Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidation
Oxidative stress in muscles is closely related to the occurrence of insulin resistance, muscle weakness and atrophy, age-related sarcopenia, and cancer. Aldehydes, a primary oxidation intermediate of polyunsaturated fatty acids, have been proven to be an important trigger for oxidative stress. Howev...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-05-01
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| Series: | Redox Biology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213231724000727 |
| _version_ | 1797235554455126016 |
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| author | Xiufei Cao Huixing Guo Yongjun Dai Guangzhen Jiang Wenbin Liu Xiangfei Li Dingdong Zhang Yangyang Huang Xi Wang Haokun Hua Jianfeng Wang Keke Chen Cheng Chi Hengtong Liu |
| author_facet | Xiufei Cao Huixing Guo Yongjun Dai Guangzhen Jiang Wenbin Liu Xiangfei Li Dingdong Zhang Yangyang Huang Xi Wang Haokun Hua Jianfeng Wang Keke Chen Cheng Chi Hengtong Liu |
| author_sort | Xiufei Cao |
| collection | DOAJ |
| description | Oxidative stress in muscles is closely related to the occurrence of insulin resistance, muscle weakness and atrophy, age-related sarcopenia, and cancer. Aldehydes, a primary oxidation intermediate of polyunsaturated fatty acids, have been proven to be an important trigger for oxidative stress. However, the potential role of linoleic acid (LA) as a donor for volatile aldehydes to trigger oxidative stress has not been reported. Here, we reported that excessive dietary LA caused muscle redox imbalance and volatile aldehydes containing hexanal, 2-hexenal, and nonanal were the main metabolites leading to oxidative stress. Importantly, we identified 5-lipoxygenase (5-LOX) as a key enzyme mediating LA peroxidation in crustaceans for the first time. The inhibition of 5-LOX significantly suppressed the content of aldehydes produced by excessive LA. Mechanistically, the activation of the cyclic adenosine monophosphate (cAMP)-protein kinase A (PKA) pathway facilitated the translocation of 5-LOX from the nucleus to the cytoplasm, where 5-LOX oxidized LA, leading to oxidative stress through the generation of aldehydes. This study suggests that 5-LOX is a potential target to prevent the production of harmful aldehydes. |
| first_indexed | 2024-03-07T22:54:33Z |
| format | Article |
| id | doaj.art-aa32bf80fb0a4273b85ba5287ee8ff92 |
| institution | Directory Open Access Journal |
| issn | 2213-2317 |
| language | English |
| last_indexed | 2024-04-24T16:49:48Z |
| publishDate | 2024-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Redox Biology |
| spelling | doaj.art-aa32bf80fb0a4273b85ba5287ee8ff922024-03-29T05:50:12ZengElsevierRedox Biology2213-23172024-05-0171103096Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidationXiufei Cao0Huixing Guo1Yongjun Dai2Guangzhen Jiang3Wenbin Liu4Xiangfei Li5Dingdong Zhang6Yangyang Huang7Xi Wang8Haokun Hua9Jianfeng Wang10Keke Chen11Cheng Chi12Hengtong Liu13Key Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaCorresponding author.; Key Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaCorresponding author. Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of China.; Key Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaKey Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, Nanjing Agricultural University, No.1 Weigang Road, 210095, Nanjing, Jiangsu, People's Republic of ChinaOxidative stress in muscles is closely related to the occurrence of insulin resistance, muscle weakness and atrophy, age-related sarcopenia, and cancer. Aldehydes, a primary oxidation intermediate of polyunsaturated fatty acids, have been proven to be an important trigger for oxidative stress. However, the potential role of linoleic acid (LA) as a donor for volatile aldehydes to trigger oxidative stress has not been reported. Here, we reported that excessive dietary LA caused muscle redox imbalance and volatile aldehydes containing hexanal, 2-hexenal, and nonanal were the main metabolites leading to oxidative stress. Importantly, we identified 5-lipoxygenase (5-LOX) as a key enzyme mediating LA peroxidation in crustaceans for the first time. The inhibition of 5-LOX significantly suppressed the content of aldehydes produced by excessive LA. Mechanistically, the activation of the cyclic adenosine monophosphate (cAMP)-protein kinase A (PKA) pathway facilitated the translocation of 5-LOX from the nucleus to the cytoplasm, where 5-LOX oxidized LA, leading to oxidative stress through the generation of aldehydes. This study suggests that 5-LOX is a potential target to prevent the production of harmful aldehydes.http://www.sciencedirect.com/science/article/pii/S2213231724000727Crab muscleLinoleic acidOxidative stressVolatile aldehydes5-LipoxygenasecAMP/PKA signaling pathway |
| spellingShingle | Xiufei Cao Huixing Guo Yongjun Dai Guangzhen Jiang Wenbin Liu Xiangfei Li Dingdong Zhang Yangyang Huang Xi Wang Haokun Hua Jianfeng Wang Keke Chen Cheng Chi Hengtong Liu Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidation Redox Biology Crab muscle Linoleic acid Oxidative stress Volatile aldehydes 5-Lipoxygenase cAMP/PKA signaling pathway |
| title | Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidation |
| title_full | Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidation |
| title_fullStr | Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidation |
| title_full_unstemmed | Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidation |
| title_short | Excessive linoleic acid induces muscle oxidative stress through 5-lipoxygenase-dependent peroxidation |
| title_sort | excessive linoleic acid induces muscle oxidative stress through 5 lipoxygenase dependent peroxidation |
| topic | Crab muscle Linoleic acid Oxidative stress Volatile aldehydes 5-Lipoxygenase cAMP/PKA signaling pathway |
| url | http://www.sciencedirect.com/science/article/pii/S2213231724000727 |
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