Integrative computational modeling of protein interactions

FEBS Journal

Volumn 281, Issue 8, 2014, Pages 1988-2003

  Rodrigues, João P G L M ^a   Bonvin, Alexandre M J J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

3D structure; complexes; data driven docking; integrative modeling; interface prediction; protein docking; protein interactions; restraints; sampling; scoring

Indexed keywords

ALGORITHM; BIOINFORMATICS; COMPLEX FORMATION; COMPUTER MODEL; COMPUTER PREDICTION; COMPUTER PROGRAM; CRYOELECTRON MICROSCOPY; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SCORING SYSTEM; X RAY CRYSTALLOGRAPHY;

3D STRUCTURE; COMPLEXES; DATA-DRIVEN DOCKING; INTEGRATIVE MODELING; INTERFACE PREDICTION; PROTEIN DOCKING; PROTEIN INTERACTIONS; RESTRAINTS; SAMPLING; SCORING;

ANIMALS; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEINS;

EID: 84899465505     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12771     Document Type: Review

References (115)

1. Vidal M, Cusick ME, &, Barabási A-L, (2011) Interactome networks and human disease. Cell 144, 986-998.
2. Von Eichborn J, Günther S, &, Preissner R, (2010) Structural features and evolution of protein-protein interactions. Genome Inform 22, 1-10.
3. Chruszcz M, Domagalski M, Osinski T, Wlodawer A, &, Minor W, (2010) Unmet challenges of structural genomics. Curr Opin Struct Biol 20, 587-597.
4. Levitt M, (2009) Nature of the protein universe. Proc Natl Acad Sci USA 106, 11079.
5. Kolodny R, Pereyaslavets L, Samson AO, &, Levitt M, (2013) On the universe of protein folds. Annu Rev Biophys 42, 559-582.
6. Mosca R, Céol A, &, Aloy P, (2013) Interactome3D: adding structural details to protein networks. Nat Method 10, 47-53.
7. Schlick T, Collepardo-Guevara R, Halvorsen LA, Jung S, &, Xiao X, (2011) Biomolecular modeling and simulation: a field coming of age. Q Rev Biophys 44, 191-228.
8. Janin J, Henrick K, Moult J, Eyck LT, Sternberg MJE, Vajda S, Vakser I, &, Wodak SJ, & Critical Assessment of Predicted Interactions (2003) CAPRI: a critical assessment of predicted interactions. Proteins 52, 2-9.
9. Méndez R, Leplae R, Lensink MF, &, Wodak SJ, (2005) Assessment of CAPRI predictions in rounds 3-5 shows progress in docking procedures. Proteins 60, 150-169.
10. Lensink MF, Méndez R, &, Wodak SJ, (2007) Docking and scoring protein complexes: CAPRI 3rd edition. Proteins 69, 704-718.
11. Lensink MF, &, Wodak SJ, (2010) Docking and scoring protein interactions: CAPRI 2009. Proteins 78, 3073-3084.
12. Lensink MF, &, Wodak SJ, (2013) Docking, scoring and affinity prediction in CAPRI. Proteins 81, 2082-2095.
13. Karaca E, &, Bonvin AMJJ, (2013) Advances in integrative modeling of biomolecular complexes. Methods 59, 372-381.
14. Rodrigues JPGLM, Melquiond ASJ, Karaca E, Trellet M, van Dijk M, van Zundert GCP, Schmitz C, de Vries SJ, Bordogna A, Bonati L, et al,. (2013) Defining the limits of homology modelling in information-driven protein docking. Proteins 81, 2119-2128.
15. Karaca E, &, Bonvin AMJJ, (2011) A multidomain flexible docking approach to deal with large conformational changes in the modeling of biomolecular complexes. Structure 19, 555-565.
16. Kastritis PL, &, Bonvin AM, (2013) Molecular origins of binding affinity: seeking the Archimedean point. Curr Opin Struct Biol 23, 868-877.
17. Kastritis PL, &, Bonvin AMJJ, (2012) On the binding affinity of macromolecular interactions: daring to ask why proteins interact. J R Soc Interface 10, 20120835.
18. Vajda S, &, Kozakov D, (2009) Convergence and combination of methods in protein-protein docking. Curr Opin Struct Biol 19, 164-170.
19. Katchalski-Katzir E, Shariv I, Eisenstein M, Friesem AA, Aflalo C, &, Vakser IA, (1992) Molecular surface recognition: determination of geometric fit between proteins and their ligands by correlation techniques. Proc Natl Acad Sci USA 89, 2195-2199.
20. Comeau SR, Kozakov D, Brenke R, Shen Y, Beglov D, &, Vajda S, (2007) ClusPro: performance in CAPRI rounds 6-11 and the new server. Proteins 69, 781-785.
