Cellular energy metabolism in T-lymphocytes

International Reviews of Immunology

Volumn 34, Issue 1, 2015, Pages 34-49

  Gaber, Timo ^a,b   Strehl, Cindy ^a,b   Sawitzki, Birgit ^a   Hoff, Paula ^a,b   Buttgereit, Frank ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

Author keywords

Autoimmune diseases; Cancer; Energy metabolism; Hypoxia; T lymphocytes

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; VACCINE; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOLOGIC FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE;

AUTOIMMUNITY; BONE REGENERATION; CELL ENERGY; CELL METABOLISM; CELL SURVIVAL; DRUG RESPONSE; ENERGY METABOLISM; HUMAN; HYPOXIA; IMMUNE RESPONSE; INFECTION; INFLAMMATION; INFLAMMATORY DISEASE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION; ANOXIA; ARTHRITIS, RHEUMATOID; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONAL ANERGY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; NEOPLASMS; PATHOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION;

ANOXIA; ARTHRITIS, RHEUMATOID; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONAL ANERGY; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOLOGIC FACTORS; LYMPHOCYTE ACTIVATION; NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

EID: 84921314065     PISSN: 08830185     EISSN: 15635244     Source Type: Journal    
DOI: 10.3109/08830185.2014.956358     Document Type: Review

References (111)

