T cell Activation Is Driven by an ADP-Dependent Glucokinase Linking Enhanced Glycolysis with Mitochondrial Reactive Oxygen Species Generation

Cell Reports

Volumn 2, Issue 5, 2012, Pages 1300-1315

  Kamiński, Marcin M ^a   Sauer, Sven W ^b   Kamiński, Marian ^c   Opp, Silvana ^b   Ruppert, Thorsten ^b   Grigaravičius, Paulius ^a   Grudnik, Przemyslaw ^d   Gröne, Hermann Josef ^a   Krammer, Peter H ^a   Gülow, Karsten ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c GDANSK UNIVERSITY OF TECHNOLOGY   (Poland)

^d JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ADP DEPENDENT GLUCOKINASE; GLUCOKINASE; GLUCOSE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REACTIVE OXYGEN METABOLITE; T LYMPHOCYTE RECEPTOR; UBIQUINONE; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ARCHAEON; ARTICLE; BIOENERGY; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOSOL; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; GENE EXPRESSION; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; HUMAN CELL; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

AMINO ACID SEQUENCE; ARCHAEA; DOWN-REGULATION; ENDOPLASMIC RETICULUM; GLUCOKINASE; GLYCEROLPHOSPHATE DEHYDROGENASE; GLYCOLYSIS; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PROTEIN STRUCTURE, SECONDARY; REACTIVE OXYGEN SPECIES; RECEPTORS, ANTIGEN, T-CELL; RNA INTERFERENCE; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT; T-LYMPHOCYTES; UBIQUINONE;

EUKARYOTA;

EID: 84870462073     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.10.009     Document Type: Article

References (52)

