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Peroxisome Proliferator-Activated Receptor-γ Activators Monascin and Rosiglitazone Attenuate Carboxymethyllysine-Induced Fibrosis in Hepatic Stellate Cells through Regulating the Oxidative Stress Pathway but Independent of the Receptor for Advanced Glycation End Products Signaling

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    Peroxisome Proliferator-Activated Receptor-γ Activators Monascin and Rosiglitazone Attenuate Carboxymethyllysine-Induced Fibrosis in Hepatic Stellate Cells through Regulating the Oxidative Stress Pathway but Independent of the Receptor for Advanced Glycation End Products Signaling
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    ‡ Department of Biochemical Science and Technology, College of Life Science, National Taiwan University, Number 1, Section 4, Roosevelt Road, Taipei 10617, Taiwan
    § SunWay Biotechnology Company Limited, Number 139, Xing’ai Road, Neihu District, Taipei 11494, Taiwan
    *Telephone: +886-2-33664519, ext. 10. Fax: +886-2-33663838. E-mail: [email protected]
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    Journal of Agricultural and Food Chemistry

    Cite this: J. Agric. Food Chem. 2013, 61, 28, 6873–6879
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    https://doi.org/10.1021/jf402082g
    Published June 24, 2013
    Copyright © 2013 American Chemical Society
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    Abstract

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    Advanced glycation end products (AGEs) signaling through its receptors (RAGE) results in an increase in reactive oxygen species (ROS) and is thought to contribute to hepatic fibrosis via hyperglycemia. Carboxymethyllysine (CML) is a key AGE, with highly reactive dicarbonyl metabolites. We investigated the inhibitory effect of Monascus-fermented metabolite monascin and rosiglitazone on CML-induced RAGE signaling in hepatic stellate cells (HSCs) and its resulting antihepatic fibrosis activity. We found that monascin and rosiglitazone upregulated peroxisome proliferator-activated receptor-γ (PPAR-γ) to attenuate α-smooth muscle actin (SMA) and ROS generation in CML-treated HSCs in a RAGE activation-independent pathway. Therefore, monascin may delay or inhibit the progression of liver fibrosis through the activation of PPAR-γ and might prove to be a major antifibrotic mechanism to prevent liver disease.

    Copyright © 2013 American Chemical Society

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    Chemical structures of (A) monascin and (B) rosiglitazone (Supplemental Figure 1). This material is available free of charge via the Internet at http://pubs.acs.org.

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    This article is cited by 24 publications.

