Cargando…

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

BACKGROUND: Maturity 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 sp...

Descripción completa

Detalles Bibliográficos
Autores principales: Yao, Ying, Voillet, Valentin, Jegou, Maeva, SanCristobal, Magali, Dou, Samir, Romé, Véronique, Lippi, Yannick, Billon, Yvon, Père, Marie-Christine, Boudry, Gaëlle, Gress, Laure, Iannucelli, Nathalie, Mormède, Pierre, Quesnel, Hélène, Canario, Laurianne, Liaubet, Laurence, Le Huërou-Luron, Isabelle
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5568345/
https://www.ncbi.nlm.nih.gov/pubmed/28830381
http://dx.doi.org/10.1186/s12864-017-4001-2
_version_ 1783258843936980992
author Yao, Ying
Voillet, Valentin
Jegou, Maeva
SanCristobal, Magali
Dou, Samir
Romé, Véronique
Lippi, Yannick
Billon, Yvon
Père, Marie-Christine
Boudry, Gaëlle
Gress, Laure
Iannucelli, Nathalie
Mormède, Pierre
Quesnel, Hélène
Canario, Laurianne
Liaubet, Laurence
Le Huërou-Luron, Isabelle
author_facet Yao, Ying
Voillet, Valentin
Jegou, Maeva
SanCristobal, Magali
Dou, Samir
Romé, Véronique
Lippi, Yannick
Billon, Yvon
Père, Marie-Christine
Boudry, Gaëlle
Gress, Laure
Iannucelli, Nathalie
Mormède, Pierre
Quesnel, Hélène
Canario, Laurianne
Liaubet, Laurence
Le Huërou-Luron, Isabelle
author_sort Yao, Ying
collection PubMed
description BACKGROUND: Maturity 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. RESULTS: A 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. CONCLUSIONS: Collectively, 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 MATERIAL: The online version of this article (doi:10.1186/s12864-017-4001-2) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5568345
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-55683452017-08-29 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 Yao, Ying Voillet, Valentin Jegou, Maeva SanCristobal, Magali Dou, Samir Romé, Véronique Lippi, Yannick Billon, Yvon Père, Marie-Christine Boudry, Gaëlle Gress, Laure Iannucelli, Nathalie Mormède, Pierre Quesnel, Hélène Canario, Laurianne Liaubet, Laurence Le Huërou-Luron, Isabelle BMC Genomics Research Article BACKGROUND: Maturity 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. RESULTS: A 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. CONCLUSIONS: Collectively, 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 MATERIAL: The online version of this article (doi:10.1186/s12864-017-4001-2) contains supplementary material, which is available to authorized users. BioMed Central 2017-08-22 /pmc/articles/PMC5568345/ /pubmed/28830381 http://dx.doi.org/10.1186/s12864-017-4001-2 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research Article
Yao, Ying
Voillet, Valentin
Jegou, Maeva
SanCristobal, Magali
Dou, Samir
Romé, Véronique
Lippi, Yannick
Billon, Yvon
Père, Marie-Christine
Boudry, Gaëlle
Gress, Laure
Iannucelli, Nathalie
Mormède, Pierre
Quesnel, Hélène
Canario, Laurianne
Liaubet, Laurence
Le Huërou-Luron, Isabelle
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
title 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_short 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
title_sort 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5568345/
https://www.ncbi.nlm.nih.gov/pubmed/28830381
http://dx.doi.org/10.1186/s12864-017-4001-2
work_keys_str_mv AT yaoying comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT voilletvalentin comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT jegoumaeva comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT sancristobalmagali comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT dousamir comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT romeveronique comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT lippiyannick comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT billonyvon comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT peremariechristine comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT boudrygaelle comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT gresslaure comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT iannucellinathalie comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT mormedepierre comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT quesnelhelene comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT canariolaurianne comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT liaubetlaurence comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity
AT lehuerouluronisabelle comparingtheintestinaltranscriptomeofmeishanandlargewhitepigletsduringlatefetaldevelopmentrevealsgenesinvolvedinglucoseandlipidmetabolismandimmunityasvaluablecluesofintestinalmaturity