Metabolic conditioning of CD8


Journal

Nature metabolism
ISSN: 2522-5812
Titre abrégé: Nat Metab
Pays: Germany
ID NLM: 101736592

Informations de publication

Date de publication:
08 2020
Historique:
received: 22 10 2019
accepted: 01 07 2020
pubmed: 5 8 2020
medline: 1 1 2021
entrez: 5 8 2020
Statut: ppublish

Résumé

CD8

Identifiants

pubmed: 32747793
doi: 10.1038/s42255-020-0256-z
pii: 10.1038/s42255-020-0256-z
doi:

Substances chimiques

Cytokines 0
Reactive Oxygen Species 0
Carbon 7440-44-0
Glucose IY9XDZ35W2

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

703-716

Références

Michalek, R. D. et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4
pubmed: 3198034 pmcid: 3198034 doi: 10.4049/jimmunol.1003613
Maciver, N. J. et al. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival. J. Leukoc. Biol. 84, 949–957 (2008).
pubmed: 18577716 pmcid: 2638731 doi: 10.1189/jlb.0108024
Chang, C.-H. et al. Metabolic competition in the tumor microenvironment is a driver of cancer progression. Cell 162, 1229–1241 (2015).
pubmed: 26321679 pmcid: 4864363 doi: 10.1016/j.cell.2015.08.016
Chang, C.-H. et al. Post-transcriptional control of T-cell effector function by aerobic glycolysis. Cell 153, 1239–1251 (2013).
pubmed: 23746840 pmcid: 23746840 doi: 10.1016/j.cell.2013.05.016
Blagih, J. et al. The energy sensor AMPK regulates T-cell metabolic adaptation and effector responses in vivo. Immunity 42, 41–54 (2015).
pubmed: 25607458 pmcid: 25607458 doi: 10.1016/j.immuni.2014.12.030
Rolf, J. et al. AMPKalpha1: a glucose sensor that controls CD8 T-cell memory. Eur. J. Immunol. 43, 889–896 (2013).
pubmed: 23310952 pmcid: 3734624 doi: 10.1002/eji.201243008
Klein Geltink, R. I. et al. Mitochondrial Priming by CD28. Cell 171, 385–397 (2017).
pubmed: 28919076 pmcid: 5637396 doi: 10.1016/j.cell.2017.08.018
Buck, M. D. et al. Mitochondrial dynamics controls T-cell fate through metabolic programming. Cell 166, 63–76 (2016).
pubmed: 27293185 pmcid: 4974356 doi: 10.1016/j.cell.2016.05.035
Sukumar, M. et al. Inhibiting glycolytic metabolism enhances CD8+ T-cell memory and anti-tumour function. J. Clin. Invest. 123, 4479–4488 (2013).
pubmed: 24091329 pmcid: 3784544 doi: 10.1172/JCI69589
Sukumar, M. et al. Mitochondrial membrane potential identifies cells with enhanced stemness for cellular therapy. Cell Metab. 23, 63–76 (2016).
pubmed: 26674251 doi: 10.1016/j.cmet.2015.11.002
Scharping, N. E. et al. The tumor microenvironment represses T cell mitochondrial biogenesis to drive intratumoral T cell metabolic insufficiency and dysfunction. Immunity 45, 374–388 (2016).
pubmed: 27496732 pmcid: 5207350 doi: 10.1016/j.immuni.2016.07.009
Chowdhury, P. S., Chamoto, K., Kumar, A. & Honjo, T. PPAR-induced fatty acid oxidation in T cells increases the number of tumour-reactive CD8. Cancer Immunol. Res. 6, 1375–1387 (2018).
pubmed: 30143538 doi: 10.1158/2326-6066.CIR-18-0095
Buck, M. D., Sowell, R. T., Kaech, S. M. & Pearce, E. L. Metabolic instruction of immunity. Cell 169, 570–586 (2017).
pubmed: 28475890 pmcid: 5648021 doi: 10.1016/j.cell.2017.04.004
Qiu, J. et al. Acetate promotes T-cell effector function during glucose restriction. Cell Rep. 27, 2063–2074 (2019).
pubmed: 31091446 pmcid: 6544383 doi: 10.1016/j.celrep.2019.04.022
Crompton, J. G., Sukumar, M. & Restifo, N. P. Targeting Akt in cell-transfer immunotherapy for cancer. Oncoimmunology 5, e1014776 (2016).
pubmed: 27757294 doi: 10.1080/2162402X.2015.1014776
Nabe, S. et al. Reinforce the anti-tumour activity of CD8
pubmed: 30302856 pmcid: 6272119 doi: 10.1111/cas.13827
Hosios, A. M. et al. Amino acids rather than glucose account for the majority of cell mass in proliferating mammalian cells. Dev. Cell 36, 540–549 (2016).
pubmed: 26954548 pmcid: 4766004 doi: 10.1016/j.devcel.2016.02.012
Garcia, D. & Shaw, R. J. AMPK: mechanisms of cellular energy sensing and restoration of metabolic balance. Mol. Cell 66, 789–800 (2017).
pubmed: 5553560 pmcid: 5553560 doi: 10.1016/j.molcel.2017.05.032
