The immune-metabolic basis of effector memory CD4+ T cell function under hypoxic conditions

Journal of Immunology

Volumn 196, Issue 1, 2016, Pages 106-114

  Dimeloe, Sarah ^a   Mehling, Matthias ^a,b   Frick, Corina ^a   Loeliger, Jordan ^a   Bantug, Glenn R ^a   Sauder, Ursula ^c   Fischer, Marco ^a   Belle, Réka ^a   Develioglu, Leyla ^a   Tay, Savaş ^b   Langenkamp, Anja ^d   Hess, Christoph ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; OXYGEN; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CELL HYPOXIA; CELL LINE; CELL MOTION; CELL SURVIVAL; GLYCOLYSIS; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; MICROFLUIDICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION;

APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL HYPOXIA; CELL LINE; CELL MOVEMENT; CELL SURVIVAL; GLUCOSE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (PHOSPHORYLATING); GLYCOLYSIS; HUMANS; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROFLUIDICS; MITOCHONDRIA; OXYGEN; PYRUVIC ACID; REACTIVE OXYGEN SPECIES;

EID: 84953264064     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501766     Document Type: Article

References (31)

1. Sallusto, R, D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
2. Mueller, S. N., T. Gebhardt, F. R. Carbone, and W. R. Heath. 2013. Memory T cell subsets, migration patterns, and tissue residence. Armu. Rev. Immunol. 31: 137-161.
3. Spence, V. A., and W. F. Walker. 1984. Tissue oxygen tension in normal and ischaemic human skin. Cardiovasc. Res. 18: 140-144.
4. Braun, R. D., J. L. Lanzen, S. A. Snyder, and M. W. Dewhirst. 2001. Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents. Am. J. Physiol. Heart Circ. Physiol. 280: H2533-H2544.
5. Caldwell, C. C, H. Kojima, D. Lukashev, J. Armstrong, M. Farber, S. G. Apasov, and M. V. Sitkovsky. 2001. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J. Immunol. 167: 6140-6149.
6. Karhausen, J., G. T. Furuta, J. E. Tomaszewski, R. S. Johnson, S. R Colgan, and V. H. Haase. 2004. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J. Clin. Invest. 114: 1098-1106.
7. Campbell, E. L., W. J. Bruyninckx, C. J. Kelly, L. E. Glover, E. N. McNamee, B. E. Bowers, A. J. Bayless, M. Scully, B. J. Saeedi, L. Golden-Mason, et al. 2014. Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity 40: 66-77.
8. Green, D. R., L. Galluzzi, and G. Kroemer. 2014. Cell biology. Metabolic control of cell death. Science 345: 1250256.
9. Chandel, N. S. 2014. Mitochondria as signaling organelles. BMC Biol. 12: 34.
10. + and CD8+ T cells. Nature 477: 216-219.
11. Campello, S., R. A. Lacalle, M. Bettella, S. Manes, L. Scorrano, and A. Viola. 2006. Orchestration of lymphocyte chemotaxis by mitochondrial dynamics. J. Exp. Med. 203: 2879-2886.
12. Pearce, E. L., M. C. Poffenberger, C.-H. Chang, and R. G. Jones. 2013. Fueling immunity: insights into metabolism and lymphocyte function. Science 342: 1242454.
13. van der Windt, G. J., D. O'Sullivan, B. Everts, S. C. Huang, M. D. Buck, J. D. Curtis, C.-H. Chang, A. M. Smith, T. Ai, B. Faubert, et al. 2013. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc. Natl. Acad. Sci. USA 110: 14336-14341.
14. Gubser, P. M., G. R. Bantug, L. Razik, M. Fischer, S. Dimeloe, G. Hoenger, B. Durovic, A. Jauch, and C. Hess. 2013. Rapid effector function of memory CD8+ T cells requires an immediate-early glycolytic switch. Nat. Immunol. 14: 1064-1072.
