Organization of the mitochondrial apoptotic BAK pore: Oligomerization of the BAK homodimers

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 2537-2551

  Aluvila, Sreevidya ^a   Mandal, Tirtha ^a   Hustedt, Eric ^b   Fajer, Peter ^c   Choe, Jun Yong ^a   Oh, Kyoung Joon ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS; BAK; BAX; BCL-2; CELL DEATH; ELECTRON PARAMAGNETIC RESONANCE (EPR); MITOCHONDRIA; OLIGOMERIZATION INTERFACE; SPIN LABELING;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; DIMERIZATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; LIPOSOMES; MICE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PERMEABILITY; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84893480044     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.526806     Document Type: Article

References (42)

1. Danial, N. N., and Korsmeyer, S. J. (2004) Cell death. Critical control points. Cell 116, 205-219
2. Llambi, F., Moldoveanu, T., Tait, S. W., Bouchier-Hayes, L., Temirov, J., McCormick, L. L., Dillon, C. P., and Green, D. R. (2011) A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol. Cell 44, 517-531
3. Wei, M. C, Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., and Korsmeyer, S. J. (2001) Proapoptotic BAX and BAK. A requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730
4. Wolter, K. G., Hsu, Y. T., Smith, C. L., Nechushtan, A., Xi, X. G., and Youle, R. J. (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139, 1281-1292
5. Cheng, E. H, Sheiko, T. V., Fisher, J. K., Craigen, W. J., and Korsmeyer, S. J. (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301, 513-517
6. Czabotar, P. E., Westphal, D., Dewson, G., Ma, S., Hockings, C, Fairlie, W. D., Lee, E. F., Yao, S., Robin, A. Y., Smith, B. J., Huang, D. C, Kluck, R. M., Adams, J. M., and Colman, P. M. (2013) Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 152, 519-531
7. Dewson, G., Kratina, T., Czabotar, P., Day, C. L., Adams, J. M., and Kluck, R. M. (2009) Bak activation for apoptosis involves oligomerization of dimers via their a6 helices. Mol. Cell 36, 696-703
8. Dewson, G., Kratina, T., Sim, H. W., Puthalakath, H, Adams, J. M., Colman, P. M., and Kluck, R. M. (2008) To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol. Cell 30, 369-380
9. Saito, M., Korsmeyer, S. J., and Schlesinger, P. H. (2000) BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat. Cell Biol. 2, 553-555
10. Martinez-Caballero, S., Dejean, L. M., Kinnally, M. S., Oh, K. J., Mannella, C. A., and Kinnally, K. W. (2009) Assembly of the mitochondrial apoptosis-induced channel, MAC. J. Biol. Chem. 284, 12235-12245
11. Dewson, G., and Kluck, R. M. (2009) Mechanisms by which Bak and Bax permeabilise mitochondria during apoptosis. J. Cell Sci. 122, 2801-2808
12. Hubbell, W. L., Lopez, C. J., Altenbach, C, and Yang, Z. (2013) Technological advances in site-directed spin labeling of proteins. Curr. Opin. Struct. Biol. 23, 725-733
13. Oh, K. J., Singh, P., Lee, K., Foss, K., Lee, S., Park, M., Lee, S., Aluvila, S., Park, M., Singh, P., Kim, R. S., Symersky, J., and Walters, D. E. (2010) 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, 28924-28937
14. Oh, K. J., Barbuto, S., Meyer, N., Kim, R. S., Collier, R. J., and Korsmeyer, S. J. (2005) Conformational changes in BID, a pro-apoptotic BCL-2 family member, upon membrane binding. A site-directed spin labeling study. J. Biol. Chem. 280, 753-767
15. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490
16. Oh, K. J., Barbuto, S., Pitter, K., Morash, J., Walensky, L. D., and Korsmeyer, S. J. (2006) A membrane-targeted BID BCL-2 homology 3 peptide is sufficient for high potency activation of BAX in vitro. J. Biol. Chem. 281, 36999-37008
17. Lutter, M., Fang, M., Luo, X., Nishijima, M., Xie, X., and Wang, X. (2000) Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat Cell Biol. 2, 754-761
18. Ardail, D., Privat, J. P., Egret-Charlier, M., Levrat, C., Lerme, F., and Louisot, P. (1990) Mitochondrial contact sites. Lipid composition and dynamics. J. Biol. Chem. 265, 18797-18802
19. Terrones, O., Antonsson, B., Yamaguchi, H., Wang, H. G., Liu, J., Lee, R. M., Herrmann, A., and Basañez, G. (2004) Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J. Biol. Chem. 279, 30081-30091