Saxton, R. A. & Sabatini, D. M. mTOR signaling in growth, metabolism, and disease. Cell 168, 960–976 (2017).
pubmed: 28283069 pmcid: 5394987 doi: 10.1016/j.cell.2017.02.004
Jacobs, S. R. et al. Glucose uptake is limiting in T-cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 180, 4476–4486 (2008).
pubmed: 2593791 pmcid: 2593791 doi: 10.4049/jimmunol.180.7.4476
Macintyre, A. N. et al. The glucose transporter Glut1 is selectively essential for CD4 T cell activation and effector function. Cell Metab. 20, 61–72 (2014).
pubmed: 4079750 pmcid: 4079750 doi: 10.1016/j.cmet.2014.05.004
Siska, P. J. et al. Suppression of Glut1 and glucose metabolism by decreased Akt/mTORC1 signaling drives T-cell impairment in B cell leukemia. J. Immunol. 197, 2532–2540 (2016).
pubmed: 27511728 pmcid: 27511728 doi: 10.4049/jimmunol.1502464
Waypa, G. B. et al. Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ. Res. 106, 526–535 (2010).
pubmed: 20019331 doi: 10.1161/CIRCRESAHA.109.206334
Schieber, M. & Chandel, N. S. ROS function in redox signaling and oxidative stress. Curr. Biol. 24, R453–R462 (2014).
pubmed: 24845678 pmcid: 4055301 doi: 10.1016/j.cub.2014.03.034
Hosios, A. M. & Vander Heiden, M. G. The redox requirements of proliferating mammalian cells. J. Biol. Chem. 293, 7490–7498 (2018).
pubmed: 29339555 pmcid: 5961062 doi: 10.1074/jbc.TM117.000239
Kong, H. & Chandel, N. S. Regulation of redox balance in cancer and T cells. J. Biol. Chem. 293, 7499–7507 (2018).
pubmed: 29282291 doi: 10.1074/jbc.TM117.000257
Mak, T. W. et al. Glutathione primes T-cell metabolism for inflammation. Immunity 46, 675–689 (2017).
pubmed: 28423341 doi: 10.1016/j.immuni.2017.03.019
Smith, C. A., Want, E. J., O’Maille, G., Abagyan, R. & Siuzdak, G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching and identification. Anal. Chem. 78, 779–787 (2006).
pubmed: 16448051 doi: 10.1021/ac051437y
Huang, X. et al. X13CMS: global tracking of isotopic labels in untargeted metabolomics. Anal. Chem. 86, 1632–1639 (2014).
pubmed: 24397582 pmcid: 3982964 doi: 10.1021/ac403384n
Ma, E. H. et al. Serine is an essential metabolite for effector T-cell expansion. Cell Metab. 25, 345–357 (2017).
pubmed: 28111214 doi: 10.1016/j.cmet.2016.12.011
Crompton, J. G. et al. Akt inhibition enhances expansion of potent tumour-specific lymphocytes with memory-cell characteristics. Cancer Res. 75, 296–305 (2015).
pubmed: 25432172 doi: 10.1158/0008-5472.CAN-14-2277
Vander Heiden, M. G., Cantley, L. C. & Thompson, C. B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029–1033 (2009).
doi: 10.1126/science.1160809
Warburg, O. The metabolism of carcinoma cells. J. Cancer Res. 9, 148–163 (1925).
doi: 10.1158/jcr.1925.148
Liberti, M. V. & Locasale, J. W. The Warburg effect: how does it benefit cancer cells?. Trends Biochem. Sci. 41, 211–218 (2016).
pubmed: 26778478 pmcid: 4783224 doi: 10.1016/j.tibs.2015.12.001
Zhao, J., Song, Y. & Liu, D. Clinical trials of dual-target CAR T cells, donor-derived CAR T cells, and universal CAR T cells for acute lymphoid leukemia. J. Hematol. Oncol. 12, 17 (2019).
pubmed: 30764841 pmcid: 6376657 doi: 10.1186/s13045-019-0705-x
Sena, L. A. et al. Mitochondria are required for antigen-specific T-cell activation through reactive oxygen species signaling. Immunity 38, 225–236 (2013).
pubmed: 23415911 pmcid: 23415911 doi: 10.1016/j.immuni.2012.10.020
Nathan, C. & Cunningham-Bussel, A. Beyond oxidative stress: an immunologist’s guide to reactive oxygen species. Nat. Rev. Immunol. 13, 349–361 (2013).
pubmed: 23618831 pmcid: 4250048 doi: 10.1038/nri3423
Chatterjee, S. et al. CD38
pubmed: 29129787 doi: 10.1016/j.cmet.2017.10.006
Johnson, M. O. et al. Distinct regulation of Th17 and Th1 cell differentiation by glutaminase-dependent metabolism. Cell 175, 1780–1795 (2018).
pubmed: 30392958 pmcid: 6361668 doi: 10.1016/j.cell.2018.10.001
Ghergurovich, J. M. et al. A small-molecule G6PD inhibitor reveals immune dependence on pentose phosphate pathway. Nat. Chem. Biol. 16, 731–739 (2020).
pubmed: 32393898 pmcid: 7311271 doi: 10.1038/s41589-020-0533-x
Ma, E. H. et al. Metabolic profiling using stable isotope tracing reveals distinct patterns of glucose utilization by physiologically activated CD8. Immunity 51, 856–870 (2019).
pubmed: 31747582 doi: 10.1016/j.immuni.2019.09.003
Yang, J. C. & Rosenberg, S. A. Adoptive T-cell therapy for cancer. Adv. Immunol. 130, 279–294 (2016).
pubmed: 26923004 pmcid: 6293459 doi: 10.1016/bs.ai.2015.12.006
Chamoto, K. et al. Mitochondrial activation chemicals synergize with surface receptor PD-1 blockade for T-cell-dependent anti-tumour activity. Proc. Natl Acad. Sci. USA 114, E761–E770 (2017).
pubmed: 28096382 doi: 10.1073/pnas.1620433114
Kumar, A., Chamoto, K., Chowdhury, P. S. & Honjo, T. Tumours attenuating the mitochondrial activity in T cells escape from PD-1 blockade therapy. eLife 9, e52330 (2020).
pubmed: 32122466 pmcid: 7105382 doi: 10.7554/eLife.52330
Wills, J., Edwards-Hicks, J. & Finch, A. J. AssayR: a simple mass spectrometry software tool for targeted metabolic and stable isotope tracer analyses. Anal. Chem. 89, 9616–9619 (2017).
pubmed: 28850215 pmcid: 5628912 doi: 10.1021/acs.analchem.7b02401
van der Windt, G. J. W., Chang, C. H. & Pearce, E. L. Measuring bioenergetics in T cells using a Seahorse extracellular flux analyser. Curr. Protoc. Immunol. 113, 3.16B.1–3.16B.14 (2016).
Pearce, E. L. et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460, 103–107 (2009).
pubmed: 19494812 pmcid: 2803086 doi: 10.1038/nature08097
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018).
pubmed: 29608179 pmcid: 29608179 doi: 10.1038/nbt.4096
Diaz-Papkovich, A., Anderson-Trocmé, L., Ben-Eghan, C. & Gravel, S. UMAP reveals cryptic population structure and phenotype heterogeneity in large genomic cohorts. PLoS Genet. 15, e1008432 (2019).
pubmed: 31675358 pmcid: 6853336 doi: 10.1371/journal.pgen.1008432
Aoki-Kinoshita, K. F. & Kanehisa, M. Gene annotation and pathway mapping in KEGG. Methods Mol. Biol. 396, 71–91 (2007).
pubmed: 18025687 doi: 10.1007/978-1-59745-515-2_6
Szklarczyk, D. et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2019).
pubmed: 30476243 pmcid: 30476243 doi: 10.1093/nar/gky1131

Auteurs

Ramon I Klein Geltink (RI)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.
Department of Pathology and Laboratory Medicine, University of British Columbia / BC Children's Hospital Research Institute, Vancouver, British Colombia, Canada.

Joy Edwards-Hicks (J)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Petya Apostolova (P)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

David O'Sullivan (D)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

David E Sanin (DE)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Annette E Patterson (AE)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Daniel J Puleston (DJ)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Nina A M Ligthart (NAM)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Joerg M Buescher (JM)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Katarzyna M Grzes (KM)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Agnieszka M Kabat (AM)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Michal Stanczak (M)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Jonathan D Curtis (JD)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Fabian Hässler (F)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Franziska M Uhl (FM)

Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Faculty of Biology, University of Freiburg, Freiburg, Germany.

Mario Fabri (M)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.
Department of Dermatology and Venereology, University of Cologne, Cologne, Germany.

Robert Zeiser (R)

Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Edward J Pearce (EJ)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.
Faculty of Biology, University of Freiburg, Freiburg, Germany.

Erika L Pearce (EL)

Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany. pearce@ie-freiburg.mpg.de.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH