Constitutive Glycolytic Metabolism Supports CD8+ T Cell Effector Memory Differentiation during Viral Infection

Immunity

Volumn 45, Issue 5, 2016, Pages 1024-1037

  Phan, Anthony T ^a   Doedens, Andrew L ^a   Palazon, Asis ^b   Tyrakis, Petros A ^b   Cheung, Kitty P ^a   Johnson, Randall S ^b,c   Goldrath, Ananda W ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; TRANSCRIPTION FACTOR; VON HIPPEL LINDAU PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL METABOLISM; CONTROLLED STUDY; EFFECTOR CELL; GLYCOLYSIS; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VIRUS INFECTION; ANIMAL; ARENAVIRUS INFECTION; CELL DIFFERENTIATION; CELL SEPARATION; DISEASE MODEL; FLOW CYTOMETRY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; ARENAVIRIDAE INFECTIONS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL SEPARATION; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GLYCOLYSIS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, TRANSGENIC; OXIDATIVE PHOSPHORYLATION;

EID: 84999751988     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.10.017     Document Type: Article

References (44)

1. Araki, K., Turner, A.P., Shaffer, V.O., Gangappa, S., Keller, S.A., Bachmann, M.F., Larsen, C.P., Ahmed, R., mTOR regulates memory CD8 T-cell differentiation. Nature 460 (2009), 108–112.
2. Blagih, J., Coulombe, F., Vincent, E.E., Dupuy, F., Galicia-Vázquez, G., Yurchenko, E., Raissi, T.C., van der Windt, G.J., Viollet, B., Pearce, E.L., et al. The energy sensor AMPK regulates T cell metabolic adaptation and effector responses in vivo. Immunity 42 (2015), 41–54.
3. Chang, C.-H., Curtis, J.D., Maggi, L.B. Jr., Faubert, B., Villarino, A.V., O'Sullivan, D., Huang, S.C., van der Windt, G.J., Blagih, J., Qiu, J., et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153 (2013), 1239–1251.
4. Chang, J.T., Wherry, E.J., Goldrath, A.W., Molecular regulation of effector and memory T cell differentiation. Nat. Immunol. 15 (2014), 1104–1115.
5. Chaoul, N., Fayolle, C., Desrues, B., Oberkampf, M., Tang, A., Ladant, D., Leclerc, C., Rapamycin Impairs Antitumor CD8+ T-cell Responses and Vaccine-Induced Tumor Eradication. Cancer Res. 75 (2015), 3279–3291.
6. Cui, G., Staron, M.M., Gray, S.M., Ho, P.C., Amezquita, R.A., Wu, J., Kaech, S.M., IL-7-Induced Glycerol Transport and TAG Synthesis Promotes Memory CD8+ T Cell Longevity. Cell 161 (2015), 750–761.
7. Dang, E.V., Barbi, J., Yang, H.-Y., Jinasena, D., Yu, H., Zheng, Y., Bordman, Z., Fu, J., Kim, Y., Yen, H.-R., et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 146 (2011), 772–784.
8. De Rosa, V., Galgani, M., Porcellini, A., Colamatteo, A., Santopaolo, M., Zuchegna, C., Romano, A., De Simone, S., Procaccini, C., La Rocca, C., et al. Glycolysis controls the induction of human regulatory T cells by modulating the expression of FOXP3 exon 2 splicing variants. Nat. Immunol. 16 (2015), 1174–1184.
9. Doedens, A.L., Phan, A.T., Stradner, M.H., Fujimoto, J.K., Nguyen, J.V., Yang, E., Johnson, R.S., Goldrath, A.W., Hypoxia-inducible factors enhance the effector responses of CD8(+) T cells to persistent antigen. Nat. Immunol. 14 (2013), 1173–1182.
10. Finlay, D.K., Rosenzweig, E., Sinclair, L.V., Feijoo-Carnero, C., Hukelmann, J.L., Rolf, J., Panteleyev, A.A., Okkenhaug, K., Cantrell, D.A., PDK1 regulation of mTOR and hypoxia-inducible factor 1 integrate metabolism and migration of CD8+ T cells. J. Exp. Med. 209 (2012), 2441–2453.
