Influence of Starvation on Biochemical, Physiological, Morphological, and Transcriptional Responses Associated with Glucose and Lipid Metabolism in the Liver of Javelin Goby (Synechogobius hasta).

Simple Summary: When faced with starvation, fish can consume energy reserves and adaptively modify the metabolic responses of main energy substrates for fundamental activity. Carbohydrates and lipids are mobilized preferentially in most fish under starvation. However, the mobilization of endogenous energy in starving fish varies with the species, tissue, and fasting duration. Liver tissue is the primary tissue for energy reserves in multiple fish, particularly lipid-associated components. Therefore, this study was conducted to investigate the phenotypic changes in physiological, metabolic, histological, and molecular characteristics of glucose and lipid metabolism in the liver of Synechogobius hasta experiencing different starvation periods. Hepatic glycogen and triglycerides were concurrently mobilized in S. hasta during starvation, which was accompanied by consistent changes in liver intermediary metabolism enzyme activities and an increase in liver antioxidant capacity to some extent. S. hasta livers exhibited evident vacuolations, larger intercellular spaces, and other microstructural abnormalities from the third day of starvation. Additionally, fasting not only transcriptionally attenuated glucose and lipid anabolism, but also enhanced the catabolic pathway and fatty acid transport in S. hasta liver. These findings may provide preliminary data for further assessing the energy strategy to cope with starvation and the underlying mechanism in S. hasta and other fish species. In this study, the influence of fasting on hepatic glucose and lipid metabolism was explored by examining biochemical, antioxidative, and morphological indicators and transcriptional expression in the liver of javelin goby (Synechogobius hasta) after 0, 3, 7, or 14 days of starvation. Marked reductions in hepatic glycogen and triglycerides occurred from the seventh day of starvation until the end of the trial (p < 0.05). However, no alterations in hepatic cholesterol or protein were detected throughout the entire experiment (p > 0.05). During fasting, the activities of pyruvate kinase, lactate dehydrogenase, and glycogen phosphorylase a all rose firstly and then fell (p < 0.05). The activities of hepatic fatty acid synthase and acetyl-CoA carboxylase were minimized to their lowest levels at the end of food deprivation (p < 0.05), while lipase was elevated after 7–14 days of fasting (p < 0.05). Catalase, glutathione, and the total antioxidative capacity were increased and maintained their higher values in the later stage of fasting (p < 0.05), whereas malondialdehyde was not significantly changed (p > 0.05). Hepatic vein congestion, remarkable cytoplasmic vacuoles, and irregular cell shape were present in S. hasta which endured 3–7 days of fasting and were less pronounced when food shortage was prolonged. In terms of genes associated with glucose and lipid metabolism, the hepatic phosphofructokinase gene was constantly up-regulated during fasting (p < 0.05). However, the mRNA levels of glycogen synthase and glucose-6-phosphatase were obviously lower when the food scarcity extended to 7 days or more (p < 0.05). Fatty acid synthase, stearoyl-CoA desaturase 1, and peroxisome proliferator-activated receptor γ were substantially down-regulated in S. hasta livers after 7–14 days of food deprivation (p < 0.05). However, genes involved in lipolysis and fatty acid transport were transcriptionally enhanced to varying extents and peaked at the end of fasting (p < 0.05). Overall, starvation lasting 7 days or more could concurrently mobilize hepatic carbohydrates and fat as energy resources and diminished their hepatic accumulation by suppressing biosynthesis and enhancing catabolism and transport, ultimately metabolically and structurally perturbing the liver in S. hasta. This work presents preliminary data on the dynamic characteristics of hepatic glucose and lipid metabolism in S. hasta in response to starvation, which may shed light on the sophisticated mechanisms of energetic homeostasis in fish facing nutrient unavailability and may benefit the utilization/conservation of S. hasta. [ABSTRACT FROM AUTHOR]