Bak Core and Latch Domains Separate during Activation, and Freed Core Domains Form Symmetric Homodimers

Molecular Cell

Volumn 55, Issue 6, 2014, Pages 938-946

  Brouwer, Jason M ^a,b   Westphal, Dana ^a,b   Dewson, Grant ^a,b   Robin, Adeline Y ^a,b   Uren, Rachel T ^a,b   Bartolo, Ray ^a   Thompson, Geoff V ^a   Colman, Peter M ^a,b   Kluck, Ruth M ^a,b   Czabotar, Peter E ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; HOMODIMER; PROTEIN BAK; PROTEIN BAX; BAX PROTEIN (53 86); BAX PROTEIN (53-86); ONCOPROTEIN; PEPTIDE FRAGMENT;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; OLIGOMERIZATION; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN STRUCTURE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLOGRAPHY; HUMAN; METABOLISM; MITOCHONDRION; MOUSE; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CRYSTALLOGRAPHY; CYSTEINE; HUMANS; MICE; MITOCHONDRIA; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS;

EID: 84907994244     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.07.016     Document Type: Article

References (42)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Aluvila S., Mandal T., Hustedt E., Fajer P., Choe J.Y., Oh K.J. Organization of the mitochondrial apoptotic BAK pore: oligomerization of the BAK homodimers. J.Biol. Chem. 2014, 289:2537-2551.
3. Bleicken S., Landeta O., Landajuela A., Basañez G., García-Sáez A.J. Proapoptotic Bax and Bak proteins form stable protein-permeable pores of tunable size. J.Biol. Chem. 2013, 288:33241-33252.
4. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Sharff, A., Smart, O., Vonrhein, C. & Womack, T. (2011). BUSTER, Version 2.10.0 Ed., Global Phasing Ltd., Cambridge, UK.
5. Czabotar P.E., Lee E.F., van Delft M.F., Day C.L., Smith B.J., Huang D.C., Fairlie W.D., Hinds M.G., Colman P.M. Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc. Natl. Acad. Sci. USA 2007, 104:6217-6222.
6. Czabotar P.E., Lee E.F., Thompson G.V., Wardak A.Z., Fairlie W.D., Colman P.M. Mutation to Bax beyond the BH3 domain disrupts interactions with pro-survival proteins and promotes apoptosis. J.Biol. Chem. 2011, 286:7123-7131.
7. 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., et al. Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 2013, 152:519-531.
8. 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. 2014, 15:49-63.
9. Dai H., Smith A., Meng X.W., Schneider P.A., Pang Y.P., Kaufmann S.H. Transient binding of an activator BH3 domain to the Bak BH3-binding groove initiates Bak oligomerization. J.Cell Biol. 2011, 194:39-48.
10. Dai H., Pang Y.P., Ramirez-Alvarado M., Kaufmann S.H. Evaluation of the BH3-only protein Puma as a direct Bak activator. J.Biol. Chem. 2014, 289:89-99.
11. Dewson G., Kratina T., Sim H.W., Puthalakath H., Adams J.M., Colman P.M., Kluck R.M. To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol. Cell 2008, 30:369-380.
12. Dewson G., Kratina T., Czabotar P., Day C.L., Adams J.M., Kluck R.M. Bak activation for apoptosis involves oligomerization of dimers via their alpha6 helices. Mol. Cell 2009, 36:696-703.
13. Dewson G., Ma S., Frederick P., Hockings C., Tan I., Kratina T., Kluck R.M. Bax dimerizes via a symmetric BH3:groove interface during apoptosis. Cell Death Differ. 2012, 19:661-670.
14. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
15. Epand R.F., Martinou J.C., Montessuit S., Epand R.M. Transbilayer lipid diffusion promoted by Bax: implications for apoptosis. Biochemistry 2003, 42:14576-14582.
16. George N.M., Evans J.J., Luo X. A three-helix homo-oligomerization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax. Genes Dev. 2007, 21:1937-1948.
17. Griffiths G.J., Dubrez L., Morgan C.P., Jones N.A., Whitehouse J., Corfe B.M., Dive C., Hickman J.A. Cell damage-induced conformational changes of the pro-apoptotic protein Bak invivo precede the onset of apoptosis. J.Cell Biol. 1999, 144:903-914.
18. Kabsch W. Xds. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:125-132.
19. Karplus P.A., Diederichs K. Linking crystallographic model and data quality. Science 2012, 336:1030-1033.