11. Haase, V.H., Glickman, J.N., Socolovsky, M., Jaenisch, R., Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc. Natl. Acad. Sci. USA 98 (2001), 1583–1588.
12. Hess Michelini, R., Doedens, A.L., Goldrath, A.W., Hedrick, S.M., Differentiation of CD8 memory T cells depends on Foxo1. J. Exp. Med. 210 (2013), 1189–1200.
13. Jameson, S.C., Masopust, D., Diversity in T cell memory: an embarrassment of riches. Immunity 31 (2009), 859–871.
14. Kaech, S.M., Wherry, E.J., Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 27 (2007), 393–405.
15. Kawalekar, O.U., O'Connor, R.S., Fraietta, J.A., Guo, L., McGettigan, S.E., Posey, A.D. Jr., Patel, P.R., Guedan, S., Scholler, J., Keith, B., et al. Distinct Signaling of Coreceptors Regulates Specific Metabolism Pathways and Impacts Memory Development in CAR T Cells. Immunity 44 (2016), 380–390.
16. Kidani, Y., Elsaesser, H., Hock, M.B., Vergnes, L., Williams, K.J., Argus, J.P., Marbois, B.N., Komisopoulou, E., Wilson, E.B., Osborne, T.F., et al. Sterol regulatory element-binding proteins are essential for the metabolic programming of effector T cells and adaptive immunity. Nat. Immunol. 14 (2013), 489–499.
17. Kim, J.W., Tchernyshyov, I., Semenza, G.L., Dang, C.V., HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3 (2006), 177–185.
18. Kim, M.V., Ouyang, W., Liao, W., Zhang, M.Q., Li, M.O., The transcription factor Foxo1 controls central-memory CD8+ T cell responses to infection. Immunity 39 (2013), 286–297.
19. Kucejova, B., Peña-Llopis, S., Yamasaki, T., Sivanand, S., Tran, T.A., Alexander, S., Wolff, N.C., Lotan, Y., Xie, X.-J., Kabbani, W., et al. Interplay between pVHL and mTORC1 pathways in clear-cell renal cell carcinoma. Mol. Cancer Res. 9 (2011), 1255–1265.
20. Lee, K., Gudapati, P., Dragovic, S., Spencer, C., Joyce, S., Killeen, N., Magnuson, M.A., Boothby, M., Mammalian target of rapamycin protein complex 2 regulates differentiation of Th1 and Th2 cell subsets via distinct signaling pathways. Immunity 32 (2010), 743–753.
21. MacIver, N.J., Michalek, R.D., Rathmell, J.C., Metabolic regulation of T lymphocytes. Annu. Rev. Immunol. 31 (2013), 259–283.
22. Mascanfroni, I.D., Takenaka, M.C., Yeste, A., Patel, B., Wu, Y., Kenison, J.E., Siddiqui, S., Basso, A.S., Otterbein, L.E., Pardoll, D.M., et al. Metabolic control of type 1 regulatory T cell differentiation by AHR and HIF1-α. Nat. Med. 21 (2015), 638–646.
23. McNamee, E.N., Korns Johnson, D., Homann, D., Clambey, E.T., Hypoxia and hypoxia-inducible factors as regulators of T cell development, differentiation, and function. Immunol. Res. 55 (2013), 58–70.
24. Michalek, R.D., Gerriets, V.A., Jacobs, S.R., Macintyre, A.N., MacIver, N.J., Mason, E.F., Sullivan, S.A., Nichols, A.G., Rathmell, J.C., Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J. Immunol. 186 (2011), 3299–3303.
25. Mueller, S.N., Gebhardt, T., Carbone, F.R., Heath, W.R., Memory T cell subsets, migration patterns, and tissue residence. Annu. Rev. Immunol. 31 (2013), 137–161.
26. Nizet, V., Johnson, R.S., Interdependence of hypoxic and innate immune responses. Nat. Rev. Immunol. 9 (2009), 609–617.
