Transient pockets on XIAP-BIR2: Toward the characterization of putative binding sites of small-molecule XIAP inhibitors

Journal of Molecular Modeling

Volumn 18, Issue 5, 2012, Pages 2031-2042

  Eyrisch, Susanne ^a,c   Medina Franco, Jose L ^b   Helms, Volkhard ^a  

^a Center for Bioinformatics   (Germany)

^b TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

^c Priaxon AG   (Germany)

Author keywords

Apoptosis; Docking; Inhibitors; Molecular dynamics simulation; Pocket detection; Protein protein interaction; Transient pockets

Indexed keywords

CASPASE 3; INHIBITOR OF APOPTOSIS PROTEIN; METHANOL; PROTEIN BIR2; PROTEIN INHIBITOR; SOLVENT; UNCLASSIFIED DRUG; WATER; X LINKED INHIBITOR OF APOPTOSIS;

APOPTOSIS; ARTICLE; BINDING SITE; CELL DAMAGE; CELL SURVIVAL; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SIMULATION;

APOPTOSIS; BINDING SITES; CASPASE 3; CRYSTALLOGRAPHY, X-RAY; EUKARYOTIC CELLS; HUMANS; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES; THERMODYNAMICS; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84861235119     PISSN: 16102940     EISSN: 09485023     Source Type: Journal    
DOI: 10.1007/s00894-011-1217-y     Document Type: Article

References (58)

