Omega-3 polyunsaturated fatty acids protect against cisplatin-induced nephrotoxicity by activating the Nrf2 signaling pathway
Nephrotoxicity is a prevalent side effect observed in patients undergoing chemotherapy. The pathogenesis of chemotherapy-induced nephrotoxicity involves various factors such as oxidative stress, DNA damage, inflammation, and apoptosis. Omega-3 polyunsaturated fatty acids (ω-3 PUFAs), particularly ei...
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| Veröffentlicht in: | International journal of biological macromolecules 2024-12, Vol.282 (Pt 6), p.137457, Article 137457 |
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| container_title | International journal of biological macromolecules |
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| creator | Zhang, Zongmeng Liu, Yueying Feng, Wenbin Mao, Ping Yang, Jianqin Zhao, Zhenggang Zhou, Sujin Zhao, Allan Zijian Li, Fanghong Mu, Yunping |
| description | Nephrotoxicity is a prevalent side effect observed in patients undergoing chemotherapy. The pathogenesis of chemotherapy-induced nephrotoxicity involves various factors such as oxidative stress, DNA damage, inflammation, and apoptosis. Omega-3 polyunsaturated fatty acids (ω-3 PUFAs), particularly eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), possess anti-inflammatory and antioxidant properties. This study investigated the effects of EPA and DHA, either alone or in combination, on cisplatin-induced nephrotoxicity in mice, as well as their underlying mechanisms of action. The combined administration of EPA and DHA demonstrated superior efficacy in mitigating cisplatin-induced nephrotoxicity compared to administration alone, including the reduction of oxidative damage, inflammation, and apoptosis. Moreover, the combination of EPA and DHA suppressed inflammation and prevented the development of chronic kidney fibrosis during prolonged observations following repeated cisplatin administration. Mechanistically, ω-3 PUFAs enhance the expression of antioxidant genes by activating the p62-Keap1-Nrf2 signaling pathway. Furthermore, Nrf2 activation can inhibit the cisplatin-induced p53 apoptosis signal by upregulating the expression of MDM2 in renal tubular epithelial cells. Consequently, ω-3 PUFAs exert a protective effect against cisplatin-induced renal injury through activating the Nrf2 signaling pathway, suggesting that ω-3 PUFAs intake holds promise as a therapeutic strategy for combating cisplatin-induced nephrotoxicity.
•Omega-3 PUFAs protect against cisplatin-induced nephrotoxicity.•Omega-3 PUFAs enhance the expression of antioxidant genes by activating the p62-Keap1-Nrf2 signaling pathway.•Omega-3 PUFAs inhibit cisplatin-induced apoptosis through the Nrf2-MDM2-p53 signaling pathway.•Omega-3 PUFAs protect against cisplatin-induced chronic kidney disease. |
| doi_str_mv | 10.1016/j.ijbiomac.2024.137457 |
| format | Article |
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•Omega-3 PUFAs protect against cisplatin-induced nephrotoxicity.•Omega-3 PUFAs enhance the expression of antioxidant genes by activating the p62-Keap1-Nrf2 signaling pathway.•Omega-3 PUFAs inhibit cisplatin-induced apoptosis through the Nrf2-MDM2-p53 signaling pathway.•Omega-3 PUFAs protect against cisplatin-induced chronic kidney disease.</description><identifier>ISSN: 0141-8130</identifier><identifier>ISSN: 1879-0003</identifier><identifier>EISSN: 1879-0003</identifier><identifier>DOI: 10.1016/j.ijbiomac.2024.137457</identifier><identifier>PMID: 39528186</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>adverse effects ; Animals ; antioxidants ; Antioxidants - pharmacology ; apoptosis ; Apoptosis - drug effects ; Cisplatin ; Cisplatin - adverse effects ; DNA damage ; docosahexaenoic acid ; Docosahexaenoic Acids - pharmacology ; drug therapy ; eicosapentaenoic acid ; Eicosapentaenoic Acid - pharmacology ; epithelium ; Fatty Acids, Omega-3 - pharmacology ; fibrosis ; inflammation ; Kelch-Like ECH-Associated Protein 1 - metabolism ; Kidney - drug effects ; Kidney - metabolism ; Kidney - pathology ; Kidney Diseases - chemically induced ; Kidney Diseases - drug therapy ; Kidney Diseases - metabolism ; Kidney Diseases - pathology ; Kidney Diseases - prevention & control ; kidneys ; Male ; Mice ; Nephrotoxicity ; NF-E2-Related