Effects of butylphthalide on hydrogen peroxide induced retinal pigment epithelial cells injury_Chinese Journal of Ocular Fundus Diseases

Authors：

Xing Xiaoli , Huang Liangyu , Zhang Zhe , Huang Xinyuan , Wang Qiong , Li Xiaorong ,  Dong Lijie

Tianjin Key Laboratory of Retinal Functions and Diseases, Eye Institute and School of Optometry, Tianjin Medical University Eye Hospital, Tianjin 300384, China;

Corresponding author：

Dong Lijie, Email: aitaomubang@126.com

Keywords：

Retinal pigment epithelium; Apoptosis; Butylphthalide; Oxidative stress

DOI：

10.3760/cma.j.issn.1005-1015.2019.05.011

Video：

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Objective To investigate the protective effect of butylphenyphthalein (NBP) on RPE apoptosis induced by H₂O₂.Methods The human RPE cell line (human ARPE-19 cell line) were used as the experimental cells and were divided as control group, model group, NBP group. Complete medium was used in control group. The model group was stimulated with 200 μmol/L H₂O₂ for 2 h, and the cells were cultured in complete medium. The NBP group was cultured with 200 μmol/L H₂O₂ and 1 μmol/L NBP for 2 h. After changing the medium, complete medium was combined with 1 μmol/L NBP to continue the culture of the cells. Cell viability were detected by MTT assay while the morphology of RPE were observed by HE staining. Moreover, Hoechst 33258 was used to detect RPE cell apoptosis. Mitochondrial membrane potential (JC-1) staining were performed to monitor changes in cell membrane potential and the characteristic change of apoptosis in RPE cells. Furthermore, 2′,7′-Dichlorofluorescin diacetate (DCFH-DA) staining were used to analyze the effect of NBP treatment on the expression of ROS. The effect of NBP on the expression of Heme oxygenase-1(HO-1) was analyzed by cellular immunofluorescence and western blotting.Results The results of MTT assay showed that the cells were cultured for 24 and 48 hours, cell viability of control group (t=17.710, 13.760; P＜0.000 1, ＜0.000 1) and treatment group (t=4.857, 9.225; P=0.000 7, ＜0.000 1) were stronger than that of model group, and the difference was statistically significant. HE staining and Hoechst33258 staining showed that compared with the control group, the number of cells in the model group was significantly less, and the cell morphology was incomplete. Compared with the model group, the number of cells in the treatment group was significantly increased, and the cell morphology was better. The results of JC-1 assay showed that the number of apoptotic cells in the model group was significantly higher than that in the control group, and the number of apoptotic cells in the treatment group was significantly lower than that in the model group. DCFH-DA staining showed that the ROS accumulation in the model group was more than that in the control group, and the ROS accumulation in the treatment group was less than that in the model group. Immunostaining observation showed that the HO-1 fluorescence intensity of the cells in the treatment group was significantly higher than that of the control group, and the difference was statistically significant (t=10.270, P=0.000 5). Western blot analysis showed that NBP up-regulated the expression level of HO-1 in a time-dependent manner. The relative expression of HO-1 at 4, 8, and 12 h of NBP showed a clear increase trend compared with 0 h, and the difference was statistically significant (F=164.91, P＜0.05).Conclusions Oxidative stress injury can down-regulate the viability of RPE cells and induce apoptosis. NBP can increase the antioxidant capacity of RPE cells, reduce cell damage and inhibit cell apoptosis by up-regulating HO-1 expression.

Citation： Xing Xiaoli, Huang Liangyu, Zhang Zhe, Huang Xinyuan, Wang Qiong, Li Xiaorong, Dong Lijie. Effects of butylphthalide on hydrogen peroxide induced retinal pigment epithelial cells injury. Chinese Journal of Ocular Fundus Diseases, 2019, 35(5): 480-487. doi: 10.3760/cma.j.issn.1005-1015.2019.05.011 Copy

