Glucose metabolism regulates T cell activation, differentiation, and functions

Frontiers in Immunology

Volumn 6, Issue JAN, 2015, Pages

  Palmer, Clovis S ^a   Ostrowski, Matias ^b   Balderson, Brad ^a   Christian, Nicole ^c   Crowe, Suzanne M ^a,d,e  

^a BURNET INSTITUTE   (Australia)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSITY OF THE WEST INDIES   (Jamaica)

^d MONASH UNIVERSITY   (Australia)

^e ALFRED HOSPITAL   (Australia)

Author keywords

Glucose transporter 1; HIF 1a; HIV; Immune activation; Inflammation; Metabolism; MTOR; PI3K

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN;

CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL LINEAGE; CELL METABOLISM; CELL PROLIFERATION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; IMMUNE RESPONSE; INFLAMMATORY DISEASE; REGULATORY T LYMPHOCYTE; SHORT SURVEY; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL;

EID: 84926640592     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00001     Document Type: Short Survey

References (60)

1. Freemerman AJ, Johnson AR, Sacks GN, Milner JJ, Kirk EL, Troester MA, et al. Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem (2014) 289:7884-96. doi: 10.1074/jbc.M113.522037
2. 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. doi:10.4049/jimmunol.180.7.4476
3. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF, et al. mTOR regulates memory CD8 T-cell differentiation. Nature (2009) 460:108-12. doi:10.1038/nature08155
4. 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. doi:10.1038/ni.2710
5. Fox CJ, Hammerman PS, Thompson CB. Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol (2005) 5:844-52. doi:10.1038/nri1710
6. Zheng Y, Delgoffe GM, Meyer CF, Chan W, Powell JD. Anergic T cells are metabolically anergic. J Immunol (2009) 183:6095-101. doi:10.4049/jimmunol.0803510
7. MacIver NJ, Michalek RD, Rathmell JC. Metabolic regulation of T lymphocytes. Annu Rev Immunol (2013) 31:259-83. doi:10.1146/annurev-immunol-032712-095956
8. Palmer CS, Crowe SM. How does monocyte metabolism impact inflammation and aging during chronic HIV infection? AIDS Res Hum Retroviruses (2014) 30:335-6. doi:10.1089/aid.2014.0022
9. Loisel-Meyer S, Swainson L, Craveiro M, Oburoglu L, Mongellaz C, Costa C, et al. Glut1-mediated glucose transport regulates HIV infection. Proc Natl Acad Sci U S A (2012) 109:2549-54. doi:10.1073/pnas.1121427109
10. Chang CH, Curtis JD, Maggi LB Jr., Faubert B, Villarino AV, O'Sullivan D, et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell (2013) 153:1239-51. doi:10.1016/j.cell.2013.05.016
11. Pearce EL, Poffenberger MC, Chang CH, Jones RG. Fueling immunity: insights into metabolism and lymphocyte function. Science (2013) 342:1242454. doi:10.1126/science.1242454
12. Michalek RD, Gerriets VA, Jacobs SR, Macintyre AN, MacIver NJ, Mason EF, et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol (2011) 186:3299-303. doi:10.4049/jimmunol.1003613
13. Krawczyk CM, Holowka T, Sun J, Blagih J, Amiel E, DeBerardinis RJ, et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood (2010) 115:4742-9. doi:10.1182/blood-2009-10-249540
14. Wieman HL, Wofford JA, Rathmell JC. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol Biol Cell (2007) 18:1437-46. doi:10.1091/mbc.E06-07-0593
15. Wofford JA, Wieman HL, Jacobs SR, Zhao Y, Rathmell JC. IL-7 promotes Glut1 trafficking and glucose uptake via STAT5-mediated activation of Akt to support T-cell survival. Blood (2008) 111:2101-11. doi:10.1182/blood-2007-06-096297
16. Ghesquiere B, Wong BW, Kuchnio A, Carmeliet P. Metabolism of stromal and immune cells in health and disease. Nature (2014) 511:167-76. doi:10.1038/nature13312
