Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload

Background The mitochondrial unfolded protein response (UPRmt) is activated when misfolded proteins accumulate within mitochondria and leads to increased expression of mitochondrial chaperones and proteases to maintain protein quality and mitochondrial function. Cardiac mitochondria are essential fo...

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Autores: Smyrnias, I. (Ioannis)|||/items/d5ab339a-af96-4b6c-a384-6588f4d711a2, Gray, S.P. (Stephen P.)|||/items/33ad7431-c580-46c5-928a-0d50a219dc7e, Okonko, D. (Darlington)|||/items/d79a3fa8-adcf-4905-bc75-e4fcacb383f0, Sawyer, G. (Greta)|||/items/22d9a898-ace6-4a51-a94b-1d2b76ceb15d, Zoccarato, A. (Anna)|||/items/bdd86a00-0deb-42de-a739-a2268fd2d6c0, Catibog, N. (Norman)|||/items/b2c6e5cc-a4b8-439c-919b-6b62d995c705, Lopez-Salazar, M.B. (María Begoña)|||/items/153e0e37-14b0-403e-afab-8af00c4edde0, Gonzalez, A. (Arantxa)|||/items/9c64c0f4-66b4-4b51-8593-0e50c091a515, Ravassa-Albéniz, S. (Susana)|||/items/df0c1eb3-9f45-4d77-a7a5-aca2bcf425e1, Diez-Espino, J. (Javier)|||/items/125690ae-ba81-4d29-a748-e644f3584853, Shah, A.M. (Ajay M.)|||/items/3bc739ce-1498-4741-8de7-e054feba2801
Tipo de recurso: artículo
Fecha de publicación:2019
País:España
Institución:Universidad de Navarra
Repositorio:Dadun. Depósito Académico Digital de la Universidad de Navarra
Idioma:inglés
OAI Identifier:oai:dadun.unav.edu:10171/63144
Acceso en línea:https://hdl.handle.net/10171/63144
Access Level:acceso abierto
Palabra clave:Cardiomyocyte
Heart
Mitochondria
Pressure overload
Unfolded protein response
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spelling Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overloadSmyrnias, I. (Ioannis)|||/items/d5ab339a-af96-4b6c-a384-6588f4d711a2Gray, S.P. (Stephen P.)|||/items/33ad7431-c580-46c5-928a-0d50a219dc7eOkonko, D. (Darlington)|||/items/d79a3fa8-adcf-4905-bc75-e4fcacb383f0Sawyer, G. (Greta)|||/items/22d9a898-ace6-4a51-a94b-1d2b76ceb15dZoccarato, A. (Anna)|||/items/bdd86a00-0deb-42de-a739-a2268fd2d6c0Catibog, N. (Norman)|||/items/b2c6e5cc-a4b8-439c-919b-6b62d995c705Lopez-Salazar, M.B. (María Begoña)|||/items/153e0e37-14b0-403e-afab-8af00c4edde0Gonzalez, A. (Arantxa)|||/items/9c64c0f4-66b4-4b51-8593-0e50c091a515Ravassa-Albéniz, S. (Susana)|||/items/df0c1eb3-9f45-4d77-a7a5-aca2bcf425e1Diez-Espino, J. (Javier)|||/items/125690ae-ba81-4d29-a748-e644f3584853Shah, A.M. (Ajay M.)|||/items/3bc739ce-1498-4741-8de7-e054feba2801CardiomyocyteHeartMitochondriaPressure overloadUnfolded protein responseBackground The mitochondrial unfolded protein response (UPRmt) is activated when misfolded proteins accumulate within mitochondria and leads to increased expression of mitochondrial chaperones and proteases to maintain protein quality and mitochondrial function. Cardiac mitochondria are essential for contractile function and regulation of cell viability, while mitochondrial dysfunction characterizes heart failure. The role of the UPRmt in the heart is unclear. Objectives The purpose of this study was to: 1) identify conditions that activate the UPRmt in the heart; and 2) study the relationship among the UPRmt, mitochondrial function, and cardiac contractile function. Methods Cultured cardiac myocytes were subjected to different stresses in vitro. Mice were subjected to chronic pressure overload. Tissues and blood biomarkers were studied in patients with aortic stenosis. Results Diverse neurohumoral or mitochondrial stresses transiently induced the UPRmt in cultured cardiomyocytes. The UPRmt was also induced in the hearts of mice subjected to chronic hemodynamic overload. Boosting the UPRmt with nicotinamide riboside (which augments NAD+ pools) in cardiomyocytes in vitro or hearts in vivo significantly mitigated