Blind prediction of interfacial water positions in CAPRI

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 4, 2014, Pages 620-632

  Lensink, Marc F ^a   Moal, Iain H ^b,e   Bates, Paul A ^b   Kastritis, Panagiotis L ^c   Melquiond, Adrien S J ^c   Karaca, Ezgi ^c   Schmitz, Christophe ^c   van Dijk, Marc ^c   Bonvin, Alexandre M J J ^c   Eisenstein, Miriam ^d   Jiménez García, Brian ^e   Grosdidier, Solène ^e,ab   Solernou, Albert ^e,ac   Pérez Cano, Laura ^e   Pallara, Chiara ^e   Fernández Recio, Juan ^e   Xu, Jianqing ^f   Muthu, Pravin ^g   Praneeth Kilambi, Krishna ^f   Gray, Jeffrey J ^f,g   Grudinin, Sergei ^h   Derevyanko, Georgy ^h   Mitchell, Julie C ⁱ   Wieting, John ⁱ   Kanamori, Eiji ^j   Tsuchiya, Yuko ^k   Murakami, Yoichi ^l   Sarmiento, Joy ^k   Standley, Daron M ^k   Shirota, Matsuyuki ^m   Kinoshita, Kengo ^m   Nakamura, Haruki ^k   Chavent, Matthieu ⁿ   Ritchie, David W ^o   Park, Hahnbeom ^p,ad   Ko, Junsu ^p,ae   Lee, Hasup ^p   Seok, Chaok ^p   Shen, Yang ^q,af   Kozakov, Dima ^r   Vajda, Sandor ^r   Kundrotas, Petras J ^s   Vakser, Ilya A ^s   Pierce, Brian G ^t   Hwang, Howook ^t   Vreven, Thom ^t   Weng, Zhiping ^t   Buch, Idit ^u   Farkash, Efrat ^u   Wolfson, Haim J ^u   Zacharias, Martin ^v   Qin, Sanbo ^w   Zhou, Huan Xiang ^w   Huang, Shen You ^x   Zou, Xiaoqin ^x   Wojdyla, Justyna A ^y   Kleanthous, Colin ^y   Wodak, Shoshana J ^z,aa   more..

^a CNRS   (France)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UTRECHT UNIVERSITY   (Netherlands)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^e BARCELONA SUPERCOMPUTING CENTER   (Spain)

^f Johns Hopkins University   (United States)

^g JOHNS HOPKINS UNIVERSITY   (United States)

^h INRIA RHÔNE ALPES   (France)

ⁱ UNIVERSITY OF WISCONSIN MADISON   (United States)

^j Koto ku   (Japan)

^k OSAKA UNIVERSITY   (Japan)

^l NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^m TOHOKU UNIVERSITY   (Japan)

ⁿ France   (France)

^o INRIA   (France)

^p Seoul National University   (South Korea)

^q MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^r Boston University   (United States)

^s UNIVERSITY OF KANSAS   (United States)

^t UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^u TEL AVIV UNIVERSITY   (Israel)

^v TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^w Florida State University   (United States)

^x UNIVERSITY OF MISSOURI   (United States)

^y UNIVERSITY OF OXFORD   (United Kingdom)

^z HOSPITAL FOR SICK CHILDREN   (Canada)

^aa UNIVERSITY OF TORONTO   (Canada)

^ab UNIVERSITAT POMPEU FABRA   (Spain)

^ac UNIVERSITY OF OXFORD   (United Kingdom)

^ad UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^ae Theragen BiO Institute   (South Korea)

^af TOYOTA TECHNOLOGICAL INSTITUTE AT CHICAGO   (United States)

more..

Author keywords

Blind prediction; CAPRI; Protein docking; Protein interface; Water

Indexed keywords

COLICIN; DEOXYRIBONUCLEASE; WATER;

ACCURACY; ARTICLE; ATOM; CRYSTAL STRUCTURE; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULE; PREDICTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; TEMPERATURE;

BLIND PREDICTION; CAPRI; PROTEIN DOCKING; PROTEIN INTERFACE; WATER;

ALGORITHMS; COLICINS; COMPUTATIONAL BIOLOGY; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; WATER;

EID: 84895561083     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24439     Document Type: Article

References (65)

