TBid undergoes multiple conformational changes at the membrane required for bax activation

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 22111-22127

  Shamas Din, Aisha ^a   Bindner, Scott ^a   Zhu, Weijia ^a   Zaltsman, Yehudit ^a   Campbell, Clinton ^a   Gross, Atan ^a   Leber, Brian ^a,b   Andrews, David W ^a   Fradin, Cecile ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BAX ACTIVATION; BCL-2 FAMILY PROTEINS; CONFORMATIONAL CHANGE; MEMBRANE-BOUND; POTENTIAL SITES;

BIOCHEMISTRY; BIOLOGY;

CELL DEATH;

CELL PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN MTCH2; PROTEIN P7; PROTEIN TBID; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PERMEABILIZATION; CONTROLLED STUDY; DOWN REGULATION; IN VITRO STUDY; MEMBRANE BINDING; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

APOPTOSIS; BAX; BCL-2 PROTEINS; BID; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER (FRET); FLUORESCENCE SPECTROSCOPY; MTCH2; PROTEIN CONFORMATION; TBID;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CASPASE 8; CELL MEMBRANE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; KINETICS; LIPOSOMES; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; PERMEABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; TIME FACTORS;

EID: 84881252568     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.482109     Document Type: Article

References (47)

1. Adams, J. M. (2003) Ways of dying. Multiple pathways to apoptosis. Genes Dev. 17, 2481-2495
2. Wang, X. (2001) The expanding role of mitochondria in apoptosis. Genes Dev. 15, 2922-2933
3. Leber, B., Lin, J., and Andrews, D. W. (2010) Still embedded together binding to membranes regulates Bcl-2 protein interactions. Oncogene 29, 5221-5230
4. Shamas-Din, A., Kale, J., Leber, B., and Andrews, D. W. (2013) Mechanisms of action of bcl-2 family proteins. Cold Spring Harb. Perspect. Biol. 5, a008714
5. Hardwick, J. M., and Youle, R. J. (2009) SnapShot. BCL-2 proteins. Cell 138, 404
6. Kvansakul, M., Yang, H., Fairlie, W. D., Czabotar, P. E., Fischer, S. F., Perugini, M. A., Huang, D. C., and Colman, P. M. (2008) 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. 15, 1564-1571
7. 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
8. Annis, M. G., Soucie, E. L., Dlugosz, P. J., Cruz-Aguado, J. A., Penn, L. Z., Leber, B., and Andrews, D. W. (2005) Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J. 24, 2096-2103
9. Wei, M. C., Lindsten, T., Mootha, V. K., Weiler, S., Gross, A., Ashiya, M., Thompson, C. B., and Korsmeyer, S. J. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14, 2060-2071
10. 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
11. Lovell, J. F., Billen, L. P., Bindner, S., Shamas-Din, A., Fradin, C., Leber, B., and Andrews, D. W. (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135, 1074-1084
12. Yethon, J. A., Epand, R. F., Leber, B., Epand, R. M., and Andrews, D. W. (2003) Interaction with a membrane surface triggers a reversible conformational change in Bax normally associated with induction of apoptosis. J. Biol. Chem. 278, 48935-48941
13. Kim, P. K., Annis, M. G., Dlugosz, P. J., Leber, B., and Andrews, D. W. (2004) During apoptosis Bcl-2 changes membrane topology at both the endoplasmic reticulum and mitochondria. Mol. Cell 14, 523-529
14. Peng, J., Tan, C., Roberts, G. J., Nikolaeva, O., Zhang, Z., Lapolla, S. M., Primorac, S., Andrews, D. W., and Lin, J. (2006) tBid elicits a conformational alteration in membrane-bound Bcl-2 such that it inhibits Bax pore formation. J. Biol. Chem. 281, 35802-35811
15. Dlugosz, P. J., Billen, L. P., Annis, M. G., Zhu, W., Zhang, Z., Lin, J., Leber, B., and Andrews, D. W. (2006) Bcl-2 changes conformation to inhibit Bax oligomerization. EMBO J. 25, 2287-2296
16. Shamas-Din, A., Brahmbhatt, H., Leber, B., and Andrews, D. W. (2011) BH3-only proteins. Orchestrators of apoptosis. Biochim. Biophys. Acta 1813, 508-520
17. Yin, X. M., Wang, K., Gross, A., Zhao, Y., Zinkel, S., Klocke, B., Roth, K. A., and Korsmeyer, S. J. (1999) Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400, 886-891
18. Li, H., Zhu, H., Xu, C. J., and Yuan, J. (1998) Cleavage of BID by Caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501
19. 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
20. Gross, A., Yin, X. M., Wang, K., Wei, M. C., Jockel, J., Milliman, C., Erdjument-Bromage, H., Tempst, P., and Korsmeyer, S. J. (1999) Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274, 1156-1163
21. Chou, J. J., Li, H., Salvesen, G. S., Yuan, J., and Wagner, G. (1999) Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell 96, 615-624
22. Kudla, G., Montessuit, S., Eskes, R., Berrier, C., Martinou, J. C., Ghazi, A., and Antonsson, B. (2000) The destabilization of lipid membranes induced by the C-terminal fragment of Caspase 8-cleaved Bid is inhibited by the N-terminal fragment. J. Biol. Chem. 275, 22713-22718