1. Chaban Y, Boekema EJ, Dudkina NV. Structures of mitochondrial oxidative phosphorylation super-complexes and mechanisms for their stabilisation. Biochim Biophys Acta 2014 Apr;1837(4):418-426.
2. Serviddio G, Sastre J. Measurement of mitochondrial membrane potential and proton leak. Methods Mol Biol 2010;594:107-121.
3. Strehl C, Fangradt M, Fearon U, et al. Hypoxia: how does the monocyte-macrophage system respond to changes in oxygen availability? J Leukoc Biol 2014 Feb;95(2):233-241.
4. Voet D, Voet JG. Biochemistry. 4th ed. Weinheim: Wiley-VCH; 2011.
5. MacIver NJ, Michalek RD, Rathmell JC. Metabolic regulation of T lymphocytes. Annu Rev Immunol 2013;31:259-283.
6. Geginat J, Paroni M, Facciotti F, et al. The CD4-centered universe of human T cell subsets. Semin Immunol 2013;25(4):252-262.
7. Chien YH, Zeng X, Prinz I. The natural and the inducible: interleukin (IL)-17-producing gammadelta T cells. Trend Immunol 2013;34(4):151-154.
8. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 cells. Annu Rev Immunol 2009;27:485-517.
9. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 2007;25:821-852.
10. Fife BT, Pauken KE, Eagar TN, et al. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat Immunol 2009;10(11):1185-1192.
11. Wu S, Rhee KJ, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 2009;15(9):1016-1022.
12. Geginat J, Sallusto F, Lanzavecchia A. Cytokine-driven proliferation and differentiation of human naive, centralmemory and effector memory CD4+ T cells. Pathol Biol (Paris) 2003;51(2):64-66.
13. Geginat J, Sallusto F, Lanzavecchia A. Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4(+) T cells. J Exp Med 2001;194(12):1711-1719.
14. Devarajan P, Chen Z. Autoimmune effector memory T cells: the bad and the good. Immunol Res 2013;57(1-3):12-22.
15. Masopust D, Choo D, Vezys V, et al. Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med 2010;207(3):553-564.
16. Gebhardt T, Wakim LM, Eidsmo L, et al. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol 2009;10(5):524-530.
17. Wakim LM, Gebhardt T, Heath WR, Carbone FR. Cutting edge: local recall responses by memory T cells newly recruited to peripheral nonlymphoid tissues. J Immunol 2008;181(9):5837-5841.
18. Teijaro JR, Turner D, Pham Q, et al. Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol 2011;187(11):5510-5514.
19. Sathaliyawala T, Kubota M, Yudanin N, et al. Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 2013;38(1):187-197.
20. Schliesser U, Streitz M, Sawitzki B. Tregs: application for solid-organ transplantation. Curr Opin Organ Transplant 2012;17(1):34-41.
21. Guppy M, Greiner E, Brand K. The role of the Crabtree effect and an endogenous fuel in the energy metabolism of resting and proliferating thymocytes. Eur J Biochem 1993;212(1):95-99.
22. Verbist KC, Wang R, Green DR. T cell metabolism and the immune response. Semin Immunol 2012;24(6):399-404.
23. Fox CJ, Hammerman PS, Thompson CB. Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol 2005;5(11):844-852.
24. Warburg O. Origin of cancer cells. Oncologia 1956;9(2):75-83.
25. Chang CH, Curtis JD, Maggi LB, Jr., et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 2013;153(6):1239-1251.
26. Maciolek JA, Alex Pasternak J, Wilson HL. Metabolism of activated T lymphocytes. Curr Opin Immunol 2014;27C:60-74.
27. van der Windt GJ, O'Sullivan D, Everts B, et al. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc Natl Acad Sci USA 2013;110(35):14336-14341.
28. van der Windt GJ, Everts B, Chang CH, et al. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cellmemory development. Immunity 2012;36(1):68-78.
29. Lucas CL, Kuehn HS, Zhao F, et al. Dominant-activating germline mutations in the gene encoding the PI(3)K catalytic subunit p110delta result in T cell senescence and human immunodeficiency. Nat Immunol 2014;15(1):88-97.
30. Michalek RD, Gerriets VA, Jacobs SR, 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(6):3299-3303.
31. Shi LZ, Wang R, Huang G, et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 2011;208(7):1367-1376.
32. Cobbold SP. The mTOR pathway and integrating immune regulation. Immunology 2013;140(4):391-398.
33. Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504(7480):451-455.
34. Bonneville M, Fournie JJ. Sensing cell stress and transformation through Vgamma9Vdelta2 T cell-mediated recognition of the isoprenoid pathway metabolites. Microbes Infect 2005;7(3):503-509.
35. Laird RM, Wolf BJ, Princiotta MF, Hayes SM. gammadelta T cells acquire effector fates in the thymus and differentiate into cytokine-producing effectors in a Listeria model of infection independently of CD28 costimulation. PloS one 2013;8(5):e63178.
36. Wang R, Dillon CP, Shi LZ, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011;35(6):871-882.
37. Altman BJ, Dang CV. Normal and cancer cell metabolism: lymphocytes and lymphoma. FEBS J 2012;279(15):2598-2609.
38. Sonoda J, Laganiere J, Mehl IR, et al. Nuclear receptor ERR alpha and coactivator PGC-1 beta are effectors of IFN-gamma-induced host defense. Genes Dev 2007;21(15):1909-1920.
39. Michalek RD, Gerriets VA, Nichols AG, et al. Estrogen-related receptor-alpha is a metabolic regulator of effector T-cell activation and differentiation. Proc Natl Acad Sci USA 2011;108(45):18348-18353.
