Hypothalamic fatty acid sensing in Senegalese sole (Solea senegalensis): response to long-chain saturated, monounsaturated, and polyunsaturated (n-3) fatty acids

Abstract

We assessed the presence of fatty acid (FA)-sensing mechanisms in hypothalamus of Senegalese sole (Solea senegalensis) and investigated their sensitivity to FA chain length and/or level of unsaturation. Stearate (SA, saturated FA), oleate (OA, monounsaturated FA of the same chain length), α-linolenate [ALA, a n-3 polyunsaturated fatty acid (PUFA) of the same chain length], and eicosapentanoate (EPA, a n-3 PUFA of a larger chain length) were injected intraperitoneally. Parameters related to FA sensing and neuropeptide expression in the hypothalamus were assessed after 3 h and changes in accumulated food intake after 4, 24, and 48 h. Three FA sensing systems characterized in rainbow trout were also found in Senegalese sole and were activated by OA in a way similar to that previously characterized in rainbow trout and mammals. These hypothalamic FA sensing systems were also activated by ALA, differing from mammals, where n-3 PUFAs do not seem to activate FA sensors. This might suggest additional roles and highlights the importance of n-3 PUFA in fish diets, especially in marine species. The activation of FA sensing seems to be partially dependent on acyl chain length and degree of saturation, as no major changes were observed after treating fish with SA or EPA. The activation of FA sensing systems by OA and ALA, but not SA or EPA, is further reflected in the expression of hypothalamic neuropeptides involved in the control of food intake. Both OA and ALA enhanced anorexigenic capacity compatible with the activation of FA sensing systems.

Orally administrated fatty acids enhanced anorectic potential but did not activate central fatty acid sensing in Senegalese sole post-larvae

“…A similar effect was also suggested in juveniles of the same species after intraperitoneal (i.p.) injection with FA (Conde-Sieira et al, 2015), although there were important differences in the responses of the different neuropeptides and FAs assessed. For instance, in the present experiment there was no response of cart2b or agrp2 to any treatment, in contrast to juvenile sole where cart2b and agrp2 were significantly regulated (increased and decreased, respectively) in the hypothalamus following i.p.…”

“…In previous studies, we characterized the presence and function of fatty acid (FA)-sensing systems in the hypothalamus of the teleost fish rainbow trout (Oncorhynchus mykiss) (Librán-Pérez et al, 2012, 2013, 2014a,b, 2015 and Senegalese sole (Solea senegalensis Kaup) (Conde-Sieira et al, 2015), which are comparable in many aspects to those in mammals (Blouet and Schwartz, 2010). These systems respond to increased levels of unsaturated long-chain FAs such as oleate (OA, C18:1 n-9) and correlate with the expression of neuropeptides involved in the control of food intake (Librán-Pérez et al, 2012, 2014a.…”

“…FA-sensing mechanisms are based on: (i) FA metabolism via carnitine palmitoyltransferase 1 (CPT-1) inhibition to import FA-coenzyme-A (CoA) into the mitochondria for oxidation; (ii) binding to FA translocase (FAT/CD36) and modulation of the transcription factors peroxisome proliferator-activated receptor type α (PPARα) and sterol regulatory element-binding protein type 1c (SREBP1c); and (iii) production of reactive oxygen species in the mitochondria, resulting in inhibition of ATP-dependent inward rectifier potassium channel (K ATP ) activity (Soengas, 2014). The activation of these systems relates to the inhibition of the orexigenic factors agouti-related protein (AgRP) and neuropeptide Y (NPY), and the enhancement of the anorexigenic factors cocaine-and amphetamine-related transcript (CART) and pro-opiomelanocortin (POMC) (Librán-Perez et al, 2012, 2014aConde-Sieira et al, 2015), ultimately leading to decreased food intake.…”

“…Furthermore, hypothalamic FA-sensing systems in Senegalese sole were activated by α-linolenate (ALA, C18:3 n-3) but not by eicosapentaenoate (EPA, C20:5 n-3) (Conde-Sieira et al, 2015), indicating that the response might be specific to certain PUFAs. Therefore, both the level of unsaturation and the chain length of the FA seem to be important factors for the hypothalamic sensing capacity, at least in Senegalese sole juveniles, but are probably not the only factors involved.…”

“…Studies in fish regarding FA-sensing systems and control of food intake have only been carried out in juveniles and adults so far (Libran-Pérez et al, 2012, 2014aConde-Sieira et al, 2015). However, it is of great importance to clearly establish when appetite regulation becomes functional in fish larvae, particularly in species of commercial interest to aquaculture.…”