Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig

Abstract

Background: Scarce is knowledge on the process regulating the development of acid secretion, orexigenic signaling, and chemosensing in the stomach of young pigs. Changes of early microbial encounters by suckling pigs can interact with the gut maturation, by the induction of different molecular signaling. Our goal was to assess if the age of offspring and the maternal environment, influenced by sow antibiotic treatment peripartum, could affect gastric morphology and the expression of genes involved in the control of hydrochloric secretion, feed intake, taste, and inflammation in offspring stomach.

Methods: 84 pigs from sows fed a diet with amoxicillin (on -d10 to +d21 from farrowing, ANT) or without (CON) were sacrificed at d14, d21, d28 (weaning) or d42. Samples of oxyntic (OXY), pyloric (PY) and cardiac mucosae close to OXY were collected and parietal and enteroendocrine cells (EECs) were counted. Relative gene expression of a set of 11 key genes (ATP4A, SSTR2, GAST, GHRL, MBOAT4, PCSK1, GNAT1, TAS1R1, TAS1R3, IL8 and TNF) was assessed by qRT-PCR. In addition, 40 offspring obtained from the same ANT and CON sows were offered a normal or a fat-enriched diet for 4 weeks between 140 and 169 d of age, and then OXY and PY were sampled.

Results: The number of parietal and EECs increased with age (P < 0.001). ATP4A increased with age (within suckling, P = 0.043, post-weaning vs. suckling, P < 0.001), SSTR2 increased only after weaning (P < 0.001). In OXY, GHRL increased during suckling (P = 0.012), and post-weaning as a trend (P = 0.088). MBOAT4 tended to increase during suckling (P = 0.062). TAS1R1 increased from suckling to post-weaning period (P =0.001) and was lower in ANT offspring (P = 0.013). GNAT1 in PY was higher in ANT offspring (P = 0.041). Antibiotic treatment of sows peripartum increased expression of GHRL and MBOAT4 in OXY of growing-finishing offspring aged 5 months.

Conclusions: Data show that sensing for umami taste and ghrelin regulation can be affected by maternal environment, but the development of acid secretion, orexigenic signaling and taste perception in the stomach are mostly developmentally controlled.

Keywords: Enteroendocrine cell; Gastrin; Ghrelin; Parietal cell; Stomach; Taste receptor.

Fig. 1

Effect of mother’s antibiotic treatment (CON = control, ANT = antibiotic) and offspring age on parietal cell counts (a), ATPase H⁺/K⁺ transporting subunit alpha (ATP4A) (b) and somatostatin receptor 2 (SSTR2) (c) expression in oxyntic mucosa and gastrin (GAST) (d) in pyloric mucosa

Fig. 2

Effect of mother’s antibiotic treatment (CON = control, ANT = antibiotic) and offspring age on enteroendocrine cell count (a), G protein subunit alpha transducin 1 (GNAT1) (b), taste 1 receptor member 1 (TAS1R1) (c) and taste 1 receptor member 3 (TAS1R3) (d) expression in pyloric mucosa

Fig. 3

Effect of mother’s antibiotic treatment (CON = control, ANT = antibiotic) and offspring age on expression of ghrelin and obestatin prepropeptide (GHRL) (a), proprotein convertase subtilisin/kexin type 1 (PCSK1) (b) and membrane bound O-acyltransferase domain containing 4 (MPBOAT4) (c) in oxyntic mucosa

Fig. 4

Effect of mother’s antibiotic treatment (CON = control, ANT = antibiotic) and offspring age on gene expression of tumor necrosis factor (TNF) (a) and interleukin 8 (IL8) (b) in the transition region between oxyntic and cardia mucosa

Fig. 5

Effect of mother’s antibiotic treatment (CON = control, ANT = antibiotic) and of dietary fat addition in growing-finishing offspring’ diet (LF = low fat, HF = high fat) on gene expression of ghrelin and obestatin prepropeptide (GHRL) (a) and membrane bound O-acyltransferase domain containing 4 (MPBOAT4) (b) in oxyntic mucosa of growing pigs