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Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity

Memory CD8 T cells can provide long-term protection against tumors, which depends on their enhanced proliferative capacity, self-renewal and unique metabolic rewiring to sustain cellular fitness. Specifically, memory CD8 T cells engage oxidative phosphorylation and fatty acid oxidation to fulfill th...

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Autores principales: Dumauthioz, Nina, Tschumi, Benjamin, Wenes, Mathias, Marti, Bastien, Wang, Haiping, Franco, Fabien, Li, Wenhui, Lopez-Mejia, Isabel C., Fajas, Lluis, Ho, Ping-Chih, Donda, Alena, Romero, Pedro, Zhang, Lianjun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245409/
https://www.ncbi.nlm.nih.gov/pubmed/32055005
http://dx.doi.org/10.1038/s41423-020-0365-3
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author Dumauthioz, Nina
Tschumi, Benjamin
Wenes, Mathias
Marti, Bastien
Wang, Haiping
Franco, Fabien
Li, Wenhui
Lopez-Mejia, Isabel C.
Fajas, Lluis
Ho, Ping-Chih
Donda, Alena
Romero, Pedro
Zhang, Lianjun
author_facet Dumauthioz, Nina
Tschumi, Benjamin
Wenes, Mathias
Marti, Bastien
Wang, Haiping
Franco, Fabien
Li, Wenhui
Lopez-Mejia, Isabel C.
Fajas, Lluis
Ho, Ping-Chih
Donda, Alena
Romero, Pedro
Zhang, Lianjun
author_sort Dumauthioz, Nina
collection PubMed
description Memory CD8 T cells can provide long-term protection against tumors, which depends on their enhanced proliferative capacity, self-renewal and unique metabolic rewiring to sustain cellular fitness. Specifically, memory CD8 T cells engage oxidative phosphorylation and fatty acid oxidation to fulfill their metabolic demands. In contrast, tumor-infiltrating lymphocytes (TILs) display severe metabolic defects, which may underlie their functional decline. Here, we show that overexpression of proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α), the master regulator of mitochondrial biogenesis (MB), favors CD8 T cell central memory formation rather than resident memory generation. PGC-1α-overexpressing CD8 T cells persist and mediate more robust recall responses to bacterial infection or peptide vaccination. Importantly, CD8 T cells with enhanced PGC-1α expression provide stronger antitumor immunity in a mouse melanoma model. Moreover, TILs overexpressing PGC-1α maintain higher mitochondrial activity and improved expansion when rechallenged in a tumor-free host. Altogether, our findings indicate that enforcing mitochondrial biogenesis promotes CD8 T cell memory formation, metabolic fitness, and antitumor immunity in vivo.
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spelling pubmed-82454092021-07-16 Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity Dumauthioz, Nina Tschumi, Benjamin Wenes, Mathias Marti, Bastien Wang, Haiping Franco, Fabien Li, Wenhui Lopez-Mejia, Isabel C. Fajas, Lluis Ho, Ping-Chih Donda, Alena Romero, Pedro Zhang, Lianjun Cell Mol Immunol Article Memory CD8 T cells can provide long-term protection against tumors, which depends on their enhanced proliferative capacity, self-renewal and unique metabolic rewiring to sustain cellular fitness. Specifically, memory CD8 T cells engage oxidative phosphorylation and fatty acid oxidation to fulfill their metabolic demands. In contrast, tumor-infiltrating lymphocytes (TILs) display severe metabolic defects, which may underlie their functional decline. Here, we show that overexpression of proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α), the master regulator of mitochondrial biogenesis (MB), favors CD8 T cell central memory formation rather than resident memory generation. PGC-1α-overexpressing CD8 T cells persist and mediate more robust recall responses to bacterial infection or peptide vaccination. Importantly, CD8 T cells with enhanced PGC-1α expression provide stronger antitumor immunity in a mouse melanoma model. Moreover, TILs overexpressing PGC-1α maintain higher mitochondrial activity and improved expansion when rechallenged in a tumor-free host. Altogether, our findings indicate that enforcing mitochondrial biogenesis promotes CD8 T cell memory formation, metabolic fitness, and antitumor immunity in vivo. Nature Publishing Group UK 2020-02-13 2021-07 /pmc/articles/PMC8245409/ /pubmed/32055005 http://dx.doi.org/10.1038/s41423-020-0365-3 Text en © The Author(s) 2020 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Dumauthioz, Nina
Tschumi, Benjamin
Wenes, Mathias
Marti, Bastien
Wang, Haiping
Franco, Fabien
Li, Wenhui
Lopez-Mejia, Isabel C.
Fajas, Lluis
Ho, Ping-Chih
Donda, Alena
Romero, Pedro
Zhang, Lianjun
Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity
title Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity
title_full Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity
title_fullStr Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity
title_full_unstemmed Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity
title_short Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity
title_sort enforced pgc-1α expression promotes cd8 t cell fitness, memory formation and antitumor immunity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245409/
https://www.ncbi.nlm.nih.gov/pubmed/32055005
http://dx.doi.org/10.1038/s41423-020-0365-3
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