Comparing the intestinal transcriptome of Meishan and Large White piglets during late fetal development reveals genes involved in glucose and lipid metabolism and immunity as valuable clues of intestinal maturity

Abstract

BackgroundMaturity of intestinal functions is critical for neonatal health and survival, but comprehensive description of mechanisms underlying intestinal maturation that occur during late gestation still remain poorly characterized. The aim of this study was to investigate biological processes specifically involved in intestinal maturation by comparing fetal jejunal transcriptomes of two representative porcine breeds (Large White, LW; Meishan, MS) with contrasting neonatal vitality and maturity, at two key time points during late gestation (gestational days 90 and 110). MS and LW sows inseminated with mixed semen (from breed LW and MS) gave birth to both purebred and crossbred fetuses. We hypothesized that part of the differences in neonatal maturity between the two breeds results from distinct developmental profiles of the fetal intestine during late gestation. Reciprocal crossed fetuses were used to analyze the effect of parental genome. Transcriptomic data and 23 phenotypic variables known to be associated with maturity trait were integrated using multivariate analysis with expectation of identifying relevant genes-phenotypic variable relationships involved in intestinal maturation.ResultsA moderate maternal genotype effect, but no paternal genotype effect, was observed on offspring intestinal maturation. Four hundred and four differentially expressed probes, corresponding to 274 differentially expressed genes (DEGs), more specifically involved in the maturation process were further studied. In day 110-MS fetuses, Ingenuity® functional enrichment analysis revealed that 46% of DEGs were involved in glucose and lipid metabolism, cell proliferation, vasculogenesis and hormone synthesis compared to day 90-MS fetuses. Expression of genes involved in immune pathways including phagocytosis, inflammation and defense processes was changed in day 110-LW compared to day 90-LW fetuses (corresponding to 13% of DEGs). The transcriptional regulator PPARGC1A was predicted to be an important regulator of differentially expressed genes in MS. Fetal blood fructose level, intestinal lactase activity and villous height were the best predicted phenotypic variables with probes mostly involved in lipid metabolism, carbohydrate metabolism and cellular movement biological pathways.ConclusionsCollectively, our findings indicate that the neonatal maturity of pig intestine may rely on functional development of glucose and lipid metabolisms, immune phagocyte differentiation and inflammatory pathways. This process may partially be governed by PPARGC1A.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-4001-2) contains supplementary material, which is available to authorized users.

Transcriptome analysis reveals differential gene expression in intramuscular adipose tissues of Jinhua and Landrace pigs

“…Our results suggest considerable changes in gene expression in fat metabolism between the two porcine breeds. Similar phenomena have been reported for fat and muscle development [ 20 , 28 ]. Annotation to COG database showed high enrichment in the groups of lipid transport and metabolism.…”

The maturity in fetal pigs using a multi-fluid metabolomic approach

“…Such a metabolic switch has also been recently reported in the metabolome of the amniotic fluid in humans between the second and the third trimesters of gestation [41]. The metabolic switch observed here is also consistent with our previous findings obtained with the same experimental design, which highlighted important variations in the muscle and intestinal transcriptomes and in the muscle and adipose tissue proteomes for a subset of the fetuses used in the present article [22,55,56,66].…”

“…However, its important role in polyamine synthesis during the pig gestation has previously been demonstrated [60]. As expected, the higher concentration of proline in MS compared to LW at 90 and 110 dg in plasma could be related to the lower maturity of LW piglet and to a potential delay in development already identified in those fetuses [22,55,56,66]. In addition, in plasma, crossbred fetuses have intermediate proline concentrations, with no specific maternal or paternal effect.…”

“…After laparotomy of the sow, blood (approximately 5 mL) was collected individually on piglets from the umbilical artery via a 21-gauge needle and a 5 mL syringe and placed in heparinized tubes. After section of the umbilical cord, the fetus was euthanized [66]. Plasma was prepared by lowspeed centrifugation (2,000 g for 10 min at 4 • C) and stored at −80 • C until further analysis.…”

“…The transcriptomic and/or proteomic analyses of the muscle, the intestine and subcutaneous adipose tissue underlined a switch in gene expressions between the two stages of gestation and a delay in the development of tissues and organs in LW piglets. Notably, genes involved in muscular development are up-regulated around 90 dg and genes linked to metabolic functions, like gluconeogenesis, are up-regulated at 110 dg either in muscle or adipose tissue whatever the genotype [22,55,56,66].…”