Dynamical systems analysis of mitochondrial BAK activation kinetics predicts resistance to BH3 domains

PLoS ONE

Volumn 3, Issue 8, 2008, Pages

  Grills, Claire ^a   Crawford, Nyree ^a   Chacko, Alex ^a   Johnston, Patrick G ^a,b   O'Rourke, Francesca ^a   Fennell, Dean A ^a,b  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b Northern Ireland Cancer Registry   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN BID; PROTEIN MCL 1; PUMA PROTEIN; APOPTOSIS REGULATORY PROTEIN; BAK1 PROTEIN, HUMAN; BAX PROTEIN (53 86); BAX PROTEIN (53-86); BCL 3 BINDING PROTEIN, HUMAN; BCL-3-BINDING PROTEIN, HUMAN; CARRIER PROTEIN; HRK PROTEIN, HUMAN; ONCOPROTEIN; PEPTIDE FRAGMENT; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOMIMETICS; CELL MEMBRANE RESISTANCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; KINETICS; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR MODEL; PREDICTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SYSTEM ANALYSIS; APOPTOSIS; HUMAN; INTRACELLULAR MEMBRANE; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; CARRIER PROTEINS; HUMANS; INTRACELLULAR MEMBRANES; KINETICS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS;

EID: 52449095864     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003038     Document Type: Article

References (32)

1. Degenhardt K, Chen G, Lindsten T, White E (2002) BAX and BAK mediate p53-independent suppression of tumorigenesis. Cancer Cell 2: 193-203.
2. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, et al. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
3. Moldoveanu T, Liu Q, Tocilj A, Watson M, Shore G, et al. (2006) The X-ray structure of a BAK homodimer reveals an inhibitory zinc binding site. Mol Cell 24: 677-688.
4. Kiefer MC, Brauer MJ, Powers VC, Wu JJ, Umansky SR, et al. (1995) Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak. Nature 374: 736-739.
5. Chittenden T, Harrington EA, O'Connor R, Flemington C, Lutz RJ, et al. (1995) Induction of apoptosis by the Bcl-2 homologue Bak. Nature 374: 733-736.
6. Griffiths GJ, Dubrez L, Morgan CP, Jones NA, Whitehouse J, et al. (1999) Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J Cell Biol 144: 903-914.
7. Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ (2001) Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153: 1265-1276.
8. Ruffolo SC, Shore GC (2003) BCL-2 selectively interacts with the BID-induced open conformer of BAK, inhibiting BAK auto-oligomerization. J Biol Chem 278: 25039-25045.
9. Cartron PF, Gallenne T, Bougras G, Gautier F, Manero F, et al. (2004) The first alpha helix of Bax plays a necessary role in its ligand-induced activation by the BH3-only proteins Bid and PUMA. Mol Cell 16: 807-818.
10. Wang K, Yin XM, Chao DT, Milliman CL, Korsmeyer SJ (1996) BID: a novel BH3 domain-only death agonist. Genes Dev 10: 2859-2869.
11. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, et al. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192.
12. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, et al. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17: 525-535.
13. Walensky LD, Pitter K, Morash J, Oh KJ, Barbuto S, et al. (2006) A stapled BID BH3 helix directly binds and activates BAX. Mol Cell 24: 199-210.
14. Kelekar A, Chang BS, Harlan JE, Fesik SW, Thompson CB (1997) Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-XL. Mol Cell Biol 17: 7040-7046.
15. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681.
16. Nguyen M, Marcellus RC, Roulston A, Watson M, Serfass L, et al. (2007) Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc Natl Acad Sci U S A 104: 19512-19517.
17. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, et al. (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17: 393-403.
18. Willis SN, Chen L, Dewson G, Wei A, Naik E, et al. (2005) 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.
19. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301: 513-517.
20. Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, et al. (1997) Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275: 983-986.
21. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, et al. (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315: 856-859.
22. Uren RT, Dewson G, Chen L, Coyne SC, Huang DC, et al. (2007) Mitochondrial permeabilization relies on BH3 ligands engaging multiple prosurvival Bcl-2 relatives, not Bak. J Cell Biol 177: 277-287.
23. Walensky LD, Kong AL, Escher I, Malia TJ, Barbuto S, et al. (2004) Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 305: 1466-1470.
24. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN (1993) Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol 4: 327-332.
25. Chen C, Cui J, Lu H, Wang R, Zhang S, et al. (2007) Modeling of the role of a Bax-activation switch in the mitochondrial apoptosis decision. Biophys J 92: 4304-4315.
26. Chen C, Cui J, Zhang W, Shen P (2007) Robustness analysis identifies the plausible model of the Bcl-2 apoptotic switch. FEBS Lett 581: 5143-5150.
27. Mathai JP, Germain M, Shore GC (2005) BH3-only BIK regulates BAX, BAK-dependent release of Ca2+ from endoplasmic reticulum stores and mitochondrial apoptosis during stress-induced cell death. J Biol Chem 280: 23829-23836.
28. Germain M, Mathai JP, Shore GC (2002) BH-3-only BIK functions at the endoplasmic reticulunt to stimulate cytochrome c release from mitochondria. J Biol Chem 277: 18053-18060.
29. Certo M, Del Gaizo Moore V, Nishino M, Wei G, Korsmeyer S, et al. (2006) Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9: 351-365.
30. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, et al. (2006) Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 8: 1348-1358.
31. Dejean LM, Martinez-Caballero S, Guo L, Hughes C, Teijido O, et al. (2005) Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Mol Biol Cell 16: 2424-2432.
32. Pavlov EV, Priault M, Pietkiewicz D, Cheng EH, Antonsson B, et al. (2001) A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. J Cell Biol 155: 725-731.