The structural biology of bh3-only proteins

Methods in Enzymology

Volumn 544, Issue , 2014, Pages 49-74

  Kvansakul, Marc ^a   Hinds, Mark G ^b,c  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Apoptosis; Bcl 2; BH3 only; Cancer; Protein structure

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ANTINEOPLASTIC AGENT; BH3 PROTEIN; BIM PROTEIN; CYTOTOXIC AGENT; DYNEIN ADENOSINE TRIPHOSPHATASE; MUTANT PROTEIN; MYOSIN V; NAVITOCLAX; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN MCL 1; PROTEIN NOXA; PROTEINASE; VENETOCLAX; VIRUS PROTEIN;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER CELL; CELL DEATH; CONFORMATIONAL TRANSITION; DRUG PROTEIN BINDING; HUMAN; MOLECULAR BIOLOGY; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION AND DEPHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; UBIQUITINATION; VIRUS SURVIVAL; ANIMAL; CHEMICAL STRUCTURE; METABOLISM; MOLECULAR GENETICS; NEOPLASM; PROCEDURES; PROTEIN ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84903460450     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/B978-0-12-417158-9.00003-0     Document Type: Chapter

References (124)

1. A. Aouacheria, F. Brunet, and M. Gouy Phylogenomics of life-or-death switches in multicellular animals: Bcl-2, BH3-Only, and BNip families of apoptotic regulators Molecular Biology and Evolution 22 2005 2395 2416
2. A. Aouacheria, V. Rech de Laval, C. Combet, and J.M. Hardwick Evolution of Bcl-2 homology motifs: Homology versus homoplasy Trends in Cell Biology 23 2013 103 111
3. L. Banadyga, S.C. Lam, T. Okamoto, M. Kvansakul, D.C. Huang, and M. Barry Deerpox virus encodes an inhibitor of apoptosis that regulates Bak and Bax Journal of Virology 85 2011 1922 1934
4. S. Barrera-Vilarmau, P. Obregon, and E. de Alba Intrinsic order and disorder in the bcl-2 member harakiri: Insights into its proapoptotic activity PLoS One 6 2011 e21413
5. T.E. Beaumont, T.M. Shekhar, L. Kaur, D. Pantaki-Eimany, M. Kvansakul, and C.J. Hawkins Yeast techniques for modeling drugs targeting Bcl-2 and caspase family members Cell Death and Disease 4 2013 e619
6. L.J. Beverly Regulation of anti-apoptotic BCL2-proteins by non-canonical interactions: The next step forward or two steps back? Journal of Cellular Biochemistry 113 2012 3 12
7. L.P. Billen, A. Shamas-Din, and D.W. Andrews Bid: A Bax-like BH3 protein Oncogene 27 Suppl. 1 2008 S93 S104
8. C.D. Bingle, R.W. Craig, B.M. Swales, V. Singleton, P. Zhou, and M.K. Whyte Exon skipping in Mcl-1 results in a bcl-2 homology domain 3 only gene product that promotes cell death Journal of Biological Chemistry 275 2000 22136 22146
9. S.V. Blaineau, and A. Aouacheria BCL2DB: Moving 'helix-bundled' BCL-2 family members to their database Apoptosis 14 2009 923 925
10. M.D. Boersma, J.D. Sadowsky, Y.A. Tomita, and S.H. Gellman Hydrophile scanning as a complement to alanine scanning for exploring and manipulating protein-protein recognition: Application to the Bim BH3 domain Protein Science 17 2008 1232 1240
11. J.M. Boyd, G.J. Gallo, B. Elangovan, A.B. Houghton, S. Malstrom, and B.J. Avery et al. Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins Oncogene 11 1995 1921 1928
12. M. Certo, V. Del Gaizo Moore, M. Nishino, G. Wei, S. Korsmeyer, and S.A. Armstrong et al. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members Cancer Cell 9 2006 351 365
13. L. Chen, S.N. Willis, A. Wei, B.J. Smith, J.I. Fletcher, and M.G. Hinds et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function Molecular Cell 17 2005 393 403
