BH3-only proteins are tail-anchored in the outer mitochondrial membrane and can initiate the activation of Bax

Cell Death and Differentiation

Volumn 19, Issue 8, 2012, Pages 1328-1336

  Wilfling, F ^a,d   Weber, A ^b   Potthoff, S ^b   Vogtle F N ^c   Meisinger, C ^c   Paschen, S A ^a,b   Hacker G ^b,c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

apoptosis; Bax; BH3 only; Bim; tail anchor

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; CYTOCHROME C; GREEN FLUORESCENT PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ISOLATION; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; UPREGULATION; YEAST;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CELL LINE; CELL LINE, TUMOR; HUMANS; MICE; MICROSCOPY, CONFOCAL; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EID: 84863726664     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2012.9     Document Type: Article

References (40)

1. Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407: 770-776.
2. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
3. Chipuk JE, Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? TrendsCell Biol 2008; 18: 157-164.
4. Willis SN, Adams JM. Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol 2005; 17: 617-625. (Pubitemid 41540411)
5. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002; 2: 183-192. (Pubitemid 41043974)
6. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 2005; 17: 393-403. (Pubitemid 40193310)
7. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007; 315: 856-859.
8. Dewson G, Kluck RM. Mechanisms by which Bak and Bax permeabilise mitochondria during apoptosis. J Cell Sci 2009; 122 (Pt 16): 2801-2808.
9. Borgese N, Brambillasca S, Colombo S. How tails guide tail-anchored proteins to their destinations. Curr Opin Cell Biol 2007; 19: 368-375. (Pubitemid 47268760)
10. Woo HN, Seo YW, Moon AR, Jeong SY, Jeong SY, Choi EK et al. Effects of the BH3-only protein human Noxa on mitochondrial dynamics. FEBS Lett 2009; 583: 2349-2354.
11. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, Leber B et al. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 2008; 135: 1074-1084.
12. Billen LP, Kokoski CL, Lovell JF, Leber B, Andrews DW. Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol 2008; 6: e147.
13. Weber A, Paschen SA, Heger K, Wilfling F, Frankenberg T, Bauerschmitt H et al. BimSinduced apoptosis requires mitochondrial localization but not interaction with anti-apoptotic Bcl-2 proteins. J Cell Biol 2007; 177: 625-636. (Pubitemid 46799834)
14. Hardwick JM, Youle RJ. SnapShot: BCL-2 proteins. Cell 2009; 138: 404 404 e1.
15. Horie C, Suzuki H, Sakaguchi M, Mihara K. Characterization of signal that directs C-tailanchored proteins to mammalian mitochondrial outer membrane. Mol Biol Cell 2002; 13: 1615-1625. (Pubitemid 34522643)
16. Mokranjac D, NeupertW. Protein import into isolated mitochondria. Methods Mol Biol 2007; 372: 277-286.
17. Dolezal P, Likic V, Tachezy J, Lithgow T. Evolution of the molecular machines for protein import into mitochondria. Science 2006; 313: 314-318. (Pubitemid 44480948)
18. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998; 94: 491-501. (Pubitemid 28391865)
19. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998; 94: 481-490. (Pubitemid 28391864)
20. Germain M, Mathai JP, Shore GC. BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J Biol Chem 2002; 277: 18053-18060. (Pubitemid 34967618)
21. Schuldiner M, Metz J, Schmid V, Denic V, Rakwalska M, Schmitt HD et al. The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 2008; 134: 634-645.
22. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005; 435: 677-681. (Pubitemid 40825512)
23. Weber A, Kirejczyk Z, Potthoff S, Ploner C, Hacker G. Endogenous Noxa determines the strong proapoptotic synergism of the BH3-mimetic ABT-737 with chemotherapeutic agents in human melanoma cells. Transl Oncol 2009; 2: 73-83.
24. Fletcher JI, Meusburger S, Hawkins CJ, Riglar DT, Lee EF, Fairlie WD et al. Apoptosis is triggered when prosurvival Bcl-2 proteins cannot restrain Bax. Proc Natl Acad Sci USA 2008; 105: 18081-18087.
25. Day CL, Chen L, Richardson SJ, Harrison PJ, Huang DC, Hinds MG. Solution structure of prosurvival Mcl-1 and characterization of its binding by proapoptotic BH3-only ligands. J Biol Chem 2005; 280: 4738-4744. (Pubitemid 40288644)
26. Gallenne T, Gautier F, Oliver L, Hervouet E, Noel B, Hickman JA et al. Bax activation by the BH3-only protein Puma promotes cell dependence on antiapoptotic Bcl-2 family members. J Cell Biol 2009; 185: 279-290.
27. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, Green DR et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 2005; 17: 525-535. (Pubitemid 40269117)
28. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG et al. BAX activation is initiated at a novel interaction site. Nature 2008; 455: 1076-1081.
29. Gavathiotis E, Reyna DE, Davis ML, Bird GH, Walensky LD. BH3-triggered structural reorganization drives the activation of proapoptotic BAX. Mol Cell 2010; 40: 481-492.
30. Kim H, Tu HC, Ren D, Takeuchi O, Jeffers JR, Zambetti GP et al. Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol Cell 2009; 36: 487-499.
31. Hsu YT, Youle RJ. Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 1997; 272: 13829-13834. (Pubitemid 27224822)
32. Hinds MG, Smits C, Fredericks-Short R, Risk JM, Bailey M, Huang DC et al. 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 2007; 14: 128-136. (Pubitemid 44911900)
33. Lohmann C, Muschaweckh A, Kirschnek S, Jennen L, Wagner H, Hacker G. Induction of tumor cell apoptosis or necrosis by conditional expression of cell death proteins: analysis of cell death pathways and in vitro immune stimulatory potential. J Immunol 2009; 182: 4538-4546.
34. Daum G, Bohni PC, Schatz G. Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 1982; 257: 13028-13033.
35. Schagger H. Tricine-SDS-PAGE. Nat Protoc 2006; 1: 16-22.
36. Shinjyo T, Kuribara R, Inukai T, Hosoi H, Kinoshita T, Miyajima A et al. Downregulation of Bim, a proapoptotic relative of Bcl-2, is a pivotal step in cytokine-initiated survival signaling in murine hematopoietic progenitors. Mol Cell Biol 2001; 21: 854-864. (Pubitemid 32104733)
37. Eskes R, Desagher S, Antonsson B, Martinou JC. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 2000; 20: 929-935. (Pubitemid 30044230)
38. Sherman F, Fink GR, Hicks J. Methods in Yeast Genetics: A Laboratory Course. Cold Spring Harbor Laboratory Press: New York, 1986.
39. Gari E, Piedrafita L, Aldea M, Herrero E. A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 1997; 13: 837-848. (Pubitemid 27285747)
40. Mumberg D, Muller R, Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 1995; 156: 119-122.