Bax Activation Initiates the Assembly of a Multimeric Catalyst that Facilitates Bax Pore Formation in Mitochondrial Outer Membranes

PLoS Biology

Volumn 10, Issue 9, 2012, Pages

  Kushnareva, Yulia ^a   Andreyev, Alexander Y ^b   Kuwana, Tomomi ^a   Newmeyer, Donald D ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL PROTEIN; GUANOSINE TRIPHOSPHATE; OUTER MEMBRANE PROTEIN; PROTEIN BAX; PROTEIN BID; PROTEIN DRP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CHANNEL GATING; CONTROLLED STUDY; MALE; MITOCHONDRIAL MEMBRANE; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PROTEIN ASSEMBLY; PROTEIN FUNCTION; RAT; THERMODYNAMICS;

ANIMALS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; BIOCATALYSIS; DYNAMIN I; HUMANS; KINETICS; LIPOSOMES; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MODELS, BIOLOGICAL; PERMEABILITY; PROTEIN MULTIMERIZATION; QUINAZOLINONES; RATS; RATS, SPRAGUE-DAWLEY; THERMODYNAMICS;

MAMMALIA;

EID: 84866650630     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001394     Document Type: Article

References (87)

1. Newmeyer DD, Farschon DM, Reed JC, (1994) Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79: 353-364.
2. Bouchier-Hayes L, Lartigue L, Newmeyer DD, (2005) Mitochondria: pharmacological manipulation of cell death. J Clin Invest 115: 2640-2647.
3. Newmeyer DD, Ferguson-Miller S, (2003) Mitochondria. Releasing power for life and unleashing the machineries of death. Cell 112: 481-490.
4. Tait SW, Parsons MJ, Llambi F, Bouchier-Hayes L, Connell S, et al. (2010) Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev Cell 18: 802-813.
5. Antonsson B, Montessuit S, Sanchez B, Martinou JC, (2001) Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276: 11615-11623.
6. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, et al. (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139: 1281-1292.
7. Hsu YT, Youle RJ, (1997) Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 272: 13829-13834.
8. Hsu YT, Wolter KG, Youle RJ, (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci U S A 94: 3668-3672.
9. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, et al. (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111: 331-342.
10. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, et al. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.
11. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, et al. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
12. Griffiths GJ, Dubrez L, Morgan CP, Jones NA, Whitehouse J, et al. (1999) Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J Cell Biol 144: 903-914.
13. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, et al. (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2,-3,-6,-7,-8, and-10 in a caspase-9-dependent manner. J Cell Biol 144: 281-292.
14. Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, et al. (2002) Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell 9: 423-432.
15. Lavrik IN, Golks A, Krammer PH, (2005) Caspases: pharmacological manipulation of cell death. J Clin Invest 115: 2665-2672.
16. Liu X, Kim CN, Yang J, Jemmerson R, Wang X, (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157.
17. Nicholson DW, (1999) Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 6: 1028-1042.
18. Taylor RC, Brumatti G, Ito S, Hengartner MO, Derry WB, et al. (2007) Establishing a blueprint for CED-3-dependent killing through identification of multiple substrates for this protease. J Biol Chem 282: 15011-15021.
19. Lartigue L, Kushnareva Y, Seong Y, Lin H, Faustin B, et al. (2009) Caspase-independent mitochondrial cell death results from loss of respiration, not cytotoxic protein release. Mol Biol Cell 20: 4871-4884.
20. Colell A, Ricci JE, Tait S, Milasta S, Maurer U, et al. (2007) GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell 129: 983-997.
21. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, et al. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17: 525-535.
22. Estaquier J, Arnoult D, (2007) Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ 14: 1086-1094.
23. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, et al. (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126: 177-189.
24. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, et al. (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67.
25. Yamaguchi R, Lartigue L, Perkins G, Scott RT, Dixit A, et al. (2008) Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol Cell 31: 557-569.
26. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, et al. (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135: 1074-1084.
27. Terrones O, Antonsson B, Yamaguchi H, Wang HG, Liu J, et al. (2004) Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J Biol Chem 279: 30081-30091.