14. T. Chittenden, C. Flemington, A.B. Houghton, R.G. Ebb, G.J. Gallo, and B. Elangovan et al. A conserved domain in Bak, distinct from BH1 and BH2, mediates cell death and protein binding functions EMBO Journal 14 1995 5589 5596
15. J.J. Chou, H. Li, G.S. Salvesen, J. Yuan, and G. Wagner Solution structure of BID, an intracellular amplifier of apoptotic signaling Cell 96 1999 615 624
16. B. Conradt, and H.R. Horvitz The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9 Cell 93 1998 519 529
17. A. Craxton, M. Butterworth, N. Harper, L. Fairall, J. Schwabe, and A. Ciechanover et al. NOXA, a sensor of proteasome integrity, is degraded by 26S proteasomes by an ubiquitin-independent pathway that is blocked by MCL-1 Cell Death and Differentiation 19 2012 1424 1434
18. A. Cuconati, and E. White Viral homologs of BCL-2: Role of apoptosis in the regulation of virus infection Genes and Development 16 2002 2465 2478
19. P.E. Czabotar, E.F. Lee, M.F. van Delft, C.L. Day, B.J. Smith, and D.C. Huang et al. Structural insights into the degradation of Mcl-1 induced by BH3 domains Proceedings of the National Academy of Sciences of the United States of America 104 2007 6217 6222
20. P.E. Czabotar, D. Westphal, G. Dewson, S. Ma, C. Hockings, and W.D. Fairlie et al. Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis Cell 152 2013 519 531
21. C.L. Day, L. Chen, S.J. Richardson, P.J. Harrison, D.C. Huang, and M.G. Hinds Solution structure of prosurvival Mcl-1 and characterization of its binding by proapoptotic BH3-only ligands Journal of Biological Chemistry 280 2005 4738 4744
22. C.L. Day, H. Puthalakath, G. Skea, A. Strasser, I. Barsukov, and L.Y. Lian et al. Localization of dynein light chains 1 and 2 and their pro-apoptotic ligands Biochemical Journal 377 2004 597 605
23. C.L. Day, C. Smits, F.C. Fan, E.F. Lee, W.D. Fairlie, and M.G. Hinds Structure of the BH3 domains from the p53-inducible BH3-only proteins Noxa and Puma in complex with Mcl-1 Journal of Molecular Biology 380 2008 958 971
24. J. DeBartolo, S. Dutta, L. Reich, and A.E. Keating Predictive Bcl-2 family binding models rooted in experiment or structure Journal of Molecular Biology 422 2012 124 144
25. A.Y. Denisov, T. Sprules, J. Fraser, G. Kozlov, and K. Gehring Heat-induced dimerization of BCL-xL through alpha-helix swapping Biochemistry 46 2007 734 740
26. K.S. Doctor, J.C. Reed, A. Godzik, and P.E. Bourne The apoptosis database Cell Death and Differentiation 10 2003 621 633
27. S. Dutta, T.S. Chen, and A.E. Keating Peptide ligands for pro-survival protein Bfl-1 from computationally guided library screening ACS Chemical Biology 8 2013 778 788
28. S. Dutta, S. Gulla, T.S. Chen, E. Fire, R.A. Grant, and A.E. Keating Determinants of BH3 binding specificity for Mcl-1 versus Bcl-xL Journal of Molecular Biology 398 2010 747 762
29. P.M. Eimon, and A. Ashkenazi The zebrafish as a model organism for the study of apoptosis Apoptosis 15 2010 331 349
30. J. Fan, Q. Zhang, H. Tochio, M. Li, and M. Zhang Structural basis of diverse sequence-dependent target recognition by the 8 kDa dynein light chain Journal of Molecular Biology 306 2001 97 108
31. Y. Feng, Z. Lin, X. Shen, K. Chen, H. Jiang, and D. Liu Bcl-xL forms two distinct homodimers at non-ionic detergents: Implications in the dimerization of Bcl-2 family proteins Journal of Biochemistry 143 2008 243 252
