Relationship between hot spot residues and ligand binding hot spots in protein-protein interfaces

Journal of Chemical Information and Modeling

Volumn 52, Issue 8, 2012, Pages 2236-2244

  Zerbe, Brandon S ^a   Hall, David R ^a   Vajda, Sandor ^a,b   Whitty, Adrian ^b   Kozakov, Dima ^a  

^a Boston University   (United States)

^b Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING SITES; FREE ENERGY; LIGANDS; MAPPING; MOLECULES; PROTEINS; SCANNING;

ALANINE-SCANNING MUTAGENESIS; BINDING FREE ENERGY; HOT SPOTS IN PROTEINS; INTERACTION ENERGIES; PHARMACEUTICAL RESEARCH; PROTEIN-PROTEIN INTERACTIONS; SMALL-MOLECULE BINDINGS; STRONG CORRELATION;

BINDING ENERGY;

LIGAND; PANCREATIC RIBONUCLEASE; PROTEIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MUTAGENESIS; PROTEIN BINDING; PROTEIN CONFORMATION;

LIGANDS; MODELS, MOLECULAR; MUTAGENESIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS; RIBONUCLEASE, PANCREATIC;

EID: 84865494461     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci300175u     Document Type: Article

References (64)

1. Wells, J. A.; McClendon, C. L. Reaching for high-hanging fruit in drug discovery at protein-protein interfaces Nature 2007, 450, 1001-1009 (Pubitemid 350273630)
2. Berg, T. Small-molecule inhibitors of protein-protein interactions Curr. Opin. Drug Discov. Devel. 2008, 11, 666-674
3. Whitty, A.; Kumaravel, G. Between a rock and a hard place? Nat. Chem. Biol. 2006, 2, 112-118 (Pubitemid 44323856)
4. DeLano, W. L. Unraveling hot spots in binding interfaces: progress and challenges Curr. Opin. Struct. Biol. 2002, 12, 14-20
5. Cunningham, B. C.; Wells, J. A. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis Science 1989, 244, 1081-1085 (Pubitemid 19152300)
6. Cunningham, B. C.; Wells, J. A. Comparison of a structural and a functional epitope J. Mol. Biol. 1993, 234, 554-563 (Pubitemid 24007786)
7. Jin, L.; Wells, J. A. Dissecting the energetics of an antibody-antigen interface by alanine shaving and molecular grafting Protein Sci. 1994, 3, 2351-2357
8. Clackson, T.; Wells, J. A. A hot spot of binding energy in a hormone-receptor interface Science 1995, 267, 383-386
9. Bogan, A. A.; Thorn, K. S. Anatomy of hot spots in protein interfaces J. Mol. Biol. 1998, 280, 1-9 (Pubitemid 28312802)
10. Thorn, K. S.; Bogan, A. A. ASEdb: a database of alanine mutations and their effects on the free energy of binding in protein interactions Bioinformatics 2001, 17, 284-285 (Pubitemid 32288219)
11. Fischer, T. B.; Arunachalam, K. V.; Bailey, D.; Mangual, V.; Bakhru, S.; Russo, R.; Huang, D.; Paczkowski, M.; Lalchandani, V.; Ramachandra, C.; Ellison, B.; Galer, S.; Shapley, J.; Fuentes, E.; Tsai, J. The binding interface database (BID): a compilation of amino acid hot spots in protein interfaces Bioinformatics 2003, 19, 1453-1454 (Pubitemid 36939831)
12. Allen, K. N.; Bellamacina, C. R.; Ding, X.; Jeffrey, C. J.; Mattos, C.; Petsko, G. A.; Ringe, D. An experimental approach to mapping binding surfaces of crystalline proteins J. Phys. Chem. 1996, 100, 595-599
13. Mattos, C.; Ringe, D. Locating and characterizing binding sites on proteins Nat. Biotechnol. 1996, 14, 595-599 (Pubitemid 26135122)
14. English, A. C.; Done, S. H.; Caves, L. S.; Groom, C. R.; Hubbard, R. E. Locating interaction sites on proteins: the crystal structure of thermolysin soaked in 2% to 100% isopropanol Proteins: Struct., Funct., Bioinf. 1999, 37, 628-640
