Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnare

The objective of this research was to investigate how dietary antimicrobial peptides (AMP), namely, Isalo scorpion cytotoxic peptide (IsCT), affect the gill physical barrier function and immune function of grass carp challenged with Flavobacterium columnare (F. columnare). Five hundred forty grass c...

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Main Authors: Qiu-Yan Chen, Qi-Yu Hu, Wei-Dan Jiang, Pei Wu, Yang Liu, Hong-Mei Ren, Xiao-Wan Jin, Lin Feng, Xiao-Qiu Zhou
Format: Article
Language:English
Published: Wiley 2024-01-01
Series:Aquaculture Nutrition
Online Access:http://dx.doi.org/10.1155/2024/8059770
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author Qiu-Yan Chen
Qi-Yu Hu
Wei-Dan Jiang
Pei Wu
Yang Liu
Hong-Mei Ren
Xiao-Wan Jin
Lin Feng
Xiao-Qiu Zhou
author_facet Qiu-Yan Chen
Qi-Yu Hu
Wei-Dan Jiang
Pei Wu
Yang Liu
Hong-Mei Ren
Xiao-Wan Jin
Lin Feng
Xiao-Qiu Zhou
author_sort Qiu-Yan Chen
collection DOAJ
description The objective of this research was to investigate how dietary antimicrobial peptides (AMP), namely, Isalo scorpion cytotoxic peptide (IsCT), affect the gill physical barrier function and immune function of grass carp challenged with Flavobacterium columnare (F. columnare). Five hundred forty grass carp were randomly allocated to six groups and fed to varying levels of IsCT in the diet (0, 0.6, 1.2, 1.8, 2.4, and 3.0 mg/kg diet) for a duration of 60 days. Afterward, the grass carps faced a challenge from F. columnare. The results revealed that the use of optimal IsCT dramatically mitigated gill damage in grass carp that were infected with F. columnare. Additionally, IsCT exhibited a notable enhancement in gill antioxidant capabilities, as evidenced by a significant reduction in ROS, MDA, and PC levels, an elevation in antioxidant enzyme activities, and an upregulation of antioxidant-related genes and Nrf2 mRNA levels. Conversely, the expression of Keap1a and Keap1b mRNA was decreased. Besides, IsCT exhibited its capability to inhibit apoptosis via downregulating the mRNA levels of caspase-2, caspase-3, caspase-7, caspase-8, caspase-9, Apaf1, Fasl, Bax, and JNK while concurrently increasing the mRNA levels of Bcl-2, Mcl-1, and IAP in fish gills. Additionally, IsCT promoted the integrity of tight junction barrier by increasing the gene expression of claudin-b, claudin-c, claudin-3c, ZO-1, ZO-2b, occludin, and JAM while suppressing MLCK signaling. Additionally, optimal dietary IsCT improved antibacterial ability, as evidenced by heightened LZ, ACP activities, and elevated levels of C3, C4, and IgM. Additionally, there was an upregulation in β-defensin-1, LEAP-2A, LEAP-2B, hepcidin, and mucin-2 mRNA expression in the gills. Simultaneously, the inclusion of optimal dietary IsCT in the diet resulted in improved gill immunity barriers through the reduction of proinflammatory cytokine mRNA levels and the increase in the expression of anti-inflammatory cytokine mRNA levels. This was partly facilitated by the IκBa/NF-κB p65 signaling pathway and TOR/S6K1 signaling pathways in the gills of grass carp. Therefore, supplementing the diet with IsCT has potential advantages in enhancing gill health by improved physical barriers and immunity in grass carp. Based on LZ activity and against lipid peroxidation, optimum IsCT concentrations in on-growing grass carp (136.88 ± 0.72 g) were found to be 1.68 and 1.54 mg/kg diet, respectively.
