Epigallocatechin gallate enhances human lens epithelial cell survival after UVB irradiation via the mitochondrial signaling pathway

Wu,Qiuxin; Song,Jike; Gao,Yan'e; Zou,Yingying; Guo,Junguo; Zhang,Xiuyan; Liu,Dongmei; Guo,Dadong; Bi,Hongsheng

doi:10.3892/mmr.2022.12603

Epigallocatechin gallate enhances human lens epithelial cell survival after UVB irradiation via the mitochondrial signaling pathway

Authors:
- Qiuxin Wu
- Jike Song
- Yan'e Gao
- Yingying Zou
- Junguo Guo
- Xiuyan Zhang
- Dongmei Liu
- Dadong Guo
- Hongsheng Bi
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Affiliations: Affiliated Eye Hospital, Shandong University of Traditional Chinese Medicine, Jinan, Shandong 250002, P.R. China, College of Ophthalmology and Optometry, Shandong Provincial Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Therapy of Ocular Diseases, Shandong Academy of Eye Disease Prevention and Therapy, Jinan, Shandong 250002, P.R. China
Published online on: January 14, 2022 https://doi.org/10.3892/mmr.2022.12603
Article Number: 87
Copyright: © Wu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The aim of the present study was to explore the mechanism underlying the ultraviolet B (UVB) irradiation‑induced apoptosis of human lens epithelial cells (HLECs), and to investigate the protective effect of epigallocatechin gallate (EGCG) against the UVB‑induced apoptosis of HLECs. HLECs were exposed to different concentrations of EGCG plus UVB (30 mJ/cm²). Cell viability was determined using the MTT assay. Furthermore, mitochondrial membrane potential (Δψm) and apoptosis were assessed by flow cytometry with JC‑1 and Annexin V/PI staining, respectively. Moreover, the activities of catalase (CAT), superoxide dismutase (SOD) and glutathione peroxidase (GSH‑Px), as well as the levels of GSH, hydrogen peroxide (H₂O₂) and hydroxyl free radicals were determined using biochemical assay techniques. Reverse transcription‑quantitative PCR and western blotting were used to detect the mRNA and protein expression levels of Bcl‑2, Bax, cytochrome c, caspase‑9 and caspase‑3, respectively. The results revealed that UVB irradiation reduced the Δψm of HLECs and induced apoptosis. Notably, EGCG significantly attenuated the generation of H₂O₂ and hydroxyl free radicals caused by UVB irradiation in HLECs, and significantly increased CAT, SOD and GSH‑Px activities, however, the GSH levels were not significantly increased. EGCG also reduced UVB‑stimulated Bax, cytochrome c, caspase‑9 and caspase‑3 expression, and elevated Bcl‑2 expression, suggesting that EGCG may possess free radical‑scavenging properties, thus increasing cell viability. In conclusion, EGCG may be able to protect against UVB‑induced HLECs apoptosis through the mitochondria‑mediated apoptotic signaling pathway, indicating its potential application in clinical practice.

