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Single cell tuning of Myc expression by antigen receptor signal strength and interleukin‐2 in T lymphocytes
Open accessAbstract
Myc controls the metabolic reprogramming that supports effector T cell differentiation. The expression of Myc is regulated by the T cell antigen receptor (TCR) and pro-inflammatory cytokines such as interleukin-2 (IL-2). We now show that the TCR is a digital switch for Myc mRNA and protein expression that allows the strength of the antigen stimulus to determine the frequency of T cells that express Myc. IL-2 signalling strength also directs Myc expression but in an analogue process that fine-tunes Myc quantity in individual cells via post-transcriptional control of Myc protein. Fine-tuning Myc matters and is possible as Myc protein has a very short half-life in T cells due to its constant phosphorylation by glycogen synthase kinase 3 (GSK3) and subsequent proteasomal degradation. We show that Myc only accumulates in T cells exhibiting high levels of amino acid uptake allowing T cells to match Myc expression to biosynthetic demands. The combination of digital and analogue processes allows tight control of Myc expression at the population and single cell level during immune responses.
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The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation
Wang, R., Dillon, C. P., Shi, L. Z., Milasta, S., Carter, R., Finkelstein, D., McCormick, L. L., Fitzgerald, P., Chi, H., Munger, J., et al. (2011) · Immunity · doi:10.1016/j.immuni.2011.09.021 · Cited by 2,140 · cited 7×
“Myc has other roles in T cells, for example to control glucose and glutamine metabolism and to regulate expression of key transcription factors such as AP4 (Wang et al , 2011a; Chou et al , 2014).”
InfluentialFinlay, D. K., Rosenzweig, E., Sinclair, L. V., Feijoo-Carnero, C., Hukelmann, J. L., Rolf, J., Panteleyev, A. A., Okkenhaug, K., & Cantrell, D. A. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20112607 · Cited by 596
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Cited by
Kumagai, S., Koyama, S., Itahashi, K., Tanegashima, T., Lin, Y.-T., Togashi, Y., Kamada, T., Irie, T., Okumura, G., Kono, H., et al. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.01.001 · Cited by 892
Immunometabolism and natural killer cell responses
O’Brien, K. L., & Finlay, D. K. (2019) · Nature Reviews Immunology · doi:10.1038/s41577-019-0139-2 · Cited by 435
Competition for nutrients and its role in controlling immune responses
Kedia-Mehta, N., & Finlay, D. K. (2019) · Nature Communications · doi:10.1038/s41467-019-10015-4 · Cited by 287
Insulin Receptor-Mediated Stimulation Boosts T Cell Immunity during Inflammation and Infection
Tsai, S., Clemente-Casares, X., Zhou, A. C., Lei, H., Ahn, J. J., Chan, Y. T., Choi, O., Luck, H., Woo, M., Dunn, S. E., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.08.003 · Cited by 272
Protein synthesis, degradation, and energy metabolism in T cell immunity
Marchingo, J. M., & Cantrell, D. A. (2022) · Cellular & Molecular Immunology · doi:10.1038/s41423-021-00792-8 · Cited by 169
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Metadata
- Authors
- Preston, G. C., Sinclair, L. V., Kaskar, A., Hukelmann, J. L., Navarro, M. N., Ferrero, I., MacDonald, H. R., Cowling, V. H., & Cantrell, D. A.
- Venue
- The EMBO Journal
- Published
- 2015-07
- Volume
- 34
- Issue
- 15
- Pages
- 2008-2024
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- OpenAlex
- W2164115182
- Cited by
- 168
- References
- 2
- FWCI
- 6.46
- Type
- journal article
- Language
- en
- Open access
- hybrid
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- Preston, G. C., Sinclair, L. V., Kaskar, A., Hukelmann, J. L., Navarro, M. N., Ferrero, I., MacDonald, H. R., Cowling, V. H., & Cantrell, D. A. (2015). Single cell tuning of Myc expression by antigen receptor signal strength and interleukin‐2 in T lymphocytes. The EMBO Journal. https://doi.org/10.15252/embj.201490252
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