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Docking Predictions of Protein-Protein Interactions and Their Assessment: The CAPRI Experiment

Chapter
Part of the Focus on Structural Biology book series (FOSB, volume 8)

Abstract

Protein-protein docking was born in the 1970s as a tool to analyze macromolecular recognition. It developed afterwards into a method of prediction of the mode of association between proteins of known structure. Since 2001, the performance of docking procedures has been assessed in blind predictions by the CAPRI (Critical Assessment of PRedicted Interactions) experiment. The results show that docking routinely yields good models of the protein-protein complexes that undergo only minor changes in conformation and associate as rigid bodies. In contrast, flexible recognition accompanying large conformation changes in the components remains difficult to simulate, and structural predictions generally yield lower quality models. In recent years, a new challenge has been to predict affinity and to estimate the stability of the complex along with its structure. Over the years, CAPRI has proved to be a strong incentive to develop new flexible docking procedures and more discriminative scoring functions, and it has provided a common ground for discussing methods and questions related to protein-protein recognition.

Keywords

Community-wide experiment Protein-protein recognition Binding affinity Protein flexibility Protein engineering Docking simulation Computational biology DOCK CAPRI Rigid body docking Cube representation Geometric hashing algorithm Monte-Carlo RosettaDock Template-based docking CASP Blind prediction Flexible docking Molecular dynamics Flexibility Affinity benchmark 

Notes

Acknowledgements

JJ acknowledges a long term collaboration with Pr. Shoshana Wodak (Free University, Brussels, and University of Toronto), fostered in its early days by Dr. Georges Cohen (Institut Pasteur, Paris), the European Molecular Biology Organisation, and Centre Européen de Calcul Atomique et Moléculaire. The CAPRI experiment owes much to R. Mendez and M. Lensink who perform the assessment together with S. Wodak, to K. Henrick and S. Velenkar who manage its Web site at the European Bioinformatics Institute (Hinxton, UK), to J. Moult, S. Vajda, I. Vakser, M. Sternberg, and L. Ten Eyck, who assist in its management, and to all the structural biologists who have contributed targets.

