Bax assembles into large ring-like structures remodeling the mitochondrial outer membrane in apoptosis

EMBO Journal

Volumn 35, Issue 4, 2016, Pages 402-413

  Große, Lena ^a,b   Wurm, Christian A ^b   Brüser, Christian ^b   Neumann, Daniel ^b   Jans, Daniel C ^a,b   Jakobs, Stefan ^a,b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Bcl 2; cell death; membrane curvature; MICOS; superresolution microscopy

Indexed keywords

CYTOCHROME C; DRP 1 PROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN BAK; PROTEIN BAX; SAM 50 PROTEIN; TOM 20 PROTEIN; TOM 22 PROTEIN; UNCLASSIFIED DRUG; BAX PROTEIN, HUMAN; PORE FORMING CYTOTOXIC PROTEIN;

APOPTOSIS; ARTICLE; CELL PERMEABILIZATION; CLINICAL ASSESSMENT; CLINICAL EVALUATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MEMBRANE PERMEABILITY; MITOCHONDRIAL OUTER MEMBRANE PERMEABILIZATION; MITOCHONDRION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; SUPER RESOLUTION MICROSCOPY; CELL LINE; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; METABOLISM; MITOCHONDRIAL MEMBRANE; PERMEABILITY; PHYSIOLOGY; PROTEIN MULTIMERIZATION;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CYTOCHROMES C; HUMANS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PERMEABILITY; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN MULTIMERIZATION;

EID: 84958604397     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592789     Document Type: Article

References (53)