Factor 2 - metabolism ; Nrf2 ; Omega-3 polyunsaturated fatty acids ; oxidative stress ; Oxidative Stress - drug effects ; pathogenesis ; Protective Agents - pharmacology ; protective effect ; Proto-Oncogene Proteins c-mdm2 - metabolism ; Signal Transduction - drug effects ; Tumor Suppressor Protein p53 - genetics ; Tumor Suppressor Protein p53 - metabolism</subject><ispartof>International journal of biological macromolecules, 2024-12, Vol.282 (Pt 6), p.137457, Article 137457</ispartof><rights>2024</rights><rights>Copyright © 2024. Published by Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c278t-722f766a7fb662268630efe21b2bafeb20e55ae56bad732297d2adfa52accd0b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0141813024082667$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39528186$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Zongmeng</creatorcontrib><creatorcontrib>Liu, Yueying</creatorcontrib><creatorcontrib>Feng, Wenbin</creatorcontrib><creatorcontrib>Mao, Ping</creatorcontrib><creatorcontrib>Yang, Jianqin</creatorcontrib><creatorcontrib>Zhao, Zhenggang</creatorcontrib><creatorcontrib>Zhou, Sujin</creatorcontrib><creatorcontrib>Zhao, Allan Zijian</creatorcontrib><creatorcontrib>Li, Fanghong</creatorcontrib><creatorcontrib>Mu, Yunping</creatorcontrib><title>Omega-3 polyunsaturated fatty acids protect against cisplatin-induced nephrotoxicity by activating the Nrf2 signaling pathway</title><title>International journal of biological macromolecules</title><addtitle>Int J Biol Macromol</addtitle><description>Nephrotoxicity is a prevalent side effect observed in patients undergoing chemotherapy. The pathogenesis of chemotherapy-induced nephrotoxicity involves various factors such as oxidative stress, DNA damage, inflammation, and apoptosis. Omega-3 polyunsaturated fatty acids (ω-3 PUFAs), particularly eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), possess anti-inflammatory and antioxidant properties. This study investigated the effects of EPA and DHA, either alone or in combination, on cisplatin-induced nephrotoxicity in mice, as well as their underlying mechanisms of action. The combined administration of EPA and DHA demonstrated superior efficacy in mitigating cisplatin-induced nephrotoxicity compared to administration alone, including the reduction of oxidative damage, inflammation, and apoptosis. Moreover, the combination of EPA and DHA suppressed inflammation and prevented the development of chronic kidney fibrosis during prolonged observations following repeated cisplatin administration. Mechanistically, ω-3 PUFAs enhance the expression of antioxidant genes by activating the p62-Keap1-Nrf2 signaling pathway. Furthermore, Nrf2 activation can inhibit the cisplatin-induced p53 apoptosis signal by upregulating the expression of MDM2 in renal tubular epithelial cells. Consequently, ω-3 PUFAs exert a protective effect against cisplatin-induced renal injury through activating the Nrf2 signaling pathway, suggesting that ω-3 PUFAs intake holds promise as a therapeutic strategy for combating cisplatin-induced nephrotoxicity.
•Omega-3 PUFAs protect against cisplatin-induced nephrotoxicity.•Omega-3 PUFAs enhance the expression of antioxidant genes by activating the p62-Keap1-Nrf2 signaling pathway.•Omega-3 PUFAs inhibit cisplatin-induced apoptosis through the Nrf2-MDM2-p53 signaling pathway.•Omega-3 PUFAs protect against cisplatin-induced chronic kidney disease.</description><subject>adverse effects</subject><subject>Animals</subject><subject>antioxidants</subject><subject>Antioxidants - pharmacology</subject><subject>apoptosis</subject><subject>Apoptosis - drug effects</subject><subject>Cisplatin</subject><subject>Cisplatin - adverse effects</subject><subject>DNA damage</subject><subject>docosahexaenoic acid</subject><subject>Docosahexaenoic Acids - pharmacology</subject><subject>drug therapy</subject><subject>eicosapentaenoic acid</subject><subject>Eicosapentaenoic Acid - pharmacology</subject><subject>epithelium</subject><subject>Fatty Acids, Omega-3 - pharmacology</subject><subject>fibrosis</subject><subject>inflammation</subject><subject>Kelch-Like ECH-Associated Protein 1 - metabolism</subject><subject>Kidney - drug effects</subject><subject>Kidney - metabolism</subject><subject>Kidney - pathology</subject><subject>Kidney