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Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis

BACKGROUND: Because the cost of cereals is unstable and represents a large part of production charges for meat-type chicken, there is an urge to formulate alternative diets from more cost-effective feedstuff. We have recently shown that meat-type chicken source is prone to adapt to dietary starch su...

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Autores principales: Desert, C., Baéza, E., Aite, M., Boutin, M., Le Cam, A., Montfort, J., Houee-Bigot, M., Blum, Y., Roux, P. F., Hennequet-Antier, C., Berri, C., Metayer-Coustard, S., Collin, A., Allais, S., Le Bihan, E., Causeur, D., Gondret, F., Duclos, M. J., Lagarrigue, S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5842524/
https://www.ncbi.nlm.nih.gov/pubmed/29514634
http://dx.doi.org/10.1186/s12864-018-4520-5
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author Desert, C.
Baéza, E.
Aite, M.
Boutin, M.
Le Cam, A.
Montfort, J.
Houee-Bigot, M.
Blum, Y.
Roux, P. F.
Hennequet-Antier, C.
Berri, C.
Metayer-Coustard, S.
Collin, A.
Allais, S.
Le Bihan, E.
Causeur, D.
Gondret, F.
Duclos, M. J.
Lagarrigue, S.
author_facet Desert, C.
Baéza, E.
Aite, M.
Boutin, M.
Le Cam, A.
Montfort, J.
Houee-Bigot, M.
Blum, Y.
Roux, P. F.
Hennequet-Antier, C.
Berri, C.
Metayer-Coustard, S.
Collin, A.
Allais, S.
Le Bihan, E.
Causeur, D.
Gondret, F.
Duclos, M. J.
Lagarrigue, S.
author_sort Desert, C.
collection PubMed
description BACKGROUND: Because the cost of cereals is unstable and represents a large part of production charges for meat-type chicken, there is an urge to formulate alternative diets from more cost-effective feedstuff. We have recently shown that meat-type chicken source is prone to adapt to dietary starch substitution with fat and fiber. The aim of this study was to better understand the molecular mechanisms of this adaptation to changes in dietary energy sources through the fine characterization of transcriptomic changes occurring in three major metabolic tissues – liver, adipose tissue and muscle – as well as in circulating blood cells. RESULTS: We revealed the fine-tuned regulation of many hepatic genes encoding key enzymes driving glycogenesis and de novo fatty acid synthesis pathways and of some genes participating in oxidation. Among the genes expressed upon consumption of a high-fat, high-fiber diet, we highlighted CPT1A, which encodes a key enzyme in the regulation of fatty acid oxidation. Conversely, the repression of lipogenic genes by the high-fat diet was clearly associated with the down-regulation of SREBF1 transcripts but was not associated with the transcript regulation of MLXIPL and NR1H3, which are both transcription factors. This result suggests a pivotal role for SREBF1 in lipogenesis regulation in response to a decrease in dietary starch and an increase in dietary PUFA. Other prospective regulators of de novo hepatic lipogenesis were suggested, such as PPARD, JUN, TADA2A and KAT2B, the last two genes belonging to the lysine acetyl transferase (KAT) complex family regulating histone and non-histone protein acetylation. Hepatic glycogenic genes were also down-regulated in chickens fed a high-fat, high-fiber diet compared to those in chickens fed a starch-based diet. No significant dietary-associated variations in gene expression profiles was observed in the other studied tissues, suggesting that the liver mainly contributed to the adaptation of birds to changes in energy source and nutrients in their diets, at least at the transcriptional level. Moreover, we showed that PUFA deposition observed in the different tissues may not rely on transcriptional changes. CONCLUSION: We showed the major role of the liver, at the gene expression level, in the adaptive response of chicken to dietary starch substitution with fat and fiber. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4520-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-58425242018-03-14 Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis Desert, C. Baéza, E. Aite, M. Boutin, M. Le Cam, A. Montfort, J. Houee-Bigot, M. Blum, Y. Roux, P. F. Hennequet-Antier, C. Berri, C. Metayer-Coustard, S. Collin, A. Allais, S. Le Bihan, E. Causeur, D. Gondret, F. Duclos, M. J. Lagarrigue, S. BMC Genomics Research Article BACKGROUND: Because the cost of cereals is unstable and represents a large part of production charges for meat-type chicken, there is an urge to formulate alternative diets from more cost-effective feedstuff. We have recently shown that meat-type chicken source is prone to adapt to dietary starch substitution with fat and fiber. The aim of this study was to better understand the molecular mechanisms of this adaptation to changes in dietary energy sources through the fine characterization of transcriptomic changes occurring in three major metabolic tissues – liver, adipose tissue and muscle – as well as in circulating blood cells. RESULTS: We revealed the fine-tuned regulation of many hepatic genes encoding key enzymes driving glycogenesis and de novo fatty acid synthesis pathways and of some genes participating in oxidation. Among the genes expressed upon consumption of a high-fat, high-fiber diet, we highlighted CPT1A, which encodes a key enzyme in the regulation of fatty acid oxidation. Conversely, the repression of lipogenic genes by the high-fat diet was clearly associated with the down-regulation of SREBF1 transcripts but was not associated with the transcript regulation of MLXIPL and NR1H3, which are both transcription factors. This result suggests a pivotal role for SREBF1 in lipogenesis regulation in response to a decrease in dietary starch and an increase in dietary PUFA. Other prospective regulators of de novo hepatic lipogenesis were suggested, such as PPARD, JUN, TADA2A and KAT2B, the last two genes belonging to the lysine acetyl transferase (KAT) complex family regulating histone and non-histone protein acetylation. Hepatic glycogenic genes were also down-regulated in chickens fed a high-fat, high-fiber diet compared to those in chickens fed a starch-based diet. No significant dietary-associated variations in gene expression profiles was observed in the other studied tissues, suggesting that the liver mainly contributed to the adaptation of birds to changes in energy source and nutrients in their diets, at least at the transcriptional level. Moreover, we showed that PUFA deposition observed in the different tissues may not rely on transcriptional changes. CONCLUSION: We showed the major role of the liver, at the gene expression level, in the adaptive response of chicken to dietary starch substitution with fat and fiber. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4520-5) contains supplementary material, which is available to authorized users. BioMed Central 2018-03-07 /pmc/articles/PMC5842524/ /pubmed/29514634 http://dx.doi.org/10.1186/s12864-018-4520-5 Text en © The Author(s). 2018 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
Desert, C.
Baéza, E.
Aite, M.
Boutin, M.
Le Cam, A.
Montfort, J.
Houee-Bigot, M.
Blum, Y.
Roux, P. F.
Hennequet-Antier, C.
Berri, C.
Metayer-Coustard, S.
Collin, A.
Allais, S.
Le Bihan, E.
Causeur, D.
Gondret, F.
Duclos, M. J.
Lagarrigue, S.
Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis
title Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis
title_full Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis
title_fullStr Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis
title_full_unstemmed Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis
title_short Multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis
title_sort multi-tissue transcriptomic study reveals the main role of liver in the chicken adaptive response to a switch in dietary energy source through the transcriptional regulation of lipogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5842524/
https://www.ncbi.nlm.nih.gov/pubmed/29514634
http://dx.doi.org/10.1186/s12864-018-4520-5
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