17. Wang R, Dillon Christopher P, Shi Lewis Z, Milasta S, Carter R, Finkelstein D, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity (2011) 35:871-82. doi:10.1016/j.immuni.2011.09.021
18. Bauer DE, Harris MH, Plas DR, Lum JJ, Hammerman PS, Rathmell JC, et al. Cytokine stimulation of aerobic glycolysis in hematopoietic cells exceeds proliferative demand. FASEB J (2004) 18:1303-5. doi:10.1096/fj.03-1001fje
19. Frauwirth K, Riley J, Harris M, Parry R, Rathmell J, Plas D, et al. The CD28 signaling pathway regulates glucose metabolism. Immunity (2002) 16:769-77. doi:10.1016/S1074-7613(02)00323-0
20. Jones RG, Thompson CB. Revving the engine: signal transduction fuels T cell activation. Immunity (2007) 27:173-8. doi:10.1016/j.immuni.2007.07.008
21. Wang T, Marquardt C, Foker J. Aerobic glycolysis during lymphocyte proliferation. Nature (1976) 261:702-5. doi:10.1038/261702a0
22. Warburg O. On respiratory impairment in cancer cells. Science (1956) 124:269-70.
23. Cao Y, Rathmell JC, Macintyre AN. Metabolic reprogramming towards aerobic glycolysis correlates with greater proliferative ability and resistance to metabolic inhibition in CD8 versus CD4 T cells. PLoS One (2014) 9:e104104. doi:10.1371/journal.pone.0104104
24. Chi H. Regulation and function of mTOR signalling in T cell fate decisions. Nat Rev Immunol (2012) 12:325-38. doi:10.1038/nri3198
25. Frauwirth KA, Thompson CB. Regulation of T lymphocyte metabolism. J Immunol (2004) 172:4661-5. doi:10.4049/jimmunol.172.8.4661
26. Palmer CS, Crowe SM. The role of glucose and lipid metabolism in the pathogenesis of HIV-1 infection. Curr Trends Immunol (2012) 13:37-50.
27. Nath MD, Ruscetti FW, Petrow-Sadowski C, Jones KS. Regulation of the cell-surface expression of an HTLV-I binding protein in human T cells during immune activation. Blood (2003) 101:3085-92. doi:10.1182/blood-2002-07-2277
28. Chakrabarti R, Jung CY, Lee TP, Liu H, Mookerjee BK. Changes in glucose transport and transporter isoforms during the activation of human peripheral blood lymphocytes by phytohemagglutinin. J Immunol (1994) 152: 2660-8.
29. Finlay DK. Regulation of glucose metabolism in T cells: new insight into the role of phosphoinositide 3-kinases. Front Immunol (2012) 3:247. doi:10.3389/fimmu.2012.00247
30. Zhang XY, Yang BY, Wang JY, Mo X, Zhang J, Hua ZC. FADD is essential for glucose uptake and survival of thymocytes. Biochem Biophys Res Commun (2014) 451:202-7. doi:10.1016/j.bbrc.2014.07.092
31. Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci (2009) 122:3589-94. doi:10.1242/jcs.051011
32. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell (2012) 149:274-93. doi:10.1016/j.cell.2012.03.017
33. Sun SY. mTOR kinase inhibitors as potential cancer therapeutic drugs. Cancer Lett (2013) 340:1-8. doi:10.1016/j.canlet.2013.06.017
34. Marko AJ, Miller RA, Kelman A, Frauwirth KA. Induction of glucose metabolism in stimulated T lymphocytes is regulated by mitogen-activated protein kinase signaling. PLoS One (2010) 5:e15425. doi:10.1371/journal.pone.0015425
35. Tamas P, Hawley SA, Clarke RG, Mustard KJ, Green K, Hardie DG, et al. Regulation of the energy sensor AMP-activated protein kinase by antigen receptor and Ca2+ in T lymphocytes. J Exp Med (2006) 203:1665-70. doi:10.1084/jem.20052469
36. Chehtane M, Khaled AR. Interleukin-7 mediates glucose utilization in lymphocytes through transcriptional regulation of the hexokinase II gene. Am J Physiol Cell Physiol (2010) 298:C1560-71. doi:10.1152/ajpcell.00506.2009
37. Sun Q, Chen X, Ma J, Peng H, Wang F, Zha X, et al. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proc Natl Acad Sci U S A (2011) 108:4129-34. doi:10.1073/pnas.1014769108
38. Yu BH, Zhou XY, Xiao XY, Yan SY, Qin T, Shi DR. [Activation and clinicopathologic significance of AKT/mTOR signaling pathway in diffuse large B-cell lymphoma]. Zhonghua Bing Li Xue Za Zhi (2009) 38:35-41.