15. Pearce, E. L., M. C. Walsh, P. J. Cejas, G. M. Harms, H. Shen, L.-S. Wang, R. G. Jones, and Y. Choi. 2009. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460: 103-107.
16. Dimeloe, S., C. Frick, M. Fischer, P. M. Gubser, L. Razik, G. R. Bantug, M. Ravon, A. Langenkamp, and C. Hess. 2014. Human regulatory T cells lack the cyclophosphamide-extruding transporter ABCB1 and are more susceptible to cyclophosphamide-induced apoptosis. Eur. J. Immunol. 44: 3614-3620.
17. Mehling, M., T. Frank, C. Albayrak, and S. Tay. 2015. Real-time tracking, retrieval and gene expression analysis of migrating human T cells. Lab Chip 15: 1276-1283.
18. Mazzola, J. L., and M. A. Sirover. 2003. Subcellular localization of human glyceraldehyde-3-phosphate dehydrogenase is independent of its glycolytic function. Biochim. Biophys. Acta 1622: 50-56.
19. Barban, S., and H. O. Schultze. 1961. The effects of 2-deoxyglucose on the growth and metabolism of cultured human cells. J. Biol. Chem. 236: 1887-1890.
20. + T cells maintain specific functions even under conditions of extremely restricted ATP production. Eur. J. Immunol. 38: 1631-1642.
21. Blagih, J., F. Coulombe, E. E. Vincent, F. Dupuy, G. Galicia-Vazquez, E. Yurchenko, T. C. Raissi, G. J. W. van der Windt, B. Viollet, E. L. Pearce, et al. 2015. The energy sensor AMPK regulates T cell metabolic adaptation and effector responses in vivo. Immunity 42: 41-54.
22. Nutt, L. K., S. S. Margolis, M. Jensen, C. E. Herman, W. G. Dunphy, J. C. Rathmell, and S. Kornbluth. 2005. Metabolic regulation of oocyte cell death through the CaMKII-mediated phosphorylation of caspase-2. Cell 123: 89-103.
23. + T cells by regulating glucose uptake. Nat. Med. 21: 55-61.
24. Shostak, A., L. Gotloib, R. Kushnier, and V. Wajsbrot. 2000. Protective effect of pyruvate upon cultured mesothelial cells exposed to 2 mM hydrogen peroxide. Nephron 84: 362-366.
25. Chang, C.-H., J. D. Curtis, L. B. Maggi, Jr., B. Faubert, A. V. Villarino, D. O'Sullivan, S. C.-C. Huang, G. J. W. van der Windt, J. Blagih, J. Qiu, et al. 2013. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153: 1239-1251.
26. Cheng, S.-C, J. Ouintin, R. A. Cramer, K. M. Shepardson, S. Saeed, V. Kumar, E. J. Giamarellos-Bourboulis, J. H. A. Martens, N. A. Rao, A. Aghajanirefah, et al. 2014. mTOR- and HIF-la-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345: 1250684.
27. 2+ buffering. Cell Death Differ. 19: 650-660.
28. Nederlof, R., O. Eerbeek, M. W. Hollmann, R. Southworth, and C. J. Zuurbier. 2014. Targeting hexokinase II to mitochondria to modulate energy metabolism and reduce ischaemia-reperfusion injury in heart. Br. J. Pharmacol. 111: 2067-2079.
29. Sena, L. A., S. Li, A. Jairaman, M. Prakriya, T. Ezponda, D. A. Hildeman, C. -R. Wang, P. T. Schumacker, J. D. Licht, H. Perlman, et al. 2013. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38: 225-236.
30. Yang, Z., H. Fujii, S. V. Mohan, J. J. Goronzy, and C. M. Weyand. 2013. Phosphofructokinase deficiency impairs ATP generation, autophagy, and redox balance in rheumatoid arthritis T cells. J. Exp. Med. 210: 2119-2134.
31. Kim, H.J., and A. E. Nel. 2005. The role of phase II antioxidant enzymes in protecting memory T cells from spontaneous apoptosis in young and old mice. J. Immunol. 175: 2948-2959.