Filling the Gap: Entirely Beige/Brite Adipose Tissues in One of the Smallest Mammals, Suncus etruscus

Abstract

Mammalian brown adipose tissue provides a means of non-shivering thermogenesis to defend normothermia in the cold by uncoupling protein 1 (UCP1) mediated uncoupling of mitochondrial respiration from ATP production. Apart from brown adipose tissue, thermogenic beige/brite adipocytes reside interspersed within white adipose tissue depots. In rodents, the number of beige/brite adipocytes is highly variable and adapts to thermogenic requirements. We here studied adipose tissue composition of the Etruscan shrew S. etruscus, an insectivore and one of the smallest known mammals with a consequently extreme thermogenic demand in its temperate habitat with cold winters. By dissection, phase contrast computer tomography, histology and mitochondrial enzyme activity assays, we mapped the distribution of adipose tissue depots in shrews from a research colony kept at room temperature. In similar anatomical locations as typically found in rodents, an especially large amount of brown adipose tissue concentrated to the interscapular and subscapular region, while white adipose tissue with a very high content of multilocular cells formed the inguinal and gluteal depots. Uniquely, shrews featured a large, interrenal adipose tissue that by visual inspection, mitochondrial density, fat content, UCP1 transcript abundance, histological analysis and mitochondrial enzyme activity appeared to be an intermediate between classical brown and very beige/brite adipose tissue. This unusual, centrally located depot expansively sheathed both the Vena cava inferior and the Aorta abdominalis, the two largest blood vessels, and must be assumed to provide considerable thermogenic capacity. In conclusion, we identified a novel adipose tissue depot with unique properties placing it in between very beige/brite and brown adipose tissue. Importantly, this finding fills in a conceptual gap within our understanding of adipose tissue plasticity previously thought to include a range from white to beige/brite on the one end, and brown on the other. Etruscan shrew fat depots, however, demonstrate the existence of a gapless continuum of white-to-brown characteristics. Functionally, the transitional, interrenal depot appears strategically placed to deliver heat into circulation via the penetrating, large blood vessels in an animal with extreme thermogenic demand.