Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegans
Aquatic animals have developed various mechanisms to live in either hyperionic or hypoionic environments, and, as such, not many species are capable of surviving in both. The red-eared slider turtle, Trachemys scripta elegans, a well-known freshwater species, has recently been found to invade and in...
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Frontiers Media S.A.
2019-07-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2019.00962/full |
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| author | Meiling Hong Na Li Jiangyue Li Weihao Li Lingyue Liang Qian Li Runqi Wang Haitao Shi Haitao Shi Kenneth B. Storey Li Ding |
| author_facet | Meiling Hong Na Li Jiangyue Li Weihao Li Lingyue Liang Qian Li Runqi Wang Haitao Shi Haitao Shi Kenneth B. Storey Li Ding |
| author_sort | Meiling Hong |
| collection | DOAJ |
| description | Aquatic animals have developed various mechanisms to live in either hyperionic or hypoionic environments, and, as such, not many species are capable of surviving in both. The red-eared slider turtle, Trachemys scripta elegans, a well-known freshwater species, has recently been found to invade and inhabit brackish water. Herein, we focus on some of the metabolic adaptations that are required to survive and cope with salinity stress. The regulation of the adenosine monophosphate (AMP)-activated protein kinase (AMPK), a main cellular “energy sensor,” and its influence on lipid metabolism were evaluated with a comparison of three groups of turtles: controls in freshwater, and turtles held in water of either 5‰ salinity (S5) or 15‰ salinity (S15) with sampling at 6, 24, and 48 h and 30 days of exposure. When subjected to elevated salinities of 5 or 15‰, AMPK mRNA levels and AMPK enzyme activity increased strongly. In addition, the high expression of the peroxisome proliferator activated receptor-α (PPARα) transcription factor that, in turn, facilitated upregulation of target genes including carnitine palmitoyltransferase (CPT) and acyl-CoA oxidase (ACO). Furthermore, the expression of transcription factors involved in lipid synthesis such as the carbohydrate-responsive element-binding protein (ChREBP) and sterol regulatory element-binding protein 1c (SREBP-1c) was inhibited, and two of their target genes, acetyl-CoA carboxylase (ACC) and fatty acid synthase (FAS), were significantly decreased. Moreover, exposure to saline environments also increased plasma triglyceride (TG) content. Interestingly, the content of low-density lipoprotein cholesterol (LDL-C) and total cholesterol (TC) in plasma was markedly higher than the control in the S15 group after 30 days, which indicated that lipid metabolism was disrupted by chronic exposure to high salinity. These findings demonstrate that activation of AMPK might regulate lipid metabolism in response to salinity stress through the inhibition of lipid synthesis and promotion of lipid oxidation in the liver of T. s. elegans. This may be an important component of the observed salinity tolerance of these turtles that allow for invasion of brackish waters. |
| first_indexed | 2024-12-19T23:03:22Z |
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| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-19T23:03:22Z |
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| spelling | doaj.art-b6349986da284cca8995ce08bacf87a22022-12-21T20:02:27ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-07-011010.3389/fphys.2019.00962457087Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegansMeiling Hong0Na Li1Jiangyue Li2Weihao Li3Lingyue Liang4Qian Li5Runqi Wang6Haitao Shi7Haitao Shi8Kenneth B. Storey9Li Ding10Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, ChinaDepartment of Biology, Carleton University, Ottawa, ON, CanadaMinistry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou, ChinaAquatic animals have developed various mechanisms to live in either hyperionic or hypoionic environments, and, as such, not many species are capable of surviving in both. The red-eared slider turtle, Trachemys scripta elegans, a well-known freshwater species, has recently been found to invade and inhabit brackish water. Herein, we focus on some of the metabolic adaptations that are required to survive and cope with salinity stress. The regulation of the adenosine monophosphate (AMP)-activated protein kinase (AMPK), a main cellular “energy sensor,” and its influence on lipid metabolism were evaluated with a comparison of three groups of turtles: controls in freshwater, and turtles held in water of either 5‰ salinity (S5) or 15‰ salinity (S15) with sampling at 6, 24, and 48 h and 30 days of exposure. When subjected to elevated salinities of 5 or 15‰, AMPK mRNA levels and AMPK enzyme activity increased strongly. In addition, the high expression of the peroxisome proliferator activated receptor-α (PPARα) transcription factor that, in turn, facilitated upregulation of target genes including carnitine palmitoyltransferase (CPT) and acyl-CoA oxidase (ACO). Furthermore, the expression of transcription factors involved in lipid synthesis such as the carbohydrate-responsive element-binding protein (ChREBP) and sterol regulatory element-binding protein 1c (SREBP-1c) was inhibited, and two of their target genes, acetyl-CoA carboxylase (ACC) and fatty acid synthase (FAS), were significantly decreased. Moreover, exposure to saline environments also increased plasma triglyceride (TG) content. Interestingly, the content of low-density lipoprotein cholesterol (LDL-C) and total cholesterol (TC) in plasma was markedly higher than the control in the S15 group after 30 days, which indicated that lipid metabolism was disrupted by chronic exposure to high salinity. These findings demonstrate that activation of AMPK might regulate lipid metabolism in response to salinity stress through the inhibition of lipid synthesis and promotion of lipid oxidation in the liver of T. s. elegans. This may be an important component of the observed salinity tolerance of these turtles that allow for invasion of brackish waters.https://www.frontiersin.org/article/10.3389/fphys.2019.00962/fullTrachemys scripta eleganssalinity adaptationfatty acid oxidationlipid synthesislipid metabolism-related transcription factors |
| spellingShingle | Meiling Hong Na Li Jiangyue Li Weihao Li Lingyue Liang Qian Li Runqi Wang Haitao Shi Haitao Shi Kenneth B. Storey Li Ding Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegans Frontiers in Physiology Trachemys scripta elegans salinity adaptation fatty acid oxidation lipid synthesis lipid metabolism-related transcription factors |
| title | Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegans |
| title_full | Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegans |
| title_fullStr | Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegans |
| title_full_unstemmed | Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegans |
| title_short | Adenosine Monophosphate-Activated Protein Kinase Signaling Regulates Lipid Metabolism in Response to Salinity Stress in the Red-Eared Slider Turtle Trachemys scripta elegans |
| title_sort | adenosine monophosphate activated protein kinase signaling regulates lipid metabolism in response to salinity stress in the red eared slider turtle trachemys scripta elegans |
| topic | Trachemys scripta elegans salinity adaptation fatty acid oxidation lipid synthesis lipid metabolism-related transcription factors |
| url | https://www.frontiersin.org/article/10.3389/fphys.2019.00962/full |
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