Inhibition of Pro-Apoptotic BAX by a Noncanonical Interaction Mechanism

Molecular Cell

Volumn 57, Issue 5, 2015, Pages 873-886

  Barclay, Lauren A ^a   Wales, Thomas E ^b   Garner, Thomas P ^c   Wachter, Franziska ^a   Lee, Susan ^a   Guerra, Rachel M ^a   Stewart, Michelle L ^a   Braun, Craig R ^a   Bird, Gregory H ^a   Gavathiotis, Evripidis ^c   Engen, John R ^b   Walensky, Loren D ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BAX; PROTEIN BCL 2; BAX PROTEIN, HUMAN; PROTEIN BINDING;

ALPHA HELIX; AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; FEMALE; HELA CELL LINE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; HUMAN CELL; HYDROGEN BOND; IMMUNOPRECIPITATION; MASS SPECTROMETRY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROCEDURES; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BINDING SITES; DEUTERIUM EXCHANGE MEASUREMENT; HELA CELLS; HUMANS; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84924044826     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.01.014     Document Type: Article

References (36)

1. Bird G.H., Bernal F., Pitter K., Walensky L.D. Synthesis and biophysical characterization of stabilized alpha-helices of BCL-2 domains. Methods Enzymol. 2008, 446:369-386.
2. Braun C.R., Mintseris J., Gavathiotis E., Bird G.H., Gygi S.P., Walensky L.D. Photoreactive stapled BH3 peptides to dissect the BCL-2 family interactome. Chem. Biol. 2010, 17:1325-1333.
3. 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.
4. Ding J., Mooers B.H., Zhang Z., Kale J., Falcone D., McNichol J., Huang B., Zhang X.C., Xing C., Andrews D.W., Lin J. After embedding in membranes antiapoptotic Bcl-XL protein binds both Bcl-2 homology region 3 and helix 1 of proapoptotic Bax protein to inhibit apoptotic mitochondrial permeabilization. J.Biol. Chem. 2014, 289:11873-11896.
5. Dlugosz P.J., Billen L.P., Annis M.G., Zhu W., Zhang Z., Lin J., Leber B., Andrews D.W. Bcl-2 changes conformation to inhibit Bax oligomerization. EMBO J. 2006, 25:2287-2296.
6. Donnini S., Solito R., Monti M., Balduini W., Carloni S., Cimino M., Bampton E.T., Pinon L.G., Nicotera P., Thorpe P.E., Ziche M. Prevention of ischemic brain injury by treatment with the membrane penetrating apoptosis inhibitor, TAT-BH4. Cell Cycle 2009, 8:1271-1278.
7. Edlich F., Banerjee S., Suzuki M., Cleland M.M., Arnoult D., Wang C., Neutzner A., Tjandra N., Youle R.J. Bcl-x(L) retrotranslocates Bax from the mitochondria into the cytosol. Cell 2011, 145:104-116.
8. Edwards A.L., Gavathiotis E., LaBelle J.L., Braun C.R., Opoku-Nsiah K.A., Bird G.H., Walensky L.D. Multimodal interaction with BCL-2 family proteins underlies the proapoptotic activity of PUMA BH3. Chem. Biol. 2013, 20:888-902.
9. Eng J.K., McCormack A.L., Yates J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J.Am. Soc. Mass Spectrom. 1994, 5:976-989.
10. Engen J.R. Analysis of protein complexes with hydrogen exchange and mass spectrometry. Analyst (Lond.) 2003, 128:623-628.
11. Engen J.R. Analysis of protein conformation and dynamics by hydrogen/deuterium exchange MS. Anal. Chem. 2009, 81:7870-7875.
12. Gavathiotis E., Suzuki M., Davis M.L., Pitter K., Bird G.H., Katz S.G., Tu H.-C., Kim H., Cheng E.H.-Y., Tjandra N., Walensky L.D. BAX activation is initiated at a novel interaction site. Nature 2008, 455:1076-1081.
13. 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 2010, 40:481-492.
14. Hirotani M., Zhang Y., Fujita N., Naito M., Tsuruo T. NH2-terminal BH4 domain of Bcl-2 is functional for heterodimerization with Bax and inhibition of apoptosis. J.Biol. Chem. 1999, 274:20415-20420.
15. Hotchkiss R.S., McConnell K.W., Bullok K., Davis C.G., Chang K.C., Schwulst S.J., Dunne J.C., Dietz G.P.H., Bähr M., McDunn J.E., et al. TAT-BH4 and TAT-Bcl-xL peptides protect against sepsis-induced lymphocyte apoptosis invivo. J.Immunol. 2006, 176:5471-5477.
