De-novo designed library of benzoylureas as inhibitors of BCL-X L: Synthesis, structural and biochemical characterization

Journal of Medicinal Chemistry

Volumn 57, Issue 4, 2014, Pages 1323-1343

  Brady, Ryan M ^a,b,c   Vom, Amelia ^a,b   Roy, Michael J ^a,b   Toovey, Nathan ^a,b   Smith, Brian J ^a,b,d   Moss, Rebecca M ^a,b   Hatzis, Effie ^a,b   Huang, David C S ^a,b   Parisot, John P ^a,b,e   Yang, Hong ^a,b   Street, Ian P ^a,b   Colman, Peter M ^a,b   Czabotar, Peter E ^a,b   Baell, Jonathan B ^a,b,c   Lessene, Guillaume ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d LA TROBE UNIVERSITY   (Australia)

^e PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

2 [3 (BIPHENYLCARBONYL) 3 PROPYLUREIDO] 3 (1H INDOLE 3 YL)PROPANOIC ACID; 2 [3 (BIPHENYLCARBONYL) 3 PROPYLUREIDO] 3 (4 HYDROXYPHENYL)PENTANOIC ACID; 2 [3 (BIPHENYLCARBONYL) 3 PROPYLUREIDO] 3 PHENYLPENTANOIC ACID; 2 [3 (BIPHENYLCARBONYL) 3 PROPYLUREIDO] 4 METHYLPENTANOIC ACID; 2 [3 (BIPHENYLCARBONYL) 3 PROPYLUREIDO] 4 PHENYLBUTANOIC ACID; 2 [3 BENZYL 3 (BIPHENYLCARBONYL)UREIDO] 3 (BENZYLTHIO)PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (2' CHLOROBIPHENYLCARBONYL) 3 PROPYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (3',4' DICHLOROBIPHENYLCARBONYL) 3 PROPYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (4' CHLOROBIPHENYLCARBONYL) 3 PROPYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (4' METHOXYBIPHENYLCARBONYL) 3 PROPYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (4' METHYLBIPHENYLCARBONYL) 3 PROPYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (BIPHENYLCARBONYL) 3 [4 METHYLBENZYL)UREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (BIPHENYLCARBONYL) 3 BUTYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (BIPHENYLCARBONYL) 3 ISOPROPYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (BIPHENYLCARBONYL) 3 PROPYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 (BIPHENYLCARBONYL) 3 SEC BUTYLUREIDO]PROPANOIC ACID; 3 (BENZYLTHIO) 2 [3 [3 (NAPHTHALEN 2 YL)BENZOYL] 3 PROPYLUREIDO]PROPANOIC ACID; ANTINEOPLASTIC AGENT; BH3 PROTEIN; METHYL 3 (BENZYLTHIO) 2 [3 (BIPHENYLCARBONYL) 3 PROPYLUREIDO]PROPANOATE; N (METHYLCARBAMOYL) N PROPYLBIPHENYL 3 CARBOXAMIDE; N [1 AMINO 3 (BENZYLTHIO) 1 OXOPROPAN 2 YLCARBAMOYL] N PROPYLBIPHENYL 3 CARBOXAMIDE; N [2 (BENZYLTHIO)ETHYLCARBAMOYL] N PROPYLBIPHENYL 3 CARBOXAMIDE; PEPTIDOMIMETIC AGENT; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN BCL XL INHIBITOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; UREA DERIVATIVE;

AMINO ACID SUBSTITUTION; ARTICLE; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG SELECTIVITY; DRUG SYNTHESIS; IC 50; MOLECULAR LIBRARY; MOLECULAR MODEL; PROTEIN PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

BCL-X PROTEIN; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR MIMICRY; MOLECULAR STRUCTURE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STRUCTURE-ACTIVITY RELATIONSHIP; UREA;

EID: 84896847690     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm401948b     Document Type: Article

References (60)

