Dynamin related protein 1-dependent mitochondrial fission regulates oxidative signalling in T cells

FEBS Letters

Volumn 588, Issue 9, 2014, Pages 1749-1754

  Röth, Daniel ^a   Krammer, Peter H ^a   Gülow, Karsten ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Activation induced T cell death (AICD); Apoptosis; CD95L FASL; Dynamin related protein 1 (Drp1); Interleukin; Mitochondrial dynamics; Reactive oxygen species (ROS); T cell

Indexed keywords

ACTIVATION INDUCED CELL DEATH; DYNAMIN RELATED PROTEIN 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEMBRANE PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRIAL FISSION; MITOCHONDRIAL MEMBRANE; NITROSYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION;

ACTIVATION INDUCED T CELL DEATH (AICD); APOPTOSIS; CD95L/FASL; DYNAMIN RELATED PROTEIN 1 (DRP1); INTERLEUKIN; MITOCHONDRIAL DYNAMICS; REACTIVE OXYGEN SPECIES (ROS); T CELL;

GENE EXPRESSION; GTP PHOSPHOHYDROLASES; HUMANS; JURKAT CELLS; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; NF-KAPPA B; NITRIC OXIDE; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REACTIVE OXYGEN SPECIES; RECEPTORS, ANTIGEN, T-CELL; S-NITROSOTHIOLS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84899657232     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.03.029     Document Type: Article

References (41)

