Resveratrol protects human luteinised granulosa cells against hydrogen peroxide-induced oxidative injury through the Sirt1
Zhaoyan Nie
A , Rui Hua B , Yanan Zhang B , Na Zhang A , Yi Zhang A , Qiaoxia Li A and Haifeng Wu C *
+ Author Affiliations
- Author Affiliations
A Department of Reproductive Medicine, Fourth Hospital of Hebei Medical University, No. 12, Jiankang Road, Shijiazhuang, Hebei 050011, China.
B Histology and Embryology, Hebei Medical University, 361 East Zhongshan,Road, Shijiazhuang, Hebei 050010, China.
C Department of Medical Laboratory, Hebei Chest Hospital, No. 372, Shengli North Street, Shijiazhuang, Hebei 050010, China.
Reproduction, Fertility and Development 33(16) 831-840 https://doi.org/10.1071/RD21069
Published online: 1 November 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Granulosa cells (GCs) control follicular development and are important for female reproduction. Resveratrol (Res) was considered as an antioxidant and Sirt1 inducer. Hydrogen peroxide (H2O2) is the classical reagent to study oxidative stress. The study was conducted to investigate the role of Res against H2O2 in human luteinised granulosa cells (LGCs). The LGCs in the H2O2 group were treated with 100 μmol/L H2O2 for 24 h. The LGCs in the Res group were treated with 50 μmol/L Res for 2 h, followed by H2O2. The LGCs in the Sirt1 blockage group were treated with 2.5 μmol/L EX527 + 50 μmol/L Res for 2 h, followed by H2O2. Results showed that Res significantly increased LGCs viability in H2O2-induced LGCs. The apoptotic rate and ROS in the H2O2 group was higher and the antioxidant enzyme activity was lower compared with other groups. Following the Res, the apoptotic rate and ROS level were reduced and the antioxidant enzyme activity were increased. In the Res blockage group, no significant alterations in the cell apoptosis, ROS and antioxidant enzyme activity were observed compared with the H2O2 group. The Res group had a Caspase-3 downregulation and Sirt1 upregulation compared with the other groups. In conclusion, Res had a protective effect against the H2O2-induced LGCs, and the mechanism may be associated with Sirt1.
Keywords: apoptosis, cell viability, human luteinised granulosa cells, hydrogen peroxide, oxidative stress, reactive oxygen species, resveratrol, Sirt1.
References
Athar, M, Back, J, Tang, X, Kim, K, Kopelovich, L, Bickers, D, and Kim, A (2007). Resveratrol: a review of preclinical studies for human cancer prevention. Toxicology and Applied Pharmacology 224, 274–283.| Resveratrol: a review of preclinical studies for human cancer prevention.Crossref | GoogleScholarGoogle Scholar | 17306316PubMed |
Bradamante, S, Barenghi, L, and Villa, A (2004). Cardiovascular protective effects of resveratrol. Cardiovascular Therapeutics 22, 169–188.
| Cardiovascular protective effects of resveratrol.Crossref | GoogleScholarGoogle Scholar |
Chai, R, Fu, H, Zheng, Z, Liu, T, Ji, S, and Li, G (2017). Resveratrol inhibits proliferation and migration through SIRT1 mediated post-translational modification of PI3K/AKT signaling in hepatocellular carcinoma cells. Molecular Medicine Reports 16, 8037–8044.
| Resveratrol inhibits proliferation and migration through SIRT1 mediated post-translational modification of PI3K/AKT signaling in hepatocellular carcinoma cells.Crossref | GoogleScholarGoogle Scholar | 28983625PubMed |
Chen, D, Bruno, J, Easlon, E, Lin, S-J, Cheng, H-L, Alt, FW, and Guarente, L (13). Tissue-specific regulation of SIRT1 by calorie restriction. Genes and Development 22, 1753–1757.
