Targets for TNFα-induced lipolysis in gilthead sea bream(Sparus aurata L.) adipocytes isolated from lean and fat juvenile fish

Abstract

SUMMARYThe present study aimed to analyze adiposity heterogeneity and the role of liver X receptor (LXRα) and peroxisome proliferatoractivated receptors (PPARs) as targets of tumour necrosis factor-α (TNFα) in gilthead sea bream (Sparus aurata L.). The screening of 20 fish at the beginning of the warm season identified two major groups with fat and lean phenotypes. Fat fish showed increased liver and mesenteric fat depots. This increased adiposity was concurrent in the adipose tissue to enhanced expression of lipoprotein lipase (LPL) whereas mRNA levels of the hormone-sensitive lipase (HSL) remained almost unchanged. The resulting LPL/HSL ratio was thereby highest in fat fish, which suggests that this group of fish has not reached its peak fat storage capacity. This is not surprising given the increased expression of PPARγ in the absence of a counter-regulatory raise of TNFα. However, this lipolytic cytokine exerted dual effects in primary adipocyte cultures that differ within and between lean and fat fish. One set of fat fish did not respond to TNFα treatment whereas a second set exhibited a lipolytic response (increased glycerol release) that was apparently mediated by the downregulated expression of PPARβ. In lean fish, TNFα exerted a strong and nontranscriptionally mediated lipolytic action. Alternatively, TNFα would inhibit lipid deposition via the downregulated expression of adipogenic nuclear factors (PPARγ and LXRα). TNFα targets are therefore different in fish with lean and fat phenotypes, which is indicative of the complex network involved in the regulation of fish lipid metabolism.

Regulation of lipid metabolism and peroxisome proliferator-activated receptors in rainbow trout adipose tissue by lipolytic and antilipolytic endocrine factors

“…In mammals and, it would appear, fish, PPARg is highly expressed in adipose tissue and acts as a promoter of fat storage and adipocyte differentiation [21,24,58]. In keeping with these findings, we found that insulin administration upregulated this PPAR isotype highly significantly in trout adipose tissue and in in vitro cell preparations, in line with the prolipogenic actions of this hormone.…”

“…This modulation of PPAR expression by TNFa was not observed in vivo, but this is not surprising given that the effects of TNFa on lipolysis and PPAR expression in adipose tissue in gilthead sea bream varied notably depending on the physiological condition of the fish. Specifically, the effects of TNFa on adipocytes differed in lean and fat fish [24].…”

“…TNFa has been shown to promote lipolysis in isolated adipocytes of rainbow trout and gilthead sea bream [23,24]. The mechanisms underlying the action of TNFa on lipolysis are complex, and modulation of the expression of peroxisome proliferator-activated receptors (PPARs) appears to be significant [24]. There are 3 known isotypes in mammals and fish, PPARa, b, and g, and these are expressed differentially in various tissues [25][26][27].…”

Insulin Stimulates Lipogenesis and Attenuates Beta‐Oxidation in White Adipose Tissue of Fed Rainbow Trout

“…As the enzymatic machinery responsible for lipid mobilization and deposition in fish, WAT is similar to that found in mammals [6], and both lipoprotein lipase (LPL) [11,12] and hormone-sensitive lipase (HSL) [13,14] have been characterized. However, other aspects of lipid metabolism such as the lipogenic and lipid oxidation potential have not been fully explored in fish WAT.…”

Tumor necrosis factor alpha is a potent regulator in fish adipose tissue

“…TNFα has been identified in several fish species and characterized as a limiting factor of lipid deposition in gilthead sea bream (Cruz-Garcia et al, 2009b;Saera-Vila et al, 2007). TNFα affects adipocyte function in rainbow trout and gilthead sea bream, and inhibits the differentiation of rainbow trout preadipocytes (Albalat et al, 2005b;Bouraoui et al, 2008;Saera-Vila et al, 2007).…”