Apoptosis-Inducing-Factor-Dependent Mitochondrial Function Is Required for T Cell but Not B Cell Function

Immunity

Volumn 44, Issue 1, 2016, Pages 88-102

  Milasta, Sandra ^a   Dillon, Christopher P ^a   Sturm, Oliver E ^b   Verbist, Katherine C ^a   Brewer, Taylor L ^a   Quarato, Giovanni ^a   Brown, Scott A ^a   Frase, Sharon ^a   Janke, Laura J ^a   Perry, S Scott ^a   Thomas, Paul G ^a   Green, Douglas R ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b RHODES COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; PDCD8 PROTEIN, MOUSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; FIBROBLAST; HOMEOSTASIS; LYMPHOCYTE FUNCTION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; THYMOCYTE; ANIMAL; APOPTOSIS; CELL RESPIRATION; GLYCOLYSIS; KNOCKOUT MOUSE; METABOLISM; MUTANT MOUSE STRAIN; PHYSIOLOGY;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; B-LYMPHOCYTES; CELL RESPIRATION; ELECTRON TRANSPORT COMPLEX I; FIBROBLASTS; GLYCOLYSIS; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MITOCHONDRIA; T-LYMPHOCYTES;

EID: 84958908189     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.12.002     Document Type: Article

References (45)

