The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability
Open accessAbstract
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“We have recently shown that increased mitochondrial mass and SRC of TM cells allows for rapid mitochondrial ATP production upon TCR engagement, conferring a bioenergetic advantage to TM cells upon secondary exposure to antigen (16).”
From Fueling Immunity: Insights into Metabolism and Lymphocyte Function (2013) · cites this paper as [16]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Posttranscriptional Control of T Cell Effector Function by Aerobic Glycolysis
Chang, C.-H., Curtis, J. D., Maggi, L. B., Faubert, B., Villarino, A. V., O’Sullivan, D., Huang, S. C.-C., van der Windt, G. J. W., Blagih, J., Qiu, J., et al. (2013) · Cell · doi:10.1016/j.cell.2013.05.016 · Cited by 2,204
Self-citationLineage 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
Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development
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-citationMolecular 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
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-citationResponse 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
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
Cited by
Sorted by citations
A guide to immunometabolism for immunologists
O'Neill, L. A. J., Kishton, R. J., & Rathmell, J. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2016.70 · Cited by 3,315
Mitochondrial Dynamics Controls T Cell Fate through Metabolic Programming
Buck, M. D., O’Sullivan, D., Geltink, R. I. K., Curtis, J. D., Chang, C., Sanin, D. E., Qiu, J., Kretz, O., Braas, D., van der Windt, G. J. W., et al. (2016) · Cell · doi:10.1016/j.cell.2016.05.035 · Cited by 1,491
Self-citationFueling Immunity: Insights into Metabolism and Lymphocyte Function
Pearce, E. L., Poffenberger, M. C., Chang, C.-H., & Jones, R. G. (2013) · Science · doi:10.1126/science.1242454 · Cited by 1,363
Self-citationThommen, D. S., & Schumacher, T. N. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.03.012 · Cited by 1,351
Homeostatic Immunity and the Microbiota
Belkaid, Y., & Harrison, O. J. (2017) · Immunity · doi:10.1016/j.immuni.2017.04.008 · Cited by 1,261
Kawalekar, O. U., O’Connor, R. S., Fraietta, J. A., Guo, L., McGettigan, S. E., Posey, A. D., Patel, P. R., Guedan, S., Scholler, J., Keith, B., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.01.021 · Cited by 1,267
T cell metabolism drives immunity
Buck, M. D., O’Sullivan, D., & Pearce, E. L. (2015) · The Journal of Experimental Medicine · doi:10.1084/jem.20151159 · Cited by 1,238
Self-citationThommen, D. S., Koelzer, V. H., Herzig, P., Roller, A., Trefny, M., Dimeloe, S., Kiialainen, A., Hanhart, J., Schill, C., Hess, C., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0057-z · Cited by 1,161
“0 10 20 30 40 50 Mitotic cell cycle (12) Cell division (9) Cell-cell signaling (9) Cell proliferation (80) Chromatin assembly (19) DNA repair (46) DNA metabolic process (70) DNA replication (41) Cell division (81) Cell cycle process (133) Cell cycle (156)”
BackgroundEverts, B., Amiel, E., Huang, S. C.-C., Smith, A. M., Chang, C.-H., Lam, W. Y., Redmann, V., Freitas, T. C., Blagih, J., van der Windt, G. J. W., et al. (2014) · Nature Immunology · doi:10.1038/ni.2833 · Cited by 1,064
Self-citationMetabolism of immune cells in cancer
Leone, R. D., & Powell, J. D. (2020) · Nature Reviews Cancer · doi:10.1038/s41568-020-0273-y · Cited by 877
Scharping, N. E., Menk, A. V., Moreci, R. S., Whetstone, R. D., Dadey, R. E., Watkins, S. C., Ferris, R. L., & Delgoffe, G. M. (2016) · Immunity · doi:10.1016/j.immuni.2016.07.009 · Cited by 848
