Pro-apoptotic Bax molecules densely populate the edges of membrane pores

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kuwana, Tomomi ^a   Olson, Norman H ^b   Kiosses, William B ^a   Peters, Bjoern ^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

APOPTOSIS REGULATORY PROTEIN; PROTEIN BAX;

CHEMISTRY; CRYOELECTRON MICROSCOPY; METABOLISM; MITOCHONDRIAL MEMBRANE; PERMEABILITY; PHYSIOLOGY;

APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CRYOELECTRON MICROSCOPY; MITOCHONDRIAL MEMBRANES; PERMEABILITY;

EID: 84973397950     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27299     Document Type: Article

References (64)

1. Danial, N. N. & Korsmeyer, S. J. Cell death: critical control points. Cell 116, 205-219 (2004).
2. Newmeyer, D. D. & Ferguson-Miller, S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112, 481-490 (2003).
3. Bender, T. & Martinou, J. C. Where killers meet-permeabilization of the outer mitochondrial membrane during apoptosis. Cold Spring Harb Perspect Biol 5, a011106, doi: 10.1101/cshperspect.a011106 (2013).
4. Youle, R. J. & Strasser, A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59 (2008).
5. Lartigue, L. et al. Caspase-independent mitochondrial cell death results from loss of respiration, not cytotoxic protein release. Mol Biol Cell 20, 4871-4884, doi: 10.1091/mbc.E09-07-0649 (2009).
6. Chipuk, J. E., Moldoveanu, T., Llambi, F., Parsons, M. J. & Green, D. R. The BCL-2 family reunion. Mol. Cell 37, 299-310, doi: 10.1016/j.molcel.2010.01.025 (2010).
7. Gillies, L. A. & Kuwana, T. Apoptosis regulation at the mitochondrial outer membrane. J. Cell. Biochem. 115, 632-640, doi: 10.1002/jcb.24709 (2014).
8. Gavathiotis, E., Reyna, D. E., Davis, M. L., Bird, G. H. & Walensky, L. D. BH3-triggered structural reorganization drives the activation of proapoptotic BAX. Mol. Cell 40, 481-492, doi: 10.1016/j.molcel.2010.10.019 (2010).
9. Gavathiotis, E. et al. BAX activation is initiated at A novel interaction site. Nature 455, 1076-1081 (2008).
10. Moldoveanu, T. et al. The X-ray structure of A BAK homodimer reveals an inhibitory zinc binding site. Mol. Cell 24, 677-688 (2006).
11. Suzuki, M., Youle, R. J. & Tjandra, N. Structure of bax. Coregulation Of dimer formation and intracellular localization. Cell 103, 645-654 (2000).
12. Annis, M. G. et al. Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J. 24, 2096-2103 (2005).
13. Westphal, D. et al. Apoptotic pore formation is associated with in-plane insertion of Bak or Bax central helices into the mitochondrial outer membrane. Proc Natl Acad Sci USA 111, E4076-4085, doi: 10.1073/pnas.1415142111 (2014).
14. Kushnareva, Y., Andreyev, A. Y., Kuwana, T. & Newmeyer, D. D. Bax Activation Initiates the Assembly of A Multimeric Catalyst that Facilitates Bax Pore Formation in Mitochondrial Outer Membranes. PLoS Biol. 10, e1001394, doi: 10.1371/journal.pbio.1001394 (2012).
15. Lovell, J. F. et al. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135, 1074-1084 (2008).
16. Czabotar, P. E., Lessene, G., Strasser, A. & Adams, J. M. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15, 49-63, doi: 10.1038/nrm3722 (2014).
17. Dewson, G. & Kluck, R. M. Mechanisms by which Bak and Bax permeabilise mitochondria during apoptosis. J. Cell Sci. 122, 2801-2808 (2009).
18. Bleicken, S. et al. Structural model of active bax at the membrane. Mol. Cell 56, 496-505, doi: 10.1016/j.molcel.2014.09.022 (2014).
19. Kim, H. et al. Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol. Cell 36, 487-499 (2009).
20. Xu, X. P. et al. Three-dimensional structure of Bax-mediated pores in membrane bilayers. Cell Death Dis 4, e683, doi: 10.1038/cddis.2013.210 (2013).
21. Kuwana, T. et al. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342 (2002).