    1. Chih-Fu Cheng and Tzu-Ming Pan . Ankaflavin and Monascin Induce Apoptosis in Activated Hepatic Stellate Cells through Suppression of the Akt/NF-κB/p38 Signaling Pathway. Journal of Agricultural and Food Chemistry 2016, 64 (49) , 9326-9334. https://doi.org/10.1021/acs.jafc.6b03700
    2. Qian Wu, Shuyi Li, Xiaopeng Li, Yong Sui, Yan Yang, Lihong Dong, Bijun Xie, and Zhida Sun . Inhibition of Advanced Glycation Endproduct Formation by Lotus Seedpod Oligomeric Procyanidins through RAGE–MAPK Signaling and NF-κB Activation in High-Fat-Diet Rats. Journal of Agricultural and Food Chemistry 2015, 63 (31) , 6989-6998. https://doi.org/10.1021/acs.jafc.5b01082
    3. Yu-Ying Chang, Wei-Hsuan Hsu, and Tzu-Ming Pan . Monascus Secondary Metabolites Monascin and Ankaflavin Inhibit Activation of RBL-2H3 Cells. Journal of Agricultural and Food Chemistry 2015, 63 (1) , 192-199. https://doi.org/10.1021/jf504013n
    4. Wei-Hsuan Hsu, Bao-Hong Lee, and Tzu-Ming Pan . Monascin Attenuates Oxidative Stress-Mediated Lung Inflammation via Peroxisome Proliferator-Activated Receptor-Gamma (PPAR-γ) and Nuclear Factor-Erythroid 2 Related Factor 2 (Nrf-2) Modulation. Journal of Agricultural and Food Chemistry 2014, 62 (23) , 5337-5344. https://doi.org/10.1021/jf501373a
    5. Liangtao Zhao, Haolan Tang, Zhangjun Cheng. Pharmacotherapy of Liver Fibrosis and Hepatitis: Recent Advances. Pharmaceuticals 2024, 17 (12) , 1724. https://doi.org/10.3390/ph17121724
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    9. Fangqiao Lv, Nan Li, Ming Kong, Jun Wu, Zhiwen Fan, Dengshun Miao, Yong Xu, Qing Ye, Yutong Wang. CDKN2a/p16 Antagonizes Hepatic Stellate Cell Activation and Liver Fibrosis by Modulating ROS Levels. Frontiers in Cell and Developmental Biology 2020, 8 https://doi.org/10.3389/fcell.2020.00176
    10. Liwei Wu, Chuanyong Guo, Jianye Wu. Therapeutic potential of PPARγ natural agonists in liver diseases. Journal of Cellular and Molecular Medicine 2020, 24 (5) , 2736-2748. https://doi.org/10.1111/jcmm.15028
    11. Ezhilarasan Devaraj, S. Rajeshkumar. Nanomedicine for Hepatic Fibrosis. 2020, 45-64. https://doi.org/10.1007/978-981-15-0391-7_2
    12. Shao-ce Zhi, Shi-zuan Chen, Yan-yan Li, Jun-jian Li, Yi-hu Zheng, Fu-xiang Yu. RETRACTED ARTICLE: Rosiglitazone Inhibits Activation of Hepatic Stellate Cells via Up-Regulating Micro-RNA-124-3p to Alleviate Hepatic Fibrosis. Digestive Diseases and Sciences 2019, 64 (6) , 1560-1570. https://doi.org/10.1007/s10620-019-5462-8
    13. Chih‐Fu Cheng, Tzu‐Ming Pan. Monascus ‐fermented red mold dioscorea protects mice against alcohol‐induced liver injury, whereas its metabolites ankaflavin and monascin regulate ethanol‐induced peroxisome proliferator‐activated receptor‐ γ and sterol regulatory element‐binding transcription factor‐1 expression in HepG2 cells. Journal of the Science of Food and Agriculture 2018, 98 (5) , 1889-1898. https://doi.org/10.1002/jsfa.8670
    14. Luca Cannizzaro, Giuseppe Rossoni, Federica Savi, Alessandra Altomare, Cristina Marinello, Thammakorn Saethang, Marina Carini, D. Michael Payne, Trairak Pisitkun, Giancarlo Aldini, Asada Leelahavanichkul. Regulatory landscape of AGE-RAGE-oxidative stress axis and its modulation by PPARγ activation in high fructose diet-induced metabolic syndrome. Nutrition & Metabolism 2017, 14 (1) https://doi.org/10.1186/s12986-016-0149-z
    15. Marcus Hollenbach. The Role of Glyoxalase-I (Glo-I), Advanced Glycation Endproducts (AGEs), and Their Receptor (RAGE) in Chronic Liver Disease and Hepatocellular Carcinoma (HCC). International Journal of Molecular Sciences 2017, 18 (11) , 2466. https://doi.org/10.3390/ijms18112466
    16. Marcus Hollenbach. Impact of Glyoxalase-I (Glo-I) and Advanced Glycation End Products (AGEs) in Chronic Liver Disease. 2017https://doi.org/10.5772/intechopen.68417
    17. Karen R. Jonscher, Alba Alfonso-Garcia, Jeffrey L. Suhalim, David J. Orlicky, Eric O. Potma, Virginia L. Ferguson, Mary L. Bouxsein, Ted A. Bateman, Louis S. Stodieck, Moshe Levi, Jacob E. Friedman, Daila S. Gridley, Michael J. Pecaut, . Spaceflight Activates Lipotoxic Pathways in Mouse Liver. PLOS ONE 2016, 11 (4) , e0152877. https://doi.org/10.1371/journal.pone.0152877
    18. Cheng-Jeng Tai, Chen-Yen Choong, Yeu-Ching Shi, Yu-Chun Lin, Chia-Woei Wang, Bao-Hong Lee, Chen-Jei Tai. Solanum nigrum Protects against Hepatic Fibrosis via Suppression of Hyperglycemia in High-Fat/Ethanol Diet-Induced Rats. Molecules 2016, 21 (3) , 269. https://doi.org/10.3390/molecules21030269
    19. Chen-Jei Tai, Chen-Yen Choong, Yu-Chun Lin, Yeu-Ching Shi, Cheng-Jeng Tai. The anti-hepatic fibrosis activity of ergosterol depended on upregulation of PPARgamma in HSC-T6 cells. Food & Function 2016, 7 (4) , 1915-1923. https://doi.org/10.1039/C6FO00117C
    20. XIAO-WEI WANG, WEI-DONG LI, JIN-RONG XIA, ZHAN LI, XIAO-GANG CAI. Small interfering RNA targeting receptor for advanced glycation end products suppresses the generation of proinflammatory cytokines. Experimental and Therapeutic Medicine 2015, 10 (2) , 584-590. https://doi.org/10.3892/etm.2015.2569
    21. Virender Kumar, Ram I. Mahato. Delivery and Targeting of miRNAs for Treating Liver Fibrosis. Pharmaceutical Research 2015, 32 (2) , 341-361. https://doi.org/10.1007/s11095-014-1497-x
    22. LI LIU, HAILUN GU, YUE ZHAO, LI AN, JUN YANG. Glypican 4 may be involved in the adipose tissue redistribution in high-fat feeding C57BL/6J mice with peroxisome proliferators-activated receptor γ agonist rosiglitazone treatment. Experimental and Therapeutic Medicine 2014, 8 (6) , 1813-1818. https://doi.org/10.3892/etm.2014.1998
    23. A. J. Czaja. Review article: the prevention and reversal of hepatic fibrosis in autoimmune hepatitis. Alimentary Pharmacology & Therapeutics 2014, 39 (4) , 385-406. https://doi.org/10.1111/apt.12592
    24. Wei-Hsuan Hsu, Tzu-Ming Pan. A novel PPARgamma agonist monascin's potential application in diabetes prevention. Food Funct. 2014, 5 (7) , 1334-1340. https://doi.org/10.1039/C3FO60575B
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    Journal of Agricultural and Food Chemistry

    Cite this: J. Agric. Food Chem. 2013, 61, 28, 6873–6879
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jf402082g
    Published June 24, 2013
    Copyright © 2013 American Chemical Society
    Request reuse permissions

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