Home LiteratureArticle Details
PMID: 23940348 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

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

van der Windt GJ, O'Sullivan D, Everts B, Huang SC, Buck MD, Curtis JD, Chang CH, Smith AM, Ai T, Faubert B, Jones RG, Pearce EJ, Pearce EL

Abstract

A characteristic of memory T (TM) cells is their ability to mount faster and stronger responses to reinfection than naïve T (TN) cells do in response to an initial infection. However, the mechanisms that allow this rapid recall are not completely understood. We found that CD8 TM cells have more mitochondrial mass than CD8 TN cells and, that upon activation, the resulting secondary effector T (TE) cells proliferate more quickly, produce more cytokines, and maintain greater ATP levels than primary effector T cells. We also found that after activation, TM cells increase oxidative phosphorylation and aerobic glycolysis and sustain this increase to a greater extent than TN cells, suggesting that greater mitochondrial mass in TM 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 TN and TM cells. We also found that fatty acid oxidation is needed for TM 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 TM cells. Our results demonstrate that greater mitochondrial mass endows TM cells with a bioenergetic advantage that underlies their ability to rapidly recall in response to reinfection.

Keywords
lymphocytes metabolism
MeSH Terms
Animals CD8-Positive T-Lymphocytes/cytology,immunology Energy Metabolism Immunologic Memory Lymphocyte Activation Mice Mitochondrial Size
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
van der Windt Gerritje J W
Department of Pathology and Immunology, Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA.
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
References (38)
38 references, click to expand
  1. A high-throughput respirometric assay for mitochondrial biogenesis and toxicity.
    Anal Biochem. 2010 Sep 1;404(1):75-81 PMID: 20465991
  2. Initial antigen encounter programs CD8+ T cells competent to develop into memory cells that are activated in an antigen-free, IL-7- and IL-15-rich environment.
    J Immunol. 2004 Jun 15;172(12):7315-23 PMID: 15187107
  3. Naive, effector and memory CD8 T-cell trafficking: parallels and distinctions.
    Immunotherapy. 2011 Oct;3(10):1223-33 PMID: 21995573
  4. Population dynamics of naive and memory CD8 T cell responses after antigen stimulations in vivo.
    J Immunol. 2012 Feb 1;188(3):1255-65 PMID: 22205031
  5. Targeting of hexokinase 1 to liver and hepatoma mitochondria.
    Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):202-6 PMID: 1309605
  6. Bioenergetic profile experiment using C2C12 myoblast cells.
    J Vis Exp. 2010 Dec 06;(46): PMID: 21189469
  7. Interaction of mitochondrial porin with cytosolic proteins.
    Experientia. 1990 Feb 15;46(2):161-7 PMID: 1689254
  8. Quick to remember, slow to forget: rapid recall responses of memory CD8+ T cells.
    Cell Res. 2010 Jan;20(1):13-23 PMID: 20029390
  9. Rapid demethylation of the IFN-gamma gene occurs in memory but not naive CD8 T cells.
    J Immunol. 2006 Apr 1;176(7):4083-93 PMID: 16547244
  10. Pathophysiological consequences of TAT-HKII peptide administration are independent of impaired vascular function and ensuing ischemia.
    Circ Res. 2013 Jan 18;112(2):e8-13 PMID: 23329797
  11. Posttranscriptional control of T cell effector function by aerobic glycolysis.
    Cell. 2013 Jun 6;153(6):1239-51 PMID: 23746840
  12. Clotrimazole and bifonazole detach hexokinase from mitochondria of melanoma cells.
    Eur J Pharmacol. 1998 Jan 19;342(1):113-7 PMID: 9544799
  13. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak.
    Mol Cell. 2004 Dec 3;16(5):819-30 PMID: 15574336
  14. Requirements for CD8 T-cell priming, memory generation and maintenance.
    Curr Opin Immunol. 2007 Jun;19(3):315-9 PMID: 17433873
  15. Signaling takes a breath--new quantitative perspectives on bioenergetics and signal transduction.