1. Arismendi-Morillo G. Electron microscopy morphology of the mitochondrial network in gliomas and their vascular microenvironment. Biochim. Biophys. Acta 2011, 1807:602-608.
2. Batandier C., Guigas B., Detaille D., El-Mir M.Y., Fontaine E., Rigoulet M., Leverve X.M. The ROS production induced by a reverse-electron flux at respiratory-chain complex 1 is hampered by metformin. J. Bioenerg. Biomembr. 2006, 38:33-42.
3. Baud V., Karin M. Is NF-κB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 2009, 8:33-40.
4. Bell E.L., Klimova T.A., Eisenbart J., Moraes C.T., Murphy M.P., Budinger G.R., Chandel N.S. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J. Cell Biol. 2007, 177:1029-1036.
5. Bental M., Deutsch C. Metabolic changes in activated T cells: an NMR study of human peripheral blood lymphocytes. Magn. Reson. Med. 1993, 29:317-326.
6. Chowdhury S.K., Gemin A., Singh G. High activity of mitochondrial glycerophosphate dehydrogenase and glycerophosphate-dependent ROS production in prostate cancer cell lines. Biochem. Biophys. Res. Commun. 2005, 333:1139-1145.
7. Collison L.W., Murphy E.J., Jolly C.A. Glycerol-3-phosphate acyltransferase-1 regulates murine T-lymphocyte proliferation and cytokine production. Am. J. Physiol. Cell Physiol. 2008, 295:C1543-C1549.
8. Cottingham I.R., Ragan C.I. The reconstitution of L-3-glycerophosphate-cytochrome c oxidoreductase from L-3-glycerophosphate dehydrogenase, ubiquinone-10 and ubiquinol-cytochrome c oxidoreductase. Biochem. J. 1980, 192:19-31.
9. Devadas S., Zaritskaya L., Rhee S.G., Oberley L., Williams M.S. 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.
10. Doherty M., Boot-Handford R.P., Grant M.E., Canfield A.E. Identification of genes expressed during the osteogenic differentiation of vascular pericytes in vitro. Biochem. Soc. Trans. 1998, 26:S4.
11. Dröge W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82:47-95.
12. Dröse S., Brandt U. Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 2012, 748:145-169.
13. Dröse S., Bleier L., Brandt U. A common mechanism links differently acting complex II inhibitors to cardioprotection: modulation of mitochondrial reactive oxygen species production. Mol. Pharmacol. 2011, 79:814-822.
14. Feske S. Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 2007, 7:690-702.
15. Gao X., Wang H., Yang J.J., Liu X., Liu Z.R. Pyruvate kinase M2 regulates gene transcription by acting as a protein kinase. Mol. Cell 2012, 45:598-609.
16. Gülow K., Kaminski M., Darvas K., Süss D., Li-Weber M., Krammer P.H. HIV-1 trans-activator of transcription substitutes for oxidative signaling in activation-induced T cell death. J. Immunol. 2005, 174:5249-5260.
17. 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, 212:95-99.
18. Hruz T., Laule O., Szabo G., Wessendorp F., Bleuler S., Oertle L., Widmayer P., Gruissem W., Zimmermann P. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinforma. 2008, 2008:420747.
19. Idahl L.A., Lembert N. Glycerol 3-phosphate-induced ATP production in intact mitochondria from pancreatic B-cells. Biochem. J. 1995, 312:287-292.
20. Jackson S.H., Devadas S., Kwon J., Pinto L.A., Williams M.S. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat. Immunol. 2004, 5:818-827.
21. Jacobs S.R., Herman C.E., Maciver N.J., Wofford J.A., Wieman H.L., Hammen J.J., Rathmell J.C. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 2008, 180:4476-4486.
22. 2+ homeostasis. Immunity 2007, 27:268-280.
23. Kamiński M., Kiessling M., Süss D., Krammer P.H., Gülow K. Novel role for mitochondria: protein kinase Cθ-dependent oxidative signaling organelles in activation-induced T-cell death. Mol. Cell. Biol. 2007, 27:3625-3639.
24. Kamiński M.M., Sauer S.W., Klemke C.D., Süss D., Okun J.G., Krammer P.H., Gülow K. Mitochondrial reactive oxygen species control T cell activation by regulating IL-2 and IL-4 expression: mechanism of ciprofloxacin-mediated immunosuppression. J. Immunol. 2010, 184:4827-4841.
25. Kamiński M.M., Röth D., Sass S., Sauer S.W., Krammer P.H., Gülow K. Manganese superoxide dismutase: a regulator of T cell activation-induced oxidative signaling and cell death. Biochim. Biophys. Acta 2012, 1823:1041-1052.
26. Krawczyk C.M., Holowka T., Sun J., Blagih J., Amiel E., DeBerardinis R.J., Cross J.R., Jung E., Thompson C.B., Jones R.G., Pearce E.J. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 2010, 115:4742-4749.