References

  1. Baldwin J, Chothia C (1979) Haemoglobin: the structural changes related to ligand binding and its allosteric mechanism. J Mol Biol 129:175–220PubMedCrossRefGoogle Scholar
  2. Beddell CR, Goodford PJ, Norrington FE, Wilkinson S, Wootton R (1976) Compounds designed to fit a site of known structure in human haemoglobin. Br J Pharmacol 57:201–209PubMedCrossRefGoogle Scholar
  3. Blow DM, Wright CS, Kukla D, Rühlmann A, Steigemann W, Huber R (1972) A model for the association of bovine pancreatic trypsin inhibitor with chymotrypsin and trypsin. J Mol Biol 69:137–144PubMedCrossRefGoogle Scholar
  4. Bode W, Schwager P, Huber R (1978) The transition of bovine trypsinogen to a trypsin-like state upon strong ligand binding. The refined crystal structures of the bovine trypsinogen-pancreatic trypsin inhibitor complex and of its ternary complex with Ile-Val at 1.9 A resolution. J Mol Biol 118:99–112PubMedCrossRefGoogle Scholar
  5. Bonvin AM (2006) Flexible protein-protein docking. Curr Opin Struct Biol 16:194–200PubMedCrossRefGoogle Scholar
  6. Camacho CJ, Vajda S (2002) Protein-protein association kinetics and protein docking. Curr Opin Struct Biol 12:36–40PubMedCrossRefGoogle Scholar
  7. Chen R, Li L, Weng Z (2003a) ZDOCK: an initial-stage protein-docking algorithm. Proteins 52:80–87PubMedCrossRefGoogle Scholar
  8. Chen R, Mintseris J, Janin J, Weng Z (2003b) A protein-protein docking benchmark. Proteins 52:88–91PubMedCrossRefGoogle Scholar
  9. Cherfils J, Duquerroy S, Janin J (1991) Protein-protein recognition analyzed by docking simulation. Proteins 11:271–280PubMedCrossRefGoogle Scholar
  10. Connolly ML (1986) Shape complementarity at the hemoglobin a1 b1 subunit interface. Biopolymers 25:1229–1247PubMedCrossRefGoogle Scholar
  11. de Vries SJ, van Dijk AD, Krzeminski M, van Dijk M, Thureau A, Hsu V, Wassenaar T, Bonvin AM (2007) HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 69:726–733PubMedCrossRefGoogle Scholar
  12. de Vries SJ, van Dijk M, Bonvin AM (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5:883–897PubMedCrossRefGoogle Scholar
  13. Dobbins SE, Lesk VI, Sternberg MJ (2008) Insights into protein flexibility: The relationship between normal modes and conformational change upon protein-protein docking. Proc Natl Acad Sci USA. 105:10390–5Google Scholar
  14. Dominguez C, Boelens R, Bonvin AM (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125:1731–1737PubMedCrossRefGoogle Scholar
  15. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN (2005) Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J 272:5129–5148PubMedCrossRefGoogle Scholar
  16. Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18:756–764PubMedCrossRefGoogle Scholar
  17. Fernández-Recio J, Totrov M, Abagyan R (2002) Soft protein-protein docking in internal coordinates. Protein Sci 11:280–291PubMedCrossRefGoogle Scholar
  18. Fieulaine S, Morera S, Poncet S, Mijakovic I, Galinier A, Janin J, Deutscher J, Nessler S (2002) X-ray structure of a bifunctional protein kinase in complex with its protein substrate HPr. Proc Natl Acad Sci USA 99:13437–13441PubMedCrossRefGoogle Scholar
  19. Fleishman SJ, Whitehead TA, Ekiert DC, Dreyfus C, Corn JE, Strauch EM, Wilson IA, Baker D (2011a) Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332:816–821PubMedCrossRefGoogle Scholar
  20. Fleishman SJ, Whitehead TA, Strauss EM et al., Wodak SJ, Janin J, Baker D (2011b) Community-wide assessment of protein-interface modeling suggests improvements to design methodology. J Mol Biol Accepted manuscript doi: 10.1016/j.jmb.2011.09.031
  21. Gabb HA, Jackson RM, Sternberg MJ (1997) Modelling protein docking using shape complementarity, electrostatics and biochemical information. J Mol Biol 272:106–120PubMedCrossRefGoogle Scholar
  22. Goodford PJ (1985) A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. J Med Chem 28:849–857PubMedCrossRefGoogle Scholar
  23. 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 331:281–299PubMedCrossRefGoogle Scholar
  24. Grünberg R, Leckner J, Nilges M (2004) Complementarity of structure ensembles in protein-protein binding. Structure 12:2125–2136PubMedCrossRefGoogle Scholar
  25. Grünberg R, Nilges M, Leckner J (2006) Flexibility and conformational entropy in protein-protein binding. Structure 14:683–693PubMedCrossRefGoogle Scholar
  26. Günther S, May P, Hoppe A, Frömmel C, Preissner R (2007) Docking without docking: ISEARCH–prediction of interactions using known interfaces. Proteins 69:839–844PubMedCrossRefGoogle Scholar
  27. Halperin I, Ma B, Wolfson H, Nussinov R (2002) Principles of docking: an overview of search algorithms and a guide to scoring functions. Proteins 47:409–443PubMedCrossRefGoogle Scholar
