Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis

Liver fibrosis is the excessive accumulation of extracellular matrix proteins that occurs in chronic liver disease. Ubiquitination is a post-translational modification that is crucial for a plethora of physiological processes. Even though the ubiquitin system has been implicated in several human dis...

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Authors: Mercado Gómez, María, Lopitz Otsoa, Fernando, Azkargorta, Mikel, Serrano Maciá, Marina, Lachiondo Ortega, Sofía, Goikoetxea Usandizaga, Naroa, Rodríguez Agudo, Rubén, Fernández Ramos, David, Bizkarguenaga, Maider, Gutiérrez de Juan, Virginia, Lectez, Benoit, Aloria Escolastico, Kerman, Arizmendi Bastarrika, Jesús María, Simón Espinosa, Jorge, Alonso, Cristina, Lozano, Juan José, Ávila, Matías A., Bañales Asurmendi, Jesús María, Marín, José J. G., Beraza, Naiara, Mato, José M., Elortza, Felix, Barrio Olano, María Rosa, Sutherland, James D., Mayor Martínez, Ugo, Martínez Chantar, María Luz, Cardoso Delgado, Teresa de Jesús
Format: article
Publication Date:2020
Country:España
Institution:Universidad del País Vasco
Repository:Addi. Archivo Digital para la Docencia y la Investigación
OAI Identifier:oai:addi.ehu.eus:10810/49028
Online Access:http://hdl.handle.net/10810/49028
Access Level:Open access
Keyword:liver fibrosis
ubiquitination
metabolomics
proliferating cell nuclear antigen (PCNA)
DNA damage response (DDR)
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dc.title.none.fl_str_mv Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
title Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
spellingShingle Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
Mercado Gómez, María
liver fibrosis
ubiquitination
metabolomics
proliferating cell nuclear antigen (PCNA)
DNA damage response (DDR)
title_short Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
title_full Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
title_fullStr Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
title_full_unstemmed Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
title_sort Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver Fibrosis
dc.creator.none.fl_str_mv Mercado Gómez, María
Lopitz Otsoa, Fernando
Azkargorta, Mikel
Serrano Maciá, Marina
Lachiondo Ortega, Sofía
Goikoetxea Usandizaga, Naroa
Rodríguez Agudo, Rubén
Fernández Ramos, David
Bizkarguenaga, Maider
Gutiérrez de Juan, Virginia
Lectez, Benoit
Aloria Escolastico, Kerman
Arizmendi Bastarrika, Jesús María
Simón Espinosa, Jorge
Alonso, Cristina
Lozano, Juan José
Ávila, Matías A.
Bañales Asurmendi, Jesús María
Marín, José J. G.
Beraza, Naiara
Mato, José M.
Elortza, Felix
Barrio Olano, María Rosa
Sutherland, James D.
Mayor Martínez, Ugo
Martínez Chantar, María Luz
Cardoso Delgado, Teresa de Jesús
author Mercado Gómez, María
author_facet Mercado Gómez, María
Lopitz Otsoa, Fernando
Azkargorta, Mikel
Serrano Maciá, Marina
Lachiondo Ortega, Sofía
Goikoetxea Usandizaga, Naroa
Rodríguez Agudo, Rubén
Fernández Ramos, David
Bizkarguenaga, Maider
Gutiérrez de Juan, Virginia
Lectez, Benoit
Aloria Escolastico, Kerman
Arizmendi Bastarrika, Jesús María
Simón Espinosa, Jorge
Alonso, Cristina
Lozano, Juan José
Ávila, Matías A.
Bañales Asurmendi, Jesús María
Marín, José J. G.
Beraza, Naiara
Mato, José M.
Elortza, Felix
Barrio Olano, María Rosa
Sutherland, James D.
Mayor Martínez, Ugo
Martínez Chantar, María Luz
Cardoso Delgado, Teresa de Jesús
author_role author
author2 Lopitz Otsoa, Fernando
Azkargorta, Mikel
Serrano Maciá, Marina
Lachiondo Ortega, Sofía
Goikoetxea Usandizaga, Naroa
Rodríguez Agudo, Rubén
Fernández Ramos, David
Bizkarguenaga, Maider
Gutiérrez de Juan, Virginia
Lectez, Benoit
Aloria Escolastico, Kerman
Arizmendi Bastarrika, Jesús María
Simón Espinosa, Jorge
Alonso, Cristina
Lozano, Juan José
Ávila, Matías A.