| Tissue-specific regulation of SIRT1 by calorie restriction.Crossref | GoogleScholarGoogle Scholar | 18550784PubMed |
Devine, PJ, Perreault, SD, and Luderer, U (2012). Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biology of Reproduction 86, 27.
| Roles of reactive oxygen species and antioxidants in ovarian toxicity.Crossref | GoogleScholarGoogle Scholar | 22034525PubMed |
Esfandyari, S, Ale-Yasin, A, Noroozi, Z, Taheri, M, and Amidi, F (2020). The protective effect of sulforaphane against oxidative stress through activation of Nrf2/ARE pathway in human granulosa cells. Yakhteh , 23.
| The protective effect of sulforaphane against oxidative stress through activation of Nrf2/ARE pathway in human granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Finkel, T, Deng, C-X, and Mostoslavsky, R (2009). Recent progress in the biology and physiology of sirtuins. Nature 460, 587–591.
| Recent progress in the biology and physiology of sirtuins.Crossref | GoogleScholarGoogle Scholar | 19641587PubMed |
Giuseppina Basini, BS, Santini, SE, and Grasselli, F (2008). Reactive oxygen species and anti-oxidant defences in swine follicular fluids. Reproduction, Fertility and Development 20, 269–274.
| Reactive oxygen species and anti-oxidant defences in swine follicular fluids.Crossref | GoogleScholarGoogle Scholar |
Harati, K, Slodnik, P, Chromik, AM, Goertz, O, and Daigeler, A (2015). Resveratrol Induces apoptosis and alters gene expression in human fibrosarcoma cells. Anticancer Research 35, 767–774.
| 25667456PubMed |
Hasegawa, K, Wakino, S, Yoshioka, K, Tatematsu, S, Hara, Y, Minakuchi, H, and Itoh, H (2008). Sirt1 protects against oxidative stress-induced renal tubular cell apoptosis by the bidirectional regulation of catalase expression. Biochemical & Biophysical Research Communications 372, 51–56.
| Sirt1 protects against oxidative stress-induced renal tubular cell apoptosis by the bidirectional regulation of catalase expression.Crossref | GoogleScholarGoogle Scholar |
Howitz, KT, Bitterman, KJ, Cohen, HY, Lamming, DW, Lavu, S, Wood, JG, and Zhang, L-L (2003). Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425, 191–196.
| Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan.Crossref | GoogleScholarGoogle Scholar | 12939617PubMed |
Keavey, K, Pons, J-F, Barker, J, Yau, WT, Amouzegh, P, Flegg, A, et al. (2005). Discovery of indoles as potent and selective inhibitors of the deacetylase SIRT1. Journal of Medical Chemistry 48, 8045–8054.
| Discovery of indoles as potent and selective inhibitors of the deacetylase SIRT1.Crossref | GoogleScholarGoogle Scholar |
Leonard, SS, Xia, C, Jiang, B-H, Stinefelt, B, Klandorf, H, Harris, GK, and Shi, X (2003). Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochemical and Biophysical Research Communications 309, 1017–1026.
| Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses.Crossref | GoogleScholarGoogle Scholar | 13679076PubMed |
Matsuda, F, Inoue, N, Manabe, N, and Ohkura, S (2012). Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. Journal of Reproductive Development 58, 44–50.
| Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Michan, S, and Sinclair, D (2007). Sirtuins in mammals: insights into their biological function. The Biochemical Journal 404, 1–13.
| Sirtuins in mammals: insights into their biological function.Crossref | GoogleScholarGoogle Scholar | 17447894PubMed |
Morita, Y, Wada-Hiraike, O, Yano, T, Shirane, A, Hirano, M, Hiraike, H, et al (2012). Resveratrol promotes expression of SIRT1 and StAR in rat ovarian granulosa cells: an implicative role of SIRT1 in the ovary. Reproductive Biology and Endocrinology 10, 14–10.
