BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis

Science

Volumn 359, Issue 6378, 2018, Pages

  McArthur, Kate ^a,b,c   Whitehead, Lachlan W ^a,b   Heddleston, John M ^d   Li, Lucy ^a   Padman, Benjamin S ^c   Oorschot, Viola ^c   Geoghegan, Niall D ^a,b   Chappaz, Stephane ^a,b,c   Davidson, Sophia ^a   Chin, Hui San ^a   Lane, Rachael M ^c   Dramicanin, Marija ^a,b   Saunders, Tahnee L ^c   Sugiana, Canny ^c   Lessene, Romina ^a,b   Osellame, Laura D ^c   Chew, Teng Leong ^d   Dewson, Grant ^a,b   Lazarou, Michael ^c   Ramm, Georg ^c   Lessene, Guillaume ^a,b   Ryan, Michael T ^c   Rogers, Kelly L ^a,b   Van Delft, Mark F ^a,b   Kile, Benjamin T ^a,b,c   more..

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CASPASE 3; CASPASE 7; CASPASE 9; CYTOCHROME C; INTERFERON; MITOCHONDRIAL DNA; PROTEIN BAK; PROTEIN BAX; BAK1 PROTEIN, MOUSE; BAX PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM BLOOD LEVEL; CELL DEATH; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; INFLAMMATORY DISEASE; INNATE IMMUNITY; INNER MEMBRANE; INTERFERON PRODUCTION; MITOCHONDRION; MOUSE; NECROPTOSIS; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PRIORITY JOURNAL; PYROPTOSIS; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; C57BL MOUSE; CHEMISTRY; FIBROBLAST; GENE KNOCKOUT; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE; PROTEIN MULTIMERIZATION;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CYTOCHROMES C; DNA, MITOCHONDRIAL; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; HELA CELLS; HUMANS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PROTEIN MULTIMERIZATION;

EID: 85042279507     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aao6047     Document Type: Article

References (81)