1. Timasheff SN. The control of protein stability and association by weak interactions with water: how do solvents affect these processes? Annu Rev Biophys Biomol Struct 1993;22:67-97.
2. Levy Y, Onuchic JN. Water mediation in protein folding and molecular recognition. Annu Rev Biophys Biomol Struct 2006;35:389-415.
3. Kauzmann W. Some factors in the interpretation of protein denaturation. Adv Protein CJEM 1959;14:239-345.
4. Kuntz ID, Jr, Kauzmann W. Hydration of proteins and polypeptides. Adv Protein Chem 1974;28:239-345.
5. Schutz CN, Warshel A. What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins 2001;44(4):400-417.
6. Mentre P. Water in the orchestration of the cell machinery. Some misunderstandings: a short review. J Biol Phys 2012;38(1):13-26.
7. Mattos C. Protein-water interactions in a dynamic world. Trends Biochem Sci 2002;27(4):203-208.
8. Zhang L, Yang Y, Kao YT, Wang L, Zhong D. Protein hydration dynamics and molecular mechanism of coupled water-protein fluctuations. J Am Chem Soc 2009;131(30):10677-10691.
9. Philips RS. How does active site water affect enzymatic stereorecognition? J Mol Catl B Enz 2002;19-20:103-107.
10. Ben-Naim A. Molecular recognition-viewed through the eyes of the solvent. Biophys Chem 2002;101-102:309-319.
11. Janin J. Wet and dry interfaces: the role of solvent in protein-protein and protein-DNA recognition. Structure 1999;7(12):R277-279.
12. Rodier F, Bahadur RP, Chakrabarti P, Janin J. Hydration of protein-protein interfaces. Proteins 2005;60(1):36-45.
13. Buckle AM, Schreiber G, Fersht AR. Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2.0-Å resolution. Biochemistry 1994;33(30):8878-8889.
14. Perkins JR, Diboun I, Dessailly BH, Lees JG, Orengo C. Transient protein-protein interactions: structural, functional, and network properties. Structure 2010;18(10):1233-1243.
15. Teeter MM. Water-protein interactions: theory and experiment. Annu Rev Biophys Biophys Chem 1991;20:577-600.
16. Huggins DJ, Tidor B. Systematic placement of structural water molecules for improved scoring of protein-ligand interactions. Protein Eng Des Sel 2011;24(10):777-789.
17. Kollman PAK, B. Perakyla, M. Computational studies of enzyme catalyzed reactions: where are we in predicting mechanisms and understanding the nature of enzyme catalysis? J Phys Chem B 2002;106:1537-1541.
18. Boobbyer DN, Goodford PJ, McWhinnie PM, Wade RC. New hydrogen-bond potentials for use in determining energetically favorable binding sites on molecules of known structure. J Med Chem 1989;32(5):1083-1094.
19. Wade RC, Goodford PJ. Further development of hydrogen bond functions for use in determining energetically favorable binding sites on molecules of known structure. 2. Ligand probe groups with the ability to form more than two hydrogen bonds. J Med Chem 1993;36(1):148-156.
20. Wade RC, Clark KJ, Goodford PJ. Further development of hydrogen bond functions for use in determining energetically favorable binding sites on molecules of known structure. 1. Ligand probe groups with the ability to form two hydrogen bonds. J Med Chem 1993;36(1):140-147.
21. Schymkowitz JW, Rousseau F, Martins IC, Ferkinghoff-Borg J, Stricher F, Serrano L. Prediction of water and metal binding sites and their affinities by using the Fold-X force field. Proc Natl Acad Sci USA 2005;102(29):10147-10152.
22. Verdonk ML, Chessari G, Cole JC, Hartshorn MJ, Murray CW, Nissink JW, Taylor RD, Taylor R. Modeling water molecules in protein-ligand docking using GOLD. J Med Chem 2005;48(20):6504-6515.
23. Osterberg F, Morris GM, Sanner MF, Olson AJ, Goodsell DS. Automated docking to multiple target structures: incorporation of protein mobility and structural water heterogeneity in AutoDock. Proteins 2002;46(1):34-40.
24. Corbeil CR, Englebienne P, Moitessier N. Docking ligands into flexible and solvated macromolecules. 1. Development and validation of FITTED 1.0. J Chem Inf Model 2007;47(2):435-449.
