Functions of the C-terminal domains of apoptosis-related proteins of the Bcl-2 family

Chemistry and Physics of Lipids

Volumn 183, Issue , 2014, Pages 77-90

  Gómez Fernández, Juan C ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BCL2 RELATED PROTEIN A1; BH3 PROTEIN; MEMBRANE PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL B; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN BID; PROTEIN BNIP3; PROTEIN BOK; PROTEIN HRK; PROTEIN MCL 1; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; PEPTIDE DERIVATIVE; PROTEIN BAD; APOPTOSIS REGULATORY PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; ENDOPLASMIC RETICULUM; HUMAN; HYDROPHOBICITY; LIPID COMPOSITION; MEMBRANE BINDING; MEMBRANE FLUIDITY; MITOCHONDRIAL MEMBRANE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STATIC ELECTRICITY; COMPARATIVE STUDY; DRUG TARGETING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; REVIEW; TRANSMEMBRANE DOMAIN; ANIMAL; CELL MEMBRANE; CHEMISTRY; METABOLISM; PHYSIOLOGY; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL MEMBRANE; HUMANS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84902466692     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2014.05.003     Document Type: Review

References (137)

1. E. Abdelwahid, T. Yokokura, R.J. Krieser, S. Balasundaram, W.H. Fowle, and K. White Mitochondrial disruption in Drosophila apoptosis Dev. Cell 12 2007 793 806
2. B.M. Abell, C. Rabu, P. Leznicki, J.C. Young, and S. High Post-translational integration of tail-anchored proteins is facilitated by defined molecular chaperones J. Cell Sci. 120 2007 1743 1751
3. J.M. Adams, and S. Cory The Bcl-2 protein family: arbiters of cell survival Science 281 1998 1322 1326
4. C. Aisenbrey, U.S. Sudheendra, H. Ridley, P. Bertani, A. Marquette, S. Nedelkina, J.H. Lakey, and B. Bechinger Helix orientations in membrane-associated Bcl-X(L) determined by 15N-solid-state NMR spectroscopy Eur. Biophys. J. 37 2007 71 80
5. Y. Akao, Y. Otsuki, S. Kataoka, Y. Ito, and Y. Tsujimoto Multiple subcellular localization of bcl-2: detection in nuclear outer membrane, endoplasmic reticulum membrane, and mitochondrial membranes Cancer Res. 54 1994 2468 2471
6. R. Allen, B. Egan, K. Gabriel, T. Beilharz, and T. Lithgow A conserved proline residue is present in the transmembrane-spanning domain of Tom7 and other tail-anchored protein subunits of the TOM translocase FEBS Lett. 514 2002 347 350
7. M.G. Annis, E.L. Soucie, P.J. Dlugosz, J.A. Cruz-Aguado, L.Z. Penn, B. Leber, and D.W. Andrews Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis EMBO J. 24 2005 2096 2103
8. A. Antignani, and R.J. Youle How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr. Opin. Cell Biol. 18 2006 685 689
9. B. Antonsson, S. Montessuit, B. Sanchez, and J.C. Martinou Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells J. Biol. Chem. 276 2001 11615 11623
10. M. Aritomi, N. Kunishima, N. Inohara, Y. Ishibashi, S. Ohta, and K. Morikawa Crystal structure of rat Bcl-xL. Implications for the function of the Bcl-2 protein family J. Biol. Chem. 272 1997 27886 27892
11. H. Arokium, N. Camougrand, F.M. Vallette, and S. Manon Studies of the interaction of substituted mutants of BAX with yeast mitochondria reveal that the C-terminal hydrophobic alpha-helix is a second ART sequence and plays a role in the interaction with anti-apoptotic BCL-xL J. Biol. Chem. 279 2004 52566 52573