21. Jiménez-García B, Pons C, &, Fernández-Recio J, (2013) pyDockWEB: a web server for rigid-body protein-protein docking using electrostatics and desolvation scoring. Bioinformatics 29, 1698-1699.
22. Pierce BG, Hourai Y, &, Weng Z, (2011) Accelerating protein docking in ZDOCK using an advanced 3D convolution library. PLoS ONE 6, e24657.
23. Fischer D, Bachar O, Nussinov R, &, Wolfson H, (1992) An efficient automated computer vision based technique for the detection of three dimensional structural motifs in proteins. J Biomol Struct Dyn 9, 769-789.
24. Mashiach E, Schneidman-Duhovny D, Peri A, Shavit Y, Nussinov R, &, Wolfson HJ, (2010) An integrated suite of fast docking algorithms. Proteins 78, 3197-3204.
25. Ritchie DW, &, Kemp GJ, (2000) Protein docking using spherical polar Fourier correlations. Proteins 39, 178-194.
26. Macindoe G, Mavridis L, Venkatraman V, Devignes MD, &, Ritchie DW, (2010) HexServer: an FFT-based protein docking server powered by graphics processors. Nucleic Acids Res 38, W445-W449.
27. Chen R, Li L, &, Weng Z, (2003) ZDOCK: an initial-stage protein-docking algorithm. Proteins 52, 80-87.
28. Cheng TM-K, Blundell TL, &, Fernández-Recio J, (2007) pyDock: electrostatics and desolvation for effective scoring of rigid-body protein-protein docking. Proteins 68, 503-515.
29. Kozakov D, Brenke R, Comeau SR, &, Vajda S, (2006) PIPER: an FFT-based protein docking program with pairwise potentials. Proteins 65, 392-406.
30. Vreven T, Hwang H, &, Weng Z, (2011) Integrating atom-based and residue-based scoring functions for protein-protein docking. Protein Sci 20, 1576-1586.
31. Dominguez C, Boelens R, &, Bonvin AMJJ, (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125, 1731-1737.
32. Moal IH, &, Bates PA, (2010) SwarmDock and the use of normal modes in protein-protein docking. Int J Mol Sci 11, 3623-3648.
33. May A, &, Zacharias M, (2005) Accounting for global protein deformability during protein-protein and protein-ligand docking. Biochim Biophys Acta 1754, 225-231.
34. Koshland DE, (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 44, 98-104.
35. Bonvin AM, (2006) Flexible protein-protein docking. Curr Opin Struct Biol 16, 194-200.
36. Zacharias M, (2010) Accounting for conformational changes during protein-protein docking. Curr Opin Struct Biol 20, 180-186.
37. Lyskov S, &, Gray JJ, (2008) The RosettaDock server for local protein-protein docking. Nucleic Acids Res 36, W233-W238.
38. Zacharias M, (2005) ATTRACT: protein-protein docking in CAPRI using a reduced protein model. Proteins 60, 252-256.
39. de Vries S, &, Zacharias M, (2013) Flexible docking and refinement with a coarse-grained protein model using ATTRACT. Proteins 81, 2167-2174.
40. Moal IH, Moretti R, Baker D, &, Fernández-Recio J, (2013) Scoring functions for protein-protein interactions. Curr Opin Struct Biol 23, 862-867.
41. Chaudhury S, Berrondo M, Weitzner BD, Muthu P, Bergman H, &, Gray JJ, (2011) Benchmarking and analysis of protein docking performance in Rosetta v3.2. PLoS ONE 6, e22477.
42. Schneidman-Duhovny D, Inbar Y, Nussinov R, &, Wolfson HJ, (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res 33, W363-W367.
43. Champ PC, &, Camacho CJ, (2007) FastContact: a free energy scoring tool for protein-protein complex structures. Nucleic Acids Res 35, W556-W560.
44. Fernández-Recio J, Totrov M, &, Abagyan R, (2004) Identification of protein-protein interaction sites from docking energy landscapes. J Mol Biol 335, 843-865.
45. Chen R, &, Weng Z, (2002) Docking unbound proteins using shape complementarity, desolvation, and electrostatics. Proteins 47, 281-294.
46. Andrusier N, Nussinov R, &, Wolfson HJ, (2007) FireDock: fast interaction refinement in molecular docking. Proteins 69, 139-159.
47. Moal IH, Torchala M, Bates PA, &, Fernández-Recio J, (2013) The scoring of poses in protein-protein docking: current capabilities and future directions. BMC Bioinformatics 14, 286.