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1	Kang LH, Zhang GW, Zhang JF, Qin B and Guan HJ: Ganoderic acid A protects lens epithelial cells from UVB irradiation and delays lens opacity. Chin J Nat Med. 18:934–940. 2020.PubMed/NCBI
2	Rong X, Rao J, Li D, Jing Q, Lu Y and Ji Y: TRIM69 inhibits cataractogenesis by negatively regulating p53. Redox Biol. 22:1011572019. View Article : Google Scholar : PubMed/NCBI
3	Chung I, Hah YS, Ju S, Kim JH, Yoo WS, Cho HY, Yoo JM, Seo SW, Choi WS and Kim SJ: Ultraviolet B radiation stimulates the interaction between nuclear factor of activated T cells 5 (NFAT5) and nuclear factor-kappa B (NF-κB) in human lens epithelial cells. Curr Eye Res. 42:987–994. 2017. View Article : Google Scholar : PubMed/NCBI
4	Cencer CS, Chintala SK, Townsend TJ, Feldmann DP, Awrow MA, Putris NA, Geno ME, Donovan MG and Giblin FJ: PARP-1/PAR activity in cultured human lens epithelial cells exposed to two levels of UVB light. Photochem Photobiol. 94:126–138. 2018. View Article : Google Scholar : PubMed/NCBI
5	Piao MJ, Kang KA, Zhen AX, Kang HK, Koh YS, Kim BS and Hyun JW: Horse oil mitigates oxidative damage to human HaCaT keratinocytes caused by ultraviolet B irradiation. Int J Mol Sci. 20:14902019. View Article : Google Scholar : PubMed/NCBI
6	Hu X, Liang Y, Zhao B and Wang Y: Oxyresveratrol protects human lens epithelial cells against hydrogen peroxide-induced oxidative stress and apoptosis by activation of Akt/HO-1 pathway. J Pharmacol Sci. 139:166–173. 2019. View Article : Google Scholar : PubMed/NCBI
7	Perdices L, Fuentes-Broto L, Segura F, Cavero A, Orduna-Hospital E, Insa-Sánchez G, Sánchez-Cano AI, Fernández-Sánchez L, Cuenca N and Pinilla I: Systemic epigallocatechin gallate protects against retinal degeneration and hepatic oxidative stress in the P23H-1 rat. Neural Regen Res. 17:625–631. 2022. View Article : Google Scholar : PubMed/NCBI
8	Unno K and Nakamura Y: Green tea suppresses brain aging. Molecules. 26:48972021. View Article : Google Scholar : PubMed/NCBI
9	Xu FW, Lv YL, Zhong YF, Xue YN, Wang Y, Zhang LY, Hu X and Tan WQ: Beneficial effects of green tea EGCG on skin wound healing: A comprehensive review. Molecules. 26:61232021. View Article : Google Scholar : PubMed/NCBI
10	Faheem NM and Ali TM: The counteracting effects of (−)-epigallocatechin-3-gallate on the immobilization stress-induced adverse reactions in rat pancreas. Cell Stress Chaperones. 26:159–172. 2021. View Article : Google Scholar : PubMed/NCBI
11	Singh BN, Shankar S and Srivastava RK: Green tea catechin, epigallocatechin-3-gallate (EGCG): Mechanisms, perspectives and clinical applications. Biochem Pharmacol. 82:1807–1821. 2011. View Article : Google Scholar : PubMed/NCBI
12	Kim E, Hwang K, Lee J, Han SY, Kim EM, Park J and Cho JY: Skin protective effect of epigallocatechin gallate. Int J Mol Sci. 19:1732018. View Article : Google Scholar : PubMed/NCBI
13	Chen MH, Tsai CF, Hsu YW and Lu FJ: Epigallocatechin gallate eye drops protect against ultraviolet B-induced corneal oxidative damage in mice. Mol Vis. 20:153–162. 2014.PubMed/NCBI
14	Kitagawa K and Niikura Y: Caspase-independent mitotic death (CIMD). Cell Cycle. 7:1001–1005. 2008. View Article : Google Scholar : PubMed/NCBI
15	Kiraz Y, Adan A, Kartal Yandim M and Baran Y: Major apoptotic mechanisms and genes involved in apoptosis. Tumour Biol. 37:8471–8486. 2016. View Article : Google Scholar : PubMed/NCBI
16	Zhou YF, Guo B, Ye MJ, Liao RF and Li SL: Protective effect of rutin against H2O2-induced oxidative stress and apoptosis in human lens epithelial cells. Curr Eye Res. 41:933–942. 2016. View Article : Google Scholar : PubMed/NCBI
17	Kim JS, Cho IA, Kang KR, Lim H, Kim TH, Yu SK, Kim HJ, Lee SA, Moon SM, Chun HS, et al: Reversine induces caspase-dependent apoptosis of human osteosarcoma cells through extrinsic and intrinsic apoptotic signaling pathways. Genes Genomics. 41:657–665. 2019. View Article : Google Scholar : PubMed/NCBI
18	Qi S, Guo L, Yan S, Lee RJ, Yu S and Chen S: Hypocrellin A-based photodynamic action induces apoptosis in A549 cells through ROS-mediated mitochondrial signaling pathway. Acta Pharm Sin B. 9:279–293. 2019. View Article : Google Scholar : PubMed/NCBI
19	Yao K, Ye P, Zhang L, Tan J, Tang X and Zhang Y: Epigallocatechin gallate protects against oxidative stress-induced mitochondria-dependent apoptosis in human lens epithelial cells. Mol Vis. 14:217–223. 2008.PubMed/NCBI
20	Wu Q, Li Z, Lu X, Song J, Wang H, Liu D, Guo D and Bi H: Epigallocatechin gallate protects the human lens epithelial cell survival against UVB irradiation through AIF/endo G signalling pathways in vitro. Cutan Ocul Toxicol. 40:187–197. 2021. View Article : Google Scholar : PubMed/NCBI
21	Yao J, Liu Y, Wang X, Shen Y, Yuan S, Wan Y and Jiang Q: UVB radiation induces human lens epithelial cell migration via NADPH oxidase-mediated generation of reactive oxygen species and up-regulation of matrix metalloproteinases. Int J Mol Med. 24:153–159. 2009.PubMed/NCBI
22	Heo J, Lee BR and Koh JW: Protective effects of epigallocatechin gallate after UV irradiation of cultured human lens epithelial cells. Korean J Ophthalmol. 22:183–186. 2008. View Article : Google Scholar : PubMed/NCBI
23	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
24	Wu Q, Guo D, Bi H, Wang D and Du Y: UVB irradiation-induced dysregulation of plasma membrane calcium ATPase1 and intracellular calcium homeostasis in human lens epithelial cells. Mol Cell Biochem. 382:263–272. 2013. View Article : Google Scholar : PubMed/NCBI
25	Oliveira MM, Ratti BA, Daré RG, Silva SO, Truiti MD, Ueda-Nakamura T, Auzély-Velty R and Nakamura CV: Dihydrocaffeic acid prevents UVB-induced oxidative stress leading to the inhibition of apoptosis and MMP-1 expression via p38 signaling pathway. Oxid Med Cell Longev. 2019:24190962019. View Article : Google Scholar : PubMed/NCBI
26	Pustisek N and Situm M: UV-radiation, apoptosis and skin. Coll Antropol. 35 (Suppl 2):S339–S341. 2011.PubMed/NCBI
27	Cadet J and Wagner JR: DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb Perspect Biol. 5:a0125592013. View Article : Google Scholar : PubMed/NCBI
28	Yin Y, Meng F, Sui C, Jiang Y and Zhang L: Arsenic enhances cell death and DNA damage induced by ultraviolet B exposure in mouse epidermal cells through the production of reactive oxygen species. Clin Exp Dermatol. 44:512–519. 2019. View Article : Google Scholar : PubMed/NCBI
29	Zhang D, Lu C, Yu Z, Wang X, Yan L, Zhang J, Li H, Wang J and Wen A: Echinacoside alleviates UVB irradiation-mediated skin damage via inhibition of oxidative stress, DNA damage, and apoptosis. Oxid Med Cell Longev. 2017:68514642017. View Article : Google Scholar : PubMed/NCBI
30	Rashikh A, Ahmad SJ, Pillai KK, Kohli K and Najmi AK: Aliskiren attenuates myocardial apoptosis and oxidative stress in chronic murine model of cardiomyopathy. Biomed Pharmacother. 66:138–143. 2012. View Article : Google Scholar : PubMed/NCBI
31	Heruye S, Maffofou N LN, Singh NU, Munt D, Njie-Mbye YF, Ohia SE and Opere CA: Standardization of a new method for assessing the development of cataract in cultured bovine lenses. J Pharmacol Toxicol Methods. 98:1065922019. View Article : Google Scholar : PubMed/NCBI
32	He L, He T, Farrar S, Ji L, Liu T and Ma X: Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol Biochem. 44:532–553. 2017. View Article : Google Scholar : PubMed/NCBI