28. Schafer B, Quispe J, Choudhary V, Chipuk JE, Ajero TG, et al. (2009) Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation. Mol Biol Cell 20: 2276-2285.
29. Zaltsman Y, Shachnai L, Yivgi-Ohana N, Schwarz M, Maryanovich M, et al. (2010) MTCH2/MIMP is a major facilitator of tBID recruitment to mitochondria. Nat Cell Biol 12: 553-562.
30. Montessuit S, Somasekharan SP, Terrones O, Lucken-Ardjomande S, Herzig S, et al. (2010) Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142: 889-901.
31. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, et al. (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 14: 193-204.
32. Brustovetsky N, Dubinsky JM, Antonsson B, Jemmerson R, (2003) Two pathways for tBID-induced cytochrome c release from rat brain mitochondria: BAK- versus BAX-dependence. J Neurochem 84: 196-207.
33. Terrones O, Etxebarria A, Landajuela A, Landeta O, Antonsson B, et al. (2008) BIM and tBID are not mechanistically equivalent when assisting BAX to permeabilize bilayer membranes. J Biol Chem 283: 7790-7803.
34. Polster BM, Kinnally KW, Fiskum G, (2001) BH3 death domain peptide induces cell type-selective mitochondrial outer membrane permeability. J Biol Chem 276: 37887-37894.
35. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ, (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301: 513-517.
36. Csordas G, Renken C, Varnai P, Walter L, Weaver D, et al. (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174: 915-921.
37. Billen LP, Kokoski CL, Lovell JF, Leber B, Andrews DW, (2008) Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol 6: e147 doi:10.1371/journal.pbio.0060147.
38. Epand RF, Martinou JC, Montessuit S, Epand RM, (2002) Membrane perturbations induced by the apoptotic Bax protein. Biochem J 367: 849-855.
39. Saito M, Korsmeyer SJ, Schlesinger PH, (2000) BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat Cell Biol 2: 553-555.
40. Kluck RM, Esposti MD, Perkins G, Renken C, Kuwana T, et al. (1999) The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J Cell Biol 147: 809-822.
41. Wojtczak L, Zaluska H, Wroniszewska A, Wojtczak AB, (1972) Assay for the intactness of the outer membrane in isolated mitochondria. Acta Biochim Pol 19: 227-234.
42. Kushnareva Y, Newmeyer DD, (2010) Bioenergetics and cell death. Ann N Y Acad Sci 1201: 50-57.
43. Lemeshko VV, (2002) Cytochrome c sorption-desorption effects on the external NADH oxidation by mitochondria: experimental and computational study. J Biol Chem 277: 17751-17757.
44. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681.
45. Du H, Wolf J, Schafer B, Moldoveanu T, Chipuk JE, et al. (2011) BH3 domains other than Bim and Bid can directly activate Bax/Bak. J Biol Chem 286: 491-501.
46. Edlich F, Banerjee S, Suzuki M, Cleland MM, Arnoult D, et al. (2011) Bcl-x(L) retrotranslocates Bax from the mitochondria into the cytosol. Cell 145: 104-116.
47. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, et al. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17: 525-535.
48. Leber B, Lin J, Andrews DW, (2007) Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 12: 897-911.
49. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, et al. (2011) A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 44: 517-531.
50. Walensky LD, Pitter K, Morash J, Oh KJ, Barbuto S, et al. (2006) A stapled BID BH3 helix directly binds and activates BAX. Mol Cell 24: 199-210.
51. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, et al. (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315: 856-859.
52. Perez D, White E, (2000) TNF-alpha signals apoptosis through a bid-dependent conformational change in Bax that is inhibited by E1B 19K. Mol Cell 6: 53-63.
53. Eskes R, Desagher S, Antonsson B, Martinou JC, (2000) Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20: 929-935.
54. Bleicken S, Classen M, Padmavathi PV, Ishikawa T, Zeth K, et al. (2010) Molecular details of Bax activation, oligomerization, and membrane insertion. J Biol Chem 285: 6636-6647.
55. Ren D, Tu HC, Kim H, Wang GX, Bean GR, et al. (2010) BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 330: 1390-1393.
56. Ott M, Norberg E, Walter KM, Schreiner P, Kemper C, et al. (2007) The mitochondrial TOM complex is required for tBid/Bax-induced cytochrome c release. J Biol Chem 282: 27633-27639.
57. Bellot G, Cartron PF, Er E, Oliver L, Juin P, et al. (2007) TOM22, a core component of the mitochondria outer membrane protein translocation pore, is a mitochondrial receptor for the proapoptotic protein Bax. Cell Death Differ 14: 785-794.
58. Etxebarria A, Terrones O, Yamaguchi H, Landajuela A, Landeta O, et al. (2009) Endophilin B1/Bif-1 stimulates BAX activation independently from its capacity to produce large scale membrane morphological rearrangements. J Biol Chem 284: 4200-4212.