27. O'Sullivan, D., van der Windt, G.J., Huang, S.C., Curtis, J.D., Chang, C.H., Buck, M.D., Qiu, J., Smith, A.M., Lam, W.Y., DiPlato, L.M., et al. Memory CD8(+) T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity 41 (2014), 75–88.
28. + T cell immunity through effects on mitochondrial respiration. Science 348 (2015), 995–1001.
29. + T cells in the memory population mediate potent protective immunity. Immunity 38 (2013), 1250–1260.
30. Pearce, E.L., Walsh, M.C., Cejas, P.J., Harms, G.M., Shen, H., Wang, L.-S., Jones, R.G., Choi, Y., Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460 (2009), 103–107.
31. Pearce, E.L., Poffenberger, M.C., Chang, C.-H., Jones, R.G., Fueling immunity: insights into metabolism and lymphocyte function. Science 342 (2013), 1242454-1–1242454-11.
32. Phan, A.T., Goldrath, A.W., Hypoxia-inducible factors regulate T cell metabolism and function. Mol. Immunol. 68:2 Pt C (2015), 527–535.
33. Rao, R.R., Li, Q., Odunsi, K., Shrikant, P.A., The mTOR kinase determines effector versus memory CD8+ T cell fate by regulating the expression of transcription factors T-bet and Eomesodermin. Immunity 32 (2010), 67–78.
34. Rao, R.R., Li, Q., Gubbels Bupp, M.R., Shrikant, P.A., Transcription factor Foxo1 represses T-bet-mediated effector functions and promotes memory CD8(+) T cell differentiation. Immunity 36 (2012), 374–387.
35. Rolf, J., Zarrouk, M., Finlay, D.K., Foretz, M., Viollet, B., Cantrell, D.A., AMPKα1: a glucose sensor that controls CD8 T-cell memory. Eur. J. Immunol. 43 (2013), 889–896.
36. Sena, L.A., Li, S., Jairaman, A., Prakriya, M., Ezponda, T., Hildeman, D.A., Wang, C.R., Schumacker, P.T., Licht, J.D., Perlman, H., et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38 (2013), 225–236.
37. Shi, L.Z., Wang, R., Huang, G., Vogel, P., Neale, G., Green, D.R., Chi, H., HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 208 (2011), 1367–1376.
38. Shrestha, S., Yang, K., Wei, J., Karmaus, P.W.F., Neale, G., Chi, H., Tsc1 promotes the differentiation of memory CD8+ T cells via orchestrating the transcriptional and metabolic programs. Proc. Natl. Acad. Sci. USA 111 (2014), 14858–14863.
39. Sukumar, M., Liu, J., Ji, Y., Subramanian, M., Crompton, J.G., Yu, Z., Roychoudhuri, R., Palmer, D.C., Muranski, P., Karoly, E.D., et al. Inhibiting glycolytic metabolism enhances CD8+ T cell memory and antitumor function. J. Clin. Invest. 123 (2013), 4479–4488.
40. Tejera, M.M., Kim, E.H., Sullivan, J.A., Plisch, E.H., Suresh, M., FoxO1 controls effector-to-memory transition and maintenance of functional CD8 T cell memory. J. Immunol. 191 (2013), 187–199.
41. van der Windt, G.J., Everts, B., Chang, C.H., Curtis, J.D., Freitas, T.C., Amiel, E., Pearce, E.J., Pearce, E.L., Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity 36 (2012), 68–78.
42. 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., et al. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc. Natl. Acad. Sci. USA 110 (2013), 14336–14341.
43. Wang, R., Dillon, C.P., Shi, L.Z., Milasta, S., Carter, R., Finkelstein, D., McCormick, L.L., Fitzgerald, P., Chi, H., Munger, J., Green, D.R., The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 35 (2011), 871–882.
44. Zhang, D.J., Wang, Q., Wei, J., Baimukanova, G., Buchholz, F., Stewart, A.F., Mao, X., Killeen, N., Selective expression of the Cre recombinase in late-stage thymocytes using the distal promoter of the Lck gene. J. Immunol. 174 (2005), 6725–6731.