1. Hotchkiss, R. S.; Strasser, A.; McDunn, J. E.; Swanson, P. E. Cell death N. Engl. J. Med. 2009, 361, 1570-1583
2. Strasser, A.; Cory, S.; Adams, J. M. Deciphering the rules of programmed cell death to improve therapy of cancer and other diseases EMBO J. 2011, 30, 3667-3683
3. Villunger, A.; Labi, V.; Bouillet, P.; Adams, J.; Strasser, A. Can the analysis of BH3-only protein knockout mice clarify the issue of "direct versus indirect" activation of Bax and Bak? Cell Death Differ. 2011, 18, 1545-1546
4. Hanahan, D.; Weinberg, R. A. The hallmarks of cancer Cell 2000, 100, 57-70
5. Beroukhim, R.; Mermel, C. H.; Porter, D.; Wei, G.; Raychaudhuri, S.; Donovan, J.; Barretina, J.; Boehm, J. S.; Dobson, J.; Urashima, M.; Henry, K. T. M.; Pinchback, R. M.; Ligon, A. H.; Cho, Y.; Haery, L.; Greulich, H.; Reich, M.; Winckler, W.; Lawrence, M. S.; Weir, B. A.; Tanaka, K. E.; Chiang, D. Y.; Bass, A. J.; Loo, A.; Hoffman, C.; Prensner, J.; Liefeld, T.; Gao, Q.; Yecies, D.; Signoretti, S.; Maher, E.; Kaye, F. J.; Sasaki, H.; Tepper, J. E.; Fletcher, J. A.; Tabernero, J.; Baselga, J.; Tsao, M.; Demichelis, F.; Rubin, M. A.; Janne, P. A.; Daly, M. J.; Nucera, C.; Levine, R. L.; Ebert, B. L.; Gabriel, S.; Rustgi, A. K.; Antonescu, C. R.; Ladanyi, M.; Letai, A.; Garraway, L. A.; Loda, M.; Beer, D. G.; True, L. D.; Okamoto, A.; Pomeroy, S. L.; Singer, S.; Golub, T.; Lander, E. S.; Getz, G.; Sellers, W. R.; Meyerson, M. The landscape of somatic copy-number alteration across human cancers Nature 2010, 463, 899-905
6. Amundson, S. A.; Myers, T. G.; Scudiero, D.; Kitada, S.; Reed, J. C.; Fornace, A. J., Jr. An informatics approach identifying markers of chemosensitivity in human cancer cell lines Cancer Res. 2000, 60, 6101-6110
7. Czabotar, P. E.; Lessene, G. Bcl-2 family proteins as therapeutic targets Curr. Pharm. Des. 2010, 16, 3132-3148
8. Lessene, G.; Czabotar, P. E.; Colman, P. M. BCL-2 family antagonists for cancer therapy Nat. Rev. Drug Discovery 2008, 7, 989-1000
9. van Delft, M. F.; Wei, A. H.; Mason, K. D.; Vandenberg, C. J.; Chen, L.; Czabotar, P. E.; Willis, S. N.; Scott, C. L.; Day, C. L.; Cory, S.; Adams, J. M.; Roberts, A. W.; Huang, D. C. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized Cancer Cell 2006, 10, 389-399
10. Varadarajan, S.; Vogler, M.; Butterworth, M.; Dinsdale, D.; Walensky, L. D.; Cohen, G. M. Evaluation and critical assessment of putative MCL-1 inhibitors Cell Death Differ. 2013, 20, 1475-1484
11. Ernst, J. T.; Becerril, J.; Park, H. S.; Yin, H.; Hamilton, A. D. Design and application of an α-helix-mimetic scaffold based on an oligoamide-foldamer strategy: antagonism of the Bak BH3/Bcl-xL complex Angew. Chem., Int. Ed. 2003, 42, 535-539
12. Kutzki, O.; Park, H. S.; Ernst, J. T.; Orner, B. P.; Yin, H.; Hamilton, A. D. Development of a potent Bcl-x(L) antagonist based on alpha-helix mimicry J. Am. Chem. Soc. 2002, 124, 11838-11839
13. Kim, I. C.; Hamilton, A. D. Diphenylindane-based proteomimetics reproduce the projection of the i, i+3, i+4, and i+7 residues on an alpha-helix Org. Lett. 2006, 8, 1751-1754
14. Yin, H.; Hamilton, A. D. Terephthalamide derivatives as mimetics of the helical region of Bak peptide target Bcl-xL protein Bioorg. Med. Chem. Lett. 2004, 14, 1375-1379