12. A. Ausili, A. de Godos, A. Torrecillas, S. Corbalan-Garcia, and J.C. Gomez-Fernandez The interaction of the Bax C-terminal domain with membranes is influenced by the presence of negatively charged phospholipids Biochim. Biophys. Acta 1788 2009 1924 1932
13. A. Ausili, A. Torrecillas, M.M. Martinez-Senac, S. Corbalan-Garcia, and J.C. Gomez-Fernandez The interaction of the Bax C-terminal domain with negatively charged lipids modifies the secondary structure and changes its way of insertion into membranes J. Struct. Biol. 164 2008 146 152
14. S. Barrera-Vilarmau, P. Obregon, and E. de Alba Intrinsic order and disorder in the bcl-2 member harakiri: insights into its proapoptotic activity PLoS ONE 6 2011 e21413
15. G. Basanez, A. Nechushtan, O. Drozhinin, A. Chanturiya, E. Choe, S. Tutt, K.A. Wood, Y. Hsu, J. Zimmerberg, and R.J. Youle Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations Proc. Natl. Acad. Sci. USA 96 1999 5492 5497
16. T. Beilharz, B. Egan, P.A. Silver, K. Hofmann, and T. Lithgow Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae J. Biol. Chem. 278 2003 8219 8223
17. A. Bernabeu, J. Guillen, A.J. Perez-Berna, M.R. Moreno, and J. Villalain Structure of the C-terminal domain of the pro-apoptotic protein Hrk and its interaction with model membranes Biochim. Biophys. Acta 1768 2007 1659 1670
18. S. Bleicken, M. Classen, P.V. Padmavathi, T. Ishikawa, K. Zeth, H.J. Steinhoff, and E. Bordignon Molecular details of Bax activation, oligomerization, and membrane insertion J. Biol. Chem. 285 2010 6636 6647
19. E.V. Bocharov, Y.E. Pustovalova, K.V. Pavlov, P.E. Volynsky, M.V. Goncharuk, Y.S. Ermolyuk, D.V. Karpunin, A.A. Schulga, M.P. Kirpichnikov, R.G. Efremov, I.V. Maslennikov, and A.S. Arseniev Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger J. Biol. Chem. 282 2007 16256 16266
20. R.J. Boohaker, G. Zhang, M.W. Lee, K.N. Nemec, S. Santra, J.M. Perez, and A.R. Khaled Rational development of a cytotoxic peptide to trigger cell death Mol. Pharm. 9 2012 2080 2093
21. C. Borner, I. Martinou, C. Mattmann, M. Irmler, E. Schaerer, J.C. Martinou, and J. Tschopp The protein bcl-2 alpha does not require membrane attachment, but two conserved domains to suppress apoptosis J. Cell Biol. 126 1994 1059 1068
22. G. Brien, A.L. Debaud, X. Robert, L. Oliver, M.C. Trescol-Biemont, N. Cauquil, O. Geneste, N. Aghajari, F.M. Vallette, R. Haser, and N. Bonnefoy-Berard C-terminal residues regulate localization and function of the antiapoptotic protein Bfl-1 J. Biol. Chem. 284 2009 30257 30263
23. P.F. Cartron, M. Priault, L. Oliver, K. Meflah, S. Manon, and F.M. Vallette The N-terminal end of Bax contains a mitochondrial-targeting signal J. Biol. Chem. 278 2003 11633 11641
24. A. Cassidy-Stone, J.E. Chipuk, E. Ingerman, C. Song, C. Yoo, T. Kuwana, M.J. Kurth, J.T. Shaw, J.E. Hinshaw, D.R. Green, and J. Nunnari Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization Dev. Cell 14 2008 193 204
25. S. Cory, and J.M. Adams The Bcl2 family: regulators of the cellular life-or-death switch Nat. Rev. Cancer 2 2002 647 656
26. C.C. Curtain, F.E. Ali, D.G. Smith, A.I. Bush, C.L. Masters, and K.J. Barnham Metal ions, pH, and cholesterol regulate the interactions of Alzheimer's disease amyloid-beta peptide with membrane lipid J. Biol. Chem. 278 2003 2977 2982
27. P.E. Czabotar, G. Lessene, A. Strasser, and J.M. Adams Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy Nat. Rev. Mol. Cell Biol. 15 2014 49 63
28. P.E. Czabotar, D. Westphal, G. Dewson, S. Ma, C. Hockings, W.D. Fairlie, E.F. Lee, S. Yao, A.Y. Robin, B.J. Smith, D.C. Huang, R.M. Kluck, J.M. Adams, and P.M. Colman Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis Cell 152 2013 519 531
