CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes

The mechanisms that control the inflammatory-immune response play a key role in tissue remodelling in cardiovascular diseases. T cell activation receptor CD69 binds to oxidized low-density lipoprotein (oxLDL), inducing the expression of anti-inflammatory NR4A nuclear receptors and modulating inflamm...

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Autores: Jiménez-Fernández, María, Rodríguez, Cristina|||0000-0002-6472-5647, Cañes Esteve, Laia|||0000-0002-9579-1321, Ballester-Servera, Carme|||0000-0001-7858-3064, Vara, Alicia, Requena, Silvia, de la Fuente, Hortensia, Martínez-González, José|||0000-0002-3894-7166, Sánchez-Madrid, Francisco|||0000-0001-5303-0762
Tipo de recurso: artículo
Fecha de publicación:2022
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:ddd.uab.cat:282323
Acceso en línea:https://ddd.uab.cat/record/282323
https://dx.doi.org/urn:doi:10.1007/s00018-022-04481-1
Access Level:acceso abierto
Palabra clave:CD69 leucocyte activation receptor
Oxldl
Cardiovascular disease
Programmed Death 1 (PD-1)
Antiinfammatory response
Infamed aorta
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spelling CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytesJiménez-Fernández, MaríaRodríguez, Cristina|||0000-0002-6472-5647Cañes Esteve, Laia|||0000-0002-9579-1321Ballester-Servera, Carme|||0000-0001-7858-3064Vara, AliciaRequena, Silviade la Fuente, HortensiaMartínez-González, José|||0000-0002-3894-7166Sánchez-Madrid, Francisco|||0000-0001-5303-0762CD69 leucocyte activation receptorOxldlCardiovascular diseaseProgrammed Death 1 (PD-1)Antiinfammatory responseInfamed aortaThe mechanisms that control the inflammatory-immune response play a key role in tissue remodelling in cardiovascular diseases. T cell activation receptor CD69 binds to oxidized low-density lipoprotein (oxLDL), inducing the expression of anti-inflammatory NR4A nuclear receptors and modulating inflammation in atherosclerosis. To understand the downstream T cell responses triggered by the CD69-oxLDL binding, we incubated CD69-expressing Jurkat T cells with oxLDL. RNA sequencing revealed a differential gene expression profile dependent on the presence of CD69 and the degree of LDL oxidation. CD69-oxLDL binding induced the expression of NR4A receptors (NR4A1 and NR4A3), but also of PD-1. These results were confirmed using oxLDL and a monoclonal antibody against CD69 in CD69-expressing Jurkat and primary CD4 + lymphocytes. CD69-mediated induction of PD-1 and NR4A3 was dependent on NFAT activation. Silencing NR4A3 slightly increased PD-1 levels, suggesting a potential regulation of PD-1 by this receptor. Moreover, expression of PD-1, CD69 and NR4A3 was increased in human arteries with chronic inflammation compared to healthy controls, with a strong correlation between PD-1 and CD69 mRNA expression (r = 0.655 P < 0.0001). Moreover, PD-1 was expressed in areas enriched in CD3 infiltrating T cells. Our results underscore a novel mechanism of PD-1 induction independent of TCR signalling that might contribute to the role of CD69 in the modulation of inflammation and vascular remodelling in cardiovascular diseases. 22022-01-0120222022-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/282323https://dx.doi.org/urn:doi:10.1007/s00018-022-04481-1reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengAgencia Estatal de Investigación https://doi.org/10.13039/501100011033 PDC2021-121719-I00Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2020-120412RB-I00Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 PI18/0919Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 RTI2018-094727-B-100Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2017/SGR-00333"la Caixa" Foundation https://doi.org/10.13039/100010434 HR17-00016open accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, fins i tot amb finalitats comercials, sempre i quan es reconegui l'autoria de l'obra original.https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:ddd.uab.cat:2823232026-06-06T12:50:31Z
dc.title.none.fl_str_mv CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
title CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
spellingShingle CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
Jiménez-Fernández, María
CD69 leucocyte activation receptor
Oxldl
Cardiovascular disease
