Comparative structural and energetic analysis of WW domain-peptide interactions

Journal of Molecular Biology

Volumn 344, Issue 3, 2004, Pages 865-881

  Schleinkofer, Karin ^a,b   Wiedemann, Urs ^c,d   Otte, Livia ^e   Wang, Ting ^b   Krause, Gerd ^c   Oschkinat, Hartmut ^c   Wade, Rebecca C ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b EML Research gGmbH   (Germany)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

binding affinity; peptide binding; protein protein interaction; structure activity relationship; WW domain

Indexed keywords

GLOBULAR PROTEIN; PEPTIDE LIBRARY;

ANALYTIC METHOD; ARTICLE; BINDING AFFINITY; COMPARATIVE MOLECULAR FIELD ANALYSIS; COMPARATIVE STUDY; LIGAND BINDING; MOLECULAR MODEL; MOLECULAR RECOGNITION; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; QUANTITATIVE STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

EID: 8344225386     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.09.063     Document Type: Article

References (64)

1. P. Bork, and M. Sudol The WW domain: a signalling site in dystrophin? Trends Biochem. Sci. 19 1994 531 533
2. M. Sudol, H.I. Chen, C. Bougeret, A. Einbond, and P. Bork Characterization of a novel protein-binding module - the WW domain FEBS Letters 369 1995 67 71
3. B.K. Kay, M.P. Williamson, and M. Sudol The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains FASEB J. 14 2000 231 241
4. M. Sudol From Src homology domains to other signaling modules: proposal of the 'protein recognition code' Oncogene 17 1998 1469 1474
5. M. Sudol, and T. Hunter NeW wrinkles for an old domain Cell 103 2000 1001 1004
6. M.J. Macias, M. Hyvonen, E. Baraldi, J. Schultz, M. Sudol, M. Saraste, and H. Oschkinat Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide Nature 382 1996 646 649
7. X. Huang, F. Poy, R. Zhang, A. Joachimiak, M. Sudol, and M.J. Eck Structure of a WW domain containing fragment of dystrophin in complex with beta-dystroglycan Nature Struct. Biol. 7 2000 634 638
8. L. Otte, U. Wiedemann, B. Schlegel, J.R. Pires, M. Beyermann, and P. Schmieder WW domain sequence activity relationships identified using ligand recognition propensities of 42 WW domains Protein Sci. 12 2003 491 500
9. N. Ferguson, C.M. Johnson, M. Macias, H. Oschkinat, and A. Fersht Ultrafast folding of WW domains without structured aromatic clusters in the denatured state Proc. Natl Acad. Sci. USA 98 2001 13002 13007
10. M.A. Verdecia, M.E. Bowman, K.P. Lu, T. Hunter, and J.P. Noel Structural basis for phosphoserine-proline recognition by group IV WW domains Nature Struct. Biol. 7 2000 639 643
11. 1H NMR study on the binding of Pin1 Trp-Trp domain with phosphothreonine peptides J. Biol. Chem. 276 2001 25150 25156
12. J.R. Pires, F. Taha-Nejad, F. Toepert, T. Ast, U. Hoffmuller, and J. Schneider-Mergener Solution structures of the YAP65 WW domain and the variant L30 K in complex with the peptides GTPPPPYTVG, N-(n-octyl)-GPPPY and PLPPY and the application of peptide libraries reveal a minimal binding epitope J. Mol. Biol. 314 2001 1147 1156
13. V. Kanelis, D. Rotin, and J.D. Forman-Kay Solution structure of a Nedd4 WW domain-ENaC peptide complex Nature Struct. Biol. 8 2001 407 412
14. F. Toepert, J.R. Pires, C. Landgraf, H. Oschkinat, and J. Schneider-Mergener Synthesis of an array comprising 837 variants of the hYAP WW protein domain Angew. Chem. Int. Ed. Engl. 40 2001 897 900
