Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infection

Abstract Background Mannan oligosaccharides (MOS) are recommended as aquaculture additives owing to their excellent antioxidant properties. In the present study, we examined the effects of dietary MOS on the head kidney and spleen of grass carp (Ctenopharyngodon idella) with Aeromonas hydrophila inf...

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Main Authors: Zhiyuan Lu, Lin Feng, Weidan Jiang, Pei Wu, Yang Liu, Jun Jiang, Shengyao Kuang, Ling Tang, Shuwei Li, Chengbo Zhong, Xiaoqiu Zhou
Format: Article
Language:English
Published: BMC 2023-04-01
Series:Journal of Animal Science and Biotechnology
Subjects:
Online Access:https://doi.org/10.1186/s40104-023-00844-1
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author Zhiyuan Lu
Lin Feng
Weidan Jiang
Pei Wu
Yang Liu
Jun Jiang
Shengyao Kuang
Ling Tang
Shuwei Li
Chengbo Zhong
Xiaoqiu Zhou
author_facet Zhiyuan Lu
Lin Feng
Weidan Jiang
Pei Wu
Yang Liu
Jun Jiang
Shengyao Kuang
Ling Tang
Shuwei Li
Chengbo Zhong
Xiaoqiu Zhou
author_sort Zhiyuan Lu
collection DOAJ
description Abstract Background Mannan oligosaccharides (MOS) are recommended as aquaculture additives owing to their excellent antioxidant properties. In the present study, we examined the effects of dietary MOS on the head kidney and spleen of grass carp (Ctenopharyngodon idella) with Aeromonas hydrophila infection. Methods A total of 540 grass carp were used for the study. They were administered six gradient dosages of the MOS diet (0, 200, 400, 600, 800, and 1,000 mg/kg) for 60 d. Subsequently, we performed a 14-day Aeromonas hydrophila challenge experiment. The antioxidant capacity of the head kidney and spleen were examined using spectrophotometry, DNA fragmentation, qRT-PCR, and Western blotting. Results After infection with Aeromonas hydrophila, 400–600 mg/kg MOS supplementation decreased the levels of reactive oxygen species, protein carbonyl, and malonaldehyde and increased the levels of anti-superoxide anion, anti-hydroxyl radical, and glutathione in the head kidney and spleen of grass carp. The activities of copper-zinc superoxide dismutase, manganese superoxide dismutase, catalase, glutathione S-transferase, glutathione reductase, and glutathione peroxidase were also enhanced by supplementation with 400–600 mg/kg MOS. Furthermore, the expression of most antioxidant enzymes and their corresponding genes increased significantly with supplementation of 200–800 mg/kg MOS. mRNA and protein levels of nuclear factor erythroid 2-related factor 2 also increased following supplementation with 400–600 mg/kg MOS. In addition, supplementation with 400–600 mg/kg MOS reduced excessive apoptosis by inhibiting the death receptor pathway and mitochondrial pathway processes. Conclusions Based on the quadratic regression analysis of the above biomarkers (reactive oxygen species, malondialdehyde, and protein carbonyl) of oxidative damage in the head kidney and spleen of on-growing grass carp, the recommended MOS supplementation is 575.21, 557.58, 531.86, 597.35, 570.16, and 553.80 mg/kg, respectively. Collectively, MOS supplementation could alleviate oxidative injury in the head kidney and spleen of grass carp infected with Aeromonas hydrophila.