the reductions in mitochondrial oxygen consumption induced by these stresses. In mice subjected to pressure overload, nicotinamide riboside reduced cardiomyocyte death and contractile dysfunction. Myocardial tissue from patients with aortic stenosis also showed evidence of UPRmt activation, which correlated with reduced tissue cardiomyocyte death and fibrosis and lower plasma levels of biomarkers of cardiac damage (high-sensitivity troponin T) and dysfunction (N-terminal pro–B-type natriuretic peptide). Conclusions These results identify the induction of the UPRmt in the mammalian (including human) heart exposed to pathological stresses. Enhancement of the UPRmt ameliorates mitochondrial and contractile dysfunction, suggesting that it may serve an important protective role in the stressed heart.Elsevier BVDadun. Depósito Académico Digital Universidad de Navarra20222022-03-1120192019-01-0120192019-01-01journal articlehttp://purl.org/coar/resource_type/c_6501info:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/10171/63144reponame:Dadun. Depósito Académico Digital de la Universidad de Navarrainstname:Universidad de NavarraInglésengopen accesshttp://purl.org/coar/access_right/c_abf2info:eu-repo/semantics/openAccessoai:dadun.unav.edu:10171/631442026-06-21T12:47:57Z
dc.title.none.fl_str_mv Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
title Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
spellingShingle Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
Smyrnias, I. (Ioannis)|||/items/d5ab339a-af96-4b6c-a384-6588f4d711a2
Cardiomyocyte
Heart
Mitochondria
Pressure overload
Unfolded protein response
title_short Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
title_full Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
title_fullStr Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
title_full_unstemmed Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
title_sort Cardioprotective effect of the mitochondrial unfolded protein response during chronic pressure overload
dc.creator.none.fl_str_mv Smyrnias, I. (Ioannis)|||/items/d5ab339a-af96-4b6c-a384-6588f4d711a2
Gray, S.P. (Stephen P.)|||/items/33ad7431-c580-46c5-928a-0d50a219dc7e
Okonko, D. (Darlington)|||/items/d79a3fa8-adcf-4905-bc75-e4fcacb383f0
Sawyer, G. (Greta)|||/items/22d9a898-ace6-4a51-a94b-1d2b76ceb15d
Zoccarato, A. (Anna)|||/items/bdd86a00-0deb-42de-a739-a2268fd2d6c0
Catibog, N. (Norman)|||/items/b2c6e5cc-a4b8-439c-919b-6b62d995c705
Lopez-Salazar, M.B. (María Begoña)|||/items/153e0e37-14b0-403e-afab-8af00c4edde0
Gonzalez, A. (Arantxa)|||/items/9c64c0f4-66b4-4b51-8593-0e50c091a515
Ravassa-Albéniz, S. (Susana)|||/items/df0c1eb3-9f45-4d77-a7a5-aca2bcf425e1
Diez-Espino, J. (Javier)|||/items/125690ae-ba81-4d29-a748-e644f3584853
Shah, A.M. (Ajay M.)|||/items/3bc739ce-1498-4741-8de7-e054feba2801
author Smyrnias, I. (Ioannis)|||/items/d5ab339a-af96-4b6c-a384-6588f4d711a2
author_facet Smyrnias, I. (Ioannis)|||/items/d5ab339a-af96-4b6c-a384-6588f4d711a2
Gray, S.P. (Stephen P.)|||/items/33ad7431-c580-46c5-928a-0d50a219dc7e
Okonko, D. (Darlington)|||/items/d79a3fa8-adcf-4905-bc75-e4fcacb383f0
Sawyer, G. (Greta)|||/items/22d9a898-ace6-4a51-a94b-1d2b76ceb15d
Zoccarato, A. (Anna)|||/items/bdd86a00-0deb-42de-a739-a2268fd2d6c0
Catibog, N. (Norman)|||/items/b2c6e5cc-a4b8-439c-919b-6b62d995c705
Lopez-Salazar, M.B. (María Begoña)|||/items/153e0e37-14b0-403e-afab-8af00c4edde0
Gonzalez, A. (Arantxa)|||/items/9c64c0f4-66b4-4b51-8593-0e50c091a515
Ravassa-Albéniz, S. (Susana)|||/items/df0c1eb3-9f45-4d77-a7a5-aca2bcf425e1
Diez-Espino, J. (Javier)|||/items/125690ae-ba81-4d29-a748-e644f3584853
Shah, A.M. (Ajay M.)|||/items/3bc739ce-1498-4741-8de7-e054feba2801
author_role author
author2 Gray, S.P. (Stephen P.)|||/items/33ad7431-c580-46c5-928a-0d50a219dc7e