1. P.H. Krammer CD95's deadly mission in the immune system Nature 407 2000 789 795
2. J.E. Smith-Garvin, G.A. Koretzky, and M.S. Jordan T cell activation Annu. Rev. Immunol. 27 2009 591 619
3. M.M. Kaminski et al. T cell activation is driven by an ADP-dependent glucokinase linking enhanced glycolysis with mitochondrial reactive oxygen species generation Cell Rep. 2 2012 1300 1315
4. W. Droge Free radicals in the physiological control of cell function Physiol. Rev. 82 2002 47 95
5. M. Los, H. Schenk, K. Hexel, P.A. Baeuerle, W. Droge, and K. Schulze-Osthoff IL-2 gene expression and NF-kappa B activation through CD28 requires reactive oxygen production by 5-lipoxygenase EMBO J. 14 1995 3731 3740
6. S.H. Jackson, S. Devadas, J. Kwon, L.A. Pinto, and M.S. Williams T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation Nat. Immunol. 5 2004 818 827
7. M.M. Kaminski, D. Roth, P.H. Krammer, and K. Gulow Mitochondria as oxidative signaling organelles in T-cell activation: physiological role and pathological implications Arch. Immunol. Ther. Exp. (Warsz) 61 2013 367 384
8. M.M. Kaminski, D. Roth, S. Sass, S.W. Sauer, P.H. Krammer, and K. Gulow Manganese superoxide dismutase: a regulator of T cell activation-induced oxidative signaling and cell death Biochim. Biophys. Acta 1823 2012 1041 1052
9. L.A. Sena et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling Immunity 38 2013 225 236
10. M. Kaminski, M. Kiessling, D. Suss, P.H. Krammer, and K. Gulow Novel role for mitochondria: protein kinase Ctheta-dependent oxidative signaling organelles in activation-induced T-cell death Mol. Cell. Biol. 27 2007 3625 3639
11. S. Devadas, L. Zaritskaya, S.G. Rhee, L. Oberley, and M.S. Williams 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 2002 59 70
12. M.M. Kaminski, S.W. Sauer, C.D. Klemke, D. Suss, J.G. Okun, P.H. Krammer, and K. Gulow Mitochondrial reactive oxygen species control T cell activation by regulating IL-2 and IL-4 expression: mechanism of ciprofloxacin-mediated immunosuppression J. Immunol. 184 2010 4827 4841
13. K. Gulow, M. Kaminski, K. Darvas, D. Suss, M. Li-Weber, and P.H. Krammer HIV-1 trans-activator of transcription substitutes for oxidative signaling in activation-induced T cell death J. Immunol. 174 2005 5249 5260
14. J. Bereiter-Hahn, and M. Jendrach Mitochondrial dynamics Int. Rev. Cell Mol. Biol. 284 2010 1 65
15. X. Fan, R. Hussien, and G.A. Brooks H2O2-induced mitochondrial fragmentation in C2C12 myocytes Free Radic. Biol. Med. 49 2010 1646 1654
16. M. Jendrach, S. Mai, S. Pohl, M. Voth, and J. Bereiter-Hahn Short- and long-term alterations of mitochondrial morphology, dynamics and mtDNA after transient oxidative stress Mitochondrion 8 2008 293 304
17. S. Wu, F. Zhou, Z. Zhang, and D. Xing Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins FEBS J. 278 2011 941 954
18. T. Yu, J.L. Robotham, and Y. Yoon Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology Proc. Natl. Acad. Sci. USA 103 2006 2653 2658
19. S. Campello, R.A. Lacalle, M. Bettella, S. Manes, L. Scorrano, and A. Viola Orchestration of lymphocyte chemotaxis by mitochondrial dynamics J. Exp. Med. 203 2006 2879 2886
20. F. Baixauli, N.B. Martin-Cofreces, G. Morlino, Y.R. Carrasco, C. Calabia-Linares, E. Veiga, J.M. Serrador, and F. Sanchez-Madrid The mitochondrial fission factor dynamin-related protein 1 modulates T-cell receptor signalling at the immune synapse EMBO J. 30 2011 1238 1250
21. K.R. Pitts, Y. Yoon, E.W. Krueger, and M.A. McNiven The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells Mol. Biol. Cell 10 1999 4403 4417
22. E. Serfling, A. Avots, and M. Neumann The architecture of the interleukin-2 promoter: a reflection of T lymphocyte activation Biochim. Biophys. Acta 1263 1995 181 200
23. M. Li-Weber, O. Laur, K. Dern, and P.H. Krammer T cell activation-induced and HIV tat-enhanced CD95(APO-1/Fas) ligand transcription involves NF-kappaB Eur. J. Immunol. 30 2000 661 670
24. A. Krueger, S.C. Fas, S. Baumann, and P.H. Krammer The role of CD95 in the regulation of peripheral T-cell apoptosis Immunol. Rev. 193 2003 58 69
25. A. Cassidy-Stone et al. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization Dev. Cell 14 2008 193 204
26. G. Nagy, A. Koncz, D. Fernandez, and A. Perl Nitric oxide, mitochondrial hyperpolarization, and T cell activation Free Radic. Biol. Med. 42 2007 1625 1631
27. M.S. Williams, S. Noguchi, P.A. Henkart, and Y. Osawa Nitric oxide synthase plays a signaling role in TCR-triggered apoptotic death J. Immunol. 161 1998 6526 6531
28. S. Ibiza et al. Endothelial nitric oxide synthase regulates T cell receptor signaling at the immunological synapse Immunity 24 2006 753 765
29. D.H. Cho, T. Nakamura, J. Fang, P. Cieplak, A. Godzik, Z. Gu, and S.A. Lipton S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury Science 324 2009 102 105
30. S. Mai, M. Klinkenberg, G. Auburger, J. Bereiter-Hahn, and M. Jendrach Decreased expression of Drp1 and Fis1 mediates mitochondrial elongation in senescent cells and enhances resistance to oxidative stress through PINK1 J. Cell Sci. 123 2010 917 926
31. P.H. Reddy, T.P. Reddy, M. Manczak, M.J. Calkins, U. Shirendeb, and P. Mao Dynamin-related protein 1 and mitochondrial fragmentation in neurodegenerative diseases Brain Res. Rev. 67 2011 103 118
32. M.I. Hernandez-Alvarez, J.C. Paz, D. Sebastian, J.P. Munoz, M. Liesa, J. Segales, M. Palacin, and A. Zorzano Glucocorticoid modulation of mitochondrial function in hepatoma cells requires the mitochondrial fission protein Drp1 Antioxid. Redox Signal. 19 2013 366 378
33. T. Yu, S.S. Sheu, J.L. Robotham, and Y. Yoon Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species Cardiovasc. Res. 79 2008 341 351
34. T. Yu, B.S. Jhun, and Y. Yoon High-glucose stimulation increases reactive oxygen species production through the calcium and mitogen-activated protein kinase-mediated activation of mitochondrial fission Antioxid. Redox Signal. 14 2011 425 437
35. X. Qi, N. Qvit, Y.C. Su, and D. Mochly-Rosen A novel Drp1 inhibitor diminishes aberrant mitochondrial fission and neurotoxicity J. Cell Sci. 126 2013 789 802
36. Y. Yoon, C.A. Galloway, B.S. Jhun, and T. Yu Mitochondrial dynamics in diabetes Antioxid. Redox Signal. 14 2011 439 457
37. J. Park et al. Mitochondrial dynamics modulate the expression of pro-inflammatory mediators in microglial cells J. Neurochem. 127 2013 221 232
38. C. Schwindling, A. Quintana, E. Krause, and M. Hoth Mitochondria positioning controls local calcium influx in T cells J. Immunol. 184 2010 184 190
39. C.R. Chang, and C. Blackstone Dynamic regulation of mitochondrial fission through modification of the dynamin-related protein Drp1 Ann. NY Acad. Sci. 1201 2010 34 39
40. B. Bossy et al. S-Nitrosylation of DRP1 does not affect enzymatic activity and is not specific to Alzheimer's disease J. Alzheimers Dis. 20 Suppl. 2 2010 S513 526
41. G. Nagy, A. Koncz, and A. Perl T cell activation-induced mitochondrial hyperpolarization is mediated by Ca2+- and redox-dependent production of nitric oxide J. Immunol. 171 2003 5188 5197