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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Physiol. | doi: 10.3389/fphys.2019.00962

AMPK signaling regulates lipid metabolism in response to salinity stress in the red-eared slider turtle Trachemys scripta

 Meiling Hong1, Na Li1, Jiangyue Li1, Weihao Li1, Lingyue Liang1, Qian Li1, RunQi Wang1, Haitao Shi1, 2, Kenneth B. Storey3 and  Li Ding1*
  • 1Hainan Normal University, China
  • 2Chengdu Institute of Biology (CAS), China
  • 3Department of Biology, Faculty of Science, Carleton University, Canada

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 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 and 15‰ salinity (S15) with sampling at 6 h, 24 h, 48 h and 30 d of exposure. When subjected to elevated salinities of 5‰ or 15‰, AMPK mRNA levels and AMPK enzyme activity increased strongly. Salinity-activated AMPK promoted the 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). Elevated AMPK also led to inhibition 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), as well as significantly decreasing two of their target genes, acetyl-CoA carboxylase (ACC) and fatty acid synthase (FAS). 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 serum were markedly higher than control levels 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 regulates 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.

Keywords: Trachemys scripta elegans, salinity adaptation, fatty acid oxidation, Lipid synthesis, lipid metabolism-related transcription factors

Received: 28 Feb 2019; Accepted: 11 Jul 2019.

Edited by:

Eduardo L. Ballester, Federal University of Paraná, Brazil

Reviewed by:

Min Jin, Ningbo University, China
Matheus D. Baldissera, Universidade Federal de Santa Maria, Brazil  

Copyright: © 2019 Hong, Li, Li, Li, Liang, Li, Wang, Shi, Storey and Ding. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Li Ding, Hainan Normal University, Haikou, China, dingli@hainnu.edu.cn