| Resveratrol promotes expression of SIRT1 and StAR in rat ovarian granulosa cells: an implicative role of SIRT1 in the ovary.Crossref | GoogleScholarGoogle Scholar | 22357324PubMed |
Nie, Z, Zhang, L, Chen, W, Zhang, Y, Hua, R, Wang, W, et al (2020). The protective effects of pretreatment with resveratrol in cyclophosphamide-induced rat ovarian granulosa cell injury: in vitro study. Reproductive Toxicology 95, 66–74.
| The protective effects of pretreatment with resveratrol in cyclophosphamide-induced rat ovarian granulosa cell injury: in vitro study.Crossref | GoogleScholarGoogle Scholar | 32446930PubMed |
Oh, WY, and Shahidi, F (2018). Antioxidant activity of resveratrol ester derivatives in food and biological model systems. Food Chemistry 261, 267–273.
| Antioxidant activity of resveratrol ester derivatives in food and biological model systems.Crossref | GoogleScholarGoogle Scholar | 29739593PubMed |
Ortega, I, and Duleba, A (2015). Ovarian actions of resveratrol. Annals of the New York Academy of Sciences 1348, 86–96.
| Ovarian actions of resveratrol.Crossref | GoogleScholarGoogle Scholar | 26315293PubMed |
Shi, J, Yoshino, O, Osuga, Y, Nishii, O, Yano, T, and Taketani, Y (2010). Bone morphogenetic protein 7 (BMP-7) increases the expression of follicle-stimulating hormone (FSH) receptor in human granulosa cells. Fertility and Sterility 93, 1273–1279.
| Bone morphogenetic protein 7 (BMP-7) increases the expression of follicle-stimulating hormone (FSH) receptor in human granulosa cells.Crossref | GoogleScholarGoogle Scholar | 19108831PubMed |
Simon, HU, Haj-Yehia, A, and Levi-Schaffer, F (2000). Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–418.
| Role of reactive oxygen species (ROS) in apoptosis induction.Crossref | GoogleScholarGoogle Scholar | 11256882PubMed |
Singh, C, Kumar, A, Hitchcock, D, Fan, D, Goodwin, R, Lavoie, H, et al (2011). Resveratrol prevents embryonic oxidative stress and apoptosis associated with diabetic embryopathy and improves glucose and lipid profile of diabetic dam. Molecular Nutrition & Food Research 55, 1186–1196.
| Resveratrol prevents embryonic oxidative stress and apoptosis associated with diabetic embryopathy and improves glucose and lipid profile of diabetic dam.Crossref | GoogleScholarGoogle Scholar |
Sohel, MH, Cinar, MU, Kalibar, M, Arslan, K, Sariozkan, S, Akyuz, B, and Konca, Y (2016). Appropriate concentration of hydrogen peroxide and sulforaphane for granulosa cells to study oxidative stress in vitro. Journal of Biotechnology 231, S24.
| Appropriate concentration of hydrogen peroxide and sulforaphane for granulosa cells to study oxidative stress in vitro.Crossref | GoogleScholarGoogle Scholar |
Solomon, JM, Pasupuleti, R, Xu, L, McDonagh, T, Curtis, R, DiStefano, PS, and Huber, LJ (2006). Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage. Molecular and Cellular Biology 26, 28–38.
| Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage.Crossref | GoogleScholarGoogle Scholar | 16354677PubMed |
Tatone, C, Di Emidio, G, Vitti, M, Di Carlo, M, Santini, S, D’Alessandro, AM, et al (2015). Sirtuin functions in female fertility: possible role in oxidative stress and aging. Oxidative Medicine and Cellular Longevity 2015, 659687.
| Sirtuin functions in female fertility: possible role in oxidative stress and aging.Crossref | GoogleScholarGoogle Scholar | 26075037PubMed |
Zhou, X, Ni, Y, and Luo, L (2015). Biological characteristics of SIRT1 and its effect on ovarian follicle development. Chinese Journal of Clinicians 22, 4166–4171.