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publishDate 2024-01-01
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series Aquaculture Nutrition
spelling doaj-art-e7a943706def454c98b13100e6d8a65b2025-08-20T03:21:02ZengWileyAquaculture Nutrition1365-20952024-01-01202410.1155/2024/8059770Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnareQiu-Yan Chen0Qi-Yu Hu1Wei-Dan Jiang2Pei Wu3Yang Liu4Hong-Mei Ren5Xiao-Wan Jin6Lin Feng7Xiao-Qiu Zhou8The Animal Nutrition InstituteThe Animal Nutrition InstituteThe Animal Nutrition InstituteThe Animal Nutrition InstituteThe Animal Nutrition InstituteThe Animal Nutrition InstituteThe Animal Nutrition InstituteThe Animal Nutrition InstituteThe Animal Nutrition InstituteThe objective of this research was to investigate how dietary antimicrobial peptides (AMP), namely, Isalo scorpion cytotoxic peptide (IsCT), affect the gill physical barrier function and immune function of grass carp challenged with Flavobacterium columnare (F. columnare). Five hundred forty grass carp were randomly allocated to six groups and fed to varying levels of IsCT in the diet (0, 0.6, 1.2, 1.8, 2.4, and 3.0 mg/kg diet) for a duration of 60 days. Afterward, the grass carps faced a challenge from F. columnare. The results revealed that the use of optimal IsCT dramatically mitigated gill damage in grass carp that were infected with F. columnare. Additionally, IsCT exhibited a notable enhancement in gill antioxidant capabilities, as evidenced by a significant reduction in ROS, MDA, and PC levels, an elevation in antioxidant enzyme activities, and an upregulation of antioxidant-related genes and Nrf2 mRNA levels. Conversely, the expression of Keap1a and Keap1b mRNA was decreased. Besides, IsCT exhibited its capability to inhibit apoptosis via downregulating the mRNA levels of caspase-2, caspase-3, caspase-7, caspase-8, caspase-9, Apaf1, Fasl, Bax, and JNK while concurrently increasing the mRNA levels of Bcl-2, Mcl-1, and IAP in fish gills. Additionally, IsCT promoted the integrity of tight junction barrier by increasing the gene expression of claudin-b, claudin-c, claudin-3c, ZO-1, ZO-2b, occludin, and JAM while suppressing MLCK signaling. Additionally, optimal dietary IsCT improved antibacterial ability, as evidenced by heightened LZ, ACP activities, and elevated levels of C3, C4, and IgM. Additionally, there was an upregulation in β-defensin-1, LEAP-2A, LEAP-2B, hepcidin, and mucin-2 mRNA expression in the gills. Simultaneously, the inclusion of optimal dietary IsCT in the diet resulted in improved gill immunity barriers through the reduction of proinflammatory cytokine mRNA levels and the increase in the expression of anti-inflammatory cytokine mRNA levels. This was partly facilitated by the IκBa/NF-κB p65 signaling pathway and TOR/S6K1 signaling pathways in the gills of grass carp. Therefore, supplementing the diet with IsCT has potential advantages in enhancing gill health by improved physical barriers and immunity in grass carp. Based on LZ activity and against lipid peroxidation, optimum IsCT concentrations in on-growing grass carp (136.88 ± 0.72 g) were found to be 1.68 and 1.54 mg/kg diet, respectively.http://dx.doi.org/10.1155/2024/8059770
spellingShingle Qiu-Yan Chen
Qi-Yu Hu
Wei-Dan Jiang
Pei Wu
Yang Liu
Hong-Mei Ren
Xiao-Wan Jin
Lin Feng
Xiao-Qiu Zhou
Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnare
Aquaculture Nutrition
title Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnare
title_full Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnare
title_fullStr Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnare
title_full_unstemmed Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnare
title_short Exploring the Potential of Isalo Scorpion Cytotoxic Peptide in Enhancing Gill Barrier Function and Immunity in Grass Carp (Ctenopharyngodon idella) Infected with Flavobacterium columnare
title_sort exploring the potential of isalo scorpion cytotoxic peptide in enhancing gill barrier function and immunity in grass carp ctenopharyngodon idella infected with flavobacterium columnare
url http://dx.doi.org/10.1155/2024/8059770
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