Abstract
Brown adipose tissue (BAT) function may depend on its anatomical location and developmental origin. Interscapular BAT (iBAT) regulates acute macronutrient metabolism, whilst perivascular BAT (PVAT) regulates vascular function. Although phenotypically similar, whether these depots respond differently to acute nutrient excess is unclear. Given their distinct anatomical locations and developmental origins and we hypothesised that iBAT and PVAT would respond differently to brief period of nutrient excess. Sprague-Dawley rats aged 12 weeks (n=12) were fed either a standard (10% fat, n=6) or high fat diet (HFD: 45% fat, n=6) for 72h and housed at thermoneutrality. Following an assessment of whole body physiology, fat was collected from both depots for analysis of gene expression and the proteome. HFD consumption for 72h induced rapid weight gain (c. 2.6%) and reduced serum non-esterified fatty acids (NEFA) with no change in either total adipose or depot mass. In iBAT, an upregulation of genes involved in insulin signalling and lipid metabolism was accompanied by enrichment of lipid-related processes and functions, plus glucagon and peroxisome proliferator-activated receptor (PPAR) signalling pathways. In PVAT, HFD induced a pronounced down-regulation of multiple metabolic pathways which was accompanied with increased abundance of proteins involved in apoptosis (e.g., Hdgf and Ywaq) and toll-like receptor signalling (Ube2n). There was also an enrichment of DNA-related processes and functions (e.g., nucleosome assembly and histone exchange) and RNA degradation and cell adhesion pathways. In conclusion, we show that iBAT and PVAT elicit divergent responses to short-term nutrient excess highlighting early adaptations in these depots before changes in fat mass.
Highlights
Adipose tissue function differs with its anatomical location and developmental origin [1].For instance, whilst interscapular brown adipose tissue shares its lineage with skeletal muscle (e.g., Myf5+), perivascular brown adipose tissue (PVAT) is thought to derive from vascular smooth muscle cells (e.g., SM22α+) [1,2]. Interscapular Brown adipose tissue (BAT) (iBAT) can play a role in whole body glucose, and lipid homeostasis as well as thermoregulation through the activation of uncoupling protein 1 (UCP1) which dissipatesNutrients 2019, 11, 1065; doi:10.3390/nu11051065 www.mdpi.com/journal/nutrientsNutrients 2019, 11, 1065 chemical energy as heat bypassing the conversion of ADP to ATP [3,4,5]
Despite perivascular BAT (PVAT) being phenotypically similar to iBAT, i.e., abundant in UCP1 and other thermogenic genes, its primary physiological role is the regulation of vascular function rather than systemic metabolism per se [2]
(Figure 1E) reflects a shift towards fat as the major fuel substrate in the high-fat diet (HFD) group. Despite this rapid weight gain, there were no differences in serum insulin, glucose or triglycerides, non-esterified fatty acids (NEFA) was reduced (Figure 1G–J)
Summary
Adipose tissue function differs with its anatomical location and developmental origin [1].For instance, whilst interscapular brown adipose tissue (iBAT) shares its lineage with skeletal muscle (e.g., Myf5+), perivascular brown adipose tissue (PVAT) is thought to derive from vascular smooth muscle cells (e.g., SM22α+) [1,2]. iBAT can play a role in whole body glucose, and lipid homeostasis as well as thermoregulation through the activation of uncoupling protein 1 (UCP1) which dissipatesNutrients 2019, 11, 1065; doi:10.3390/nu11051065 www.mdpi.com/journal/nutrientsNutrients 2019, 11, 1065 chemical energy as heat bypassing the conversion of ADP to ATP [3,4,5]. Despite PVAT being phenotypically similar to iBAT, i.e., abundant in UCP1 and other thermogenic genes, its primary physiological role is the regulation of vascular function rather than systemic metabolism per se [2]. Insulin resistance can be induced after 24h of a saturated-fatty acid (SFA) rich diet, with longer periods of overfeeding causing similar results to those seen in animal models [17]. Both iBAT and PVAT contain abundant UCP1 and express glycolytic/lipolytic genes [18], their response to brief nutrient excess is unclear. We determined whether iBAT and PVAT differ in their response to a short-term (i.e., 72h) caloric surplus
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