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

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 signa...

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Autores principales: Trevisi, P., Luise, D., Correa, F., Messori, S., Mazzoni, M., Lallès, J. P., Bosi, P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7972225/
https://www.ncbi.nlm.nih.gov/pubmed/33731211
http://dx.doi.org/10.1186/s40104-021-00557-3
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author Trevisi, P.
Luise, D.
Correa, F.
Messori, S.
Mazzoni, M.
Lallès, J. P.
Bosi, P.
author_facet Trevisi, P.
Luise, D.
Correa, F.
Messori, S.
Mazzoni, M.
Lallès, J. P.
Bosi, P.
author_sort Trevisi, P.
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-021-00557-3.
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spelling pubmed-79722252021-03-19 Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig Trevisi, P. Luise, D. Correa, F. Messori, S. Mazzoni, M. Lallès, J. P. Bosi, P. J Anim Sci Biotechnol Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-021-00557-3. BioMed Central 2021-03-18 /pmc/articles/PMC7972225/ /pubmed/33731211 http://dx.doi.org/10.1186/s40104-021-00557-3 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Trevisi, P.
Luise, D.
Correa, F.
Messori, S.
Mazzoni, M.
Lallès, J. P.
Bosi, P.
Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig
title Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig
title_full Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig
title_fullStr Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig
title_full_unstemmed Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig
title_short Maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig
title_sort maternal antibiotic treatment affects offspring gastric sensing for umami taste and ghrelin regulation in the pig
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7972225/
https://www.ncbi.nlm.nih.gov/pubmed/33731211
http://dx.doi.org/10.1186/s40104-021-00557-3
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