Unraveling the Complex Interplay Between T Cell Metabolism and Function
Geltink, R. I. K., Kyle, R. L., & Pearce, E. L. (2018) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053019 · Cited by 849
Self-citationO’Sullivan, D., van der Windt, G. J. W., Huang, S. C.-C., Curtis, J. D., Chang, C.-H., Buck, M. D., Qiu, J., Smith, A. M., Lam, W. Y., DiPlato, L. M., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.005 · Cited by 790
Self-citationMetabolic coordination of T cell quiescence and activation
Chapman, N. M., Boothby, M. R., & Chi, H. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0203-y · Cited by 793
Scharping, N. E., Menk, A. V., Moreci, R. S., Whetstone, R. D., Dadey, R., Watkins, S. C., Ferris, R. L., & Delgoffe, G. M. (2016) · Immunity · doi:10.1016/j.immuni.2016.08.009 · Cited by 708
The Energy Sensor AMPK Regulates T Cell Metabolic Adaptation and Effector Responses In Vivo
Blagih, J., Coulombe, F., Vincent, E. E., Dupuy, F., Galicia-Vázquez, G., Yurchenko, E., Raissi, T. C., van der Windt, G. J. W., Viollet, B., Pearce, E. L., et al. (2015) · Immunity · doi:10.1016/j.immuni.2014.12.030 · Cited by 679
Self-citationGlycolysis – a key player in the inflammatory response
Soto‐Heredero, G., Heras, M. M. G. D. L., Gabandé‐Rodríguez, E., Oller, J., & Mittelbrunn, M. (2020) · FEBS Journal · doi:10.1111/febs.15327 · Cited by 660
CD8+ T cell metabolism in infection and cancer
Reina‐Campos, M., Scharping, N. E., & Goldrath, A. W. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00537-8 · Cited by 657
T memory stem cells in health and disease
Gattinoni, L., Speiser, D. E., Lichterfeld, M. D., & Bonini, C. (2017) · Nature Medicine · doi:10.1038/nm.4241 · Cited by 648
Argüello, R. J., Combes, A. J., Char, R., Gigan, J. P., Baaziz, A. I., Bousiquot, E., Camosseto, V., Samad, B., Tsui, J. L., Yan, P., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.11.007 · Cited by 607
Regulatory circuits of T cell function in cancer
Speiser, D. E., Ho, P., & Verdeil, G. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.80 · Cited by 570
Understanding subset diversity in T cell memory
Jameson, S. C., & Masopust, D. (2018) · Immunity · doi:10.1016/j.immuni.2018.02.010 · Cited by 523
Redox regulation of immunometabolism
Muri, J., & Köpf, M. (2020) · Nature reviews. Immunology · doi:10.1038/s41577-020-00478-8 · Cited by 519
Pearce, E. J., & Everts, B. (2014) · Nature reviews. Immunology · doi:10.1038/nri3771 · Cited by 500
Self-citationMenk, A. V., Scharping, N. E., Moreci, R. S., Zeng, X., Guy, C. S., Salvatore, S. R., Bae, H. R., Xie, J., Young, H. A., Wendell, S. G., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.040 · Cited by 496
Metabolic pathways in T cell activation and lineage differentiation
Almeida, L., Lochner, M., Berod, L., & Sparwasser, T. D. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.10.009 · Cited by 492
CD8+ T cells in the cancer-immunity cycle
Giles, J. R., Globig, A.-M., Kaech, S. M., & Wherry, E. J. (2023) · Immunity · doi:10.1016/j.immuni.2023.09.005 · Cited by 507
Immunometabolism: Cellular Metabolism Turns Immune Regulator
Loftus, R. M., & Finlay, D. K. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.693903 · Cited by 460
Fatty acid metabolism in the regulation of T cell function
Lochner, M., Berod, L., & Sparwasser, T. D. (2015) · Trends in Immunology · doi:10.1016/j.it.2014.12.005 · Cited by 427
Chamoto, K., Chowdhury, P. S., Kumar, A., Sonomura, K., Matsuda, F., Fagarasan, S., & Honjo, T. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620433114 · Cited by 419
mTORC1 and mTORC2 selectively regulate CD8+ T cell differentiation