15. Bruncko, M.; Oost, T. K.; Belli, B. A.; Ding, H.; Joseph, M. K.; Kunzer, A.; Martineau, D.; McClellan, W. J.; Mitten, M.; Ng, S. C.; Nimmer, P. M.; Oltersdorf, T.; Park, C. M.; Petros, A. M.; Shoemaker, A. R.; Song, X. H.; Wang, X. L.; Wendt, M. D.; Zhang, H. C.; Fesik, S. W.; Rosenberg, S. H.; Elmore, S. W. Studies leading to potent, dual inhibitors of Bcl-2 and Bcl-xL J. Med. Chem. 2007, 50, 641-662
16. Oltersdorf, T.; Elmore, S. W.; Shoemaker, A. R.; Armstrong, R. C.; Augeri, D. J.; Belli, B. A.; Bruncko, M.; Deckwerth, T. L.; Dinges, J.; Hajduk, P. J.; Joseph, M. K.; Kitada, S.; Korsmeyer, S. J.; Kunzer, A. R.; Letai, A.; Li, C.; Mitten, M. J.; Nettesheim, D. G.; Ng, S.; Nimmer, P. M.; O'Connor, J. M.; Oleksijew, A.; Petros, A. M.; Reed, J. C.; Shen, W.; Tahir, S. K.; Thompson, C. B.; Tomaselli, K. J.; Wang, B. L.; Wendt, M. D.; Zhang, H. C.; Fesik, S. W.; Rosenberg, S. H. An inhibitor of Bcl-2 family proteins induces regression of solid tumours Nature 2005, 435, 677-681
17. Park, C. M.; Bruncko, M.; Adickes, J.; Bauch, J.; Ding, H.; Kunzer, A.; Marsh, K. C.; Nimmer, P.; Shoemaker, A. R.; Song, X.; Tahir, S. K.; Tse, C.; Wang, X.; Wendt, M. D.; Yang, X.; Zhang, H.; Fesik, S. W.; Rosenberg, S. H.; Elmore, S. W. Discovery of an orally bioavailable small molecule inhibitor of prosurvival B-cell lymphoma 2 proteins J. Med. Chem. 2008, 51, 6902-6915
18. Souers, A. J.; Leverson, J. D.; Boghaert, E. R.; Ackler, S. L.; Catron, N. D.; Chen, J.; Dayton, B. D.; Ding, H.; Enschede, S. H.; Fairbrother, W. J.; Huang, D. C.; Hymowitz, S. G.; Jin, S.; Khaw, S. L.; Kovar, P. J.; Lam, L. T.; Lee, J.; Maecker, H. L.; Marsh, K. C.; Mason, K. D.; Mitten, M. J.; Nimmer, P. M.; Oleksijew, A.; Park, C. H.; Park, C. M.; Phillips, D. C.; Roberts, A. W.; Sampath, D.; Seymour, J. F.; Smith, M. L.; Sullivan, G. M.; Tahir, S. K.; Tse, C.; Wendt, M. D.; Xiao, Y.; Xue, J. C.; Zhang, H.; Humerickhouse, R. A.; Rosenberg, S. H.; Elmore, S. W. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets Nat. Med. 2013, 19, 202-208
19. Zhou, H.; Aguilar, A.; Chen, J.; Bai, L.; Liu, L.; Meagher, J. L.; Yang, C.-Y.; Mceachern, D.; Cong, X.; Stuckey, J. A.; Wang, S. Structure-based design of potent Bcl-2/Bcl-xL inhibitors with strong in vivo antitumor activity J. Med. Chem. 2012, 55, 6149-6161
20. Zhou, H.; Chen, J.; Meagher, J. L.; Yang, C.-Y.; Aguilar, A.; Liu, L.; Bai, L.; Cong, X.; Cai, Q.; Fang, X.; Stuckey, J. A.; Wang, S. Design of Bcl-2 and Bcl-xL inhibitors with subnanomolar binding affinities based upon a new scaffold J. Med. Chem. 2012, 55, 4664-4682
21. Sleebs, B. E.; Czabotar, P. E.; Fairbrother, W. J.; Fairlie, W. D.; Flygare, J. A.; Huang, D. C.; Kersten, W. J.; Koehler, M. F.; Lessene, G.; Lowes, K.; Parisot, J. P.; Smith, B. J.; Smith, M. L.; Souers, A. J.; Street, I. P.; Yang, H.; Baell, J. B. Quinazoline sulfonamides as dual binders of the proteins B-cell lymphoma 2 and B-cell lymphoma extra long with potent proapoptotic cell-based activity J. Med. Chem. 2011, 54, 1914-1926