40. Perry DJ, Yin Y, Telarico T, et al. Murine lupus susceptibility locus Sle1c2 mediates CD4+ T cell activation andmaps to estrogen-related receptor gamma. J Immunol 2012;189(2):793-803.
41. Frauwirth KA, Riley JL, Harris MH, et al. The CD28 signaling pathway regulates glucose metabolism. Immunity 2002;16(6):769-777.
42. van der Windt GJ, Pearce EL. Metabolic switching and fuel choice during T-cell differentiation and memory development. Immunol Rev 2012;249(1):27-42.
43. Gerriets VA, Rathmell JC. Metabolic pathways in T cell fate and function. Trends Immunol 2012;33(4):168-173.
44. Edinger AL. Controlling cell growth and survival through regulated nutrient transporter expression. Biochem J 2007;406(1):1-12.
45. John S, Weiss JN, Ribalet B. Subcellular localization of hexokinases I and II directs the metabolic fate of glucose. PloS one 2011;6(3):e17674.
46. Tandon P, Gallo CA, Khatri S, et al. Requirement for ribosomal protein S6 kinase 1 to mediate glycolysis and apoptosis resistance induced by Pten deficiency. Proc Natl Acad Sci USA 2011;108(6):2361-2365.
47. Powell JD, Delgoffe GM. The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity 2010;33(3):301-311.
48. Hardie DG. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 2007;8(10):774-785.
49. MacIver NJ, Blagih J, Saucillo DC, et al. The liver kinase B1 is a central regulator of T cell development, activation, and metabolism. J Immunol 2011;187(8):4187-4198.
50. Shaw RJ, Kosmatka M, Bardeesy N, et al. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 2004;101(10):3329-3335.
51. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 2003;13(22):2004-2008.
52. McNamee EN, Korns Johnson D, Homann D, Clambey ET. Hypoxia and hypoxia-inducible factors as regulators of T cell development, differentiation, and function. Immunol Res 2013;55(1-3):58-70.
53. Ward JP. Oxygen sensors in context. Biochim Biophys Acta 2008;1777(1):1-14.
54. Caldwell CC, Kojima H, Lukashev D, et al. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J Immunol 2001;167(11):6140-6149.
55. Gaber T, Dziurla R, Tripmacher R, et al. Hypoxia inducible factor (HIF) in rheumatology: low O2! See what HIF can do! Ann Rheum Dis 2005;64(7):971-980.
56. Buttgereit F, Burmester GR, Brand MD. Bioenergetics of immune functions: fundamental and therapeutic aspects. Immunol Today 2000;21(4):192-199.
57. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell 2012;148(3):399-408.
58. Semenza GL. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Annu Rev Pathol 2014;9:47-71.
59. Barbi J, Pardoll D, Pan F. Metabolic control of the Treg/Th17 axis. Immunol Rev 2013;252(1):52-+-77.
60. Bruzzese L, Fromonot J, By Y, et al. NF-kappaB enhances hypoxia-driven T-cell immunosuppression via upregulation of adenosine A2A receptors. Cell Signal 2014;26(5):1060-1067.
61. Scholz CC, Taylor CT. Hydroxylase-dependent regulation of the NF-kappaB pathway. Biol Chem 2013;394(4):479-493.
62. Semenza GL. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007;2007(407):cm8.
63. Schodel J, Oikonomopoulos S, et al. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 2011;117(23):e207-e217.
64. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005;2005(306):re12.
65. Ohta A, Diwanji R, Kini R, Subramanian M, et al. In vivo T cell activation in lymphoid tissues is inhibited in the oxygen-poor microenvironment. Front Immunol 2011;2:27.
66. Bollinger T, Gies S, Naujoks J, et al. HIF-1alpha- and hypoxia-dependent immune responses in human CD4+CD25high T cells and T helper 17 cells. J Leukoc Biol 2014;96(2):305-312.
67. Ben-Shoshan J, Maysel-Auslender S, Mor A, et al. Hypoxia controls CD4+CD25 +regulatory T-cell homeostasis via hypoxia-inducible factor-1alpha. Eur J Immunol 2008;38(9):2412-2418.
68. Dang EV, Barbi J, Yang HY, et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 2011;146(5):772-784.
69. Wang H, Flach H, Onizawa M, et al. Negative regulation of Hif1a expression and TH17 differentiation by the hypoxia-regulated microRNA miR-210. Nat Immunol 2014;15(4):393-401.
70. Ikejiri A, Nagai S, Goda N, et al. Dynamic regulation of Th17 differentiation by oxygen concentrations. Int Immunol 2012;24(3):137-146.
71. Crespo J, Sun H, Welling TH, et al. T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. Curr Opin Immunol 2013;25(2):214-221.
72. Du JW, Xu KY, Fang LY, Qi XL. Interleukin-17, produced by lymphocytes, promotes tumor growth and angiogenesis in a mouse model of breast cancer. Mol Med Rep 2012;6(5):1099-1102.
73. Numasaki M, Fukushi J, Ono M, et al. Interleukin-17 promotes angiogenesis and tumor growth. Blood 2003;101(7):2620-2627.
74. Ohta A, Gorelik E, Prasad SJ, et al. A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci USA 2006;103(35):13132-13137.
75. Ohta A, Kini R, Subramanian M, et al. The development and immunosuppressive functions of CD4(+) CD25(+) FoxP3(+) regulatory T cells are under influence of the adenosine-A2A adenosine receptor pathway. Front Immunol 2012;3:190.
76. Ohta A, Madasu M, Kini R, et al. A2A adenosine receptor may allow expansion of T cells lacking effector functions in extracellular adenosine-rich microenvironments. J Immunol 2009;183(9):5487-5493.