Okonko, D. (Darlington)|||/items/d79a3fa8-adcf-4905-bc75-e4fcacb383f0
Sawyer, G. (Greta)|||/items/22d9a898-ace6-4a51-a94b-1d2b76ceb15d
Zoccarato, A. (Anna)|||/items/bdd86a00-0deb-42de-a739-a2268fd2d6c0
Catibog, N. (Norman)|||/items/b2c6e5cc-a4b8-439c-919b-6b62d995c705
Lopez-Salazar, M.B. (María Begoña)|||/items/153e0e37-14b0-403e-afab-8af00c4edde0
Gonzalez, A. (Arantxa)|||/items/9c64c0f4-66b4-4b51-8593-0e50c091a515
Ravassa-Albéniz, S. (Susana)|||/items/df0c1eb3-9f45-4d77-a7a5-aca2bcf425e1
Diez-Espino, J. (Javier)|||/items/125690ae-ba81-4d29-a748-e644f3584853
Shah, A.M. (Ajay M.)|||/items/3bc739ce-1498-4741-8de7-e054feba2801
author2_role author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Dadun. Depósito Académico Digital Universidad de Navarra
dc.subject.none.fl_str_mv Cardiomyocyte
Heart
Mitochondria
Pressure overload
Unfolded protein response
topic Cardiomyocyte
Heart
Mitochondria
Pressure overload
Unfolded protein response
description Background The mitochondrial unfolded protein response (UPRmt) is activated when misfolded proteins accumulate within mitochondria and leads to increased expression of mitochondrial chaperones and proteases to maintain protein quality and mitochondrial function. Cardiac mitochondria are essential for contractile function and regulation of cell viability, while mitochondrial dysfunction characterizes heart failure. The role of the UPRmt in the heart is unclear. Objectives The purpose of this study was to: 1) identify conditions that activate the UPRmt in the heart; and 2) study the relationship among the UPRmt, mitochondrial function, and cardiac contractile function. Methods Cultured cardiac myocytes were subjected to different stresses in vitro. Mice were subjected to chronic pressure overload. Tissues and blood biomarkers were studied in patients with aortic stenosis. Results Diverse neurohumoral or mitochondrial stresses transiently induced the UPRmt in cultured cardiomyocytes. The UPRmt was also induced in the hearts of mice subjected to chronic hemodynamic overload. Boosting the UPRmt with nicotinamide riboside (which augments NAD+ pools) in cardiomyocytes in vitro or hearts in vivo significantly mitigated the reductions in mitochondrial oxygen consumption induced by these stresses. In mice subjected to pressure overload, nicotinamide riboside reduced cardiomyocyte death and contractile dysfunction. Myocardial tissue from patients with aortic stenosis also showed evidence of UPRmt activation, which correlated with reduced tissue cardiomyocyte death and fibrosis and lower plasma levels of biomarkers of cardiac damage (high-sensitivity troponin T) and dysfunction (N-terminal pro–B-type natriuretic peptide). Conclusions These results identify the induction of the UPRmt in the mammalian (including human) heart exposed to pathological stresses. Enhancement of the UPRmt ameliorates mitochondrial and contractile dysfunction, suggesting that it may serve an important protective role in the stressed heart.
publishDate 2019
dc.date.none.fl_str_mv 2019
2019-01-01
2019
2019-01-01
2022
2022-03-11
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/10171/63144
url https://hdl.handle.net/10171/63144
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
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
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier BV
publisher.none.fl_str_mv Elsevier BV
dc.source.none.fl_str_mv reponame:Dadun. Depósito Académico Digital de la Universidad de Navarra
instname:Universidad de Navarra
instname_str Universidad de Navarra
reponame_str Dadun. Depósito Académico Digital de la Universidad de Navarra
collection Dadun. Depósito Académico Digital de la Universidad de Navarra
repository.name.fl_str_mv
repository.mail.fl_str_mv
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