protective effect against PM-induced oxidative stress and inflammation both in vitro and in vivo and has the potential as a candidate for the development of pharmaceutical and cosmeceutical products.

Keywords

Particulate matter / Inflammation / Oxidative stress / Sargassum pallidum / Ethyl acetate fraction / Zebrafish

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Wook Chul Kim, Ji-Won Park, Bohyun Yun, Won Woo Lee, Kyung-Min Choi, Seung-Hong Lee. Ethyl acetate fraction of Sargassum pallidum extract attenuates particulate matter-induced oxidative stress and inflammation in keratinocytes and zebrafish. Asian Pacific Journal of Tropical Biomedicine, 2024, 14 (4) : 137-146 DOI:10.4103/apjtb.apjtb_921_23

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Acknowledgments

This work was supported by the Soonchunhyang University Research Fund. Also, this research was supported by the Ministry of Education and National Research Foundation of Korea through “Leaders in Industry-university Cooperation 3.0” Project.

Conflict of interest statement

The authors declare that there is no conflict of interest.

Funding

This work was supported financially by Korea Environment Industry & Technology Institute through Project to make multi-ministerial national biological research resources more advanced program, funded by Korea Ministry of Environment (grant number RS-2023-00230403).

Data availability statement

The data supporting the findings of this study are available from the corresponding authors upon request.

Authors’ contributions

WCK and SHL designed the study. WCK performed experimental analysis. WCK, JWP, BY, WWL and KMC performed the analytic calculations and numerical simulations. WCK and SHL contributed to the final version of the manuscript. SHL supervised the project.

References

[1]

Peden D, Reed CE. Environmental and occupational allergies. J Allergy Clin Immunol 2010; 125: S150-S160.

[2]

Krall JR, Anderson GB, Dominici F, Bell ML, Peng RD. Short-term exposure to particulate matter constituents and mortality in a national study of U.S. urban communities. Environ Health Perspect 2013; 121: 1148-1153.

[3]

Arias-Pérez RD, Taborda NA, Gómez DM, Narvaez JF, Porras J, Hernandez JC. Inflammatory effects of particulate matter air pollution. Environ Sci Pollut Res Int 2020; 27(34): 42390-42404.

[4]

Kim KE, Cho D, Park HJ. Air pollution and skin diseases. Life Sci 2016; 152: 126-134.

[5]

Sander CS, Chang H, Hamm F, Elsner P, Thiele JJ. Role of oxidative stress and the antioxidant network in cutaneous carcinogenesis. Int J Dermatol 2004; 43: 326-335.

[6]

Tang KT, Ku KC, Chen DY, Lin CH, Tsuang BJ, Chen YH. Adult atopic dermatitis and exposure to air pollutants a nationwide population-based study. Ann Allergy Asthma Immunol 2017; 118: 351-355.

[7]

Piao MJ, Ahn MJ, Kang KA, Ryu YS, Hyun YJ, Shilnikova K, et al. Particulate matter 2.5 damages skin cells by inducing oxidative stress, subcellular organelle dysfunction, and apoptosis. Arch Toxicol 2018; 92: 2077-2091.

[8]

Lee CW, Lin ZC, Hu SC, Chiang YC, Hsu LF, Lin YC, et al. Urban particulate matter downregulates filaggrin via COX2 expression/PGE2 production leading to skin barrier dysfunction . Sci Rep 2016; 6. doi: 10.1038/srep27995.

[9]

Liu K, Hua S, Song L. PM2.5 Exposure and asthma development: The key role of oxidative stress. Oxid Med Cell Longev 2022; 2022. doi: 10.1155/2022/3618806.

[10]

Kumar N, Goel N. Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnol Rep (Amst) 2019; 24. doi: 10.1016/j.btre.2019.e00370.

[11]

Qin N, Li CB, Jin MN, Shi LH, Duan HQ, Niu WY. Synthesis and biological activity of novel tiliroside derivants. Eur J Med Chem 2011; 46: 5189-5195.