1.	田芳, 胡博杰, 李文博, 等. 高表达多聚嘧啶序列结合蛋白相关剪接因子对糖基化终产物诱导下视网膜Müller细胞凋亡的影响[J]. 中华眼底病杂志, 2019, 35(1): 70-75. DOI: 10.3760/cma.j.issn.1005-1015.2019.01.015.Tian F, Hu BJ, Li WB, et al. Effects of polypyramidine tract binding protein-associated splicing factor overexpression on apoptosis of human Müller cells under advanced glycation end products treatment[J]. Chin J Ocul Fundus Dis, 2019, 35(1): 70-75. DOI: 10.3760/cma.j.issn.1005-1015.2019.01.015.
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3.	田芳, 赵今稚, 滕贺, 等. Krüppel样因子6经活化转录因子4通路对晶状体上皮细胞凋亡的调控作用[J]. 中华实验眼科杂志, 2018, 36(3): 181-186. DOI: 10.3760/cma.j.issn.2095-0160.2018.03.005.Tian F, Zhao JZ, Teng H, et al. Regulation of Krüppel-like factor 6 via activating transcription factor 4 pathway to apoptosis of human lens epithelial cells[J]. Chin J Exp Ophthalmol, 2018, 36(3): 181-186. DOI: 10.3760/cma.j.issn.2095-0160.2018.03.005.
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8.	田芳, 东莉洁, 吉洁, 等. 多聚嘧啶序列结合蛋白相关剪接因子对视网膜血管内皮细胞IGF-1/VEGF信号通路的抑制作用[J]. 中华实验眼科杂志, 2016, 34(1): 11-16. DOI: 10.3760/cma.j.issn.2095-0160.2016.01.003.Tian F, Dong LJ, Ji J, et al. Inhibition of PTB-associated splicing factor on IGF-1/VEGF signaling pathway in retinal vascular endothelial cells[J]. Chin J of Exp Ophthalmol, 2016, 34(1): 11-16. DOI: 10.3760/cma.j.issn.2095-0160.2016.01.003.
9.	田芳, 东莉洁, 周玉, 等. 重组腺相关病毒-多聚嘧啶序列结合蛋白相关剪接因子对氧诱导视网膜新生血管形成的抑制作用[J]. 中华眼底病杂志, 2014, 30(5): 504-508. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.019.Tian F, Dong LJ, Zhou Y, et al. Inhibition of oxygen induced retinal neovascularization by recombinant adeno-associated virus-polypyrimidine tract-binding protein-associated splicing factor intraocular injection in mice[J]. Chin J Ocul Fundus Dis, 2014, 30(5): 504-508. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.019.
10.	田芳, 赵今稚, 黄亮瑜, 等. 高表达Krüppel样因子6对紫外线B诱导的人晶状体上皮细胞凋亡的影响[J]. 中华实验眼科杂志, 2019, 37(4): 257-262. DOI: 10.3760/cma.j.issn.2095-0160.2019.04.004.Tian F, Zhao JZ, Huang LY, et al. Effects of Krüppel-like factor 6 overexpression towards apoptosis of human lens epithelial cells with ultra violetradiation B treatment[J]. Chin J Exp Ophthalmol, 2019, 37(4): 257-262. DOI: 10.3760/cma.j.issn.2095-0160.2019.04.004.
11.	Tian F, Dong L, Zhou Y, et al. Rapamycin-induced apoptosis in HGF-stimulated lens epithelial cells by AKT/mTOR, ERK and JAK2/STAT3 pathways[J]. Int J Mol Sci, 2014, 15(8): 13833-13848. DOI: 10.3390/ijms150813833.
12.	Dong L, Nian H, Shao Y, et al. PTB-associated splicing factor inhibits IGF-1-induced VEGF upregulation in a mouse model of oxygen-induced retinopathy[J]. Cell Tissue Res, 2015, 360(2): 233-243. DOI: 10.1007/s00441-014-2104-5.
13.	Li W, Wei D, Lin J, et al. Dl-3-n-butylphthalide reduces cognitive impairment induced by chronic cerebral hypoperfusion through GDNF/GFRα1/ret signaling preventing hippocampal neuron apoptosis[J/OL]. Front Cell Neurosci, 2019, 13:351[2019-08-13]. https://doi.org/10.3389/fncel.2019.00351. DOI: 10.3389/fncel.2019.00351.
14.	Chen Y, Jiang M, Li L, et al. DL-3-n-butylphthalide reduces microglial activation in lipopolysaccharide-induced Parkinson's disease model mice[J]. Mol Med Rep, 2017, 17(3): 3884-3890. DOI: 10.3892/mmr.2017.8332.