15. English, A. C.; Groom, C. R.; Hubbard, R. E. Experimental and computational mapping of the binding surface of a crystalline protein Protein Eng. 2001, 14, 47-59 (Pubitemid 32318937)
16. Dechene, M.; Wink, G.; Smith, M.; Swartz, P.; Mattos, C. Multiple solvent crystal structures of ribonuclease A: an assessment of the method Proteins: Struct., Funct., Bioinf. 2009, 76, 861-881
17. Shuker, S. B.; Hajduk, P. J.; Meadows, R. P.; Fesik, S. W. Discovering high-affinity ligands for proteins: SAR by NMR Science 1996, 274, 1531-1534 (Pubitemid 26403929)
18. Hajduk, P. J.; Huth, J. R.; Fesik, S. W. Druggability indices for protein targets derived from NMR-based screening data J. Med. Chem. 2005, 48, 2518-2525 (Pubitemid 40516441)
19. Congreve, M.; Chessari, G.; Tisi, D.; Woodhead, A. J. Recent developments in fragment-based drug discovery J. Med. Chem. 2008, 51, 3661-3680 (Pubitemid 351956496)
20. Erlanson, D. A.; McDowell, R. S.; O'Brien, T. Fragment-based drug discovery J. Med. Chem. 2004, 47, 3463-3482 (Pubitemid 38822007)
21. Neumann, T.; Junker, H. D.; Schmidt, K.; Sekul, R. SPR-based fragment screening: advantages and applications Curr. Top. Med. Chem. 2007, 7, 1630-1642 (Pubitemid 350131018)
22. Hann, M. M.; Leach, A. R.; Harper, G. Molecular complexity and its impact on the probability of finding leads for drug discovery J. Chem. Inf. Comput. Sci. 2001, 41, 856-864
23. Boehm, H. J.; Boehringer, M.; Bur, D.; Gmuender, H.; Huber, W.; Klaus, W.; Kostrewa, D.; Kuehne, H.; Luebbers, T.; Meunier-Keller, N.; Mueller, F. Novel inhibitors of DNA gyrase: 3D structure based biased needle screening, hit validation by biophysical methods, and 3D guided optimization. A promising alternative to random screening J. Med. Chem. 2000, 43, 2664-2674 (Pubitemid 30463915)
24. Hartshorn, M. J.; Murray, C. W.; Cleasby, A.; Frederickson, M.; Tickle, I. J.; Jhoti, H. Fragment-based lead discovery using X-ray crystallography J. Med. Chem. 2005, 48, 403-413 (Pubitemid 40139783)
25. Ciulli, A.; Williams, G.; Smith, A. G.; Blundell, T. L.; Abell, C. Probing hot spots at protein-ligand binding sites: a fragment-based approach using biophysical methods J. Med. Chem. 2006, 49, 4992-5000 (Pubitemid 44201057)
26. Arkin, M. R.; Wells, J. A. Small-molecule inhibitors of protein-protein interactions: progressing towards the dream Nat. Rev. Drug Discovery 2004, 3, 301-317 (Pubitemid 38499758)
27. Lesuisse, D.; Lange, G.; Deprez, P.; Benard, D.; Schoot, B.; Delettre, G.; Marquette, J. P.; Broto, P.; Jean-Baptiste, V.; Bichet, P.; Sarubbi, E.; Mandine, E. SAR and X-ray. A new approach combining fragment-based screening and rational drug design: application to the discovery of nanomolar inhibitors of Src SH2 J. Med. Chem. 2002, 45, 2379-2387 (Pubitemid 34595209)
28. Schade, M.; Oschkinat, H. NMR fragment screening: tackling protein-protein interaction targets Curr. Opin. Drug Discov. Devel. 2005, 8, 365-373 (Pubitemid 40593431)
29. Petros, A. M. Discovery of a potent inhibitor of the antiapoptotic protein Bcl-xL from NMR and parallel synthesis J. Med. Chem. 2006, 49, 656-663 (Pubitemid 43157495)
30. Berman, H. M.; Bhat, T. N.; Bourne, P. E.; Feng, Z.; Gilliland, G.; Weissig, H.; Westbrook, J. The Protein Data Bank and the challenge of structural genomics Nat. Struct. Biol. 2000, 7 (Suppl) 957-959
31. Kozakov, D.; Hall, D. R.; Chuang, G. Y.; Cencic, R.; Brenke, R.; Grove, L. E.; Beglov, D.; Pelletier, J.; Whitty, A.; Vajda, S. Structural conservation of druggable hot spots in protein-protein interfaces Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 13528-13533