1. Alkhaja AK, Jans DC, Nikolov M, Vukotic M, Lytovchenko O, Ludewig F, Schliebs W, Riedel D, Urlaub H, Jakobs S, Deckers M, (2012) MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol Biol Cell 23: 247-257
2. Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I, Bernasconi L, Bernard A, Mermod JJ, Mazzei G, Maundrell K, Gambale F, Sadoul R, Martinou JC, (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277: 370-372
3. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD, (2007) Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 9: 550-555
4. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, Craessaerts K, Metzger K, Frezza C, Annaert W, D'Adamio L, Derks C, Dejaegere T, Pellegrini L, D'Hooge R, Scorrano L, De Strooper B, (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126: 163-175
5. Edlich F, Banerjee S, Suzuki M, Cleland MM, Arnoult D, Wang C, Neutzner A, Tjandra N, Youle RJ, (2011) Bcl-x(L) retrotranslocates Bax from the mitochondria into the cytosol. Cell 145: 104-116
6. 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
7. 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
8. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T, Bartoli D, Polishuck RS, Danial NN, De Strooper B, Scorrano L, (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126: 177-189
9. Gillies LA, Du H, Peters B, Knudson CM, Newmeyer DD, Kuwana T, (2015) Visual and functional demonstration of growing Bax-induced pores in mitochondrial outer membranes. Mol Biol Cell 26: 339-349
10. Green DR, Kroemer G, (2004) The pathophysiology of mitochondrial cell death. Science 305: 626-629
11. Gross A, Jockel J, Wei MC, Korsmeyer SJ, (1998) Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 17: 3878-3885
12. Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W, (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 30: 4356-4370
13. Hell SW, (2009) Microscopy and its focal switch. Nat Methods 6: 24-32
14. Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM, Lackner LL, Westermann B, Schuldiner M, Weissman JS, Nunnari J, (2011) A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J Cell Biol 195: 323-340
15. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE, (2009) Cell death. N Engl J Med 361: 1570-1583
16. Hsu YT, Wolter KG, Youle RJ, (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 94: 3668-3672
17. Jakobs S, Wurm CA, (2014) Super-resolution microscopy of mitochondria. Curr Opin Chem Biol 20: 9-15
18. Jans DC, Wurm CA, Riedel D, Wenzel D, Stagge F, Deckers M, Rehling P, Jakobs S, (2013) STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria. Proc Natl Acad Sci USA 110: 8936-8941
19. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD, (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136
20. Kolmakov K, Belov VN, Bierwagen J, Ringemann C, Muller V, Eggeling C, Hell SW, (2010) Red-emitting rhodamine dyes for fluorescence microscopy and nanoscopy. Chemistry 16: 158-166
21. Kroemer G, Galluzzi L, Brenner C, (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163
22. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD, (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111: 331-342
23. 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
24. 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
25. von der Malsburg K, Muller JM, Bohnert M, Oeljeklaus S, Kwiatkowska P, Becker T, Loniewska-Lwowska A, Wiese S, Rao S, Milenkovic D, Hutu DP, Zerbes RM, Schulze-Specking A, Meyer HE, Martinou JC, Rospert S, Rehling P, Meisinger C, Veenhuis M, Warscheid B, et al, (2011) Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell 21: 694-707
26. Martinez-Caballero S, Dejean LM, Kinnally MS, Oh KJ, Mannella CA, Kinnally KW, (2009) Assembly of the mitochondrial apoptosis-induced channel, MAC. J Biol Chem 284: 12235-12245
27. Martinou JC, Youle RJ, (2011) Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 21: 92-101
28. Mattson MP, (2000) Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1: 120-129
29. Meier P, Finch A, Evan G, (2000) Apoptosis in development. Nature 407: 796-801
30. Moldoveanu T, Follis AV, Kriwacki RW, Green DR, (2014) Many players in BCL-2 family affairs. Trends Biochem Sci 39: 101-111
31. Montessuit S, Somasekharan SP, Terrones O, Lucken-Ardjomande S, Herzig S, Schwarzenbacher R, Manstein DJ, Bossy-Wetzel E, Basanez G, Meda P, Martinou JC, (2010) Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142: 889-901
32. Nechushtan A, Smith CL, Hsu YT, Youle RJ, (1999) Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J 18: 2330-2341
33. Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ, (2001) Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153: 1265-1276
34. Parone PA, James DI, Da Cruz S, Mattenberger Y, Donze O, Barja F, Martinou JC, (2006) Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol Cell Biol 26: 7397-7408
35. Peng R, Tong JS, Li H, Yue B, Zou F, Yu J, Zhang L, (2013) Targeting Bax interaction sites reveals that only homo-oligomerization sites are essential for its activation. Cell Death Differ 20: 744-754
36. Renault TT, Manon S, (2011) Bax: addressed to kill. Biochimie 93: 1379-1391
37. Salvador-Gallego R, Mund M, Cosentino K, Schneider J, Unsay J, Schraermeyer U, Engelhardt J, Ries J, García-Sáez AJ, (2016) Bax assembly into rings and arcs in apoptotic mitochondria is linked to membrane pores. EMBO J 35: 389-401
38. Schafer B, Quispe J, Choudhary V, Chipuk JE, Ajero TG, Du H, Schneiter R, Kuwana T, (2009) Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation. Mol Biol Cell 20: 2276-2285
39. Schellenberg B, Wang P, Keeble JA, Rodriguez-Enriquez R, Walker S, Owens TW, Foster F, Tanianis-Hughes J, Brennan K, Streuli CH, Gilmore AP, (2013) Bax exists in a dynamic equilibrium between the cytosol and mitochondria to control apoptotic priming. Mol Cell 49: 959-971
40. Schinzel A, Kaufmann T, Schuler M, Martinalbo J, Grubb D, Borner C, (2004) Conformational control of Bax localization and apoptotic activity by Pro168. J Cell Biol 164: 1021-1032
41. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, Korsmeyer SJ, (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67
42. Tait SW, Green DR, (2010) Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11: 621-632
43. Todt F, Cakir Z, Reichenbach F, Youle RJ, Edlich F, (2013) The C-terminal helix of Bcl-x(L) mediates Bax retrotranslocation from the mitochondria. Cell Death Differ 20: 333-342
44. Todt F, Cakir Z, Reichenbach F, Emschermann F, Lauterwasser J, Kaiser A, Ichim G, Tait SW, Frank S, Langer HF, Edlich F, (2015) Differential retrotranslocation of mitochondrial Bax and Bak. EMBO J 34: 67-80
45. Vaux DL, Korsmeyer SJ, (1999) Cell death in development. Cell 96: 245-254
46. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ, (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139: 1281-1292
47. Wurm CA, Neumann D, Schmidt R, Egner A, Jakobs S, (2010) Sample preparation for STED microscopy. In Live Cell Imaging: Methods and Protocols, Papkovsky DB, (ed.), pp 185-199. New York, NY: Humana Press
48. Wurm CA, Neumann D, Lauterbach MA, Harke B, Egner A, Hell SW, Jakobs S, (2011) Nanoscale distribution of mitochondrial import receptor Tom20 is adjusted to cellular conditions and exhibits an inner-cellular gradient. Proc Natl Acad Sci USA 108: 13546-13551
49. Yamaguchi R, Lartigue L, Perkins G, Scott RT, Dixit A, Kushnareva Y, Kuwana T, Ellisman MH, Newmeyer DD, (2008) Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol Cell 31: 557-569
50. Yang RF, Zhao GW, Liang ST, Zhang Y, Sun LH, Chen HZ, Liu DP, (2012) Mitofilin regulates cytochrome c release during apoptosis by controlling mitochondrial cristae remodeling. Biochem Biophys Res Commun 428: 93-98
51. Youle RJ, Karbowski M, (2005) Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 6: 657-663
52. Yuan J, Yankner BA, (2000) Apoptosis in the nervous system. Nature 407: 802-809
53. 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