1. R. J. Youle, A. Strasser, The BCL-2 protein family: Opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59 (2008). doi: 10.1038/nrm2308; pmid: 18097445
2. P. E. Czabotar, G. Lessene, A. Strasser, J. M. Adams, Control of apoptosis by the BCL-2 protein family: Implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15, 49-63 (2014). doi: 10.1038/nrm3722; pmid: 24355989
3. R. M. Kluck, E. Bossy-Wetzel, D. R. Green, D. D. Newmeyer, The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136 (1997). doi: 10.1126/science.275.5303.1132; pmid: 9027315
4. J. Yang et al., Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 275, 1129-1132 (1997). doi: 10.1126/science.275.5303.1129; pmid: 9027314
5. O. Julien, J. A. Wells, Caspases and their substrates. Cell Death Differ. 24, 1380-1389 (2017). doi: 10.1038/cdd.2017.44; pmid: 28498362
6. M. J. White et al., Apoptotic caspases suppress mtDNAinduced STING-mediated type I IFN production. Cell 159, 1549-1562 (2014). doi: 10.1016/j.cell.2014.11.036; pmid: 25525874
7. A. Rongvaux et al., Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 159, 1563-1577 (2014). doi: 10.1016/j.cell.2014.11.037; pmid: 25525875
8. M. Patrushev et al., Mitochondrial permeability transition triggers the release of mtDNA fragments. Cell. Mol. Life Sci. 61, 3100-3103 (2004). doi: 10.1007/s00018-004-4424-1; pmid: 15583871
9. M. Patrushev et al., Release of mitochondrial DNA fragments from brain mitochondria of irradiated mice. Mitochondrion 6, 43-47 (2006). doi: 10.1016/j.mito.2005.12.001; pmid: 16413832
10. A. P. West et al., Mitochondrial DNA stress primes the antiviral innate immune response. Nature 520, 553-557 (2015). doi: 10.1038/nature14156; pmid: 25642965
11. K. Shimada et al., Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 36, 401-414 (2012). doi: 10.1016/j.immuni.2012.01.009; pmid: 22342844
12. T.-D. Kanneganti, M. Kundu, D. R. Green, Innate immune recognition of mtDNA-an undercover signal? Cell Metab. 21, 793-794 (2015). doi: 10.1016/j.cmet.2015.05.019; pmid: 26039443
13. A. P. West, G. S. Shadel, Mitochondrial DNA in innate immune responses and inflammatory pathology. Nat. Rev. Immunol. 17, 363-375 (2017). doi: 10.1038/nri.2017.21; pmid: 28393922
14. B.-C. Chen et al., Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution. Science 346, 1257998-1257998 (2014). doi: 10.1126/science.1257998; pmid: 25342811
15. T. Oltersdorf et al., An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681 (2005). doi: 10.1038/nature03579; pmid: 15902208
16. M. F. van Delft et al., The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399 (2006). doi: 10.1016/j.ccr.2006.08.027; pmid: 17097561
17. J. B. Grimm et al., A general method to improve fluorophores for live-cell and single-molecule microscopy. Nat. Methods 12, 244-250 (2015). doi: 10.1016/j.ccr.2006.08.027; pmid: 17097561
18. N. C. Shaner et al., A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum. Nat. Methods 10, 407-409 (2013). doi: 10.1038/nmeth.2413; pmid: 23524392
19. T. M. Caserta, A. N. Smith, A. D. Gultice, M. A. Reedy, T. L. Brown, Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis 8, 345-352 (2003). doi: 10.1023/A:1024116916932; pmid: 12815277
20. A. Kotschy et al., The MCL1 inhibitor S63845 is tolerable and effective in diverse cancer models. Nature 538, 477-482 (2016). doi: 10.1038/nature19830; pmid: 27760111
21. N. Ashley, D. Harris, J. Poulton, Detection of mitochondrial DNA depletion in living human cells using PicoGreen staining. Exp. Cell Res. 303, 432-446 (2005). doi: 10.1016/j.yexcr.2004.10.013; pmid: 15652355
22. P. D. Bhola, A. L. Mattheyses, S. M. Simon, Spatial and temporal dynamics of mitochondrial membrane permeability waves during apoptosis. Biophys. J. 97, 2222-2231 (2009). doi: 10.1016/j.bpj.2009.07.056; pmid: 19843454
23. M. Rehm et al., Dynamics of outer mitochondrial membrane permeabilization during apoptosis. Cell Death Differ. 16, 613-623 (2009). doi: 10.1038/cdd.2008.187; pmid: 19136937
24. M. Rehm, H. Düssmann, J. H. M. Prehn, Real-time single cell analysis of Smac/DIABLO release during apoptosis. J. Cell Biol. 162, 1031-1043 (2003). doi: 10.1083/jcb.200303123; pmid: 12975347
25. J. C. Goldstein, N. J. Waterhouse, P. Juin, G. I. Evan, D. R. Green, The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2, 156-162 (2000). doi: 10.1038/35004029; pmid: 10707086
26. L. Lartigue et al., An intracellular wave of cytochrome c propagates and precedes Bax redistribution during apoptosis. J. Cell Sci. 121, 3515-3523 (2008). doi: 10.1242/jcs.029587; pmid: 18840646
27. J. Schindelin et al., Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012). doi: 10.1038/nmeth.2019; pmid: 22743772
28. B. Westermann, Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 11, 872-884 (2010). doi: 10.1038/nrm3013; pmid: 21102612
