The dynamics of bax channel formation: Influence of ionic strength

Biophysical Journal

Volumn 103, Issue 3, 2012, Pages 483-491

  Ganesan, Vidyaramanan ^a   Walsh, Timothy ^a   Chang, Kai Ti ^a   Colombini, Marco ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHLORIDE; PROTEIN BAX; PROTEIN BCL X; PROTEIN BID;

ANIMAL; ARTICLE; CELL MEMBRANE PERMEABILITY; DOSE RESPONSE; DRUG EFFECT; METABOLISM; MITOCHONDRIAL MEMBRANE; OSMOLARITY; RAT;

ANIMALS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CELL MEMBRANE PERMEABILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; MITOCHONDRIAL MEMBRANES; OSMOLAR CONCENTRATION; POTASSIUM CHLORIDE; RATS;

EID: 84864710153     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.06.047     Document Type: Article

References (52)

1. J.C. Reed, J.M. Jurgensmeier, and S. Matsuyama Bcl-2 family proteins and mitochondria Biochim. Biophys. Acta 1366 1998 127 137 (Pubitemid 28467027)
2. J.E. Chipuk, and D.R. Green How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18 2008 157 164
3. A. Antignani, and R.J. Youle How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr. Opin. Cell Biol. 18 2006 685 689 (Pubitemid 44692478)
4. A. Gross, J.M. McDonnell, and S.J. Korsmeyer BCL-2 family members and the mitochondria in apoptosis Genes Dev. 13 1999 1899 1911 (Pubitemid 29407357)
5. A.M. Petros, E.T. Olejniczak, and S.W. Fesik Structural biology of the Bcl-2 family of proteins Biochim. Biophys. Acta 1644 2004 83 94 (Pubitemid 38281265)
6. A. Shamas-Din, and H. Brahmbhatt D.W. Andrews BH3-only proteins: orchestrators of apoptosis Biochim. Biophys. Acta 1813 2011 508 520
7. S.J. Korsmeyer, and M.C. Wei P.H. Schlesinger Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c Cell Death Differ. 7 2000 1166 1173 (Pubitemid 32042223)
8. L.M. Dejean, and S. Martinez-Caballero K.W. Kinnally Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel Mol. Biol. Cell 16 2005 2424 2432 (Pubitemid 40632223)
9. B. Antonsson, and S. Montessuit J.C. Martinou Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria Biochem. J. 345 2000 271 278 (Pubitemid 30077167)
10. R. Eskes, and S. Desagher J.C. Martinou Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane Mol. Cell. Biol. 20 2000 929 935 (Pubitemid 30044230)
11. L.P. Billen, and C.L. Kokoski D.W. Andrews Bcl-XL inhibits membrane permeabilization by competing with Bax PLoS Biol. 6 2008 e147 10.1371/journal.pbio.0060147 (Pubitemid 351888310)
12. E. Gavathiotis, and M. Suzuki L.D. Walensky BAX activation is initiated at a novel interaction site Nature 455 2008 1076 1081
13. G. Heimlich, and A.D. McKinnon J.M. Jürgensmeier Bax-induced cytochrome c release from mitochondria depends on α-helices-5 and -6 Biochem. J. 378 2004 247 255 (Pubitemid 38299564)
14. J.P. Upton, and A.J. Valentijn A.P. Gilmore The N-terminal conformation of Bax regulates cell commitment to apoptosis Cell Death Differ. 14 2007 932 942 (Pubitemid 46629833)
15. A.J. Valentijn, and J.P. Upton A.P. Gilmore Bax targeting to mitochondria occurs via both tail anchor-dependent and -independent mechanisms Cell Death Differ. 15 2008 1243 1254 (Pubitemid 351984754)
16. H. Zhou, and Q. Hou Y.T. Hsu Complete activation of Bax by a single site mutation Oncogene 26 2007 7092 7102 (Pubitemid 350059677)
17. C. Muñoz-Pinedo, and A. Guío-Carrión D.R. Green Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiated but can vary in duration Proc. Natl. Acad. Sci. USA 103 2006 11573 11578 (Pubitemid 44182493)
18. J.C. Goldstein, and C. Muñoz-Pinedo D.R. Green Cytochrome c is released in a single step during apoptosis Cell Death Differ. 12 2005 453 462 (Pubitemid 40662843)
19. P.D. Bhola, and S.M. Simon Determinism and divergence of apoptosis susceptibility in mammalian cells J. Cell Sci. 122 2009 4296 4302
20. P.D. Bhola, A.L. Mattheyses, and S.M. Simon Spatial and temporal dynamics of mitochondrial membrane permeability waves during apoptosis Biophys. J. 97 2009 2222 2231
21. E. Christenson, and S. Merlin P. Schlesinger Cholesterol effects on BAX pore activation J. Mol. Biol. 381 2008 1168 1183
22. S. Montessuit, and S.P. Somasekharan J.C. Martinou Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization Cell 142 2010 889 901
23. L. Scorrano, and M. Ashiya S.J. Korsmeyer A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis Dev. Cell 2 2002 55 67 (Pubitemid 34065906)
24. E. Gottlieb, S.M. Armour, and C.B. Thompson Mitochondrial respiratory control is lost during growth factor deprivation Proc. Natl. Acad. Sci. USA 99 2002 12801 12806