Diseases - chemically induced</subject><subject>Kidney Diseases - drug therapy</subject><subject>Kidney Diseases - metabolism</subject><subject>Kidney Diseases - pathology</subject><subject>Kidney Diseases - prevention & control</subject><subject>kidneys</subject><subject>Male</subject><subject>Mice</subject><subject>Nephrotoxicity</subject><subject>NF-E2-Related Factor 2 - metabolism</subject><subject>Nrf2</subject><subject>Omega-3 polyunsaturated fatty acids</subject><subject>oxidative stress</subject><subject>Oxidative Stress - drug effects</subject><subject>pathogenesis</subject><subject>Protective Agents - pharmacology</subject><subject>protective effect</subject><subject>Proto-Oncogene Proteins c-mdm2 - metabolism</subject><subject>Signal Transduction - drug effects</subject><subject>Tumor Suppressor Protein p53 - genetics</subject><subject>Tumor Suppressor Protein p53 - metabolism</subject><issn>0141-8130</issn><issn>1879-0003</issn><issn>1879-0003</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkctuFDEQRS0EIkPgFyIv2fTEj_ZjdqCIR6SIbGBtld3VMx71i7Y7ZBb8O25NwhZWlkrnVsn3EHLF2ZYzrq-P23j0cewhbAUT9ZZLUyvzgmy4NbuKMSZfkg3jNa8sl-yCvEnpWKZacfuaXMidEpZbvSG_73vcQyXpNHanZUiQlxkyNrSFnE8UQmwSneYxY8gU9hCHlGmIaeogx6GKQ7OEQg84HQo0PsYQS8yvyRwfVmZP8wHpt7kVNMX9AN06miAffsHpLXnVQpfw3dN7SX58_vT95mt1d__l9ubjXRWEsbkyQrRGazCt11oIbbVk2KLgXnho0QuGSgEq7aExUoidaQQ0LSgBITTMy0vy_ry3_OTngim7PqaAXQcDjktykqtalEps_R-osEYZq3RB9RkN85jSjK2b5tjDfHKcudWSO7pnS2615M6WSvDq6cbie2z-xp61FODDGcBSykPE2aUQcShNx7mIcM0Y_3XjDyJTqcI</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Zhang, Zongmeng</creator><creator>Liu, Yueying</creator><creator>Feng, Wenbin</creator><creator>Mao, Ping</creator><creator>Yang, Jianqin</creator><creator>Zhao, Zhenggang</creator><creator>Zhou, Sujin</creator><creator>Zhao, Allan Zijian</creator><creator>Li, Fanghong</creator><creator>Mu, Yunping</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>202412</creationdate><title>Omega-3 polyunsaturated fatty acids protect against cisplatin-induced nephrotoxicity by activating the Nrf2 signaling pathway</title><author>Zhang, Zongmeng ; Liu, Yueying ; Feng, Wenbin ; Mao, Ping ; Yang, Jianqin ; Zhao, Zhenggang ; Zhou, Sujin ; Zhao, Allan Zijian ; Li, Fanghong ; Mu, Yunping</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c278t-722f766a7fb662268630efe21b2bafeb20e55ae56bad732297d2adfa52accd0b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>adverse effects</topic><topic>Animals</topic><topic>antioxidants</topic><topic>Antioxidants - pharmacology</topic><topic>apoptosis</topic><topic>Apoptosis - drug effects</topic><topic>Cisplatin</topic><topic>Cisplatin - adverse effects</topic><topic>DNA damage</topic><topic>docosahexaenoic acid</topic><topic>Docosahexaenoic Acids - pharmacology</topic><topic>drug therapy</topic><topic>eicosapentaenoic acid</topic><topic>Eicosapentaenoic Acid - pharmacology</topic><topic>epithelium</topic><topic>Fatty Acids, Omega-3 - pharmacology</topic><topic>fibrosis</topic><topic>inflammation</topic><topic>Kelch-Like ECH-Associated Protein 1 - metabolism</topic><topic>Kidney - drug effects</topic><topic>Kidney - metabolism</topic><topic>Kidney - pathology</topic><topic>Kidney Diseases - chemically induced</topic><topic>Kidney Diseases - drug therapy</topic><topic>Kidney Diseases - metabolism</topic><topic>Kidney Diseases - pathology</topic><topic>Kidney Diseases - prevention & control</topic><topic>kidneys</topic><topic>Male</topic><topic>Mice</topic><topic>Nephrotoxicity</topic><topic>NF-E2-Related Factor 2 - metabolism</topic><topic>Nrf2</topic><topic>Omega-3 polyunsaturated fatty acids</topic><topic>oxidative stress</topic><topic>Oxidative Stress - drug effects</topic><topic>pathogenesis</topic><topic>Protective Agents - pharmacology</topic><topic>protective effect</topic><topic>Proto-Oncogene Proteins c-mdm2 - metabolism</topic><topic>Signal Transduction - drug effects</topic><topic>Tumor Suppressor Protein p53 - genetics</topic><topic>Tumor Suppressor Protein p53 - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Zongmeng</creatorcontrib><creatorcontrib>Liu, Yueying</creatorcontrib><creatorcontrib>Feng, Wenbin</creatorcontrib><creatorcontrib>Mao, Ping</creatorcontrib><creatorcontrib>Yang, Jianqin</creatorcontrib><creatorcontrib>Zhao, Zhenggang</creatorcontrib><creatorcontrib>Zhou, Sujin</creatorcontrib><creatorcontrib>Zhao, Allan