Pollizzi, K. N., Patel, C. H., Sun, I., Oh, M. H., Waickman, A. T., Wen, J., Delgoffe, G. M., & Powell, J. D. (2015) · Journal of Clinical Investigation · doi:10.1172/jci77746 · Cited by 417
Raud, B., Roy, D. G., Divakaruni, A. S., Tarasenko, T. N., Franke, R., Ma, E. H., Samborska, B., Hsieh, W. Y., Wong, A., Stüve, P., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.06.002 · Cited by 401
Self-citationStaron, M. M., Gray, S. M., Marshall, H. D., Parish, I. A., Chen, J. H., Perry, C. J., Cui, G., Li, M. O., & Kaech, S. M. (2014) · Immunity · doi:10.1016/j.immuni.2014.10.013 · Cited by 398
Integrating canonical and metabolic signalling programmes in the regulation of T cell responses
Pollizzi, K. N., & Powell, J. D. (2014) · Nature reviews. Immunology · doi:10.1038/nri3701 · Cited by 395
Ma, E. H., Verway, M. J., Johnson, R. M., Roy, D. G., Steadman, M., Hayes, S., Williams, K. S., Sheldon, R. D., Samborska, B., Kosinski, P. A., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.09.003 · Cited by 379
Self-citationBalmer, M. L., Ma, E. H., Bantug, G. R., Grählert, J., Pfister, S., Glatter, T., Jauch, A., Dimeloe, S., Slack, E., Dehio, P., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.03.016 · Cited by 361
Self-citationCrompton, J. G., Sukumar, M., Roychoudhuri, R., Clever, D. C., Gros, A., Eil, R. L., Tran, E., Hanada, K., Yu, Z., Palmer, D. C., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-2277 · Cited by 354
Emerging concepts of T cell metabolism as a target of immunotherapy
Chang, C., & Pearce, E. L. (2016) · Nature Immunology · doi:10.1038/ni.3415 · Cited by 345
Self-citationMetabolic signaling in T cells
Shyer, J. A., Flavell, R. A., & Bailis, W. (2020) · Cell Research · doi:10.1038/s41422-020-0379-5 · Cited by 346
Reactive Oxygen Species: Involvement in T Cell Signaling and Metabolism
Franchina, D. G., Dostert, C., & Brenner, D. (2018) · Trends in Immunology · doi:10.1016/j.it.2018.01.005 · Cited by 334
Marchetti, P., Fovez, Q., Germain, N., Khamari, R., & Kluza, J. (2020) · The FASEB Journal · doi:10.1096/fj.202000767r · Cited by 321
Metabolic regulation of inflammation
Gaber, T., Strehl, C., & Buttgereit, F. (2017) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2017.37 · Cited by 320
Menk, A. V., Scharping, N. E., Rivadeneira, D. B., Calderon, M. J., Watson, M. J., Dunstane, D., Watkins, S. C., & Delgoffe, G. M. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20171068 · Cited by 322
Targeting metabolism to regulate immune responses in autoimmunity and cancer
Patel, C. H., Leone, R. D., Horton, M. R., & Powell, J. D. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0032-5 · Cited by 311
Mathew, N. R., Baumgartner, F., Braun, L. M., O’Sullivan, D., Thomas, S., Waterhouse, M., Müller, T. A., Hanke, K., Taromi, S., Apostolova, P., et al. (2018) · Nature Medicine · doi:10.1038/nm.4484 · Cited by 300
Self-citationGeltink, R. I. K., O’Sullivan, D., Corrado, M., Bremser, A., Buck, M. D., Buescher, J. M., Firat, E., Zhu, X., Niedermann, G., Caputa, G., et al. (2017) · Cell · doi:10.1016/j.cell.2017.08.018 · Cited by 305
Self-citationMetabolic and Epigenetic Coordination of T Cell and Macrophage Immunity
Phan, A. T., Goldrath, A. W., & Glass, C. K. (2017) · Immunity · doi:10.1016/j.immuni.2017.04.016 · Cited by 296
High salt reduces the activation of IL-4– and IL-13–stimulated macrophages
Binger, K. J., Gebhardt, M., Heinig, M., Rintisch, C., Schroeder, A., Neuhofer, W., Hilgers, K. F., Manzel, A., Schwartz, C., Kleinewietfeld, M., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci80919 · Cited by 283