23. Zha, J., Weiler, S., Oh, K. J., Wei, M. C., and Korsmeyer, S. J. (2000) Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 290, 1761-1765
24. Tan, K. O., Tan, K. M., and Yu, V. C. (1999) A novel BH3-like domain in BID is required for intramolecular interaction and autoinhibition of proapoptotic activity. J. Biol. Chem. 274, 23687-23690
25. Zaltsman, Y., Shachnai, L., Yivgi-Ohana, N., Schwarz, M., Maryanovich, M., Houtkooper, R. H., Vaz, F. M., De Leonardis, F., Fiermonte, G., Palmieri, F., Gillissen, B., Daniel, P. T., Jimenez, E., Walsh, S., Koehler, C. M., Roy, S. S., Walter, L., Hajnóczky, G., and Gross, A. (2010) MTCH2/MIMP is a major facilitator of tBID recruitment to mitochondria. Nat. Cell Biol. 12, 553-562
26. Robinson, A. J., Kunji, E. R., and Gross, A. (2012) Mitochondrial carrier homolog 2 (MTCH2). The recruitment and evolution of a mitochondrial carrier protein to a critical player in apoptosis. Exp. Cell Res. 318, 1316-1323
27. Suzuki, M., Youle, R. J., and Tjandra, N. (2000) Structure of Bax. Coregulation of dimer formation and intracellular localization. Cell 103, 645-654
28. 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., Ng, S. L., and Fesik, S. W. (1996) X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381, 335-341
29. Hinds, M. G., Smits, C., Fredericks-Short, R., Risk, J. M., Bailey, M., Huang, D. C., and Day, C. L. (2007) Bim, Bad and Bmf. Intrinsically unstructured BH3-only proteins that undergo a localized conformational change upon binding to prosurvival Bcl-2 targets. Cell Death Differ. 14, 128-136
30. McDonnell, J. M., Fushman, D., Milliman, C. L., Korsmeyer, S. J., and Cowburn, D. (1999) Solution structure of the proapoptotic molecule BID. Astructural basis for apoptotic agonists and antagonists. Cell 96, 625-634
31. Hu, X., Han, Z., Wyche, J. H., and Hendrickson, E. A. (2003) Helix 6 of tBid is necessary but not sufficient for mitochondrial binding activity. Apoptosis 8, 277-289
32. 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. J. Biol. Chem. 280, 753-767
33. Wang, K., Yin, X. M., Chao, D. T., Milliman, C. L., and Korsmeyer, S. J. (1996) BID. A novel BH3 domain-only death agonist. Genes Dev. 10, 2859-2869
34. Youle, R. J., and Strasser, A. (2008) The BCL-2 protein family. Opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59
35. Billen, L. P., Shamas-Din, A., and Andrews, D. W. (2008) Bid. A Bax-like BH3 protein. Oncogene 27, S93-S104
36. Polster, B. M., Basañez, G., Young, M., Suzuki, M., and Fiskum, G. (2003) Inhibition of Bax-induced cytochrome c release from neural cell and brain mitochondria by dibucaine and propranolol. J. Neurosci. 23, 2735-2743
37. Satsoura, D., Kučerka, N., Shivakumar, S., Pencer, J., Griffiths, C., Leber, B., Andrews, D. W., Katsaras, J., and Fradin, C. (2012) Interaction of the full-length Bax protein with biomimetic mitochondrial liposomes. A small-angle neutron scattering and fluorescence study. Biochim. Biophys. Acta 1818, 384-401
38. Billen, L. P., Kokoski, C. L., Lovell, J. F., Leber, B., and Andrews, D. W. (2008) Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol. 6, e147
39. Veresov, V. G., and Davidovskii, A. I. (2007) Monte Carlo simulations of tBid association with the mitochondrial outer membrane. Eur. Biophys. J. 37, 19-33
40. Yamaguchi, R., Andreyev, A., Murphy, A. N., Perkins, G. A., Ellisman, M. H., and Newmeyer, D. D. (2007) Mitochondria frozen with trehalose retain a number of biological functions and preserve outer membrane integrity. Cell Death Differ. 14, 616-624
41. Middleton, E. R., and Rhoades, E. (2010) Effects of curvature and composition on-synuclein binding to lipid vesicles. Biophys. J. 99, 2279-2288
42. Stankiewicz, A. R., Lachapelle, G., Foo, C. P., Radicioni, S. M., and Mosser, D. D. (2005) Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J. Biol. Chem. 280, 38729-38739
43. Hamilton, N. A., Pantelic, R. S., Hanson, K., and Teasdale, R. D. (2007) Fast automated cell phenotype image classification.BMCBioinformatics 8, 110
44. Berg, O. G., and von Hippel, P. H. (1985) Diffusion-controlled macromolecular interactions. Annu. Rev. Biophys. Biophys. Chem. 14, 131-160
45. Alder, N. N., Jensen, R. E., and Johnson, A. E. (2008) Fluorescence mapping of mitochondrial TIM23 complex reveals a water-facing, substrateinteracting helix surface. Cell 134, 439-450
46. Katz, C., Zaltsman-Amir, Y., Mostizky, Y., Kollet, N., Gross, A., and Friedler, A. (2012) Molecular basis of the interaction between proapoptotic truncated BID (tBID) protein and mitochondrial carrier homologue 2 (MTCH2) protein. Key players in mitochondrial death pathway. J. Biol. Chem. 287, 15016-15023
47. Liu, X., Dai, S., Zhu, Y., Marrack, P., and Kappler, J. W. (2003) The structure of a Bcl-xL/Bim fragment complex. Implications for Bim function. Immunity 19, 341-352