29. Z. Chen-Levy, J. Nourse, and M.L. Cleary The bcl-2 candidate proto-oncogene product is a 24-kilodalton integral-membrane protein highly expressed in lymphoid cell lines and lymphomas carrying the t(14;18) translocation Mol. Cell. Biol. 9 1989 701 710
30. J.E. Chipuk, and D.R. Green How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18 2008 157 164
31. T. Chittenden, E.A. Harrington, R. O'Connor, C. Flemington, R.J. Lutz, G.I. Evan, and B.C. Guild Induction of apoptosis by the Bcl-2 homologue Bak Nature 374 1995 733 736
32. A. D'Arrigo, E. Manera, R. Longhi, and N. Borgese The specific subcellular localization of two isoforms of cytochrome b5 suggests novel targeting pathways J. Biol. Chem. 268 1993 2802 2808
33. C. D'Sa-Eipper, and G. Chinnadurai Functional dissection of Bfl-1, a Bcl-2 homolog: anti-apoptosis, oncogene-cooperation and cell proliferation activities Oncogene 16 1998 3105 3114
34. M. del Mar Martinez-Senac, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Study of the secondary structure of the C-terminal domain of the antiapoptotic protein bcl-2 and its interaction with model membranes Biochemistry 39 2000 7744 7752
35. M. del Mar Martinez-Senac, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Conformation of the C-terminal domain of the pro-apoptotic protein Bax and mutants and its interaction with membranes Biochemistry 40 2001 9983 9992
36. A.Y. Denisov, M.S. Madiraju, G. Chen, A. Khadir, P. Beauparlant, G. Attardo, G.C. Shore, and K. Gehring Solution structure of human BCL-w: modulation of ligand binding by the C-terminal helix J. Biol. Chem. 278 2003 21124 21128
37. G. Dewson, T. Kratina, P. Czabotar, C.L. Day, J.M. Adams, and R.M. Kluck Bak activation for apoptosis involves oligomerization of dimers via their alpha6 helices Mol. Cell 36 2009 696 703
38. G. Dewson, T. Kratina, H.W. Sim, H. Puthalakath, J.M. Adams, P.M. Colman, and R.M. Kluck To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions Mol. Cell 30 2008 369 380
39. G. Dewson, S. Ma, P. Frederick, C. Hockings, I. Tan, T. Kratina, and R.M. Kluck Bax dimerizes via a symmetric BH3:groove interface during apoptosis Cell Death Differ. 19 2012 661 670
40. N. Echeverry, D. Bachmann, F. Ke, A. Strasser, H.U. Simon, and T. Kaufmann Intracellular localization of the BCL-2 family member BOK and functional implications Cell Death Differ. 20 2013 785 799
41. R.F. Epand, J.C. Martinou, M. Fornallaz-Mulhauser, D.W. Hughes, and R.M. Epand The apoptotic protein tBid promotes leakage by altering membrane curvature J. Biol. Chem. 277 2002 32632 32639
42. S.N. Farrow, J.H. White, I. Martinou, T. Raven, K.T. Pun, C.J. Grinham, J.C. Martinou, and R. Brown Cloning of a bcl-2 homologue by interaction with adenovirus E1B 19K Nature 374 1995 731 733
43. P.E. Ferrer, P. Frederick, J.M. Gulbis, G. Dewson, and R.M. Kluck 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 2012 e31510
44. A.J. Garcia-Saez, I. Mingarro, E. Perez-Paya, and J. Salgado Membrane-insertion fragments of Bcl-xL, Bax, and Bid Biochemistry 43 2004 10930 10943
45. P. Garg, K.N. Nemec, A.R. Khaled, and S.A. Tatulian Transmembrane pore formation by the carboxyl terminus of Bax protein Biochim. Biophys. Acta 1828 2013 732 742
46. E. Gavathiotis, D.E. Reyna, M.L. Davis, G.H. Bird, and L.D. Walensky BH3-triggered structural reorganization drives the activation of proapoptotic BAX Mol. Cell 40 2010 481 492