Zijian</creatorcontrib><creatorcontrib>Li, Fanghong</creatorcontrib><creatorcontrib>Mu, Yunping</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>International journal of biological macromolecules</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Zongmeng</au><au>Liu, Yueying</au><au>Feng, Wenbin</au><au>Mao, Ping</au><au>Yang, Jianqin</au><au>Zhao, Zhenggang</au><au>Zhou, Sujin</au><au>Zhao, Allan Zijian</au><au>Li, Fanghong</au><au>Mu, Yunping</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Omega-3 polyunsaturated fatty acids protect against cisplatin-induced nephrotoxicity by activating the Nrf2 signaling pathway</atitle><jtitle>International journal of biological macromolecules</jtitle><addtitle>Int J Biol Macromol</addtitle><date>2024-12</date><risdate>2024</risdate><volume>282</volume><issue>Pt 6</issue><spage>137457</spage><pages>137457-</pages><artnum>137457</artnum><issn>0141-8130</issn><issn>1879-0003</issn><eissn>1879-0003</eissn><abstract>Nephrotoxicity is a prevalent side effect observed in patients undergoing chemotherapy. The pathogenesis of chemotherapy-induced nephrotoxicity involves various factors such as oxidative stress, DNA damage, inflammation, and apoptosis. Omega-3 polyunsaturated fatty acids (ω-3 PUFAs), particularly eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), possess anti-inflammatory and antioxidant properties. This study investigated the effects of EPA and DHA, either alone or in combination, on cisplatin-induced nephrotoxicity in mice, as well as their underlying mechanisms of action. The combined administration of EPA and DHA demonstrated superior efficacy in mitigating cisplatin-induced nephrotoxicity compared to administration alone, including the reduction of oxidative damage, inflammation, and apoptosis. Moreover, the combination of EPA and DHA suppressed inflammation and prevented the development of chronic kidney fibrosis during prolonged observations following repeated cisplatin administration. Mechanistically, ω-3 PUFAs enhance the expression of antioxidant genes by activating the p62-Keap1-Nrf2 signaling pathway. Furthermore, Nrf2 activation can inhibit the cisplatin-induced p53 apoptosis signal by upregulating the expression of MDM2 in renal tubular epithelial cells. Consequently, ω-3 PUFAs exert a protective effect against cisplatin-induced renal injury through activating the Nrf2 signaling pathway, suggesting that ω-3 PUFAs intake holds promise as a therapeutic strategy for combating cisplatin-induced nephrotoxicity.
•Omega-3 PUFAs protect against cisplatin-induced nephrotoxicity.•Omega-3 PUFAs enhance the expression of antioxidant genes by activating the p62-Keap1-Nrf2 signaling pathway.•Omega-3 PUFAs inhibit cisplatin-induced apoptosis through the Nrf2-MDM2-p53 signaling pathway.•Omega-3 PUFAs protect against cisplatin-induced chronic kidney disease.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>39528186</pmid><doi>10.1016/j.ijbiomac.2024.137457</doi></addata></record> |
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| subjects | adverse effects Animals antioxidants Antioxidants - pharmacology apoptosis Apoptosis - drug effects Cisplatin Cisplatin - adverse effects DNA damage docosahexaenoic acid Docosahexaenoic Acids - pharmacology drug therapy eicosapentaenoic acid Eicosapentaenoic Acid - pharmacology epithelium Fatty Acids, Omega-3 - pharmacology fibrosis inflammation Kelch-Like ECH-Associated Protein 1 - metabolism Kidney - drug effects Kidney - metabolism Kidney - pathology Kidney Diseases - chemically induced Kidney Diseases - drug therapy Kidney Diseases - metabolism Kidney Diseases - pathology Kidney Diseases - prevention & control kidneys Male Mice Nephrotoxicity NF-E2-Related Factor 2 - metabolism Nrf2 Omega-3 polyunsaturated fatty acids oxidative stress Oxidative Stress - drug effects pathogenesis Protective Agents - pharmacology protective effect Proto-Oncogene Proteins c-mdm2 - metabolism Signal Transduction - drug effects Tumor Suppressor Protein p53 - genetics Tumor Suppressor Protein p53 - metabolism |
| title | Omega-3 polyunsaturated fatty acids protect against cisplatin-induced nephrotoxicity by activating the Nrf2 signaling pathway |
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