32. J.I. Fletcher, S. Meusburger, C.J. Hawkins, D.T. Riglar, E.F. Lee, and W.D. Fairlie et al. Apoptosis is triggered when prosurvival Bcl-2 proteins cannot restrain Bax Proceedings of the National Academy of Sciences of the United States of America 105 2008 18081 18087
33. A.V. Follis, J.E. Chipuk, J.C. Fisher, M.K. Yun, C.R. Grace, and A. Nourse et al. PUMA binding induces partial unfolding within BCL-xL to disrupt p53 binding and promote apoptosis Nature Chemical Biology 9 2013 163 168
34. P. Fuentes-Prior, and G.S. Salvesen The protein structures that shape caspase activity, specificity, activation and inhibition Biochemical Journal 384 2004 201 232
35. E. Gavathiotis, M. Suzuki, M.L. Davis, K. Pitter, G.H. Bird, and S.G. Katz et al. BAX activation is initiated at a novel interaction site Nature 455 2008 1076 1081
36. M. Giam, T. Okamoto, J.D. Mintern, A. Strasser, and P. Bouillet Bcl-2 family member Bcl-G is not a proapoptotic protein Cell Death and Disease 3 2012 e404
37. S.P. Glaser, E.F. Lee, E. Trounson, P. Bouillet, A. Wei, and W.D. Fairlie et al. Anti-apoptotic Mcl-1 is essential for the development and sustained growth of acute myeloid leukemia Genes and Development 26 2012 120 125
38. P. Gomez-Bougie, R. Bataille, and M. Amiot Endogenous association of Bim BH3-only protein with Mcl-1, Bcl-xL and Bcl-2 on mitochondria in human B cells European Journal of Immunology 35 2005 971 976
39. J. Gsponer, M.E. Futschik, S.A. Teichmann, and M.M. Babu Tight regulation of unstructured proteins: From transcript synthesis to protein degradation Science 322 2008 1365 1368
40. J.M. Gump, and A. Thorburn Autophagy and apoptosis: What is the connection? Trends in Cell Biology 21 2011 387 392
41. J. Han, C. Flemington, A.B. Houghton, Z. Gu, G.P. Zambetti, and R.J. Lutz et al. Expression of bbc3, a pro-apoptotic BH3-only gene, is regulated by diverse cell death and survival signals Proceedings of the National Academy of Sciences of the United States of America 98 2001 11318 11323
42. M. Hanada, C. Aime-Sempe, T. Sato, and J.C. Reed Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax Journal of Biological Chemistry 270 1995 11962 11969
43. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: The next generation Cell 144 2011 646 674
44. J.M. Hardwick, Y.B. Chen, and E.A. Jonas Multipolar functions of BCL-2 proteins link energetics to apoptosis Trends in Cell Biology 22 2012 318 328
45. M.G. Hinds, and C.L. Day Regulation of apoptosis: Uncovering the binding determinants Current Opinion in Structural Biology 15 2005 690 699
46. M.G. Hinds, M. Lackmann, G.L. Skea, P.J. Harrison, D.C. Huang, and C.L. Day The structure of Bcl-w reveals a role for the C-terminal residues in modulating biological activity EMBO Journal 22 2003 1497 1507
47. M.G. Hinds, C. Smits, R. Fredericks-Short, J.M. Risk, M. Bailey, and D.C. Huang 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 and Differentiation 14 2007 128 136
48. S.Y. Hsu, P. Lin, and A.J. Hsueh BOD (Bcl-2-related ovarian death gene) is an ovarian BH3 domain-containing proapoptotic Bcl-2 protein capable of dimerization with diverse antiapoptotic Bcl-2 members Molecular Endocrinology 12 1998 1432 1440
49. W.L. Hsu, C.J. Oldfield, B. Xue, J. Meng, F. Huang, and P. Romero et al. Exploring the binding diversity of intrinsically disordered proteins involved in one-to-many binding Protein Science 22 2013 258 273