47. E. Gavathiotis, M. Suzuki, M.L. Davis, K. Pitter, G.H. Bird, S.G. Katz, H.C. Tu, H. Kim, E.H. Cheng, N. Tjandra, and L.D. Walensky BAX activation is initiated at a novel interaction site Nature 455 2008 1076 1081
48. N.M. George, J.J. Evans, and X. Luo A three-helix homo-oligomerization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax Genes Dev. 21 2007 1937 1948
49. L.A. Gillies, and T. Kuwana Apoptosis regulation at the mitochondrial outer membrane J. Cell. Biochem. 115 2014 632 640
50. J.C. Gomez-Fernandez, and S. Corbalan-Garcia Diacylglycerols, multivalent membrane modulators Chem. Phys. Lipids 148 2007 1 25
51. I.S. Goping, A. Gross, J.N. Lavoie, M. Nguyen, R. Jemmerson, K. Roth, S.J. Korsmeyer, and G.C. Shore Regulated targeting of BAX to mitochondria J. Cell Biol. 143 1998 207 215
52. D.R. Green, and J.C. Reed Mitochondria and apoptosis Science 281 1998 1309 1312
53. G.J. Griffiths, B.M. Corfe, P. Savory, S. Leech, M.D. Esposti, J.A. Hickman, and C. Dive Cellular damage signals promote sequential changes at the N-terminus and BH-1 domain of the pro-apoptotic protein Bak Oncogene 20 2001 7668 7676
54. A. Gross, J. Jockel, M.C. Wei, and S.J. Korsmeyer Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis EMBO J. 17 1998 3878 3885
55. R.P. Guedes, E. Rocha, J. Mahiou, H.P. Moll, M.B. Arvelo, J.M. Taube, C.R. Peterson, E. Kaczmarek, C.R. Longo, C.G. da Silva, and C. Ferran The C-terminal domain of A1/Bfl-1 regulates its anti-inflammatory function in human endothelial cells Biochim. Biophys. Acta 1833 2013 1553 1561
56. M. Hekman, S. Albert, A. Galmiche, U.E. Rennefahrt, J. Fueller, A. Fischer, D. Puehringer, S. Wiese, and U.R. Rapp Reversible membrane interaction of BAD requires two C-terminal lipid binding domains in conjunction with 14-3-3 protein binding J. Biol. Chem. 281 2006 17321 17336
57. M.J. Herold, J. Zeitz, C. Pelzer, C. Kraus, A. Peters, G. Wohlleben, and I. Berberich The stability and anti-apoptotic function of A1 are controlled by its C terminus J. Biol. Chem. 281 2006 13663 13671
58. M.G. Hinds, M. Lackmann, G.L. Skea, P.J. Harrison, D.C. Huang, and C.L. Day The structure of Bcl-w reveals a role for the C-terminal residues in modulating biological activity EMBO J. 22 2003 1497 1507
59. D.M. Hockenbery, Z.N. Oltvai, X.M. Yin, C.L. Milliman, and S.J. Korsmeyer Bcl-2 functions in an antioxidant pathway to prevent apoptosis Cell 75 1993 241 251
60. C. Horie, H. Suzuki, M. Sakaguchi, and K. Mihara Characterization of signal that directs C-tail-anchored proteins to mammalian mitochondrial outer membrane Mol. Biol. Cell 13 2002 1615 1625
61. S.Y. Hsu, A. Kaipia, E. McGee, M. Lomeli, and A.J. Hsueh Bok is a pro-apoptotic Bcl-2 protein with restricted expression in reproductive tissues and heterodimerizes with selective anti-apoptotic Bcl-2 family members Proc. Natl. Acad. Sci. USA 94 1997 12401 12406
62. S. Isenmann, Y. Khew-Goodall, J. Gamble, M. Vadas, and B.W. Wattenberg A splice-isoform of vesicle-associated membrane protein-1 (VAMP-1) contains a mitochondrial targeting signal Mol. Biol. Cell 9 1998 1649 1660
63. S.Y. Jeong, B. Gaume, Y.J. Lee, Y.T. Hsu, S.W. Ryu, S.H. Yoon, and R.J. Youle Bcl-x(L) sequesters its C-terminal membrane anchor in soluble, cytosolic homodimers EMBO J. 23 2004 2146 2155
64. Y. Kang, D.C. Lee, J. Han, S. Yoon, M. Won, J.H. Yeom, M.J. Seong, J.J. Ko, K.A. Lee, K. Lee, and J. Bae NM23-H2 involves in negative regulation of Diva and Bcl2L10 in apoptosis signaling Biochem. Biophys. Res. Commun. 359 2007 76 82
