Mitochondria are gate-keepers of T cell function by producing the ATP that drives purinergic signaling

Journal of Biological Chemistry

Volumn 289, Issue 37, 2014, Pages 25936-25945

  Ledderose, Carola ^a   Bao, Yi ^a   Lidicky, Markus ^a   Zipperle, Johannes ^a   Li, Linglin ^a   Strasser, Katharina ^a   Shapiro, Nathan I ^b   Junger, Wolfgang G ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

^c LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELL MEMBRANES; CELLS; CHEMICAL ACTIVATION; CYTOLOGY; ENZYME ACTIVITY; MITOCHONDRIA; NETWORK SECURITY; T-CELLS;

EXTRACELLULAR SPACE; INTRACELLULAR ATP; INTRACELLULAR CA; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE PHOSPHORYLATION; PURINERGIC RECEPTORS; RAPID ACTIVATION; SIGNALING MECHANISMS;

CELL SIGNALING;

ADENOSINE TRIPHOSPHATE; CALCIUM; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CD69 ANTIGEN; INTERLEUKIN 2; POTASSIUM CHANNEL; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC RECEPTOR; REACTIVE OXYGEN METABOLITE; ROTENONE;

ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; AUTOCRINE EFFECT; CALCIUM TRANSPORT; CD4+ T LYMPHOCYTE; CELL STIMULATION; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; EXTRACELLULAR SPACE; HOST RESISTANCE; IMMUNE RESPONSE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; BIOSYNTHESIS; CALCIUM SIGNALING; CELLULAR IMMUNITY; COMMUNICABLE DISEASE; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; METABOLISM; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; AUTOCRINE COMMUNICATION; CALCIUM SIGNALING; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; COMMUNICABLE DISEASES; HUMANS; IMMUNITY, CELLULAR; IMMUNOSUPPRESSION; INFLAMMATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; RECEPTORS, PURINERGIC; T-LYMPHOCYTES;

EID: 84907168821     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.575308     Document Type: Article

References (51)