50. W. Huang, T. Jiang, W. Choi, S. Qi, Y. Pang, and Q. Hu et al. Mechanistic insights into CED-4-mediated activation of CED-3 Genes and Development 27 2013 2039 2048
51. D.C. Huang, and A. Strasser BH3-Only proteins-essential initiators of apoptotic cell death Cell 103 2000 839 842
52. T. Igaki, and M. Miura Role of Bcl-2 family members in invertebrates Biochimica et Biophysica Acta 1644 2004 73 81
53. K. Imaizumi, M. Tsuda, Y. Imai, A. Wanaka, T. Takagi, and M. Tohyama Molecular cloning of a novel polypeptide, DP5, induced during programmed neuronal death Journal of Biological Chemistry 272 1997 18842 18848
54. N. Inohara, L. Ding, S. Chen, and G. Nunez harakiri, a novel regulator of cell death, encodes a protein that activates apoptosis and interacts selectively with survival-promoting proteins Bcl-2 and Bcl-X(L) EMBO Journal 16 1997 1686 1694
55. C. James, S. Gschmeissner, A. Fraser, and G.I. Evan CED-4 induces chromatin condensation in Schizosaccharomyces pombe and is inhibited by direct physical association with CED-9 Current Biology 7 1997 246 252
56. B. Juhasova, M. Mentel, I. Bhatia-Kissova, I. Zeman, J. Kolarov, and M. Forte et al. BH3-only protein Bim inhibits activity of antiapoptotic members of Bcl-2 family when expressed in yeast FEBS Letters 585 2011 2709 2713
57. R. Kang, H.J. Zeh, M.T. Lotze, and D. Tang The Beclin 1 network regulates autophagy and apoptosis Cell Death and Differentiation 18 2011 571 580
58. T. Kuwana, L. Bouchier-Hayes, J.E. Chipuk, C. Bonzon, B.A. Sullivan, and D.R. Green et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly Molecular Cell 17 2005 525 535
59. M. Kvansakul, and M.G. Hinds Structural biology of the Bcl-2 family and its mimicry by viral proteins Cell Death and Disease 4 2013 e909
60. M. Kvansakul, M.F. van Delft, E.F. Lee, J.M. Gulbis, W.D. Fairlie, and D.C. Huang et al. A structural viral mimic of prosurvival Bcl-2: A pivotal role for sequestering proapoptotic Bax and Bak Molecular Cell 25 2007 933 942
61. M. Kvansakul, A.H. Wei, J.I. Fletcher, S.N. Willis, L. Chen, and A.W. Roberts et al. Structural basis for apoptosis inhibition by Epstein-Barr virus BHRF1 PLoS Pathogens 6 2010 e1001236
62. M. Kvansakul, H. Yang, W.D. Fairlie, P.E. Czabotar, S.F. Fischer, and M.A. Perugini et al. Vaccinia virus anti-apoptotic F1L is a novel Bcl-2-like domain-swapped dimer that binds a highly selective subset of BH3-containing death ligands Cell Death and Differentiation 15 2008 1564 1571
63. C. Lanave, M. Santamaria, and C. Saccone Comparative genomics: The evolutionary history of the Bcl-2 family Gene 333 2004 71 79
64. M. Lasi, B. Pauly, N. Schmidt, M. Cikala, B. Stiening, and T. Kasbauer et al. The molecular cell death machinery in the simple cnidarian Hydra includes an expanded caspase family and pro- and anti-apoptotic Bcl-2 proteins Cell Research 20 2010 812 825
65. E.F. Lee, P.E. Czabotar, M.F. van Delft, E.M. Michalak, M.J. Boyle, and S.N. Willis et al. A novel BH3 ligand that selectively targets Mcl-1 reveals that apoptosis can proceed without Mcl-1 degradation The Journal of Cell Biology 180 2008 341 355
66. E.F. Lee, G. Dewson, B.J. Smith, M. Evangelista, A. Pettikiriarachchi, and C. Dogovski et al. Crystal structure of a BCL-W domain-swapped dimer: Implications for the function of BCL-2 family proteins Structure 19 2011 1467 1476
67. E.S. Leshchiner, C.R. Braun, G.H. Bird, and L.D. Walensky Direct activation of full-length proapoptotic BAK Proceedings of the National Academy of Sciences of the United States of America 110 2013 986 995