65. J.A. Kaufmann, M. Perez, W. Zhang, P.C. Bickford, D.B. Holmes, and G. Taglialatela Free radical-dependent nuclear localization of Bcl-2 in the central nervous system of aged rats is not associated with Bcl-2-mediated protection from apoptosis J. Neurochem. 87 2003 981 994
66. T. Kaufmann, S. Schlipf, J. Sanz, K. Neubert, R. Stein, and C. Borner Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane J. Cell Biol. 160 2003 53 64
67. N. Ke, A. Godzik, and J.C. Reed Bcl-B, a novel Bcl-2 family member that differentially binds and regulates Bax and Bak J. Biol. Chem. 276 2001 12481 12484
68. C. Kemper, S.J. Habib, G. Engl, P. Heckmeyer, K.S. Dimmer, and D. Rapaport Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components J. Cell Sci. 121 2008 1990 1998
69. M.C. Kiefer, M.J. Brauer, V.C. Powers, J.J. Wu, S.R. Umansky, L.D. Tomei, and P.J. Barr Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak Nature 374 1995 736 739
70. J.K. Ko, K.H. Choi, Z. Pan, P. Lin, N. Weisleder, C.W. Kim, and J. Ma The tail-anchoring domain of Bfl1 and HCCS1 targets mitochondrial membrane permeability to induce apoptosis J. Cell Sci. 120 2007 2912 2923
71. J.K. Ko, K.H. Choi, J. Peng, F. He, Z. Zhang, N. Weisleder, J. Lin, and J. Ma Amphipathic tail-anchoring peptide and Bcl-2 homology domain-3 (BH3) peptides from Bcl-2 family proteins induce apoptosis through different mechanisms J. Biol. Chem. 286 2011 9038 9048
72. S. Krajewski, S. Tanaka, S. Takayama, M.J. Schibler, W. Fenton, and J.C. Reed Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes Cancer Res. 53 1993 4701 4714
73. M. Kvansakul, H. Yang, W.D. Fairlie, P.E. Czabotar, S.F. Fischer, M.A. Perugini, D.C. Huang, and P.M. Colman Vaccinia virus anti-apoptotic F1L is a novel Bcl-2-like domain-swapped dimer that binds a highly selective subset of BH3-containing death ligands Cell Death Differ. 15 2008 1564 1571
74. L. Lan, S. Isenmann, and B.W. Wattenberg Targeting and insertion of C-terminally anchored proteins to the mitochondrial outer membrane is specific and saturable but does not strictly require ATP or molecular chaperones Biochem. J. 349 2000 611 621
75. B.A. Lewis, and D.M. Engelman Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles J. Mol. Biol. 166 1983 211 217
76. H. Li, H. Zhu, C.J. Xu, and J. Yuan Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis Cell 94 1998 491 501
77. S.H. Lin, M.N. Perera, T. Nguyen, D. Datskovskiy, M. Miles, and M. Colombini Bax forms two types of channels, one of which is voltage-gated Biophys. J. 101 2011 2163 2169
78. T. Lindsten, A.J. Ross, A. King, W.X. Zong, J.C. Rathmell, H.A. Shiels, E. Ulrich, K.G. Waymire, P. Mahar, K. Frauwirth, Y. Chen, M. Wei, V.M. Eng, D.M. Adelman, M.C. Simon, A. Ma, J.A. Golden, G. Evan, S.J. Korsmeyer, G.R. MacGregor, and C.B. Thompson The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues Mol. Cell 6 2000 1389 1399
79. E. Lomonosova, and G. Chinnadurai BH3-only proteins in apoptosis and beyond: an overview Oncogene 27 Suppl. 1 2008 S2L 19
80. J.F. Lovell, L.P. Billen, S. Bindner, A. Shamas-Din, C. Fradin, B. Leber, and D.W. Andrews Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax Cell 135 2008 1074 1084
81. M. Martinez-Senac Mdel, S. Corbalan-Garcia, and J.C. Gomez-Fernandez The structure of the C-terminal domain of the pro-apoptotic protein Bak and its interaction with model membranes Biophys. J. 82 2002 233 243
82. J.C. Martinou, and D.R. Green Breaking the mitochondrial barrier Nat. Rev. Mol. Cell Biol. 2 2001 63 67
