Membrane promotes tBID interaction with BCL XL

Nature Structural and Molecular Biology

Volumn 16, Issue 11, 2009, Pages 1178-1185

  García Sáez, Ana J ^a   Ries, Jonas ^a   Orzáez, Mar ^b   Pérez Payà, Enrique ^b,c   Schwille, Petra ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^c INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID;

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; FLUORESCENCE CORRELATION SPECTROSCOPY; HUMAN; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

BCL-X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; HUMANS; MEMBRANES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SPECTROMETRY, FLUORESCENCE;

EID: 70350768995     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1671     Document Type: Article

References (53)

1. Kroemer, G., Galluzzi, L. & Brenner, C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99-163 (2007). (Pubitemid 46209992)
2. Danial, N.N. BCL-2 family proteins: critical checkpoints of apoptotic cell death. Clin. Cancer Res. 13, 7254-7263 (2007).
3. Youle, R.J. & Strasser, A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59 (2008).
4. 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).
5. Chipuk, J.E. et al. Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc. Natl. Acad. Sci. USA 105, 20327-20332 (2008).
6. Gross, A. et al. 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 (1999).
7. Chipuk, J.E. & Green, D.R. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18, 157-164 (2008).
8. Chen, L. et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol. Cell 17, 393-403 (2005).
9. Willis, S.N. et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 19, 1294-1305 (2005).
10. Willis, S.N. et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315, 856-859 (2007).
11. Kuwana, T. et al. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342 (2002).
12. Wei, M.C. et al. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14, 2060-2071 (2000).
13. Leber, B., Lin, J. & Andrews, D.W. Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 12, 897-911 (2007).
14. Kuwana, T. et al. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111, 331-342 (2002).
15. Terrones, O. et al. Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J. Biol. Chem. 279, 30081-30091 (2004).
16. Epand, R.F., Martinou, J.C., Fornallaz-Mulhauser, M., Hughes, D.W. & Epand, R.M. The apoptotic protein tBid promotes leakage by altering membrane curvature. J. Biol. Chem. 277, 32632-32639 (2002).
17. Esposti, M.D., Cristea, I.M., Gaskell, S.J., Nakao, Y. & Dive, C. Proapoptotic Bid binds to monolysocardiolipin, a new molecular connection between mitochondrial membranes and cell death. Cell Death Differ. 10, 1300-1309 (2003).
18. Gonzalvez, F., Bessoule, J.J., Rocchiccioli, F., Manon, S. & Petit, P.X. Role of cardiolipin on tBid and tBid/Bax synergistic effects on yeast mitochondria. Cell Death Differ. 12, 659-667 (2005).
19. Kim, T.H. et al. Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome C release. Mol. Biol. Cell 15, 3061-3072 (2004).
20. Liu, J., Weiss, A., Durrant, D., Chi, N.W. & Lee, R.M. The cardiolipin-binding domain of Bid affects mitochondrial respiration and enhances cytochrome c release. Apoptosis 9, 533-541 (2004).
21. Lutter, M., Perkins, G.A. & Wang, X. The pro-apoptotic Bcl-2 family member tBid localizes to mitochondrial contact sites. BMC Cell Biol. 2, 22 (2001).
22. Thuduppathy, G.R., Terrones, O., Craig, J.W., Basanez, G. & Hill, R.B. The N-Terminal Domain of Bcl-xL Reversibly Binds Membranes in a pH-Dependent Manner. Biochemistry 45, 14533-14542 (2006).
23. Peng, J. et al. tBid elicits a conformational alteration in membrane-bound Bcl-2 such that it inhibits Bax pore formation. J. Biol. Chem. 281, 35802-35811 (2006).
24. García-Sáez, A.J., Mingarro, I., Pérez-Payà, E. & Salgado, J. Membrane-insertion fragments of Bcl-xL, Bax, and Bid. Biochemistry 43, 10930-10943 (2004).
25. Schön, P. et al. Equinatoxin II permeabilizing activity depends on the presence of sphingomyelin and lipid phase coexistence. Biophys. J. 95, 691-698 (2008).