39. Oestreich KJ, Read KA, Gilbertson SE, Hough KP, McDonald PW, Krishnamoorthy V, et al. Bcl-6 directly represses the gene program of the glycolysis pathway. Nat Immunol (2014) 15:957-64. doi:10.1038/ni.2985
40. Dang EV, Barbi J, Yang HY, Jinasena D, Yu H, Zheng Y, et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell (2011) 146:772-84. doi:10.1016/j.cell.2011.07.033
41. Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR, et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med (2011) 208:1367-76. doi:10.1084/jem.20110278
42. Wan YY, Flavell RA. How diverse-CD4 effector T cells and their functions. J Mol Cell Biol (2009) 1:20-36. doi:10.1093/jmcb/mjp001
43. Waickman AT, Powell JD. mTOR, metabolism, and the regulation of T-cell differentiation and function. Immunol Rev (2012) 249:43-58. doi:10.1111/j.1600-065X.2012.01152.x
44. Delgoffe GM, Kole TP, Zheng Y, Zarek PE, Matthews KL, Xiao B, et al. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity (2009) 30:832-44. doi:10.1016/j.immuni.2009.04.014
45. Gaber T, Strehl C, Sawitzki B, Hoff P, Buttgereit F. Cellular energy metabolism in T-lymphocytes. Int Rev Immunol (2014). doi:10.3109/08830185.2014.956358
46. Delgoffe GM, Pollizzi KN, Waickman AT, Heikamp E, Meyers DJ, Horton MR, et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol (2011) 12:295-303. doi:10.1038/ni.2005
47. Cham CM, Gajewski TF. Glucose availability regulates IFN-gamma production and p70S6 kinase activation in CD8+ effector T cells. J Immunol (2005) 174:4670-7. doi:10.4049/jimmunol.174.8.4670
48. Peters A, Lee Y, Kuchroo VK. The many faces of Th17 cells. Curr Opin Immunol (2011) 23:702-6. doi:10.1016/j.coi.2011.08.007
49. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell (2006) 126:1121-33. doi:10.1016/j.cell.2006.07.035
50. Neildez-Nguyen TM, Bigot J, Da Rocha S, Corre G, Boisgerault F, Paldi A, et al. Hypoxic culture conditions enhance the generation of regulatory T cells. Immunology (2014). doi:10.1111/imm.12388
51. Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J Biol Chem (2001) 276:9519-25. doi:10.1074/jbc.M010144200
52. Palmer CS, Ostrowski M, Gouillou M, Tsai L, Yu D, Zhou J, et al. Increased glucose metabolic activity is associated with CD4+ T-cell activation and depletion during chronic HIV infection. AIDS (2014) 28:297-309. doi:10.1097/QAD.0000000000000128
53. Macintyre AN, Gerriets VA, Nichols AG, Michalek RD, Rudolph MC, Deoliveira D, et al. The glucose transporter Glut1 is selectively essential for CD4 T cell activation and effector function. Cell Metab (2014) 20:61-72. doi:10.1016/j.cmet.2014.05.004
54. Anzinger JJ, Butterfield TR, Angelovich TA, Crowe SM, Palmer CS. Monocytes as regulators of inflammation and HIV-related comorbidities during cART. J Immunol Res (2014) 2014:569819. doi:10.1155/2014/569819
55. Palmer CS, Anzinger JJ, Zhou J, Gouillou M, Landay A, Jaworowski A, et al. Glut1 expressing pro-inflammatory monocytes are elevated in cART-treated and untreated HIV-1+ subjects. J Immunol (2014) 193:5595-603. doi:10.4049/jimmunol.1303092
56. Battaglia M, Stabilini A, Roncarolo MG. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood (2005) 105:4743-8. doi:10.1182/blood-2004-10-3932
57. 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. doi:10.1016/j.immuni.2012.10.020
58. Devadas S, Zaritskaya L, Rhee SG, Oberley L, Williams MS. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J Exp Med (2002) 195:59-70. doi:10.1084/jem.20010659
59. Fracchia KM, Walsh CM. Metabolic mysteries of the inflammatory response: T cell polarization and plasticity. Int Rev Immunol (2014). doi:10.3109/08830185.2014.974748
60. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med (2009) 15:921-9. doi:10.1038/nm.2001