83. J.C. Martinou, and R.J. Youle Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics Dev. Cell 21 2011 92 101
84. V. Mikhailov, M. Mikhailova, K. Degenhardt, M.A. Venkatachalam, E. White, and P. Saikumar Association of Bax and Bak homo-oligomers in mitochondria, Bax requirement for Bak reorganization and cytochrome c release J. Biol. Chem. 278 2003 5367 5376
85. C. Motz, H. Martin, T. Krimmer, and J. Rassow Bcl-2 and porin follow different pathways of TOM-dependent insertion into the mitochondrial outer membrane J. Mol. Biol. 323 2002 729 738
86. A.D. Mozdy, J.M. McCaffery, and J.M. Shaw Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p J. Cell Biol. 151 2000 367 380
87. S.W. Muchmore, M. Sattler, H. Liang, R.P. Meadows, J.E. Harlan, H.S. Yoon, D. Nettesheim, B.S. Chang, C.B. Thompson, S.L. Wong, S.L. Ng, and S.W. Fesik X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death Nature 381 1996 335 341
88. M. Narita, S. Shimizu, T. Ito, T. Chittenden, R.J. Lutz, H. Matsuda, and Y. Tsujimoto Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria Proc. Natl. Acad. Sci. USA 95 1998 14681 14686
89. A. Nechushtan, C.L. Smith, Y.T. Hsu, and R.J. Youle Conformation of the Bax C-terminus regulates subcellular location and cell death EMBO J. 18 1999 2330 2341
90. Y. Nemoto, and P. De Camilli Recruitment of an alternatively spliced form of synaptojanin 2 to mitochondria by the interaction with the PDZ domain of a mitochondrial outer membrane protein EMBO J. 18 1999 2991 3006
91. M. Nguyen, P.E. Branton, P.A. Walton, Z.N. Oltvai, S.J. Korsmeyer, and G.C. Shore Role of membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus J. Biol. Chem. 269 1994 16521 16524
92. M. Nguyen, D.G. Millar, V.W. Yong, S.J. Korsmeyer, and G.C. Shore Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence J. Biol. Chem. 268 1993 25265 25268
93. S. Nouraini, E. Six, S. Matsuyama, S. Krajewski, and J.C. Reed The putative pore-forming domain of Bax regulates mitochondrial localization and interaction with Bcl-X(L) Mol. Cell. Biol. 20 2000 1604 1615
94. K.J. Oh, P. Singh, K. Lee, K. Foss, S. Lee, M. Park, S. Aluvila, R.S. Kim, J. Symersky, and D.E. Walters Conformational changes in BAK, a pore-forming proapoptotic Bcl-2 family member, upon membrane insertion and direct evidence for the existence of BH3-BH3 contact interface in BAK homo-oligomers J. Biol. Chem. 285 2010 28924 28937
95. E. Oldfield, and D. Chapman Dynamics of lipids in membranes: heterogeneity and the role of cholesterol FEBS Lett. 23 1972 285 297
96. L. Oliver, M. Priault, K. Tremblais, M. LeCabellec, K. Meflah, S. Manon, and F.M. Vallette The substitution of the C-terminus of bax by that of bcl-xL does not affect its subcellular localization but abrogates its pro-apoptotic properties FEBS Lett. 487 2000 161 165
97. A. Ospina, A. Lagunas-Martinez, J. Pardo, and J.A. Carrodeguas Protein oligomerization mediated by the transmembrane carboxyl terminal domain of Bcl-XL FEBS Lett. 585 2011 2935 2942
98. M. Ott, E. Norberg, B. Zhivotovsky, and S. Orrenius Mitochondrial targeting of tBid/Bax: a role for the TOM complex? Cell Death Differ. 16 2009 1075 1082
99. L. Polzien, A. Baljuls, H.M. Roth, J. Kuper, R. Benz, K. Schweimer, M. Hekman, and U.R. Rapp Pore-forming activity of BAD is regulated by specific phosphorylation and structural transitions of the C-terminal part Biochim. Biophys. Acta 1810 2011 162 169