25. S. Bleicken, and M. Classen E. Bordignon Molecular details of Bax activation, oligomerization, and membrane insertion J. Biol. Chem. 285 2010 6636 6647
26. J.F. Lovell, and L.P. Billen D.W. Andrews Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax Cell 135 2008 1074 1084
27. O. Landeta, and A. Landajuela G. Basañez Reconstitution of proapoptotic BAK function in liposomes reveals a dual role for mitochondrial lipids in the BAK-driven membrane permeabilization process J. Biol. Chem. 286 2011 8213 8230
28. F. Llambi, and T. Moldoveanu D.R. Green A unified model of mammalian BCL-2 protein family interactions at the mitochondria Mol. Cell 44 2011 517 531
29. A.J. Valentijn, J.P. Upton, and A.P. Gilmore Analysis of endogenous Bax complexes during apoptosis using blue native PAGE: implications for Bax activation and oligomerization Biochem. J. 412 2008 347 357 (Pubitemid 351758241)
30. T.W. Owens, and A.J. Valentijn A.P. Gilmore Apoptosis commitment and activation of mitochondrial Bax during anoikis is regulated by p38MAPK Cell Death Differ. 16 2009 1551 1562
31. L.M. Dejean, and S. Martinez-Caballero K.W. Kinnally Regulation of the mitochondrial apoptosis-induced channel, MAC, by BCL-2 family proteins Biochim. Biophys. Acta 1762 2006 191 201 (Pubitemid 43006025)
32. D. Westphal, and G. Dewson R.M. Kluck Molecular biology of Bax and Bak activation and action Biochim. Biophys. Acta 1813 2011 521 531
33. M.G. Annis, and E.L. Soucie D.W. Andrews Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis EMBO J. 24 2005 2096 2103 (Pubitemid 40961794)
34. V. Mikhailov, and M. Mikhailova P. Saikumar Bcl-2 prevents Bax oligomerization in the mitochondrial outer membrane J. Biol. Chem. 276 2001 18361 18374
35. M. Ott, and J.D. Robertson S. Orrenius Cytochrome c release from mitochondria proceeds by a two-step process Proc. Natl. Acad. Sci. USA 99 2002 1259 1263 (Pubitemid 34136480)
36. R.T. Uren, and G. Dewson R.M. Kluck Mitochondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes J. Biol. Chem. 280 2005 2266 2274
37. H. Yuan, and S.D. Williams R.A. Gottlieb Cytochrome c dissociation and release from mitochondria by truncated Bid and ceramide Mitochondrion 2 2003 237 244 (Pubitemid 36342345)
38. E. Doran, and A.P. Halestrap Cytochrome c release from isolated rat liver mitochondria can occur independently of outer-membrane rupture: possible role of contact sites Biochem. J. 348 2000 343 350 (Pubitemid 30345207)
39. D.M. Finucane, and E. Bossy-Wetzel D.R. Green Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL J. Biol. Chem. 274 1999 2225 2233
40. J. Zhuang, and G.M. Cohen Release of mitochondrial cytochrome c is upstream of caspase activation in chemical-induced apoptosis in human monocytic tumor cells Toxicol. Lett. 102-103 1998 121 129 (Pubitemid 29021211)
41. T. Li, and T. Brustovetsky N. Brustovetsky Dissimilar mechanisms of cytochrome c release induced by octyl glucoside-activated BAX and by BAX activated with truncated BID Biochim. Biophys. Acta 1797 2010 52 62
42. T. Kuwana, and M.R. Mackey D.D. Newmeyer Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane Cell 111 2002 331 342 (Pubitemid 35341388)
43. B. Schafer, and J. Quispe T. Kuwana Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation Mol. Biol. Cell 20 2009 2276 2285
44. R.M. Kluck, and M.D. Esposti D.D. Newmeyer The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol J. Cell Biol. 147 1999 809 822
45. L.J. Siskind, R.N. Kolesnick, and M. Colombini Ceramide channels increase the permeability of the mitochondrial outer membrane to small proteins J. Biol. Chem. 277 2002 26796 26803 (Pubitemid 34951684)
46. M. Suzuki, R.J. Youle, and N. Tjandra Structure of Bax: coregulation of dimer formation and intracellular localization Cell 103 2000 645 654
47. G. Basañez, and J. Zhang J. Zimmerberg Pro-apoptotic cleavage products of Bcl-xL form cytochrome c-conducting pores in pure lipid membranes J. Biol. Chem. 276 2001 31083 31091
48. G.R. Thuduppathy, and O. Terrones R.B. Hill The N-terminal domain of Bcl-xL reversibly binds membranes in a pH-dependent manner Biochemistry 45 2006 14533 14542 (Pubitemid 44865207)
49. L.J. Siskind, and L. Feinstein M. Colombini Anti-apoptotic Bcl-2 proteins disassemble ceramide channels J. Biol. Chem. 283 2008 6622 6630
50. O. Teijido, and L. Dejean Upregulation of Bcl2 inhibits apoptosis-driven Bax insertion but favors Bax relocalization in mitochondria FEBS Lett. 584 2010 3305 3310
51. H. Ahmed Principles and Reactions of Protein Extraction, Purification, and Characterization 1959 CRC Press Boca Raton, FL
52. R.L. Hill, and R.A. Bradshaw Fumarase Methods Enzymol. 13 1969 91 99