Effects of cold stress on the blood-brain barrier in Plectropomus leopardus
Abstract Background The leopard coral grouper (Plectropomus leopardus) is a commercially valuable tropical marine fish species known to be sensitive to low temperatures. A comprehensive understanding of the molecular mechanisms governing its response to acute cold stress is of great importance. Howe...
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2024-11-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-024-10943-6 |
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| author | Yilan Guo Cun Wei Hui Ding Peiyu Li Yurui Gao Kangning Zhong Zhenmin Bao Zhe Qu Bo Wang Jingjie Hu |
| author_facet | Yilan Guo Cun Wei Hui Ding Peiyu Li Yurui Gao Kangning Zhong Zhenmin Bao Zhe Qu Bo Wang Jingjie Hu |
| author_sort | Yilan Guo |
| collection | DOAJ |
| description | Abstract Background The leopard coral grouper (Plectropomus leopardus) is a commercially valuable tropical marine fish species known to be sensitive to low temperatures. A comprehensive understanding of the molecular mechanisms governing its response to acute cold stress is of great importance. However, there is a relative scarcity of fundamental research on low-temperature tolerance in the leopard coral grouper. Methods In this study, a cooling and rewarming experiment was conducted on 6-month-old leopard coral groupers. Within 24 h, we decreased the ambient temperature from 25 °C to 13 °C and subsequently allowed it to naturally return to 25 °C. During this process, a comprehensive investigation of serum hormone levels, enzyme activity, and brain transcriptome analysis was performed. Results P. leopardus displayed a noticeable adaptive response to the initial temperature decrease by temporarily reducing its life activities. Our transcriptome analysis revealed that the differentially expressed genes (DEGs) were primarily concentrated in crucial pathways including the blood-brain barrier (BBB), inflammatory response, and coagulation cascade. In situ hybridization of claudin 15a (cldn15a), a key gene for BBB maintaining, further confirmed that exposure to low temperatures led to the disruption of the blood-brain barrier and stimulated a pronounced inflammatory reaction within the brain. Upon rewarming, there was a recovery of BBB integrity accompanied by the persistence of inflammation within the brain tissue. Conclusions Our study reveals the complex interactions between blood-brain barrier function, inflammation, and recovery in P. leopardus during short-term temperature drops and rewarming. These findings provide valuable insights into the physiological responses of this species under cold stress conditions. |
| format | Article |
| id | doaj-art-7d967496c2ca4a1396a6da6519432feb |
| institution | Kabale University |
| issn | 1471-2164 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj-art-7d967496c2ca4a1396a6da6519432feb2024-11-10T12:09:21ZengBMCBMC Genomics1471-21642024-11-0125111510.1186/s12864-024-10943-6Effects of cold stress on the blood-brain barrier in Plectropomus leopardusYilan Guo0Cun Wei1Hui Ding2Peiyu Li3Yurui Gao4Kangning Zhong5Zhenmin Bao6Zhe Qu7Bo Wang8Jingjie Hu9MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences/Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of ChinaAbstract Background The leopard coral grouper (Plectropomus leopardus) is a commercially valuable tropical marine fish species known to be sensitive to low temperatures. A comprehensive understanding of the molecular mechanisms governing its response to acute cold stress is of great importance. However, there is a relative scarcity of fundamental research on low-temperature tolerance in the leopard coral grouper. Methods In this study, a cooling and rewarming experiment was conducted on 6-month-old leopard coral groupers. Within 24 h, we decreased the ambient temperature from 25 °C to 13 °C and subsequently allowed it to naturally return to 25 °C. During this process, a comprehensive investigation of serum hormone levels, enzyme activity, and brain transcriptome analysis was performed. Results P. leopardus displayed a noticeable adaptive response to the initial temperature decrease by temporarily reducing its life activities. Our transcriptome analysis revealed that the differentially expressed genes (DEGs) were primarily concentrated in crucial pathways including the blood-brain barrier (BBB), inflammatory response, and coagulation cascade. In situ hybridization of claudin 15a (cldn15a), a key gene for BBB maintaining, further confirmed that exposure to low temperatures led to the disruption of the blood-brain barrier and stimulated a pronounced inflammatory reaction within the brain. Upon rewarming, there was a recovery of BBB integrity accompanied by the persistence of inflammation within the brain tissue. Conclusions Our study reveals the complex interactions between blood-brain barrier function, inflammation, and recovery in P. leopardus during short-term temperature drops and rewarming. These findings provide valuable insights into the physiological responses of this species under cold stress conditions.https://doi.org/10.1186/s12864-024-10943-6Low temperatureBrainBlood brain barrierTranscriptomeClaudin |
| spellingShingle | Yilan Guo Cun Wei Hui Ding Peiyu Li Yurui Gao Kangning Zhong Zhenmin Bao Zhe Qu Bo Wang Jingjie Hu Effects of cold stress on the blood-brain barrier in Plectropomus leopardus BMC Genomics Low temperature Brain Blood brain barrier Transcriptome Claudin |
| title | Effects of cold stress on the blood-brain barrier in Plectropomus leopardus |
| title_full | Effects of cold stress on the blood-brain barrier in Plectropomus leopardus |
| title_fullStr | Effects of cold stress on the blood-brain barrier in Plectropomus leopardus |
| title_full_unstemmed | Effects of cold stress on the blood-brain barrier in Plectropomus leopardus |
| title_short | Effects of cold stress on the blood-brain barrier in Plectropomus leopardus |
| title_sort | effects of cold stress on the blood brain barrier in plectropomus leopardus |
| topic | Low temperature Brain Blood brain barrier Transcriptome Claudin |
| url | https://doi.org/10.1186/s12864-024-10943-6 |
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