32. Brenke, R.; Kozakov, D.; Chuang, G. Y.; Beglov, D.; Hall, D.; Landon, M. R.; Mattos, C.; Vajda, S. Fragment-based identification of druggable 'hot spots' of proteins using Fourier domain correlation techniques Bioinformatics 2009, 25, 621-627
33. Dennis, S.; Kortvelyesi, T.; Vajda, S. Computational mapping identifies the binding sites of organic solvents on proteins Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 4290-4295 (Pubitemid 34285978)
34. Silberstein, M.; Dennis, S.; Brown, L.; Kortvelyesi, T.; Clodfelter, K.; Vajda, S. Identification of substrate binding sites in enzymes by computational solvent mapping J. Mol. Biol. 2003, 332, 1095-1113 (Pubitemid 37108802)
35. Landon, M. R.; Lieberman, R. L.; Hoang, Q. Q.; Ju, S.; Caaveiro, J. M.; Orwig, S. D.; Kozakov, D.; Brenke, R.; Chuang, G. Y.; Beglov, D.; Vajda, S.; Petsko, G. A.; Ringe, D. Detection of ligand binding hot spots on protein surfaces via fragment-based methods: application to DJ-1 and glucocerebrosidase J. Comput.-Aided Mol. Des. 2009, 23, 491-500
36. Chuang, G. Y.; Kozakov, D.; Brenke, R.; Beglov, D.; Guarnieri, F.; Vajda, S. Binding hot spots and amantadine orientation in the influenza a virus M2 proton channel Biophys. J. 2009, 97, 2846-2853
37. Hall, D. H.; Grove, L. E.; Yueh, C.; Ngan, C. H.; Kozakov, D.; Vajda, S. Robust identification of binding hot spots using continuum electrostatics: application to hen egg-white lysozyme J. Am. Chem. Soc. 2011, 133, 20668-20671
38. Lichtarge, O.; Bourne, H. R.; Cohen, F. E. An evolutionary trace method defines binding surfaces common to protein families J. Mol. Biol. 1996, 257, 342-58 (Pubitemid 26114038)
39. Casari, G.; Sander, C.; Valencia, A. A method to predict functional residues in proteins Nat. Struct. Biol. 1995, 2, 171-8 (Pubitemid 26040653)
40. Konc, J.; Janezic, D. ProBiS algorithm for detection of structurally similar protein binding sites by local structural alignment Bioinformatics 2010, 26, 1160-8
41. Carl, N.; Konc, J.; Vehar, B.; Janezic, D. Protein-protein binding site prediction by local structural alignment J. Chem. Inf. Model. 2010, 50, 1906-13
42. Buhrman, G.; O'Connor, C.; Zerbe, B.; Kearney, B. M.; Napoleon, R.; Kovrigina, E. A.; Vajda, S.; Kozakov, D.; Kovrigin, E. L.; Mattos, C. Analysis of binding site hot spots on the surface of Ras GTPase J. Mol. Biol. 2011, 413, 773-789
43. Ngan, C. H.; Hall, D. R.; Zerbe, B.; Grove, L. E.; Kozakov, D.; Vajda, S. FTSite: high accuracy detection of ligand binding sites on unbound protein structures Bioinformatics 2012, 28, 286-287
44. Kortemme, T.; Baker, D. A simple physical model for binding energy hot spots in protein-protein complexes Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 14116-14121 (Pubitemid 35257634)
45. 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 (Pubitemid 27087715)
46. Darnell, S. J.; Page, D.; Mitchell, J. C. An automated decision-tree approach to predicting protein interaction hot spots Proteins: Struct., Funct., Bioinf. 2007, 68, 813-823 (Pubitemid 47434706)
47. Mosyak, L.; Zhang, Y.; Glasfeld, E.; Haney, S.; Stahl, M.; Seehra, J.; Somers, W. S. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography EMBO J. 2000, 19, 3179-3191 (Pubitemid 30428197)
