Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary protein
Nitrite poses a serious threat to intensive aquaculture. Protein, as a major nutrient in animals, is vital for protecting animal tissues from damage. In this study, we investigated the protective effect of dietary protein on gill tissue structure and the underlying mechanisms in sub-adult grass carp...
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| Format: | Article |
| Language: | English |
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Elsevier
2022-09-01
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| Series: | Ecotoxicology and Environmental Safety |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S014765132200834X |
| _version_ | 1798032273578131456 |
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| author | Hong-Ju Liu Min Dong Wei-Dan Jiang Pei Wu Yang Liu Xiao-Wan Jin Sheng-Yao Kuang Ling Tang Lu Zhang Lin Feng Xiao-Qiu Zhou |
| author_facet | Hong-Ju Liu Min Dong Wei-Dan Jiang Pei Wu Yang Liu Xiao-Wan Jin Sheng-Yao Kuang Ling Tang Lu Zhang Lin Feng Xiao-Qiu Zhou |
| author_sort | Hong-Ju Liu |
| collection | DOAJ |
| description | Nitrite poses a serious threat to intensive aquaculture. Protein, as a major nutrient in animals, is vital for protecting animal tissues from damage. In this study, we investigated the protective effect of dietary protein on gill tissue structure and the underlying mechanisms in sub-adult grass carp (Ctenopharyngodon idella) exposed to nitrite stress. Six iso-energetic semi-purified diets containing different protein levels (16–31 %) were formulated, and fed to fish for 60 d. The fish were then exposed to a nitrite solution for 4 d. Histopathological observation and determination of related indices (serum glucose, serum cortisol, nitric oxide, peroxynitrite, reactive oxygen species, malondialdehyde, and protein carbonyl) showed that 22–25 % dietary protein significantly alleviated the nitrite-induced stress response, gill tissue damage and oxidative damage. Further research found that a suitable dietary protein suppressed the nitrite-induced endoplasmic reticulum stress (ERS) 78 kDa glucose-regulated protein (GRP78) related signaling pathway which possibly activated autophagy and apoptosis. Interestingly, we discovered that proper dietary protein reduced autophagy, probably through unc-51-like kinase 1 (Ulk1), BCL-2-interacting myosin-like coiled-coil protein (Beclin1), autophagy-related gene 5 (Atg5), Atg12, microtubule-associated protein1 light chain 3 (LC3), BCL-2 interacting protein 3 (BNIP3) and autophagy receptor P62 (p62). We also found that an appropriate dietary protein inhibited nitrite-induced apoptosis via mitochondrial and death receptor pathways. In summary, our findings are the first to demonstrate that 22–25 % of dietary protein levels can play a protective role against nitrite-induced gill injury. |
| first_indexed | 2024-04-11T20:11:26Z |
| format | Article |
| id | doaj.art-3112096579814b33ae6b747862637a77 |
| institution | Directory Open Access Journal |
| issn | 0147-6513 |
| language | English |
| last_indexed | 2024-04-11T20:11:26Z |
| publishDate | 2022-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj.art-3112096579814b33ae6b747862637a772022-12-22T04:05:06ZengElsevierEcotoxicology and Environmental Safety0147-65132022-09-01243113994Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary proteinHong-Ju Liu0Min Dong1Wei-Dan Jiang2Pei Wu3Yang Liu4Xiao-Wan Jin5Sheng-Yao Kuang6Ling Tang7Lu Zhang8Lin Feng9Xiao-Qiu Zhou10Animal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education, Ministry of Agriculture and Rural Affairs, Key Laboratory of Sichuan Province, Sichuan 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education, Ministry of Agriculture and Rural Affairs, Key Laboratory of Sichuan Province, Sichuan 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education, Ministry of Agriculture and Rural Affairs, Key Laboratory of Sichuan Province, Sichuan 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education, Ministry of Agriculture and Rural Affairs, Key Laboratory of Sichuan Province, Sichuan 