Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic mice

Advanced glycation end products (AGEs) have adverse effects on the development of diabetic complications. Berberine (BBR), a natural alkaloid, has demonstrated its ability to promote the delayed healing of skin wounds. However, the impact of BBR on AGEs-induced ferroptosis in skin cells and the unde...

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Main Authors: Chunjie Jiang, Guojuan Lao, Jianmin Ran, Ping Zhu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Experimental Biology and Medicine
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Online Access:https://www.ebm-journal.org/articles/10.3389/ebm.2024.10280/full
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author Chunjie Jiang
Guojuan Lao
Jianmin Ran
Jianmin Ran
Ping Zhu
Ping Zhu
author_facet Chunjie Jiang
Guojuan Lao
Jianmin Ran
Jianmin Ran
Ping Zhu
Ping Zhu
author_sort Chunjie Jiang
collection DOAJ
description Advanced glycation end products (AGEs) have adverse effects on the development of diabetic complications. Berberine (BBR), a natural alkaloid, has demonstrated its ability to promote the delayed healing of skin wounds. However, the impact of BBR on AGEs-induced ferroptosis in skin cells and the underlying molecular mechanisms remains unexplored. This study investigated the involvement of ferroptosis in AGEs-induced keratinocyte death, and the impact of BBR on ferroptosis in a db/db mouse model with long-term hyperglycemia was elucidated. A remarkable reduction in cell viability was observed along with increased malondialdehyde (MDA) production in AGEs-induced HaCaT cells. Intracellular reactive oxygen species (ROS) and iron levels were elevated in cells exposed to AGEs. Meanwhile, the protein expression of glutathione peroxidase 4 (GPX4) and ferritin light chain (FTL) was significantly decreased in AGEs-treated cells. However, pretreatment with BBR markedly protected cell viability and inhibited MDA levels, attenuating the intracellular ROS and iron levels and increased expression of GPX4 and FTL in vitro. Significantly diminished antiferroptotic effects of BBR on AGEs-treated keratinocytes were observed upon the knockdown of the nuclear factor E2–related factor 2 (NRF2) gene. In vivo, GPX4, FTL, and FTH expression in the epidermis of diabetic mice was significantly reduced, accompanied by enhanced lipid peroxidation. Treatment with BBR effectively rescued lipid peroxidation accumulation and upregulated GPX4, FTL, FTH, and NRF2 levels in diabetic skin. Collectively, the findings indicate that ferroptosis may play a significant role in AGEs-induced keratinocyte death. BBR protects diabetic keratinocytes against ferroptosis, partly by activating NRF2.
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spelling doaj-art-6f0f4d12101445948c495c7fdb9dfd2e2024-12-13T14:55:22ZengFrontiers Media S.A.Experimental Biology and Medicine1535-36992024-12-0124910.3389/ebm.2024.1028010280Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic miceChunjie Jiang0Guojuan Lao1Jianmin Ran2Jianmin Ran3Ping Zhu4Ping Zhu5Institute of Disease-Oriented Nutritional Research, Guangzhou Red Cross Hospital, Jinan University, Guangzhou, ChinaDepartment of Endocrinology and Metabolism, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou, ChinaInstitute of Disease-Oriented Nutritional Research, Guangzhou Red Cross Hospital, Jinan University, Guangzhou, ChinaDepartment of Endocrinology and Metabolism, Guangzhou Red Cross Hospital, Jinan University, Guangzhou, ChinaInstitute of Disease-Oriented Nutritional Research, Guangzhou Red Cross Hospital, Jinan University, Guangzhou, ChinaDepartment of Endocrinology and Metabolism, Guangzhou Red Cross Hospital, Jinan University, Guangzhou, ChinaAdvanced glycation end products (AGEs) have adverse effects on the development of diabetic complications. Berberine (BBR), a natural alkaloid, has demonstrated its ability to promote the delayed healing of skin wounds. However, the impact of BBR on AGEs-induced ferroptosis in skin cells and the underlying molecular mechanisms remains unexplored. This study investigated the involvement of ferroptosis in AGEs-induced keratinocyte death, and the impact of BBR on ferroptosis in a db/db mouse model with long-term hyperglycemia was elucidated. A remarkable reduction in cell viability was observed along with increased malondialdehyde (MDA) production in AGEs-induced HaCaT cells. Intracellular reactive oxygen species (ROS) and iron levels were elevated in cells exposed to AGEs. Meanwhile, the protein expression of glutathione peroxidase 4 (GPX4) and ferritin light chain (FTL) was significantly decreased in AGEs-treated cells. However, pretreatment with BBR markedly protected cell viability and inhibited MDA levels, attenuating the intracellular ROS and iron levels and increased expression of GPX4 and FTL in vitro. Significantly diminished antiferroptotic effects of BBR on AGEs-treated keratinocytes were observed upon the knockdown of the nuclear factor E2–related factor 2 (NRF2) gene. In vivo, GPX4, FTL, and FTH expression in the epidermis of diabetic mice was significantly reduced, accompanied by enhanced lipid peroxidation. Treatment with BBR effectively rescued lipid peroxidation accumulation and upregulated GPX4, FTL, FTH, and NRF2 levels in diabetic skin. Collectively, the findings indicate that ferroptosis may play a significant role in AGEs-induced keratinocyte death. BBR protects diabetic keratinocytes against ferroptosis, partly by activating NRF2.https://www.ebm-journal.org/articles/10.3389/ebm.2024.10280/fulladvanced glycation end productionsferroptosisberberinekeratinocytesNRF2
spellingShingle Chunjie Jiang
Guojuan Lao
Jianmin Ran
Jianmin Ran
Ping Zhu
Ping Zhu
Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic mice
Experimental Biology and Medicine
advanced glycation end productions
ferroptosis
berberine
keratinocytes
NRF2
title Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic mice
title_full Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic mice
title_fullStr Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic mice
title_full_unstemmed Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic mice
title_short Berberine alleviates AGEs-induced ferroptosis by activating NRF2 in the skin of diabetic mice
title_sort berberine alleviates ages induced ferroptosis by activating nrf2 in the skin of diabetic mice
topic advanced glycation end productions
ferroptosis
berberine
keratinocytes
NRF2
url https://www.ebm-journal.org/articles/10.3389/ebm.2024.10280/full
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