Regulatory T Cell Migration Is Dependent on Glucokinase-Mediated Glycolysis
Kishore, M., Cheung, K. C.-P., Fu, H., Bonacina, F., Wang, G., Coe, D., Ward, E. J., Colamatteo, A., Jangani, M., Baragetti, A., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.10.017 · Cited by 281
mTORC 1 and mTORC 2 as regulators of cell metabolism in immunity
Linke, M., Fritsch, S. D., Sukhbaatar, N., Hengstschläger, M., & Weichhart, T. (2017) · FEBS Letters · doi:10.1002/1873-3468.12711 · Cited by 283
Baldwin, J., Heuser-Loy, C., Saha, T., Schelker, R. C., Slavkovic‐Lukic, D., Strieder, N., Hernandez-Lopez, I., Rana, N., Barden, M., Mastrogiovanni, F., et al. (2024) · Cell · doi:10.1016/j.cell.2024.08.029 · Cited by 266
Complement Regulates Nutrient Influx and Metabolic Reprogramming during Th1 Cell Responses
Kolev, M. V., Dimeloe, S., Friec, G. L., Navarini, A. A., Arbore, G., Povoleri, G. A. M., Fischer, M., Belle, R., Loeliger, J., Develioglu, L., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.05.024 · Cited by 269
Targeting T cell metabolism for therapy
O’Sullivan, D., & Pearce, E. L. (2015) · Trends in Immunology · doi:10.1016/j.it.2014.12.004 · Cited by 261
Self-citationHan, S., Zaretsky, A. G., Andrade‐Oliveira, V., Collins, N., Dzutsev, A. H., Shaik, J. S., da Fonseca, D. M., Harrison, O. J., Tamoutounour, S., Byrd, A. L., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.11.009 · Cited by 250
Mitochondrial function in immune cells in health and disease
Faas, M. M., & de Vos, P. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165845 · Cited by 252
Targeting memory T cell metabolism to improve immunity
Corrado, M., & Pearce, E. L. (2022) · Journal of Clinical Investigation · doi:10.1172/jci148546 · Cited by 250
Self-citationMetabolic Control of CD8+ T Cell Fate Decisions and Antitumor Immunity
Zhang, L., & Romero, P. J. (2017) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.11.005 · Cited by 241
Pollizzi, K. N., Sun, I., Patel, C. H., Lo, Y.-C., Oh, M. H., Waickman, A. T., Tam, A. J., Blosser, R. L., Wen, J., Delgoffe, G. M., et al. (2016) · Nature Immunology · doi:10.1038/ni.3438 · Cited by 243
A guide to adaptive immune memory
Lam, N., Lee, Y. S., & Färber, D. L. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-01040-6 · Cited by 236
Immunometabolic circuits in trained immunity
Arts, R. J. W., Joosten, L. A. B., & Netea, M. G. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.09.002 · Cited by 228
Modification of Proteins by Metabolites in Immunity
Diskin, C., Ryan, T. A. J., & O'Neill, L. A. J. (2020) · Immunity · doi:10.1016/j.immuni.2020.09.014 · Cited by 215
Time-resolved systems immunology reveals a late juncture linked to fatal COVID-19
Liu, C., Martins, A. J., Lau, W. W., Rachmaninoff, N., Chen, J., Imberti, L., Mostaghimi, D., Fink, D. L., Burbelo, P. D., Dobbs, K., et al. (2021) · Cell · doi:10.1016/j.cell.2021.02.018 · Cited by 214
Metabolic Barriers to T Cell Function in Tumors
Sugiura, A., & Rathmell, J. C. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701041 · Cited by 208
Wilhelm, C., Harrison, O. J., Schmitt, V., Pelletier, M., Spencer, S. P., Urban, J. F., Ploch, M., Ramalingam, T. R., Siegel, R. M., & Belkaid, Y. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20151448 · Cited by 215
Role of mitochondrial alterations in human cancer progression and cancer immunity
Wang, S., Tseng, L., & Lee, H. (2023) · Journal of Biomedical Science · doi:10.1186/s12929-023-00956-w · Cited by 225
The CPT1a inhibitor, etomoxir induces severe oxidative stress at commonly used concentrations
