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

Abstract

It has been proposed that the performance of lactating animals is limited by the capacity of the female to dissipate body heat - the 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.