Autophagy capacity and sub-mitochondrial heterogeneity shape Bnip3-induced mitophagy regulation of apoptosis

Cell Communication and Signaling

Volumn 13, Issue 1, 2015, Pages

  Choe, Sehyo Charley ^a,b,c   Hamacher Brady, Anne ^a,c   Brady, Nathan Ryan ^a,b,c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PROTEIN; PROTEIN BNIP3; REACTIVE OXYGEN METABOLITE; BNIP3 PROTEIN, HUMAN; BNIP3 PROTEIN, MOUSE; CYTOCHROME C; MEMBRANE PROTEIN; ONCOPROTEIN; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL HETEROGENEITY; CELL STIMULATION; CELLULAR PARAMETERS; CONTROLLED STUDY; DYNAMICS; EMBRYO; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; MITOCHONDRIAL OUTER MEMBRANE PERMEABILIZATION; MITOPHAGY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; ANIMAL; BIOLOGICAL MODEL; CELL LINE; HELA CELL LINE; METABOLISM; MITOCHONDRION;

ANIMALS; APOPTOSIS; CELL LINE; CYTOCHROMES C; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84938690751     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/s12964-015-0115-9     Document Type: Article

References (72)

1. Duchen MR. Roles of mitochondria in health and disease. Diabetes. 2004;53 Suppl 1:S96-102.
2. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ, et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol. 2006;8(12):1348-58.
3. Albeck JG, Burke JM, Aldridge BB, Zhang M, Lauffenburger DA, Sorger PK. Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol Cell. 2008;30(1):11-25.
4. Liu X, He Y, Li F, Huang Q, Kato TA, Hall RP, et al. Caspase-3 promotes genetic instability and carcinogenesis. Mol Cell. 2015;58(2):284-96.
5. Tang HL, Tang HM, Fung MC, Hardwick JM. In vivo CaspaseTracker biosensor system for detecting anastasis and non-apoptotic caspase activity. Sci Rep. 2015;5:9015.
6. Tang HL, Tang HM, Mak KH, Hu S, Wang SS, Wong KM, et al. Cell survival, DNA damage, and oncogenic transformation after a transient and reversible apoptotic response. Mol Biol Cell. 2012;23(12):2240-52.
7. Ichim G, Lopez J, Ahmed SU, Muthalagu N, Giampazolias E, Delgado ME, et al. Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death. Mol Cell. 2015;57(5):860-72.
8. Hamacher-Brady A. Autophagy regulation and integration with cell signaling. Antioxid Redox Signal. 2012;17(5):756-65.
9. Chourasia AH, Boland ML, Macleod KF. Mitophagy and cancer. Cancer Metab. 2015;3:4.
10. Zhang J, Ney PA. Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 2009;16(7):939-46.
11. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy. 2011;7(3):279-96.
12. Hanna RA, Quinsay MN, Orogo AM, Giang K, Rikka S, Gustafsson AB. 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(23):19094-104.
13. Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010;11(1):45-51.
14. Zhu Y, Massen S, Terenzio M, Lang V, Chen-Lindner S, Eils R, et al. Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J Biol Chem. 2013;288(2):1099-113.
15. Glick D, Zhang W, Beaton M, Marsboom G, Gruber M, Simon MC, et al. BNip3 regulates mitochondrial function and lipid metabolism in the liver. Mol Cell Biol. 2012;32(13):2570-84.
16. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci U S A. 2007;104(49):19500-5.
17. Dorn 2nd GW. Mitochondrial pruning by Nix and BNip3: an essential function for cardiac-expressed death factors. J Cardiovasc Transl Res. 2010;3(4):374-83.
18. Thorburn A. Autophagy and its effects: making sense of double-edged swords. PLoS Biol. 2014;12(10), e1001967.
19. Kim I, Lemasters JJ. Mitophagy selectively degrades individual damaged mitochondria after photoirradiation. Antioxid Redox Signal. 2011;14(10):1919-28.
20. Narendra DP, Youle RJ. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid Redox Signal. 2011;14(10):1929-38.
21. Jiang J, Huang Z, Zhao Q, Feng W, Belikova NA, Kagan VE. Interplay between bax, reactive oxygen species production, and cardiolipin oxidation during apoptosis. Biochem Biophys Res Commun. 2008;368(1):145-50.
