Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease

BACKGROUND: Although the role of Th17 and regulatory T cells in the progression of atherosclerosis has been highlighted in recent years, their molecular mediators remain elusive. We aimed to evaluate the association between the CD69 receptor, a regulator of Th17/regulatory T cell immunity, and ather...

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Autores: Tsilingiri, Katerina, Fuente, Hortensia de la, Relaño, Marta, Sánchez-Díaz, Raquel, Rodríguez-Sinovas, Cristina, Crespo, Javier, Sánchez-Cabo, Fátima, Dopazo, Ana, Alonso-Lebrero, José Luis, Vara, Alicia, Vázquez, Jesús, Casasnovas, José María, Alfonso, Fernando, Ibáñez, Borja, Fuster, Valentín, Martínez-González, José, Martín, Pilar, Sánchez-Madrid, Francisco
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/201708
Acceso en línea:http://hdl.handle.net/10261/201708
Access Level:acceso abierto
Palabra clave:Atherosclerosis
CD69 antigen
Oxidized low density lipoprotein
Regulatory T
Lymphocytes
Th17 cells
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
title Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
spellingShingle Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
Tsilingiri, Katerina
Atherosclerosis
CD69 antigen
Oxidized low density lipoprotein
Regulatory T
Lymphocytes
Th17 cells
title_short Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
title_full Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
title_fullStr Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
title_full_unstemmed Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
title_sort Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical Disease
dc.creator.none.fl_str_mv Tsilingiri, Katerina
Fuente, Hortensia de la
Relaño, Marta
Sánchez-Díaz, Raquel
Rodríguez-Sinovas, Cristina
Crespo, Javier
Sánchez-Cabo, Fátima
Dopazo, Ana
Alonso-Lebrero, José Luis
Vara, Alicia
Vázquez, Jesús
Casasnovas, José María
Alfonso, Fernando
Ibáñez, Borja
Fuster, Valentín
Martínez-González, José
Martín, Pilar
Sánchez-Madrid, Francisco
author Tsilingiri, Katerina
author_facet Tsilingiri, Katerina
Fuente, Hortensia de la
Relaño, Marta
Sánchez-Díaz, Raquel
Rodríguez-Sinovas, Cristina
Crespo, Javier
Sánchez-Cabo, Fátima
Dopazo, Ana
Alonso-Lebrero, José Luis
Vara, Alicia
Vázquez, Jesús
Casasnovas, José María
Alfonso, Fernando
Ibáñez, Borja
Fuster, Valentín
Martínez-González, José
Martín, Pilar
Sánchez-Madrid, Francisco
author_role author
author2 Fuente, Hortensia de la
Relaño, Marta
Sánchez-Díaz, Raquel
Rodríguez-Sinovas, Cristina
Crespo, Javier
Sánchez-Cabo, Fátima
Dopazo, Ana
Alonso-Lebrero, José Luis
Vara, Alicia
Vázquez, Jesús
Casasnovas, José María
Alfonso, Fernando
Ibáñez, Borja
Fuster, Valentín
Martínez-González, José
Martín, Pilar
Sánchez-Madrid, Francisco
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Agencia Estatal de Investigación (España)
Ministerio de Economía y Competitividad (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Instituto de Salud Carlos III
Red Temática de Investigación Cooperativa en Enfermedades Cardiovasculares (España)
European Research Council
Fundació La Marató de TV3
Comunidad de Madrid
European Commission
Centro Nacional de Investigaciones Cardiovasculares (España)
Fundación Pro CNIC
Banco Santander
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Atherosclerosis
CD69 antigen
Oxidized low density lipoprotein
Regulatory T
Lymphocytes
Th17 cells
topic Atherosclerosis
CD69 antigen
Oxidized low density lipoprotein
Regulatory T
Lymphocytes
Th17 cells
description BACKGROUND: Although the role of Th17 and regulatory T cells in the progression of atherosclerosis has been highlighted in recent years, their molecular mediators remain elusive. We aimed to evaluate the association between the CD69 receptor, a regulator of Th17/regulatory T cell immunity, and atherosclerosis development in animal models and in patients with subclinical disease. METHODS: Low-density lipoprotein receptor-deficient chimeric mice expressing or not expressing CD69 on either myeloid or lymphoid cells were subjected to a high fat diet. In vitro functional assays with human T cells were performed to decipher the mechanism of the observed phenotypes. Expression of CD69 and NR4A nuclear receptors was evaluated by reverse transcription-polymerase chain reaction in 305 male participants of the PESA study (Progression of Early Subclinical Atherosclerosis) with extensive (n=128) or focal (n=55) subclinical atherosclerosis and without disease (n=122). RESULTS: After a high fat diet, mice lacking CD69 on lymphoid cells developed large atheroma plaque along with an increased Th17/regulatory T cell ratio in blood. Oxidized low-density lipoprotein was shown to bind specifically and functionally to CD69 on human T lymphocytes, inhibiting the development of Th17 cells through the activation of NR4A nuclear receptors. Participants of the PESA study with evidence of subclinical atherosclerosis displayed a significant CD69 and NR4A1 mRNA downregulation in peripheral blood leukocytes compared with participants without disease. The expression of CD69 remained associated with the risk of subclinical atherosclerosis in an adjusted multivariable logistic regression model (odds ratio, 0.62; 95% CI, 0.40-0.94; P=0.006) after adjustment for traditional risk factors, the expression of NR4A1, the level of oxidized low-density lipoprotein, and the counts of different leucocyte subsets. CONCLUSIONS: CD69 depletion from the lymphoid compartment promotes a Th17/regulatory T cell imbalance and exacerbates the development of atherosclerosis. CD69 binding to oxidized low-density lipoprotein on T cells induces the expression of anti-inflammatory transcription factors. Data from a cohort of the PESA study with subclinical atherosclerosis indicate that CD69 expression in PBLs inversely correlates with the presence of disease. The expression of CD69 remained an independent predictor of subclinical atherosclerosis after adjustment for traditional risk factors.
publishDate 2019
dc.date.none.fl_str_mv 2019
2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/201708
url http://hdl.handle.net/10261/201708
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/SAF2017-82886-R
SAF2017-82886-R/AEI/10.13039/501100011033
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2015-64767-R
info:eu-repo/grantAgreement/EC/FP7/294340
S2017/BMD-3671/INFLAMUNE-CM
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SEV-2015-0505
http://dx.doi.org/10.1161/CIRCULATIONAHA.118.034326

