Lithocarpus polystachyus Rehd. leaves aqueous extract protects against hydrogen peroxide‑induced SH-SY5Y cells injury through activation of Sirt3 signaling pathway

Gao,Jianmei; Xu,Yingshu; Zhang,Jianyong; Shi,Jingshan; Gong,Qihai

doi:10.3892/ijmm.2018.3916

Lithocarpus polystachyus Rehd. leaves aqueous extract protects against hydrogen peroxide‑induced SH-SY5Y cells injury through activation of Sirt3 signaling pathway

Authors:
- Jianmei Gao
- Yingshu Xu
- Jianyong Zhang
- Jingshan Shi
- Qihai Gong
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Affiliations: Department of Clinical Pharmacotherapeutics, School of Pharmacy, Zunyi Medical University, Zunyi, Guizhou 563000, P.R. China, Department of Pharmacology, Key Laboratory of Basic Pharmacology of Ministry of Education, Zunyi Medical University, Zunyi, Guizhou 563000, P.R. China
Published online on: October 5, 2018 https://doi.org/10.3892/ijmm.2018.3916
Pages: 3485-3494

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Abstract

Lithocarpus polystachyus Rehd. (sweet tea; ST) leaves is a type of Chinese folkloric medicine from southern China. The purpose of the present study was to explore the neuroprotective effect of ST, and to explore its underlying mechanisms in hydrogen peroxide (H2O2)‑induced neuronal cell injury in cultured human neuroblastoma. H2O2 was used as oxidant inducer and human SH‑SY5Y neuroblastoma cells were treated with various concentrations of ST. Cell viability and cell death were detected using MTT and LDH assays, respectively. Additionally, the production of intracellular and mitochondrial reactive oxygen species (ROS) were determined by 2',7'‑dichlorodihydrofluorescein diacetate (DCFH‑DA) and MitoSOX Red, respectively. The production of malondialdehyde (MDA), reduced glutathione (GSH) level, glutathione peroxidase (GSH‑Px), superoxide dismutase (SOD) activities, and NAD+/NADH ratio were confirmed using relevant kits. The expression of adenosine monophosphate‑activated protein kinase (AMPK), peroxisome proliferator‑activated receptor coactivator (PGC)‑1α, Sirt3, isocitrate dehydrogenase (IDH)2, forkhead boxO3a (Foxo3a), and SOD2 were analyzed by western blot analysis. It was demonstrated that pre‑treatment with ST enhanced cell viability and repressed cell death, and it also reduced intracellular and mitochondrial ROS accumulation. Additionally, ST attenuated MDA production and enhanced GSH level, GSH‑Px and SOD activities. Furthermore, ST not only increased NAD+/NADH ratio, but also inhibited the decrease of AMPK, PGC‑1α, Sirt3, IDH2, Foxo3a, and SOD2. The present study revealed that ST exerts protective effects against oxidative stress‑induced SH‑SY5Y cells injury, and the underlying mechanisms are, at least partly, associated with its antioxidant capacity and function through mitochondrial Sirt3 signaling pathway.