1. Hotchkiss, R. S., Monneret, G., and Payen, D. (2013) Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect. Dis. 13, 260-268
2. Hotchkiss, R. S., Monneret, G., and Payen, D. (2013) Sepsis-induced immunosuppression: from cellular dysfunction to immunotherapy. Nat. Rev. Immunol. 13, 862-874
3. Schenk, U., Westendorf, A. M., Radaelli, E., Casati, A., Ferro, M., Fumagalli, M., Verderio, C., Buer, J., Scanziani, E., and Grassi, F. (2008) Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal 1, ra6
4. Yip, L., Woehrle, T., Corriden, R., Hirsh, M., Chen, Y., Inoue, Y., Ferrari, V., Insel, P. A., and Junger, W. G. (2009) Autocrine regulation of T-cell activation by ATP release and P2X7 receptors. FASEB J. 23, 1685-1693
5. Woehrle, T., Yip, L., Elkhal, A., Sumi, Y., Chen, Y., Yao, Y., Insel, P. A., and Junger, W. G. (2010) Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 116, 3475-3484
6. Junger, W. G. (2011) Immune cell regulation by autocrine purinergic signaling. Nat. Rev. Immunol. 11, 201-212
7. Pearce, E. L. (2010) Metabolism in T cell activation and differentiation. Curr. Opin Immunol. 22, 314-320
8. Fox, C. J., Hammerman, P. S., and Thompson, C. B. (2005) Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 5, 844-852
9. Wang, R., and Green, D. R. (2012) Metabolic reprogramming and metabolic dependency in T cells. Immunol. Rev. 249, 14-26
10. Gerriets, V. A., and Rathmel J. C. (2012) Metabolic pathways in T cell fate and function. Trends Immunol. 33, 168-173
11. Hoth, M., Fanger, C. M., and Lewis, R. S. (1997) Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J. Cell Biol. 137, 633-648
12. Quintana, A., Schwindling, C., Wenning, A. S., Becherer, U., Rettig, J., Schwarz, E. C., and Hoth, M. (2007) T cell activation requires mitochondrial translocation to the immunological synapse. Proc. Natl. Acad. Sci. U.S.A. 104, 14418-14423
13. Sena, L. A., Li, S., Jairaman, A., Prakriya, M., Ezponda, T., Hildeman, D. T., Wang, C., Schumacker, P. T., Licht, J. D., Perlman, H., Bryce, P. J., and Chandel, N. S. (2013) Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38, 225-236
14. Wu, J., Liu, L., Matsuda, T., Zhao, Y., Rebane, A., Drobizhev, M., Chang, Y. F., Araki, S., Arai, Y., March, K., Hughes, T. E., Sagou, K., Miyata, T., Nagai, T., Li, W., and Campbell, R. E. (2013) Improved orange and red Ca2+ indicators and photophysical considerations for optogenetic applications. ACS Chem. Neurosci. 4, 963-972
15. Bone, R. C., Sibbald, W. J., and Sprung, C. L. (1992) The ACCP-SCCM consensus conference on sepsis and organ failure. Chest 101, 1481-1483
16. Lazarowski, E. R., Tarran, R., Grubb, B. R., van Heusden, C. A., Okada, S., and Boucher, R. C. (2004) Nucleotide release provides a mechanism for airway surface liquid homeostasis. J. Biol. Chem. 279, 36855-36864
17. Kurishita, Y., Kohira, T., Ojida, A., and Hamachi, I. (2012) Organellelocalizable fluorescent chemosensors for site-specific multicolor imaging of nucleoside polyphosphate dynamics in living cells. J. Am. Chem. Soc. 134, 18779-18789
18. Royall J. A., and Ischiropoulos, H. (1993) Evaluation of 2',7'-dichlorofluorescein and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch. Biochem. Biophys. 302, 348-355
19. Woehrle, T., Yip, L., Manohar, M., Sumi, Y., Yao, Y., Chen, Y., and Junger, W. G. (2010) Hypertonic stress regulates T cell function via pannexin-1 hemichannels and P2X receptors. J. Leukoc Biol. 88, 1181-1189
20. Séror, C., Melki, M. T., Subra, F., Raza, S. Q., Bras, M., Saïdi, H., Nardacci, R., Voisin, L., Paoletti, A., Law, F., Martins, I., Amendola, A., Abdul-Sater, A. A., Ciccosanti, F., Delelis, O., Niedergang, F., Thierry, S., Said-Sadier, N., Lamaze, C., Métivier, D., Estaquier, J., Fimia, G. M., Falasca, L., Casetti, R., Modjtahedi, N., Kanellopoulos, J., Mouscadet, J. F., Ojcius, D. M., Piacentini, M., Gougeon, M. L., Kroemer, G., and Perfettini, J. L. (2011) Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J. Exp. Med. 208, 1823-1834
21. Zhang, Y., Li, H., Wang, X., Gao, X., and Liu, X. (2009) Regulation of T cell development and activation by creatine kinase B. PLoS One 4, e5000
22. Choi, O., Heathcote, D. A., Ho, K. K, Müller, P. J., Ghani, H., Lam, E. W., Ashton-Rickardt, P. G., and Rutschmann, S. (2012) A deficiency in nucleoside salvage impairs murine lymphocyte development, homeostasis, and survival. J. Immunol. 188, 3920-3927
23. Monks, C. R., Freiberg, B. A., Kupfer, H., Sciaky, N., and Kupfer, A. (1998) Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86
