The pro-apoptotic BH3-only protein bim interacts with components of the translocase of the outer mitochondrial membrane (TOM)

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Frank, Daniel O ^a,b   Dengjel, Jörn ^b   Wilfling, Florian ^c   Kozjak Pavlovic, Vera ^d   Häcker, Georg ^a,b   Weber, Arnim ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; CASPASE 3; PROTEIN BAX; SMALL INTERFERING RNA; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 20; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 22; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 40; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 70; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BCL2L11 PROTEIN, HUMAN; BCL2L11 PROTEIN, MOUSE; CARRIER PROTEIN; CELL SURFACE RECEPTOR; MEMBRANE PROTEIN; ONCOPROTEIN; PROTEIN BAK; PROTEIN BINDING; TOM22 PROTEIN, HUMAN; TOM40 PROTEIN HUMAN; TOMM20 PROTEIN, HUMAN; TOMM70A PROTEIN, HUMAN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GENE SILENCING; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OUTER MEMBRANE; OUTER MITOCHONDRIAL MEMBRANE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; STEADY STATE; YEAST CELL; ANIMAL; CELL CULTURE; GENETICS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BCL-2-LIKE PROTEIN 11; BLOTTING, WESTERN; CELLS, CULTURED; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS; RECEPTORS, CELL SURFACE; RNA INTERFERENCE;

EID: 84929492306     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123341     Document Type: Article

References (36)

1. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996; 86(1):147-57. PMID: 8689682
2. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol. 2008; 9(1):47-59. PMID: 18097445
3. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Molecular cell. 2010; 37(3):299-310. doi: 10.1016/j.molcel.2010.01.025 PMID: 20159550
4. Czabotar PE, Westphal D, Dewson G, Ma S, Hockings C, Fairlie WD, et al. Bax Crystal Structures Reveal How BH3 Domains Activate Bax and Nucleate Its Oligomerization to Induce Apoptosis. Cell. 2013; 152(3):519-31. Epub 2013/02/05. doi: 10.1016/j.cell.2012.12.031 PMID: 23374347
5. Weber K, Harper N, Schwabe J, Cohen GM. BIM-Mediated Membrane Insertion of the BAK Pore Domain Is an Essential Requirement for Apoptosis. Cell reports. 2013. Epub 2013/10/15.
6. 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(3):183-92. PMID: 12242151
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(5813):856-9. PMID: 17289999
8. Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol. 2001; 153(6):1265-76. PMID: 11402069
9. Wilfling F, Weber A, Potthoff S, Vogtle FN, Meisinger C, Paschen SA, et al. BH3-only proteins are tail-anchored in the outer mitochondrial membrane and can initiate the activation of Bax. Cell Death Differ. 2012; 19(8):1328-36. Epub 2012/02/22. doi: 10.1038/cdd.2012.9 PMID: 22343714
10. Hardwick JM, Youle RJ. SnapShot: BCL-2 proteins. Cell. 2009; 138(2):404, e1. doi: 10.1016/j.cell.2009.07.003 PMID: 19632186
11. Weber A, Paschen SA, Heger K, Wilfling F, Frankenberg T, Bauerschmitt H, et al. BimS-induced apoptosis requires mitochondrial localization but not interaction with anti-apoptotic Bcl-2 proteins. The Journal of cell biology. 2007; 177(4):625-36. PMID: 17517961
12. Young JC, Hoogenraad NJ, Hartl FU. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell. 2003; 112(1):41-50. Epub 2003/01/16. PMID: 12526792
13. Neupert W, Herrmann JM. Translocation of Proteins into Mitochondria. Annu Rev Biochem. 2007.
14. Dolezal P, Likic V, Tachezy J, Lithgow T. Evolution of the molecular machines for protein import into mitochondria. Science. 2006; 313(5785):314-8. PMID: 16857931
15. Dukanovic J, Rapaport D. Multiple pathways in the integration of proteins into the mitochondrial outer membrane. Biochim Biophys Acta. 2011; 1808(3):971-80. Epub 2010/07/06. doi: 10.1016/j.bbamem.2010.06.021 PMID: 20599689
16. Kozjak-Pavlovic V, Ross K, Benlasfer N, Kimmig S, Karlas A, Rudel T. Conserved roles of Sam50 and metaxins in VDAC biogenesis. EMBO Rep. 2007; 8(6):576-82. PMID: 17510655
17. 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. Molecular and cellular biology. 2001; 21(3):854-64. PMID: 11154272
18. Vince JE, Chau D, Callus B, Wong WW, Hawkins CJ, Schneider P, et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. The Journal of cell biology. 2008; 182(1):171-84. Epub 2008/07/09. doi: 10.1083/jcb.200801010 PMID: 18606850
19. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nature protocols. 2006; 1(6):2856-60. Epub 2007/04/05. PMID: 17406544
20. Rappsilber J, Mann M, Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nature protocols. 2007; 2(8):1896-906. Epub 2007/08/19. PMID: 17703201
21. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature biotechnology. 2008; 26(12):1367-72. Epub 2008/11/26. doi: 10.1038/nbt.1511 PMID: 19029910
22. Weber A, Auslander D, Hacker G. Mouse Noxa uses only the C-terminal BH3-domain to inactivate Mcl-1. Apoptosis. 2013. Epub 2013/06/05.
23. Moczko M, Ehmann B, Gartner F, Honlinger A, Schafer E, Pfanner N. Deletion of the receptor MOM19 strongly impairs import of cleavable preproteins into Saccharomyces cerevisiae mitochondria. The Journal of biological chemistry. 1994; 269(12):9045-51. Epub 1994/03/25. PMID: 8132642
24. van Wilpe S, Ryan MT, Hill K, Maarse AC, Meisinger C, Brix J, et al. Tom22 is a multifunctional organizer of the mitochondrial preprotein translocase. Nature. 1999; 401(6752):485-9. Epub 1999/10/16. PMID: 10519552
25. Meisinger C, Pfanner N, Truscott KN. Isolation of yeast mitochondria. Methods Mol Biol. 2006; 313:33-9. Epub 2005/08/25. PMID: 16118422
26. Sherman F, Fink GR, Hicks J. Methods in Yeast Genetics: A Laboratory Course. New York: Cold Spring Harbor Laboratory Press; 1986.
27. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002; 1(5):376-86. PMID: 12118079
28. Sato T, Hanada M, Bodrug S, Irie S, Iwama N, Boise LH, et al. Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. ProcNatlAcadSciUSA. 1994; 91 (20):9238-42. PMID: 7937747
29. Kemper C, Habib SJ, Engl G, Heckmeyer P, Dimmer KS, Rapaport D. Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. Journal of cell science. 2008; 121(Pt 12):1990-8. Epub 2008/05/23. doi: 10.1242/jcs.024034 PMID: 18495843
30. Meisinger C, Ryan MT, Hill K, Model K, Lim JH, Sickmann A, et al. Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with preproteins, small tom proteins, and import receptors. Molecular and cellular biology. 2001; 21(7):2337-48. Epub 2001/03/22. PMID: 11259583
31. Ley R, Ewings KE, Hadfield K, Cook SJ. Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ. 2005; 12(8):1008-14. PMID: 15947788
32. Dehan E, Bassermann F, Guardavaccaro D, Vasiliver-Shamis G, Cohen M, Lowes KN, et al. betaTrCP-and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Molecular cell. 2009; 33(1):109-16. Epub 2009/01/20. doi: 10.1016/j.molcel.2008.12.020 PMID: 19150432
33. Geissler A, Haun F, Frank DO, Wieland K, Simon MM, Idzko M, et al. Apoptosis induced by the fungal pathogen gliotoxin requires a triple phosphorylation of Bim by JNK. Cell Death Differ. 2013.
34. Clybouw C, Merino D, Nebl T, Masson F, Robati M, O'Reilly L, et al. Alternative splicing of Bim and Erk-mediated Bim(EL) phosphorylation are dispensable for hematopoietic homeostasis in vivo. Cell Death Differ. 2012; 19(6):1060-8. Epub 2012/01/14. doi: 10.1038/cdd.2011.198 PMID: 22240894
35. Parish IA, Rao S, Smyth GK, Juelich T, Denyer GS, Davey GM, et al. The molecular signature of CD8+ T cells undergoing deletional tolerance. Blood. 2009; 113(19):4575-85. doi: 10.1182/blood-2008-10-185223 PMID: 19204323
36. Huntington ND, Puthalakath H, Gunn P, Naik E, Michalak EM, Smyth MJ, et al. Interleukin 15-mediated survival of natural killer cells is determined by interactions among Bim, Noxa and Mcl-1. Nat Immunol. 2007; 8(8):856-63. PMID: 17618288