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Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study
From a general structural perspective, a mucosal tissue is constituted by two main matrices: the tissue and the secreted mucus. Jointly, they fulfill a wide range of functions including the protection of the epithelial layer. In this study, we simultaneously analyzed the epithelial tissue and the se...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7890662/ https://www.ncbi.nlm.nih.gov/pubmed/33613538 http://dx.doi.org/10.3389/fimmu.2020.613824 |
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author | Reyes-López, Felipe E. Ibarz, Antoni Ordóñez-Grande, Borja Vallejos-Vidal, Eva Andree, Karl B. Balasch, Joan Carles Fernández-Alacid, Laura Sanahuja, Ignasi Sánchez-Nuño, Sergio Firmino, Joana P. Pavez, Leonardo Polo, Javier Tort, Lluis Gisbert, Enric |
author_facet | Reyes-López, Felipe E. Ibarz, Antoni Ordóñez-Grande, Borja Vallejos-Vidal, Eva Andree, Karl B. Balasch, Joan Carles Fernández-Alacid, Laura Sanahuja, Ignasi Sánchez-Nuño, Sergio Firmino, Joana P. Pavez, Leonardo Polo, Javier Tort, Lluis Gisbert, Enric |
author_sort | Reyes-López, Felipe E. |
collection | PubMed |
description | From a general structural perspective, a mucosal tissue is constituted by two main matrices: the tissue and the secreted mucus. Jointly, they fulfill a wide range of functions including the protection of the epithelial layer. In this study, we simultaneously analyzed the epithelial tissue and the secreted mucus response using a holistic interactome-based multi-omics approach. The effect of the gilthead sea bream (Sparus aurata) skin mucosa to a dietary inclusion of spray-dried porcine plasma (SDPP) was evaluated. The epithelial skin microarrays-based transcriptome data showed 194 differentially expressed genes, meanwhile the exuded mucus proteome analysis 35 differentially synthesized proteins. Separately, the skin transcripteractome revealed an expression profile that favored biological mechanisms associated to gene expression, biogenesis, vesicle function, protein transport and localization to the membrane. Mucus proteome showed an enhanced protective role with putatively higher antioxidant and antimicrobial properties. The integrated skin mucosa multi-interactome analysis evidenced the interrelationship and synergy between the metabolism and the exuded mucus functions improving specifically the tissue development, innate defenses, and environment recognition. Histologically, the skin increased in thickness and in number of mucous cells. A positive impact on animal performance, growth and feed efficiency was also registered. Collectively, the results suggest an intimate crosstalk between skin tissue and its exuded mucus in response to the nutritional stimulus (SDPP supplementation) that favors the stimulation of cell protein turnover and the activation of the exudation machinery in the skin mucosa. Thus, the multi-omics-based interactome analysis provides a comprehensive understanding of the biological context of response that takes place in a mucosal tissue. In perspective, this strategy is applicable for evaluating the effect of any experimental variable on any mucosal tissue functionality, including the benefits this assessment may provide on the study of the mammalian mucosa. |
format | Online Article Text |
id | pubmed-7890662 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-78906622021-02-19 Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study Reyes-López, Felipe E. Ibarz, Antoni Ordóñez-Grande, Borja Vallejos-Vidal, Eva Andree, Karl B. Balasch, Joan Carles Fernández-Alacid, Laura Sanahuja, Ignasi Sánchez-Nuño, Sergio Firmino, Joana P. Pavez, Leonardo Polo, Javier Tort, Lluis Gisbert, Enric Front Immunol Immunology From a general structural perspective, a mucosal tissue is constituted by two main matrices: the tissue and the secreted mucus. Jointly, they fulfill a wide range of functions including the protection of the epithelial layer. In this study, we simultaneously analyzed the epithelial tissue and the secreted mucus response using a holistic interactome-based multi-omics approach. The effect of the gilthead sea bream (Sparus aurata) skin mucosa to a dietary inclusion of spray-dried porcine plasma (SDPP) was evaluated. The epithelial skin microarrays-based transcriptome data showed 194 differentially expressed genes, meanwhile the exuded mucus proteome analysis 35 differentially synthesized proteins. Separately, the skin transcripteractome revealed an expression profile that favored biological mechanisms associated to gene expression, biogenesis, vesicle function, protein transport and localization to the membrane. Mucus proteome showed an enhanced protective role with putatively higher antioxidant and antimicrobial properties. The integrated skin mucosa multi-interactome analysis evidenced the interrelationship and synergy between the metabolism and the exuded mucus functions improving specifically the tissue development, innate defenses, and environment recognition. Histologically, the skin increased in thickness and in number of mucous cells. A positive impact on animal performance, growth and feed efficiency was also registered. Collectively, the results suggest an intimate crosstalk between skin tissue and its exuded mucus in response to the nutritional stimulus (SDPP supplementation) that favors the stimulation of cell protein turnover and the activation of the exudation machinery in the skin mucosa. Thus, the multi-omics-based interactome analysis provides a comprehensive understanding of the biological context of response that takes place in a mucosal tissue. In perspective, this strategy is applicable for evaluating the effect of any experimental variable on any mucosal tissue functionality, including the benefits this assessment may provide on the study of the mammalian mucosa. Frontiers Media S.A. 2021-02-04 /pmc/articles/PMC7890662/ /pubmed/33613538 http://dx.doi.org/10.3389/fimmu.2020.613824 Text en Copyright © 2021 Reyes-López, Ibarz, Ordóñez-Grande, Vallejos-Vidal, Andree, Balasch, Fernández-Alacid, Sanahuja, Sánchez-Nuño, Firmino, Pavez, Polo, Tort and Gisbert http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Immunology Reyes-López, Felipe E. Ibarz, Antoni Ordóñez-Grande, Borja Vallejos-Vidal, Eva Andree, Karl B. Balasch, Joan Carles Fernández-Alacid, Laura Sanahuja, Ignasi Sánchez-Nuño, Sergio Firmino, Joana P. Pavez, Leonardo Polo, Javier Tort, Lluis Gisbert, Enric Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study |
title | Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study |
title_full | Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study |
title_fullStr | Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study |
title_full_unstemmed | Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study |
title_short | Skin Multi-Omics-Based Interactome Analysis: Integrating the Tissue and Mucus Exuded Layer for a Comprehensive Understanding of the Teleost Mucosa Functionality as Model of Study |
title_sort | skin multi-omics-based interactome analysis: integrating the tissue and mucus exuded layer for a comprehensive understanding of the teleost mucosa functionality as model of study |
topic | Immunology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7890662/ https://www.ncbi.nlm.nih.gov/pubmed/33613538 http://dx.doi.org/10.3389/fimmu.2020.613824 |
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