22. Tanaka, Y.; Aikawa, K.; Nishida, G.; Homma, M.; Sogabe, S.; Igaki, S.; Hayano, Y.; Sameshima, T.; Miyahisa, I.; Kawamoto, T.; Tawada, M.; Imai, Y.; Inazuka, M.; Cho, N.; Imaeda, Y.; Ishikawa, T. Discovery of potent Mcl-1/Bcl-xL dual inhibitors by using a hybridization strategy based on structural analysis of target proteins J. Med. Chem. 2013, 56, 9635-9345
23. Sleebs, B. E.; Kersten, W. J.; Kulasegaram, S.; Nikolakopoulos, G.; Hatzis, E.; Moss, R. M.; Parisot, J. P.; Yang, H.; Czabotar, P. E.; Fairlie, W. D.; Lee, E. F.; Adams, J. M.; Chen, L.; van Delft, M. F.; Lowes, K. N.; Wei, A.; Huang, D. C.; Colman, P. M.; Street, I. P.; Baell, J. B.; Watson, K.; Lessene, G. Discovery of potent and selective benzothiazole hydrazone inhibitors of Bcl-XL J. Med. Chem. 2013, 56, 5514-5540
24. Lessene, G.; Czabotar, P. E.; Sleebs, B. E.; Zobel, K.; Lowes, K. N.; Adams, J. M.; Baell, J. B.; Colman, P. M.; Deshayes, K.; Fairbrother, W. J.; Flygare, J. A.; Gibbons, P.; Kersten, W. J. A.; Kulasegaram, S.; Moss, R. M.; Parisot, J. P.; Smith, B. J.; Street, I. P.; Yang, H.; Huang, D. C. S.; Watson, K. G. Structure-guided design of a selective BCL-XL inhibitor Nat. Chem. Biol. 2013, 9, 390-397
25. Baell, J. B.; Duggan, P. J.; Forsyth, S. A.; Lewis, R. J.; Lok, Y. P.; Schroeder, C. I.; Shepherd, N. E. Synthesis and biological evaluation of anthranilamide-based non-peptide mimetics of ω-conotoxin GVIA Tetrahedron 2006, 62, 7284-7292
26. Clackson, T.; Wells, J. A. A hot spot of binding energy in a hormone-receptor interface Science 1995, 267, 383-386
27. Baell, J. B.; Duggan, P. J.; Forsyth, S. A.; Lewis, R. J.; Lok, Y. P.; Schroeder, C. I. Synthesis and biological evaluation of nonpeptide mimetics of co-conotoxin GVIA Bioorg. Med. Chem. 2004, 12, 4025-4037
28. Baell, J. B.; Forsyth, S. A.; Gable, R. W.; Norton, R. S.; Mulder, R. J. Design and synthesis of type-III mimetics of omega-conotoxin GVIA J. Comput.-Aided Mol. Des. 2001, 15, 1119-1136
29. Brady, R. M.; Zhang, M.; Gable, R.; Norton, R. S.; Baell, J. B. De novo design and synthesis of a μ-conotoxin KIIIA peptidomimetic Bioorg. Med. Chem. Lett. 2013, 23, 4892-4895
30. Sattler, M.; Liang, H.; Nettesheim, D.; Meadows, R. P.; Harlan, J. E.; Eberstadt, M.; Yoon, H. S.; Shuker, S. B.; Chang, B. S.; Minn, A. J.; Thompson, C. B.; Fesik, S. W. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis Science 1997, 275, 983-986
31. Petros, A. M.; Nettesheim, D. G.; Wang, Y.; Olejniczak, E. T.; Meadows, R. P.; Mack, J.; Swift, K.; Matayoshi, E. D.; Zhang, H.; Thompson, C. B.; Fesik, S. W. Rationale for Bcl-xL/Bad peptide complex formation from structure, mutagenesis, and biophysical studies Protein Sci. 2000, 9, 2528-2534
32. Liu, X.; Dai, S.; Zhu, Y.; Marrack, P.; Kappler, J. W. The structure of a Bcl-xL/Bim fragment complex: implications for Bim function Immunity 2003, 19, 341-352
33. Czabotar, P. E.; Lee, E. F.; Thompson, G. V.; Wardak, A. Z.; Fairlie, W. D.; Colman, P. M. Mutations to Bax beyond the BH3 domain disrupts interactions with pro-survival proteins and promotes apoptosis J. Biol. Chem. 2011, 286, 7123-7131