22. Rehm M, Huber HJ, Hellwig CT, Anguissola S, Dussmann H, Prehn JH. Dynamics of outer mitochondrial membrane permeabilization during apoptosis. Cell Death Differ. 2009;16(4):613-23.
23. Liu L, Feng D, Chen G, Chen M, Zheng Q, Song P, et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol. 2012;14(2):177-85.
24. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183(5):795-803.
25. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature. 2008;454(7201):232-5.
26. Betin VM, Lane JD. Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis. J Cell Sci. 2009;122(Pt 14):2554-66.
27. Luo S, Rubinsztein DC. Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL. Cell Death Differ. 2010;17(2):268-77.
28. Wirawan E, Vande Walle L, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I, et al. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis. 2010;1:e18.
29. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, et al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol. 2006;8(10):1124-32.
30. Fleury C, Mignotte B, Vayssiere JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie. 2002;84(2-3):131-41.
31. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007;26(7):1749-60.
32. Song M, Chen Y, Gong G, Murphy E, Rabinovitch PS, Dorn 2nd GW. Super-suppression of mitochondrial reactive oxygen species signaling impairs compensatory autophagy in primary mitophagic cardiomyopathy. Circ Res. 2014;115(3):348-53.
33. Aon MA, Cortassa S, Marban E, O'Rourke B. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J Biol Chem. 2003;278(45):44735-44.
34. Brady NR, Elmore SP, van Beek JJ, Krab K, Courtoy PJ, Hue L, et al. Coordinated behavior of mitochondria in both space and time: a reactive oxygen species-activated wave of mitochondrial depolarization. Biophys J. 2004;87(3):2022-34.
35. Garcia-Perez C, Roy SS, Naghdi S, Lin X, Davies E, Hajnoczky G. Bid-induced mitochondrial membrane permeabilization waves propagated by local reactive oxygen species (ROS) signaling. Proc Natl Acad Sci U S A. 2012;109(12):4497-502.
36. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature. 2009;459(7245):428-32.
37. Thorburn J, Andrysik Z, Staskiewicz L, Gump J, Maycotte P, Oberst A, et al. Autophagy controls the kinetics and extent of mitochondrial apoptosis by regulating PUMA levels. Cell Rep. 2014;7(1):45-52.
38. Tait SW, Parsons MJ, Llambi F, Bouchier-Hayes L, Connell S, Munoz-Pinedo C, et al. Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev Cell. 2010;18(5):802-13.
39. Weaver D, Eisner V, Liu X, Varnai P, Hunyady L, Gross A, et al. Distribution and apoptotic function of outer membrane proteins depend on mitochondrial fusion. Mol Cell. 2014;54(5):870-8.
40. Ray R, Chen G, Vande Velde C, Cizeau J, Park JH, Reed JC, et al. BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J Biol Chem. 2000;275(2):1439-48.
41. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 1998;94(4):491-501.
42. Kirkland RA, Windelborn JA, Kasprzak JM, Franklin JL. A Bax-induced pro-oxidant state is critical for cytochrome c release during programmed neuronal death. J Neurosci. 2002;22(15):6480-90.
43. Kubli DA, Quinsay MN, Huang C, Lee Y, Gustafsson AB. Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion. Am J Physiol Heart Circ Physiol. 2008;295(5):H2025-2031.
44. Zong WX, Lindsten T, Ross AJ, MacGregor GR, Thompson CB. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 2001;15(12):1481-6.
45. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008;27(2):433-46.
46. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, et al. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 2007;14(1):146-57.
47. Gomes LC, Di Benedetto G, Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol. 2011;13(5):589-98.
48. Holmstrom KM, Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol. 2014;15(6):411-21.