27. Krivanek J., Novakova L. ATP-citrate lyase is another enzyme the histidine phosphorylation of which is inhibited by vanadate. FEBS Lett. 1991, 282:32-34.
28. Kwon J., Shatynski K.E., Chen H., Morand S., de Deken X., Miot F., Leto T.L., Williams M.S. The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling. Sci. Signal. 2010, 3:ra59.
29. Lambert A.J., Brand M.D. Reactive oxygen species production by mitochondria. Methods Mol. Biol. 2009, 554:165-181.
30. Los M., Schenk H., Hexel K., Baeuerle P.A., Dröge W., Schulze-Osthoff K. IL-2 gene expression and NF-κB activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J. 1995, 14:3731-3740.
31. Mannella C.A. Structure and dynamics of the mitochondrial inner membrane cristae. Biochim. Biophys. Acta 2006, 1763:542-548.
32. Miccheli A., Tomassini A., Puccetti C., Valerio M., Peluso G., Tuccillo F., Calvani M., Manetti C., Conti F. Metabolic profiling by 13C-NMR spectroscopy: [1,2-13C2]glucose reveals a heterogeneous metabolism in human leukemia T cells. Biochimie 2006, 88:437-448.
33. Miwa S., St-Pierre J., Partridge L., Brand M.D. Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic. Biol. Med. 2003, 35:938-948.
34. Netzker R., Greiner E., Eigenbrodt E., Noguchi T., Tanaka T., Brand K. Cell cycle-associated expression of M2-type isozyme of pyruvate kinase in proliferating rat thymocytes. J. Biol. Chem. 1992, 267:6421-6424.
35. Nishikawa T., Edelstein D., Du X.L., Yamagishi S., Matsumura T., Kaneda Y., Yorek M.A., Beebe D., Oates P.J., Hammes H.P., et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404:787-790.
36. Qin J., Chai G., Brewer J.M., Lovelace L.L., Lebioda L. Fluoride inhibition of enolase: crystal structure and thermodynamics. Biochemistry 2006, 45:793-800.
37. Richter S., Richter J.P., Mehta S.Y., Gribble A.M., Sutherland-Smith A.J., Stowell K.M., Print C.G., Ronimus R.S., Wilson W.R. Expression and role in glycolysis of human ADP-dependent glucokinase. Mol. Cell. Biochem. 2012, 364:131-145.
38. Ronimus R.S., Morgan H.W. Cloning and biochemical characterization of a novel mouse ADP-dependent glucokinase. Biochem. Biophys. Res. Commun. 2004, 315:652-658.
39. 2+ within electropermeabilized insulin-secreting cells (INS-1). Biochim. Biophys. Acta 1992, 1175:107-113.
40. Stentz F.B., Kitabchi A.E. Hyperglycemia-induced activation of human T-lymphocytes with de novo emergence of insulin receptors and generation of reactive oxygen species. Biochem. Biophys. Res. Commun. 2005, 335:491-495.
41. Tretter L., Takacs K., Hegedus V., Adam-Vizi V. Characteristics of α-glycerophosphate-evoked H2O2 generation in brain mitochondria. J. Neurochem. 2007, 100:650-663.
42. Tsuge H., Sakuraba H., Kobe T., Kujime A., Katunuma N., Ohshima T. Crystal structure of the ADP-dependent glucokinase from Pyrococcus horikoshii at 2.0-å resolution: a large conformational change in ADP-dependent glucokinase. Protein Sci. 2002, 11:2456-2463.
43. Tu K.Y., Ju H.S., Pettit F., Shive W., Topek N.H., Matthews R., Matthews K. Glycerol-3-phosphate dehydrogenase activity in human lymphocytes: effects of insulin, obesity and weight loss. Biochem. Biophys. Res. Commun. 1995, 207:183-190.
44. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
45. Vander Heiden M.G., Locasale J.W., Swanson K.D., Sharfi H., Heffron G.J., Amador-Noguez D., Christofk H.R., Wagner G., Rabinowitz J.D., Asara J.M., Cantley L.C. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 2010, 329:1492-1499.
46. Wang T., Marquardt C., Foker J. Aerobic glycolysis during lymphocyte proliferation. Nature 1976, 261:702-705.
47. Warburg O. On respiratory impairment in cancer cells. Science 1956, 124:269-270.
48. Wellen K.E., Thompson C.B. Cellular metabolic stress: considering how cells respond to nutrient excess. Mol. Cell 2010, 40:323-332.
49. Wick A.N., Drury D.R., Nakada H.I., Wolfe J.B. Localization of the primary metabolic block produced by 2-deoxyglucose. J. Biol. Chem. 1957, 224:963-969.
50. Wilson J.E. Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J. Exp. Biol. 2003, 206:2049-2057.
51. Wu C., Orozco C., Boyer J., Leglise M., Goodale J., Batalov S., Hodge C.L., Haase J., Janes J., Huss J.W., Su A.I. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009, 10:R130.
52. Yi J.S., Holbrook B.C., Michalek R.D., Laniewski N.G., Grayson J.M. Electron transport complex I is required for CD8+ T cell function. J. Immunol. 2006, 177:852-862.