Cited by 523T-cell and B-cell ImmunologyMitochondrial Function and PathologyCancer, Hypoxia, and Metabolism

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CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability

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van der Windt, Gerritje J. W., O’Sullivan, David, Everts, Bart, Huang, Stanley Ching-Cheng, Buck, Michael D., Curtis, Jonathan D., Chang, Chih-Hao, Smith, Amber M., Ai, Teresa, Faubert, Brandon, Jones, Russell G., Pearce, Edward J., Pearce, Erika L.·2013·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1221740110PMC PMC3761631

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Abstract

A characteristic of memory T (T M ) cells is their ability to mount faster and stronger responses to reinfection than naïve T (T N ) cells do in response to an initial infection. However, the mechanisms that allow this rapid recall are not completely understood. We found that CD8 T M cells have more mitochondrial mass than CD8 T N cells and, that upon activation, the resulting secondary effector T (T E ) cells proliferate more quickly, produce more cytokines, and maintain greater ATP levels than primary effector T cells. We also found that after activation, T M cells increase oxidative phosphorylation and aerobic glycolysis and sustain this increase to a greater extent than T N cells, suggesting that greater mitochondrial mass in T M cells not only promotes oxidative capacity, but also glycolytic capacity. We show that mitochondrial ATP is essential for the rapid induction of glycolysis in response to activation and the initiation of proliferation of both T N and T M cells. We also found that fatty acid oxidation is needed for T M cells to rapidly respond upon restimulation. Finally, we show that dissociation of the glycolysis enzyme hexokinase from mitochondria impairs proliferation and blocks the rapid induction of glycolysis upon T-cell receptor stimulation in T M cells. Our results demonstrate that greater mitochondrial mass endows T M cells with a bioenergetic advantage that underlies their ability to rapidly recall in response to reinfection.

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Lineage relationship and protective immunity of memory CD8 T cell subsets
Wherry, E. J., Teichgräber, V., Becker, T. C., Masopust, D., Kaech, S. M., Antia, R., von Andrian, U. H., & Ahmed, R. (2003) · Nature Immunology · doi:10.1038/ni889 · Cited by 1,864
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van der Windt, G. J. W., Everts, B., Chang, C.-H., Curtis, J. D., Freitas, T. C., Amiel, E., Pearce, E. J., & Pearce, E. L. (2012) · Immunity · doi:10.1016/j.immuni.2011.12.007 · Cited by 1,540
Self-citation
Molecular and functional profiling of memory CD8 T cell differentiation.
Kaech, S., Hemby, S., Kersh, E., & Ahmed, R. (2002) · Cell · doi:10.1016/s0092-8674(02)01139-x · Cited by 1,081
A Mitochondrial Pyruvate Carrier Required for Pyruvate Uptake in Yeast, Drosophila , and Humans
Bricker, D. K., Taylor, E. B., Schell, J. C., Orsak, T., Boutron, A., Chen, Y.-C., Cox, J. E., Cardon, C. M., Van Vranken, J. G., Dephoure, N., et al. (2012) · Science · doi:10.1126/science.1218099 · Cited by 843
Fuel feeds function: energy metabolism and the T-cell response
Fox, C. J., Hammerman, P. S., & Thompson, C. B. (2005) · Nature reviews. Immunology · doi:10.1038/nri1710 · Cited by 841
Hexokinase-Mitochondria Interaction Mediated by Akt Is Required to Inhibit Apoptosis in the Presence or Absence of Bax and Bak
Majewski, N., Nogueira, V., Bhaskar, P. T., Coy, P. E., Skeen, J. E., Gottlob, K., Chandel, N. S., Thompson, C. B., Robey, R. B., & Hay, N. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.11.014 · Cited by 638
Metabolic switching and fuel choice during T‐cell differentiation and memory development
van der Windt, G. J. W., & Pearce, E. L. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01150.x · Cited by 563
Self-citation
Response of naïve and memory CD8+ T cells to antigen stimulation in vivo
Veiga‐Fernandes, H., Walter, U., Bourgeois, C., McLean, A. R., & Rocha, B. (2000) · Nature Immunology · doi:10.1038/76907 · Cited by 547
In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability
Rathmell, J. C., Heiden, M. G. V., Harris, M. H., Frauwirth, K. A., & Thompson, C. B. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00066-6 · Cited by 467

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Authors: van der Windt, G. J. W., O’Sullivan, D., Everts, B., Huang, S. C.-C., Buck, M. D., Curtis, J. D., Chang, C.-H., Smith, A. M., Ai, T., Faubert, B., Jones, R. G., Pearce, E. J., & Pearce, E. L.
Affiliations: Department of Pathology and Immunology, Washington University School of Medicine in St. Louis, St. Louis, MO 63110; and
Washington University in St. Louis (US)
McGill University (CA)
ORCID: O’Sullivan, David
Everts, Bart
Huang, Stanley Ching-Cheng
Buck, Michael D.
Curtis, Jonathan D.
Chang, Chih-Hao
Smith, Amber M.
Ai, Teresa
Faubert, Brandon
Jones, Russell G.
Pearce, Edward J.
Pearce, Erika L.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2013-08-12
Volume: 110
Issue: 35
Pages: 14336-14341
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1221740110
PMC: PMC3761631
OpenAlex: W2061318708
Cited by: 523
References: 39
Citations by year: 2026: 27 · 2025: 29 · 2024: 27 · 2023: 40 · 2022: 50 · 2021: 54 · 2020: 55 · 2019: 56 · 2018: 44 · 2017: 46 · 2016: 44 · 2015: 30 · 2014: 19 · 2013: 2
FWCI: 17.50
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Pure Amsterdam UMC (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders: National Cancer Institute (R01CA164062)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Keywords: memory CD8+ T cells, mitochondrial mass, recall response, oxidative phosphorylation, aerobic glycolysis, fatty acid oxidation, hexokinase, mitochondrial ATP, T cell proliferation, T cell receptor stimulation, cytokine production
MeSH terms: Animals, Energy Metabolism, Immunologic Memory, Lymphocyte Activation, CD8-Positive T-Lymphocytes, Mice, Mitochondrial Size

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CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability

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