49. Hamacher-Brady A, Brady NR, Gottlieb RA, Gustafsson AB. Autophagy as a protective response to Bnip3-mediated apoptotic signaling in the heart. Autophagy. 2006;2(4):307-9.
50. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science. 2011;333(6039):228-33.
51. Mizushima N. Autophagy: process and function. Genes Dev. 2007;21(22):2861-73.
52. Kwon KY, Viollet B, Yoo OJ. CCCP induces autophagy in an AMPK-independent manner. Biochem Biophys Res Commun. 2011;416(3-4):343-8.
53. Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol. 2001;11(21):1680-5.
54. Aerbajinai W, Giattina M, Lee YT, Raffeld M, Miller JL. The proapoptotic factor Nix is coexpressed with Bcl-xL during terminal erythroid differentiation. Blood. 2003;102(2):712-7.
55. Wang Y, Nartiss Y, Steipe B, McQuibban GA, Kim PK. ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy. 2012;8(10):1462-76.
56. Hamacher-Brady A, Stein HA, Turschner S, Toegel I, Mora R, Jennewein N, et al. Artesunate activates mitochondrial apoptosis in breast cancer cells via iron-catalyzed lysosomal reactive oxygen species production. J Biol Chem. 2011;286(8):6587-601.
57. Wu W, Tian W, Hu Z, Chen G, Huang L, Li W, et al. ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. EMBO Rep. 2014;15(5):566-75.
58. Wu H, Xue D, Chen G, Han Z, Huang L, Zhu C, et al. The BCL2L1 and PGAM5 axis defines hypoxia-induced receptor-mediated mitophagy. Autophagy. 2014;10(10):1712-25.
59. Wang X, Winter D, Ashrafi G, Schlehe J, Wong YL, Selkoe D, et al. PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell. 2011;147(4):893-906.
60. Song M, Gong G, Burelle Y, Gustafsson AB, Kitsis RN, Matkovich SJ, Dorn GW, 2nd. Interdependence of Parkin-Mediated Mitophagy and Mitochondrial Fission in Adult Mouse Hearts. Cir Res. 2015.
61. Hollville E, Carroll RG, Cullen SP, Martin SJ. Bcl-2 family proteins participate in mitochondrial quality control by regulating Parkin/PINK1-dependent mitophagy. Mol Cell. 2014;55(3):451-66.
62. Carroll RG, Hollville E, Martin SJ. Parkin sensitizes toward apoptosis induced by mitochondrial depolarization through promoting degradation of Mcl-1. Cell Rep. 2014;9(4):1538-53.
63. Johnson BN, Berger AK, Cortese GP, Lavoie MJ. The ubiquitin E3 ligase parkin regulates the proapoptotic function of Bax. Proc Natl Acad Sci U S A. 2012;109(16):6283-8.
64. Itakura E, Kishi-Itakura C, Koyama-Honda I, Mizushima N. Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J Cell Sci. 2012;125(Pt 6):1488-99.
65. Borlin CS, Lang V, Hamacher-Brady A, Brady NR. Agent-based modeling of autophagy reveals emergent regulatory behavior of spatio-temporal autophagy dynamics. Cell Commun Signal. 2014;12(1):56.
66. Mazure NM, Pouyssegur J. Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia. Autophagy. 2009;5(6):868-9.
67. Li Y, Wang Y, Kim E, Beemiller P, Wang CY, Swanson J, et al. Bnip3 mediates the hypoxia-induced inhibition on mammalian target of rapamycin by interacting with Rheb. J Biol Chem. 2007;282(49):35803-13.
68. Gama V, Swahari V, Schafer J, Kole AJ, Evans A, Huang Y, et al. The E3 ligase PARC mediates the degradation of cytosolic cytochrome c to promote survival in neurons and cancer cells. Sci Signal. 2014;7(334):ra67.
69. Hamacher-Brady A, Choe SC, Krijnse-Locker J, Brady NR. Intramitochondrial recruitment of endolysosomes mediates Smac degradation and constitutes a novel intrinsic apoptosis antagonizing function of XIAP E3 ligase. Cell Death Differ. 2014;21(12):1862-76.
70. Colell A, Ricci JE, Tait S, Milasta S, Maurer U, Bouchier-Hayes L, et al. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell. 2007;129(5):983-97.
71. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol. 2007;8(9):741-52.
72. Lee Y, Lee HY, Hanna RA, Gustafsson AB. Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes. Am J Physiol Heart Circ Physiol. 2011;301(5):H1924-1931.