25. de Graaf C, Pospisil P, Pos W, Folkers G, Vermeulen NP. Binding mode prediction of cytochrome p450 and thymidine kinase protein-ligand complexes by consideration of water and rescoring in automated docking. J Med Chem 2005;48(7):2308-2318.
26. Friesner RA, Murphy RB, Repasky MP, Frye LL, Greenwood JR, Halgren TA, Sanschagrin PC, Mainz DT. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J Med Chem 2006;49(21):6177-6196.
27. Forli S, Olson AJ. A force field with discrete displaceable waters and desolvation entropy for hydrated ligand docking. J Med Chem 2012;55(2):623-638.
28. Wang L, Berne BJ, Friesner RA. Ligand binding to protein-binding pockets with wet and dry regions. Proc Natl Acad Sci USA 2011;108(4):1326-1330.
29. Ross GA, Morris GM, Biggin PC. Rapid and accurate prediction and scoring of water molecules in protein binding sites. PLoS One 2012;7(3):e32036.
30. Verdonk ML, Cole JC, Taylor R. SuperStar: a knowledge-based approach for identifying interaction sites in proteins. J Mol Biol 1999;289(4):1093-1108.
31. Rossato G, Ernst B, Vedani A, Smiesko M. AcquaAlta: a directional approach to the solvation of ligand-protein complexes. J Chem Inf Model 2011;51(8):1867-1881.
32. Jiang L, Kuhlman B, Kortemme T, Baker D. A "solvated rotamer" approach to modeling water-mediated hydrogen bonds at protein-protein interfaces. Proteins 2005;58(4):893-904.
33. Bui HH, Schiewe AJ, Haworth IS. WATGEN: an algorithm for modeling water networks at protein-protein interfaces. J Comput Chem 2007;28(14):2241-2251.
34. Camacho CJ, Gatchell DW, Kimura SR, Vajda S. Scoring docked conformations generated by rigid-body protein-protein docking. Proteins 2000;40(3):525-537.
35. Kastritis PL, Visscher KM, van Dijk AD, Bonvin AM. Solvated protein-protein docking using Kyte-Doolittle-based water preferences. Proteins 2013;81(3):510-518.
36. Ahmad M, Gu W, Geyer T, Helms V. Adhesive water networks facilitate binding of protein interfaces. Nat Commun 2011;2:261.
37. Wodak SJ, Janin J. Computer analysis of protein-protein interaction. J Mol Biol 1978;124(2):323-342.
38. Cherfils J, Duquerroy S, Janin J. Protein-protein recognition analyzed by docking simulation. Proteins 1991;11(4):271-280.
39. Vakser IA. Protein docking for low-resolution structures. Protein Eng 1995;8(4):371-377.
40. Katchalski-Katzir E, Shariv I, Eisenstein M, Friesem AA, Aflalo C, Vakser IA. Molecular surface recognition: determination of geometric fit between proteins and their ligands by correlation techniques. Proc Natl Acad Sci USA 1992;89(6):2195-2199.
41. Fiser A, Sali A. Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol 2003;374:461-491.
42. Wodak SJ, Janin J. Structural basis of macromolecular recognition. Adv Protein Chem 2002;61:9-73.
43. Zacharias M. Accounting for conformational changes during protein-protein docking. Curr Opin Struct Biol 2010;20(2):180-186.
44. Ritchie DW. Recent progress and future directions in protein-protein docking. Curr Protein Pept Sci 2008;9(1):1-15.
45. Lensink MF, Wodak SJ. Docking and scoring protein interactions: CAPRI 2009. Proteins 2010;78(15):3073-3084.
46. Janin J. Protein-protein docking tested in blind predictions: the CAPRI experiment. Mol Biosyst 2010;6(12):2351-2362.
47. Lensink MF, Mendez R, Wodak SJ. Docking and scoring protein complexes: CAPRI 3rd Edition. Proteins 2007;69(4):704-718.
48. Fleishman SJ, Whitehead TA, Strauch EM, Corn JE, Qin S, Zhou HX, Mitchell JC, Demerdash ON, Takeda-Shitaka M, Terashi G, Moal IH, Li X, Bates PA, Zacharias M, Park H, Ko JS, Lee H, Seok C, Bourquard T, Bernauer J, Poupon A, Aze J, Soner S, Ovali SK, Ozbek P, Tal NB, Haliloglu T, Hwang H, Vreven T, Pierce BG, Weng Z, Perez-Cano L, Pons C, Fernandez-Recio J, Jiang F, Yang F, Gong X, Cao L, Xu X, Liu B, Wang P, Li C, Wang C, Robert CH, Guharoy M, Liu S, Huang Y, Li L, Guo D, Chen Y, Xiao Y, London N, Itzhaki Z, Schueler-Furman O, Inbar Y, Potapov V, Cohen M, Schreiber G, Tsuchiya Y, Kanamori E, Standley DM, Nakamura H, Kinoshita K, Driggers CM, Hall RG, Morgan JL, Hsu VL, Zhan J, Yang Y, Zhou Y, Kastritis PL, Bonvin AM, Zhang W, Camacho CJ, Kilambi KP, Sircar A, Gray JJ, Ohue M, Uchikoga N, Matsuzaki Y, Ishida T, Akiyama Y, Khashan R, Bush S, Fouches D, Tropsha A, Esquivel-Rodriguez J, Kihara D, Stranges PB, Jacak R, Kuhlman B, Huang SY, Zou X, Wodak SJ, Janin J, Baker D. Community-wide assessment of protein-interface modeling suggests improvements to design methodology. J Mol Biol 2011;414(2):289-302.