Programmed Death 1 (PD-1)
Antiinfammatory response
Infamed aorta
title_short CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
title_full CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
title_fullStr CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
title_full_unstemmed CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
title_sort CD69-oxLDL ligand engagement induces Programmed Cell Death 1 (PD-1) expression in human CD4 + T lymphocytes
dc.creator.none.fl_str_mv Jiménez-Fernández, María
Rodríguez, Cristina|||0000-0002-6472-5647
Cañes Esteve, Laia|||0000-0002-9579-1321
Ballester-Servera, Carme|||0000-0001-7858-3064
Vara, Alicia
Requena, Silvia
de la Fuente, Hortensia
Martínez-González, José|||0000-0002-3894-7166
Sánchez-Madrid, Francisco|||0000-0001-5303-0762
author Jiménez-Fernández, María
author_facet Jiménez-Fernández, María
Rodríguez, Cristina|||0000-0002-6472-5647
Cañes Esteve, Laia|||0000-0002-9579-1321
Ballester-Servera, Carme|||0000-0001-7858-3064
Vara, Alicia
Requena, Silvia
de la Fuente, Hortensia
Martínez-González, José|||0000-0002-3894-7166
Sánchez-Madrid, Francisco|||0000-0001-5303-0762
author_role author
author2 Rodríguez, Cristina|||0000-0002-6472-5647
Cañes Esteve, Laia|||0000-0002-9579-1321
Ballester-Servera, Carme|||0000-0001-7858-3064
Vara, Alicia
Requena, Silvia
de la Fuente, Hortensia
Martínez-González, José|||0000-0002-3894-7166
Sánchez-Madrid, Francisco|||0000-0001-5303-0762
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CD69 leucocyte activation receptor
Oxldl
Cardiovascular disease
Programmed Death 1 (PD-1)
Antiinfammatory response
Infamed aorta
topic CD69 leucocyte activation receptor
Oxldl
Cardiovascular disease
Programmed Death 1 (PD-1)
Antiinfammatory response
Infamed aorta
description The mechanisms that control the inflammatory-immune response play a key role in tissue remodelling in cardiovascular diseases. T cell activation receptor CD69 binds to oxidized low-density lipoprotein (oxLDL), inducing the expression of anti-inflammatory NR4A nuclear receptors and modulating inflammation in atherosclerosis. To understand the downstream T cell responses triggered by the CD69-oxLDL binding, we incubated CD69-expressing Jurkat T cells with oxLDL. RNA sequencing revealed a differential gene expression profile dependent on the presence of CD69 and the degree of LDL oxidation. CD69-oxLDL binding induced the expression of NR4A receptors (NR4A1 and NR4A3), but also of PD-1. These results were confirmed using oxLDL and a monoclonal antibody against CD69 in CD69-expressing Jurkat and primary CD4 + lymphocytes. CD69-mediated induction of PD-1 and NR4A3 was dependent on NFAT activation. Silencing NR4A3 slightly increased PD-1 levels, suggesting a potential regulation of PD-1 by this receptor. Moreover, expression of PD-1, CD69 and NR4A3 was increased in human arteries with chronic inflammation compared to healthy controls, with a strong correlation between PD-1 and CD69 mRNA expression (r = 0.655 P < 0.0001). Moreover, PD-1 was expressed in areas enriched in CD3 infiltrating T cells. Our results underscore a novel mechanism of PD-1 induction independent of TCR signalling that might contribute to the role of CD69 in the modulation of inflammation and vascular remodelling in cardiovascular diseases.
publishDate 2022
dc.date.none.fl_str_mv 2
2022-01-01
2022
2022-01-01
dc.type.none.fl_str_mv Article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://ddd.uab.cat/record/282323
https://dx.doi.org/urn:doi:10.1007/s00018-022-04481-1
url https://ddd.uab.cat/record/282323
https://dx.doi.org/urn:doi:10.1007/s00018-022-04481-1
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PDC2021-121719-I00
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2020-120412RB-I00
Instituto de Salud Carlos III https://doi.org/10.13039/501100004587 PI18/0919
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 RTI2018-094727-B-100
Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2017/SGR-00333
"la Caixa" Foundation https://doi.org/10.13039/100010434 HR17-00016
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dipòsit Digital de Documents de la UAB
instname:Universitat Autònoma de Barcelona
instname_str Universitat Autònoma de Barcelona
reponame_str Dipòsit Digital de Documents de la UAB
collection Dipòsit Digital de Documents de la UAB
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