Bh3 induced conformational changes in Bcl-Xl revealed by crystal structure and comparative analysis

Proteins: Structure, Function and Bioinformatics

Volumn 83, Issue 7, 2015, Pages 1262-1272

  Rajan, Sreekanth ^a   Choi, Minjoo ^a   Baek, Kwanghee ^b   Yoon, Ho Sup ^a,b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b Kyung Hee University   (South Korea)

Author keywords

Apoptosis; Bcl XL; BH3 binding; BID; BIM; Mitochondria; Structure comparison

Indexed keywords

A1 PROTEIN; BH3 PROTEIN; F1L PROTEIN; PROTEIN; PROTEIN BAX; PROTEIN BCL XL; PROTEIN BID; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BCL2L1 PROTEIN, HUMAN; BCL2L11 PROTEIN, HUMAN; BID PROTEIN, HUMAN; BIM PROTEIN; MEMBRANE PROTEIN; ONCOPROTEIN; PEPTIDE; PROTEIN BCL X; PROTEIN BINDING; RECOMBINANT PROTEIN;

ALPHA HELIX; APOPTOSIS; ARTICLE; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLIZATION; HYDROGEN BOND; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL PHENOMENA; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR CLONING; MOLECULAR GENETICS; MOLECULAR MODEL; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; APOPTOSIS REGULATORY PROTEINS; BCL-2-LIKE PROTEIN 11; BCL-X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; BINDING SITES; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84931004856     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24816     Document Type: Article

References (76)

1. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495-516.
2. Orrenius S. Apoptosis: molecular mechanisms and implications for human disease. J Intern Med 1995;237:529-536.
3. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995;267:1456-1462.
4. Yan N, Shi Y. Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol 2005;21:35-56.
5. Volkmann N, Marassi FM, Newmeyer DD, Hanein D. The rheostat in the membrane: BCL-2 family proteins and apoptosis. Cell Death Differ 2013;21:206-215.
6. Petros AM, Olejniczak ET, Fesik SW. Structural biology of the Bcl-2 family of proteins. Biochim Biophys Acta 2004;1644:83-94.
7. Czabotar PE, Lessene G, Strasser A, Adams JM. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 2014;15:49-63.
8. Kvansakul M, Hinds MG. Structural biology of the Bcl-2 family and its mimicry by viral proteins. Cell Death Dis 2013;4:e909
9. Wilson WH, O'Connor OA, Czuczman MS, LaCasce AS, Gerecitano JF, Leonard JP, Tulpule A, Dunleavy K, Xiong H, Chiu YL, Cui Y, Busman T, Elmore SW, Rosenberg SH, Krivoshik AP, Enschede SH, Humerickhouse RA. 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 Oncol 2010;11:1149-1159.
10. Vogler M, Dinsdale D, Dyer MJ, Cohen GM. Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ 2009;16:360-367.
11. Hann CL, Daniel VC, Sugar EA, Dobromilskaya I, Murphy SC, Cope L, Lin X, Hierman JS, Wilburn DL, Watkins DN, Rudin CM. Therapeutic efficacy of ABT-737, a selective inhibitor of BCL-2, in small cell lung cancer. Cancer Res 2008;68:2321-2328.
12. Lessene G, Czabotar PE, Sleebs BE, Zobel K, Lowes KN, Adams JM, Baell JB, Colman PM, Deshayes K, Fairbrother WJ, Flygare JA, Gibbons P, Kersten WJ, Kulasegaram S, Moss RM, Parisot JP, Smith BJ, Street IP, Yang H, Huang DC, Watson KG. Structure-guided design of a selective BCL-X(L) inhibitor. Nat Chem Biol 2013;9:390-397.
13. Wang JL, Liu D, Zhang ZJ, Shan S, Han X, Srinivasula SM, Croce CM, Alnemri ES, Huang Z. Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc Natl Acad Sci U S A 2000;97:7124-7129.
14. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, Joseph MK, Kitada S, Korsmeyer SJ, Kunzer AR, Letai A, Li C, Mitten MJ, Nettesheim DG, Ng S, Nimmer PM, O'Connor JM, Oleksijew A, Petros AM, Reed JC, Shen W, Tahir SK, Thompson CB, Tomaselli KJ, Wang B, Wendt MD, Zhang H, Fesik SW, Rosenberg SH. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005;435:677-681.
15. Souers AJ, Leverson JD, Boghaert ER, Ackler SL, Catron ND, Chen J, Dayton BD, Ding H, Enschede SH, Fairbrother WJ, Huang DC, Hymowitz SG, Jin S, Khaw SL, Kovar PJ, Lam LT, Lee J, Maecker HL, Marsh KC, Mason KD, Mitten MJ, Nimmer PM, Oleksijew A, Park CH, Park CM, Phillips DC, Roberts AW, Sampath D, Seymour JF, Smith ML, Sullivan GM, Tahir SK, Tse C, Wendt MD, Xiao Y, Xue JC, Zhang H, Humerickhouse RA, Rosenberg SH, Elmore SW. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med 2013;19:202-208.
16. Reed JC. Mechanisms of apoptosis. Am J Pathol 2000;157:1415-1430.
17. Kvansakul M, Hinds MG. The structural biology of BH3-only proteins. Methods Enzymol 2014;544:49-74.
18. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SL, Ng SL, Fesik SW. Xray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 1996;381:335-341.
19. Liu X, Dai S, Zhu Y, Marrack P, Kappler JW. The structure of a Bcl-xL/bim fragment complex: implications for bim function. Immunity 2003;19:341-352.
20. Lee EF, Sadowsky JD, Smith BJ, Czabotar PE, Peterson-Kaufman KJ, Colman PM, Gellman SH, Fairlie WD. High-resolution structural characterization of a helical alpha/beta-peptide foldamer bound to the anti-apoptotic protein Bcl-xL. Angew Chem Int Ed Engl 2009;48:4318-4322.
21. Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, Eberstadt M, Yoon HS, Shuker SB, Chang BS, Minn AJ, Thompson CB, Fesik SW. Structure of Bcl-xL-bak peptide complex: recognition between regulators of apoptosis. Science 1997;275:983-986.
22. Czabotar PE, Lee EF, Thompson GV, Wardak AZ, Fairlie WD, Colman PM. Mutation to bax beyond the bh3 domain disrupts interactions with pro-survival proteins and promotes apoptosis. J Biol Chem 2011;286:7123-7131.
23. Follis AV, Chipuk JE, Fisher JC, Yun MK, Grace CR, Nourse A, Baran K, Ou L, Min L, White SW, Green DR, Kriwacki RW. PUMA binding induces partial unfolding within BCL-xL to disrupt p53 binding and promote apoptosis. Nat Chem Biol 2013;9:163-168.
