Naringenin mitigates cadmium-induced cell death, oxidative stress, mitochondrial dysfunction, and inflammation in KGN cells by regulating the expression of sirtuin-1

References

• Abu-Hayyeh, S., Sian, M., Jones, K. G., Manuel, A., & Powell, J. T. (2001). Cadmium accumulation in aortas of smokers. Arteriosclerosis, Thrombosis, and Vascular Biology, 21(5), 863–867. https://doi.org/10.1161/01.atv.21.5.863
   PubMed Web of Science ®Google Scholar
• Alam, M. A., Subhan, N., Rahman, M. M., Uddin, S. J., Reza, H. M., & Sarker, S. D. (2014). Effect of citrus flavonoids, naringin and naringenin, on metabolic syndrome and their mechanisms of action. Advances in Nutrition (Bethesda, Md.), 5(4), 404–417. https://doi.org/10.3945/an.113.005603
   PubMed Web of Science ®Google Scholar
• Alfwuaires, M. A., Famurewa, A. C., Algefare, A. I., & Sedky, A. (2023). Naringenin blocks hepatic cadmium accumulation and suppresses cadmium-induced hepatotoxicity via amelioration of oxidative inflammatory signaling and apoptosis in rats. Drug and Chemical Toxicology. Advance online publication. https://doi.org/10.1080/01480545.2023.2196377
   PubMed Web of Science ®Google Scholar
• Arab, H. H., Ashour, A. M., Eid, A. H., Arafa, E. A., Al Khabbaz, H. J., & Abd El-Aal, S. A. (2022). Targeting oxidative stress, apoptosis, and autophagy by galangin mitigates cadmium-induced renal damage: Role of SIRT1/Nrf2 and AMPK/mTOR pathways. Life Sciences, 291, 120300 https://doi.org/10.1016/j.lfs.2021.120300
   PubMed Web of Science ®Google Scholar
• Assini, J. M., Mulvihill, E. E., Sutherland, B. G., Telford, D. E., Sawyez, C. G., Felder, S. L., Chhoker, S., Edwards, J. Y., Gros, R., & Huff, M. W. (2013). Naringenin prevents cholesterol-induced systemic inflammation, metabolic dysregulation, and atherosclerosis in Ldlr-/- mice. Journal of Lipid Research, 54(3), 711–724. https://doi.org/10.1194/jlr.M032631
   PubMed Web of Science ®Google Scholar
• Barreca, D., Gattuso, G., Bellocco, E., Calderaro, A., Trombetta, D., Smeriglio, A., Laganà, G., Daglia, M., Meneghini, S., & Nabavi, S. M. (2017). Flavanones: Citrus phytochemical with health-promoting properties. BioFactors (Oxford, England), 43(4), 495–506. https://doi.org/10.1002/biof.1363
   PubMed Web of Science ®Google Scholar
• Borra, M. T., Smith, B. C., & Denu, J. M. (2005). Mechanism of human SIRT1 activation by resveratrol. The Journal of Biological Chemistry, 280(17), 17187–17195. https://doi.org/10.1074/jbc.M501250200
   PubMed Web of Science ®Google Scholar
• Chen, W., Lin, B., Xie, S., Yang, W., Lin, J., Li, Z., Zhan, Y., Gui, S., & Lin, B. (2021). Naringenin protects RPE cells from NaIO(3)-induced oxidative damage in vivo and in vitro through up-regulation of SIRT1. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology, 80, 153375 https://doi.org/10.1016/j.phymed.2020.153375
   PubMed Web of Science ®Google Scholar
• Chou, X., Ding, F., Zhang, X., Ding, X., Gao, H., & Wu, Q. (2019). Sirtuin-1 ameliorates cadmium-induced endoplasmic reticulum stress and pyroptosis through XBP-1s deacetylation in human renal tubular epithelial cells. Archives of Toxicology, 93(4), 965–986. https://doi.org/10.1007/s00204-019-02415-8
   PubMed Web of Science ®Google Scholar