22. Gillies, L. A. et al. Visual and functional demonstration of growing Bax-induced pores in mitochondrial outer membranes. Mol Biol Cell 26, 339-349, doi: 10.1091/mbc.E13-11-0638 (2015).
23. Schafer, B. et al. Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation. Mol Biol Cell 20, 2276-2285 (2009).
24. Aluvila, S. et al. Organization of the mitochondrial apoptotic BAK pore: oligomerization of the BAK homodimers. J. Biol. Chem. 289, 2537-2551, doi: 10.1074/jbc.M113.526806 (2014).
25. Czabotar, P. E. et al. Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 152, 519-531, doi: 10.1016/j.cell.2012.12.031 (2013).
26. Sobko, A. A., Kotova, E. A., Antonenko, Y. N., Zakharov, S. D. & Cramer, W. A. Effect of lipids with different spontaneous curvature on the channel activity of colicin E1: evidence in favor of A toroidal pore. FEBS Lett. 576, 205-210 (2004).
27. Tilley, S. J. & Saibil, H. R. The mechanism of pore formation by bacterial toxins. Curr. Opin. Struct. Biol. 16, 230-236 (2006).
28. Kuwana, T. et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 17, 525-535 (2005).
29. Grosse, L. et al. Bax assembles into large ring-like structures remodeling the mitochondrial outer membrane in apoptosis. EMBO J 35, 402-413, doi: 10.15252/embj.201592789 (2016).
30. Salvador-Gallego, R. et al. Bax assembly into rings and arcs in apoptotic mitochondria is linked to membrane pores. EMBO J 35, 389-401, doi: 10.15252/embj.201593384 (2016).
31. Tilley, S. J., Orlova, E. V., Gilbert, R. J., Andrew, P. W. & Saibil, H. R. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121, 247-256 (2005).
32. Chanturiya, A. N. et al. PB1-F2, an influenza A virus-encoded proapoptotic mitochondrial protein, creates variably sized pores in planar lipid membranes. J. Virol. 78, 6304-6312, doi: 10.1128/JVI.78.12.6304-6312.2004 (2004).
33. Qian, S., Wang, W., Yang, L. & Huang, H. W. Structure of transmembrane pore induced by Bax-derived peptide: evidence for lipidic pores. Proc Natl Acad Sci USA 105, 17379-17383 (2008).
34. Garcia-Saez, A. J., Chiantia, S., Salgado, J. & Schwille, P. Pore formation by A Bax-derived peptide: effect on the line tension of the membrane probed by AFM. Biophys. J. 93, 103-112 (2007).
35. Garcia-Saez, A. J. et al. Peptides corresponding to helices 5 and 6 of Bax can independently form large lipid pores. FEBS J. 273, 971-981, doi: 10.1111/j.1742-4658.2006.05123.x (2006).
36. Garcia-Saez, A. J. et al. Peptides derived from apoptotic Bax and Bid reproduce the poration activity of the parent full-length proteins. Biophys. J. 88, 3976-3990 (2005).
37. Basanez, G. et al. Bax-type apoptotic proteins porate pure lipid bilayers through A mechanism sensitive to intrinsic monolayer curvature. J. Biol. Chem. 277, 49360-49365, doi: 10.1074/jbc.M206069200 (2002).
38. Yandek, L. E., Pokorny, A. & Almeida, P. F. Wasp mastoparans follow the same mechanism as the cell-penetrating peptide transportan 10. Biochemistry 48, 7342-7351, doi: 10.1021/bi9008243 (2009).
39. Lee, M. T., Hung, W. C., Chen, F. Y. & Huang, H. W. Mechanism and kinetics of pore formation in membranes by water-soluble amphipathic peptides. Proc Natl Acad Sci USA 105, 5087-5092, doi: 10.1073/pnas.0710625105 (2008).
40. Sun, T. L., Sun, Y., Lee, C. C. & Huang, H. W. Membrane permeability of hydrocarbon-cross-linked peptides. Biophys. J. 104, 1923-1932, doi: 10.1016/j.bpj.2013.03.039 (2013).
41. Leontiadou, H., Mark, A. E. & Marrink, S. J. Antimicrobial peptides in action. J. Am. Chem. Soc. 128, 12156-12161, doi: 10.1021/ja062927q (2006).
42. Matsuzaki, K., Yoneyama, S., Murase, O. & Miyajima, K. Transbilayer transport of ions and lipids coupled with mastoparan X translocation. Biochemistry 35, 8450-8456, doi: 10.1021/bi960342a (1996).