1. Wells AL,McClendon CL (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450:1001-1009 (Pubitemid 350273630)
2. Roy N, Deveraux QL, Takahashi R, Salvesen GS, Reed JC (1997) The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J 16:6914-6925 (Pubitemid 27520792)
3. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 17:2215-2223 (Pubitemid 28171907)
4. Reed JC (2001) The survivin saga goes in vivo. J Clin Invest 108:965-969 (Pubitemid 32946070)
5. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1-16 (Pubitemid 27386911)
6. Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281:1312-1316 (Pubitemid 28406817)
7. Tamm I, Kornblau SM, Segall H, Krajewski S, Welsh K, Kitada S, Scudiero DA, Tudor G, Qui YH, Monks A, Andreeff M, Reed JC (2000) Expression and prognostic significance of IAP-family genes in human cancers and myeloid leukemias. Clin Cancer Res 6:1796-1803 (Pubitemid 30305074)
8. Takahashi R, Deveraux Q, Tamm I, Welsh K, Assa-Munt N, Salvesen GS, Reed JC (1998) A single BIR domain of XIAP sufficient for inhibiting caspases. J Biol Chem 14:7787-7790 (Pubitemid 28168819)
9. Deveraux QL, Leo E, Stennicke HR, Welsh K, Salvesen GS, Reed JC (1999) Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J 18:5242-5251 (Pubitemid 29465575)
10. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33-42
11. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, Liddington RC, Salvesen GS (2001) Structural basis for the inhibition of caspase-3 by XIAP. Cell 104:791-800 (Pubitemid 32241028)
12. Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES, Shi Y (2001) Structural basis of caspase-7 inhibition by XIAP. Cell 104:769-780 (Pubitemid 32241026)
13. Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM, Alnemri ES, Fairman R, Shi Y (2003) Mechanism of XIAPmediated inhibition of caspase-9. Mol Cell 11:519-527
14. Liu Z, Sun C, Olejniczak ET, Meadows RP, Betz SF, Oost T, Herrmann J, Wu JC, Fesik SW (2000) Structural basis for binding of Smac/Diablo to the XIAP BIR3 domain. Nature 408:1004-1008 (Pubitemid 32101650)
15. Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X, Shi Y (2000) Structural basis of IAP recognition by Smac/Diablo. Nature 408:1008-1012 (Pubitemid 32101651)
16. Wist AD, Gu L, Riedl SJ, Shi Y, McLendon GL (2007) Structureactivity based study of the Smac-binding pocket within the BIR3 domain of XIAP. Bioorg Med Chem 15:2935-2943 (Pubitemid 46400464)
17. Sun H, Stuckey JA, Nikolovska-Coleska Z, Qin D, Meagher JL, Qiu S, Lu J, Yang CY, Saito NG, Wang S (2008) Structure-based design, synthesis, evaluation, and crystallographic studies of conformationally constrained Smac mimetics as inhibitors of the X-linked inhibitor of apoptosis protein (XIAP). J Med Chem 51:7169-7180
18. Mastrangelo E, Cossu F, Milani M, Sorrentino G, Lecis D, Delia D, Manzoni L, Drago C, Seneci P, Scolastico C, Rizzo V, Bolognesi M (2008) Targeting the X-linked inhibitor of apoptosis protein through 4-substituted azabicyclo[5.3.0]alkane Smac mimetics. Structure, activity, and recognition principles. J Mol Biol 384:673-689
19. Nikolovska-Coleska Z, Meagher JL, Jiang S, Yang CY, Qiu S, Roller PP, Stuckey JA, Wang S (2008) Interaction of a cyclic, bivalent Smac mimetic with the x-linked inhibitor of apoptosis protein. Biochemistry 47:9811-9824
20. Cossu F, Milani M, Mastrangelo E, Vachette P, Servida F, Lecis D, Canevari G, Delia D, Drago C, Rizzo V, Manzoni L, Seneci P, Scolastico C, Bolognesi M (2009) Structural basis for bivalent Smac-mimetics recognition in the IAP protein family. J Mol Biol 392:630-644
21. Schimmer AD, Welsh K, Pinilla C, Wang Z, Krajewska M, Bonneau MJ, Pedersen IM, Kitada S, Scott FL, Bailly-Maitre B, Glinsky G, Scudiero D, Sausville E, Salvesen G, Nefzi A, Ostresh JM, Houghten RA, Reed JC (2004) Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell 5:25-35 (Pubitemid 38121594)
22. Wang Z, Cuddy M, Samuel T, Welsh K, Schimmer A, Hanaii F, Houghten R, Pinilla C, Reed JC (2004) Cellular, biochemical, and genetic analysis of mechanism of small molecule IAP inhibitors. J Biol Chem 279:48168-48176 (Pubitemid 39540972)
23. Kater AP, Dicker F, Mangiola M, Welsh K, Houghten R, Ostresh J, Nefzi A, Reed JC, Pinilla C, Kipps TJ (2005) Inhibitors of XIAP sensitize CD40-activated chronic lymphocytic leukemia cells to CD95-mediated apoptosis. Blood 106:1742-1748 (Pubitemid 41208589)
24. Scott FL, Denault JB, Riedl SJ, Shin H, Renatus M, Salvesen GS (2005) XIAP inhibits caspase-3 and -7 using two binding sites: evolutionarily conserved mechanism of IAPs. EMBO J 24:645-655 (Pubitemid 40343265)
25. Sun C, Cai M, Gunasekera AH, Meadows RP, Wang H, Chen J, Zhang H, Wu W, Xu N, Ng SC, Fesik SW (1999) NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP. Nature 401:818-822
26. Eyrisch S, Helms V (2007) Transient pockets on protein surfaces involved in protein-protein interaction. J Med Chem 50:3457-3464 (Pubitemid 47195455)