29. R. J. Youle, A. M. van der Bliek, Mitochondrial fission, fusion, and stress. Science 337, 1062-1065 (2012). doi: 10.1126/science.1219855; pmid: 22936770
30. L. Pernas, L. Scorrano, Mito-morphosis: Mitochondrial fusion, fission, and cristae remodeling as key mediators of cellular function. Annu. Rev. Physiol. 78, 505-531 (2016). doi: 10.1146/annurev-physiol-021115-105011; pmid: 26667075
31. J. R. Friedman, J. Nunnari, Mitochondrial form and function. Nature 505, 335-343 (2014). doi: 10.1038/nature12985; pmid: 24429632
32. E. Smirnova, L. Griparic, D. L. Shurland, A. M. van der Bliek, Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256 (2001). doi: 10.1091/mbc.12.8.2245; pmid: 11514614
33. J. Prudent, H. M. McBride, Mitochondrial dynamics: ER actin tightens the Drp1 noose. Curr. Biol. 26, R207-R209 (2016). doi: 10.1016/j.cub.2016.01.009; pmid: 26954442
34. N. Ishihara, Y. Eura, K. Mihara, Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J. Cell Sci. 117, 6535-6546 (2004). doi: 10.1242/jcs.01565; pmid: 15572413
35. S. Cipolat, O. Martins de Brito, B. Dal Zilio, L. Scorrano, OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. U.S.A. 101, 15927-15932 (2004). doi: 10.1073/pnas.0407043101; pmid: 15509649
36. I. Martinou et al., The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Cell Biol. 144, 883-889 (1999). doi: 10.1083/jcb.144.5.883; pmid: 10085288
37. S. Frank et al., The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525 (2001). doi: 10.1016/S1534-5807(01)00055-7; pmid: 11703942
38. M. Karbowski et al., Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J. Cell Biol. 164, 493-499 (2004). doi: 10.1083/jcb.200309082; pmid: 14769861
39. C. Sheridan, P. Delivani, S. P. Cullen, S. J. Martin, Bax- or Bak-induced mitochondrial fission can be uncoupled from cytochrome C release. Mol. Cell 31, 570-585 (2008). doi: 10.1016/j.molcel.2008.08.002; pmid: 18722181
40. M. Karbowski et al., Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159, 931-938 (2002). doi: 10.1083/jcb.200209124; pmid: 12499352
41. S. Wasiak, R. Zunino, H. M. McBride, Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177, 439-450 (2007). doi: 10.1083/jcb.200610042; pmid: 17470634
42. S. Montessuit et al., Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142, 889-901 (2010). doi: 10.1016/j.cell.2010.08.017; pmid: 20850011
43. H. Otera, N. Miyata, O. Kuge, K. Mihara, Drp1-dependent mitochondrial fission via MiD49/51 is essential for apoptotic cristae remodeling. J. Cell Biol. 212, 531-544 (2016). doi: 10.1083/jcb.201508099; pmid: 26903540
44. D.-F. Suen, K. L. Norris, R. J. Youle, Mitochondrial dynamics and apoptosis. Genes Dev. 22, 1577-1590 (2008). doi: 10.1101/gad.1658508; pmid: 18559474
45. J. C. Martinou, R. J. Youle, Which came first, the cytochrome c release or the mitochondrial fission? Cell Death Differ. 13, 1291-1295 (2006). doi: 10.1038/sj.cdd.4401985; pmid: 16763618
46. L. A. Gillies, T. Kuwana, Apoptosis regulation at the mitochondrial outer membrane. J. Cell. Biochem. 115, 632-640 (2014). doi: 10.1002/jcb.24709; pmid: 24453042
47. B. Oettinghaus et al., DRP1-dependent apoptotic mitochondrial fission occurs independently of BAX, BAK and APAF1 to amplify cell death by BID and oxidative stress. Biochim. Biophys. Acta 1857, 1267-1276 (2016). doi: 10.1016/j.bbabio.2016.03.016; pmid: 26997499
48. A. Olichon et al., Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278, 7743-7746 (2003). doi: 10.1074/jbc.C200677200; pmid: 12509422
49. R. Sugioka, S. Shimizu, Y. Tsujimoto, Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J. Biol. Chem. 279, 52726-52734 (2004). doi: 10.1074/jbc.M408910200; pmid: 15459195
50. D. Arnoult, A. Grodet, Y.-J. Lee, J. Estaquier, C. Blackstone, Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J. Biol. Chem. 280, 35742-35750 (2005). doi: 10.1074/jbc.M505970200; pmid: 16115883
51. N. Ishihara et al., Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol. 11, 958-966 (2009). doi: 10.1038/ncb1907; pmid: 19578372
52. J. Wakabayashi et al., The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J. Cell Biol. 186, 805-816 (2009). doi: 10.1083/jcb.200903065; pmid: 19752021
53. C. P. Baines et al., Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662 (2005). doi: 10.1038/nature03434; pmid: 15800627
54. V. Petronilli, A. Nicolli, P. Costantini, R. Colonna, P. Bernardi, Regulation of the permeability transition pore, a voltagedependent mitochondrial channel inhibited by cyclosporin A. Biochim. Biophys. Acta 1187, 255-259 (1994). doi: 10.1016/0005-2728(94)90122-8; pmid: 7521212
55. K. G. Wolter et al., Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139, 1281-1292 (1997). doi: 10.1083/jcb.139.5.1281; pmid: 9382873