48. Gordon, N. C.; Pan, B.; Hymowitz, S. G.; Yin, J.; Kelley, R. F.; Cochran, A. G.; Yan, M.; Dixit, V. M.; Fairbrother, W. J.; Starovasnik, M. A. BAFF/BLyS receptor 3 comprises a minimal TNF receptor-like module that encodes a highly focused ligand-binding site Biochemistry 2003, 42, 5977-5983 (Pubitemid 36605100)
49. Li, C.; Pazgier, M.; Li, C.; Yuan, W.; Liu, M.; Wei, G.; Lu, W. Y.; Lu, W. Systematic mutational analysis of peptide inhibition of the p53-MDM2/MDMX interactions J. Mol. Biol. 2010, 398, 200-213
50. Rushe, M.; Silvian, L.; Bixler, S.; Chen, L. L.; Cheung, A.; Bowes, S.; Cuervo, H.; Berkowitz, S.; Zheng, T.; Guckian, K.; Pellegrini, M.; Lugovskoy, A. Structure of a NEMO/IKK-associating domain reveals architecture of the interaction site Structure 2008, 16, 798-808 (Pubitemid 351615013)
51. Cho, K. I.; Kim, D.; Lee, D. A feature-based approach to modeling protein-protein interaction hot spots Nucleic Acids Res. 2009, 37, 2672-2687
52. Tuncbag, N.; Gursoy, A.; Keskin, O. Identification of computational hot spots in protein interfaces: combining solvent accessibility and inter-residue potentials improves the accuracy Bioinformatics 2009, 25, 1513-1520
53. Xia, J. F.; Zhao, X. M.; Song, J.; Huang, D. S. APIS: accurate prediction of hot spots in protein interfaces by combining protrusion index with solvent accessibility BMC Bioinf. 2010, 11, 174
54. Liepinsh, E.; Otting, G. Specificity of urea binding to proteins J. Am. Chem. Soc. 1994, 116, 9670-9674
55. Hall, D. R.; Ngan, C. H.; Zerbe, B. S.; Kozakov, D.; Vajda, S. Hot spot analysis for driving the development of hits into leads in fragment-based drug discovery J. Chem. Inf. Model. 2012, 52, 199-209
56. Wells, J. A. Systematic mutational analyses of protein-protein interfaces Methods Enzymol. 1991, 202, 390-411
57. Li, X.; Keskin, O.; Ma, B.; Nussinov, R.; Liang, J. Protein-protein interactions: hot spots and structurally conserved residues often locate in complemented pockets that pre-organized in the unbound states: implications for docking J. Mol. Biol. 2004, 344, 781-795 (Pubitemid 39469220)
58. Shulman-Peleg, A.; Shatsky, M.; Nussinov, R.; Wolfson, H. J. Spatial chemical conservation of hot spot interactions in protein-protein complexes BMC Biol. 2007, 5, 43
59. Landon, M. R.; Lancia, D. R.; Yu, J.; Thiel, S. C.; Vajda, S. Identification of hot spots within druggable binding regions by computational solvent mapping of proteins J. Med. Chem. 2007, 50, 1231-1240 (Pubitemid 46496323)
60. Liu, Z.; Sun, C.; Olejniczak, E. T.; Meadows, R. P.; Betz, S. F.; Oost, T.; Herrmann, J.; Wu, J. C.; Fesik, S. W. Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain Nature 2000, 408, 1004-1008 (Pubitemid 32101650)
61. Doyle, D. A.; Lee, A.; Lewis, J.; Kim, E.; Sheng, M.; MacKinnon, R. Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ Cell 1996, 85, 1067-1076 (Pubitemid 26231173)
62. Verdecia, M. A.; Bowman, M. E.; Lu, K. P.; Hunter, T.; Noel, J. P. Structural basis for phosphoserine-proline recognition by group IV WW domains Nat. Struct. Biol. 2000, 7, 639-643 (Pubitemid 30636673)
63. Moerke, N. J.; Aktas, H.; Chen, H.; Cantel, S.; Reibarkh, M. Y.; Fahmy, A.; Gross, J. D.; Degterev, A.; Yuan, J.; Chorev, M.; Halperin, J. A.; Wagner, G. Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G Cell 2007, 128, 257-267 (Pubitemid 46137991)
64. Meireles, L. M.; Domling, A. S.; Camacho, C. J. ANCHOR: a web server and database for analysis of protein-protein interaction binding pockets for drug discovery Nucleic Acids Res. 2010, 38, W407-411