    Immunity. 2001 Oct;15(4):497-502 PMID: 11672532
  16. Biochemical signaling pathways for memory T cell recall.
    Semin Immunol. 2009 Apr;21(2):84-91 PMID: 19298946
  17. Molecular and functional profiling of memory CD8 T cell differentiation.
    Cell. 2002 Dec 13;111(6):837-51 PMID: 12526810
  18. Naive, effector, and memory CD8 T cells in protection against pulmonary influenza virus infection: homing properties rather than initial frequencies are crucial.
    J Immunol. 1999 Nov 15;163(10):5535-43 PMID: 10553081
  19. Response of naïve and memory CD8+ T cells to antigen stimulation in vivo.
    Nat Immunol. 2000 Jul;1(1):47-53 PMID: 10881174
  20. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development.
    Immunity. 2012 Jan 27;36(1):68-78 PMID: 22206904
  21. Phosphatidylinositol 3-kinase-dependent modulation of carnitine palmitoyltransferase 1A expression regulates lipid metabolism during hematopoietic cell growth.
    J Biol Chem. 2006 Dec 8;281(49):37372-80 PMID: 17030509
  22. Revving the engine: signal transduction fuels T cell activation.
    Immunity. 2007 Aug;27(2):173-8 PMID: 17723208
  23. Functional differences between memory and naive CD8 T cells.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2976-81 PMID: 10077622
  24. TCR signal transduction in antigen-specific memory CD8 T cells.
    J Immunol. 2003 Jun 1;170(11):5455-63 PMID: 12759421
  25. The antigen-specific CD8+ T cell repertoire in unimmunized mice includes memory phenotype cells bearing markers of homeostatic expansion.
    J Exp Med. 2009 Feb 16;206(2):435-48 PMID: 19188498
  26. In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability.
    Mol Cell. 2000 Sep;6(3):683-92 PMID: 11030347
  27. Changes in the carbohydrate metabolism of mitogenically stimulated human peripheral lymphocytes. II. Relative importance of glycolysis and oxidative phosphorylation on phytohaemagglutinin stimulation.
    Exp Cell Res. 1973 Mar 15;77(1):127-35 PMID: 4690164
  28. Carnitine acyltransferases and their influence on CoA pools in health and disease.
    Mol Aspects Med. 2004 Oct-Dec;25(5-6):475-93 PMID: 15363637
  29. Cutting edge: chromatin remodeling as a molecular basis for the enhanced functionality of memory CD8 T cells.
    J Immunol. 2008 Jul 15;181(2):865-8 PMID: 18606637
  30. Interaction of mitochondrially bound rat brain hexokinase with intramitochondrial compartments of ATP generated by oxidative phosphorylation and creatine kinase.
    Arch Biochem Biophys. 1992 Nov 15;299(1):116-24 PMID: 1444444
  31. Differential sensitivity of naive and memory CD8+ T cells to apoptosis in vivo.
    J Immunol. 2002 Oct 1;169(7):3760-70 PMID: 12244170
  32. Spare respiratory capacity, oxidative stress and excitotoxicity.
    Biochem Soc Trans. 2009 Dec;37(Pt 6):1385-8 PMID: 19909281
  33. Further studies on the coupling of mitochondrially bound hexokinase to intramitochondrially compartmented ATP, generated by oxidative phosphorylation.
    Arch Biochem Biophys. 1998 Feb 1;350(1):109-17 PMID: 9466827
  34. A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans.
    Science. 2012 Jul 6;337(6090):96-100 PMID: 22628558
  35. Fuel feeds function: energy metabolism and the T-cell response.
    Nat Rev Immunol. 2005 Nov;5(11):844-52 PMID: 16239903
  36. Metabolic switching and fuel choice during T-cell differentiation and memory development.
    Immunol Rev. 2012 Sep;249(1):27-42 PMID: 22889213
  37. Epigenetic remodeling of the IL-2 and IFN-gamma loci in memory CD8 T cells is influenced by CD4 T cells.
    J Immunol. 2006 Jul 15;177(2):1062-9 PMID: 16818762
  38. Lineage relationship and protective immunity of memory CD8 T cell subsets.
    Nat Immunol. 2003 Mar;4(3):225-34 PMID: 12563257
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2013-08-27
Epub
2013-00-12
Pages
14336-41
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3761631
Subset
IM
Grants
NCI NIH HHS · R01 CA164062 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com