15.	Wang C, Wang Z, Xie J, et al. Dl-3-n-butylphthalide-induced upregulation of antioxidant defense is involved in the enhancement of cross talk between CREB and Nrf2 in an Alzheimer's disease mouse model[J]. Neurobiol Aging, 2016, 38: 32-46. DOI: 10.1016/j.neurobiolaging.2015.10.024.
16.	Feng X, Peng Y, Liu M, et al. Dl-3-n-butylphthalide extends survival by attenuating glial activation in a mouse model of amyotrophic lateral sclerosis[J]. Neuropharmacology, 2012, 62(2): 1004-1010. DOI: 10.1016/j.neuropharm.2011.10.009.
17.	Qi Q, Xu J, Lv P, et al. DL-3-n-butylphthalide alleviates vascular cognitive impairment induced by chronic cerebral hypoperfusion by activating the Akt/Nrf2 signaling pathway in the hippocampus of rats[J]. Neurosci Lett, 2018, 672: 59-64. DOI: 10.1016/j.neulet.2017.11.051.
18.	Qiu H, Ma J, Wu H, et al. DL-3-n-butylphthalide improves ventricular function, and prevents ventricular remodeling and arrhythmias in post-MI rats[J]. Naunyn Schmiedebergs Arch Pharmacol, 2018, 391(6): 627-637. DOI: 10.1007/s00210-018-1490-8.
19.	Wang F, Ma J, Han F, et al. DL-3-n-butylphthalide delays the onset and progression of diabetic cataract by inhibiting oxidative stress in rat diabetic model[J]. Sci Rep, 2016, 6(1): 19396. DOI: 10.1038/srep19396.
20.	漆晨, 东莉洁, 乐毅, 等. 多聚嘧啶序列结合蛋白相关剪接因子对体外培养的视网膜色素上皮细胞磷脂酰肌醇3激酶/丝氨酸-苏氨酸蛋白激酶信号通路的调控作用[J]. 中华眼底病杂志, 2015, 31(4): 363-367. DOI: 10.3760/cma.j.issn.1005-1015.2015.04.013.Qi C, Dong LJ, Le Y, et al. The regulation of PTB-associated splicing factor on phosphatidylinositol 3 kinase/Akt signaling pathway in retinal pigment epithelial cells[J]. Chin J Ocul Fundus Dis, 2015, 31(4): 363-367. DOI: 10.3760/cma.j.issn.1005-1015.2015.04.013.
21.	Shao Y, Dong L, Takahashi Y, et al. miRNA-451a regulates RPE function through promoting mitochondrial function in proliferative diabetic retinopathy[J]. Am J Physiol-Endoc M, 2019, 316(3): 443-452. DOI: 10.1152/ajpendo.00360.2018.
22.	田芳, 李文博, 黄亮瑜, 等. 聚嘧啶束结合蛋白相关剪接因子对过氧化氢诱导下视网膜色素上皮细胞凋亡的影响[J]. 中华眼底病杂志, 2018, 34(2): 159-163. DOI: 10.3760/cma.j.issn.1005-1015.2018.02.012.Tian F, Li WB, Huang LY, et al. The effect of polypyrimidine tract binding protein-associated splicing factor on hydrogen peroxide induced apoptosis of retinal pigment epithelial[J]. Chin J Ocul Fundus Dis, 2018, 34(2): 159-163. DOI: 10.3760/cma.j.issn.1005-1015.2018.02.012.
23.	邢小丽, 黄亮瑜, 苏睿虹, 等. 丁基苯酞对过氧化氢诱导下视网膜Müller细胞凋亡的影响[J]. 中华眼底病杂志, 2018, 34(5): 481-486. DOI: 10.3760/cma.j.issn.1005-1015.2018.05.014.Xing XL, Huang LY, Su RH, et al. Effect of dl-3-n-Butylphthalide on apoptosis of retinal müller cells induced by hydrogen peroxide[J]. Chin J Ocul Fundus Dis, 2018, 34(5): 481-486. DOI: 10.3760/cma.j.issn.1005-1015.2018.05.014.
24.	Abed DA, Goldstein M, Albanyan H, et al. Discovery of direct inhibitors of Keap1-Nrf2 protein–protein interaction as potential therapeutic and preventive agents[J]. Acta Pharm Sin B, 2015, 5(4): 285-299. DOI: 10.1016/j.apsb.2015.05.008.
25.	Cullinan S B, Zhang D, Hannink M, et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival[J]. Mol Cell Biol, 2003, 23(20): 7198-7209. DOI: 10.1128/MCB.23.20.7198-7209.2003.