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1	Liu L, Zhang K, Sandoval H, Yamamoto S, Jaiswal M, Sanz E, Li Z and Hui J: Glial lipid droplets and ROS induced by mitochondrial defects promote neurodegeneration. Cell. 160:177–190. 2015. View Article : Google Scholar : PubMed/NCBI
2	Zhang JX, Wang R, Xi J, Shen L, Zhu AY, Qi Q, Wang QY, Zhang LJ, Wang FC, Lü HZ and Hu JG: Morroniside protects SK-N-SH human neuroblastoma cells against H₂O₂-induced damage. Int J Mol Med. 39:603–612. 2017. View Article : Google Scholar : PubMed/NCBI
3	Hanschmann EM, Godoy JR, Berndt C, Hudemann C and Lillig CH: Thioredoxins, glutaredoxins, and peroxire-doxins-molecular mechanisms and health significance: From cofactors to antioxidants to redox signaling. Antioxid Redox Signal. 19:1539–1605. 2013. View Article : Google Scholar : PubMed/NCBI
4	Tseng AH, Shieh SS and Wang DL: SIRT3 deacetylates FOXO3 to protect mitochondria against oxidative damage. Free Radic Biol Med. 63:222–234. 2013. View Article : Google Scholar : PubMed/NCBI
5	Wang Y, Wang Y, Li J, Hua L, Han B, Zhang Y, Yang X, Zeng Z, Bai H, Yin H and Lou J: Effects of caffeic acid on learning deficits in a model of Alzheimer's disease. Int J Mol Med. 38:869–875. 2016. View Article : Google Scholar : PubMed/NCBI
6	Wang J, Huang Y, Li K, Chen Y, Vanegas D, McLamore ES and Shen Y: Leaf extract from Lithocarpus polystachyus Rehd promote glycogen synthesis in T2DM mice. PLoS One. 11:e01665572016. View Article : Google Scholar
7	Hou SZ, Chen SX, Huang S, Jiang DX, Zhou CJ, Chen CQ, Liang YM and Lai XP: The hypoglycemic activity of Lithocarpus polystachyus Rehd leaves in the experimental hyperglycemic rats. J Ethnopharmacol. 138:142–149. 2011. View Article : Google Scholar : PubMed/NCBI
8	Hou SZ, Xu SJ, Jiang DX, Chen SX, Wang LL, Huang S and Lai XP: Effect of the flavonoid fraction of Lithocarpus polys-tachyus Rehd on spontaneously hypertensive and normotensive rats. J Ethnopharmacol. 143:441–447. 2012. View Article : Google Scholar : PubMed/NCBI
9	Zhou CJ, Huang S, Liu JQ, Qiu SQ, Xie FY, Song HP, Li YS, Hou SZ and Lai XP: Sweet tea leaves extract improves leptin resistance in diet-induced obese rats. J Ethnopharmacol. 145:386–392. 2013. View Article : Google Scholar
10	Gao XY, Wang SN, Yang XH, Lan WJ, Chen ZW, Chen JK, Xie JH, Han YF, Pi RB and Yang XB: Gartanin protects neurons against glutamate-induced cell death in HT22 cells: Independence of Nrf-2 but involvement of HO-1 and AMPK. Neurochem Res. 41:2267–2277. 2016. View Article : Google Scholar : PubMed/NCBI
11	Cheng L, Li B, Chen X, Su J, Wang H, Yu S and Zheng Q: CTRP9 induces mitochondrial biogenesis and protects high glucose-induced endothelial oxidative damage via AdipoR1-SIRT1-PGC-1α activation. Biochem Biophys Res Commun. 477:685–691. 2016. View Article : Google Scholar : PubMed/NCBI
12	Kincaid B and Bossy-Wetzel E: Forever young: SIRT3 a shield against mitochondrial meltdown, aging, and neurodegeneration. Front Aging Neurosci. 5:482013. View Article : Google Scholar : PubMed/NCBI
13	Guan Y, Cui ZJ, Sun B, Han LP, Li CJ and Chen LM: Celastrol attenuates oxidative stress in the skeletal muscle of diabetic rats by regulating the AMPK-PGC1α-SIRT3 signaling pathway. Int J Mol Med. 37:1229–1238. 2016. View Article : Google Scholar : PubMed/NCBI
14	Wang Q, Li L, Li CY, Pei Z, Zhou M and Li N: SIRT3 protects cells from hypoxia via PGC-1α- and MnSOD-dependent pathways. Neuroscience. 286:109–121. 2015. View Article : Google Scholar
15	Rangarajan P, Karthikeyan A, Lu J, Ling EA and Dheen ST: Sirtuin 3 regulates Foxo3a-mediated antioxidant pathway in microglia. Neuroscience. 311:398–414. 2015. View Article : Google Scholar : PubMed/NCBI
16	Dong H, Ning Z, Yu L, Li L, Lin L and Huang J: Preparative separation and identification of the flavonoid phlorhizin from the crude extract of Lithocarpus polystachyus Rehd. Molecules. 12:552–562. 2007. View Article : Google Scholar : PubMed/NCBI
17	Chen TY, Chi KH, Wang JS, Chien CL and Lin WW: Reactive oxygen species are involved in FasL-induced caspase-independent cell death and inflammatory responses. Free Radic Biol Med. 46:643–655. 2009. View Article : Google Scholar
18	Ishii T, Takanashi Y, Sugita K, Miyazawa M, Yanagihara R, Yasuda K, Onouchi H, Kawabe N, Nakata M, Yamamoto Y, et al: Endogenous reactive oxygen species cause astrocyte defects and neuronal dysfunctions in the hippocampus: A new model for aging brain. Aging Cell. 16:39–51. 2017. View Article : Google Scholar :
19	Gao JM, Li R, Zhang L, Jia LL, Ying XX, Dou DQ, Li JC and Li HB: Cuscuta chinensis seeds water extraction protecting murine osteoblastic MC3T3-E1 cells against tertiary butyl hydroperoxide induced injury. J Ethnopharmacol. 148:587–595. 2013. View Article : Google Scholar : PubMed/NCBI