24. Baixauli, F., Martín-Cófreces, N. B., Morlino, G., Carrasco, Y. R., Calabia-Linares, C., Veiga, E., Serrador, J. M., and Sánchez-Madrid, F. (2011) The mitochondrial fission factor dynamin-related protein 1 modulates T-cell receptor signalling at the immune synapse. EMBO J. 30, 1238-1250
25. Campi, G., Varma, R., and Dustin, M. L. (2005) Actin and agonist MHCpeptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J. Exp. Med. 202, 1031-1036
26. Kann O., and Kovács, R. (2007) Mitochodria and neuronal activity. Am. J. Physiol. Cell Physiol 292, C641-C657
27. McCormack, J. G., Halestrap, A. P., and Denton, R. M. (1990) Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev. 70, 391-425
28. Gunter, T. E., Yule, D. I., Gunter, K. K., Eliseev, R. A., and Salter, J. D. (2004) Calcium and mitochondria. FEBS Lett. 567, 96-102
29. Glancy, B., and Balaban, R. S. (2012) Role of mitochondrial Ca2+ in the regulation of cellular energetic. Biochemistry 51, 2959-2973
30. Ojida, A., Takashima, I., Kohira, T., Nonaka, H., and Hamachi, I. (2008) Turn-on fluorescence sensing of nucleoside polyphosphates using a xanthene- based Zn(II) complex chemosensor. J. Am. Chem. Soc. 130, 12095-12101
31. Lewis, R. S. (2001) Calcium signaling mechanisms in T lymphocytes. Annu. Rev. Immunol. 19, 497-521
32. Jones, R. G., and Thompson, C. B. (2007) Revving the engine: signal transduction fuels T cell activation. Immunity 72, 173-178
33. Krauss, S., Brand, M. D., and Buttgereit, F. (2001) Signaling takes a breath - new quantitative perspectives on bioenergetics and signal transduction. Immunity 15, 497-502
34. Sena, L. A., and Chandel, N. S. (2012) Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48, 158-167
35. Dehkordy, S. F., Aghamohammadi, A., Ochs, H. D., and Rezaei, N. (2012) Primary immunodeficiency diseases associated with neurologic manifestations. J. Clin. Immunol. 32, 1-24
36. Nyhan, W. (2005) Disorders of purine and pyrimidine metabolism. Mol. Genet. Metab. 86, 25-33
37. Markert, M. L. (1991) Purine nucleoside phosphorylase deficiency. Immunodefic Rev. 3, 45-81
38. Schwindling, C., Quintana, A., Krause, E., and Hoth, M. (2010) Mitochondria positioning controls local calcium influx in T cells. J. Immunol. 184, 184-190
39. Devadas, S., Zaritskaya, L., Rhee, S. G., Oberley, L., and Williams, M. S. (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, 59-70
40. Kaminski, M. M., Sauer, S. W., Klemke, C. D., Süss, D., Okun, J. G., Krammer, P. H., and Gülow, K. (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, 4827-4841
41. Kamiński, M. M., Röth, D., Sass, S., Sauer, S. W., Krammer, P. H., and Gülow, K. (2012) Manganese superoxide dismutase: a regulator of T cell activation induced oxidative signaling and cell death. Biochim. Biophys. Acta 1823, 1041-1052
42. Van der Merwe, P. A., and Davis, S. J. (2003) Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 21, 659-684
43. Tokunaga, A., Tsukimoto, M., Harada, H., Moriyama, Y., and Kojima, S. (2010) Involvement of SLC-17A9-dependent vesicular exocytosis in the mechanism of ATP release during T cell activation. J. Biol. Chem. 285, 17406-17416
44. Wherry, E. J. (2011) T cell exhaustion. Nat. Immunol. 12, 492-499
45. Faist, E., Schinkel, C., Zimmer, S., Kremer, J. P., Von Donnersmarck, G. H., and Schildberg, F. W. (1993) Inadequate interleukin-2 synthesis and interleukin- 2 messenger expression following thermal and mechanical trauma in humans is caused by defective transmembrane signalling. J. Trauma 34, 846-853
46. Chaudry, I. H., and Bland, K. I. (2009) Cellular mechanisms of injury after major trauma. Br. J. Surg 96, 1097-1098
47. Hoyt, D. B., Junger, W. G., Loomis, W. H., and Liu, F. C. (1994) Effects of trauma on immune cell function: impairment of intracellular calcium signaling. Shock 2, 23-28
48. Belikova, I., Lukaszewicz, A. C., Faivre, V., Damoisel, C., Singer, M., and Payen, D. (2007) Oxygen consumption of human peripheral blood mononuclear cells in severe human sepsis. Crit. Care Med. 35, 2702-2708
49. Japiassú, A. M., Santiago, A. P., d'Avila, J. C., Garcia-Souza, L., Galina, A., Castro Faria-Neto, H. C., Bozza, F. A., and Oliveira, M. F. (2011) Bioenergetic failure of human peripheral blood monocytes in septic shock patients is mediated by reduced F1F0 ATP synthase activity. Crit. Care Med. 39, 1056-1063
50. Chida, J., Ono, R., Yamane, K., Hiyoshi, M., Nishimura, M., Onodera, M., Nakataki, E., Shichijo, K., Matushita, M., and Kido, H. (2013) Blood lactate/ ATP ratio, as an alarm index and real-time biomarker in critical illness. PloS One 8, e60561
51. Gray, M. W., Burger, G., and Lang, B. F. (1999) Mitochondrial evolution. Science 283, 1476-1481