  28. Heifetz A, Katchalski-Katzir E, Eisenstein M (2002) Electrostatics in protein-protein docking. Protein Sci 11:571–587PubMedCrossRefGoogle Scholar
  29. Horton N, Lewis M (1992) Calculation of the free energy of association for protein complexes. Protein Sci 1:169–181PubMedCrossRefGoogle Scholar
  30. Huber R, Kukla D, Bode W, Schwager P, Bartels K, Deisenhofer J, Steigemann W (1974) Structure of the complex formed by bovine trypsin and bovine pancreatic trypsin inhibitor. II. Crystallographic refinement at 1.9 A resolution. J Mol Biol 89:73–101PubMedCrossRefGoogle Scholar
  31. Hwang H, Vreven T, Janin J, Weng Z (2010) Protein-protein docking benchmark version 4.0. Proteins 78:3111–3114PubMedCrossRefGoogle Scholar
  32. Isabet T, Montagnac G, Regazzoni K, Raynal B, Elkhadali F, Franco M, England P, Chavrier P, Houdusse A, Menetrey J (2009) The structural basis of Arf effector specificity: the crystal structure of ARF6 in a complex with JIP4. EMBO J 28:2835–2845Google Scholar
  33. Janin J (2005) Assessing predictions of protein-protein interaction: the CAPRI experiment. Protein Sci 14:278–283PubMedCrossRefGoogle Scholar
  34. Janin J (2010) Protein-protein docking tested in blind predictions: the CAPRI experiment. Mol Biosyst 6:2351–2362PubMedCrossRefGoogle Scholar
  35. Janin J, Chothia C (1990) The structure of protein-protein recognition sites. J Biol Chem 265:16027–16030PubMedGoogle Scholar
  36. Janin J, Wodak SJ (1981) Report on the workshop on non-bonded interactions and the specificity of protein association and folding. CECAM, Orsay, France pp 5–64Google Scholar
  37. Janin J, Wodak SJ (1985) Reaction pathway for the quaternary structure change in hemoglobin. Biopolymers 24:509–526PubMedCrossRefGoogle Scholar
  38. Janin J, Henrick K, Moult J, Eyck LT, Sternberg MJ, Vajda S, Vakser I, Wodak SJ (2003) CAPRI: a critical assessment of PRedicted interactions. Proteins 52:2–9PubMedCrossRefGoogle Scholar
  39. Jiang F, Kim SH (1991) “Soft docking”: matching of molecular surface cubes. J Mol Biol 219:79–102PubMedCrossRefGoogle Scholar
  40. Karanicolas J, Corn JE, Chen I, Joachimiak LA, Dym O, Peck SH, Albeck S, Unger T, Hu W, Liu G, Delbecq S, Montelione GT, Spiegel CP, Liu DR, Baker D (2011) A de novo protein binding pair by computational design and directed evolution. Mol Cell 42:250–260PubMedCrossRefGoogle Scholar
  41. Kastritis PL, Bonvin AM (2010) Are scoring functions in protein-protein docking ready to predict interactomes? Clues from a novel binding affinity benchmark. J Proteome Res 9:2216–2225, Erratum in: J Proteome Res 10:921–2, 2011PubMedCrossRefGoogle Scholar
  42. Kastritis PL, Moal IH, Hwang H, Weng Z, Bates PA, Bonvin AM, Janin J (2011) A structure-based benchmark for protein-protein binding affinity. Protein Sci 20:482–491PubMedCrossRefGoogle Scholar
  43. 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 89:2195–2199PubMedCrossRefGoogle Scholar
  44. Keskin O, Nussinov R, Gursoy A (2008) PRISM: protein-protein interaction prediction by structural matching. Methods Mol Biol 484:505–521PubMedCrossRefGoogle Scholar
  45. 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.109:9438–41Google Scholar
  46. Kuntz ID, Blaney JM, Oatley SJ, Langridge R, Ferrin TE (1982) A geometric approach to macromolecule-ligand interactions. J Mol Biol 161:269–288PubMedCrossRefGoogle Scholar
  47. Lensink MF, Wodak SJ (2010) Docking and scoring protein interactions: CAPRI 2009. Proteins 78:3073–3084PubMedCrossRefGoogle Scholar
  48. Lensink MF, Méndez R, Wodak SJ (2007) Docking and scoring protein complexes: CAPRI 3rd edition. Proteins 69:704–718PubMedCrossRefGoogle Scholar
  49. Lesk VI, Sternberg MJ (2008) 3D-Garden: a system for modelling protein-protein complexes based on conformational refinement of ensembles generated with the marching cubes algorithm. Bioinformatics 24:1137–1144PubMedCrossRefGoogle Scholar
  50. Levinthal C, Wodak SJ, Kahn P, Dadivanian AK (1975) Hemoglobin interaction in sickle cell fibers. I: theoretical approaches to the molecular contacts. Proc Natl Acad Sci USA 72:1330–1334PubMedCrossRefGoogle Scholar
  51. Levitt M (1976) A simplified representation of protein conformations for rapid simulation of protein folding. J Mol Biol 104:59–107PubMedCrossRefGoogle Scholar
  52. Levitt M, Lifson S (1969) Refinement of protein conformations using a macromolecular energy minimization procedure. J Mol Biol 46(2):269–279PubMedCrossRefGoogle Scholar
  53. Lu L, Arakaki AK, Lu H, Skolnick J (2003). Multimeric threading-based prediction of protein-protein interactions on a genomic scale: application to the Saccharomyces cerevisiae proteome. Genome Res. 13:1146–54Google Scholar
  54. Lu L, Lu H, Skolnick J (2002) MULTIPROSPECTOR: an algorithm for the prediction of protein-protein interactions by multimeric threading. Proteins 49:350–364PubMedCrossRefGoogle Scholar