[12]

Jin HY, Choi YJ, Moon HJ, Jeong JH, Nam JH, Lee SC, et al. Antioxidant activities of Rhus verniciflua seed extract and quality characteristics of fermented milk containing Rhus verniciflua seed extract. Korean J Food Preserv 2016; 26: 825-831.

[13]

Chew YL, Lim YY, Omar M, Khoo KS. Antioxidant activity of three edible seaweeds from two areas in South East Asia. LWT 2008; 41: 1067-1072.

[14]

Hong J. Role of natural product diversity in chemical biology. Curr Opin Chem Biol 2011; 15: 350-354.

[15]

Kim KN, Heo SJ, Cha SH, Jeon YJ. Evaluation of DPPH radical scavenging activity of jeju seaweeds using high throughput screening (HTS) technique. Hanguk Haeyang Paio Hakhoe 2006; 1: 170-177.

[16]

Woonnoi W, Moolsap F, Tanasawet S, Khumpirapang N, Aenglong C, Sukketsiri W. In vitro antioxidant and wound healing activity of Sargassum polycystum hydroethanolic extract in fibroblasts and keratinocytes. Asian Pac J Trop Biomed 2023; 13(5): 222-232.

[17]

Choi S, Lee JH, Oh SW, Yu E, Kwon K, Jang SJ, et al. Anti-pollutant activity of Porphyra yezoensis water extract and its active compound, porphyra 334, against urban particulate matter-induced keratinocyte cell damage. Mar Drugs 2023; 21(2): 121.

[18]

Ye H, Wang K, Zhou C, Liu J, Zeng X. Purification, antitumor and antioxidant activities in vitro of polysaccharides from the brown seaweed Sargassum pallidum. Food Chem 2008; 111: 428-432.

[19]

Zhang RL, Luo WD, Bi NT, Zhou SK. Evaluation of antioxidant and immunity-enhancing activities of Sargassum pallidum aqueous extract in gastric cancer rats. Molecules 2012; 17: 8419-8429.

[20]

Ye H, Zhou C, Sun Y, Zhang X, Liu J, Hu Q, et al. Antioxidant activities in vitro of ethanol extract from brown seaweed Sargassum pallidum. Eur Food Res Technol 2009; 230: 101-109.

[21]

Fernando IPS, Kim HS, Asanka Sanjeewa KK, Oh JY, Jeon YJ, Lee WW. Inhibition of inflammatory responses elicited by urban fine dust particles in keratinocytes and macrophages by diphlorethohydroxycarmalol isolated from a brown alga Ishige okamurae. Algae 2017; 32(3): 261-273.

[22]

Zhen AX, Hyun YJ, Piao MJ, Fernando PDSM, Kang KA, Ahn MJ, et al. Eckol inhibits particulate matter 2.5-induced skin keratinocyte damage via MAPK signaling pathway. Mar Drugs 2019; 17. doi: 10.3390/md17080444.

[23]

Mun H, Lee SH. Anti-skin aging activities of ethanol extract from Echinodorus cordifolius L. in human keratinocytes. J Appl Biol Chem 2022; 65: 405-412.

[24]

Lee SH, Ko CI, Jee YH, Jeong YH, Kim MS, Kim JS, et al. Anti-inflammatory effect of fucoidan extracted from Ecklonia cava in zebrafish model. Carbohydr Polym 2013; 92: 84-89.

[25]

Kim SY, Kim EA, Kim YS, Yu SK, Choi CY, Lee JS, et al. Protective effects of polysaccharides from Psidium guajava leaves against oxidative stresses. Int J Biol Macromol 2016; 91: 804-811.

[26]

Jayawardena TU, Wang L, Sanjeewa KKA, Kang SI, Lee JS, Jeon YJ. Antioxidant potential of sulfated polysaccharides from Padina boryana; protective effect against oxidative stress in in vitro and in vivo zebrafish model. Mar Drugs 2020; 18. doi: 10.3390/md18040212.