• Das, A., Roy, A., Das, R., Bhattacharya, S., & Haldar, P. K. (2016). Naringenin alleviates cadmium-induced toxicity through the abrogation of oxidative stress in Swiss albino mice. Journal of Environmental Pathology, Toxicology and Oncology: Official Organ of the International Society for Environmental Toxicology and Cancer, 35(2), 161–169. https://doi.org/10.1615/JEnvironPatholToxicolOncol.2016015892
   PubMed Web of Science ®Google Scholar
• de Oliveira, M. R., Brasil, F. B., & Andrade, C. M. B. (2017). Naringenin attenuates H(2)O(2)-induced mitochondrial dysfunction by an Nrf2-dependent mechanism in SH-SY5Y cells. Neurochemical Research, 42(11), 3341–3350. https://doi.org/10.1007/s11064-017-2376-8
   PubMed Web of Science ®Google Scholar
• Ding, H., Li, Z., Li, X., Yang, X., Zhao, J., Guo, J., Lu, W., Liu, H., & Wang, J. (2022). FTO alleviates CdCl(2)-induced apoptosis and oxidative stress via the AKT/Nrf2 pathway in bovine granulosa cells. International Journal of Molecular Sciences, 23(9). https://doi.org/10.3390/ijms23094948
   Web of Science ®Google Scholar
• Feng, K., Chen, Z., Pengcheng, L., Zhang, S., & Wang, X. (2019). Quercetin attenuates oxidative stress-induced apoptosis via SIRT1/AMPK-mediated inhibition of ER stress in rat chondrocytes and prevents the progression of osteoarthritis in a rat model. Journal of Cellular Physiology, 234(10), 18192–18205. https://doi.org/10.1002/jcp.28452
   PubMed Web of Science ®Google Scholar
• Genchi, G., Sinicropi, M. S., Lauria, G., Carocci, A., & Catalano, A. (2020). The effects of cadmium toxicity. International Journal of Environmental Research and Public Health, 17(11), 3782 https://doi.org/10.3390/ijerph17113782
   PubMed Web of Science ®Google Scholar
• Gogola-Mruk, J., Tworzydło, W., Krawczyk, K., Marynowicz, W., & Ptak, A. (2023). Visfatin induces ovarian cancer resistance to anoikis by regulating mitochondrial activity. Endocrine, 80(2), 448–458. https://doi.org/10.1007/s12020-023-03305-x
   PubMed Web of Science ®Google Scholar
• Haigis, M. C., & Guarente, L. P. (2006). Mammalian sirtuins–emerging roles in physiology, aging, and calorie restriction. Genes & Development, 20(21), 2913–2921. https://doi.org/10.1101/gad.1467506
   PubMed Web of Science ®Google Scholar
• Howitz, K. T., Bitterman, K. J., Cohen, H. Y., Lamming, D. W., Lavu, S., Wood, J. G., Zipkin, R. E., Chung, P., Kisielewski, A., Zhang, L. L., Scherer, B., & Sinclair, D. A. (2003). Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature, 425(6954), 191–196. https://doi.org/10.1038/nature01960
   PubMed Web of Science ®Google Scholar
• Hua, Y. Q., Zeng, Y., Xu, J., & Xu, X. L. (2021). Naringenin alleviates nonalcoholic steatohepatitis in middle-aged Apoe(-/-)mice: role of SIRT1. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology, 81, 153412 https://doi.org/10.1016/j.phymed.2020.153412
   PubMed Web of Science ®Google Scholar
• Idrees, M., Kumar, V., Khan, A. M., Joo, M. D., Uddin, Z., Lee, K. W., & Kong, I. K. (2022). Hesperetin activated SIRT1 neutralizes cadmium effects on the early bovine embryo development. Theriogenology, 189, 209–221. https://doi.org/10.1016/j.theriogenology.2022.06.008
   PubMed Web of Science ®Google Scholar