20. Kuwana, T., Bouchier-Hayes, L., Chipuk, J. E., Bonzon, C., Sullivan, B. A., Green, D. R., and Newmeyer, D. D. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 17, 525-535
21. Kuwana, T., Mackey, M. R., Perkins, G., Ellisman, M. H., Latterich, M., Schneiter, R., Green, D. R., and Newmeyer, D. D. (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342
22. Böttcher, C. J. F., Van Gent, C. M., and Pries, C. (1961) Arapid and sensitive sub-micro phosphorus determination. Anal. Chim. Acta 24, 203-204
23. Rabenstein, M. D., and Shin, Y. K. (1995) Determination of the distance between two spin labels attached to a macromolecule. Proc. Natl. Acad. Sci. U. S. A. 92, 8239-8243
24. Altenbach, C., Oh, K. J., Trabanino, R. J., Hideg, K., and Hubbell, W. L. (2001) Estimation of inter-residue distances in spin labeled proteins at physiological temperatures. Experimental strategies and practical limitations. Biochemistry 40, 15471-15482
25. Pannier, M., Veit, S., Godt, A., Jeschke, G., and Spiess, H. W. (2000) Deadtime free measurement of dipole-dipole interactions between electron spins. J. Magn. Reson. 142, 331-340
26. Jeschke, G., Chechik, V., Ionita, P., Godt, A., Zimmermann, H., Banham, J., Timmel, C. R., Hilger, D., and Jung, H. (2006) DeerAnalysis2006 - a comprehensive software package for analyzing pulsed ELDOR data. Appl. Magn. Res. 30, 473-498
27. Sen, K. I., Logan, T. M., and Fajer, P. G. (2007) Protein dynamics and monomer-monomer interactions in AntR activation by electron paramagnetic resonance and double electron-electron resonance. Biochemistry 46, 11639-11649
28. Brandon, S., Beth, A. H., and Hustedt, E. J. (2012) The global analysis of DEER data. J. Magn. Reson. 218, 93-104
29. Hustedt, E. J., and Beth, A. H. (1999) Nitroxide spin-spin interactions. Applications to protein structure and dynamics. Annu. Rev. Biophys. Biomol. Struct. 28, 129-153
30. Hustedt, E. J., Smirnov, A. I., Laub, C. F., Cobb, C. E., and Beth, A. H. (1997) Molecular distances from dipolar coupled spin-labels. The global analysis of multifrequency continuous wave electron paramagnetic resonance data. Biophys. J. 72, 1861-1877
31. Hustedt, E. J., Stein, R. A., Sethaphong, L., Brandon, S., Zhou, Z., and Desensi, S. C. (2006) Dipolar coupling between nitroxide spin labels. The development and application of a tether-in-a-cone model. Biophys. J. 90, 340-356
32. Moldoveanu, T., Liu, Q., Tocilj, A., Watson, M., Shore, G., and Gehring, K. (2006) The x-ray structure of a BAK homodimer reveals an inhibitory zinc binding site. Mol. Cell 24, 677-688
33. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D 66, 486-501
34. Careaga, C. L., and Falke, J. J. (1992) Thermal motions of surface a-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping. J. Mol. Biol. 226, 1219-1235
35. Langen, R., Oh, K. J., Cascio, D., and Hubbell, W. L. (2000) Crystal structures of spin labeled T4 lysozyme mutants. Implications for the interpretation of EPR spectra in terms of structure. Biochemistry 39, 8396-8405
36. Fleissner, M. R., Bridges, M. D., Brooks, E. K., Cascio, D., Kalai, T., Hideg, K., and Hubbell, W. L. (2011) Structure and dynamics of a conformationally constrained nitroxide side chain and applications in EPR spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 108, 16241-16246
37. Kim, H., Tu, H. C, Ren, D., Takeuchi, O., Jeffers, J. R., Zambetti, G. P., Hsieh, J. J., and Cheng, E. H. (2009) Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol. Cell 36, 487-499
38. O'Neill, J. W., Manion, M. K., Maguire, B., and Hockenbery, D. M. (2006) BCL-XL dimerization by three-dimensional domain swapping. J. Mol. Biol. 356, 367-381
39. Ma, S., Hockings, C, Anwari, K., Kratina, T., Fennell, S., Lazarou, M., Ryan, M. T., Kluck, R. M., and Dewson, G. (2013) Assembly of the Bak Apoptotic Pore, A critical role for the BAK protein a6 helix in the multimerization of homodimers during apoptosis. J. Biol. Chem. 288, 26027-26038
40. Schafer, B., Quispe, J., Choudhary, V., Chipuk, J. E., Ajero, T. G., Du, H, Schneiter, R., and Kuwana, T. (2009) Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation. Mol. Biol. Cell 20, 2276-2285
41. Suzuki, M., Youle, R. J., and Tjandra, N. (2000) Structure of Bax. Coregulation of dimer formation and intracellular localization. Cell 103, 645-654
42. De Lano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA