T-cell metabolism governing activation, proliferation and differentiation; a modular view

Immunology

Volumn 150, Issue 1, 2017, Pages 35-44

  Dimeloe, Sarah ^a   Burgener, Anne Valérie ^a   Grählert, Jasmin ^a   Hess, Christoph ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

cell activation; cell differentiation; cell proliferation; inflammation; T cells

Indexed keywords

AMINO ACID; CHOLESTEROL; CYTOKINE; GLUCOSE;

AMINO ACID METABOLISM; AMINO ACID TRANSPORT; CELL ACTIVATION; CELL DIFFERENTIATION; CELL METABOLISM; CELL PROLIFERATION; CHOLESTEROL METABOLISM; CITRIC ACID CYCLE; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; INFECTION; LIPOGENESIS; MALIGNANT NEOPLASM; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TRANSFORMED CELL; ANIMAL; AUTOIMMUNE DISEASE; BIOLOGICAL MODEL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; NEOPLASM; PHYSIOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; INFECTION; LYMPHOCYTE ACTIVATION; MODELS, IMMUNOLOGICAL; NEOPLASMS; T-LYMPHOCYTES;

EID: 84994514596     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12655     Document Type: Review

References (81)

1. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, Plas DR et al. The CD28 signaling pathway regulates glucose metabolism. Immunity 2002; 16:769–77.
2. Warburg O. On the origin of cancer cells. Science 1956; 123:309–14.
3. Lunt SY, Vander MG. Heiden, aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Ann Rev Cell Dev Biol 2011; 27:441–64.
4. Jacobs SR, Herman CE, MacIver NJ, Wofford JA, Wieman HL, Hammen JJ et al. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J Immunol 2008; 180:4476–86.
5. Frauwirth KA, Thompson CB. Regulation of T lymphocyte metabolism. J Immunol 2004; 172:4661–5.
6. Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR et al. HIF1α-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 2011; 208:1367–76.
7. + T cells requires an immediate-early glycolytic switch. Nat Immunol 2013; 14:1064–72.
8. Kolev M, Dimeloe S, Le Friec G, Navarini A, Arbore G, Povoleri GA et al. Complement regulates nutrient influx and metabolic reprogramming during Th1 cell responses. Immunity 2015; 42:1033–47.
9. Michalek RD, Gerriets VA, Nichols AG, Inoue M, Kazmin D, Chang C-Y et al. Estrogen-related receptor-α is a metabolic regulator of effector T-cell activation and differentiation. Proc Natl Acad Sci USA 2011; 108:18348–53.
10. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011; 35:871–82.
11. Preston GC, Sinclair LV, Kaskar A, Hukelmann JL, Navarro MN, Ferrero I et al. Single cell tuning of Myc expression by antigen receptor signal strength and interleukin-2 in T lymphocytes. EMBO J 2015; 34:2008–24.
12. Man K, Miasari M, Shi W, Xin A, Henstridge DC, Preston S et al. The transcription factor IRF4 is essential for TCR affinity-mediated metabolic programming and clonal expansion of T cells. Nat Immunol 2013; 14:1155–65.
13. + T cells by regulating glucose uptake. Nat Med 2014; 21:55–61.
14. + T cell function under hypoxic conditions. J Immunol 2016; 196:106–14.
15. Chang C-H, Curtis JD, Maggi LB, Faubert B, Villarino AV, Sullivan DO et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 2013; 153:1239–51.
16. + T cell subsets and inflammation. J Clin Invest 2015; 125:194–207.
17. + T cell subsets. J Immunol 2011; 186:3299–303.
