Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets

Polyunsaturated fatty acids (PUFA), such as omega-6 (n-6) and omega-3 (n-3), play a vital role in nutrient metabolism, inflammatory response, and gene regulation. microRNAs (miRNA), which can potentially degrade targeted messenger RNAs (mRNA) and/or inhibit their translation, might play a relevant r...

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Autores: Manaig, Yron Joseph Yabut, Mármol-Sánchez, Emilio, Castelló, Anna, Esteve-Codina, Anna, Sandrini, Silvia, Savoini, Giovanni, Agazzi, Alessandro, Sánchez, Armand, Folch, Josep M.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/58564
Acceso en línea:http://hdl.handle.net/10230/58564
http://dx.doi.org/10.1093/jas/skad271
Access Level:acceso abierto
Palabra clave:Exon–intron split analysis
PUFA
Messenger RNA
microRNA
Piglets
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oai_identifier_str oai:repositori.upf.edu:10230/58564
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network_name_str España
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dc.title.none.fl_str_mv Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
title Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
spellingShingle Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
Manaig, Yron Joseph Yabut
Exon–intron split analysis
PUFA
Messenger RNA
microRNA
Piglets
title_short Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
title_full Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
title_fullStr Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
title_full_unstemmed Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
title_sort Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in piglets
dc.creator.none.fl_str_mv Manaig, Yron Joseph Yabut
Mármol-Sánchez, Emilio
Castelló, Anna
Esteve-Codina, Anna
Sandrini, Silvia
Savoini, Giovanni
Agazzi, Alessandro
Sánchez, Armand
Folch, Josep M.
author Manaig, Yron Joseph Yabut
author_facet Manaig, Yron Joseph Yabut
Mármol-Sánchez, Emilio
Castelló, Anna
Esteve-Codina, Anna
Sandrini, Silvia
Savoini, Giovanni
Agazzi, Alessandro
Sánchez, Armand
Folch, Josep M.
author_role author
author2 Mármol-Sánchez, Emilio
Castelló, Anna
Esteve-Codina, Anna
Sandrini, Silvia
Savoini, Giovanni
Agazzi, Alessandro
Sánchez, Armand
Folch, Josep M.
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Exon–intron split analysis
PUFA
Messenger RNA
microRNA
Piglets
topic Exon–intron split analysis
PUFA
Messenger RNA
microRNA
Piglets
description Polyunsaturated fatty acids (PUFA), such as omega-6 (n-6) and omega-3 (n-3), play a vital role in nutrient metabolism, inflammatory response, and gene regulation. microRNAs (miRNA), which can potentially degrade targeted messenger RNAs (mRNA) and/or inhibit their translation, might play a relevant role in PUFA-related changes in gene expression. Although differential expression analyses can provide a comprehensive picture of gene expression variation, they are unable to disentangle when in the mRNA life cycle the regulation of expression is taking place, including any putative functional miRNA-driven repression. To capture this, we used an exon-intron split analysis (EISA) approach to account for posttranscriptional changes in response to extreme values of n-6/n-3 PUFA ratio. Longissimus dorsi muscle samples of male and female piglets from sows fed with n-6/n-3 PUFA ratio of 13:1 (SOY) or 4:1 (LIN), were analyzed in a bidirectional contrast (LIN vs. SOY, SOY vs. LIN). Our results allowed the identification of genes showing strong posttranscriptional downregulation signals putatively targeted by significantly upregulated miRNA. Moreover, we identified genes primarily involved in the regulation of lipid-related metabolism and immune response, which may be associated with the pro- and anti-inflammatory functions of the n-6 and n-3 PUFA, respectively. EISA allowed us to uncover regulatory networks complementing canonical differential expression analyses, thus providing a more comprehensive view of muscle metabolic changes in response to PUFA concentration.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/58564
http://dx.doi.org/10.1093/jas/skad271
url http://hdl.handle.net/10230/58564