611130, ChinaAnimal Nutrition Institute, Sichuan Academy of Animal Science, Sichuan Animtech Feed Co. Ltd，Chengdu 610066, Sichuan, ChinaAnimal Nutrition Institute, Sichuan Academy of Animal Science, Sichuan Animtech Feed Co. Ltd，Chengdu 610066, Sichuan, ChinaTongwei Co., Ltd., Chengdu, China, Healthy Aquaculture Key Laboratory of Sichuan Province, Sichuan 610041, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education, Ministry of Agriculture and Rural Affairs, Key Laboratory of Sichuan Province, Sichuan 611130, China; Corresponding authors at: Animal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory of Animal Disease-Resistance Nutrition, Ministry of Education, Ministry of Agriculture and Rural Affairs, Key Laboratory of Sichuan Province, Sichuan 611130, China; Corresponding authors at: Animal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, ChinaNitrite poses a serious threat to intensive aquaculture. Protein, as a major nutrient in animals, is vital for protecting animal tissues from damage. In this study, we investigated the protective effect of dietary protein on gill tissue structure and the underlying mechanisms in sub-adult grass carp (Ctenopharyngodon idella) exposed to nitrite stress. Six iso-energetic semi-purified diets containing different protein levels (16–31 %) were formulated, and fed to fish for 60 d. The fish were then exposed to a nitrite solution for 4 d. Histopathological observation and determination of related indices (serum glucose, serum cortisol, nitric oxide, peroxynitrite, reactive oxygen species, malondialdehyde, and protein carbonyl) showed that 22–25 % dietary protein significantly alleviated the nitrite-induced stress response, gill tissue damage and oxidative damage. Further research found that a suitable dietary protein suppressed the nitrite-induced endoplasmic reticulum stress (ERS) 78 kDa glucose-regulated protein (GRP78) related signaling pathway which possibly activated autophagy and apoptosis. Interestingly, we discovered that proper dietary protein reduced autophagy, probably through unc-51-like kinase 1 (Ulk1), BCL-2-interacting myosin-like coiled-coil protein (Beclin1), autophagy-related gene 5 (Atg5), Atg12, microtubule-associated protein1 light chain 3 (LC3), BCL-2 interacting protein 3 (BNIP3) and autophagy receptor P62 (p62). We also found that an appropriate dietary protein inhibited nitrite-induced apoptosis via mitochondrial and death receptor pathways. In summary, our findings are the first to demonstrate that 22–25 % of dietary protein levels can play a protective role against nitrite-induced gill injury.http://www.sciencedirect.com/science/article/pii/S014765132200834XNitriteGillEndoplasmic reticulum stress (ERS)AutophagyProteinGrass carp (Ctenopharyngodon idella) |
| spellingShingle | Hong-Ju Liu Min Dong Wei-Dan Jiang Pei Wu Yang Liu Xiao-Wan Jin Sheng-Yao Kuang Ling Tang Lu Zhang Lin Feng Xiao-Qiu Zhou Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary protein Ecotoxicology and Environmental Safety Nitrite Gill Endoplasmic reticulum stress (ERS) Autophagy Protein Grass carp (Ctenopharyngodon idella) |
| title | Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary protein |
| title_full | Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary protein |
| title_fullStr | Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary protein |
| title_full_unstemmed | Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary protein |
| title_short | Acute nitrite exposure-induced oxidative damage, endoplasmic reticulum stress, autophagy and apoptosis caused gill tissue damage of grass carp (Ctenopharyngodon idella): Relieved by dietary protein |
| title_sort | acute nitrite exposure induced oxidative damage endoplasmic reticulum stress autophagy and apoptosis caused gill tissue damage of grass carp ctenopharyngodon idella relieved by dietary protein |
| topic | Nitrite Gill Endoplasmic reticulum stress (ERS) Autophagy Protein Grass carp (Ctenopharyngodon idella) |
| url | http://www.sciencedirect.com/science/article/pii/S014765132200834X |
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