24. Ambrosi E, Capaldi S, Bovi M, Saccomani G, Perduca M, Monaco HL. Structural changes in the bh3 domain of SOUL protein upon interaction with the anti-apoptotic protein Bcl-xL. Biochem J 2011;438:291-301.
25. Oberstein A, Jeffrey PD, Shi Y. Crystal structure of the Bcl-XL-beclin 1 peptide complex: beclin 1 is a novel BH3-only protein. J Biol Chem 2007; 282:13123-13132.
26. Boersma MD, Haase HS, Peterson-Kaufman KJ, Lee EF, Clarke OB, Colman PM, Smith BJ, Horne WS, Fairlie WD, Gellman SH. Evaluation of diverse alpha/beta-backbone patterns for functional alpha-helix mimicry: analogues of the bim bh3 domain. J Am Chem Soc 2012;134:315-323.
27. Lee EF, Czabotar PE, Yang H, Sleebs BE, Lessene G, Colman PM, Smith BJ, Fairlie WD. Conformational changes in Bcl-2 pro-survival proteins determine their capacity to bind ligands. J Biol Chem 2009;284:30508-30517.
28. Okamoto T, Zobel K, Fedorova A, Quan C, Yang H, Fairbrother WJ, Huang DC, Smith BJ, Deshayes K, Czabotar PE. Stabilizing the pro-apoptotic BimBH3 helix (BimSAHB) does not necessarily enhance affinity or biological activity. ACS Chem Biol 2013;8:297-302.
29. Wysoczanski P, Mart RJ, Loveridge EJ, Williams C, Whittaker SB, Crump MP, Allemann RK. NMR solution structure of a photoswitchable apoptosis activating bak peptide bound to Bcl-xL. J Am Chem Soc 2012;134:7644-7647.
30. DeBartolo J, Taipale M, Keating AE. Genome-wide prediction and validation of peptides that bind human prosurvival bcl-2 proteins. PLoS Comput Biol 2014;10:e1003693
31. Walensky LD, Kung AL, Escher I, Malia TJ, Barbuto S, Wright RD, Wagner G, Verdine GL, Korsmeyer SJ. Activation of apoptosis in vivo by a hydrocarbon-stapled bh3 helix. Science 2004;305:1466-1470.
32. Bhat V, Olenick MB, Schuchardt BJ, Mikles DC, McDonald CB, Farooq A. Molecular determinants of the binding specificity of bh3 ligands to BclXL apoptotic repressor. Biopolymers 2014;101:573-582.
33. Chi X, Kale J, Leber B, Andrews DW. Regulating cell death at, on, and in membranes. Biochim Biophys Acta 2014;1843:2100-2113.
34. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, Leber B, Andrews DW. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by bax. Cell 2008;135:1074-1084.
35. 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.
36. Chou JJ, Li H, Salvesen GS, Yuan J, Wagner G. Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell 1999;96:615-624.
37. McDonnell JM, Fushman D, Milliman CL, Korsmeyer SJ, Cowburn D. Solution structure of the proapoptotic molecule BID: a structural basis for apoptotic agonists and antagonists. Cell 1999;96:625-634.
38. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988;335:440-442.
39. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 2011;67:271-281.
40. Evans P. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 2006;62:72-82.
41. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. Overview of the ccp4 suite and current developments. Acta Crystallogr D Biol Crystallogr 2011;67:235-242.
42. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr 2007;40:658-674.
43. Schroeder GM, Wei D, Banfi P, Cai ZW, Lippy J, Menichincheri M, Modugno M, Naglich J, Penhallow B, Perez HL, Sack J, Schmidt RJ, Tebben A, Yan C, Zhang L, Galvani A, Lombardo LJ, Borzilleri RM. Pyrazole and pyrimidine phenylacylsulfonamides as dual Bcl-2/Bcl-xL antagonists. Bioorg Med Chem Lett 2012;22:3951-3956.
44. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010;66:213-221.
45. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004;60:2126-2132.
46. Chen VB, Arendall WB, 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010;66:12-21.
47. Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol 2007;372:774-797.
48. Yap K. University of Toronto.
49. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 2006; 34:W116-118.
50. Ramachandran GN, Ramakrishnan C, Sasisekharan V. Stereochemistry of polypeptide chain configurations. J Mol Biol 1963; 7:95-99.
51. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and clustal X version 2.0. Bioinformatics 2007; 23:2947-2948.
52. Robert X, Gouet P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 2014;42:W320-W324.
53. DeLano WL. The PyMOL molecular graphics system. Palo Alto, CA, USA: DeLano Scientific; 2002.