http://dx.doi.org/10.1093/jas/skad271
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv J Anim Sci. 2023 Jan 3;101:skad271
info:eu-repo/grantAgreement/EC/H2020/765423
info:eu-repo/grantAgreement/ES/2PE/AGL2017-82641-R
info:eu-repo/grantAgreement/ES/2PE/PID2020-112677RB-C22
info:eu-repo/grantAgreement/ES/2PE/CEX2019-000902-S
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Exon-intron split analysis reveals posttranscriptional regulatory signals induced by high and low n-6/n-3 polyunsaturated fatty acid ratio diets in pigletsManaig, Yron Joseph YabutMármol-Sánchez, EmilioCastelló, AnnaEsteve-Codina, AnnaSandrini, SilviaSavoini, GiovanniAgazzi, AlessandroSánchez, ArmandFolch, Josep M.Exon–intron split analysisPUFAMessenger RNAmicroRNAPigletsPolyunsaturated fatty acids (PUFA), such as omega-6 (n-6) and omega-3 (n-3), play a vital role in nutrient metabolism, inflammatory response, and gene regulation. microRNAs (miRNA), which can potentially degrade targeted messenger RNAs (mRNA) and/or inhibit their translation, might play a relevant role in PUFA-related changes in gene expression. Although differential expression analyses can provide a comprehensive picture of gene expression variation, they are unable to disentangle when in the mRNA life cycle the regulation of expression is taking place, including any putative functional miRNA-driven repression. To capture this, we used an exon-intron split analysis (EISA) approach to account for posttranscriptional changes in response to extreme values of n-6/n-3 PUFA ratio. Longissimus dorsi muscle samples of male and female piglets from sows fed with n-6/n-3 PUFA ratio of 13:1 (SOY) or 4:1 (LIN), were analyzed in a bidirectional contrast (LIN vs. SOY, SOY vs. LIN). Our results allowed the identification of genes showing strong posttranscriptional downregulation signals putatively targeted by significantly upregulated miRNA. Moreover, we identified genes primarily involved in the regulation of lipid-related metabolism and immune response, which may be associated with the pro- and anti-inflammatory functions of the n-6 and n-3 PUFA, respectively. EISA allowed us to uncover regulatory networks complementing canonical differential expression analyses, thus providing a more comprehensive view of muscle metabolic changes in response to PUFA concentration.This work was supported by the European Union Horizon 2020 Research and Innovation programme H2020-MSCA-ITN-2017-EJD: Marie Skłodowska-Curie Innovative Training Networks (European Joint Doctorate) – Grant agreement: 765423—MANNA. Additionally, it was supported by the Spanish Ministerio de Ciencia e Innovación (MICINN) and the Fondo Europeo de Desarrollo Regional (FEDER) with project references: AGL2017-82641-R and PID2020-112677RB-C22. We also acknowledge the support of the Spanish Ministerio de Economía y Competitividad for the “Severo Ochoa” Programme for Centres of Excellence in R&D (Project CEX2019-000902-S) to the Centre for Research in Agricultural Genomics (CRAG) and to the programmes of Centres de Recerca de Catalunya (CERCA). Funding organizations were not involved in the execution of the project or the interpretation of results. All experimental protocols were approved by the ethical committee of the University of Milan (OPBA 22/2020). We also thank for help of Dr. Eleonora Munari and the University of Milan farm personnel with the in vivo trials, and Dr. Sara Panseri and Giacomo Mosconi for fatty acid analysis.Oxford University Press202320232023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/58564http://dx.doi.org/10.1093/jas/skad271reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésJ Anim Sci. 2023 Jan 3;101:skad271info:eu-repo/grantAgreement/EC/H2020/765423info:eu-repo/grantAgreement/ES/2PE/AGL2017-82641-Rinfo:eu-repo/grantAgreement/ES/2PE/PID2020-112677RB-C22info:eu-repo/grantAgreement/ES/2PE/CEX2019-000902-S© The Author(s) 2023. Published by Oxford University Press on behalf of the American Society of Animal Science. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.comhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/585642026-06-12T07:21:37Z
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