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Heart Association
publisher.none.fl_str_mv American Heart Association
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
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spelling Oxidized Low-Density Lipoprotein Receptor in Lymphocytes Prevents Atherosclerosis and Predicts Subclinical DiseaseTsilingiri, KaterinaFuente, Hortensia de laRelaño, MartaSánchez-Díaz, RaquelRodríguez-Sinovas, CristinaCrespo, JavierSánchez-Cabo, FátimaDopazo, AnaAlonso-Lebrero, José LuisVara, AliciaVázquez, JesúsCasasnovas, José MaríaAlfonso, FernandoIbáñez, BorjaFuster, ValentínMartínez-González, JoséMartín, PilarSánchez-Madrid, FranciscoAtherosclerosisCD69 antigenOxidized low density lipoproteinRegulatory TLymphocytesTh17 cellsBACKGROUND: Although the role of Th17 and regulatory T cells in the progression of atherosclerosis has been highlighted in recent years, their molecular mediators remain elusive. We aimed to evaluate the association between the CD69 receptor, a regulator of Th17/regulatory T cell immunity, and atherosclerosis development in animal models and in patients with subclinical disease. METHODS: Low-density lipoprotein receptor-deficient chimeric mice expressing or not expressing CD69 on either myeloid or lymphoid cells were subjected to a high fat diet. In vitro functional assays with human T cells were performed to decipher the mechanism of the observed phenotypes. Expression of CD69 and NR4A nuclear receptors was evaluated by reverse transcription-polymerase chain reaction in 305 male participants of the PESA study (Progression of Early Subclinical Atherosclerosis) with extensive (n=128) or focal (n=55) subclinical atherosclerosis and without disease (n=122). RESULTS: After a high fat diet, mice lacking CD69 on lymphoid cells developed large atheroma plaque along with an increased Th17/regulatory T cell ratio in blood. Oxidized low-density lipoprotein was shown to bind specifically and functionally to CD69 on human T lymphocytes, inhibiting the development of Th17 cells through the activation of NR4A nuclear receptors. Participants of the PESA study with evidence of subclinical atherosclerosis displayed a significant CD69 and NR4A1 mRNA downregulation in peripheral blood leukocytes compared with participants without disease. The expression of CD69 remained associated with the risk of subclinical atherosclerosis in an adjusted multivariable logistic regression model (odds ratio, 0.62; 95% CI, 0.40-0.94; P=0.006) after adjustment for traditional risk factors, the expression of NR4A1, the level of oxidized low-density lipoprotein, and the counts of different leucocyte subsets. CONCLUSIONS: CD69 depletion from the lymphoid compartment promotes a Th17/regulatory T cell imbalance and exacerbates the development of atherosclerosis. CD69 binding to oxidized low-density lipoprotein on T cells induces the expression of anti-inflammatory transcription factors. Data from a cohort of the PESA study with subclinical atherosclerosis indicate that CD69 expression in PBLs inversely correlates with the presence of disease. The expression of CD69 remained an independent predictor of subclinical atherosclerosis after adjustment for traditional risk factors.Funding was provided by the Spanish Ministry of Economy and Competitiveness: Plan Nacional de Salud SAF2017-82886-R to Dr Sánchez-Madrid, SAF2015-64767-R to Dr Martínez-González; Instituto de Salud Carlos III (AES 2016): PI16/01956 to Dr Martin, Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares; European Research Council, ERC-2011-AdG294340-GENTRIS to Dr Sánchez-Madrid; Proyecto Integrado de Excelencia PIE13/041 and Fundació La Marató TV3 (20152330 31); and Comunidad Autónoma de Madrid CAM (S2017/BMD-3671) to Drs Martin and Sánchez-Madrid. Dr Tsilingiri is cofunded by the European Union Marie Curie Program. M. Relaño is supported by a Contratos Predoctorales Severo Ochoa para la formación de doctores (BES-2015–072625) from the Spanish Ministry of Economy and Competitiveness. This research has been cofinanced by Fondo Europeo de Desarrollo Regional. Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain, is supported by the Ministerio de Ciencia, Innovación y Universidades, and the Pro CNIC Foundation and is a Severo Ochoa Center of Excellence (SEV-2015-0505). The PESA study is cofunded equally by the Pro CNIC Foundation and Banco Santander, Madrid, Spain.American Heart AssociationAgencia Estatal de Investigación (España)Ministerio de Economía y Competitividad (España)Ministerio de Ciencia, Innovación y Universidades (España)Instituto de Salud Carlos IIIRed Temática de Investigación Cooperativa en Enfermedades Cardiovasculares (España)European Research CouncilFundació La Marató de TV3Comunidad de MadridEuropean CommissionCentro Nacional de Investigaciones Cardiovasculares (España)Fundación Pro CNICBanco SantanderConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2020202020192020info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/201708reponame:DIGITAL.CSIC. 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