68. G. Lessene, P.E. Czabotar, and P.M. Colman BCL-2 family antagonists for cancer therapy Nature Reviews Drug Discovery 7 2008 989 1000
69. X. Liu, S. Dai, Y. Zhu, P. Marrack, and J.W. Kappler The structure of a Bcl-xL/Bim fragment complex: Implications for Bim function Immunity 19 2003 341 352
70. J. Loh, Q. Huang, A.M. Petros, D. Nettesheim, L.F. van Dyk, and L. Labrada et al. A surface groove essential for viral Bcl-2 function during chronic infection in vivo PLoS Pathogens 1 2005 e10
71. J.F. Lovell, L.P. Billen, S. Bindner, A. Shamas-Din, C. Fradin, and B. Leber et al. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax Cell 135 2008 1074 1084
72. M. Marani, T. Tenev, D. Hancock, J. Downward, and N.R. Lemoine Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis Molecular and Cellular Biology 22 2002 3577 3589
73. J.M. McDonnell, D. Fushman, C.L. Milliman, S.J. Korsmeyer, and D. Cowburn Solution structure of the proapoptotic molecule BID: A structural basis for apoptotic agonists and antagonists Cell 96 1999 625 634
74. D. Merino, M. Giam, P.D. Hughes, O.M. Siggs, K. Heger, and L.A. O'Reilly et al. The role of BH3-only protein Bim extends beyond inhibiting Bcl-2-like prosurvival proteins The Journal of Cell Biology 186 2009 355 362
75. C. Mestre-Escorihuela, F. Rubio-Moscardo, J.A. Richter, R. Siebert, J. Climent, and V. Fresquet et al. Homozygous deletions localize novel tumor suppressor genes in B-cell lymphomas Blood 109 2007 271 280
76. T. Moldoveanu, C.R. Grace, F. Llambi, A. Nourse, P. Fitzgerald, and K. Gehring et al. BID-induced structural changes in BAK promote apoptosis Nature Structural and Molecular Biology 20 2013 589 597
77. S.W. Muchmore, M. Sattler, H. Liang, R.P. Meadows, J.E. Harlan, and H.S. Yoon et al. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death Nature 381 1996 335 341
78. K. Nakano, and K.H. Vousden PUMA, a novel proapoptotic gene, is induced by p53 Molecular Cell 7 2001 683 694
79. T. Ni Chonghaile, K.A. Sarosiek, T.T. Vo, J.A. Ryan, A. Tammareddi, and G. Moore Vdel et al. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy Science 334 2011 1129 1133
80. A. Oberstein, P.D. Jeffrey, and Y. Shi Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein Journal of Biological Chemistry 282 2007 13123 13132
81. L. O'Connor, A. Strasser, L.A. O'Reilly, G. Hausmann, J.M. Adams, and S. Cory et al. Bim: A novel member of the Bcl-2 family that promotes apoptosis EMBO Journal 17 1998 384 395
82. E. Oda, R. Ohki, H. Murasawa, J. Nemoto, T. Shibue, and T. Yamashita et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis Science 288 2000 1053 1058
83. T. Okamoto, S. Campbell, N. Mehta, J. Thibault, P.M. Colman, and M. Barry et al. Sheeppox virus SPPV14 encodes a Bcl-2-like cell death inhibitor that counters a distinct set of mammalian proapoptotic proteins Journal of Virology 86 2012 11501 11511
84. T. Oltersdorf, S.W. Elmore, A.R. Shoemaker, R.C. Armstrong, D.J. Augeri, and B.A. Belli et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours Nature 435 2005 677 681
85. J.W. O'Neill, M.K. Manion, B. Maguire, and D.M. Hockenbery BCL-XL dimerization by three-dimensional domain swapping Journal of Molecular Biology 356 2006 367 381
86. Z. Peng, B. Xue, L. Kurgan, and V.N. Uversky Resilience of death: Intrinsic disorder in proteins involved in the programmed cell death Cell Death and Differentiation 20 2013 1257 1267
