Use of human cancer cell lines mitochondria to explore the mechanisms of BH3 peptides and ABT-737-induced mitochondrial membrane permeabilization

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Buron, Nelly ^a,b   Porceddu, Mathieu ^a,b   Brabant, Magali ^a   Desgué, Diana ^a   Racoeur, Cindy ^a   Lassalle, Myriam ^a   Péchoux, Christine ^c   Rustin, Pierre ^b,d   Jacotot, Etienne ^a,e   Borgne Sanchez, Annie ^a,b  

^a Theraptosis SA   (France)

^b HÔPITAL ROBERT DEBRÉ   (France)

^c INRA Institut National de la Recherche Agronomique   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ABT-737; BAX PROTEIN (53 86); BAX PROTEIN (53-86); BIPHENYL DERIVATIVE; CROSS LINKING REAGENT; NITROPHENOL; ONCOPROTEIN; PEPTIDE FRAGMENT; PIPERAZINE DERIVATIVE; PROTEIN BCL 2; SULFONAMIDE;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; CELL MEMBRANE POTENTIAL; CHEMISTRY; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; PERMEABILITY; TUMOR CELL LINE;

ANIMALS; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; CROSS-LINKING REAGENTS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NITROPHENOLS; PEPTIDE FRAGMENTS; PERMEABILITY; PIPERAZINES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SULFONAMIDES;

EID: 77955643496     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009924     Document Type: Article

References (49)

1. Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116: 205-219.
2. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305: 626-629.
3. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X (1999) Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15: 269-290.
4. Chipuk JE, Bouchier-Hayes L, Green DR (2006) Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ 13: 1396-1402.
5. Danial NN (2007) BCL-2 family proteins: critical checkpoints of apoptotic cell death. Clin Cancer Res 13: 7254-7263.
6. Er E, Oliver L, Cartron PF, Juin P, Manon S, et al. (2006) Mitochondria as the target of the pro-apoptotic protein Bax. Biochim Biophys Acta 1757: 1301-1311.
7. Goldsmith KC, Lestini BJ, Gross M, Ip L, Bhumbla A, et al. (2009) BH3 response profiles from neuroblastoma mitochondria predict activity of small molecule Bcl-2 family antagonists. Cell Death Differ.
8. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59.
9. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, et al. (1999) Bidinduced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144: 891-901.
10. Martinou JC, Green DR (2001) Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2: 63-67.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163.
17. Reed JC, Green DR (2002) Remodeling for demolition: changes in mitochondrial ultrastructure during apoptosis. Mol Cell 9: 1-3.
18. Gottlieb E, Armour SM, Harris MH, Thompson CB (2003) Mitochondrial membrane potential regulates matrix configuration and cytochrome c release during apoptosis. Cell Death Differ 10: 709-717.
19. Galluzzi L, Morselli E, Kepp O, Vitale I, Rigoni A, et al. (2009) Mitochondrial gateways to cancer. Mol Aspects Med.
20. Brenner D, Mak TW (2009) Mitochondrial cell death effectors. Curr Opin Cell Biol.
21. Aouacheria A, Cibiel A, Guillemin Y, Gillet G, Lalle P (2007) Modulating Mitochondria-Mediated Apoptotic Cell Death through Targeting of Bcl-2 Family Proteins. Recent Patents on DNA & Gene Sequences 1: 43-61.
22. Letai A (2005) Pharmacological manipulation of Bcl-2 family members to control cell death. J Clin Invest 115: 2648-2655.
23. Goldsmith KC, Liu X, Dam V, Morgan BT, Shabbout M, et al. (2006) BH3 peptidomimetics potently activate apoptosis and demonstrate single agent efficacy in neuroblastoma. Oncogene 25: 4525-4533.
24. Jansen B, Schlagbauer-Wadl H, Brown BD, Bryan RN, van Elsas A, et al. (1998) bcl-2 antisense therapy chemosensitizes human melanoma in SCID mice. Nat Med 4: 232-234.
25. Fu GF, Lin XH, Han QW, Fan YR, Xu YF, et al. (2005) RNA interference remarkably suppresses bcl-2 gene expression in cancer cells in vitro and in vivo. Cancer Biol Ther 4: 822-829.
26. 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.
27. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, et al. (2006) The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10: 389-399.
28. 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.
29. Konopleva M, Contractor R, Tsao T, Samudio I, Ruvolo PP, et al. (2006) Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 10: 375-388.
30. Lecoeur H, Langonne A, Baux L, Rebouillat D, Rustin P, et al. (2004) Real-time flow cytometry analysis of permeability transition in isolated mitochondria. Exp Cell Res 294: 106-117.
31. Billen LP, Kokoski CL, Lovell JF, Leber B, Andrews DW (2008) Bcl-XL Inhibits Membrane Permeabilization by Competing with Bax. PLoS Biol 6: e147.
32. Goping IS, Gross A, Lavoie JN, Nguyen M, Jemmerson R, et al. (1998) Regulated targeting of BAX to mitochondria. J Cell Biol 143: 207-215.
33. Bombrun A, Gerber P, Casi G, Terradillos O, Antonsson B, et al. (2003) 3,6-dibromocarbazole piperazine derivatives of 2-propanol as first inhibitors of cytochrome c release via Bax channel modulation. J Med Chem 46: 4365-4368.
34. Polster BM, Basanez G, Young M, Suzuki M, 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.
35. Chipuk JE, Fisher JC, Dillon CP, Kriwacki RW, Kuwana T, et al. (2008) Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc Natl Acad Sci U S A 105: 20327-20332.
36. Polster BM, Kinnally KW, Fiskum G (2001) BH3 death domain peptide induces cell type-selective mitochondrial outer membrane permeability. J Biol Chem 276: 37887-37894.
37. Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, et al. (2003) Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. Embo J 22: 4385-4399.
38. Hermanson D, Addo SN, Bajer AA, Marchant JS, Das SG, et al. (2009) Dual mechanisms of sHA 14-1 in inducing cell death through endoplasmic reticulum and mitochondria. Mol Pharmacol 76: 667-678.
39. Paoluzzi L, Gonen M, Bhagat G, Furman RR, Gardner JR, et al. (2008) The BH3-only mimetic ABT-737 synergizes the antineoplastic activity of proteasome inhibitors in lymphoid malignancies. Blood 112: 2906-2916.
40. Saito M, Korsmeyer SJ, Schlesinger PH (2000) BAX-dependent transport of cytochrome c reconstituted in pure liposomes. Nat Cell Biol 2: 553-555.
41. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, et al. (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111: 331-342.
42. Roucou X, Montessuit S, Antonsson B, Martinou JC (2002) Bax oligomerization in mitochondrial membranes requires tBid (caspase-8-cleaved Bid) and a mitochondrial protein. Biochem J 368: 915-921.
43. Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JA, Penn LZ, et al. (2005) Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. Embo J 24: 2096-2103.
44. Cartron PF, Bellot G, Oliver L, Grandier-Vazeille X, Manon S, et al. (2008) Bax inserts into the mitochondrial outer membrane by different mechanisms. FEBS Lett 582: 3045-3051.
45. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, et al. (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135: 1074-1084.
46. Letai A (2006) Restoring cancer's death sentence. Cancer Cell 10: 343-345.
47. Chen S, Dai Y, Pei XY, Grant S (2009) Bim Up-regulation by Histone Deacetylase Inhibitors Mediates Interactions with the Bcl-2 Antagonist ABT-737: Evidence for Distinct Roles for Bcl-2, Bcl-xL and Mcl-1. Mol Cell Biol.
48. Kim H, Farris J, Christman SA, Kong BW, Foster LK, et al. (2002) Events in the immortalizing process of primary human mammary epithelial cells by the catalytic subunit of human telomerase. Biochem J 365: 765-772.
49. Rustin P, Chretien D, Bourgeron T, Gerard B, Rotig A, et al. (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228: 35-51.