54. Liao SM, Du QS, Meng JZ, Pang ZW, Huang RB. The multiple roles of histidine in protein interactions. Chem Cent J 2013; 7:44
55. Park CM, Oie T, Petros AM, Zhang H, Nimmer PM, Henry RF, Elmore SW. Design, synthesis, and computational studies of inhibitors of Bcl-XL. J Am Chem Soc 2006;128:16206-16212.
56. Lessene G, Czabotar PE, Colman PM. BCL-2 family antagonists for cancer therapy. Nat Rev Drug Discov 2008;7:989-1000.
57. Czabotar PE, Westphal D, Dewson G, Ma S, Hockings C, Fairlie WD, Lee EF, Yao S, Robin AY, Smith BJ, Huang DC, Kluck RM, Adams JM, Colman PM. Bax crystal structures reveal how bh3 domains activate bax and nucleate its oligomerization to induce apoptosis. Cell 2013;152:519-531.
58. Rautureau GJ, Day CL, Hinds MG. The structure of boo/diva reveals a divergent Bcl-2 protein. Proteins 2010;78:2181-2186.
59. Yoon SJ, Kim EY, Kim YS, Lee HS, Kim KH, Bae J, Lee KA. Role of Bcl2-like 10 (bcl2l10) in regulating mouse oocyte maturation. Biol Reprod 2009; 81:497-506.
60. Sreekanth R, Rajan SS. The study of helical distortions due to environmental changes: choice of parameters. Biophys Chem 2007;125:191-200.
61. Moldoveanu T, Grace CR, Llambi F, Nourse A, Fitzgerald P, Gehring K, Kriwacki RW, Green DR. BID-induced structural changes in BAK promote apoptosis. Nat Struct Mol Biol 2013;20:589-597.
62. Marshall B, Puthalakath H, Caria S, Chugh S, Doerflinger M, Colman PM, Kvansakul M. Variola virus F1L is a Bcl-2-like protein that unlike its vaccinia virus counterpart inhibits apoptosis independent of bim. Cell Death Dis 2015;6:e1680
63. Smits C, Czabotar PE, Hinds MG, Day CL. Structural plasticity underpins promiscuous binding of the prosurvival protein a1. Structure 2008;16:818-829.
64. Ji H, Shekhtman A, Ghose R, McDonnell JM, Cowburn D. NMR determination that an extended bh3 motif of pro-apoptotic BID is specifically bound to BCL-XL. Magn Reson Chem 2006;44 Spec No:S101-S107.
65. Xia T, Jiang CS, Li LJ, Zhang Y, Jin HJ, Liu SS, Wu CH, Chen Q. Bid bh3 peptide, but not its mutant form G(94)E, induces permeability transition pore opening and cytochrome c release in vitro. Chinese Sci Bull 2002;47:553-557.
66. Wang K, Yin XM, Chao DT, Milliman CL, Korsmeyer SJ. BID: a novel bh3 domain-only death agonist. Genes Dev 1996;10:2859-2869.
67. Ku B, Liang C, Jung JU, Oh BH. Evidence that inhibition of BAX activation by BCL-2 involves its tight and preferential interaction with the bh3 domain of BAX. Cell Res 2011;21:627-641.
68. Rautureau GJ, Yabal M, Yang H, Huang DC, Kvansakul M, Hinds MG. The restricted binding repertoire of Bcl-B leaves bim as the universal BH3-only prosurvival Bcl-2 protein antagonist. Cell Death Dis 2012; 3:e443
69. Fire E, Gulla SV, Grant RA, Keating AE. Mcl-1-bim complexes accommodate surprising point mutations via minor structural changes. Protein Sci 2010;19:507-519.
70. Herman MD, Nyman T, Welin M, Lehtio L, Flodin S, Tresaugues L, Kotenyova T, Flores A, Nordlund P. Completing the family portrait of the anti-apoptotic Bcl-2 proteins: crystal structure of human Bfl-1 in complex with bim. FEBS Lett 2008;582:3590-3594.
71. Kvansakul M, Wei AH, Fletcher JI, Willis SN, Chen L, Roberts AW, Huang DC, Colman PM. Structural basis for apoptosis inhibition by Epstein-barr virus bhrf1. PLoS Pathog 2010;6:e1001236
72. Kvansakul M, van Delft MF, Lee EF, Gulbis JM, Fairlie WD, Huang DC, Colman PM. A structural viral mimic of prosurvival Bcl-2: a pivotal role for sequestering proapoptotic bax and bak. Mol Cell 2007;25:933-942.
73. Ku B, Woo JS, Liang C, Lee KH, Hong HS, Kim EX, Jung KS, Oh JUBH. Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog 2008; 4:e25
74. Campbell S, Thibault J, Mehta N, Colman PM, Barry M, Kvansakul M. Structural insight into bh3 domain binding of vaccinia virus antiapoptotic F1L. J Virol 2014;88:8667-8677.
75. Woo JS, Jung JS, Ha NC, Shin J, Kim KH, Lee W, Oh BH. Unique structural features of a BCL-2 family protein CED-9 and biophysical characterization of CED-9/EGL-1 interactions. Cell Death Differ 2003;10:1310-1319.
76. Yan N, Gu L, Kokel D, Chai J, Li W, Han A, Chen L, Xue D, Shi Y. Structural, biochemical, and functional analyses of CED-9 recognition by the proapoptotic proteins EGL-1 and CED-4. Mol Cell 2004;15:999-1006.