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spelling doaj.art-3c0d80be7e0a43a7a9e016b57cfadaec2023-04-16T11:21:12ZengBMCJournal of Animal Science and Biotechnology2049-18912023-04-0114111510.1186/s40104-023-00844-1Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infectionZhiyuan Lu0Lin Feng1Weidan Jiang2Pei Wu3Yang Liu4Jun Jiang5Shengyao Kuang6Ling Tang7Shuwei Li8Chengbo Zhong9Xiaoqiu Zhou10Animal Nutrition Institute, Sichuan Agricultural UniversityAnimal Nutrition Institute, Sichuan Agricultural UniversityAnimal Nutrition Institute, Sichuan Agricultural UniversityAnimal Nutrition Institute, Sichuan Agricultural UniversityAnimal Nutrition Institute, Sichuan Agricultural UniversityAnimal Nutrition Institute, Sichuan Agricultural UniversitySichuan Animal Science Academy, Sichuan Animtech Feed Co. LtdSichuan Animal Science Academy, Sichuan Animtech Feed Co. LtdSichuan Animal Science Academy, Sichuan Animtech Feed Co. LtdSichuan Animal Science Academy, Sichuan Animtech Feed Co. LtdAnimal Nutrition Institute, Sichuan Agricultural UniversityAbstract Background Mannan oligosaccharides (MOS) are recommended as aquaculture additives owing to their excellent antioxidant properties. In the present study, we examined the effects of dietary MOS on the head kidney and spleen of grass carp (Ctenopharyngodon idella) with Aeromonas hydrophila infection. Methods A total of 540 grass carp were used for the study. They were administered six gradient dosages of the MOS diet (0, 200, 400, 600, 800, and 1,000 mg/kg) for 60 d. Subsequently, we performed a 14-day Aeromonas hydrophila challenge experiment. The antioxidant capacity of the head kidney and spleen were examined using spectrophotometry, DNA fragmentation, qRT-PCR, and Western blotting. Results After infection with Aeromonas hydrophila, 400–600 mg/kg MOS supplementation decreased the levels of reactive oxygen species, protein carbonyl, and malonaldehyde and increased the levels of anti-superoxide anion, anti-hydroxyl radical, and glutathione in the head kidney and spleen of grass carp. The activities of copper-zinc superoxide dismutase, manganese superoxide dismutase, catalase, glutathione S-transferase, glutathione reductase, and glutathione peroxidase were also enhanced by supplementation with 400–600 mg/kg MOS. Furthermore, the expression of most antioxidant enzymes and their corresponding genes increased significantly with supplementation of 200–800 mg/kg MOS. mRNA and protein levels of nuclear factor erythroid 2-related factor 2 also increased following supplementation with 400–600 mg/kg MOS. In addition, supplementation with 400–600 mg/kg MOS reduced excessive apoptosis by inhibiting the death receptor pathway and mitochondrial pathway processes. Conclusions Based on the quadratic regression analysis of the above biomarkers (reactive oxygen species, malondialdehyde, and protein carbonyl) of oxidative damage in the head kidney and spleen of on-growing grass carp, the recommended MOS supplementation is 575.21, 557.58, 531.86, 597.35, 570.16, and 553.80 mg/kg, respectively. Collectively, MOS supplementation could alleviate oxidative injury in the head kidney and spleen of grass carp infected with Aeromonas hydrophila.https://doi.org/10.1186/s40104-023-00844-1AntioxidantApoptosisFunctional organsGrass carpMannan oligosaccharides
spellingShingle Zhiyuan Lu
Lin Feng
Weidan Jiang
Pei Wu
Yang Liu
Jun Jiang
Shengyao Kuang
Ling Tang
Shuwei Li
Chengbo Zhong
Xiaoqiu Zhou
Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infection
Journal of Animal Science and Biotechnology
Antioxidant
Apoptosis
Functional organs
Grass carp
Mannan oligosaccharides
title Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infection
title_full Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infection
title_fullStr Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infection
title_full_unstemmed Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infection
title_short Mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp (Ctenopharyngodon idella) via the Nrf2 signaling pathway after Aeromonas hydrophila infection
title_sort mannan oligosaccharides alleviate oxidative injury in the head kidney and spleen in grass carp ctenopharyngodon idella via the nrf2 signaling pathway after aeromonas hydrophila infection
topic Antioxidant
Apoptosis
Functional organs
Grass carp
Mannan oligosaccharides
url https://doi.org/10.1186/s40104-023-00844-1
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