Negative correlation between milk production and brown adipose tissue gene expression in lactating mice

Abstract

SUMMARYIt has been proposed that the performance of lactating animals is limited by the capacity of the female to dissipate body heatthe heat dissipation limit (HDL) theory. This theory predicts that milk production might be constrained not by intrinsic properties of the mammary glands but rather by competitive heat production such as thermogenesis in brown adipose tissue (BAT). To test this prediction, we measured the expression of genes linked to thermogenesis in BAT of lactating laboratory mice. The applicability of BAT gene expression to reflect thermogenic activity of BAT was confirmed by a positive relationship between expression levels of several BAT genes (summarised by the first principal component following principal component analysis) and daily energy expenditure in virgin mice. Milk production at peak lactation was strongly and negatively associated with the expression of thermogenic genes in BAT. Downregulation of these genes during lactation was correlated with low levels of circulating leptin and high levels of circulating prolactin. Our results are consistent with the HDL theory. However, we cannot discount the converse interpretation that milk production may reduce BAT activity. If the reduction in BAT activity does facilitate increased milk production, then reducing the heat generated by competitive processes may be a more productive route to increase lactational performance than attempts to improve mammary gland performance in isolation from the other body systems. Supplementary material available online at

Limits to sustained energy intake XIX: A test of the heat dissipation limitation hypothesis in Mongolian gerbils (Meriones unguiculatus)

“…In the prolactin group this was significantly lower than that in the saline group. This reduction is consistent with the model suggested by Król et al (Król et al, 2011), where gene expression in BAT during lactation appeared to be responsive to both prolactin and leptin levels. Normally in lactation the reduced heat production by BAT is more than compensated for by the heat production associated with milk synthesis.…”

Brown adipose tissue: physiological function and evolutionary significance

“…In this scenario, BAT represents a potential driving force for the evolution of endothermy. This role of BAT during reproduction is in contrast to modern eutherian mammals with higher body temperatures, where BAT is switched off, possibly to avoid overheating (Trayhurn et al 1982;Trayhurn 1983;Trayhurn and Wusteman 1987;Król et al 2011;Yang et al 2013). However, the notion that the endothermic temperature of the tenrec may resemble optimal temperatures for gamete incubation may also be extrapolated from other vertebrate species, e.g.…”

Limits to sustained energy intake XX: body temperatures and physical activity of female mice during lactation

“…Alternatively, or additionally, the elevation in T b might be associated indirectly with the hormonal secretions that induce and maintain milk production such as prolactin (Svennersten-Sjaunja and Olsson, 2005) and other hormonal changes that are linked to lactation such as the reduced levels of circulating leptin (Cui et al, 2011;Król et al, 2011). In fact, prolactin appears to be strongly positively correlated with T b during exertional heat stress (Pitsiladis et al, 2002;Wright et al, 2012), although in this case it appears the causal relationship is that elevated temperature stimulates prolactin release (Low et al, 2005) and not the reverse.…”