49. Moretti R, Fleishman SJ, Agius R, Torchala M, Bates PA, Kastritis PL, Rodrigues JP, Trellet M, Bonvin AM, Cui M, Rooman M, Gillis D, Dehouck Y, Moal I, Romero-Durana M, Perez-Cano L, Pallara C, Jimenez B, Fernandez-Recio J, Flores S, Pacella M, Praneeth Kilambi K, Gray JJ, Popov P, Grudinin S, Esquivel-Rodriguez J, Kihara D, Zhao N, Korkin D, Zhu X, Demerdash ON, Mitchell JC, Kanamori E, Tsuchiya Y, Nakamura H, Lee H, Park H, Seok C, Sarmiento J, Liang S, Teraguchi S, Standley DM, Shimoyama H, Terashi G, Takeda-Shitaka M, Iwadate M, Umeyama H, Beglov D, Hall DR, Kozakov D, Vajda S, Pierce BG, Hwang H, Vreven T, Weng Z, Huang Y, Li H, Yang X, Ji X, Liu S, Xiao Y, Zacharias M, Qin S, Zhou HX, Huang SY, Zou X, Velankar S, Janin J, Wodak SJ, Baker D. Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions. Proteins 2013;81(11):1980-1987.
50. Wojdyla JA, Fleishman SJ, Baker D, Kleanthous C. Structure of the ultra-high-affinity colicin E2 DNase-Im2 complex. J Mol Biol 2012;417(1-2):79-94.
51. Kuhlmann UC, Pommer AJ, Moore GR, James R, Kleanthous C. Specificity in protein-protein interactions: the structural basis for dual recognition in endonuclease colicin-immunity protein complexes. J Mol Biol 2000;301(5):1163-1178.
52. Meenan NA, Sharma A, Fleishman SJ, Macdonald CJ, Morel B, Boetzel R, Moore GR, Baker D, Kleanthous C. The structural and energetic basis for high selectivity in a high-affinity protein-protein interaction. Proc Natl Acad Sci USA 2010;107(22):10080-10085.
53. Nakasako M. Water-protein interactions from high-resolution protein crystallography. Philos Trans R Soc Lond B Biol Sci 2004;359(1448):1191-1204; discussion 1204-1196.
54. Brooks BR, Brooks CL, 3rd, Mackerell AD, Jr, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M. CHARMM: the biomolecular simulation program. J Comput Chem 2009;30(10):1545-1614.
55. Case DA, Cheatham TE, 3rd, Darden T, Gohlke H, Luo R, Merz KM, Jr, Onufriev A, Simmerling C, Wang B, Woods RJ. The Amber biomolecular simulation programs. J Comput Chem 2005;26(16):1668-1688.
56. Song Y, Tyka M, Leaver-Fay A, Thompson J, Baker D. Structure-guided forcefield optimization. Proteins 2011;79(6):1898-1909.
57. Zhang L, Hermans J. Hydrophilicity of cavities in proteins. Proteins 1996;24(4):433-438.
58. Li W, Keeble AH, Giffard C, James R, Moore GR, Kleanthous C. Highly discriminating protein-protein interaction specificities in the context of a conserved binding energy hotspot. J Mol Biol 2004;337(3):743-759.
59. Pronk S, Pall S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, Shirts MR, Smith JC, Kasson PM, van der Spoel D, Hess B, Lindahl E. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 2013;29(7):845-854.
60. Toukan KR, A. Molecular-dynamics study of atomic motion in water. Phys Rev B Conds Matter 1985;31:2643-2648.
61. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh Ewald method. J Chem Phys 1995;103(19):8577-8593.
62. Pettit BM, Makarov VA, Andrews BK. Protein hydration density: theory simulations and crystallography. Curr Opin Struct Biol 1998;8:218-221.
63. Bizzarri AR, Cannistraro S. Molecular dynamics of water at the protein-solvent interface. J Phys Chem B 2002;106:6617-6633.
64. Cappel D, Wahlstrom R, Brenk R, Sotriffer CA. Probing the dynamic nature of water molecules and their influences on ligand binding in a model binding site. J Chem Inf Model 2011;51(10):2581-2594.
65. van Dijk AD, Bonvin AM. Solvated docking: introducing water into the modelling of biomolecular complexes. Bioinformatics 2006;22(19):2340-2347.