• Jia, Y., Lin, J., Mi, Y., & Zhang, C. (2011). Quercetin attenuates cadmium-induced oxidative damage and apoptosis in granulosa cells from chicken ovarian follicles. Reproductive Toxicology (Elmsford, N.Y.), 31(4), 477–485. https://doi.org/10.1016/j.reprotox.2010.12.057
   PubMed Web of Science ®Google Scholar
• Jin, Y., & Wang, H. (2019). Naringenin inhibit the hydrogen peroxide-induced SH-SY5Y cells injury through Nrf2/HO-1 pathway. Neurotoxicity Research, 36(4), 796–805. https://doi.org/10.1007/s12640-019-00046-6
   PubMed Web of Science ®Google Scholar
• Kelts, J. L., Cali, J. J., Duellman, S. J., & Shultz, J. (2015). Altered cytotoxicity of ROS-inducing compounds by sodium pyruvate in cell culture medium depends on the location of ROS generation. SpringerPlus, 4(1), 269. https://doi.org/10.1186/s40064-015-1063-y
   PubMedGoogle Scholar
• Liang, S., Li, X., Liu, R., Hu, J., Li, Y., Sun, J., & Bai, W. (2023). Malvidin-3-O-glucoside ameliorates cadmium-mediated cell dysfunction in the estradiol generation of human granulosa cells. Nutrients, 15(3), 753 https://doi.org/10.3390/nu15030753
   PubMed Web of Science ®Google Scholar
• Lim, K. H., & Kim, G. R. (2018). Inhibitory effect of naringenin on LPS-induced skin senescence by SIRT1 regulation in HDFs. Biomedical Dermatology, 2(1), 26 https://doi.org/10.1186/s41702-018-0035-6
   Google Scholar
• Liu, J., Li, L., Zhu, J., Luo, L., Li, Y., Zhang, C., & Zhang, W. (2022). Cadmium disrupts mouse embryonic stem cell differentiation into ovarian granulosa cells through epigenetic mechanisms. Ecotoxicology and Environmental Safety, 235, 113431. https://doi.org/10.1016/j.ecoenv.2022.113431
   PubMed Web of Science ®Google Scholar
• Liu, J., Luo, L. F., Wang, D. L., Wang, W. X., Zhu, J. L., Li, Y. C., Chen, N. Z., Huang, H. L., & Zhang, W. C. (2019). Cadmium induces ovarian granulosa cell damage by activating PERK-eIF2α-ATF4 through endoplasmic reticulum stress. Biology of Reproduction, 100(1), 292–299. https://doi.org/10.1093/biolre/ioy169
   PubMed Web of Science ®Google Scholar
• López-Almada, G., Domínguez-Avila, J. A., Mejía-León, M. E., Robles-Sánchez, M., González-Aguilar, G. A., & Salazar-López, N. J. (2023). Could naringenin participate as a regulator of obesity and satiety? Molecules (Basel, Switzerland), 28(3), 1450 https://doi.org/10.3390/molecules28031450
   PubMed Web of Science ®Google Scholar
• Massányi, P., Massányi, M., Madeddu, R., Stawarz, R., & Lukáč, N. (2020). Effects of cadmium, lead, and mercury on the structure and function of reproductive organs. Toxics, 8(4), 94 https://doi.org/10.3390/toxics8040094
   PubMed Web of Science ®Google Scholar
• Munteanu, I. G., & Apetrei, C. (2021). Analytical methods used in determining antioxidant activity: A review. International Journal of Molecular Sciences, 22(7), 3380 https://doi.org/10.3390/ijms22073380
   PubMed Web of Science ®Google Scholar
• Naraki, K., Rezaee, R., & Karimi, G. (2021). A review on the protective effects of naringenin against natural and chemical toxic agents. Phytotherapy Research: Ptr, 35(8), 4075–4091. https://doi.org/10.1002/ptr.7071
   PubMed Web of Science ®Google Scholar
• Orhan, I. E., Nabavi, S. F., Daglia, M., Tenore, G. C., Mansouri, K., & Nabavi, S. M. (2015). Naringenin and atherosclerosis: a review of literature. Current Pharmaceutical Biotechnology, 16(3), 245–251. https://doi.org/10.2174/1389201015666141202110216