18. De Rosa V, Galgani M, Porcellini A, Colamatteo A, Santopaolo M, Zuchegna C et al. Glycolysis controls the induction of human regulatory T cells by modulating the expression of FOXP3 exon 2 splicing variants. Nat Immunol 2015; 16:1174–84.
19. Procaccini C, Carbone F, Di Silvestre D, Brambilla F, De Rosa V, Galgani M et al. The proteomic landscape of human ex vivo regulatory and conventional T cells reveals specific metabolic requirements. Immunity 2016; 44:406–21.
20. Ostroukhova M, Goplen N, Karim MZ, Michalec L, Guo L, Liang Q et al. The role of low-level lactate production in airway inflammation in asthma. Am J Physiol Lung Cell Mol Physiol 2012; 302:L300–7.
21. + T-cell activation and depletion during chronic HIV infection. AIDS 2013; 28:297–309.
22. + T cell metabolism reverses lupus. Sci Transl Med 2015; 7:274ra18.
23. Lee C-F, Lo Y-C, Cheng C-H, Furtmüller GJ, Oh B, Andrade-Oliveira V et al. Preventing allograft rejection by targeting immune metabolism. Cell Rep 2015; 13:760–70.
24. Yang Z, Fujii H, Mohan SV, Goronzy JJ, Weyand CM. Phosphofructokinase deficiency impairs ATP generation, autophagy, and redox balance in rheumatoid arthritis T cells. J Exp Med 2013; 210:2119–34.
25. Chang C-H, Qiu J, O'Sullivan D, Buck MD, Noguchi T, Curtis JD et al. Metabolic competition in the tumor microenvironment is a driver of cancer progression. Cell 2015; 162:1229–41.
26. Ho P-C, Bihuniak JD, Macintyre AN, Staron M, Liu X, Amezquita R et al. Phosphoenolpyruvate is a metabolic checkpoint of anti-tumor T cell responses. Cell 2015; 162:1217–28.
27. Zhao E, Maj T, Kryczek I, Li W, Wu K, Zhao L et al. Cancer mediates effector T cell dysfunction by targeting microRNAs and EZH2 via glycolysis restriction. Nat Immunol 2016; 17:95–103.
28. Patsoukis N, Bardhan K, Chatterjee P, Sari D, Liu B, Bell LN et al. PD-1 alters T-cell metabolic reprogramming by inhibiting glycolysis and promoting lipolysis and fatty acid oxidation. Nat Commun 2015; 6:6692.
29. + T cell activation in a mouse model of systemic lupus erythematosus. J Immunol 2015; 196:80–90.
30. Sena LA, Li S, Jairaman A, Prakriya M, Ezponda T, Hildeman DA et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 2013; 38:225–36.
31. Nakaya M, Xiao Y, Zhou X, Chang J-H, Chang M, Cheng X et al. Inflammatory T cell responses rely on amino acid transporter ASCT2 facilitation of glutamine uptake and mTORC1 kinase activation. Immunity 2014; 40:692–705.
32. Carr EL, Kelman A, Wu GS, Gopaul R, Senkevitch E, Aghvanyan A et al. Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J Immunol 2010; 185:1037–44.
33. Nicklin P, Bergman P, Zhang B, Triantafellow E, Wang H, Nyfeler B et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 2009; 136:521–34.
34. Durán RV, Oppliger W, Robitaille AM, Heiserich L, Skendaj R, Gottlieb E et al. Glutaminolysis activates Rag-mTORC1 signaling. Mol Cell 2012; 47:349–58.
35. Blagih J, Coulombe F, Vincent EE, Dupuy F, Galicia-Vazquez G, Yurchenko E et al. The energy sensor AMPK regulates T cell metabolic adaptation and effector responses in vivo. Immunity 2015; 42:41–54.
36. + T cells require increased concentrations of acetate induced by stress for optimal function. Immunity 2016; 44:1312–24.
37. Wahl DR, Petersen B, Warner R, Richardson BC, Glick GD, Opipari AW. Characterization of the metabolic phenotype of chronically activated lymphocytes. Lupus 2010; 19:1492–501.
