Mitochondria Are Required for Antigen-Specific T Cell Activation through Reactive Oxygen Species Signaling

Immunity - Tập 38 - Trang 225-236 - 2013
Laura A. Sena1, Sha Li2, Amit Jairaman3, Murali Prakriya3, Teresa Ezponda1, David A. Hildeman4, Chyung-Ru Wang2, Paul T. Schumacker5, Jonathan D. Licht1, Harris Perlman1, Paul J. Bryce1, Navdeep S. Chandel1
1Department of Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA
2Department of Microbiology and Immunology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA
3Department of Molecular Pharmacology and Biological Chemistry, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA
4Division of Immunobiology, Department of Pediatrics, University of Cincinnati College of Medicine and Children’s Hospital Medical Center, Cincinnati, OH 45229, USA
5Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA

Tài liệu tham khảo

Afshar, 2008, Allergic asthma: a tale of many T cells, Clin. Exp. Allergy, 38, 1847, 10.1111/j.1365-2222.2008.03119.x Bell, 2007, The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production, J. Cell Biol., 177, 1029, 10.1083/jcb.200609074 Bryce, 2006, The H1 histamine receptor regulates allergic lung responses, J. Clin. Invest., 116, 1624, 10.1172/JCI26150 Bulua, 2011, Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS), J. Exp. Med., 208, 519, 10.1084/jem.20102049 Byun, 2008, Mitochondrial dysfunction by complex II inhibition delays overall cell cycle progression via reactive oxygen species production, J. Cell. Biochem., 104, 1747, 10.1002/jcb.21741 Carr, 2010, Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation, J. Immunol., 185, 1037, 10.4049/jimmunol.0903586 Cho, 2011, Nonconventional CD8+ T cell responses to Listeria infection in mice lacking MHC class Ia and H2-M3, J. Immunol., 186, 489, 10.4049/jimmunol.1002639 Dal Porto, 1993, A soluble divalent class I major histocompatibility complex molecule inhibits alloreactive T cells at nanomolar concentrations, Proc. Natl. Acad. Sci. USA, 90, 6671, 10.1073/pnas.90.14.6671 DeBerardinis, 2007, Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis, Proc. Natl. Acad. Sci. USA, 104, 19345, 10.1073/pnas.0709747104 DeBerardinis, 2008, The biology of cancer: metabolic reprogramming fuels cell growth and proliferation, Cell Metab., 7, 11, 10.1016/j.cmet.2007.10.002 Devadas, 2002, 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., 195, 59, 10.1084/jem.20010659 Dhanasekaran, 2005, Mitochondria superoxide dismutase mimetic inhibits peroxide-induced oxidative damage and apoptosis: role of mitochondrial superoxide, Free Radic. Biol. Med., 39, 567, 10.1016/j.freeradbiomed.2005.04.016 Finkel, 2000, Oxidants, oxidative stress and the biology of ageing, Nature, 408, 239, 10.1038/35041687 Frauwirth, 2002, The CD28 signaling pathway regulates glucose metabolism, Immunity, 16, 769, 10.1016/S1074-7613(02)00323-0 Guzman, 2010, Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1, Nature, 468, 696, 10.1038/nature09536 Han, 2003, Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol, J. Biol. Chem., 278, 5557, 10.1074/jbc.M210269200 Jones, 2007, Revving the engine: signal transduction fuels T cell activation, Immunity, 27, 173, 10.1016/j.immuni.2007.07.008 Kamata, 2005, Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases, Cell, 120, 649, 10.1016/j.cell.2004.12.041 Kaminski, 2010, Mitochondrial reactive oxygen species control T cell activation by regulating IL-2 and IL-4 expression: mechanism of ciprofloxacin-mediated immunosuppression, J. Immunol., 184, 4827, 10.4049/jimmunol.0901662 Krauss, 2001, Signaling takes a breath—new quantitative perspectives on bioenergetics and signal transduction, Immunity, 15, 497, 10.1016/S1074-7613(01)00205-9 Laniewski, 2004, Antioxidant treatment