Maternal overnutrition enhances mRNA expression of adipogenic markers and collagen deposition in skeletal muscle of beef cattle fetuses1

Abstract

Twenty-four pregnant Nellore cows were randomly assigned into 2 feeding level groups (control [CTL]; fed 1.0 times the maintenance requirement; n = 12; and overnourished [ON]; fed at 1.5 times the maintenance requirement; n = 12) to evaluate effects of maternal overnutrition on fetal skeletal muscle development. Cows were slaughtered at 135, 190, and 240 d of gestation and samples of fetal LM were collected for analysis of mRNA expression analysis and for histological evaluation of collagen content and number of muscle cells. There was no interaction between gestational period and maternal nutrition for the variables evaluated (P > 0.05). The mRNA expression of Cadherin-associated protein, β 1 (β-catenin) tended to be greater in fetuses from ON cows (P = 0.08), while myogenic differentiation 1 (MyoD; P = 0.56), myogenin (MyoG; P = 0.70), and the number of muscle cells (P = 0.90) were not affected by maternal overnutrition. Gestational period did not affect the mRNA expression of β-catenin (P = 0.60) and MyoG (P = 0.21). The mRNA expression of MyoD tended to increase with days of gestation (P = 0.06). The mRNA expression of zinc finger protein 423 (Zfp423; P < 0.0001), C/EBPα (P = 0.01), and PPARγ (P < 0.0001) were enhanced in ON fetuses. No effects of days of gestation were observed for mRNA expression of Zfp423 (P = 0.75) and C/EBPα (P = 0.48). The mRNA expression of PPARγ in fetuses at 190 d of gestation tended to be greater than those at 135 and 240 d of gestation (P = 0.06). The mRNA expression of transforming growth factor β (TGF-β; P < 0.0001), collagen type III, α I (COL3A1; P < 0.0001), and collagen content (P = 0.01) were increased in ON fetuses. Gestational period did not affect the mRNA expression of collagen type I, α I (COL1A1; P = 0.65). The mRNA expression of COL3A1 (P = 0.09) in fetuses at 190 d of gestation tended to be greater than fetuses at 135 and 240 d of gestation. The mRNA expression of TGF-β in fetuses at 190 d of gestation was greater than in fetuses at 135 d of gestation (P = 0.03), and the values observed in fetuses at 240 d of gestation did not differ from the other gestational time points. The least value of collagen content (P = 0.01) was observed in fetuses at 135 d of gestation, and no differences were observed among the other gestational time points. These data shows that maternal overnutrition enhances fibrogenesis and likely adipogenesis without compromising myogenesis in fetal skeletal muscle of cattle.

Foetal development of skeletal muscle in bovines as a function of maternal nutrition, foetal sex and gestational age

“…We observed an increase in expression of CTNNB1 mRNA associated with an increased number of myocytes at 139 days of gestation in the group of maternal ON; although, no differences were observed among MN levels in the subsequent time points of gestation. In a previous study using beef cattle as a model, maternal overnutrition tended to decrease gene expression of CTNNB1 (Duarte et al., ), contrary to what we observed in this study. Perhaps, this may suggest that maternal nutrition affects differently the foetal muscular development in breeds selected for beef production over cross‐bred animals composed of dairy and beef breeds, as the animals used in this study was Holstein x Gyr cross‐bred cows.…”

“…These findings are in agreement with those previously observed by Duarte et al. () in beef cattle foetuses and revised by Du et al. () using data from studies in sheep, rodents and humans.…”

“…Such scenario raises questions and need of more foetal programming studies in beef systems as a model to better understand how manipulation of the intra‐uterine development minimises environmental effects on the offspring performance throughout their post‐natal life. Therefore, considerably research has shown that maternal nutrition during pregnancy alters intestinal (Duarte et al., ; Hammer et al., ; Meyer et al., ; Prezotto et al., ; Reed et al., ; Trahair, DeBarro, Robinson, & Owens, ; Yanusova et al., ) and muscular (Du et al., ; Duarte et al., ; Vonnahme, ; Wu, Bazer, Wallace, & Spencer, ) development of the ruminants' foetuses with effects in muscle and internal organs development that can be permanent (Underwood et al., ; Wu et al., ). Moreover, it has also been suggested that maternal nutrition may program the mesenchymal stem cells in the skeletal muscle to undergo adipo/fibrogenic differentiation, which predisposes the offspring to intramuscular fat deposition later in life (Du et al., ).…”

Expression of genes involved in adipogenesis and lipid metabolism in subcutaneous adipose tissue and longissimus muscle in low-marbled Pirenaica beef cattle

“…However, no differences in IMF content were observed between the age and dietary treatment groups in this study; and, though caution is called for, the estimated differences seem to be ascribable to gene expression. Adipogenic and lipid metabolism gene expression quantified from mRNA extracted from muscle has, for instance, previously been associated with regulation of these processes in IMF (Jeong et al, 2013, Duarte et al, 2014, Moisá et al, 2014.…”

Review: Animal model and the current understanding of molecule dynamics of adipogenesis

“…Skeletal muscle is derived from the mesoderm and is postnatally surrounded by small multipotent myogenic satellite cells (SC) that play an important role in muscle hypertrophy and regeneration (Kook et al, 2006;Lee et al, 2012;Duarte et al, 2014). SC are multipotent cells capable of transdifferentiating into intramuscular adipocytes when exposed to local cellular signaling (Taylor-Jones et al, 2002;Singh et al, 2007;Lee et al, 2012;Ryan et al, 2013).…”