   PubMed Web of Science ®Google Scholar
• Paksy, K., Rajczy, K., Forgács, Z., Lázár, P., Bernard, A., Gáti, I., & Kaáli, G. S. (1997). Effect of cadmium on morphology and steroidogenesis of cultured human ovarian granulosa cells. Journal of Applied Toxicology, 17(5), 321–327. https://doi.org/10.1002/(SICI)1099-1263(199709)17:5<321::AID-JAT443>3.0.CO;2-E
   PubMed Web of Science ®Google Scholar
• Park, S. S., Skaar, D. A., Jirtle, R. L., & Hoyo, C. (2017). Epigenetics, obesity and early-life cadmium or lead exposure. Epigenomics, 9(1), 57–75. https://doi.org/10.2217/epi-2016-0047
   PubMed Web of Science ®Google Scholar
• Qi, J., Liu, L., Yang, J., Gao, X., & Zhang, W. (2020). Bisphenol A decreases progesterone synthesis in human ovarian granulosa cells. Birth Defects Research, 112(20), 1843–1849. https://doi.org/10.1002/bdr2.1817
   PubMedGoogle Scholar
• Qu, J., Wang, Q., Sun, X., & Li, Y. (2022). The environment and female reproduction: Potential mechanism of cadmium poisoning to the growth and development of ovarian follicle. Ecotoxicology and Environmental Safety, 244, 114029 https://doi.org/10.1016/j.ecoenv.2022.114029
   PubMed Web of Science ®Google Scholar
• Rani, N., Bharti, S., Krishnamurthy, B., Bhatia, J., Sharma, C., Kamal, M. A., Ojha, S., & Arya, D. S. (2016). Pharmacological properties and therapeutic potential of naringenin: A citrus flavonoid of pharmaceutical promise. Current Pharmaceutical Design, 22(28), 4341–4359. https://doi.org/10.2174/1381612822666160530150936
   PubMed Web of Science ®Google Scholar
• Renugadevi, J., & Prabu, S. M. (2009). Naringenin protects against cadmium-induced oxidative renal dysfunction in rats. Toxicology, 256(1–2), 128–134. https://doi.org/10.1016/j.tox.2008.11.012
   PubMed Web of Science ®Google Scholar
• Renugadevi, J., & Prabu, S. M. (2010). Cadmium-induced hepatotoxicity in rats and the protective effect of naringenin. Experimental and Toxicologic Pathology: Official Journal of the Gesellschaft Fur Toxikologische Pathologie, 62(2), 171–181. https://doi.org/10.1016/j.etp.2009.03.010
   PubMed Web of Science ®Google Scholar
• Shokri Afra, H., Zangooei, M., Meshkani, R., Ghahremani, M. H., Ilbeigi, D., Khedri, A., Shahmohamadnejad, S., Khaghani, S., & Nourbakhsh, M. (2019). Hesperetin is a potent bioactivator that activates SIRT1-AMPK signaling pathway in HepG2 cells. Journal of Physiology and Biochemistry, 75(2), 125–133. https://doi.org/10.1007/s13105-019-00678-4
   PubMed Web of Science ®Google Scholar
• Sun, Y., Lv, Y., Li, Y., Li, J., Liu, J., Luo, L., Zhang, C., & Zhang, W. (2022). Maternal genetic effect on apoptosis of ovarian granulosa cells induced by cadmium. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 165, 113079 https://doi.org/10.1016/j.fct.2022.113079
   PubMed Web of Science ®Google Scholar
• Tsikas, D. (2017). Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: Analytical and biological challenges. Analytical Biochemistry, 524, 13–30. https://doi.org/10.1016/j.ab.2016.10.021
   PubMed Web of Science ®Google Scholar
• Uetani, M., Kobayashi, E., Suwazono, Y., Honda, R., Nishijo, M., Nakagawa, H., Kido, T., & Nogawa, K. (2006). Tissue cadmium (Cd) concentrations of people living in a Cd polluted area, Japan. Biometals: An International Journal on the Role of Metal Ions in Biology, Biochemistry, and Medicine, 19(5), 521–525. https://doi.org/10.1007/s10534-005-5619-0
