Conformational Heterogeneity of Bax Helix 9 Dimer for Apoptotic Pore Formation

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Liao, Chenyi ^a   Zhang, Zhi ^b   Kale, Justin ^c,d   Andrews, David W ^a,c,d   Lin, Jialing ^b,e   Li, Jianing ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

^e Stephenson Cancer Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAK1 PROTEIN, HUMAN; BAX PROTEIN, HUMAN; DISULFIDE; LIPID; PROTEIN BAK; PROTEIN BAX;

APOPTOSIS; CHEMISTRY; COMPUTER SIMULATION; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR DYNAMICS; PHYSIOLOGY; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

AMINO ACID MOTIFS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; COMPUTER SIMULATION; DISULFIDES; HUMANS; LIPIDS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MOLECULAR DYNAMICS SIMULATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84978152191     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29502     Document Type: Article

References (36)

1. Westphal, D., Kluck, R. M. & Dewson, G. Building blocks of the apoptotic pore: how Bax and Bak are activated and oligomerize during apoptosis. Cell Death Differ. 21, 196-205 (2014).
2. Moldoveanu, T., Follis, A. V., Kriwacki, R. W. & Green, D. R. Many players in BCL-2 family affairs. Trends Biochem. Sci 39, 101-111 (2014).
3. Chi, X. K., Kale, J., Leber, B. & Andrews, D. W. Regulating cell death at, on, and in membranes. Biochim. Biophys. Acta, Mol. Cell Res. 1843, 2100-2113 (2014).
4. Robin, A. Y. et al. Crystal structure of Bax bound to the BH3 peptide of Bim identifies important contacts for interaction. Cell Death Dis. 6, e1809 (2015).
5. 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 (2010).
6. Gavathiotis, E. et al. BAX activation is initiated at a novel interaction site. Nature 455, 1076-1081 (2008).
7. 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).
8. 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 (2013).
9. Westphal, D., Dewson, G., Czabotar, P. E. & Kluck, R. M. Molecular biology of Bax and Bak activation and action. Biochim. Biophys. Acta, Mol. Cell Res. 1813, 521-531 (2011).
10. Gahl, R. F., He, Y., Yu, S. Q. & Tjandra, N. Conformational rearrangements in the pro-apoptotic protein, Bax, as it inserts into mitochondria a cellular death switch. J. Biol. Chem. 289, 32871-32882 (2014).
11. Suzuki, M., Youle, R. J. & Tjandra, N. Structure of Bax: Coregulation of dimer formation and intracellular localization. Cell 103, 645-654 (2000).
12. Zhang, Z. et al. BH3-in-groove dimerization initiates and helix 9 dimerization expands Bax pore assembly in membranes. EMBO J. 35, 208-236 (2016).
13. Iyer, S. et al. Bak apoptotic pores involve a flexible C-terminal region and juxtaposition of the C-terminal transmembrane domains. Cell Death Differ. 22, 1665-1675 (2015).
14. Tsai, C. J. et al. BAX-induced apoptosis can be initiated through a conformational selection mechanism. Structure 23, 139-148 (2015).
15. 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).
16. Mueller, B. K., Subramaniam, S. & Senes, A. A frequent, GxxxG-mediated, transmembrane association motif is optimized for the formation of interhelical C alpha-H hydrogen bonds. Proc. Natl. Acad. Sci. USA 111, E888-E895 (2014).
17. Cartron, P. F. et al. Distinct domains control the addressing and the insertion of Bax into mitochondria. J. Biol. Chem. 280, 10587-10598 (2005).
18. Renault, T. T. & Chipuk, J. E. Death upon a kiss: mitochondrial outer membrane composition and organelle communication govern sensitivity to BAK/BAX-dependent apoptosis. Chem. Biol. 21, 114-123 (2014).
19. Renault, T. T. et al. Mitochondrial shape governs BAX-induced membrane permeabilization and apoptosis. Mol. Cell 57, 69-82 (2015).
20. Mancinelli, F., Caraglia, M., Budillon, A., Abbruzzese, A. & Bismuto, E. Molecular dynamics simulation and automated docking of the pro-apoptotic Bax protein and its complex with a peptide designed from the Bax-binding domain of anti-apoptotic Ku70. J. Cell. Biochem. 99, 305-318 (2006).
21. Koshy, C., Parthiban, M. & Sowdhamini, R. 100 ns molecular dynamics simulations to study intramolecular conformational changes in Bax. J. Biomol. Struct. Dyn. 28, 71-83 (2010).
22. Rosas-Trigueros, J. L., Correa-Basurto, J., Benitez-Cardoza, C. G. & Zamorano-Carrillo, A. Insights into the structural stability of Bax from molecular dynamics simulations at high temperatures. Protein Sci. 20, 2035-2046 (2011).
23. Liao, C. Y. et al. Melittin aggregation in aqueous solutions: insight from molecular dynamics simulations. J. Phys. Chem. B 119, 10390-10398 (2015).
24. Klocek, G., Schulthess, T., Shai, Y. & Seelig, J. Thermodynamics of melittin binding to lipid bilayers. aggregation and pore formation. Biochemistry 48, 2586-2596 (2009).
25. Kuwana, T. et al. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342 (2002).
26. Shamas-Din, A. et al. Distinct lipid effects on tBid and Bim activation of membrane permeabilization by pro-apoptotic Bax. Biochem. J 467, 495-505 (2015).
27. Ausili, A., de Godos, A., Torrecillas, A., Corbalán-García, S. & Gómez-Fernández, J. C. The interaction of the Bax C-terminal domain with membranes is influenced by the presence of negatively charged phospholipids. Biochim. Biophys. Acta, Biomembr. 1788, 1924-1932 (2009).
28. Lucken-Ardjomande, S., Montessuit, S. & Martinou, J. C. Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane. Cell Death Differ. 15, 929-937 (2008).
29. Xin, M. et al. Small-molecule Bax agonists for cancer therapy. Nat. Commun. 5, 4935 (2014).
30. Jo, S., Kim, T., Iyer, V. G. & Im, W. CHARMM-GUI: a web-based graphical user interface for CHARMM. J. Comput. Chem. 29, 1859-1865 (2008).
31. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).
32. Klauda, J. B. et al. Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J. Phys. Chem. B 114, 7830-7843 (2010).
33. Iannuzzi, M., Laio, A. & Parrinello, M. Efficient exploration of reactive potential energy surfaces using Car-Parrinello molecular dynamics. Phys. Rev. Lett. 90 (2003).
34. Laio, A. & Parrinello, M. Escaping free-energy minima. Proc. Natl. Acad. Sci. USA 99, 12562-12566 (2002).
35. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. Model. 14, 33-38 (1996).
36. Klauda, J. B., Brooks, B. R. & Pastor, R. W. Dynamical motions of lipids and a finite size effect in simulations of bilayers. J. Chem. Phys. 125, 144710 (2006).