43. Tamba, Y. & Yamazaki, M. Single giant unilamellar vesicle method reveals effect of antimicrobial peptide magainin 2 on membrane permeability. Biochemistry 44, 15823-15833, doi: 10.1021/bi051684w (2005).
44. Matsuzaki, K. et al. Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 37, 11856-11863, doi: 10.1021/bi980539y (1998).
45. Gregory, S. M., Pokorny, A. & Almeida, P. F. Magainin 2 revisited: A test of the quantitative model for the all-or-none permeabilization of phospholipid vesicles. Biophys. J. 96, 116-131, doi: 10.1016/j.bpj.2008.09.017 (2009).
46. Marassi, F. M. The discreet charm of the curve. Biophys. J. 104, 1215-1216, doi: 10.1016/j.bpj.2013.01.046 (2013).
47. Lee, M. T., Sun, T. L., Hung, W. C. & Huang, H. W. Process of inducing pores in membranes by melittin. Proc Natl Acad Sci USA 110, 14243-14248, doi: 10.1073/pnas.1307010110 (2013).
48. Weber, K., Harper, N., Schwabe, J. & Cohen, G. M. BIM-mediated membrane insertion of the BAK pore domain is an essential requirement for apoptosis. Cell Rep 5, 409-420, doi: 10.1016/j.celrep.2013.09.010 (2013).
49. Basanez, G. et al. Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad Sci USA 96, 5492-5497 (1999).
50. Martinez-Caballero, S. et al. Assembly of the mitochondrial apoptosis-induced channel, MAC. J. Biol. Chem. 284, 12235-12245 (2009).
51. Han, M., Mei, Y., Khant, H. & Ludtke, S. J. Characterization of antibiotic peptide pores using cryo-EM and comparison to neutron scattering. Biophys. J. 97, 164-172, doi: 10.1016/j.bpj.2009.04.039 (2009).
52. Henriksen, J. R. & Andresen, T. L. Thermodynamic profiling of peptide membrane interactions by isothermal titration calorimetry: A search for pores and micelles. Biophys. J. 101, 100-109, doi: 10.1016/j.bpj.2011.05.047 (2011).
53. Parker, M. W., Postma, J. P., Pattus, F., Tucker, A. D. & Tsernoglou, D. Refined structure of the pore-forming domain of colicin A at 2.4 A resolution. J. Mol. Biol. 224, 639-657 (1992).
54. Sharpe, J. C. & London, E. Diphtheria toxin forms pores of different sizes depending on its concentration in membranes: probable relationship to oligomerization. J. Membr. Biol. 171, 209-221 (1999).
55. Muchmore, S. W. et al. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381, 335-341, doi: 10.1038/381335a0 (1996).
56. McDonnell, J. M., Fushman, D., Milliman, C. L., Korsmeyer, S. J. & Cowburn, D. Solution structure of the proapoptotic molecule BID: A structural basis for apoptotic agonists and antagonists. Cell 96, 625-634 (1999).
57. Suzuki, M., Youle, R. J. & Tjandra, N. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103, 645-654 (2000).
58. Bleicken, S. et al. Molecular details of Bax activation, oligomerization, and membrane insertion. J. Biol. Chem. 285, 6636-6647, doi: 10.1074/jbc.M109.081539 (2010).
59. Zhang, Z. et al. BH3-in-groove dimerization initiates and helix 9 dimerization expands Bax pore assembly in membranes. EMBO J 35, 208-236, doi: 10.15252/embj.201591552 (2016).
60. Tait, S. W. et al. Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev. Cell 18, 802-813, doi: 10.1016/j.devcel.2010.03.014 (2010).
61. Ichim, G. et al. Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death. Mol. Cell 57, 860-872, doi: 10.1016/j.molcel.2015.01.018 (2015).
62. von Ahsen, O. et al. Preservation of mitochondrial structure and function after Bid-or Bax-mediated cytochrome c release. J. Cell Biol. 150, 1027-1036 (2000).
63. Baker, T. S., Olson, N. H. & Fuller, S. D. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Micro Biol Mol Biol Rev 63, 862-922 (1999).
64. Nechushtan, A., Smith, C. L., Hsu, Y. T. & Youle, R. J. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J. 18, 2330-2341 (1999).