1. Badea T.C., Wang Y., Nathans J. A noninvasive genetic/pharmacologic strategy for visualizing cell morphology and clonal relationships in the mouse. J. Neurosci. 2003, 23:2314-2322.
2. Banerjee H., Das A., Srivastava S., Mattoo H.R., Thyagarajan K., Khalsa J.K., Tanwar S., Das D.S., Majumdar S.S., George A., et al. A role for apoptosis-inducing factor in T cell development. J. Exp. Med. 2012, 209:1641-1653.
3. Bénit P., Goncalves S., Dassa E.P., Brière J.J., Rustin P. The variability of the harlequin mouse phenotype resembles that of human mitochondrial-complex I-deficiency syndromes. PLoS ONE 2008, 3:e3208.
4. Bettini M.L., Bettini M., Nakayama M., Guy C.S., Vignali D.A.A. Generation of T cell receptor-retrogenic mice: improved retroviral-mediated stem cell gene transfer. Nat. Protoc. 2013, 8:1837-1840.
5. Brown D., Yu B.D., Joza N., Bénit P., Meneses J., Firpo M., Rustin P., Penninger J.M., Martin G.R. Loss of Aif function causes cell death in the mouse embryo, but the temporal progression of patterning is normal. Proc. Natl. Acad. Sci. USA 2006, 103:9918-9923.
6. Candé C., Cohen I., Daugas E., Ravagnan L., Larochette N., Zamzami N., Kroemer G. Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria. Biochimie 2002, 84:215-222.
7. Caro-Maldonado A., Wang R., Nichols A.G., Kuraoka M., Milasta S., Sun L.D., Gavin A.L., Abel E.D., Kelsoe G., Green D.R., Rathmell J.C. Metabolic reprogramming is required for antibody production that is suppressed in anergic but exaggerated in chronically BAFF-exposed B cells. J. Immunol. 2014, 192:3626-3636.
8. Chinta S.J., Rane A., Yadava N., Andersen J.K., Nicholls D.G., Polster B.M. Reactive oxygen species regulation by AIF- and complex I-depleted brain mitochondria. Free Radic. Biol. Med. 2009, 46:939-947.
9. Daugas E., Nochy D., Ravagnan L., Loeffler M., Susin S.A., Zamzami N., Kroemer G. Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett. 2000, 476:118-123.
10. Daugas E., Susin S.A., Zamzami N., Ferri K.F., Irinopoulou T., Larochette N., Prévost M.C., Leber B., Andrews D., Penninger J., Kroemer G. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 2000, 14:729-739.
11. Duchen M.R. Mitochondria in health and disease: perspectives on a new mitochondrial biology. Mol. Aspects Med. 2004, 25:365-451.
12. Hangen E., Féraud O., Lachkar S., Mou H., Doti N., Fimia G.M., Lam N.-V., Zhu C., Godin I., Muller K., et al. Interaction between AIF and CHCHD4 Regulates Respiratory Chain Biogenesis. Mol. Cell 2015, 58:1001-1014.
13. Hennet T., Hagen F.K., Tabak L.A., Marth J.D. T-cell-specific deletion of a polypeptide N-acetylgalactosaminyl-transferase gene by site-directed recombination. Proc. Natl. Acad. Sci. USA 1995, 92:12070-12074.
14. Holst J., Szymczak-Workman A.L., Vignali K.M. Generation of T-cell receptor retrogenic mice: Abstract: Nature Protocols. Nature Protocols 2006.
15. Holst J., Vignali K.M., Burton A.R., Vignali D.A.A. Rapid analysis of T-cell selection in vivo using T cell-receptor retrogenic mice. Nat. Methods 2006, 3:191-197.
16. Holst J., Wang H., Eder K.D., Workman C.J., Boyd K.L., Baquet Z., Singh H., Forbes K., Chruscinski A., Smeyne R., et al. Scalable signaling mediated by T cell antigen receptor-CD3 ITAMs ensures effective negative selection and prevents autoimmunity. Nat. Immunol. 2008, 9:658-666.
17. Jia W., He Y.-W. Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J. Immunol. 2011, 186:5313-5322.
18. Johnson S.C., Yanos M.E., Kayser E.-B., Quintana A., Sangesland M., Castanza A., Uhde L., Hui J., Wall V.Z., Gagnidze A., et al. mTOR inhibition alleviates mitochondrial disease in a mouse model of Leigh syndrome. Science 2013, 342:1524-1528.
19. Joza N., Susin S.A., Daugas E., Stanford W.L., Cho S.K., Li C.Y.J., Sasaki T., Elia A.J., Cheng H.Y.M., Ravagnan L., et al. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 2001, 410:549-554.
20. Joza N., Oudit G.Y., Brown D., Bénit P., Kassiri Z., Vahsen N., Benoit L., Patel M.M., Nowikovsky K., Vassault A., et al. Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol. Cell. Biol. 2005, 25:10261-10272.
21. Joza N., Pospisilik J.A., Hangen E., Hanada T., Modjtahedi N., Penninger J.M., Kroemer G. AIF: not just an apoptosis-inducing factor. Ann. N Y Acad. Sci. 2009, 1171:2-11.
22. Kamiński M.M., Sauer S.W., Kamiński M., Opp S., Ruppert T., Grigaravičius P., Grudnik P., Gröne H.-J., Krammer P.H., Gülow K. T cell activation is driven by an ADP-dependent glucokinase linking enhanced glycolysis with mitochondrial reactive oxygen species generation. Cell Rep. 2012, 2:1300-1315.
23. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 2002, 419:367-374.
24. Kruse S.E., Watt W.C., Marcinek D.J., Kapur R.P., Schenkman K.A., Palmiter R.D. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 2008, 7:312-320.
25. Nicholls D.G. Mitochondrial function and dysfunction in the cell: its relevance to aging and aging-related disease. Int. J. Biochem. Cell Biol. 2002, 34:1372-1381.
26. Pitkanen S., Robinson B.H. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J. Clin. Invest. 1996, 98:345-351.
27. Pospisilik J.A., Knauf C., Joza N., Bénit P., Orthofer M., Cani P.D., Ebersberger I., Nakashima T., Sarao R., Neely G., et al. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 2007, 131:476-491.
28. Pua H.H., Guo J., Komatsu M., He Y.-W. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J. Immunol. 2009, 182:4046-4055.
29. Qiu J., Weber J.D., Pearce E.J., Jones R.G., Pearce E.L. Posttranscriptional Control of T Cell Effector Function by Aerobic Glycolysis. Cell 2013, 153:1239-1251.
30. Rickert R.C., Roes J., Rajewsky K. B lymphocyte-specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res. 1997, 25:1317-1318.
31. Robinson B. Human Complex I deficiency: Clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect. Biochimica Et Biophysica Acta (BBA) -Bioenergetics 1998, 1364:271-286.
32. Santidrian A.F., Matsuno-Yagi A., Ritland M., Seo B.B., LeBoeuf S.E., Gay L.J., Yagi T., Felding-Habermann B. Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression. J. Clin. Invest. 2013, 123:1068-1081.
33. Sena L.A., Li S., Jairaman A., Prakriya M., Ezponda T., Hildeman D.A., Wang C.-R., Schumacker P.T., Licht J.D., Perlman H., et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 2013, 38:225-236.
34. Seo B. Modulation of oxidative phosphorylation of human kidney 293 cells by transfection with the internal rotenone-insensitive NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae. Bioenergetics 1999, 1412:56-65.
35. Seo B.B., Wang J., Flotte T.R., Yagi T., Matsuno-Yagi A. Use of the NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae as a possible cure for complex I defects in human cells. J. Biol. Chem. 2000, 275:37774-37778.
36. Seo, B.B., Nakamaru-Ogiso, E., Cruz, P., Flotte, T.R., Yagi, T., and Matsuno-Yagi, A. (2004). Functional Expression of the Single Subunit NADH Dehydrogenase in Mitochondria In Vivo: A Potential Therapy for Complex I Deficiencies. doi:10.1089/Hum.2004.15.887.
37. Srinivas S., Watanabe T., Lin C.-S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
38. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
39. Tait S.W.G., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 2010, 11:621-632.
40. Takeuchi O., Fisher J., Suh H., Harada H., Malynn B.A., Korsmeyer S.J. Essential role of BAX,BAK in B cell homeostasis and prevention of autoimmune disease. Proc. Natl. Acad. Sci. USA 2005, 102:11272-11277.
41. Vahsen N., Candé C., Brière J.J., Bénit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., et al. AIF deficiency compromises oxidative phosphorylation. EMBO J. 2004, 23:4679-4689.
42. Wang R., Dillon C.P., Shi L.Z., Milasta S., Carter R., Finkelstein D., McCormick L.L., Fitzgerald P., Chi H., Munger J., Green D.R. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011, 35:871-882.
43. Weinberg F., Hamanaka R., Wheaton W.W., Weinberg S., Joseph J., Lopez M., Kalyanaraman B., Mutlu G.M., Budinger G.R.S., Chandel N.S. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc. Natl. Acad. Sci. USA 2010, 107:8788-8793.
44. Wissing S., Ludovico P., Herker E., Büttner S., Engelhardt S.M., Decker T., Link A., Proksch A., Rodrigues F., Corte-Real M., et al. An AIF orthologue regulates apoptosis in yeast. J. Cell Biol. 2004, 166:969-974.
45. 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.