48. Pons C, Talavera D, la Cruz de X, Orozco M, &, Fernández-Recio J, (2011) Scoring by intermolecular pairwise propensities of exposed residues (SIPPER): a new efficient potential for protein-protein docking. J Chem Inf Model 51, 370-377.
49. Liu S, &, Vakser IA, (2011) DECK: distance and environment-dependent, coarse-grained, knowledge-based potentials for protein-protein docking. BMC Bioinformatics 12, 280.
50. Viswanath S, Ravikant DVS, &, Elber R, (2013) Improving ranking of models for protein complexes with side chain modeling and atomic potentials. Proteins 81, 592-606.
51. Pierce B, &, Weng Z, (2007) ZRANK: reranking protein docking predictions with an optimized energy function. Proteins 67, 1078-1086.
52. Liu S, Zhang C, Zhou H, &, Zhou Y, (2004) A physical reference state unifies the structure-derived potential of mean force for protein folding and binding. Proteins 56, 93-101.
53. Khashan R, Zheng W, &, Tropsha A, (2012) Scoring protein interaction decoys using exposed residues (SPIDER): a novel multibody interaction scoring function based on frequent geometric patterns of interfacial residues. Proteins 80, 2207-2217.
54. Andreani J, Faure G, &, Guerois R, (2013) InterEvScore: a novel coarse-grained interface scoring function using a multi-body statistical potential coupled to evolution. Bioinformatics 29, 1742-1749.
55. Tress M, de Juan D, Graña O, Gómez MJ, Gómez-Puertas P, González JM, López G, &, Valencia A, (2005) Scoring docking models with evolutionary information. Proteins 60, 275-280.
56. Vangone A, Cavallo L, &, Oliva R, (2013) Using a consensus approach based on the conservation of inter-residue contacts to rank CAPRI models. Proteins 81, 2210-2220.
57. Yang Y, &, Zhou Y, (2008) Ab initio folding of terminal segments with secondary structures reveals the fine difference between two closely related all-atom statistical energy functions. Protein Sci 17, 1212-1219.
58. Shortle D, Simons KT, &, Baker D, (1998) Clustering of low-energy conformations near the native structures of small proteins. Proc Natl Acad Sci USA 95, 11158-11162.
59. Camacho CJ, Weng Z, Vajda S, &, DeLisi C, (1999) Free energy landscapes of encounter complexes in protein-protein association. Biophys J 76, 1166-1178.
60. Comeau SR, Gatchell DW, Vajda S, &, Camacho CJ, (2004) ClusPro: a fully automated algorithm for protein-protein docking. Nucleic Acids Res 32, W96-W99.
61. Vreven T, Pierce BG, Hwang H, &, Weng Z, (2013) Performance of ZDOCK in CAPRI rounds 20-26. Proteins 81, 2175-2182.
62. Rodrigues JPGLM, Trellet M, Schmitz C, Kastritis P, Karaca E, Melquiond ASJ, &, Bonvin AMJJ, (2012) Clustering biomolecular complexes by residue contacts similarity. Proteins 80, 1810-1817.
63. van Dijk ADJ, Boelens R, &, Bonvin AMJJ, (2004) Data-driven docking for the study of biomolecular complexes. FEBS J 272, 293-312.
64. Moreira IS, Fernandes PA, &, Ramos MJ, (2009) Protein-protein docking dealing with the unknown. J Comput Chem 31, 317-342.
65. de Vries SJ, Melquiond ASJ, Kastritis PL, Karaca E, Bordogna A, van Dijk M, Rodrigues JPGLM, &, Bonvin AMJJ, (2010) Strengths and weaknesses of data-driven docking in critical assessment of prediction of interactions. Proteins 78, 3242-3249.
66. Kozakov D, Beglov D, Bohnood T, Mottarella SE, Xia B, Hall DR, &, Vajda S, (2013) How good is automated protein docking? Proteins 81, 2159-2166.
67. Tovchigrechko A, &, Vakser IA, (2006) GRAMM-X public web server for protein-protein docking. Nucleic Acids Res 34, W310-W314.
68. Pons C, D'Abramo M, Svergun DI, Orozco M, Bernadó P, &, Fernández-Recio J, (2010) Structural characterization of protein-protein complexes by integrating computational docking with small-angle scattering data. J Mol Biol 403, 217-230.
69. Chelliah V, Blundell TL, &, Fernández-Recio J, (2006) Efficient restraints for protein-protein docking by comparison of observed amino acid substitution patterns with those predicted from local environment. J Mol Biol 357, 1669-1682.