26. Tamba, Y. & Yamazaki, M. Single giant unilamellar vesicle method reveals effect of antimicrobial peptide magainin 2 on membrane permeability. Biochemistry 44, 15823-15833 (2005).
27. Bacia, K., Kim, S.A. & Schwille, P. Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods 3, 83-89 (2006).
28. Haustein, E. & Schwille, P. Single-molecule spectroscopic methods. Curr. Opin. Struct. Biol. 14, 531-540 (2004).
29. Ries, J. & Schwille, P. Studying slow membrane dynamics with continuous wave scanning fuorescence correlation spectroscopy. Biophys. J. 91, 1915-1924 (2006).
30. Certo, M. et al. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9, 351-365 (2006).
31. Letai, A. et al. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2, 183-192 (2002).
32. Dertinger, T. et al. Two-focus fuorescence correlation spectroscopy: a new tool for accurate and absolute diffusion measurements. ChemPhysChem 8, 433-443 (2007).
33. Petrásek, Z. & Schwille, P. Precise measurement of diffusion coeffcients using scanning fuorescence correlation spectroscopy. Biophys. J. 94, 1437-1448 (2008).
34. Saffman, P.G. & Delbruck, M. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA 72, 3111-3113 (1975).
35. Kahya, N. & Schwille, P. Fluorescence correlation studies of lipid domains in model membranes. Mol. Membr. Biol. 23, 29-39 (2006).
36. Petros, A.M. et al. Rationale for Bcl-xL/Bad peptide complex formation from structure, mutagenesis, and biophysical studies. Protein Sci. 9, 2528-2534 (2000).
37. Sattler, M. et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275, 983-986 (1997).
38. Oh, K.J. et al. A membrane-targeted BID BCL-2 homology 3 peptide is suffcient for high potency activation of BAX in vitro. J. Biol. Chem. 281, 36999-37008 (2006).
39. Billen, L.P., Kokoski, C.L., Lovell, J.F., Leber, B. & Andrews, D.W. Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol. 6, e147 (2008).
40. Hsu, Y.T., Wolter, K.G. & Youle, R.J. Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc. Natl. Acad. Sci. USA 94, 3668-3672 (1997).
41. Desagher, S. et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144, 891-901 (1999).
42. Yano, M., Terada, K., Gotoh, T. & Mori, M. In vitro analysis of Bcl-2 proteins in mitochondria and endoplasmic reticulum: Similarities in anti-apoptotic functions and differences in regulation. Exp. Cell Res. 313, 3767-3778 (2007).
43. White, C. et al. The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat. Cell Biol. 7, 1021-1028 (2005).
44. Gureasko, J. et al. Membrane-dependent signal integration by the Ras activator Son of sevenless. Nat. Struct. Mol. Biol. 15, 452-461 (2008).
45. Ye, J. & Esmon, C.T. Factor Xa-factor Va complex assembles in two dimensions with unexpectedly high affnity: an experimental and theoretical approach. Biochemistry 34, 6448-6453 (1995).
46. Melo, E. & Martins, J. Kinetics of bimolecular reactions in model bilayers and biological membranes. A critical review. Biophys. Chem. 123, 77-94 (2006).
47. Rajendran, L. et al. Effcient inhibition of the Alzheimer's disease beta-secretase by membrane targeting. Science 320, 520-523 (2008).
48. Chipuk, J.E. et al. Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc. Natl. Acad. Sci. USA (2008).
49. Nguyen, M. et al. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc. Natl. Acad. Sci. USA 104, 19512-19517 (2007).
50. Chou, J.J., Li, H., Salvesen, G.S., Yuan, J. & Wagner, G. Solution structure of BID, an intracellular amplifer of apoptotic signaling. Cell 96, 615-624 (1999).
51. Muchmore, S.W. et al. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381, 335-341 (1996).
52. Zha, J., Weiler, S., Oh, K.J., Wei, M.C. & Korsmeyer, S.J. Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 290, 1761-1765 (2000).
53. Yamaguchi, R. et al. Mitochondria frozen with trehalose retain a number of biological functions and preserve outer membrane integrity. Cell Death Differ. 14, 616-624 (2007)