BNIP3- and BNIP3L-Mediated Mitophagy Promotes the Generation of Natural Killer Cell Memory

Immunity

Volumn 43, Issue 2, 2015, Pages 331-342

  O'Sullivan, Timothy E ^a   Johnson, Lexus R ^a   Kang, Helen H ^b   Sun, Joseph C ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 3; CARRIER PROTEIN; CELL PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN BNIP3; PROTEIN BNIP3 LIKE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ATG3 PROTEIN, MOUSE; BNIP3 PROTEIN, MOUSE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; NIX PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE; UBIQUITIN CONJUGATING ENZYME;

ADENOVIRIDAE; ANIMAL CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; MITOCHONDRION; MITOPHAGY; NATURAL KILLER CELL; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; RAT; VIRUS INFECTION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MOUSE; MUROMEGALOVIRUS; VIROLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELLS, CULTURED; HERPESVIRIDAE INFECTIONS; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL PROTEINS; MUROMEGALOVIRUS; REACTIVE OXYGEN SPECIES; TOR SERINE-THREONINE KINASES; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84940978095     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.07.012     Document Type: Article

References (55)

1. Araki K., Turner A.P., Shaffer V.O., Gangappa S., Keller S.A., Bachmann M.F., Larsen C.P., Ahmed R. mTOR regulates memory CD8 T-cell differentiation. Nature 2009, 460:108-112.
2. Arase H., Mocarski E.S., Campbell A.E., Hill A.B., Lanier L.L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002, 296:1323-1326.
3. Beaulieu A.M., Zawislak C.L., Nakayama T., Sun J.C. The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection. Nat. Immunol. 2014, 15:546-553.
4. Chen M., Hong M.J., Sun H., Wang L., Shi X., Gilbert B.E., Corry D.B., Kheradmand F., Wang J. Essential role for autophagy in the maintenance of immunological memory against influenza infection. Nat. Med. 2014, 20:503-510.
5. Cunningham J.T., Rodgers J.T., Arlow D.H., Vazquez F., Mootha V.K., Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 2007, 450:736-740.
6. Daniels K.A., Devora G., Lai W.C., O'Donnell C.L., Bennett M., Welsh R.M. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J. Exp. Med. 2001, 194:29-44.
7. Della Chiesa M., Falco M., Podestà M., Locatelli F., Moretta L., Frassoni F., Moretta A. Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus?. Blood 2012, 119:399-410.
8. Diwan A., Koesters A.G., Odley A.M., Pushkaran S., Baines C.P., Spike B.T., Daria D., Jegga A.G., Geiger H., Aronow B.J., et al. Unrestrained erythroblast development in Nix-/- mice reveals a mechanism for apoptotic modulation of erythropoiesis. Proc. Natl. Acad. Sci. USA 2007, 104:6794-6799.
9. Diwan A., Krenz M., Syed F.M., Wansapura J., Ren X., Koesters A.G., Li H., Kirshenbaum L.A., Hahn H.S., Robbins J., et al. Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice. J. Clin. Invest. 2007, 117:2825-2833.
10. Dokun A.O., Kim S., Smith H.R., Kang H.S., Chu D.T., Yokoyama W.M. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2001, 2:951-956.
11. Elmore S.P., Qian T., Grissom S.F., Lemasters J.J. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 2001, 15:2286-2287.
12. Fodil-Cornu N., Lee S.H., Belanger S., Makrigiannis A.P., Biron C.A., Buller R.M., Vidal S.M. Ly49h-deficient C57BL/6 mice: a new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex. J. Immunol. 2008, 181:6394-6405.
13. Foley B., Cooley S., Verneris M.R., Curtsinger J., Luo X., Waller E.K., Anasetti C., Weisdorf D., Miller J.S. Human cytomegalovirus (CMV)-induced memory-like NKG2C(+) NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J. Immunol. 2012, 189:5082-5088.
14. Foley B., Cooley S., Verneris M.R., Pitt M., Curtsinger J., Luo X., Lopez-Vergès S., Lanier L.L., Weisdorf D., Miller J.S. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 2012, 119:2665-2674.
15. Glick D., Zhang W., Beaton M., Marsboom G., Gruber M., Simon M.C., Hart J., Dorn G.W., Brady M.J., Macleod K.F. BNip3 regulates mitochondrial function and lipid metabolism in the liver. Mol. Cell. Biol. 2012, 32:2570-2584.
16. Grayson J.M., Laniewski N.G., Lanier J.G., Ahmed R. Mitochondrial potential and reactive oxygen intermediates in antigen-specific CD8+ T cells during viral infection. J. Immunol. 2003, 170:4745-4751.
17. Green D.R., Galluzzi L., Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011, 333:1109-1112.
18. Hanna R.A., Quinsay M.N., Orogo A.M., Giang K., Rikka S., Gustafsson A.B. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J. Biol. Chem. 2012, 287:19094-19104.
19. Hendricks D.W., Balfour H.H., Dunmire S.K., Schmeling D.O., Hogquist K.A., Lanier L.L. Cutting edge: NKG2C(hi)CD57+ NK cells respond specifically to acute infection with cytomegalovirus and not Epstein-Barr virus. J. Immunol. 2014, 192:4492-4496.
20. Jia W., He Y.W. Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J. Immunol. 2011, 186:5313-5322.
21. Karo J.M., Schatz D.G., Sun J.C. The RAG recombinase dictates functional heterogeneity and cellular fitness in natural killer cells. Cell 2014, 159:94-107.
22. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
23. Klionsky D.J., Abdalla F.C., Abeliovich H., Abraham R.T., Acevedo-Arozena A., Adeli K., Agholme L., Agnello M., Agostinis P., Aguirre-Ghiso J.A., et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8:445-544.
24. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nat. Med. 2000, 6:513-519.
25. Kurtulus S., Tripathi P., Opferman J.T., Hildeman D.A. Contracting the 'mus cells'--does down-sizing suit us for diving into the memory pool?. Immunol. Rev. 2010, 236:54-67.
26. Lanier L.L. NK cell recognition. Annu. Rev. Immunol. 2005, 23:225-274.
27. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
28. +NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 2011, 108:14725-14732.
29. Mammucari C., Milan G., Romanello V., Masiero E., Rudolf R., Del Piccolo P., Burden S.J., Di Lisi R., Sandri C., Zhao J., et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007, 6:458-471.
30. Marçais A., Cherfils-Vicini J., Viant C., Degouve S., Viel S., Fenis A., Rabilloud J., Mayol K., Tavares A., Bienvenu J., et al. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat. Immunol. 2014, 15:749-757.
31. Mariño G., Niso-Santano M., Baehrecke E.H., Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2014, 15:81-94.
32. Marrack P., Kappler J. Control of T cell viability. Annu. Rev. Immunol. 2004, 22:765-787.
33. Min-Oo G., Bezman N.A., Madera S., Sun J.C., Lanier L.L. Proapoptotic Bim regulates antigen-specific NK cell contraction and the generation of the memory NK cell pool after cytomegalovirus infection. J. Exp. Med. 2014, 211:1289-1296.
34. Mizushima N., Yamamoto A., Matsui M., Yoshimori T., Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 2004, 15:1101-1111.
35. Narni-Mancinelli E., Chaix J., Fenis A., Kerdiles Y.M., Yessaad N., Reynders A., Gregoire C., Luche H., Ugolini S., Tomasello E., et al. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 2011, 108:18324-18329.
36. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., Rogov V., Löhr F., Popovic D., Occhipinti A., et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
37. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., Øvervatn A., Bjørkøy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282:24131-24145.
38. Pearce E.L., Walsh M.C., Cejas P.J., Harms G.M., Shen H., Wang L.S., Jones R.G., Choi Y. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009, 460:103-107.
39. 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.
40. Puleston D.J., Zhang H., Powell T.J., Lipina E., Sims S., Panse I., Watson A.S., Cerundolo V., Townsend A.R., Klenerman P., Simon A.K. Autophagy is a critical regulator of memory CD8(+) T cell formation. eLife 2014, 3:3.
41. Sandoval H., Thiagarajan P., Dasgupta S.K., Schumacher A., Prchal J.T., Chen M., Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008, 454:232-235.
42. Schweers R.L., Zhang J., Randall M.S., Loyd M.R., Li W., Dorsey F.C., Kundu M., Opferman J.T., Cleveland J.L., Miller J.L., Ney P.A. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA 2007, 104:19500-19505.
43. Singh R., Kaushik S., Wang Y., Xiang Y., Novak I., Komatsu M., Tanaka K., Cuervo A.M., Czaja M.J. Autophagy regulates lipid metabolism. Nature 2009, 458:1131-1135.
44. Smith H.R., Heusel J.W., Mehta I.K., Kim S., Dorner B.G., Naidenko O.V., Iizuka K., Furukawa H., Beckman D.L., Pingel J.T., et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. USA 2002, 99:8826-8831.
45. Sterky F.H., Lee S., Wibom R., Olson L., Larsson N.G. Impaired mitochondrial transport and Parkin-independent degeneration of respiratory chain-deficient dopamine neurons in vivo. Proc. Natl. Acad. Sci. USA 2011, 108:12937-12942.
46. + T cells. Nat. Rev. Immunol. 2011, 11:645-657.
47. Sun J.C., Beilke J.N., Lanier L.L. Adaptive immune features of natural killer cells. Nature 2009, 457:557-561.
48. Sun J.C., Madera S., Bezman N.A., Beilke J.N., Kaplan M.H., Lanier L.L. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 2012, 209:947-954.
49. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008, 27:433-446.
50. van der Windt G.J., Everts B., Chang C.H., Curtis J.D., Freitas T.C., Amiel E., Pearce E.J., Pearce E.L. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity 2012, 36:68-78.
51. Vivier E., Raulet D.H., Moretta A., Caligiuri M.A., Zitvogel L., Lanier L.L., Yokoyama W.M., Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science 2011, 331:44-49.
52. Webster K.A., Graham R.M., Bishopric N.H. BNip3 and signal-specific programmed death in the heart. J. Mol. Cell. Cardiol. 2005, 38:35-45.
53. Xu X., Araki K., Li S., Han J.H., Ye L., Tan W.G., Konieczny B.T., Bruinsma M.W., Martinez J., Pearce E.L., et al. Autophagy is essential for effector CD8(+) T cell survival and memory formation. Nat. Immunol. 2014, 15:1152-1161.
54. Zhang J., Ney P.A. Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 2009, 16:939-946.
55. Zhu Y., Massen S., Terenzio M., Lang V., Chen-Lindner S., Eils R., Novak I., Dikic I., Hamacher-Brady A., Brady N.R. Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J. Biol. Chem. 2013, 288:1099-1113.