1. 田芳, 胡博杰, 李文博, 等. 高表达多聚嘧啶序列结合蛋白相关剪接因子对糖基化终产物诱导下视网膜Müller细胞凋亡的影响[J]. 中华眼底病杂志, 2019, 35(1): 70-75. DOI: 10.3760/cma.j.issn.1005-1015.2019.01.015.Tian F, Hu BJ, Li WB, et al. Effects of polypyramidine tract binding protein-associated splicing factor overexpression on apoptosis of human Müller cells under advanced glycation end products treatment[J]. Chin J Ocul Fundus Dis, 2019, 35(1): 70-75. DOI: 10.3760/cma.j.issn.1005-1015.2019.01.015.
2. 滕贺, 黄亮瑜, 田芳, 等. 衰老标记蛋白30高表达对紫外线诱导人晶状体上皮细胞凋亡的影响[J]. 中华眼科杂志, 2017, 53(11): 835-841. DOI: 10.3760/cma.j.issn.0412-4081.2017.11.007.Teng H, Huang LY, Tian F, et al. Effects of SMP-30 overexpression on apoptosis of human lens epithelial cells induced by ultraviolet B irradiation[J]. Chin J Ophthalmol, 2017, 53(11): 835-841. DOI: 10.3760/cma.j.issn.0412-4081.2017.11.007.
3. 田芳, 赵今稚, 滕贺, 等. Krüppel样因子6经活化转录因子4通路对晶状体上皮细胞凋亡的调控作用[J]. 中华实验眼科杂志, 2018, 36(3): 181-186. DOI: 10.3760/cma.j.issn.2095-0160.2018.03.005.Tian F, Zhao JZ, Teng H, et al. Regulation of Krüppel-like factor 6 via activating transcription factor 4 pathway to apoptosis of human lens epithelial cells[J]. Chin J Exp Ophthalmol, 2018, 36(3): 181-186. DOI: 10.3760/cma.j.issn.2095-0160.2018.03.005.
4. 刘爱华, 高美子, 黄亮瑜, 等. 叉头框转录因子F2小发夹RNA对人眼小梁网细胞外基质蛋白表达的抑制作用[J]. 中华实验眼科杂志, 2019, 37(6): 405-410. DOI: 10.3760/cma.j.issn.2095-0160.2019.06.002.Liu AH, Gao MZ, Huang LY, et al. The inhibitory effect of FoxF2 shRNA on the expression of extracellular matrix of human trabecular meshwork[J]. Chin J Exp Ophthalmol, 2019, 37(6): 405-410. DOI: 10.3760/cma.j.issn.2095-0160.2019.06.002.
5. Zhang P, Xu R, Guo Y, et al. DL-3-n-butylphthalide promotes dendrite development in cortical neurons subjected to oxygen-glucose deprivation/reperfusion[J]. Cell Biol Int, 2018, 42(8): 1041-1049. DOI: 10.1002/cbin.10980.
6. He Z, Zhou Y, Huang Y, et al. Dl-3-n-butylphthalide improves functional recovery in rats with spinal cord injury by inhibiting endoplasmic reticulum stress-induced apoptosis[J]. Am J Transl Res, 2017, 9(3): 1075-1087.
7. Liu Z, Wang H, Shi X, et al. Dl-3-n-butylphthalide (NBP) provides neuroprotection in the mice models after traumatic brain injury via Nrf2-ARE signaling pathway[J]. Neurochem Res, 2017, 42(5): 1375-1386. DOI: 10.1007/s11064-017-2186-z.
8. 田芳, 东莉洁, 吉洁, 等. 多聚嘧啶序列结合蛋白相关剪接因子对视网膜血管内皮细胞IGF-1/VEGF信号通路的抑制作用[J]. 中华实验眼科杂志, 2016, 34(1): 11-16. DOI: 10.3760/cma.j.issn.2095-0160.2016.01.003.Tian F, Dong LJ, Ji J, et al. Inhibition of PTB-associated splicing factor on IGF-1/VEGF signaling pathway in retinal vascular endothelial cells[J]. Chin J of Exp Ophthalmol, 2016, 34(1): 11-16. DOI: 10.3760/cma.j.issn.2095-0160.2016.01.003.
9. 田芳, 东莉洁, 周玉, 等. 重组腺相关病毒-多聚嘧啶序列结合蛋白相关剪接因子对氧诱导视网膜新生血管形成的抑制作用[J]. 中华眼底病杂志, 2014, 30(5): 504-508. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.019.Tian F, Dong LJ, Zhou Y, et al. Inhibition of oxygen induced retinal neovascularization by recombinant adeno-associated virus-polypyrimidine tract-binding protein-associated splicing factor intraocular injection in mice[J]. Chin J Ocul Fundus Dis, 2014, 30(5): 504-508. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.019.
10. 田芳, 赵今稚, 黄亮瑜, 等. 高表达Krüppel样因子6对紫外线B诱导的人晶状体上皮细胞凋亡的影响[J]. 中华实验眼科杂志, 2019, 37(4): 257-262. DOI: 10.3760/cma.j.issn.2095-0160.2019.04.004.Tian F, Zhao JZ, Huang LY, et al. Effects of Krüppel-like factor 6 overexpression towards apoptosis of human lens epithelial cells with ultra violetradiation B treatment[J]. Chin J Exp Ophthalmol, 2019, 37(4): 257-262. DOI: 10.3760/cma.j.issn.2095-0160.2019.04.004.
11. Tian F, Dong L, Zhou Y, et al. Rapamycin-induced apoptosis in HGF-stimulated lens epithelial cells by AKT/mTOR, ERK and JAK2/STAT3 pathways[J]. Int J Mol Sci, 2014, 15(8): 13833-13848. DOI: 10.3390/ijms150813833.
12. Dong L, Nian H, Shao Y, et al. PTB-associated splicing factor inhibits IGF-1-induced VEGF upregulation in a mouse model of oxygen-induced retinopathy[J]. Cell Tissue Res, 2015, 360(2): 233-243. DOI: 10.1007/s00441-014-2104-5.
13. Li W, Wei D, Lin J, et al. Dl-3-n-butylphthalide reduces cognitive impairment induced by chronic cerebral hypoperfusion through GDNF/GFRα1/ret signaling preventing hippocampal neuron apoptosis[J/OL]. Front Cell Neurosci, 2019, 13:351[2019-08-13]. https://doi.org/10.3389/fncel.2019.00351. DOI: 10.3389/fncel.2019.00351.
14. Chen Y, Jiang M, Li L, et al. DL-3-n-butylphthalide reduces microglial activation in lipopolysaccharide-induced Parkinson's disease model mice[J]. Mol Med Rep, 2017, 17(3): 3884-3890. DOI: 10.3892/mmr.2017.8332.
15. Wang C, Wang Z, Xie J, et al. Dl-3-n-butylphthalide-induced upregulation of antioxidant defense is involved in the enhancement of cross talk between CREB and Nrf2 in an Alzheimer's disease mouse model[J]. Neurobiol Aging, 2016, 38: 32-46. DOI: 10.1016/j.neurobiolaging.2015.10.024.
16. Feng X, Peng Y, Liu M, et al. Dl-3-n-butylphthalide extends survival by attenuating glial activation in a mouse model of amyotrophic lateral sclerosis[J]. Neuropharmacology, 2012, 62(2): 1004-1010. DOI: 10.1016/j.neuropharm.2011.10.009.
17. Qi Q, Xu J, Lv P, et al. DL-3-n-butylphthalide alleviates vascular cognitive impairment induced by chronic cerebral hypoperfusion by activating the Akt/Nrf2 signaling pathway in the hippocampus of rats[J]. Neurosci Lett, 2018, 672: 59-64. DOI: 10.1016/j.neulet.2017.11.051.
18. Qiu H, Ma J, Wu H, et al. DL-3-n-butylphthalide improves ventricular function, and prevents ventricular remodeling and arrhythmias in post-MI rats[J]. Naunyn Schmiedebergs Arch Pharmacol, 2018, 391(6): 627-637. DOI: 10.1007/s00210-018-1490-8.
19. Wang F, Ma J, Han F, et al. DL-3-n-butylphthalide delays the onset and progression of diabetic cataract by inhibiting oxidative stress in rat diabetic model[J]. Sci Rep, 2016, 6(1): 19396. DOI: 10.1038/srep19396.
20. 漆晨, 东莉洁, 乐毅, 等. 多聚嘧啶序列结合蛋白相关剪接因子对体外培养的视网膜色素上皮细胞磷脂酰肌醇3激酶/丝氨酸-苏氨酸蛋白激酶信号通路的调控作用[J]. 中华眼底病杂志, 2015, 31(4): 363-367. DOI: 10.3760/cma.j.issn.1005-1015.2015.04.013.Qi C, Dong LJ, Le Y, et al. The regulation of PTB-associated splicing factor on phosphatidylinositol 3 kinase/Akt signaling pathway in retinal pigment epithelial cells[J]. Chin J Ocul Fundus Dis, 2015, 31(4): 363-367. DOI: 10.3760/cma.j.issn.1005-1015.2015.04.013.
21. Shao Y, Dong L, Takahashi Y, et al. miRNA-451a regulates RPE function through promoting mitochondrial function in proliferative diabetic retinopathy[J]. Am J Physiol-Endoc M, 2019, 316(3): 443-452. DOI: 10.1152/ajpendo.00360.2018.
22. 田芳, 李文博, 黄亮瑜, 等. 聚嘧啶束结合蛋白相关剪接因子对过氧化氢诱导下视网膜色素上皮细胞凋亡的影响[J]. 中华眼底病杂志, 2018, 34(2): 159-163. DOI: 10.3760/cma.j.issn.1005-1015.2018.02.012.Tian F, Li WB, Huang LY, et al. The effect of polypyrimidine tract binding protein-associated splicing factor on hydrogen peroxide induced apoptosis of retinal pigment epithelial[J]. Chin J Ocul Fundus Dis, 2018, 34(2): 159-163. DOI: 10.3760/cma.j.issn.1005-1015.2018.02.012.
23. 邢小丽, 黄亮瑜, 苏睿虹, 等. 丁基苯酞对过氧化氢诱导下视网膜Müller细胞凋亡的影响[J]. 中华眼底病杂志, 2018, 34(5): 481-486. DOI: 10.3760/cma.j.issn.1005-1015.2018.05.014.Xing XL, Huang LY, Su RH, et al. Effect of dl-3-n-Butylphthalide on apoptosis of retinal müller cells induced by hydrogen peroxide[J]. Chin J Ocul Fundus Dis, 2018, 34(5): 481-486. DOI: 10.3760/cma.j.issn.1005-1015.2018.05.014.
24. Abed DA, Goldstein M, Albanyan H, et al. Discovery of direct inhibitors of Keap1-Nrf2 protein–protein interaction as potential therapeutic and preventive agents[J]. Acta Pharm Sin B, 2015, 5(4): 285-299. DOI: 10.1016/j.apsb.2015.05.008.
25. Cullinan S B, Zhang D, Hannink M, et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival[J]. Mol Cell Biol, 2003, 23(20): 7198-7209. DOI: 10.1128/MCB.23.20.7198-7209.2003.

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