reduces expansion and contraction of antigen-specific CD8+ T cells during primary but not secondary viral infection, J. Virol., 78, 11246, 10.1128/JVI.78.20.11246-11257.2004 Lunt, 2011, Aerobic glycolysis: meeting the metabolic requirements of cell proliferation, Annu. Rev. Cell Dev. Biol., 27, 441, 10.1146/annurev-cellbio-092910-154237 McCormack, 1990, Role of calcium ions in regulation of mammalian intramitochondrial metabolism, Physiol. Rev., 70, 391, 10.1152/physrev.1990.70.2.391 Michalek, 2011, Estrogen-related receptor-α is a metabolic regulator of effector T-cell activation and differentiation, Proc. Natl. Acad. Sci. USA, 108, 18348, 10.1073/pnas.1108856108 Morgan, 2011, Crosstalk of reactive oxygen species and NF-κB signaling, Cell Res., 21, 103, 10.1038/cr.2010.178 Muller, 2004, Complex III releases superoxide to both sides of the inner mitochondrial membrane, J. Biol. Chem., 279, 49064, 10.1074/jbc.M407715200 Murphy, 2009, How mitochondria produce reactive oxygen species, Biochem. J., 417, 1, 10.1042/BJ20081386 Pamer, 2004, Immune responses to Listeria monocytogenes, Nat. Rev. Immunol., 4, 812, 10.1038/nri1461 Pearce, 2010, Metabolism in T cell activation and differentiation, Curr. Opin. Immunol., 22, 314, 10.1016/j.coi.2010.01.018 Piganelli, 2002, A metalloporphyrin-based superoxide dismutase mimic inhibits adoptive transfer of autoimmune diabetes by a diabetogenic T-cell clone, Diabetes, 51, 347, 10.2337/diabetes.51.2.347 Schieke, 2008, Coordination of mitochondrial bioenergetics with G1 phase cell cycle progression, Cell Cycle, 7, 1782, 10.4161/cc.7.12.6067 Schwindling, 2010, Mitochondria positioning controls local calcium influx in T cells, J. Immunol., 184, 184, 10.4049/jimmunol.0902872 Sena, 2012, Physiological roles of mitochondrial reactive oxygen species, Mol. Cell, 48, 158, 10.1016/j.molcel.2012.09.025 Smith-Garvin, 2009, T cell activation, Annu. Rev. Immunol., 27, 591, 10.1146/annurev.immunol.021908.132706 Snyder, 1999, Role of the Rieske iron-sulfur protein midpoint potential in the protonmotive Q-cycle mechanism of the cytochrome bc1 complex, J. Bioenerg. Biomembr., 31, 235, 10.1023/A:1005419712731 Tal, 2009, Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling, Proc. Natl. Acad. Sci. USA, 106, 2770, 10.1073/pnas.0807694106 Tormos, 2011, Mitochondrial complex III ROS regulate adipocyte differentiation, Cell Metab., 14, 537, 10.1016/j.cmet.2011.08.007 Turrens, 2003, Mitochondrial formation of reactive oxygen species, J. Physiol., 552, 335, 10.1113/jphysiol.2003.049478 Wang, 1976, Aerobic glycolysis during lymphocyte proliferation, Nature, 261, 702, 10.1038/261702a0 Wang, 1998, Catalytic galactose oxidase models: biomimetic Cu(II)-phenoxyl-radical reactivity, Science, 279, 537, 10.1126/science.279.5350.537 Wang, 2011, The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation, Immunity, 35, 871, 10.1016/j.immuni.2011.09.021 Weinberg, 2010, Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity, Proc. Natl. Acad. Sci. USA, 107, 8788, 10.1073/pnas.1003428107 Wellen, 2010, The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism, Genes Dev., 24, 2784, 10.1101/gad.1985910 West, 2011, TLR signalling augments macrophage bactericidal activity through mitochondrial ROS, Nature, 472, 476, 10.1038/nature09973 West, 2011, Mitochondria in innate immune responses, Nat. Rev. Immunol., 11, 389, 10.1038/nri2975 Wojciechowski, 2006, Bim mediates apoptosis of CD127(lo) effector T cells and limits T cell memory, Eur. J. Immunol., 36, 1694, 10.1002/eji.200635897 Yi, 2006, Electron transport complex I is required for CD8+ T cell function, J. Immunol., 177, 852, 10.4049/jimmunol.177.2.852 Zhou, 2011, A role for mitochondria in NLRP3 inflammasome activation, Nature, 469, 221, 10.1038/nature09663