Ontogeny and Thermogenic Role for Sternal Fat in Female Sheep

Abstract

Brown adipose tissue acting through a unique uncoupling protein (UCP1) has a critical role in preventing hypothermia in newborn sheep but is then thought to rapidly disappear during postnatal life. The extent to which the anatomical location of fat influences postnatal development and thermogenic function in adulthood, particularly following feeding, is unknown, and we examined both in our study. Changes in gene expression of functionally important pathways (i.e., thermogenesis, development, adipogenesis, and metabolism) were compared between sternal and retroperitoneal fat depots together with a representative skeletal muscle over the first month of postnatal life, coincident with the loss of brown fat and the accumulation of white fat. In adult sheep, implanted temperature probes were used to characterize the thermogenic response of fat and muscle to feeding and the effects of reduced or increased adiposity. UCP1 was more abundant in sternal fat than in retroperitoneal fat and was retained only in the sternal depot of adults. Distinct differences in the abundance of gene pathway markers were apparent between tissues, with sternal fat exhibiting some similarities with muscle that were not apparent in the retroperitoneal depot. In adults, the postprandial rise in temperature was greater and more prolonged in sternal fat than in retroperitoneal fat and muscle, a difference that was maintained with altered adiposity. In conclusion, sternal adipose tissue retains UCP1 into adulthood, when it shows a greater thermogenic response to feeding than do muscle and retroperitoneal fat. Sternal fat may be more amenable to targeted interventions that promote thermogenesis in large mammals.

Exercise counteracts the homeostatic decrease in thermogenesis caused by caloric restriction in sheep

“…The current study demonstrates that moderate food restriction decreases thermogenesis specifically in adipose tissue, with little effect in skeletal muscle. This contrasts our previous work in sheep showing that chronic food restriction and substantial weight loss decreases thermogenesis in adipose tissue (sternal and retroperitoneal) and skeletal muscle (12). This discrepancy is most likely due to the more severe undernutrition imposed in the study by Henry et al (12), where animals were food restricted to 50% of ad libitum for 12 mo, compared with the current study, where we imposed 30% food restriction for 4 wk.…”

“…Tissue temperature profiles demonstrated that the greatest effect of caloric restriction occurred at night, which is consistent with previously published work (12). We therefore calculated the mean overnight temperature between 2:00 and 6:00 AM.…”

“…We have shown that regular moderate exercise restores night-time thermogenesis in animals on mild dietary restriction. Caloric restriction reduces thermogenesis in BAT of female sheep, as in other species (30)(31)(32)(33)(34), which constitutes a homeostatic mechanism to reduce energy expenditure in response to energy deficit, offsetting the effect of weight loss (12,35). We have demonstrated that implementation of an exercise regime counteracts this inhibitory effect of food restriction on thermogenesis in sternal and retroperitoneal adipose tissues.…”

“…Indeed, reduced thermogenesis is a key component contributing to the decrease in energy expenditure (11). In sheep, low body weight is associated with a reduction in BAT and skeletal muscle thermogenesis, which occurs primarily across the overnight period when animals are resting and sedentary (12). In obese rats, weight regain in response to food restriction is attenuated by exercise due to the lowering of the steady-state body weight (38).…”

“…Furthermore, inherent variation in thermogenesis contributes to the ability of an individual to lose weight (9,10). Weight loss in sheep and humans leads to a long-term reduction in thermogenesis (11,12), which is sustained for at least 1-2 yr after weight loss. Thus, strategies to counteract such a reduction in thermogenesis may assist in maintaining weight loss.…”