Foetal bovine intermuscular adipose tissue exhibits histological and metabolic features of brown and white adipocytes during the last third of pregnancy

Abstract

This study reports the metabolic and morphological characteristics of bovine intermuscular adipose tissue (AT) throughout foetal growth. Our hypothesis was that the histological and molecular features of intermuscular AT would be different from those previously reported for foetal perirenal AT, based on its anatomical location near the muscle and the recent identification of two distinct adipocyte precursors in mouse AT depending on their locations. To address this question, intermuscular AT was sampled from Charolais and Blond d'Aquitaine foetuses at 180, 210 and 260 days post conception (dpc). The two bovine breeds were chosen because of the higher adiposity of Charolais than Blond d'Aquitaine cattle during the postnatal life. Regardless of the breed, adipocyte volume increased slightly (138%, P , 0.01) with increasing foetal age. This was concomitant with a decrease ( P , 0.05) in the activity of enzymes involved in de novo fatty acid (FA) synthesis (FA synthase and glucose-6-phosphate dehydrogenase) and FA esterification (glycerol-3-phosphate dehydrogenase) when expressed per million adipocytes, and with an increase ( P < 0.01) in mRNA abundances for uncoupling protein 1, adiponectin and leptin (LEP) between 180 and 260 dpc. No difference was observed in the adipocyte volume between breeds, which was consistent with the lack of major between-breed differences in mRNA abundances or activities of enzymes involved in lipid metabolism. The mRNA abundance of lipoprotein lipase was maintained across ages, suggesting a storage of circulating FA rather than of FA synthesized de novo. Plasma LEP increased with foetal age, but only in the Charolais breed (171%, P < 0.01), and was two-to threefold higher in Charolais than Blond d'Aquitaine foetuses. Regardless of the breed, bovine intermuscular AT contained predominantly unilocular adipocytes believed to be white adipocytes that were larger at 260 dpc than at 180 dpc. These data thus challenge current concepts of the largely brown nature of bovine foetal AT (based on histological and metabolic features of perirenal AT as previously reported a few days before or after birth).

Intermuscular and intramuscular adipose tissues: Bad vs. good adipose tissues

“…47 In bovine fetuses, these INTMF brown adipocytes appear to convert into white INTMF adipocytes later in life. [47][48][49] In these two studies, INTMF brown adipogenesis was not examined due to the absence of distinguishable IM fat in bovine fetal muscle. There is no evidence of INTMF/IM brown adipogenesis in pigs.…”

“…48,49 Adipogenesis is briefly separated into two stages: determination and differentiation. 50 Recently, zincfinger protein Zfp423 was identified as a transcriptional factor responsible for the adipogenic commitment of progenitor cells, or adipocyte determination.…”

“…Myogenic lineage cells further develop into muscle fibers, INTMF/IM brown adipocytes, and satellite cells, while fibro/adipogenic lineage cells develop into the stromal vascular fraction of muscle where white adipocytes, fibroblasts and resident fibro/adipogenic progenitors reside (FAPs, the counterpart of satellite cells). 48,53,88 These resident FAPs become largely quiescent and form the stem cell pool for later adipogenesis and fibrogenesis in mature muscle. [89][90][91] Because both myogenic and fibro/adipogenic cells are from the same pool of progenitor cells, the initial myogenic or fibro/adipogenic commitment can be considered as a competitive process, with enhancing myogenesis reducing fibro/adipogenesis, and vice versa.…”

Preadipocyte and Adipose Tissue Differentiation in Meat Animals: Influence of Species and Anatomical Location

“…A recent proteomics study of fetal bovine perirenal BAT using 2D gel electrophoresis and mass spectrometry identified proteins that may regulate brown adipocyte precursor cell-cycle progression and/or apoptosis or delay differentiation induced by PPARg (30,31). Furthermore, increases in adipocyte volume and number from days 110 to 260 of fetal development coincided with changes in the abundance of more than one hundred proteins (30,31).…”

“…Furthermore, increases in adipocyte volume and number from days 110 to 260 of fetal development coincided with changes in the abundance of more than one hundred proteins (30,31). However, increased upregulation of several proteins considered characteristic of WAT, coupled with the abundance of unilocular adipocytes at days 180 and 260, led the authors to suggest that fetal bovine perirenal BAT may be more like WAT than BAT (30,31).…”