27. Eyrisch S, Helms V (2009) What induces pocket openings on protein surface patches involved in protein-protein interactions? J Comput Aid Mol Des 23:73-86
28. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 19:1639-1662 (Pubitemid 128590223)
29. Berwanger A, Eyrisch S, Schuster I, Helms V, Bernhardt R (2010) Polyamines: naturally occurring small molecule modulators of electrostatic protein-protein interactions. J Inorg Biochem 104:118-125
30. Lerner MG, Bowman AL, Carlson HA (2007) Incorporating dynamics in E. coli dihydrofolate reductase enhances structurebased drug discovery. J Chem Inf Model 47:2358-2365 (Pubitemid 350275100)
31. Bowman AL, Lerner MG, Carlson HA (2007) Protein flexibility and species specificity in structure-based drug discovery: dihydrofolate reductase as a test system. J Am Chem Soc 129:3634-3640 (Pubitemid 46502724)
32. Bogan AA, Thorn KS (1998) Anatomy of hot spots in protein interfaces. J Mol Biol 280:1
33. Clackson T, Wells J (1995) A hot-spot of binding energy in a hormone-receptor interface. Science 267:383-386
34. Moreira IS, Fernandes PA, Ramos MJ (2007) Hot spots-a review of the protein-protein interface determinant amino-acid residues. Proteins 68:803-812 (Pubitemid 47434705)
35. Halperin I, Wolfson H, Nussinov R (2004) Protein-protein interactions: coupling of structurally conserved residues and of hot spots across interfaces. Implications for docking. Structure 12:1027-1038 (Pubitemid 38748774)
36. Keskin O, Ma B, Nussinov R (2005) Hot regions in protein-protein interactions: the organization and contribution of structurally conserved hot spot residues. J Mol Biol 345:1281-1294 (Pubitemid 40092239)
37. Kortemme T, Baker D (2002) A simple physical model for binding energy hot spots in protein-protein complexes. Proc Natl Acad Sci USA 99:14116-14121 (Pubitemid 35257634)
38. Guerois R, Nielsen J, Serrano L (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320:369-387 (Pubitemid 34722226)
39. Tuncbag N, Gursoy A, Keskin O (2009) Identification of computational hot spots in protein interfaces: combining solvent accessibility and inter-residue potentials improves the accuracy. Bioinformatics 25:1513-1520
40. Bylaska EJ, de Jong WA, Kowalski K, Straatsma TP, Valiev M et al (2006) NWChem, a computational chemistry package for parallel computers, version 5.0, Pacific Northwest National Laboratory, Richland, Washington 99352-0999, USA
41. Becke AD (1997) Density-functional thermochemistry. V. Systematic optimization of exchange-correlation functionals. J Chem Phys 107:8554
42. Bayly CI, Cieplak P, Cornell W, Kollman PA (1993) A wellbehaved electrostatic potential based method using charge restraints for determining atom-centered charges: the RESP model. J Phys Chem 97:10269-10280
43. Jorgensen WL, Maxwell DS, Tirado-Rives J (1996) Development and testing of the opls all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 118:11225-11236 (Pubitemid 26399746)
44. Merz KM (1991) Carbon dioxide binding to human carbonic anhydrase ii. J Am Chem Soc 113:406-411
45. Lindahl E, Hess B, van der Spoel D (2001) GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model 7:306-317 (Pubitemid 36153547)
46. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926-935
47. Darden T, York D, Pedersen L (1993) Particle mesh ewald: an n log(n) method for ewald sums in large systems. J Chem Phys 98:10089-10092
48. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684-3690
49. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463-1472 (Pubitemid 127637344)
50. Brady GP Jr, Stouten PF (2000) Fast prediction and visualization of protein binding pockets with pass. J Comput Aided Mol Des 14:383-401 (Pubitemid 30219399)
51. Gasteiger J, Marsili M (1980) Iterative partial equilibration of orbital electronegativity - a rapid access to atomic charges. Tetrahedron 36:3219-3228
52. Sanner MF (1999) Python: a programming language for software integration and development. J Mol Graph Model 17:57-61 (Pubitemid 30029318)
53. Solis FJ, Wets JB (1981) Minimization by random search techniques. Math Oper Res 6:19-30
54. Huey R, Morris GM, Olson AJ, Goodsell DS (2007) A semiempirical free energy force field with charge-based desolvation. J Comput Chem 28:1145-1152 (Pubitemid 46506716)
55. Boehr DD, Wright PE (2008) How do proteins interact? Science 320:1429-1430 (Pubitemid 351929416)
56. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 30:2785-2791
57. Obiol-Pardo C, Granadino-Roldan JM, Rubio-Martinez J (2008) Protein-protein recognition as a first step towards the inhibition of XIAP and Survivin anti-apoptotic proteins. J Mol Recognit 21:190-204 (Pubitemid 351821992)
58. Pang YP, Xu K, El Yazal J, Prendergast PG (2000) Successful molecular dynamics simulation of the zinc-bound farnesyltransferase using the cationic dummy atom approach. Protein Sci 9:1857-1865