77. Wherry EJ. T cell exhaustion. Nat Immunol 2011;12(6):492-499.
78. Riley JL. PD-1 signaling in primary T cells. Immunol Rev 2009;229(1):114-125.
79. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003;423(6937):356-361.
80. Choy E. Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology 2012;51(Suppl 5):v3-v11.
81. Gibofsky A. Overview of epidemiology, pathophysiology, and diagnosis of rheumatoid arthritis. Am J Manag Care 2012;18(13 Suppl):S295-S302.
82. Panichi V, Migliori M, De Pietro S, et al. The link of biocompatibility to cytokine production. Kidney Int Suppl 2000;76:S96-S103.
83. Nikolaisen C, Figenschau Y, Nossent JC. Anemia in early rheumatoid arthritis is associated with interleukin 6-mediated bone marrow suppression, but has no effect on disease course or mortality. J Rheumatol 2008;35(3):380-386.
84. Sattar N, McCarey DW, Capell H, McInnes IB. Explaining how "high-grade" systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation 2003;108(24):2957-2963.
85. Ridker PM, Rifai N, Stampfer MJ, Hennekens CH. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation 2000;101(15):1767-1772.
86. De Benedetti F, Rucci N, Del Fattore A, et al. Impaired skeletal development in interleukin-6-transgenic mice: a model for the impact of chronic inflammation on the growing skeletal system. Arthritis Rheumat 2006;54(11):3551-3563.
87. Chrousos GP, Gold PW. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA: The J Amer Med Assoc 1992;267(9):1244-1252.
88. Pawelec G, Solana R. Immunoageing - the cause or effect of morbidity. Trends Immunol 2001;22(7):348-349.
89. Vallejo AN, Weyand CM, Goronzy JJ. T-cell senescence: a culprit of immune abnormalities in chronic inflammation and persistent infection. Trends Mol Med 2004;10(3):119-124.
90. Schmidt-Bleek K, Petersen A, Dienelt A, et al. Initiation and early control of tissue regeneration - bone healing as a model system for tissue regeneration. Expert Opin Biol Ther 2014;14(2):247-259.
91. Kolar P, Schmidt-Bleek K, Schell H, et al. The early fracture hematoma and its potential role in fracture healing. Tissue Eng Part B Rev 2010;16(4):427-434.
92. Haertel E, Werner S, Schafer M. Transcriptional regulation of wound inflammation. Semin Immunol 2014.
93. Simpson DM, Ross R. The neutrophilic leukocyte in wound repair a study with antineutrophil serum. J Clin Invest 1972;51(8):2009-2023.
94. Canturk NZ, Esen N, Vural B, et al. The relationship between neutrophils and incisional wound healing. Skin Pharmacol Appl Skin Physiol 2001;14(2):108-116.
95. Schaffer M, Barbul A. Lymphocyte function in wound healing and following injury. Br J Surg 1998;85(4):444-460.
96. Park JE, Barbul A. Understanding the role of immune regulation in wound healing. Am J Surg 2004;187(5A):11S-16S.
97. Spencer JA, Ferraro F, Roussakis E, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 2014;508(7495):269-273.
98. Wray JB. The biochemical characteristics of the fracture hematoma in man. Surg Gynecol Obstet 1970;130(5):847-852.
99. Brighton CT, Krebs AG. Oxygen tension of healing fractures in the rabbit. J Bone Joint Surg Am 1972;54(2):323-332.
100. Brighton CT, Krebs AG. Oxygen tension of nonunion of fractured femurs in the rabbit. Surg Gynecol Obstet 1972;135(3):379-385.
101. Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003;112(5):645-657.
102. Gaber T, Haupl T, Sandig G, et al. Adaptation of human CD4+ T cells to pathophysiological hypoxia: a transcriptome analysis. J Rheumatol 2009;36(12):2655-2669.
103. Wagegg M, Gaber T, Lohanatha FL, et al. Hypoxia promotes osteogenesis but suppresses adipogenesis of human mesenchymal stromal cells in a hypoxia-inducible factor-1 dependent manner. PloS one 2012;7(9):e46483.
104. Kolar P, Gaber T, Perka C, et al. Human early fracture hematoma is characterized by inflammation and hypoxia. Clin Orthop Relat Res 2011;469(11):3118-3126.
105. Hoff P, Maschmeyer P, Gaber T, et al. Human immune cells' behavior and survival under bioenergetically restricted conditions in an in vitro fracture hematoma model. Cell Mol Immunol 2013;10(2):151-158.
106. Hoff P, Gaber T, Schmidt-Bleek K, et al. Immunologically restricted patients exhibit a pronounced inflammation and inadequate response to hypoxia in fracture hematomas. Immunol Res 2011;51(1):116-122.
107. Hoff P, Rakow A, Gaber T, et al. Preoperative irradiation for the prevention of heterotopic ossification induces local inflammation in humans. Bone 2013;55(1):93-101.
108. Reinke S, Geissler S, Taylor WR, et al. Terminally differentiated CD8(+) T cells negatively affect bone regeneration in humans. Sci Transl Med 2013;5(177):177ra36.
109. Toben D, Schroeder I, El Khassawna T, et al. Fracture healing is accelerated in the absence of the adaptive immune system. J Bone Miner Res 2011;26(1):113-124.
110. Lienau J, Schell H, Duda GN, et al. Initial vascularization and tissue differentiation are influenced by fixation stability. J Orthop Res 2005;23(3):639-645.
111. Schell H, Epari DR, Kassi JP, et al. The course of bone healing is influenced by the initial shear fixation stability. J Orthop Res 2005;23(5):1022-1028.