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Synergistic Activation of the Nrf2-Signaling Pathway by Glyceollins under Oxidative Stress Induced by Glutathione Depletion

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    Synergistic Activation of the Nrf2-Signaling Pathway by Glyceollins under Oxidative Stress Induced by Glutathione Depletion
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    † School of Applied Biosciences and Food Science and Biotechnology, Kyungpook National University, Daegu 702-701, Republic of Korea
    ‡ Research Institute for Biological Functions, Chubu University, Kasugai-shi, Aichi 487-8501, Japan
    # Department of Food Science and Nutrition, Hallym University, Chuncheon 200-702, Republic of Korea
    § Department of Pharmaceutics, Earnest Mario School of Pharmacy, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854, United States
    ⊥ Department of Bioscience and Biotechnology, Konkuk University, Seoul 143-701, Republic of Korea
    *Mailing address: School of Food Science and Biotecnology, Kyungpook National University, Daegu 702-701, Republic of Korea. Phone: 82-53-950-5752. Fax: 82-53-950-6750. E-mail: [email protected]
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    Journal of Agricultural and Food Chemistry

    Cite this: J. Agric. Food Chem. 2013, 61, 17, 4072–4078
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jf303948c
    Published April 10, 2013
    Copyright © 2013 American Chemical Society
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    Abstract

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    Oxidative stress state such as depletion of the intracellular glutathione (GSH) is associated with the development of cancer. Some dietary phytochemicals have been shown to possess a cancer preventive effect, although the understanding of the involved mechanisms is still limited. Recent study has shown that glyceollins, phytoalexins derived from soybean by biotic elicitor, might have a cancer preventive effect through induction of detoxifying/antioxidant enzymes. The objective of this study was to investigate the effects of glyceollins on the Nrf2 signaling pathway under excessive oxidative stress induced by GSH depletion. In mouse hepatoma cells (Hepa1c1c7) subjected to the buthionine sulfoximine (BSO), an inhibitor of γ-glutamylcysteine synthetase (γGCS), the intracellular GSH content was significantly lowered. On the other hand, incubation with glyceollins in the presence of BSO increased the level of GSH, expression of γGCS, and nuclear translocation of NF-E2-related factor-2 (Nrf2), compared to the cells treated with BSO only. Nrf2-antioxidant responsive element (ARE)-reporter activity assay in HepG2-C8 showed that BSO increased the ARE-reporter activity in a dose-dependent manner, compared to vehicle-treated cells, whereas cotreatment with glyceollins caused further increase in reporter luciferase activity relative to BSO alone. Taken together, glyceollins synergistically activated the Nrf2 signaling pathway and subsequently the expression of phase 2/antioxidant enzymes in the presence of BSO, suggesting that BSO-induced oxidative stress and that glyceollins regulate the expression of phase 2/antioxidant enzymes through different mechanisms from each other.

    Copyright © 2013 American Chemical Society

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    This article is cited by 8 publications.

    1. Zhongxing Chu, Lingfeng Zhu, Yaping Zhou, Feiyan Yang, Zuomin Hu, Yi Luo, Wen Li, Feijun Luo. Targeting Nrf2 by bioactive peptides alleviate inflammation: expanding the role of gut microbiota and metabolites. Critical Reviews in Food Science and Nutrition 2024, , 1-20. https://doi.org/10.1080/10408398.2024.2367570
    2. Zhiyong Yue, Shanhong He, Jinpei Wang, Qi Jiang, Hanping Wang, Jia Wu, Chenxi Li, Zixian Wang, Xuan He, Nannan Jia. Glyceollins from soybean: Their pharmacological effects and biosynthetic pathways. Heliyon 2023, 9 (11) , e21874. https://doi.org/10.1016/j.heliyon.2023.e21874
    3. Xu‐Dong Zhou, Jing‐Lin Wang, Da‐Dong Guo, Wen‐Wen Jiang, Ze‐Kun Li, Li Wang, Yong Zou, Ming‐Jun Bi, Qin Li. Neuroprotective effect of targeted regulatory Nrf2 gene on rats with acute brain injury induced by carbon monoxide poisoning. Environmental Toxicology 2021, 36 (9) , 1742-1757. https://doi.org/10.1002/tox.23295
    4. Thu Ha Pham, Sylvain Lecomte, Theo Efstathiou, Francois Ferriere, Farzad Pakdel. An Update on the Effects of Glyceollins on Human Health: Possible Anticancer Effects and Underlying Mechanisms. Nutrients 2019, 11 (1) , 79. https://doi.org/10.3390/nu11010079
    5. Jie Ren, Ling Yuan, Yue Wang, Guangtong Chen, Kun Hu. Benzyl sulforaphane is superior to sulforaphane in inhibiting the Akt/MAPK and activating the Nrf2/ARE signalling pathways in HepG2 cells. Journal of Pharmacy and Pharmacology 2018, 70 (12) , 1643-1653. https://doi.org/10.1111/jphp.13015
    6. Marcus Cebula, Edward E. Schmidt, Elias S.J. Arnér. TrxR1 as a Potent Regulator of the Nrf2-Keap1 Response System. Antioxidants & Redox Signaling 2015, 23 (10) , 823-853. https://doi.org/10.1089/ars.2015.6378
    7. M. Pilar Valdecantos, Pedro Luis Prieto-Hontoria, Virginia Pardo, Teresa Módol, Beatriz Santamaría, Minéia Weber, Laura Herrero, Dolors Serra, Jordi Muntané, Antonio Cuadrado, María Jesús Moreno-Aliaga, J. Alfredo Martínez, Ángela M. Valverde. Essential role of Nrf2 in the protective effect of lipoic acid against lipoapoptosis in hepatocytes. Free Radical Biology and Medicine 2015, 84 , 263-278. https://doi.org/10.1016/j.freeradbiomed.2015.03.019
    8. Hyo Jung Kim, Chae Lim Jung, Yeon Shin Jeong, Jong-Sang Kim. Soybean-derived glyceollins induce apoptosis through ROS generation. Food & Function 2014, 5 (4) , 688. https://doi.org/10.1039/c3fo60379b
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    Journal of Agricultural and Food Chemistry

    Cite this: J. Agric. Food Chem. 2013, 61, 17, 4072–4078
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jf303948c
    Published April 10, 2013
    Copyright © 2013 American Chemical Society
    Request reuse permissions

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