56. A. Nechushtan, C. L. Smith, I. Lamensdorf, S. H. Yoon, R. J. Youle, Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J. Cell Biol. 153, 1265-1276 (2001). doi: 10.1083/jcb.153.6.1265; pmid: 11402069
57. S. S. Smaili, Y. T. Hsu, K. M. Sanders, J. T. Russell, R. J. Youle, Bax translocation to mitochondria subsequent to a rapid loss of mitochondrial membrane potential. Cell Death Differ. 8, 909-920 (2001). doi: 10.1038/sj.cdd.4400889; pmid: 11526446
58. G. Dewson, R. M. Kluck, Mechanisms by which Bak and Bax permeabilise mitochondria during apoptosis. J. Cell Sci. 122, 2801-2808 (2009). doi: 10.1242/jcs.038166; pmid: 19795525
59. S. W. G. Tait, D. R. Green, Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11, 621-632 (2010). doi: 10.15252/embj.201592789; pmid: 26783364
60. L. Große et al., Bax assembles into large ring-like structures remodeling the mitochondrial outer membrane in apoptosis. EMBO J. 35, 402-413 (2016). doi: 10.15252/embj.201592789; pmid: 26783364
61. R. Salvador-Gallego et al., Bax assembly into rings and arcs in apoptotic mitochondria is linked to membrane pores. EMBO J. 35, 389-401 (2016). doi: 10.15252/embj.201593384; pmid: 26783362
62. H. Düssmann et al., Single-cell quantification of Bax activation and mathematical modelling suggest pore formation on minimal mitochondrial Bax accumulation. Cell Death Differ. 17, 278-290 (2010). doi: 10.1038/cdd.2009.123; pmid: 19745831
63. D. A. Stroud et al., Accessory subunits are integral for assembly and function of human mitochondrial complex I. Nature 538, 123-126 (2016). doi: 10.1038/nature19754; pmid: 27626371
64. L. Andreeva et al., cGAS senses long and HMGB/TFAM-bound U-turn DNA by forming protein-DNA ladders. Nature 549, 394-398 (2017). doi: 10.1038/nature23890; pmid: 28902841
65. R. J. Youle, M. Karbowski, Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6, 657-663 (2005). doi: 10.1038/nrm1697; pmid: 16025099
66. P. A. Parone et al., Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol. Cell. Biol. 26, 7397-7408 (2006). doi: 10.1128/MCB.02282-05; pmid: 17015472
67. J. R. Friedman et al., ER tubules mark sites of mitochondrial division. Science 334, 358-362 (2011). doi: 10.1126/science.1207385; pmid: 21885730
68. S. C. Lewis, L. F. Uchiyama, J. Nunnari, ER-mitochondria contacts couple mtDNA synthesis with mitochondrial division in human cells. Science 353, aaf5549 (2016). doi: 10.1126/science.aaf5549; pmid: 27418514
69. R. K. Boyapati, A. Tamborska, D. A. Dorward, G.-T. Ho, Advances in the understanding of mitochondrial DNA as a pathogenic factor in inflammatory diseases. F1000 Res. 6, 169 (2017). doi: 10.12688/f1000research.10397.1; pmid: 28299196
70. S. Aguirre et al., Dengue virus NS2B protein targets cGAS for degradation and prevents mitochondrial DNA sensing during infection. Nat. Microbiol. 2, 17037 (2017). doi: 10.1038/nmicrobiol.2017.37; pmid: 28346446
71. A. Sugiura, G.-L. McLelland, E. A. Fon, H. M. McBride, A new pathway for mitochondrial quality control: Mitochondrial-derived vesicles. EMBO J. 33, 2142-2156 (2014). doi: 10.15252/embj.201488104; pmid: 25107473
72. F. A. Ran et al., Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013). doi: 10.1038/nprot.2013.143; pmid: 24157548
73. M. Raab et al., ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352, 359-362 (2016). doi: 10.1126/science.aad7611; pmid: 27013426
74. A. J. Lam et al., Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012 (2012). doi: 10.1038/nmeth.2171; pmid: 22961245
75. D. S. Bindels et al., mScarlet: A bright monomeric red fluorescent protein for cellular imaging. Nat. Methods 14, 53-56 (2017). doi: 10.1038/nmeth.4074; pmid: 27869816
76. R. Fiolka, L. Shao, E. H. Rego, M. W. Davidson, M. G. L. Gustafsson, Time-lapse two-color 3D imaging of live cells with doubled resolution using structured illumination. Proc. Natl. Acad. Sci. U.S.A. 109, 5311-5315 (2012). doi: 10.1073/pnas.1119262109; pmid: 22431626
77. G. Ball et al., SIMcheck: A toolbox for successful superresolution structured illumination microscopy. Sci. Rep. 5, 15915 (2015). doi: 10.1038/srep15915; pmid: 26525406
78. J. W. Slot, H. J. Geuze, Cryosectioning and immunolabeling. Nat. Protoc. 2, 2480-2491 (2007). doi: 10.1038/nprot.2007.365; pmid: 17947990
79. B. S. Padman, M. Bach, G. Ramm, An improved procedure for subcellular spatial alignment during live-cell CLEM. PLOS ONE 9, e95967 (2014). doi: 10.1371/journal.pone.0095967; pmid: 24755651
80. S. Preibisch, S. Saalfeld, P. Tomancak, Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25, 1463-1465 (2009). doi: 10.1093/bioinformatics/btp184; pmid: 19346324
81. V. Kaynig, B. Fischer, E. Müller, J. M. Buhmann, Fully automatic stitching and distortion correction of transmission electron microscope images. J. Struct. Biol. 171, 163-173 (2010). doi: 10.1016/j.jsb.2010.04.012; pmid: 20450977