O’Connor, R. S., Guo, L., Ghassemi, S., Snyder, N. W., Worth, A. J., Weng, L., Kam, Y., Philipson, B. I., Trefely, S., Nuñez-Cruz, S., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-24676-6 · Cited by 216
Phan, A. T., Doedens, A. L., Palazón, A., Tyrakis, P. A., Cheung, K. P., Johnson, R. S., & Goldrath, A. W. (2016) · Immunity · doi:10.1016/j.immuni.2016.10.017 · Cited by 207
Immunometabolism in the Single-Cell Era
Artyomov, M. N., & den Bossche, J. V. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.09.013 · Cited by 217
T‐cell metabolism governing activation, proliferation and differentiation; a modular view
Dimeloe, S., Burgener-Gasser, A.-V., Grählert, J., & Hess, C. (2016) · Immunology · doi:10.1111/imm.12655 · Cited by 202
Bantug, G. R., Fischer, M., Grählert, J., Balmer, M. L., Unterstab, G., Develioglu, L., Steiner, R., Zhang, L., Costa, A. S. H., Gubser, P. M., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.02.012 · Cited by 196
Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity
Dumauthioz, N., Tschumi, B., Wenes, M., Marti, B., Wang, H., Franco, F., Li, W., López‐Mejía, I. C., Fajas, L., Ho, P., et al. (2020) · Cellular and Molecular Immunology · doi:10.1038/s41423-020-0365-3 · Cited by 199
Valle‐Casuso, J. C., Angin, M., Volant, S., Passaes, C., Monceaux, V., Mikhailova, A., Bourdic, K., Avettand-Fènoël, V., Boufassa, F., Sitbon, M., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.11.015 · Cited by 205
Tumor Microenvironment: A Metabolic Player that Shapes the Immune Response
Cassim, S., & Pouysségur, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010157 · Cited by 192
van Bruggen, J. A. C., Martens, A. W. J., Fraietta, J. A., Hofland, T., Tonino, S. H., Eldering, E., Levin, M.-D., Siska, P. J., Endstra, S., Rathmell, J. C., et al. (2019) · Blood · doi:10.1182/blood.2018885863 · Cited by 187
Measuring Bioenergetics in T Cells Using a Seahorse Extracellular Flux Analyzer
van der Windt, G. J. W., Chang, C., & Pearce, E. L. (2016) · Current Protocols in Immunology · doi:10.1002/0471142735.im0316bs113 · Cited by 189
Self-citationMetabolic Modulation of Immunity: A New Concept in Cancer Immunotherapy
Guerra, L., Bonetti, L., & Brenner, D. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107848 · Cited by 194
Glucose, glycolysis and lymphocyte responses
Donnelly, R. P., & Finlay, D. K. (2015) · Molecular Immunology · doi:10.1016/j.molimm.2015.07.034 · Cited by 193
Tarasenko, T. N., Pacheco, S. E., Koenig, M. K., Gómez‐Rodríguez, J., Kapnick, S. M., Díaz, F., Zerfas, P. M., Barca, E., Sudderth, J., DeBerardinis, R. J., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.05.007 · Cited by 186
Classification of T-cell activation via autofluorescence lifetime imaging
Walsh, A. J., Mueller, K. P., Tweed, K. E., Jones, I., Walsh, C. M., Piscopo, N. J., Niemi, N. M., Pagliarini, D. J., Saha, K., & Skala, M. C. (2020) · Nature Biomedical Engineering · doi:10.1038/s41551-020-0592-z · Cited by 179
The Good and the Bad of Mitochondrial Breakups
Sprenger, H., & Langer, T. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.08.003 · Cited by 179
Sukocheva, O. A., Maksoud, R., Beeraka, N. M., Madhunapantula, S. V., Sinelnikov, M. Y., Nikolenko, V. N., Неганова, М. Е., Klochkov, S. G., Kamal, M. A., Staines, D., et al. (2021) · Journal of Advanced Research · doi:10.1016/j.jare.2021.11.013 · Cited by 182
Targeting Mitochondrial-Derived Reactive Oxygen Species in T Cell-Mediated Autoimmune Diseases
Chávez, M. D., & Tse, H. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.703972 · Cited by 172
C13orf31 (FAMIN) is a central regulator of immunometabolic function
