Differential retrotranslocation of mitochondrial Bax and Bak

EMBO Journal

Volumn 34, Issue 1, 2015, Pages 67-80

  Todt, Franziska ^a   Cakir, Zeynep ^a   Reichenbach, Frank ^a   Emschermann, Frederic ^b,c   Lauterwasser, Joachim ^a   Kaiser, Andrea ^a   Ichim, Gabriel ^d   Tait, Stephen W G ^d   Frank, Stephan ^e   Langer, Harald F ^b,c   Edlich, Frank ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

apoptosis; Bcl 2 proteins; membrane association; tail anchor

Indexed keywords

PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; BAK1 PROTEIN, HUMAN; BAX PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN;

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CELL FRACTIONATION; CELL STRESS; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; CYTOSOL; CYTOSOLIC FRACTION; HUMAN; HYDROPHOBICITY; MITOCHONDRION; NONHUMAN; WILD TYPE; CELL LINE; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CYTOSOL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEIN TRANSPORT;

EID: 84920387957     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488806     Document Type: Article

References (45)

1. Antonsson B, Montessuit S, Lauper S, Eskes R, Martinou JC, (2000) Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 345 (Pt 2): 271-278
2. Banaszynski LA, Chen L-C, Maynard-Smith LA, Ooi AGL, Wandless TJ, (2006) A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell 126: 995-1004
3. Bratton SB, Cohen GM, (2001) Caspase cascades in chemically-induced apoptosis. Adv Exp Med Biol 500: 407-420
4. Dai H, Smith A, Meng XW, Schneider PA, Pang Y-P, Kaufmann SH, (2011) Transient binding of an activator BH3 domain to the Bak BH3-binding groove initiates Bak oligomerization. J Cell Biol 194: 39-48
5. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B, Martinou JC, (1999) Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144: 891-901
6. Dewson G, Kratina T, Sim HW, Puthalakath H, Adams JM, Colman PM, Kluck RM, (2008) To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol Cell 30: 369-380
7. 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
8. Eskes R, Antonsson B, Osen-Sand A, Montessuit S, Richter C, Sadoul R, Mazzei G, Nichols A, Martinou JC, (1998) Bax-induced cytochrome C release from mitochondria is independent of the permeability transition pore but highly dependent on Mg2 + ions. J Cell Biol 143: 217-224
9. Ferrer PE, Frederick P, Gulbis JM, Dewson G, Kluck RM, (2012) Translocation of a Bak C-terminus mutant from cytosol to mitochondria to mediate cytochrome C release: implications for Bak and Bax apoptotic function. PLoS One 7: e31510
10. García-Sáez AJ, Ries J, Orzáez M, Pérez-Payà E, Schwille P, (2009) Membrane promotes tBID interaction with BCL(XL). Nat Struct Mol Biol 16: 1178-1185
11. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG, Tu HC, Kim H, Cheng EH, Tjandra N, Walensky LD, (2008) BAX activation is initiated at a novel interaction site. Nature 455: 1076-1081
12. Green DR, Kroemer G, (2004) The pathophysiology of mitochondrial cell death. Science 305: 626-629
13. Habib SJ, Vasiljev A, Neupert W, Rapaport D, (2003) Multiple functions of tail-anchor domains of mitochondrial outer membrane proteins. FEBS Lett 555: 511-515
14. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674
15. Hsu YT, Youle RJ, (1997) Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 272: 13829-13834
16. Ishikawa-Ankerhold HC, Ankerhold R, Drummen GPC, (2012) Advanced Fluorescence Microscopy Techniques-FRAP, FLIP, FLAP, FRET and FLIM. Molecules 17: 4047-4132
17. Karbowski M, Lee Y-J, Gaume B, Jeong S-Y, Frank S, Nechushtan A, Santel A, Fuller M, Smith CL, Youle RJ, (2002) Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J Cell Biol 159: 931-938
18. Kim H, Rafiuddin-Shah M, Tu H-C, Jeffers JR, Zambetti GP, Hsieh JJ-D, Cheng EH-Y, (2006) Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 8: 1348-1358
19. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, Green DR, Newmeyer DD, (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17: 525-535