   PubMed Web of Science ®Google Scholar
• Wang, J., Zhu, H., Lin, S., Wang, K., Wang, H., & Liu, Z. (2021). Protective effect of naringenin against cadmium-induced testicular toxicity in male SD rats. Journal of Inorganic Biochemistry, 214, 111310 https://doi.org/10.1016/j.jinorgbio.2020.111310
   PubMed Web of Science ®Google Scholar
• Wang, C., Ma, W., & Su, Y. (2013). NF-κB pathway contributes to cadmium-induced apoptosis of porcine granulosa cells. Biological Trace Element Research, 153(1–3), 403–410. https://doi.org/10.1007/s12011-013-9650-7
   PubMed Web of Science ®Google Scholar
• Wang, R., Sang, P., Guo, Y., Jin, P., Cheng, Y., Yu, H., Xie, Y., Yao, W., & Qian, H. (2023). Cadmium in food: Source, distribution and removal. Food Chemistry, 405(Pt A), 134666 https://doi.org/10.1016/j.foodchem.2022.134666
   PubMedGoogle Scholar
• Wang, R., Wang, L., Wang, L., Cui, Z., Cheng, F., Wang, W., & Yang, X. (2022). FGF2 is protective towards cisplatin-induced KGN cell toxicity by promoting FTO expression and autophagy. Frontiers in Endocrinology, 13, 890623 https://doi.org/10.3389/fendo.2022.890623
   PubMed Web of Science ®Google Scholar
• Wen, S., Xu, M., Zhang, W., Song, R., Zou, H., Gu, J., Liu, X., Bian, J., Liu, Z., & Yuan, Y. (2023). Cadmium induces mitochondrial dysfunction via SIRT1 suppression-mediated oxidative stress in neuronal cells. Environmental Toxicology, 38(4), 743–753. https://doi.org/10.1002/tox.23724
   PubMed Web of Science ®Google Scholar
• Xu, G., Liu, S., Huang, M., Jiang, X., & Yang, M. (2021). Cadmium induces apoptosis of human granulosa cell line KGN via mitochondrial dysfunction-mediated pathways. Ecotoxicology and Environmental Safety, 220, 112341 https://doi.org/10.1016/j.ecoenv.2021.112341
   PubMed Web of Science ®Google Scholar
• Yu, L. M., Dong, X., Xue, X. D., Zhang, J., Li, Z., Wu, H. J., Yang, Z. L., Yang, Y., & Wang, H. S. (2019). Naringenin improves mitochondrial function and reduces cardiac damage following ischemia-reperfusion injury: the role of the AMPK-SIRT3 signaling pathway. Food & Function, 10(5), 2752–2765. https://doi.org/10.1039/c9fo00001a
   PubMed Web of Science ®Google Scholar
• Zhang, X., Li, M., Wu, H., Fan, W., Zhang, J., Su, W., Wang, Y., & Li, P. (2022). Naringenin attenuates inflammation, apoptosis, and ferroptosis in silver nanoparticle-induced lung injury through a mechanism associated with Nrf2/HO-1 axis: In vitro and in vivo studies. Life Sciences, 311(Pt A), 121127. https://doi.org/10.1016/j.lfs.2022.121127
   PubMedGoogle Scholar
• Zhao, P., Lu, Y., & Wang, Z. (2023). Naringenin attenuates cerebral ischemia/reperfusion injury by inhibiting oxidative stress and inflammatory response via the activation of SIRT1/FOXO1 signaling pathway in vitro. Acta Cirurgica Brasileira, 38, e380823.
   PubMed Web of Science ®Google Scholar
• Zhu, M., Miao, S., Zhou, W., Elnesr, S. S., Dong, X., & Zou, X. (2021). MAPK, AKT/FoxO3a and mTOR pathways are involved in cadmium regulating the cell cycle, proliferation and apoptosis of chicken follicular granulosa cells. Ecotoxicology and Environmental Safety, 217, 112187. https://doi.org/10.1016/j.ecoenv.2021.112187
   PubMed Web of Science ®Google Scholar