100. M. Priault, P.F. Cartron, N. Camougrand, B. Antonsson, F.M. Vallette, and S. Manon Investigation of the role of the C-terminus of Bax and of tc-Bid on Bax interaction with yeast mitochondria Cell Death Differ. 10 2003 1068 1077
101. E. Raemy, and J.C. Martinou Involvement of cardiolipin in tBID-induced activation of BAX during apoptosis Chem. Phys. Lipids 179 2014 70 74
102. G.J. Rautureau, C.L. Day, and M.G. Hinds The structure of Boo/Diva reveals a divergent Bcl-2 protein Proteins 78 2010 2181 2186
103. J. Ren, S. Lew, Z. Wang, and E. London Transmembrane orientation of hydrophobic alpha-helices is regulated both by the relationship of helix length to bilayer thickness and by the cholesterol concentration Biochemistry 36 1997 10213 10220
104. A.N. Ridder, W. van de Hoef, J. Stam, A. Kuhn, B. de Kruijff, and J.A. Killian Importance of hydrophobic matching for spontaneous insertion of a single-spanning membrane protein Biochemistry 41 2002 4946 4952
105. K. Ross, T. Rudel, and V. Kozjak-Pavlovic TOM-independent complex formation of Bax and Bak in mammalian mitochondria during TNFalpha-induced apoptosis Cell Death Differ. 16 2009 697 707
106. S.L. Schendel, Z. Xie, M.O. Montal, S. Matsuyama, M. Montal, and J.C. Reed Channel formation by antiapoptotic protein Bcl-2 Proc. Natl. Acad. Sci. USA 94 1997 5113 5118
107. A. Schinzel, T. Kaufmann, M. Schuler, J. Martinalbo, D. Grubb, and C. Borner Conformational control of Bax localization and apoptotic activity by Pro168 J. Cell Biol. 164 2004 1021 1032
108. P.H. Schlesinger, A. Gross, X.M. Yin, K. Yamamoto, M. Saito, G. Waksman, and S.J. Korsmeyer Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2 Proc. Natl. Acad. Sci. USA 94 1997 11357 11362
109. Z.T. Schug, and E. Gottlieb Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis Biochim. Biophys. Acta 1788 2009 2022 2031
110. K. Setoguchi, H. Otera, and K. Mihara Cytosolic factor- and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins EMBO J. 25 2006 5635 5647
111. C.D. Sperka-Gottlieb, A. Hermetter, F. Paltauf, and G. Daum Lipid topology and physical properties of the outer mitochondrial membrane of the yeast, Saccharomyces cerevisiae Biochim. Biophys. Acta 946 1988 227 234
112. S. Stefanovic, and R.S. Hegde Identification of a targeting factor for posttranslational membrane protein insertion into the ER Cell 128 2007 1147 1159
113. E.S. Sulistijo, T.M. Jaszewski, and K.R. MacKenzie Sequence-specific dimerization of the transmembrane domain of the BH3-only protein BNIP3 in membranes and detergent J. Biol. Chem. 278 2003 51950 51956
114. E.S. Sulistijo, and K.R. Mackenzie Structural basis for dimerization of the BNIP3 transmembrane domain Biochemistry 48 2009 5106 5120
115. M. Suzuki, R.J. Youle, and N. Tjandra Structure of Bax: coregulation of dimer formation and intracellular localization Cell 103 2000 645 654
116. S. Tanaka, K. Saito, and J.C. Reed Structure-function analysis of the Bcl-2 oncoprotein, Addition of a heterologous transmembrane domain to portions of the Bcl-2 beta protein restores function as a regulator of cell survival J. Biol. Chem. 268 1993 10920 10926
117. S.A. Tatulian, P. Garg, K.N. Nemec, B. Chen, and A.R. Khaled Molecular basis for membrane pore formation by Bax protein carboxyl terminus Biochemistry 51 2012 9406 9419
118. K. Terasaki, S. Won, and S. Makino The C-terminal region of Rift Valley fever virus NSm protein targets the protein to the mitochondrial outer membrane and exerts antiapoptotic function J. Virol. 87 2013 676 682
