Delayed muscle development in small pig fetuses around birth cannot be rectified by maternal early feed restriction and subsequent overfeeding during gestation

Abstract

Intrauterine variations in nutrient allowance can alter body composition and tissue features of the porcine offspring around birth. This study aimed to determine the effects of fetal weight variations between littermates and of maternal dietary regimen during gestation on fetal muscle traits just before birth. Fourteen pregnant gilts were reared under a conventional (control, CTL; n = 7) or an experimental (treatment, TRT; n = 7) dietary regimen during gestation. The dietary treatment provided 70% of the protein and digestible energy contents of the CTL diet during the first 70 days of gestation and then, 115% of the protein and digestible energy contents up to farrowing. At 110 days of gestation, sows were sacrificed and one fetus having a low (824 ± 140 g) and one having a normal (1218 ± 192 g) BW per litter were sampled. Irrespective of maternal dietary regimen, the longissimus muscle of the small fetuses exhibited higher expression levels of DLK1/Pref1 and NCAM1/CD56, two genes known to be downregulated during normal skeletal muscle development. Expression levels of the embryonic isoform of the myosin heavy chain (MyHC), both at the mRNA and at the protein levels, were also higher in small fetuses. In addition, the ratios of perinatal to embryonic and of adult fast to developmental MyHC isoforms were generally lower in light fetuses compared with their medium-weight littermates. These modifications suggest a delayed myofiber development in spontaneous growth-retarded fetuses. Finally, GLUT1 was expressed to a lesser extent in the muscle of small v. normal fetuses, suggesting decreased ability for glucose uptake in muscle. Initial feed restriction and subsequent overfeeding of sows during gestation led to a lower expression of the myogenic factor MYOD1, a prerequisite for myogenic initiation in skeletal muscle. This maternal strategy was also associated with a lower expression level of insulin-like growth factor 1 receptor (IGFR) but an upregulation of IGF2. This suggests an altered susceptibility of muscle cells to IGFs' signal in fetuses from treated sows. Altogether, intrauterine growth restriction impaired fetal muscle development, and restricted feeding followed by overfeeding of gestating sows did not allow small fetuses to recover normal contractile and metabolic characteristics.

Postnatal development of skeletal muscle in pigs with intrauterine growth restriction: morphofunctional phenotype and molecular mechanisms

“…Hence, the presence of embryonic MyHC may impair muscle functionality in IUGR pigs. Our results corroborate those reported by Perruchot et al (), which demonstrated a greater amount of the embryonic MyHC isoform in small fetuses, suggesting delayed myofiber development. Thus, IUGR individuals exhibit compromised postnatal growth which may be attributable to skeletal muscle delayed maturity.…”

Postnatal development of skeletal muscle in IUGR pigs: morphofunctional phenotype and molecular mechanisms

“…Hence, the presence of embryonic MyHC may impair muscle functionality in IUGR pigs. Our results corroborate with those reported by Perruchot and colleagues[20] which demonstrated greater amount of the embryonic MyHC isoform in small fetuses,suggesting delayed myofiber development. The molecular regulation of skeletal muscle postnatal myogenesis in IUGR animals still lack clarification, especially regarding postnatal development.…”

“…Thus, IUGR individuals exhibit compromised postnatal growth [17] [18] which may be due to skeletal muscle damage [19] and delayed skeletal muscle maturity [20].…”

2. Lean and fat development in piglets

“…Foetal myogenesis in IUGR piglets is impaired due to many changes in the mRNA abundance of muscle proteins that are involved in cellular structure, macronutrient metabolism, protein synthesis and degradation, immune response, extracellular matrix and antioxidant function (Wang et al, 2008). The longissimus muscle of small foetuses especially exhibits higher expression levels of DLK1 and NCAM1/CD56 (Perruchot et al, 2015), two genes known to be downregulated during myogenesis in normal littermates. Expression levels of the embryonic MyHC, both at the mRNA and protein levels, are also higher in small foetuses, whereas the ratios of perinatal to embryonic and of adult fast to developmental MyHC isoforms are lower in IUGR foetuses when compared with their medium-weight littermates .…”

“…Birth weight of piglets from sows receiving an increased feed supply during gestation is generally not affected, as reviewed in Chapter 1 (Farmer and Edwards, 2020), and there are inconsistent results on the myofibre types and postnatal growth rate of those piglets (Bee 2004;Cerisuelo et al, 2009;Gatford et al, 2003;McNamara et al, 2011;Nissen et al, 2003). Moreover, overfeeding subsequent to a period of early maternal diet deprivation does not modify the expression levels of stem cell markers, myogenic signals and MyHC isoforms in skeletal muscle of piglets just before birth, but upregulates IGF2 expression (Perruchot et al, 2015). Such findings demonstrate that this feeding strategy aiming to induce catch-up growth in later gestation cannot counteract the deleterious effect of IUGR and, in fact, it even tends to reduce piglet birth weight when compared to sows fed adequate diets throughout gestation (Farmer et al, 2014).…”