Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys crocea

Hypoxia is one of the major environmental stressors, frequently resulting in serious yield losses for maricultured large yellow croaker (Larimichthys crocea). We know that pyroptosis contributes to tissue damage under hypoxic conditions. However, whether GSDMEs-mediated pyroptosis is involved in hyp...

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Main Authors: Lin Wang, Shuaiyu Chen, Yongyang Wang, Weini Zhang, Yinnan Mu, Yudong Jia, Changtao Guan, Meng Xue, Xinhua Chen
Format: Article
Language:English
Published: KeAi Communications Co. Ltd. 2025-01-01
Series:Water Biology and Security
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Online Access:http://www.sciencedirect.com/science/article/pii/S2772735124000945
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author Lin Wang
Shuaiyu Chen
Yongyang Wang
Weini Zhang
Yinnan Mu
Yudong Jia
Changtao Guan
Meng Xue
Xinhua Chen
author_facet Lin Wang
Shuaiyu Chen
Yongyang Wang
Weini Zhang
Yinnan Mu
Yudong Jia
Changtao Guan
Meng Xue
Xinhua Chen
author_sort Lin Wang
collection DOAJ
description Hypoxia is one of the major environmental stressors, frequently resulting in serious yield losses for maricultured large yellow croaker (Larimichthys crocea). We know that pyroptosis contributes to tissue damage under hypoxic conditions. However, whether GSDMEs-mediated pyroptosis is involved in hypoxia-induced tissue damage in fish remains unclear. In the present study, two Lcgsdme genes, Lcgsdmea/b, were cloned and characterized from the large yellow croaker. Both genes contain a conserved N-terminal pore-forming domain, a C-terminal autoinhibitory domain, and a flexible hinge region. After hypoxia stress, the expression of Lcgsdmea/b transcripts and proteins in the liver were significantly higher than in unstressed fish. The proteins of LcGSDMEa/b could be cleaved under hypoxic conditions. Compared to LcGSDMEb, the expression of LcGSDMEa was higher in both mRNA and protein levels, thus exhibiting a stronger response during hypoxia stress. Furthermore, after 48 ​h of hypoxia stress, approximately 65% liver cells exhibited abnormalities, with pyroptosis being detected using a transmission electron microscope. TUNEL/LcGSDMEa double staining assay revealed a high expression of LcGSDMEa in the dead cells. We observed a significant up-regulation of pyroptosis pathway genes (asc, caspase-3) and pro-inflammatory cytokine genes (il-1β, il-18). After simultaneous knockdown of Lcgsdmea/b in vivo, the liver exhibited better health compared to the control group, with less cell swelling and vacuolation. Taken together, these findings demonstrate that hypoxia stress could activate LcGSDMEa/b and induce pyroptosis in the liver of large yellow croakers, thereby contributing to tissue damage. Our study improves the understanding of hypoxia-induced tissue damage in fish, and provides new clues for protecting fish against hypoxia-induced damage.
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spelling doaj-art-68f7252570474addb1a2678ec509eea82025-01-27T04:22:42ZengKeAi Communications Co. Ltd.Water Biology and Security2772-73512025-01-0141100322Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys croceaLin Wang0Shuaiyu Chen1Yongyang Wang2Weini Zhang3Yinnan Mu4Yudong Jia5Changtao Guan6Meng Xue7Xinhua Chen8State Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Life Sciences, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, ChinaKey Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Life Sciences, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Life Sciences, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Life Sciences, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaKey Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, ChinaKey Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, ChinaWomen and Children's Hospital, Qingdao University, Qingdao, 266000, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Life Sciences, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Corresponding author.Hypoxia is one of the major environmental stressors, frequently resulting in serious yield losses for maricultured large yellow croaker (Larimichthys crocea). We know that pyroptosis contributes to tissue damage under hypoxic conditions. However, whether GSDMEs-mediated pyroptosis is involved in hypoxia-induced tissue damage in fish remains unclear. In the present study, two Lcgsdme genes, Lcgsdmea/b, were cloned and characterized from the large yellow croaker. Both genes contain a conserved N-terminal pore-forming domain, a C-terminal autoinhibitory domain, and a flexible hinge region. After hypoxia stress, the expression of Lcgsdmea/b transcripts and proteins in the liver were significantly higher than in unstressed fish. The proteins of LcGSDMEa/b could be cleaved under hypoxic conditions. Compared to LcGSDMEb, the expression of LcGSDMEa was higher in both mRNA and protein levels, thus exhibiting a stronger response during hypoxia stress. Furthermore, after 48 ​h of hypoxia stress, approximately 65% liver cells exhibited abnormalities, with pyroptosis being detected using a transmission electron microscope. TUNEL/LcGSDMEa double staining assay revealed a high expression of LcGSDMEa in the dead cells. We observed a significant up-regulation of pyroptosis pathway genes (asc, caspase-3) and pro-inflammatory cytokine genes (il-1β, il-18). After simultaneous knockdown of Lcgsdmea/b in vivo, the liver exhibited better health compared to the control group, with less cell swelling and vacuolation. Taken together, these findings demonstrate that hypoxia stress could activate LcGSDMEa/b and induce pyroptosis in the liver of large yellow croakers, thereby contributing to tissue damage. Our study improves the understanding of hypoxia-induced tissue damage in fish, and provides new clues for protecting fish against hypoxia-induced damage.http://www.sciencedirect.com/science/article/pii/S2772735124000945Hypoxia stressLarimichthys croceaPyroptosisGasderminTissue damage
spellingShingle Lin Wang
Shuaiyu Chen
Yongyang Wang
Weini Zhang
Yinnan Mu
Yudong Jia
Changtao Guan
Meng Xue
Xinhua Chen
Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys crocea
Water Biology and Security
Hypoxia stress
Larimichthys crocea
Pyroptosis
Gasdermin
Tissue damage
title Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys crocea
title_full Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys crocea
title_fullStr Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys crocea
title_full_unstemmed Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys crocea
title_short Understanding the mechanisms of hypoxia-induced tissue damage in fish: The role of GasderminEa/b in Larimichthys crocea
title_sort understanding the mechanisms of hypoxia induced tissue damage in fish the role of gasderminea b in larimichthys crocea
topic Hypoxia stress
Larimichthys crocea
Pyroptosis
Gasdermin
Tissue damage
url http://www.sciencedirect.com/science/article/pii/S2772735124000945
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