119. G.R. Thuduppathy, J.W. Craig, V. Kholodenko, A. Schon, and R.B. Hill Evidence that membrane insertion of the cytosolic domain of Bcl-xL is governed by an electrostatic mechanism J. Mol. Biol. 359 2006 1045 1058
120. F. Todt, Z. Cakir, F. Reichenbach, R.J. Youle, and F. Edlich The C-terminal helix of Bcl-x(L) mediates Bax retrotranslocation from the mitochondria Cell Death Differ. 20 2013 333 342
121. A. Torrecillas, M.M. Martinez-Senac, A. Ausili, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Interaction of the C-terminal domain of Bcl-2 family proteins with model membranes Biochim. Biophys. Acta 1768 2007 2931 2939
122. A. Torrecillas, M.M. Martinez-Senac, E. Goormaghtigh, A. de Godos, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Modulation of the membrane orientation and secondary structure of the C-terminal domains of Bak and Bcl-2 by lipids Biochemistry 44 2005 10796 10809
123. G.V. V, and A.I. Davidovskii Structural insights into proapoptotic signaling mediated by MTCH2, VDAC2 TOM40 and TOM22 Cell Signal 26 2014 370 382
124. A.J. Valentijn, J.P. Upton, and A.P. Gilmore Analysis of endogenous Bax complexes during apoptosis using blue native PAGE: implications for Bax activation and oligomerization Biochem. J. 412 2008 347 357
125. B.A. Vance, C.M. Zacharchuk, and D.M. Segal Recombinant mouse Bcl-2(1-203). Two domains connected by a long protease-sensitive linker J. Biol. Chem. 271 1996 30811 30815
126. R.J. Webb, J.M. East, R.P. Sharma, and A.G. Lee Hydrophobic mismatch and the incorporation of peptides into lipid bilayers: a possible mechanism for retention in the Golgi Biochemistry 37 1998 673 679
127. M.C. Wei, T. Lindsten, V.K. Mootha, S. Weiler, A. Gross, M. Ashiya, C.B. Thompson, and S.J. Korsmeyer tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c Genes Dev. 14 2000 2060 2071
128. M.C. Wei, W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 2001 727 730
129. C. Weng, Y. Li, D. Xu, Y. Shi, and H. Tang Specific cleavage of Mcl-1 by caspase-3 in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in Jurkat leukemia T cells J. Biol. Chem. 280 2005 10491 10500
130. D. Westphal, G. Dewson, P.E. Czabotar, and R.M. Kluck Molecular biology of Bax and Bak activation and action Biochim. Biophys. Acta 1813 2011 521 531
131. F. Wilfling, A. Weber, S. Potthoff, F.N. Vogtle, C. Meisinger, S.A. Paschen, and G. Hacker BH3-only proteins are tail-anchored in the outer mitochondrial membrane and can initiate the activation of Bax Cell Death Differ. 19 2012 1328 1336
132. K.G. Wolter, Y.T. Hsu, C.L. Smith, A. Nechushtan, X.G. Xi, and R.J. Youle Movement of Bax from the cytosol to mitochondria during apoptosis J. Cell Biol. 139 1997 1281 1292
133. W.M. Yau, W.C. Wimley, K. Gawrisch, and S.H. White The preference of tryptophan for membrane interfaces Biochemistry 37 1998 14713 14718
134. R.J. Youle, and A. Strasser The BCL-2 protein family: opposing activities that mediate cell death Nat. Rev. Mol. Cell Biol. 9 2008 47 59
135. T. Zhang, and A. Saghatelian Emerging roles of lipids in BCL-2 family-regulated apoptosis Biochim. Biophys. Acta 1831 2013 1542 1554
136. Z. Zhang, W. Zhu, S.M. Lapolla, Y. Miao, Y. Shao, M. Falcone, D. Boreham, N. McFarlane, J. Ding, A.E. Johnson, X.C. Zhang, D.W. Andrews, and J. Lin Bax forms an oligomer via separate, yet interdependent, surfaces J. Biol. Chem. 285 2010 17614 17627
137. J.Y. Zheng, Y.C. Tsai, P. Kadimcherla, R. Zhang, J. Shi, G.A. Oyler, and N.N. Boustany The C-terminal transmembrane domain of Bcl-xL mediates changes in mitochondrial morphology Biophys. J. 94 2008 286 297