16. Hsu Y.T., Youle R.J. Nonionic detergents induce dimerization among members of the Bcl-2 family. J.Biol. Chem. 1997, 272:13829-13834.
17. Huang D.C., Adams J.M., Cory S. The conserved N-terminal BH4 domain of Bcl-2 homologues is essential for inhibition of apoptosis and interaction with CED-4. EMBO J. 1998, 17:1029-1039.
18. Kim P.K., Annis M.G., Dlugosz P.J., Leber B., Andrews D.W. During apoptosis bcl-2 changes membrane topology at both the endoplasmic reticulum and mitochondria. Mol. Cell 2004, 14:523-529.
19. Leber B., Lin J., Andrews D.W. Still embedded together binding to membranes regulates Bcl-2 protein interactions. Oncogene 2010, 29:5221-5230.
20. Lee L.C., Hunter J.J., Mujeeb A., Turck C., Parslow T.G. Evidence for α-helical conformation of an essential N-terminal region in the human Bcl2 protein. J.Biol. Chem. 1996, 271:23284-23288.
21. 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.
22. Lovell J.F., Billen L.P., Bindner S., Shamas-Din A., Fradin C., Leber B., Andrews D.W. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 2008, 135:1074-1084.
23. Ma J., Edlich F., Bermejo G.A., Norris K.L., Youle R.J., Tjandra N. Structural mechanism of Bax inhibition by cytomegalovirus protein vMIA. Proc. Natl. Acad. Sci. USA 2012, 109:20901-20906.
24. Ma P., Schwarten M., Schneider L., Boeske A., Henke N., Lisak D., Weber S., Mohrlüder J., Stoldt M., Strodel B., et al. Interaction of Bcl-2 with the autophagy-related GABAA receptor-associated protein (GABARAP): biophysical characterization and functional implications. J.Biol. Chem. 2013, 288:37204-37215.
25. Marintchev A., Frueh D., Wagner G. NMR methods for studying protein-protein interactions involved in translation initiation. Methods Enzymol. 2007, 430:283-331.
26. Monaco G., Decrock E., Nuyts K., Wagner L.E., Luyten T., Strelkov S.V., Missiaen L., De Borggraeve W.M., Leybaert L., Yule D.I., et al. α-helical destabilization of the Bcl-2-BH4-domain peptide abolishes its ability to inhibit the IP3 receptor. PLoS ONE 2013, 8:e73386.
27. Pagliari L.J., Kuwana T., Bonzon C., Newmeyer D.D., Tu S., Beere H.M., Green D.R. The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc. Natl. Acad. Sci. USA 2005, 102:17975-17980.
28. Petros A.M., Medek A., Nettesheim D.G., Kim D.H., Yoon H.S., Swift K., Matayoshi E.D., Oltersdorf T., Fesik S.W. Solution structure of the antiapoptotic protein bcl-2. Proc. Natl. Acad. Sci. USA 2001, 98:3012-3017.
29. 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.
30. Shi X.E., Wales T.E., Elkin C., Kawahata N., Engen J.R., Annis D.A. Hydrogen exchange-mass spectrometry measures stapled peptide conformational dynamics and predicts pharmacokinetic properties. Anal. Chem. 2013, 85:11185-11188.
31. Souers A.J., Leverson J.D., Boghaert E.R., Ackler S.L., Catron N.D., Chen J., Dayton B.D., Ding H., Enschede S.H., Fairbrother W.J., et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 2013, 19:202-208.
32. Sugioka R., Shimizu S., Funatsu T., Tamagawa H., Sawa Y., Kawakami T., Tsujimoto Y. BH4-domain peptide from Bcl-xL exerts anti-apoptotic activity invivo. Oncogene 2003, 22:8432-8440.
33. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas M., Ulrich E.L., Markley J.L., Ionides J., Laue E.D. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 2005, 59:687-696.
34. Walensky L.D., Bird G.H. Hydrocarbon-stapled peptides: principles, practice, and progress. J.Med. Chem. 2014, 57:6275-6288.
35. Walensky L.D., Pitter K., Morash J., Oh K.J., Barbuto S., Fisher J., Smith E., Verdine G.L., Korsmeyer S.J. A stapled BID BH3 helix directly binds and activates BAX. Mol. Cell 2006, 24:199-210.
36. Wang K., Gross A., Waksman G., Korsmeyer S.J. Mutagenesis of the BH3 domain of BAX identifies residues critical for dimerization and killing. Mol. Cell. Biol. 1998, 18:6083-6089.