87. A.M. Petros, D.G. Nettesheim, Y. Wang, E.T. Olejniczak, R.P. Meadows, and J. Mack et al. Rationale for Bcl-xL/Bad peptide complex formation from structure, mutagenesis, and biophysical studies Protein Science 9 2000 2528 2534
88. A.M. Petros, E.T. Olejniczak, and S.W. Fesik Structural biology of the Bcl-2 family of proteins Biochimica et Biophysica Acta 1644 2004 83 94
89. W.J. Placzek, M. Sturlese, B. Wu, J.F. Cellitti, J. Wei, and M. Pellecchia Identification of a novel Mcl-1 protein binding motif Journal of Biological Chemistry 286 2011 39829 39835
90. H. Puthalakath, D.C. Huang, L.A. O'Reilly, S.M. King, and A. Strasser The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex Molecular Cell 3 1999 287 296
91. H. Puthalakath, and A. Strasser Keeping killers on a tight leash: Transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins Cell Death and Differentiation 9 2002 505 512
92. H. Puthalakath, A. Villunger, L.A. O'Reilly, J.G. Beaumont, L. Coultas, and R.E. Cheney et al. Bmf: A proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis Science 293 2001 1829 1832
93. S. Qi, Y. Pang, Q. Hu, Q. Liu, H. Li, and Y. Zhou et al. Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4 Cell 141 2010 446 457
94. G.J. Rautureau, C.L. Day, and M.G. Hinds Intrinsically disordered proteins in bcl-2 regulated apoptosis International Journal of Molecular Sciences 11 2010 1808 1824
95. G.J. Rautureau, M. Yabal, H. Yang, D.C. Huang, M. Kvansakul, and M.G. Hinds The restricted binding repertoire of Bcl-B leaves Bim as the universal BH3-only prosurvival Bcl-2 protein antagonist Cell Death and Disease 3 2012 e443
96. K.A. Sarosiek, X. Chi, J.A. Bachman, J.J. Sims, J. Montero, and L. Patel et al. BID preferentially activates BAK while BIM preferentially activates BAX, affecting chemotherapy response Molecular Cell 51 2013 751 765
97. T. Sato, M. Hanada, S. Bodrug, S. Irie, N. Iwama, and L.H. Boise et al. Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system Proceedings of the National Academy of Sciences of the United States of America 91 1994 9238 9242
98. T. Sato, S. Irie, S. Krajewski, and J.C. Reed Cloning and sequencing of a cDNA encoding the rat Bcl-2 protein Gene 140 1994 291 292
99. M. Sattler, H. Liang, D. Nettesheim, R.P. Meadows, J.E. Harlan, and M. Eberstadt et al. Structure of Bcl-xL-Bak peptide complex: Recognition between regulators of apoptosis Science 275 1997 983 986
100. B. Schumacher, C. Schertel, N. Wittenburg, S. Tuck, S. Mitani, and A. Gartner et al. C. elegans ced-13 can promote apoptosis and is induced in response to DNA damage Cell Death and Differentiation 12 2005 153 161
101. A. Shamas-Din, S. Bindner, W. Zhu, Y. Zaltsman, C. Campbell, and A. Gross et al. tBid undergoes multiple conformational changes at the membrane required for Bax activation Journal of Biological Chemistry 288 2013 22111 22127
102. A. Shamas-Din, J. Kale, B. Leber, and D.W. Andrews Mechanisms of action of Bcl-2 family proteins Cold Spring Harbor Perspectives in Biology 5 2013 a008714
103. A.J. Souers, J.D. Leverson, E.R. Boghaert, S.L. Ackler, N.D. Catron, and J. Chen et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets Nature Medicine 19 2013 202 208
104. M.L. Stewart, E. Fire, A.E. Keating, and L.D. Walensky The MCL-1 BH3 helix is an exclusive MCL-1 inhibitor and apoptosis sensitizer Nature Chemical Biology 6 2010 595 601