20. Knudson C.M., Tung K.S., Tourtellotte W.G., Brown G.A., Korsmeyer S.J. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 1995, 270:96-99.
21. Ku B., Liang C., Jung J.U., Oh B.H. Evidence that inhibition of BAX activation by BCL-2 involves its tight and preferential interaction with the BH3 domain of BAX. Cell Res. 2011, 21:627-641.
22. Kvansakul M., Yang H., Fairlie W.D., Czabotar P.E., Fischer S.F., Perugini M.A., Huang D.C., Colman P.M. 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. 2008, 15:1564-1571.
23. Leshchiner E.S., Braun C.R., Bird G.H., Walensky L.D. Direct activation of full-length proapoptotic BAK. Proc. Natl. Acad. Sci. USA 2013, 110:E986-E995.
24. Letai A., Bassik M.C., Walensky L.D., Sorcinelli M.D., Weiler S., Korsmeyer S.J. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002, 2:183-192.
25. Lindsten T., Ross A.J., King A., Zong W.X., Rathmell J.C., Shiels H.A., Ulrich E., Waymire K.G., Mahar P., Frauwirth K., et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell 2000, 6:1389-1399.
26. Liu X., Dai S., Zhu Y., Marrack P., Kappler J.W. The structure of a Bcl-xL/Bim fragment complex: implications for Bim function. Immunity 2003, 19:341-352.
27. Llambi F., Moldoveanu T., Tait S.W., Bouchier-Hayes L., Temirov J., McCormick L.L., Dillon C.P., Green D.R. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol. Cell 2011, 44:517-531.
28. Ma S., Hockings C., Anwari K., Kratina T., Fennell S., Lazarou M., Ryan M.T., Kluck R.M., Dewson G. Assembly of the Bak apoptotic pore: a critical role for the Bak protein α6 helix in the multimerization of homodimers during apoptosis. J.Biol. Chem. 2013, 288:26027-26038.
29. Matsuzaki K., Sugishita K., Ishibe N., Ueha M., Nakata S., Miyajima K., Epand R.M. Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 1998, 37:11856-11863.
30. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J.Appl. Cryst. 2007, 40:658-674.
31. Moldoveanu T., Liu Q., Tocilj A., Watson M., Shore G., Gehring K. The X-ray structure of a BAK homodimer reveals an inhibitory zinc binding site. Mol. Cell 2006, 24:677-688.
32. Moldoveanu T., Grace C.R., Llambi F., Nourse A., Fitzgerald P., Gehring K., Kriwacki R.W., Green D.R. BID-induced structural changes in BAK promote apoptosis. Nat. Struct. Mol. Biol. 2013, 20:589-597.
33. Muchmore S.W., Sattler M., Liang H., Meadows R.P., Harlan J.E., Yoon H.S., Nettesheim D., Chang B.S., Thompson C.B., Wong S.L., et al. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 1996, 381:335-341.
34. Oh K.J., Singh P., Lee K., Foss K., Lee S., Park M., Lee S., Aluvila S., Park M., Singh P., et al. 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. 2010, 285:28924-28937.
35. Ruffolo S.C., Shore G.C. BCL-2 selectively interacts with the BID-induced open conformer of BAK, inhibiting BAK auto-oligomerization. J.Biol. Chem. 2003, 278:25039-25045.
36. Sarosiek K.A., Chi X., Bachman J.A., Sims J.J., Montero J., Patel L., Flanagan A., Andrews D.W., Sorger P., Letai A. BID preferentially activates BAK while BIM preferentially activates BAX, affecting chemotherapy response. Mol. Cell 2013, 51:751-765.
37. Sattler M., Liang H., Nettesheim D., Meadows R.P., Harlan J.E., Eberstadt M., Yoon H.S., Shuker S.B., Chang B.S., Minn A.J., et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 1997, 275:983-986.
38. Suzuki M., Youle R.J., Tjandra N. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 2000, 103:645-654.
39. Terrones O., Antonsson B., Yamaguchi H., Wang H.G., Liu J., Lee R.M., Herrmann A., Basañez G. Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J.Biol. Chem. 2004, 279:30081-30091.
40. 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 2013, 5:409-420.
41. 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., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
42. Willis S.N., Chen L., Dewson G., Wei A., Naik E., Fletcher J.I., Adams J.M., Huang D.C. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 2005, 19:1294-1305.