34. Czabotar, P. E.; Lee, E. F.; van Delft, M. F.; Day, C. L.; Smith, B. J.; Huang, D. C.; Fairlie, W. D.; Hinds, M. G.; Colman, P. M. Structural insights into the degradation of Mcl-1 induced by BH3 domains Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 6217-6222
35. Hinds, M. G.; Day, C. L. Regulation of apoptosis: uncovering the binding determinants Curr. Opin. Struct. Biol. 2005, 15, 690-699
36. Baell, J. B.; Gill, J. H.; Lacey, E. Computational chemistry and antiparasitic agents Chem. Aust. 1996, 63, 125-129
37. Our work based on the benzoylurea scaffold has been presented in a number of fora: posters (1st Conforth Conference, Sydney 2002; 19th RACI Conference, Lorne 2003; 20th RACI Conference, Cairns 2004) and oral presentations (Connect 2005, 12th RACI Convention, Sydney 2005; 5th and 7th ESH Conference on Mechanisms of Cell Death and Disease: Advances in Therapeutic Intervention and Drug Development, 2004 and 2008). Inspired by our results (note 11 and 13 in Rodriguez, J. M.; Ross, N. T.; Katt, W. P.; Dhar, D.; Lee, G.-i.; Hamilton, A. D. Structure and function of benzoylurea-derived α-helix mimetics targeting the Bcl-xL/Bak binding interface. ChemMedChem 2009, 4, 649-656), the Hamilton group reported a similar use of this core for the preparation of extended α-helical mimetics.
38. Lessene, G.; Smith, B. J.; Gable, R. W.; Baell, J. B. Characterization of the two fundamental conformations of benzoylureas and elucidation of the factors that facilitate their conformational interchange J. Org. Chem. 2009, 74, 6511-6525
39. Brady, R. M.; Hatzis, E.; Connor, T.; Street, I. P.; Baell, J. B.; Lessene, G. Synthesis of conformationally constrained benzoylureas as BH3-mimetics Org. Biomol. Chem. 2012, 10, 5230-5237
40. Brady, R. M.; Khakham, Y.; Lessene, G.; Baell, J. B. Benzoylureas as removable cis amide inducers: synthesis of cyclic amides via ring closing metathesis (RCM) Org. Biomol. Chem. 2011, 9, 656-658
41. Leadbeater, N. E.; Tominack, B. J. Rapid, easy copper-free Sonogashira couplings using aryl iodides and activated aryl bromides Tetrahedron Lett. 2003, 44, 8653-8656
42. Fürstner, A.; Leitner, A. Iron-catalyzed cross-coupling reactions of alkyl-Grignard reagents with aryl chlorides, tosylates, and triflates Angew. Chem., Int. Ed. 2002, 41, 609-612
43. Seko, T.; Kato, M.; Kohno, H.; Ono, S.; Hashimura, K.; Takimizu, H.; Nakai, K.; Maegawa, H.; Katsube, N.; Toda, M. Structure-activity study of l-amino acid-based N-type calcium channel blockers Bioorg. Med. Chem. 2003, 11, 1901-1913
44. Petros, A. M.; Dinges, J.; Augeri, D. J.; Baumeister, S. A.; Betebenner, D. A.; Bures, M. G.; Elmore, S. W.; Hajduk, P. J.; Joseph, M. K.; Landis, S. K.; Nettesheim, D. G.; Rosenberg, S. H.; Shen, W.; Thomas, S.; Wang, X.; Zanze, I.; Zhang, H.; Fesik, S. W. Discovery of a potent inhibitor of the antiapoptotic protein Bcl-xL from NMR and parallel synthesis J. Med. Chem. 2006, 49, 656-663
45. Chen, L.; Willis, S. N.; Wei, A.; Smith, B. J.; Fletcher, J. I.; Hinds, M. G.; Colman, P. M.; Day, C. L.; Adams, J. M.; Huang, D. C. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function Mol. Cell 2005, 17, 393-403