20	Yang YY, Sun XT, Li ZX, Chen WY, Wang X, Liang ML, Shi H, Yang ZS and Zeng WT: Protective effect of angiotensin-(1-7) against hyperglycaemia-induced injury in H9c2 cardiomyoblast cells via the PI3KAkt signaling pathway. Int J Mol Med. 41:1283–1292. 2018.
21	Roelofs BA, Ge SX, Studlack PE and Polster BM: Low micromolar concentrations of the superoxide probe MitoSOX uncouple neural mitochondria and inhibit complex IV. Free Radic Biol Med. 86:250–258. 2015. View Article : Google Scholar : PubMed/NCBI
22	Lee Y, Heo G, Lee KM, Kim AH, Chung KW, Im E, Chung HY and Lee J: Neuroprotective effects of 2,4-dinitrophenol in an acute model of Parkinson's disease. Brain Res. 1663:184–193. 2017. View Article : Google Scholar : PubMed/NCBI
23	Hong YA, Lim JH, Kim MY, Kim Y, Park HS, Kim HW, Choi BS, Chang YS, Kim HW, Kim TY and Park CW: Extracellular superoxide dismutase attenuates renal oxidative stress through the activation of adenosine monophosphate-activated protein kinase in diabetic nephropathy. Antioxid Redox Signal. 28:1543–1561. 2018. View Article : Google Scholar
24	Gao C, Chang P, Yang L, Wang Y, Zhu S, Shan H, Zhang M and Tao L: Neuroprotective effects of hydrogen sulfide on sodium azide-induced oxidative stress in PC12 cells. Int J Mol Med. 41:242–250. 2018.
25	Di Domenico F, Barone E, Perluigi M and Butterfield DA: The triangle of death in Alzheimer's disease brain: The aberrant cross-talk among energy metabolism, mammalian target of rapamycin signaling, and protein homeostasis revealed by redox proteomics. Antioxid Redox Signal. 26:364–387. 2017. View Article : Google Scholar
26	Wang X, Dong W, Yuan B, Yang Y, Yang D, Lin X, Chen C and Zhang W: Vitamin E confers cytoprotective effects on cardiomyocytes under conditions of heat stress by increasing the expression of metallothionein. Int J Mol Med. 37:1429–1436. 2016. View Article : Google Scholar : PubMed/NCBI
27	Gao J, Deng Y, Yin C, Liu Y, Zhang W, Shi J and Gong Q: Icariside II, a novel phosphodiesterase 5 inhibitor, protects against H₂O₂-induced PC12 cells death by inhibiting mitochondria-mediated autophagy. J Cell Mol Med. 21:375–386. 2017. View Article : Google Scholar
28	Zhong J, Xu C, Gabbay-Benziv R, Lin X and Yang P: Superoxide dismutase 2 overexpression alleviates maternal diabetes-induced neural tube defects, restores mitochondrial function and suppresses cellular stress in diabetic embryopathy. Free Radic Biol Med. 96:234–244. 2016. View Article : Google Scholar : PubMed/NCBI
29	Rottenberg H and Hoek JB: The path from mitochondrial ROS to aging runs through the mitochondrial permeability transition pore. Aging Cell. 16:943–955. 2017. View Article : Google Scholar : PubMed/NCBI
30	Zhang JY, Deng YN, Zhang M, Su H and Qu QM: SIRT3 acts as a neuroprotective agent in rotenone-induced Parkinson cell model. Neurochem Res. 41:1761–1773. 2016. View Article : Google Scholar : PubMed/NCBI
31	Yin J, Han P, Tang Z, Liu Q and Shi J: Sirtuin 3 mediates neuro-protection of ketones against ischemic stroke. J Cereb Blood Flow Metab. 35:1783–1789. 2015. View Article : Google Scholar : PubMed/NCBI
32	Zhou X, Chen M, Zeng X, Yang J, Deng H, Yi L and Mi MT: Resveratrol regulates mitochondrial reactive oxygen species homeostasis through Sirt3 signaling pathway in human vascular endothelial cells. Cell Death Dis. 5:e15762014. View Article : Google Scholar : PubMed/NCBI
33	Guo Q, Li S, Xie Y, Zhang Q, Liu M, Xu Z, Sun H and Yang Y: The NAD⁺-dependent deacetylase, Bifidobacterium longum Sir2 in response to oxidative stress by deacetylating SigH (sigmaH) and FOXO3a in Bifidobacterium longum and HEK293T cell respectively. Free Radic Biol Med. 108:929–939. 2017. View Article : Google Scholar : PubMed/NCBI
34	Guo Y, Li Z, Shi C, Li J, Yao M and Chen X: Trichostatin A attenuates oxidative stress-mediated myocardial injury through the FoxO3a signaling pathway. Int J Mol Med. 40:999–1008. 2017. View Article : Google Scholar : PubMed/NCBI
35	Yu L, Gong B, Duan W, Fan C, Zhang J, Li Z, Xue X, Xu Y, Meng D, Li B, et al: Melatonin ameliorates myocardial ischemia/reperfusion injury in type 1 diabetic rats by preserving mitochondrial function: Role of AMPK-PGC-1α-SIRT3 signaling. Sci Rep. 7:413372017. View Article : Google Scholar
36	Dai SH, Chen T, Wang YH, Zhu J, Luo P, Rao W, Yang YF, Fei Z and Jiang XF: Sirt3 attenuates hydrogen peroxide-induced oxidative stress through the preservation of mitochondrial function in HT22 cells. Int J Mol Med. 34:1159–1168. 2014. View Article : Google Scholar : PubMed/NCBI
37	Karnewar S, Neeli PK, Panuganti D, Kotagiri S, Mallappa S, Jain N, Jerald MK and Kotamraju S: Metformin regulates mitochondrial biogenesis and senescence through AMPK mediated H3K79 methylation: Relevance in age-associated vascular dysfunction. Biochim Biophys Acta. 1864:1115–1128. 2018. View Article : Google Scholar