70. 15N-relaxation data. Proteins 60, 367-381.
71. Schmitz C, &, Bonvin AMJJ, (2011) Protein-protein HADDocking using exclusively pseudocontact shifts. J Biomol NMR 50, 263-266.
72. Karaca E, &, Bonvin AMJJ, (2013) On the usefulness of ion-mobility mass spectrometry and SAXS data in scoring docking decoys. Acta Crystallogr D 69, 683-694.
73. Nilges M, Gronenborn AM, Brünger AT, &, Clore GM, (1988) Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2. Protein Eng 2, 27-38.
74. Karaca E, Melquiond ASJ, de Vries SJ, Kastritis PL, &, Bonvin AMJJ, (2010) Building macromolecular assemblies by information-driven docking: introducing the HADDOCK multibody docking server. Mol Cell Proteomics 9, 1784-1794.
75. Trellet M, Melquiond ASJ, &, Bonvin AMJJ, (2013) A unified conformational selection and induced fit approach to protein-peptide docking. PLoS ONE 8, e58769.
76. de Vries SJ, &, Zacharias M, (2012) ATTRACT-EM: a new method for the computational assembly of large molecular machines using cryo-EM maps. PLoS ONE 7, e49733.
77. Schneidman-Duhovny D, Inbar Y, Nussinov R, &, Wolfson HJ, (2005) Geometry-based flexible and symmetric protein docking. Proteins 60, 224-231.
78. Mashiach-Farkash E, Nussinov R, &, Wolfson HJ, (2011) SymmRef: a flexible refinement method for symmetric multimers. Proteins 79, 2607-2623.
79. Tjioe E, Lasker K, Webb B, Wolfson HJ, &, Sali A, (2011) MultiFit: a web server for fitting multiple protein structures into their electron microscopy density map. Nucleic Acids Res 39, W167-W170.
80. Gray JJ, Moughon S, Wang C, Schueler-Furman O, Kuhlman B, Rohl CA, &, Baker D, (2003) Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J Mol Biol 331, 281-299.
81. Choi UB, Strop P, Vrljic M, Chu S, Brunger AT, &, Weninger KR, (2010) Single-molecule FRET-derived model of the synaptotagmin 1-SNARE fusion complex. Nature 17, 318-324.
82. Kalisman N, Adams CM, &, Levitt M, (2012) Subunit order of eukaryotic TRiC/CCT chaperonin by cross-linking, mass spectrometry, and combinatorial homology modeling. Proc Natl Acad Sci USA 109, 2884-2889.
83. Feng C, (2012) Mechanism of nitric oxide synthase regulation: electron transfer and interdomain interactions. Coord Chem Rev 256, 393-411.
84. Schwieters CD, Suh J-Y, Grishaev A, Ghirlando R, Takayama Y, &, Clore GM, (2010) Solution structure of the 128 kDa enzyme I dimer from Escherichia coli and its 146 kDa complex with HPr using residual dipolar couplings and small- and wide-angle X-ray scattering. J Am Chem Soc 132, 13026-13045.
85. Hennig J, Wang I, Sonntag M, Gabel F, &, Sattler M, (2013) Combining NMR and small angle X-ray and neutron scattering in the structural analysis of a ternary protein-RNA complex. J Biomol NMR 56, 17-30.
86. Uetrecht C, Rose RJ, van Duijn E, Lorenzen K, &, Heck AJR, (2010) Ion mobility mass spectrometry of proteins and protein assemblies. Chem Soc Rev 39, 1633-1655.
87. de Vries SJ, van Dijk ADJ, &, Bonvin AMJJ, (2006) WHISCY: what information does surface conservation yield? Application to data-driven docking. Proteins 63, 479-489.
88. Zhang QC, Deng L, Fisher M, Guan J, Honig B, &, Petrey D, (2011) PredUs: a web server for predicting protein interfaces using structural neighbors. Nucleic Acids Res 39, W283-W287.
89. Ashkenazy H, Erez E, Martz E, Pupko T, &, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38, W529-W533.
90. Negi SS, Schein CH, Oezguen N, Power TD, &, Braun W, (2007) InterProSurf: a web server for predicting interacting sites on protein surfaces. Bioinformatics 23, 3397-3399.
91. Porollo A, &, Meller J, (2007) Prediction-based fingerprints of protein-protein interactions. Proteins 66, 630-645.
92. Neuvirth H, Raz R, &, Schreiber G, (2004) ProMate: a structure based prediction program to identify the location of protein-protein binding sites. J Mol Biol 338, 181-199.
93. de Vries SJ, &, Bonvin AMJJ, (2011) CPORT: a consensus interface predictor and its performance in prediction-driven docking with HADDOCK. PLoS ONE 6, e17695.