33	Gopi N, Vijayakumar S, Thaya R, Govindarajan M, Alharbi NS, Kadaikunnan S, Khaled JM, Al-Anbr MN and Vaseeharan B: Chronic exposure of oreochromis niloticus to sub-lethal copper concentrations: Effects on growth, antioxidant, non-enzymatic antioxidant, oxidative stress and non-specific immune responses. J Trace Elem Med Biol. 55:170–179. 2019. View Article : Google Scholar : PubMed/NCBI
34	Gokul S, Patil VS, Jailkhani R, Hallikeri K and Kattappagari KK: Oxidant-antioxidant status in blood and tumor tissue of oral squamous cell carcinoma patients. Oral Dis. 16:29–33. 2010. View Article : Google Scholar : PubMed/NCBI
35	Katiyar SK, Afaq F, Azizuddin K and Mukhtar H: Inhibition of UVB-induced oxidative stress-mediated phosphorylation of mitogen-activated protein kinase signaling pathways in cultured human epidermal keratinocytes by green tea polyphenol (−)-epigallocatechin-3-gallate. Toxicol Appl Pharmacol. 176:110–117. 2001. View Article : Google Scholar : PubMed/NCBI
36	Yamamoto T, Hsu S, Lewis J, Wataha J, Dickinson D, Singh B, Bollag WB, Lockwood P, Ueta E, Osaki T and Schuster G: Green tea polyphenol causes differential oxidative environments in tumor versus normal epithelial cells. J Pharmacol Exp Ther. 307:230–236. 2003. View Article : Google Scholar : PubMed/NCBI
37	Cao G, Chen M, Song Q, Liu Y, Xie L, Han Y, Liu Z, Ji Y and Jiang Q: EGCG protects against UVB-induced apoptosis via oxidative stress and the JNK1/c-Jun pathway in ARPE19 cells. Mol Med Rep. 5:54–59. 2012.PubMed/NCBI
38	Kim HS, Quon MJ and Kim JA: New insights into the mechanisms of polyphenols beyond antioxidant properties; lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biol. 2:187–195. 2014. View Article : Google Scholar : PubMed/NCBI
39	Katiyar SK, Afaq F, Perez A and Mukhtar H: Green tea polyphenol (−)-epigallocatechin-3-gallate treatment of human skin inhibits ultraviolet radiation-induced oxidative stress. Carcinogenesis. 22:287–294. 2001. View Article : Google Scholar : PubMed/NCBI
40	Elbling L, Herbacek I, Weiss RM, Jantschitsch C, Micksche M, Gerner C, Pangratz H, Grusch M, Knasmüller S and Berger W: Hydrogen peroxide mediates EGCG-induced antioxidant protection in human keratinocytes. Free Radic Biol Med. 49:1444–1452. 2010. View Article : Google Scholar : PubMed/NCBI
41	Mary Momo CM, Ferdinand N, Omer Bebe NK, Alexane Marquise MN, Augustave K, Bertin Narcisse V, Herve T and Joseph T: Oxidative effects of potassium dichromate on biochemical, hematological characteristics, and hormonal levels in rabbit doe (oryctolagus cuniculus). Vet Sci. 6:302019. View Article : Google Scholar : PubMed/NCBI
42	Ibrahim IA, Abdulla MA, Hajrezaie M, Bader A, Shahzad N, Al-Ghamdi SS, Gushash AS and Hasanpourghadi M: The gastroprotective effects of hydroalcoholic extract of Monolluma quadrangula against ethanol-induced gastric mucosal injuries in sprague dawley rats. Drug Des Dev Ther. 10:93–105. 2015. View Article : Google Scholar : PubMed/NCBI
43	Bhattacharyya A, Chattopadhyay R, Mitra S and Crowe SE: Oxidative stress: An essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev. 92:329–354. 2014. View Article : Google Scholar : PubMed/NCBI
44	Kumar J, Khan S, Mandotra SK, Dhar P, Tayade AB, Verma S, Toppo K, Arora R, Upreti DK and Chaurasia OP: Nutraceutical profile and evidence of alleviation of oxidative stress by spirogyra porticalis (Muell.) cleve inhabiting the high altitude trans-himalayan region. Sci Rep. 9:40912019. View Article : Google Scholar : PubMed/NCBI
45	Santhakumaran I, Kesavan SS and Arumugam G: Asperyellone pretreatment protects HaCaT cells from UVB irradiation induced oxidative damages: Assessment under in vitro and in vivo conditions and at molecular level. J Cell Biochem. 120:10715–10725. 2019. View Article : Google Scholar : PubMed/NCBI