Bañales Asurmendi, Jesús María
Marín, José J. G.
Beraza, Naiara
Mato, José M.
Elortza, Felix
Barrio Olano, María Rosa
Sutherland, James D.
Mayor Martínez, Ugo
Martínez Chantar, María Luz
Cardoso Delgado, Teresa de Jesús
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv liver fibrosis
ubiquitination
metabolomics
proliferating cell nuclear antigen (PCNA)
DNA damage response (DDR)
topic liver fibrosis
ubiquitination
metabolomics
proliferating cell nuclear antigen (PCNA)
DNA damage response (DDR)
description Liver fibrosis is the excessive accumulation of extracellular matrix proteins that occurs in chronic liver disease. Ubiquitination is a post-translational modification that is crucial for a plethora of physiological processes. Even though the ubiquitin system has been implicated in several human diseases, the role of ubiquitination in liver fibrosis remains poorly understood. Here, multi-omics approaches were used to address this. Untargeted metabolomics showed that carbon tetrachloride (CCl4)-induced liver fibrosis promotes changes in the hepatic metabolome, specifically in glycerophospholipids and sphingolipids. Gene ontology analysis of public deposited gene array-based data and validation in our mouse model showed that the biological process “protein polyubiquitination” is enriched after CCl4-induced liver fibrosis. Finally, by using transgenic mice expressing biotinylated ubiquitin (bioUb mice), the ubiquitinated proteome was isolated and characterized by mass spectrometry in order to unravel the hepatic ubiquitinated proteome fingerprint in CCl4-induced liver fibrosis. Under these conditions, ubiquitination appears to be involved in the regulation of cell death and survival, cell function, lipid metabolism, and DNA repair. Finally, ubiquitination of proliferating cell nuclear antigen (PCNA) is induced during CCl4-induced liver fibrosis and associated with the DNA damage response (DDR). Overall, hepatic ubiquitome profiling can highlight new therapeutic targets for the clinical management of liver fibrosis.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10810/49028
url http://hdl.handle.net/10810/49028
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv info:eu-repo/grantAgreement/MCIU/SAF2017-87301-R/
info:eu-repo/grantAgreement/MCIU/SAF2017-88041-R/
info:eu-repo/grantAgreement/MCIU/RTI2018-096759-A-100/
info:eu-repo/grantAgreement/MCIU/SAF2016-76898-P/
info:eu-repo/grantAgreement/MINECO/SAF2016-75197-R/
https://www.mdpi.com/1422-0067/21/23/9043/htm
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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eu_rights_str_mv openAccess
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dc.source.none.fl_str_mv reponame:Addi. Archivo Digital para la Docencia y la Investigación
instname:Universidad del País Vasco
instname_str Universidad del País Vasco
reponame_str Addi. Archivo Digital para la Docencia y la Investigación
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spelling Multi-Omics Integration Highlights the Role of Ubiquitination in CCl4-Induced Liver FibrosisMercado Gómez, MaríaLopitz Otsoa, FernandoAzkargorta, MikelSerrano Maciá, MarinaLachiondo Ortega, SofíaGoikoetxea Usandizaga, NaroaRodríguez Agudo, RubénFernández Ramos, DavidBizkarguenaga, MaiderGutiérrez de Juan, VirginiaLectez, BenoitAloria Escolastico, KermanArizmendi Bastarrika, Jesús MaríaSimón Espinosa, JorgeAlonso, CristinaLozano, Juan JoséÁvila, Matías A.Bañales Asurmendi, Jesús MaríaMarín, José J. G.Beraza, NaiaraMato, José M.Elortza, FelixBarrio Olano, María RosaSutherland, James D.Mayor Martínez, UgoMartínez Chantar, María LuzCardoso Delgado, Teresa de Jesúsliver fibrosisubiquitinationmetabolomicsproliferating cell nuclear antigen (PCNA)DNA damage response (DDR)Liver fibrosis is the excessive accumulation of extracellular matrix proteins that occurs in chronic liver disease. Ubiquitination is a