94. Zellner H, Staudigel M, Trenner T, Bittkowski M, Wolowski V, Icking C, &, Merkl R, (2012) PresCont: predicting protein-protein interfaces utilizing four residue properties. Proteins 80, 154-168.
95. Qin S, &, Zhou H-X, (2007) meta-PPISP: a meta web server for protein-protein interaction site prediction. Bioinformatics 23, 3386-3387.
96. Ahmad S, &, Mizuguchi K, (2011) Partner-aware prediction of interacting residues in protein-protein complexes from sequence data. PLoS ONE 6, e29104.
97. Xue LC, Jordan RA, El-Manzalawy Y, Dobbs D, &, Honavar V, (2014) DockRank: ranking docked conformations using partner-specific sequence homology based protein interface prediction. Proteins 82, 250-267.
98. Dago AE, Schug A, Procaccini A, Hoch JA, Weigt M, &, Szurmant H, (2012) Structural basis of histidine kinase autophosphorylation deduced by integrating genomics, molecular dynamics, and mutagenesis. Proc Natl Acad Sci USA 109, E1733-E1742.
99. Hwang H, Vreven T, &, Weng Z, (2014) Binding interface prediction by combining protein-protein docking results. Proteins 82, 57-66.
100. Russel D, Lasker K, Webb B, Velázquez-Muriel J, Tjioe E, Schneidman-Duhovny D, Peterson B, &, Sali A, (2012) Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies. PLoS Biol 10, e1001244.
101. Aytuna AS, Gursoy A, &, Keskin O, (2005) Prediction of protein-protein interactions by combining structure and sequence conservation in protein interfaces. Bioinformatics 21, 2850-2855.
102. Mukherjee S, &, Zhang Y, (2011) Protein-protein complex structure predictions by multimeric threading and template recombination. Structure 19, 955-966.
103. Kundrotas PJ, Zhu Z, Janin J, &, Vakser IA, (2012) Templates are available to model nearly all complexes of structurally characterized proteins. Proc Natl Acad Sci USA 109, 9438-9441.
104. Ghoorah AW, Devignes M-D, Smaïl-Tabbone M, &, Ritchie DW, (2013) Protein docking using case-based reasoning. Proteins 81, 2150-2158.
105. Vreven T, Hwang H, Pierce BG, &, Weng Z, (2013) Evaluating template-based and template-free protein-protein complex structure prediction. Brief Bioinform 15, 169-176.
106. Aloy P, Ceulemans H, Stark A, &, Russell RB, (2003) The relationship between sequence and interaction divergence in proteins. J Mol Biol 332, 989-998.
107. van Wijk SJL, Melquiond ASJ, de Vries SJ, Timmers HTM, &, Bonvin AMJJ, (2012) Dynamic control of selectivity in the ubiquitination pathway revealed by an ASP to GLU substitution in an intra-molecular salt-bridge network. PLoS Comput Biol 8, e1002754.
108. Liger D, Mora L, Lazar N, Figaro S, Henri J, Scrima N, Buckingham RH, van Tilbeurgh H, Heurgué-Hamard V, &, Graille M, (2011) Mechanism of activation of methyltransferases involved in translation by the Trm112 -'hub' protein. Nucleic Acids Res 39, 6249-6259.
109. Wodak SJ, &, Janin J, (1978) Computer analysis of protein-protein interaction. J Mol Biol 124, 323-342.
110. Levitt M, (2001) The birth of computational structural biology. Nat Struct Mol Biol 8, 392-393.
111. Melquiond AS, Karaca E, Kastritis PL, &, Bonvin AM, (2012) Next challenges in protein-protein docking: from proteome to interactome and beyond. Wiley Interdiscip Rev Comput Mol Sci 2, 642-651.
112. Das K, Acton T, Chiang Y, Shih L, Arnold E, &, Montelione GT, (2004) Crystal structure of RlmAI: implications for understanding the 23S rRNA G745/G748-methylation at the macrolide antibiotic-binding site. Proc Natl Acad Sci USA 101, 4041-4046.
113. Xue LC, Dobbs D, &, Honavar V, (2011) HomPPI: a class of sequence homology based protein-protein interface prediction methods. BMC Bioinform 12, 244.
114. de Vries SJ, &, Bonvin AMJJ, (2008) How proteins get in touch: interface prediction in the study of biomolecular complexes. Curr Protein Pept Sci 9, 394-406.
115. Ezkurdia I, Bartoli L, Fariselli P, Casadio R, Valencia A, &, Tress ML, (2008) Progress and challenges in predicting protein-protein interaction sites. Brief Bioinform 10, 233-246.