38. Gatza E, Wahl DR, Opipari AW, Sundberg TB, Reddy P, Liu C et al. Manipulating the bioenergetics of alloreactive T cells causes their selective apoptosis and arrests graft-versus-host disease. Sci Transl Med 2011; 3:67ra8.
39. Byersdorfer CA, Tkachev V, Opipari AW, Goodell S, Swanson J, Sandquist S et al. Effector T cells require fatty acid metabolism during murine graft-versus-host disease. Blood 2013; 122:3230–7.
40. + T cell immunity through effects on mitochondrial respiration. Science 2015; 348:995–1001.
41. D'Souza AD, Parikh N, Kaech SM, Shadel GS. Convergence of multiple signaling pathways is required to coordinately up-regulate mtDNA and mitochondrial biogenesis during T cell activation. Mitochondrion 2007; 7:374–85.
42. Baixauli F, Acín-Pérez R, Villarroya-Beltrí C, Mazzeo C, Nuñez-Andrade N, Gabandé-Rodriguez E et al. Mitochondrial respiration controls lysosomal function during inflammatory T cell responses. Cell Metab 2015; 22:485–98.
43. + T cell memory development. Immunity 2012; 36:68–78.
44. Pearce EL, Walsh MC, Cejas PJ, Harms GM, Shen H, Wang L-S et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009; 460:103–7.
45. + T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity 2014; 41:75–88.
46. + T cell longevity. Cell 2015; 161:750–61.
47. van der Windt GJW, O'Sullivan D, Everts B, Huang SC-C, Buck MD, Curtis JD et al. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc Natl Acad Sci USA 2013; 110:14336–41.
48. Schwindling C, Quintana A, Krause E, Hoth M. Mitochondria positioning controls local calcium influx in T cells. J Immunol 2010; 184:184–90.
49. Henson SM, Lanna A, Riddell NE, Franzese O, Macaulay R, Griffiths SJ et al. p38 signaling inhibits mTORC1-independent autophagy in senescent human CD8⁺ T cells. J Clin Invest 2014; 124:4004–16.
50. Buck MD, O'Sullivan D, Klein GR, Curtis JD, Chang C-H, Sanin DE et al. Mitochondrial dynamics controls T cell fate through metabolic programming. Cell 2016; 166:63–76.
51. + T cell mitochondrial metabolism by the respiratory chain repressor MCJ dictates protection to influenza virus. Immunity 2016; 44:1299–311.
52. Sinclair LV, Rolf J, Emslie E, Shi Y-B, Taylor PM, Cantrell DA. Control of amino-acid transport by antigen receptors coordinates the metabolic reprogramming essential for T cell differentiation. Nat Immunol 2013; 14:500–8.
53. Long X, Ortiz-Vega S, Lin Y, Avruch J. Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J Biol Chem 2005; 280:23433–6.
54. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010; 141:290–303.
55. Bar-Peled L, Schweitzer LD, Zoncu R, Sabatini DM. Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1. Cell 2012; 150:1196–208.
56. Saxton RA, Knockenhauer KE, Wolfson RL, Chantranupong L, Pacold ME, Wang T et al. Structural basis for leucine sensing by the Sestrin2-mTORC1 pathway. Science 2016; 351:53–8.
57. Wolfson RL, Chantranupong L, Saxton RA, Shen K, Scaria SM, Cantor JR et al. Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 2016; 351:43–8.
58. Chantranupong L, Scaria SM, Saxton RA, Gygi MP, Shen K, Wyant GA et al. The CASTOR proteins are arginine sensors for the mTORC1 pathway. Cell 2016; 165:153–64.
59. Verbist KC, Guy CS, Milasta S, Liedmann S, Kamiński MM, Wang R et al. Metabolic maintenance of cell asymmetry following division in activated T lymphocytes. Nature 2016; 532:389–93.