post-translational modification that is crucial for a plethora of physiological processes. Even though the ubiquitin system has been implicated in several human diseases, the role of ubiquitination in liver fibrosis remains poorly understood. Here, multi-omics approaches were used to address this. Untargeted metabolomics showed that carbon tetrachloride (CCl4)-induced liver fibrosis promotes changes in the hepatic metabolome, specifically in glycerophospholipids and sphingolipids. Gene ontology analysis of public deposited gene array-based data and validation in our mouse model showed that the biological process “protein polyubiquitination” is enriched after CCl4-induced liver fibrosis. Finally, by using transgenic mice expressing biotinylated ubiquitin (bioUb mice), the ubiquitinated proteome was isolated and characterized by mass spectrometry in order to unravel the hepatic ubiquitinated proteome fingerprint in CCl4-induced liver fibrosis. Under these conditions, ubiquitination appears to be involved in the regulation of cell death and survival, cell function, lipid metabolism, and DNA repair. Finally, ubiquitination of proliferating cell nuclear antigen (PCNA) is induced during CCl4-induced liver fibrosis and associated with the DNA damage response (DDR). Overall, hepatic ubiquitome profiling can highlight new therapeutic targets for the clinical management of liver fibrosis.This work was supported by grants from Gobierno Vasco-Departamento de Salud 2013111114 (to M.L.M.-C.), ELKARTEK 2016, Departamento de Industria del Gobierno Vasco (to M.L.M.-C.), Ministerio de Ciencia, Innovación y Universidades MICINN: SAF2017-87301-R, SAF2017-88041-R, RTI2018-096759-A-100 and SAF2016-76898-P integrado en el Plan Estatal de Investigación Cientifica y Técnica y Innovación, cofinanciado con Fondos FEDER (to M.L.M.-C., J.M.M., T.C.D. and U.M. respectively); AECC Bizkaia (M.S.-M.); Asociación Española contra el Cáncer (T.C.D.), Fundación Científica de la Asociación Española Contra el Cancer (AECC Scientific Foundation) Rare Tumor Calls 2017 (to M.L.M., J.M.B., M.A.A., J.J.G.M.), La Caixa Foundation Program (to M.L.M.), 2018 BBVA Foundation Grants for Scientific Research Teams (to M.L.M.-C.). This research was also funded by the CIBERehd (EHD15PI05/2016) and “Fondo de Investigaciones Sanitarias, Instituto de Salud Carlos III”, Spain (PI16/00598 and PI19/00819, co-funded by European Regional Development Fund/European Social Fund, “Investing in your future”); Spanish Ministry of Economy, Industry and Competitiveness (SAF2016-75197-R); “Junta de Castilla y Leon” (SA063P17); AECC Scientific Foundation (2017/2020), Spain; “Centro Internacional sobre el Envejecimiento” (OLD-HEPAMARKER, 0348_CIE_6_E), Spain; University of Salamanca Foundation, Spain (PC-TCUE18-20_051), and Fundació Marato TV3 (Ref. 201916-31), Spain (to J.J.G.M.). The UPV/EHU Lab and the Proteomics Platform are members of Proteored, PRB3 and is supported by grant PT17/0019, of the PE I + D + i 2013-2016, funded by ISCIII and ERDF. Ciberehd_ISCIII_MINECO is funded by the Instituto de Salud Carlos III. We thank MINECO for the Severo Ochoa Excellence Accreditation to CIC bioGUNE (SEV-2016-0644).MDPI2020202020202020info:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10810/49028reponame:Addi. Archivo Digital para la Docencia y la Investigacióninstname:Universidad del País VascoInglésinfo:eu-repo/grantAgreement/MCIU/SAF2017-87301-R/info:eu-repo/grantAgreement/MCIU/SAF2017-88041-R/info:eu-repo/grantAgreement/MCIU/RTI2018-096759-A-100/info:eu-repo/grantAgreement/MCIU/SAF2016-76898-P/info:eu-repo/grantAgreement/MINECO/SAF2016-75197-R/https://www.mdpi.com/1422-0067/21/23/9043/htminfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/3.0/es/2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).oai:addi.ehu.eus:10810/490282026-06-18T09:23:17Z
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