Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)

TNFα belongs to superfamily of tumor necrosis factor that can exert the pleiotropic effort in a large quantity of biological processes, including immune homeostasis, intracellular modulation and etiopathogenesis, but its regulatory role in mucosal immune regulation of fish is unclear. Currently, thi...

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Main Authors: Jin-Fang Huang, Ning-Xia Xiong, Shi-Yun Li, Ke-Xin Li, Jie Ou, Fei Wang, Sheng-Wei Luo
Format: Article
Language:English
Published: KeAi Communications Co. Ltd. 2023-12-01
Series:Reproduction and Breeding
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2667071223000467
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author Jin-Fang Huang
Ning-Xia Xiong
Shi-Yun Li
Ke-Xin Li
Jie Ou
Fei Wang
Sheng-Wei Luo
author_facet Jin-Fang Huang
Ning-Xia Xiong
Shi-Yun Li
Ke-Xin Li
Jie Ou
Fei Wang
Sheng-Wei Luo
author_sort Jin-Fang Huang
collection DOAJ
description TNFα belongs to superfamily of tumor necrosis factor that can exert the pleiotropic effort in a large quantity of biological processes, including immune homeostasis, intracellular modulation and etiopathogenesis, but its regulatory role in mucosal immune regulation of fish is unclear. Currently, this study aimed to evaluate the immunoregulatory function of TNFα1 on gut barrier in teleost fish. In this study, TNFα1 sequences were identified from red crucian carp (RCC, Carassius auratus red var). The high-level expression of RCC-TNFα1 mRNA was detected in gill among all the isolated samples. Then, RCC-TNFα1 expression increased dramatically in immune-related tissues after A. hydrophila infection and in cultured fish cells after lipopolysaccharide (LPS) treatment. RCC-TNFα1 fusion protein was generated and purified in vitro. RCC receiving RCC-TNFα1 perfusion showed an increased levels of villi fusion and edema in injured midgut with the fuzzy appearance. In addition, The mRNA expressions of tight junction (TJ) genes, mucin genes and redox sensitive genes decreased sharply in TNFα1-treated midgut in comparison with those of the control (P < 0.05), whereas the expression levels of apoptotic genes involved in caspase signals and unfolded protein response (UPR) attained the dramatic increase. These results demonstrated that RCC-TNFα1 stimulation could impair midgut structural integrity and immune function by induction of antioxidant collapse and apoptotic activation.
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spelling doaj.art-76c734bfff8c4c61812c45b64bc1227d2023-11-30T05:11:49ZengKeAi Communications Co. Ltd.Reproduction and Breeding2667-07122023-12-0134208218Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)Jin-Fang Huang0Ning-Xia Xiong1Shi-Yun Li2Ke-Xin Li3Jie Ou4Fei Wang5Sheng-Wei Luo6State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, PR ChinaState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, PR China; Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, 430070, PR ChinaState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, PR ChinaState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, PR ChinaState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, PR ChinaState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, PR ChinaState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, PR China; Corresponding author. College of Life Science, Hunan Normal University, Changsha, 410081, PR China.TNFα belongs to superfamily of tumor necrosis factor that can exert the pleiotropic effort in a large quantity of biological processes, including immune homeostasis, intracellular modulation and etiopathogenesis, but its regulatory role in mucosal immune regulation of fish is unclear. Currently, this study aimed to evaluate the immunoregulatory function of TNFα1 on gut barrier in teleost fish. In this study, TNFα1 sequences were identified from red crucian carp (RCC, Carassius auratus red var). The high-level expression of RCC-TNFα1 mRNA was detected in gill among all the isolated samples. Then, RCC-TNFα1 expression increased dramatically in immune-related tissues after A. hydrophila infection and in cultured fish cells after lipopolysaccharide (LPS) treatment. RCC-TNFα1 fusion protein was generated and purified in vitro. RCC receiving RCC-TNFα1 perfusion showed an increased levels of villi fusion and edema in injured midgut with the fuzzy appearance. In addition, The mRNA expressions of tight junction (TJ) genes, mucin genes and redox sensitive genes decreased sharply in TNFα1-treated midgut in comparison with those of the control (P < 0.05), whereas the expression levels of apoptotic genes involved in caspase signals and unfolded protein response (UPR) attained the dramatic increase. These results demonstrated that RCC-TNFα1 stimulation could impair midgut structural integrity and immune function by induction of antioxidant collapse and apoptotic activation.http://www.sciencedirect.com/science/article/pii/S2667071223000467Crucian carpCytokinesGene expressionGut immunity
spellingShingle Jin-Fang Huang
Ning-Xia Xiong
Shi-Yun Li
Ke-Xin Li
Jie Ou
Fei Wang
Sheng-Wei Luo
Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)
Reproduction and Breeding
Crucian carp
Cytokines
Gene expression
Gut immunity
title Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)
title_full Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)
title_fullStr Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)
title_full_unstemmed Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)
title_short Tumor necrosis factor α1 (TNFα1) administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp (Carassius auratus red var)
title_sort tumor necrosis factor α1 tnfα1 administration can disrupt barrier function and attenuate redox defense in midgut of red crucian carp carassius auratus red var
topic Crucian carp
Cytokines
Gene expression
Gut immunity
url http://www.sciencedirect.com/science/article/pii/S2667071223000467
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