Cader, M. Z., Boroviak, K., Zhang, Q., Assadi, G., Kempster, S. L., Sewell, G. W., Saveljeva, S., Ashcroft, J., Clare, S., Mukhopadhyay, S., et al. (2016) · Nature Immunology · doi:10.1038/ni.3532 · Cited by 173
Mitochondrial activity in T cells
Desdín-Micó, G., Soto‐Heredero, G., & Mittelbrunn, M. (2017) · Mitochondrion · doi:10.1016/j.mito.2017.10.006 · Cited by 171
Metabolic Regulation of Natural Killer Cell IFN-γ Production
Mah-Som, A. Y., & Cooper, M. A. (2016) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.2016017387 · Cited by 170
Dysfunctional T cell metabolism in the tumor microenvironment
Beckermann, K. E., Dudzinski, S. O., & Rathmell, J. C. (2017) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2017.04.003 · Cited by 165
Yu, W., Wang, X., Zhao, J., Liu, R., Liu, J., Wang, Z., Peng, J., Wu, H., Zhang, X., Long, Z., et al. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101761 · Cited by 158
Moreno‐Fernandez, M. E., Giles, D. A., Oates, J. R., Chan, C. C., Damen, M. S. M. A., Doll, J., Stankiewicz, T. E., Chen, X., Chetal, K., Karns, R. A., et al. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.04.018 · Cited by 163
Microenvironmental Metabolism Regulates Antitumor Immunity
Ngwa, V. M., Edwards, D. N., Philip, M., & Chen, J. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-0617 · Cited by 156
Mitochondrial Metabolism Regulation of T Cell–Mediated Immunity
Steinert, E. M., Vasan, K., & Chandel, N. S. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101819-082015 · Cited by 161
Cao, Y., Rathmell, J. C., & Macintyre, A. N. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104104 · Cited by 157
Fatty acid metabolism in CD 8 + T cell memory: Challenging current concepts
Raud, B., McGuire, P. J., Jones, R. G., Sparwasser, T. D., & Berod, L. (2018) · Immunological Reviews · doi:10.1111/imr.12655 · Cited by 155
Self-citationSirt2 Inhibition Enhances Metabolic Fitness and Effector Functions of Tumor-Reactive T Cells
Hamaidi, I., Zhang, L., Kim, N., Wang, M.-H., Iclozan, C., Fang, B., Liu, M., Koomen, J. M., Berglund, A., Yoder, S., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.07.008 · Cited by 148
Exercise immunology: Future directions
Nieman, D. C., & Pence, B. D. (2019) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2019.12.003 · Cited by 154
Klotz, L., Eschborn, M., Lindner, M., Liebmann, M., Herold, M. V. B., Janoschka, C., Garrido, B. T., Schulte‐Mecklenbeck, A., Groß, C. C., Breuer, J., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aao5563 · Cited by 151
Mechanosensing through YAP controls T cell activation and metabolism
Meng, K., Majedi, F. S., Thauland, T. J., & Butte, M. J. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20200053 · Cited by 147
Fundamentals of T Cell Metabolism and Strategies to Enhance Cancer Immunotherapy
Rivera, G. O. R., Knochelmann, H. M., Dwyer, C. J., Smith, A. S., Wyatt, M. M., Rivera-Reyes, A. M., Thaxton, J. E., & Paulos, C. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.645242 · Cited by 154
Self-citationFatty acid oxidation is dispensable for human macrophage IL-4-induced polarization
Namgaladze, D., & Brüne, B. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.06.007 · Cited by 142
Rivadeneira, D. B., DePeaux, K., Wang, Y., Kulkarni, A., Tabib, T., Menk, A. V., Sampath, P., Lafyatis, R., Ferris, R. L., Sarkar, S. N., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.07.003 · Cited by 142
Kouidhi, S., Elgaaïed, A. B., & Chouaïb, S. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00270 · Cited by 145
Metadata
- 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
- 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
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