[27]

Jin SP, Li Z, Choi EK, Lee S, Kim YK, Seo EY, et al. Urban particulate matter in air pollution penetrates into the barrier-disrupted skin and produces ROS-dependent cutaneous inflammatory response in vivo. J Dermatol Sci 2018; 91: 175-183.

[28]

Fernando IPS, Jayawardena TU, Kim HS, Vaas APJP, De Silva HIC, Nanayakkara CM, et al. A keratinocyte and integrated fibroblast culture model for studying particulate matter-induced skin lesions and therapeutic intervention of fucosterol. Life Sci 2019; 233. doi: 10.1016/j.lfs.2019.116714.

[29]

Choi H, Shin DW, Kim W, Doh SJ, Lee SH, Noh M. Asian dust storm particles induce a broad toxicological transcriptional program in human epidermal keratinocytes. Toxicol Lett 2011; 200: 92-99.

[30]

Piao MJ, Ahn MJ, Kang KA, Ryu YS, Hyun YJ, Shilnikova K, et al. Particulate matter 2.5 damages skin cells by inducing oxidative stress, subcellular organelle dysfunction, and apoptosis. Arch Toxicol 2018; 92: 2077-2091.

[31]

Kim SK, Himaya SW. Medicinal effects of phlorotannins from marine brown algae. Adv Food Nutr Res 2011; 64: 97-109.

[32]

Chouh A, Nouadri T, Catarino MD, Silva AMS, Cardoso SM. Phlorotannins of the brown algae Sargassum vulgare from the mediterranean sea coast. Antioxidants 2022; 11(6): 1055.

[33]

Li Y, Lei D, Swindell WR, Xia W, Weng S, Fu J, et al. Age-associated increase in skin fibroblast-derived prostaglandin E2 contributes to reduced collagen levels in elderly human skin . J Invest Dermatol 2015; 135: 2181-2188.

[34]

Man MQ, Wakefield JS, Mauro TM, Elias PM. Role of nitric oxide in regulating epidermal permeability barrier function. Exp Dermatol 2022; 31(3): 290-298.

[35]

Lee CW, Lin ZC, Hsu LF, Fang JY, Chiang YC, Tsai MH, et al. Eupafolin ameliorates COX-2 expression and PGE2 production in particulate pollutants-exposed human keratinocytes through ROS/MAPKs pathways . J Ethnopharmacol 2016; 189: 300-309.

[36]

Kleiner H, Pautz A, Linker K, Schwarz PM. Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 2004; 500: 255-266.

[37]

Cho W, Choe J. Prostaglandin E2 stimulates COX-2 expression via mitogen-activated protein kinase p38 but not ERK in human follicular dendritic cell-like cells . BMC Immunol 2020; 21: 20.

[38]

Fernando IPS, Nah JW, Jeon YJ. Potential anti-inflammatory natural products from marine algae. Environ Toxicol Pharmacol 2016; 48: 22-30.

[39]

Zhang JM, An J. Cytokines, inflammation, and pain. Int Anesthesiol Clin 2007; 45(2): 27-37.

[40]

Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-κB signaling pathways. Nat Immunol 2011; 12: 695-708.

[41]

Dong L, Hu R, Yang D, Zhao J, Kan H, Tan J, et al. Fine particulate matter (PM2.5) upregulates expression of inflammasome NLRP1 via ROS/NF-κB signaling in HaCaT cells. Int J Med Sci 2020; 17(14): 2200-2206.

[42]

Jung YH, Roh YW, Chong M. Anti-inflammatory effects of myrrh ethanol extract on particulate matter-induced skin injury. J Korean Med 2022; 43(3): 1-15.

[43]

Catarino MD, Silva A, Cruz MT, Mateus N, Silva AMS, Cardoso SM. Phlorotannins from Fucus vesiculosus: Modulation of inflammatory response by blocking NF-κB signaling pathway. Int J Mol Sci 2020; 21(18). doi: 10.3390/ijms21186897.

[44]

Han JS. Oocyte maturation process of zebrafish (Danio rerio), an emerging animal. Model J Life Sci 2015; 25: 1184-1195.

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