46. Lee, E. F.; Czabotar, P. E.; Smith, B. J.; Deshayes, K.; Zobel, K.; Colman, P. M.; Fairlie, W. D. Crystal structure of ABT-737 complexed with Bcl-x(L): implications for selectivity of antagonists of the Bcl-2 family Cell Death Differ. 2007, 14, 1711-1713
47. Friberg, A.; Vigil, D.; Zhao, B.; Daniels, R. N.; Burke, J. P.; Garcia-Barrantes, P. M.; Camper, D.; Chauder, B. A.; Lee, T.; Olejniczak, E. T.; Fesik, S. W. Discovery of potent myeloid cell leukemia 1 (Mcl-1) inhibitors using fragment-based methods and structure-based design J. Med. Chem. 2013, 56, 15-30
48. van Herwijnen, H. W.; Brinker, U. H. Meta selectivity in the Friedel-Crafts reaction induced by a faujasite-type zeolite J. Org. Chem. 2001, 66, 2874-2876
49. Lee, E. F.; Czabotar, P. E.; van Delft, M. F.; Michalak, E. M.; Boyle, M. J.; Willis, S. N.; Puthalakath, H.; Bouillet, P.; Colman, P. M.; Huang, D. C.; Fairlie, W. D. A novel BH3 ligand that selectively targets Mcl-1 reveals that apoptosis can proceed without Mcl-1 degradation J. Cell Biol. 2008, 180, 341-355
50. Lee, E. F.; Fedorova, A.; Zobel, K.; Boyle, M. J.; Yang, H.; Perugini, M. A.; Colman, P. M.; Huang, D. C.; Deshayes, K.; Fairlie, W. D. Novel Bcl-2 homology-3 domain-like sequences identified from screening randomized peptide libraries for inhibitors of the pro-survival Bcl-2 proteins J. Biol. Chem. 2009, 284, 31315-31326
51. Kvansakul, M.; Yang, H.; Fairlie, W. D.; Czabotar, P. E.; Fischer, S. F.; Perugini, M. A.; Huang, D. C.; Colman, P. M. 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 Differ. 2008, 15, 1564-1571
52. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode. In Macromolecular Crystallography. Part A; Carter, C. W., Jr.; Sweet, R. M., Eds.; Methods in Enzymology, Vol. 276; Academic Press: San Diego, CA, 1997; pp 307-326.
53. Kabsch, W. Xds. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 125-132
54. McCoy, A. J.; Grosse-Kunstleve, R. W.; Adams, P. D.; Winn, M. D.; Storoni, L. C.; Read, R. J. Phaser crystallographic software J. App. Crystallogr. 2007, 40, 658-674
55. Read, R. J. Pushing the boundaries of molecular replacement with maximum likelihood Acta Crystallogr., Sect. D: Biol. Crystallogr. 2001, 57, 1373-1382
56. Storoni, L. C.; McCoy, A. J.; Read, R. J. Likelihood-enhanced fast rotation functions Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 432-438
57. Muchmore, S. W.; Sattler, M.; Liang, H.; Meadows, R. P.; Harlan, J. E.; Yoon, H. S.; Nettesheim, D.; Chang, B. S.; Thompson, C. B.; Wong, S. L.; Ng, S. L.; Fesik, S. W. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death Nature 1996, 381, 335-341
58. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 2126-2132
59. Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 1997, 53, 240-255
60. Adams, P. D.; Afonine, P. V.; Bunkoczi, G.; Chen, V. B.; Davis, I. W.; Echols, N.; Headd, J. J.; Hung, L. W.; Kapral, G. J.; Grosse-Kunstleve, R. W.; McCoy, A. J.; Moriarty, N. W.; Oeffner, R.; Read, R. J.; Richardson, D. C.; Richardson, J. S.; Terwilliger, T. C.; Zwart, P. H. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 213-221