59. Roucou X, Montessuit S, Antonsson B, Martinou JC, (2002) Bax oligomerization in mitochondrial membranes requires tBid (caspase-8-cleaved Bid) and a mitochondrial protein. Biochem J 368: 915-921.
60. Lepock JR, Frey HE, Ritchie KP, (1993) Protein denaturation in intact hepatocytes and isolated cellular organelles during heat shock. J Cell Biol 122: 1267-1276.
61. Pagliari LJ, Kuwana T, Bonzon C, Newmeyer DD, Tu S, et al. (2005) The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc Natl Acad Sci U S A 102: 17975-17980.
62. Parone PA, James DI, Da Cruz S, Mattenberger Y, Donze O, et al. (2006) Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol Cell Biol 26: 7397-7408.
63. Sheridan C, Martin SJ, (2010) Mitochondrial fission/fusion dynamics and apoptosis. Mitochondrion 10: 640-648.
64. Sheridan C, Delivani P, Cullen SP, Martin SJ, (2008) Bax- or Bak-induced mitochondrial fission can be uncoupled from cytochrome C release. Mol Cell 31: 570-585.
65. Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ, (2004) Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell 15: 5001-5011.
66. Costa V, Giacomello M, Hudec R, Lopreiato R, Ermak G, et al. (2010) Mitochondrial fission and cristae disruption increase the response of cell models of Huntington's disease to apoptotic stimuli. EMBO Mol Med 2: 490-503.
67. Chang CR, Manlandro CM, Arnoult D, Stadler J, Posey AE, et al. (2010) A lethal de novo mutation in the middle domain of the dynamin-related GTPase Drp1 impairs higher order assembly and mitochondrial division. J Biol Chem 285: 32494-32503.
68. Smirnova E, Griparic L, Shurland DL, van der Bliek AM, (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 12: 2245-2256.
69. Zhou HX, (2009) Crowding effects of membrane proteins. J Phys Chem B 113: 7995-8005.
70. Martinez-Caballero S, Dejean LM, Kinnally MS, Oh KJ, Mannella CA, et al. (2009) Assembly of the mitochondrial apoptosis-induced channel, MAC. J Biol Chem 284: 12235-12245.
71. Lin SH, Perera MN, Nguyen T, Datskovskiy D, Miles M, et al. (2011) Bax forms two types of channels, one of which is voltage-gated. Biophys J 101: 2163-2169.
72. Qian S, Wang W, Yang L, Huang HW, (2008) Structure of transmembrane pore induced by Bax-derived peptide: evidence for lipidic pores. Proc Natl Acad Sci U S A 105: 17379-17383.
73. Garcia-Saez AJ, Coraiola M, Dalla Serra M, Mingarro I, Menestrina G, et al. (2005) Peptides derived from apoptotic Bax and Bid reproduce the poration activity of the parent full-length proteins. Biophys J 88: 3976-3990.
74. Basanez G, Nechushtan A, Drozhinin O, Chanturiya A, Choe E, et al. (1999) Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad Sci U S A 96: 5492-5497.
75. Zhou L, Chang DC, (2008) Dynamics and structure of the Bax-Bak complex responsible for releasing mitochondrial proteins during apoptosis. J Cell Sci 121: 2186-2196.
76. Lucken-Ardjomande S, Martinou JC, (2005) Newcomers in the process of mitochondrial permeabilization. J Cell Sci 118: 473-483.
77. McMahon HT, Kozlov MM, Martens S, (2010) Membrane curvature in synaptic vesicle fusion and beyond. Cell 140: 601-605.
78. Campelo F, Fabrikant G, McMahon HT, Kozlov MM, (2010) Modeling membrane shaping by proteins: focus on EHD2 and N-BAR domains. FEBS Lett 584: 1830-1839.
79. Rostovtseva TK, Boukari H, Antignani A, Shiu B, Banerjee S, et al. (2009) Bax activates endophilin B1 oligomerization and lipid membrane vesiculation. J Biol Chem 284: 34390-34399.
80. Lapidus RG, Sokolove PM, (1993) Spermine inhibition of the permeability transition of isolated rat liver mitochondria: an investigation of mechanism. Arch Biochem Biophys 306: 246-253.
81. Andreyev AY, Shen Z, Guan Z, Ryan A, Fahy E, et al. (2009) Application of proteomic marker ensembles to subcellular organelle identification. Mol Cell Proteomics.
82. von Ahsen O, Renken C, Perkins G, Kluck RM, Bossy-Wetzel E, et al. (2000) Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release. J Cell Biol 150: 1027-1036.
83. Suzuki M, Youle RJ, Tjandra N, (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103: 645-654.
84. Luciano F, Jacquel A, Colosetti P, Herrant M, Cagnol S, et al. (2003) Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22: 6785-6793.
85. Ivanova PT, Milne SB, Byrne MO, Xiang Y, Brown HA, (2007) Glycerophospholipid identification and quantitation by electrospray ionization mass spectrometry. Methods Enzymol 432: 21-57.
86. Ricchelli F, Gobbo S, Moreno G, Salet C, (1999) Changes of the fluidity of mitochondrial membranes induced by the permeability transition. Biochemistry 38: 9295-9300.
87. Arrigoni O, Singer TP, (1962) Limitations of the phenazine methosulphate assay for succinic and related dehydrogenases. Nature 193: 1256-1258.