105. A. Strasser, S. Cory, and J.M. Adams Deciphering the rules of programmed cell death to improve therapy of cancer and other diseases EMBO Journal 30 2011 3667 3683
106. S.W. Tait, and D.R. Green Mitochondria and cell death: Outer membrane permeabilization and beyond Nature Reviews Molecular Cell Biology 11 2010 621 632
107. J.M. Taylor, and M. Barry Near death experiences: Poxvirus regulation of apoptotic death Virology 344 2006 139 150
108. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochimica et Biophysica Acta 1804 2010 1231 1264
109. L.D. Walensky, A.L. Kung, I. Escher, T.J. Malia, S. Barbuto, and R.D. Wright et al. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix Science 305 2004 1466 1470
110. K. Wang, X.M. Yin, D.T. Chao, C.L. Milliman, and S.J. Korsmeyer BID: A novel BH3 domain-only death agonist Genes and Development 10 1996 2859 2869
111. D. Westphal, E.C. Ledgerwood, J.D. Tyndall, M.H. Hibma, N. Ueda, and S.B. Fleming et al. The orf virus inhibitor of apoptosis functions in a Bcl-2-like manner, binding and neutralizing a set of BH3-only proteins and active Bax Apoptosis 14 2009 1317 1330
112. C.M. Wiggins, P. Tsvetkov, M. Johnson, C.L. Joyce, C.A. Lamb, and N.J. Bryant et al. BIM(EL), an intrinsically disordered protein, is degraded by 20S proteasomes in the absence of poly-ubiquitylation Journal of Cell Science 124 2011 969 977
113. F. Wilfling, A. Weber, S. Potthoff, F.N. Vogtle, C. Meisinger, and S.A. Paschen et al. BH3-only proteins are tail-anchored in the outer mitochondrial membrane and can initiate the activation of Bax Cell Death and Differentiation 19 2012 1328 1336
114. W.H. Wilson, O.A. O'Connor, M.S. Czuczman, A.S. LaCasce, J.F. Gerecitano, and J.P. Leonard et al. Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: A phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity Lancet Oncology 11 2010 1149 1159
115. J. Wilson-Annan, L.A. O'Reilly, S.A. Crawford, G. Hausmann, J.G. Beaumont, and L.P. Parma et al. Proapoptotic BH3-only proteins trigger membrane integration of prosurvival Bcl-w and neutralize its activity The Journal of Cell Biology 162 2003 877 887
116. N. Yan, J. Chai, E.S. Lee, L. Gu, Q. Liu, and J. He et al. Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans Nature 437 2005 831 837
117. N. Yan, L. Gu, D. Kokel, J. Chai, W. Li, and A. Han et al. Structural, biochemical, and functional analyses of CED-9 recognition by the proapoptotic proteins EGL-1 and CED-4 Molecular Cell 15 2004 999 1006
118. E. Yang, J. Zha, J. Jockel, L.H. Boise, C.B. Thompson, and S.J. Korsmeyer Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death Cell 80 1995 285 291
119. Y. Yao, A.A. Bobkov, L.A. Plesniak, and F.M. Marassi Mapping the interaction of pro-apoptotic tBID with pro-survival BCL-XL Biochemistry 48 2009 8704 8711
120. X.M. Yin, Z.N. Oltvai, and S.J. Korsmeyer BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax Nature 369 1994 321 323
121. R.J. Youle, and A. Strasser The BCL-2 protein family: Opposing activities that mediate cell death Nature Reviews Molecular Cell Biology 9 2008 47 59
122. J. Yu, L. Zhang, P.M. Hwang, K.W. Kinzler, and B. Vogelstein PUMA induces the rapid apoptosis of colorectal cancer cells Molecular Cell 7 2001 673 682
123. J. Zha, H. Harada, E. Yang, J. Jockel, and S.J. Korsmeyer Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L) Cell 87 1996 619 628
124. S. Zhang, and A.J. Link Bcl-2 family interactome analysis using bacterial surface display Integrative Biology 3 2011 823 831