60. + T cell differentiation. Nat Immunol 2016; 17:704–11.
61. Munder M, Schneider H, Luckner C, Giese T, Langhans C-D, Fuentes JM et al. Suppression of T-cell functions by human granulocyte arginase. Blood 2006; 108:1627–34.
62. Pallett LJ, Gill US, Quaglia A, Sinclair LV, Jover-Cobos M, Schurich A et al. Metabolic regulation of hepatitis B immunopathology by myeloid-derived suppressor cells. Nat Med 2015; 21:591–600.
63. Modolell M, Choi B-S, Ryan RO, Hancock M, Titus RG, Abebe T et al. Local suppression of T cell responses by arginase-induced l-arginine depletion in nonhealing leishmaniasis. PLoS Negl Trop Dis 2009; 3:e480.
64. Fu H, Khan A, Coe D, Zaher S, Chai J-G, Kropf P et al. Arginine depletion as a mechanism for the immune privilege of corneal allografts. Eur J Immunol 2011; 41:2997–3005.
65. Munder M, Engelhardt M, Knies D, Medenhoff S, Wabnitz G, Luckner-Minden C et al. Cytotoxicity of tumor antigen specific human T cells is unimpaired by arginine depletion. PLoS ONE 2013; 8:e63521.
66. Rodriguez PC, Quiceno DG, Zabaleta J, Ortiz B, Zea AH, Piazuelo MB et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res 2004; 64:5839–49.
67. Kropf P, Baud D, Marshall SE, Munder M, Mosley A, Fuentes JM et al. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur J Immunol 2007; 37:935–45.
68. Kidani Y, Elsaesser H, Hock MB, Vergnes L, Williams KJ, Argus JP et al. Sterol regulatory element-binding proteins are essential for the metabolic programming of effector T cells and adaptive immunity. Nat Immunol 2013; 14:489–99.
69. + T cells by modulating cholesterol metabolism. Nature 2016; 531:651–5.
70. Zeng H, Yang K, Cloer C, Neale G, Vogel P, Chi H. mTORC1 couples immune signals and metabolic programming to establish Treg-cell function. Nature 2013; 499:485–90.
71. Berod L, Friedrich C, Nandan A, Freitag J, Hagemann S, Harmrolfs K et al. De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nat Med 2014; 20:1327–33.
72. + T cells from lupus patients. J Clin Invest 2014; 124:712–24.
73. + T lymphocyte loss and promotes hepatocarcinogenesis. Nature 2016; 531:253–7.
74. Powell JD, Delgoffe GM. The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity 2010; 33:301–11.
75. Hukelmann JL, Anderson KE, Sinclair LV, Grzes KM, Murillo AB, Hawkins PT et al. The cytotoxic T cell proteome and its shaping by the kinase mTOR. Nat Immunol 2016; 17:104–12.
76. + T cell memory and antitumor function. J Clin Invest 2013; 123:4479–88.
77. Berezhnoy A, Castro I, Levay A, Malek TR, Gilboa E. Aptamer-targeted inhibition of mTOR in T cells enhances antitumor immunity. J Clin Invest 2014; 124:188–97.
78. + T-cell responses to vaccinia virus vaccination in rhesus macaques. Am J Transplant 2011; 11:613–8.
79. MacIver NJ, Blagih J, Saucillo DC, Tonelli L, Griss T, Rathmell JC et al. The liver kinase B1 is a central regulator of T cell development, activation, and metabolism. J Immunol 2011; 187:4187–98.
80. Nath N, Khan M, Paintlia MK, Singh I, Hoda MN, Giri S. Metformin attenuated the autoimmune disease of the central nervous system in animal models of multiple sclerosis. J Immunol 2009; 182:8005–14.
81. Bai A, Yong M, Ma AG, Ma Y, Weiss CR, Guan Q et al. Novel anti-inflammatory action of 5-aminoimidazole-4-carboxamide ribonucleoside with protective effect in dextran sulfate sodium-induced acute and chronic colitis. J Pharmacol Exp Ther 2010; 333:717–25.