20. Kvansakul M, van Delft MF, Lee EF, Gulbis JM, Fairlie WD, Huang DCS, Colman PM, (2007) A structural viral mimic of prosurvival Bcl-2: a pivotal role for sequestering proapoptotic Bax and Bak. Mol Cell 25: 933-942
21. 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
22. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ, (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192
23. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC, Shiels HA, Ulrich E, Waymire KG, Mahar P, Frauwirth K, Chen Y, Wei M, Eng VM, Adelman DM, Simon MC, Ma A, Golden JA, Evan G, Korsmeyer SJ, MacGregor GR, Thompson CB, (2000) The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 6: 1389-1399
24. Llambi F, Moldoveanu T, Tait SWG, Bouchier-Hayes L, Temirov J, McCormick LL, Dillon CP, Green DR, (2011) A Unified Model of Mammalian BCL-2 Protein Family Interactions at the Mitochondria. Mol Cell 44: 517-531
25. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, Leber B, Andrews DW, (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135: 1074-1084
26. Moldoveanu T, Grace CR, Llambi F, Nourse A, Fitzgerald P, Gehring K, Kriwacki RW, Green DR, (2013) BID-induced structural changes in BAK promote apoptosis. Nat Struct Mol Biol 20: 589-597
27. 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
28. Ni Chonghaile T, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, Moore Vdel G, Deng J, Anderson KC, Richardson P, Tai YT, Mitsiades CS, Matulonis UA, Drapkin R, Stone R, Deangelo DJ, McConkey DJ, Sallan SE, Silverman L, Hirsch MS, Carrasco DR, Letai A, (2011) Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 334: 1129-1133
29. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, Joseph MK, Kitada S, Korsmeyer SJ, Kunzer AR, Letai A, Li C, Mitten MJ, Nettesheim DG, Ng S, Nimmer PM, O'Connor JM, Oleksijew A, Petros AM, (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681
30. Roucou X, Montessuit S, Antonsson B, Martinou J-C, (2002) Bax oligomerization in mitochondrial membranes requires tBid (caspase-8-cleaved Bid) and a mitochondrial protein. Biochem J 368: 915-921
31. Sarosiek KA, Chi X, Bachman JA, Sims JJ, Montero J, Patel L, Flanagan A, Andrews DW, Sorger P, Letai A, (2013) BID preferentially activates BAK while BIM preferentially activates BAX affecting chemotherapy response. Mol Cell 51: 751-765
32. 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
33. 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
34. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, Thompson CB, Korsmeyer SJ, (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci 92: 7834-7838
35. Setoguchi K, Otera H, Mihara K, (2006) Cytosolic factor- and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J 25: 5635-5647
36. Suzuki M, Youle RJ, Tjandra N, (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103: 645-654
37. Tait SWG, Parsons MJ, Llambi F, Bouchier-Hayes L, Connell S, Muñoz-Pinedo C, Green DR, (2010) Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev Cell 18: 802-813
38. 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
39. Valentijn AJ, Metcalfe AD, Kott J, Streuli CH, Gilmore AP, (2003) Spatial and temporal changes in Bax subcellular localization during anoikis. J Cell Biol 162: 599-612
40. Vo T-T, Ryan J, Carrasco R, Neuberg D, Rossi DJ, Stone RM, Deangelo DJ, Frattini MG, Letai A, (2012) Relative mitochondrial priming of myeloblasts and normal HSCs determines chemotherapeutic success in AML. Cell 151: 344-355
41. Wang K, Gross A, Waksman G, Korsmeyer SJ, (1998) Mutagenesis of the BH3 domain of BAX identifies residues critical for dimerization and killing. Mol Cell Biol 18: 6083-6089
42. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ, (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730
43. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, Huang DCS, (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19: 1294-1305
44. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE, Ierino H, Lee EF, Fairlie WD, Bouillet P, Strasser A, Kluck RM, Adams JM, Huang DC, (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315: 856-859
45. 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