Metabolic response in liver and Brockmann bodies of rainbow trout to inhibition of lipolysis; possible involvement of the hypothalamus–pituitary–interrenal (HPI) axis

Abstract

We previously demonstrated in rainbow trout that the decrease in circulating levels of fatty acid (FA) induced by treating fish with SDZ WAG 994 (SDZ) induced a counter-regulatory response in which the activation of the hypothalamus-pituitary-interrenal (HPI, equivalent to mammalian hypothalamus-pituitary-adrenal) axis was likely involved. This activation, probably not related to the control of food intake through FA sensor systems but to the modulation of lipolysis in peripheral tissues, liver and Brockmann bodies (BB, the main site of pancreatic endocrine cells in fish), would target the restoration of FA levels in plasma. To assess this hypothesis, we lowered circulating FA levels by treating fish with SDZ alone, or SDZ in the presence of metyrapone (an inhibitor of cortisol synthesis). In liver, the changes observed were not compatible with a direct FA-sensing response but with a stress response, which allows us to suggest that the detection of a FA decrease in the hypothalamus elicits a counter-regulatory response in liver, resulting in an activation of lipolysis to restore FA levels in plasma. The activation of these metabolic changes in liver could be attributable to the activation of the HPI axis and/or to the action of sympathetic pathways. In contrast, in BB, changes in circulating FA levels induce changes in several parameters compatible with the function of FA-sensing systems informing about the decrease in circulating FA levels.

Effects of insulin treatment on the response to oleate and octanoate of food intake and fatty acid–sensing systems in rainbow trout

“…If insulin treatment enhances FA-sensing response in hypothalamus, a strong inhibitory signal would therefore arrive to the liver resulting in a potentiation of the responses elicited by FA alone. In BB, we had previously reported that FA-sensing systems present in this tissue respond directly to changes in circulating levels of OL and OCT [8,10,12] although they could be influenced by endocrine systems such as insulin and previous hypothalamic FA sensing [14,15]. In the present study, we obtained information regarding the modulatory action of insulin on FA-sensing response in BB.…”

“…We also evaluated in hypothalamus, liver, and BB concentrations of FA, triglyceride, total lipid, glucose, and glycogen (only in liver), as well as variables related to putative FA-sensing systems based on (1) FA metabolism, such as activities of fatty acid synthase (FAS), malonyl-CoA decarboxylase activity (MCD; only in liver), ATPcitrate lyase (ACLY; only in hypothalamus), and CPT-1, and mRNA abundance of acetyl-CoA carboxylase (ACC; only in hypothalamus), ACLY, CPT-1a (in BB), CPT-1b (in BB), CPT-1c (hypothalamus), and FAS; (2) binding to FAT/CD36 and further modulation of transcription factors, such as mRNA abundance of FAT/CD36, PPARa, SREBP1c, and liver X receptor a (LXRa); and (3) mitochondrial activity, such as mRNA abundance of mitochondrial uncoupling protein 2a (UCP2a), hydroxyacyl-CoA dehydrogenase (HOAD), inward rectifier K þ channel pore type 6.x-like (Kir6.x-like), and sulfonylurea receptor-like (SUR-like; only in liver). These variables have been previously reported to change in the same species in response to increased levels of OL or OCT [8][9][10][11][12][13][14][15][16].…”

“…In liver, we had previously observed that most changes displayed by FA-sensing systems in response to increased levels of OL or OCT were the result of previous hypothalamic FA sensing [12,14,15] resulting in increased outflow arriving to the liver via vagal and/or splanchnic pathways. In general, most of the changes observed in liver indicate that insulin treatment potentiates the effect of both OL and OCT alone on FA-sensing systems.…”

“…In fish, in previous studies in rainbow trout (Oncorhynchus mykiss Walbaum) [8][9][10][11][12][13][14][15][16], we have characterized in hypothalamus, liver, and Brockmann bodies (BB; main accumulation of pancreatic endocrine tissue in this species) the presence and functioning of putative FA-sensing systems. These systems respond to changes not only in a LCFA such as oleate (OL) but, unlike mammals, also in a MCFA-like octanoate (OCT) [16] and are related to the control of FI (hypothalamus), hormone release (BB), or metabolic homeostasis (liver).…”

Nutrient Sensing Systems in Fish: Impact on Food Intake Regulation and Energy Homeostasis

“…A similar experimental approach in rainbow trout also resulted in the inhibition of fatty acid sensing systems in hypothalamus, BB, and liver, and these changes apparently relate to the activation of hypothalamus-pituitary-interrenal (HPI) axis (Librán-Pérez et al, 2014b, 2015d). …”