  55. Mandell JG, Roberts VA, Pique ME, Kotlovyi V, Mitchell JC, Nelson E, Tsigelny I, Ten Eyck LF (2001) Protein docking using continuum electrostatics and geometric fit. Protein Eng 14:105–113PubMedCrossRefGoogle Scholar
  56. Mashiach E, Schneidman-Duhovny D, Peri A, Shavit Y, Nussinov R, Wolfson HJ (2010) An integrated suite of fast docking algorithms. Proteins 78:3197–3204PubMedCrossRefGoogle Scholar
  57. Méndez R, Leplae R, De Maria L, Wodak SJ (2003) Assessment of blind predictions of protein-protein interactions: current status of docking methods. Proteins 52:51–67PubMedCrossRefGoogle Scholar
  58. Méndez R, Leplae R, Lensink MF, Wodak SJ (2005) Assessment of CAPRI predictions in rounds 3–5 shows progress in docking procedures. Proteins 60:150–169PubMedCrossRefGoogle Scholar
  59. Moult J, Pedersen JT, Judson R, Fidelis K (1995) A large-scale experiment to assess protein structure prediction methods. Proteins 23(3):ii–vPubMedCrossRefGoogle Scholar
  60. Némethy G, Scheraga HA (1977) Protein folding. Q Rev Biophys 10:239–252PubMedCrossRefGoogle Scholar
  61. Norel R, Lin SL, Wolfson HJ, Nussinov R (1994) Molecular surface complementarity at protein-protein interfaces: the critical role played by surface normals at well placed, sparse, points in docking. J Mol Biol 252:263–273CrossRefGoogle Scholar
  62. Nussinov R, Wolfson HJ (1991) Efficient detection of three-dimensional structural motifs in biological macromolecules by computer vision techniques. Proc Natl Acad Sci USA 88:10495–10499PubMedCrossRefGoogle Scholar
  63. Ritchie DW (2008) Recent progress and future directions in protein-protein docking. Curr Protein Pept Sci 9:1–15PubMedCrossRefGoogle Scholar
  64. Ritchie DW, Kemp GJ (2000) Protein docking using spherical polar Fourier correlations. Proteins 39:178–194PubMedCrossRefGoogle Scholar
  65. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ (2005) Geometry-based flexible and symmetric protein docking. Proteins 60:224–231PubMedCrossRefGoogle Scholar
  66. Schueler-Furman O, Wang C, Bradley P, Misura K, Baker D (2005) Progress in modeling of protein structures and interactions. Science 310:638–642PubMedCrossRefGoogle Scholar
  67. Sinha R, Kundrotas PJ, Vakser IA (2010) Docking by structural similarity at protein-protein interfaces. Proteins 78:3235–3241PubMedCrossRefGoogle Scholar
  68. Smith GR, Sternberg MJ (2002) Prediction of protein-protein interactions by docking methods. Curr Opin Struct Biol 12:28–35PubMedCrossRefGoogle Scholar
  69. Stein A, Mosca R, Aloy P (2011) Three-dimensional modeling of protein interactions and complexes is going ‘omics. Curr Opin Struct Biol 21:200–208PubMedCrossRefGoogle Scholar
  70. Stratmann D, Boelens R, Bonvin AM (2011) Quantitative use of chemical shifts for the modeling of protein complexes. Proteins 79:2662–2670PubMedCrossRefGoogle Scholar
  71. Strynadka NC, Eisenstein M, Katchalski-Katzir E, Shoichet BK, Kuntz ID, Abagyan R, Totrov M, Janin J, Cherfils J, Zimmerman F, Olson A, Duncan B, Rao M, Jackson R, Sternberg M, James MN (1996) Molecular docking programs successfully predict the binding of a b-lactamase inhibitory protein to TEM-1 b-lactamase. Nat Struct Biol 3:233–239PubMedCrossRefGoogle Scholar
  72. 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–W170PubMedCrossRefGoogle Scholar
  73. Tompa P, Fuxreiter M, Oldfield CJ, Simon I, Dunker AK, Uversky VN (2009) Close encounters of the third kind: disordered domains and the interactions of proteins. Bioessays 31:328–335PubMedCrossRefGoogle Scholar
  74. Totrov M, Abagyan R (1994) Detailed ab initio prediction of lysozyme-antibody complex with 1.6 A accuracy. Nat Struct Biol 1:259–263PubMedCrossRefGoogle Scholar
  75. Tuncbag N, Gursoy A, Guney E, Nussinov R, Keskin O (2008) Architectures and functional coverage of protein-protein interfaces. J Mol Biol 381:785–802PubMedCrossRefGoogle Scholar
  76. Vajda S, Vakser IA, Sternberg MJ, Janin J (2002) Modeling of protein interactions in genomes. Proteins 47:444–446PubMedCrossRefGoogle Scholar
  77. Vakser IA, Aflalo C (1994) Hydrophobic docking: a proposed enhancement to molecular recognition techniques. Proteins 20:320–329PubMedCrossRefGoogle Scholar
  78. Wodak SJ, Janin J (1978) Computer analysis of protein-protein interaction. J Mol Biol 124:323–342PubMedCrossRefGoogle Scholar
  79. Zacharias M (2003) Protein-protein docking with a reduced protein model accounting for side-chain flexibility. Protein Sci 12:1271–1282PubMedCrossRefGoogle Scholar
  80. Zacharias M (2010) Accounting for conformational changes during protein-protein docking. Curr Opin Struct Biol 20:180–186PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.IBBMCUniversité Paris-SudOrsayFrance

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