46	Filip A, Daicoviciu D, Clichici S, Mocan T, Muresan A and Postescu ID: Photoprotective effects of two natural products on ultraviolet B-induced oxidative stress and apoptosis in SKH-1 mouse skin. J Med Food. 14:761–766. 2011. View Article : Google Scholar : PubMed/NCBI
47	Jeong SY and Seol DW: The role of mitochondria in apoptosis. BMB Rep. 41:11–22. 2008. View Article : Google Scholar : PubMed/NCBI
48	Kim SH and Kim H: Inhibitory effect of astaxanthin on oxidative stress-induced mitochondrial dysfunction-A mini-review. Nutrients. 10:11372018. View Article : Google Scholar : PubMed/NCBI
49	Cosentino K and García-Sáez AJ: Mitochondrial alterations in apoptosis. Chem Phys Lipids. 181:62–75. 2014. View Article : Google Scholar : PubMed/NCBI
50	Jing L, Kumari S, Mendelev N and Li PA: Coenzyme q10 ameliorates ultraviolet B irradiation induced cell death through inhibition of mitochondrial intrinsic cell death pathway. Int J Mol Sci. 12:8302–8315. 2011. View Article : Google Scholar : PubMed/NCBI
51	Onishi M, Yamano K, Sato M, Matsuda N and Okamoto K: Molecular mechanisms and physiological functions of mitophagy. EMBO J. 40:e1047052021. View Article : Google Scholar : PubMed/NCBI
52	Adikesavan G, Vinayagam MM, Abdulrahman LA and Chinnasamy T: (−)-Epigallocatechin-gallate (EGCG) stabilize the mitochondrial enzymes and inhibits the apoptosis in cigarette smoke-induced myocardial dysfunction in rats. Mol Biol Rep. 40:6533–6545. 2013. View Article : Google Scholar : PubMed/NCBI
53	Zhang W, Zhao L, Liu J, Du J, Wang Z, Ruan C and Dai K: Cisplatin induces platelet apoptosis through the ERK signaling pathway. Thromb Res. 130:81–91. 2012. View Article : Google Scholar : PubMed/NCBI
54	Zhou X, Liang L, Zhao Y and Zhang H: Epigallocatechin-3-gallate ameliorates angiotensin II-induced oxidative stress and apoptosis in human umbilical vein endothelial cells through the activation of Nrf2/caspase-3 signaling. J Vasc Res. 54:299–308. 2017. View Article : Google Scholar : PubMed/NCBI
55	Estrov Z, Thall PF, Talpaz M, Estey EH, Kantarjian HM, Andreeff M, Harris D, Van Q, Walterscheid M and Kornblau SM: Caspase 2 and caspase 3 protein levels as predictors of survival in acute myelogenous leukemia. Blood. 92:3090–3097. 1998. View Article : Google Scholar : PubMed/NCBI
56	Kuwana T and Newmeyer DD: Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol. 15:691–699. 2003. View Article : Google Scholar : PubMed/NCBI
57	Lv J and Xing Y: Effects of UV on apoptotic factors in lens epithelial cells of an animal model. Exp Ther Med. 16:2309–2312. 2018.PubMed/NCBI
58	Qiu X, Rong X, Yang J and Lu Y: Evaluation of the antioxidant effects of different histone deacetylase inhibitors (HDACis) on human lens epithelial cells (HLECs) after UVB exposure. BMC Ophthalmol. 19:422019. View Article : Google Scholar : PubMed/NCBI
59	Liu S, Sun Z, Chu P, Li H, Ahsan A, Zhou Z, Zhang Z, Sun B, Wu J, Xi Y, et al: EGCG protects against homocysteine-induced human umbilical vein endothelial cells apoptosis by modulating mitochondrial-dependent apoptotic signaling and PI3K/Akt/eNOS signaling pathways. Apoptosis. 22:672–680. 2017. View Article : Google Scholar : PubMed/NCBI
60	Ye P, Lin K, Li Z, Liu J, Yao K and Xu W: (−)-Epigallocatechin gallate regulates expression of apoptotic genes and protects cultured human lens epithelial cells under hyperglycemia. Mol Biol (Mosk). 47:251–257. 2013.(In Russian). View Article : Google Scholar : PubMed/NCBI
61	Luo D, Min W, Lin XF, Wu D, Xu Y and Miao X: Effect of epigallocatechingallate on ultraviolet B-induced photo-damage in keratinocyte cell line. Am J Chin Med. 34:911–922. 2006. View Article : Google Scholar : PubMed/NCBI