Adipocyte metabolism and cellularity are related to differences in adipose tissue maturity between Holstein and Charolais or Blond d'Aquitaine fetuses1

Abstract

This paper reports the metabolic and morphological characteristics of bovine adipose tissue (AT) at end of fetal life and its variability with breed and anatomical site of AT. Our hypothesis was that, in cattle, end-of-fetal-life differences in adipocyte number, size, and histology may account for differences in AT maturity. To address this question, perirenal and intermuscular AT were sampled from Charolais, Blond d'Aquitaine, and Holstein fetuses at 260 d postconception. Holstein fetuses showed greater leptin mRNA abundance, which is consistent with the greater perirenal AT weight (P = 0.03) than Blond d'Aquitaine fetuses. Compared with Blond d'Aquitaine or Charolais fetuses, Holstein fetuses had larger (P< 0.001) adipocytes, greater (P < 0.05) activities of enzymes involved in de novo fatty acid (FA) synthesis (FA synthase, glucose-6-phosphate dehydrogenase, malic enzyme) and FA esterification (glycerol-3-phosphate dehydrogenase), and greater (P = 0.06, P = 0.10, P < 0.001) mRNA abundance for lipolytic enzymes (hormone-sensitive lipase and adipose triglyceride lipase) and uncoupling protein 1 in both perirenal and intermuscular AT. This indicates increased FA turnover in Holstein adipocytes through FA storage, mobilization, and oxidation pathways. Whatever the breed, adipocytes were smaller in perirenal AT than intermuscular AT. Whatever the breed or anatomical site, bovine AT at 260 d postconception contained predominantly unilocular adipocytes believed to be white adipocytes together with a few multilocular brown adipocytes. We conclude that the greater metabolic and morphologic maturity of adipocytes from Holstein than Blond d'Aquitaine and Charolais fetuses may contribute to the greater thermogenic aptitude of Holstein newborns. Moreover, the presence of both white and brown adipocytes at the end of fetal life highlights the complexity of AT structure and may indicate that the cellular and functional heterogeneity of AT repeatedly observed postnatally has a developmental origin.

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

“…Foetuses were collected at 180 dpc (n 5 5 Charolais and n 5 3 Blond d'Aquitaine), 210 dpc (n 5 5 Charolais and n 5 3 Blond d'Aquitaine) and 260 dpc (n 5 10 Charolais and n 5 3 Blond d'Aquitaine; in INRA herds, full gestation averages 287 and 290 days for primiparous Charolais and Blond d'Aquitaine cows, respectively) from cows slaughtered at the INRA's experimental abattoir. Foetuses at 260 dpc were the same as those previously used to compare three breeds for one part of the parameters described in this study (Taga et al, 2011). At slaughter, foetal AT samples were collected from intermuscular depots between the main forequarter and hindquarter muscles.…”

“…For paraffin embedding, samples were dehydrated in ethanol, cleared in xylene and embedded in melted paraffin at 608C. Sections of 4-mm thickness were mounted on clean slides, counterstained with haematoxylin and eosin, and examined by light microscopy as previously described (Taga et al, 2011). AT was digitized at magnifications of 103, 203, 403 and 1003.…”

“…The abundances of FABP4, LIPE, PNPLA2, PLIN, UCP1, UCP2, DIO2 and ADIPOQ mRNA plus the three housekeeping genes TBP (TATA box-binding protein), UXT (ubiquitously expressed transcript) and EIF3K (eukaryotic translation initiation factor 3, subunit k) were quantified as previously reported (Taga et al, 2011). Plasma LEP analysis Intracardiac foetal blood was sampled on EDTA at slaughter.…”

“…It has been shown that in the last third of foetal growth or at birth, bovine perirenal AT exhibits in vitro lipogenesis from acetate and palmitate (Landis et al, 2002), expresses lipoprotein lipase (LPL; Hocquette et al, 2006) and uncoupling protein 1 (UCP 1; Casteilla et al, 1989), and contains multilocular adipocytes with a high number of mitochondria that highlight the presence of brown adipocytes in foetal AT (Alexander et al, 1975;Landis et al, 2002). However, we recently reported that at the end of foetal life (260 dpc), bovine perirenal and intermuscular AT are a mixture of brown and mainly white adipocytes (Taga et al, 2011). It is not yet clear whether intermuscular AT from appearance onwards expresses the cellular and molecular features of primarily brown AT or of both brown and white AT.…”

“…The main objective of this study was to characterize intermuscular AT throughout foetal growth, in order to complement cellular and molecular features that we previously reported at 260 dpc (Taga et al, 2011) by cellular and molecular features assayed at 180 and 210 dpc. This study was conducted in two bovine breeds chosen for their large use for meat production from growing cattle in France and because of their differences in muscular development and adiposity during the postnatal life (Picard et al, 2010).…”