15. N. Blomberg, R.R. Gabdoulline, M. Nilges, and R.C. Wade Classification of protein sequences by homology modeling and quantitative analysis of electrostatic similarity Proteins: Struct. Funct. Genet. 37 1999 379 387
16. F. De Rienzo, R.R. Gabdoulline, M.C. Menziani, and R.C. Wade Blue copper proteins: a comparative analysis of their molecular interaction properties Protein Sci. 9 2000 1439 1454
17. R.C. Wade Derivation of QSARs using 3D structural models of protein-ligand complexes by COMBINE analysis H.-D. Holtje W. Sippl Rational Approaches to Drug Design: 13th European Symposium on Quantitative Structure-Activity Relationships 2001 Prous Science S.A. Barcelona 23 28
18. B. Honig, and A. Nicholls Classical electrostatics in biology and chemistry Science 268 1995 1144 1149
19. G. Cruciani, and K.A. Watson Comparative molecular field analysis using GRID force-field and GOLPE variable selection methods in a study of inhibitors of glycogen phosphorylase b J. Med. Chem. 37 1994 2589 2601
20. R.D. Cramer III, D.E. Patterson, and J.D. Bunce Comparative molecular field analysis (CoMFA). 1. Effect of shape on binding of steroids to carrier proteins J. Am. Chem. Soc. 110 1988 5959 5967
21. H. Kubinyi 3D QSAR Drug Design. Theory, Methods and Applications 1993 ESCOM Science Publishers B.V. Leiden, The Netherlands
22. A.R. Ortiz, M.T. Pisabarro, F. Gago, and R.C. Wade Prediction of drug binding affinities by comparative binding energy analysis J. Med. Chem. 38 1995 2681 2691
23. A.R. Ortiz, M. Pastor, A. Palomer, G. Cruciani, F. Gago, and R.C. Wade Reliability of comparative molecular field analysis models: effects of data scaling and variable selection using a set of human synovial fluid phospholipase A2 inhibitors J. Med. Chem. 40 1997 1136 1148
24. M. Pastor, F. Gago, and G. Cruciani Comparative binding energy (COMBINE) analysis on a series of glycogen phosphorylase inhibitors: comparison with GRID/GOLPE methods K. Gundertofter F.S. Jorgensen Molecular Modeling and Prediction of Bioactivity 2000 Kluwer New York 329 330
25. T. Wang, and R.C. Wade Comparative binding energy (COMBINE) analysis of influenza neuraminidase-inhibitor complexes J. Med. Chem. 44 2001 961 971
26. J.J. Lozano, M. Pastor, G. Cruciani, K. Gaedt, N.B. Centeno, F. Gago, and F. Sanz 3D-QSAR methods on the basis of ligand receptor complexes. Application of COMBINE and GRID/GOLPE methodologies to a series of CYP1A2 ligands J. Comput. Aided Mol. Des. 14 2000 341 353
27. J. Kmunicek, S. Luengo, F. Gago, A.R. Ortiz, R.C. Wade, and J. Damborsky Comparative binding energy (COMBINE) analysis of the substrate specificity of haloalkane dehalogenase from Xanthobacter autotrophicus GJ10 Biochemistry 40 2001 8905 8917
28. S. Tomic, and B. Kojic-Prodic A quantitative model for predicting enzyme enantioselectivity: application to burkholderia cepacia lipase and 3-(aryloxy)-1,2-propanediol derivatives J. Mol. Graph. Model. 21 2002 241 252
29. T. Wang, and R.C. Wade Comparative binding energy (COMBINE) analysis of OppA-peptide complexes to relate structure to binding thermodynamics J. Med. Chem. 45 2002 4828 4837
30. S. Tomic, and R.C. Wade COMBINE analysis of nuclear receptor-DNA binding specificity: comparison of two datasets Croat. Chem. Acta 74 2001 295 314
31. N. Ferguson, J.R. Pires, F. Toepert, C.M. Johnson, Y.P. Pan, and R. Volkmer-Engert Using flexible loop mimetics to extend phi-value analysis to secondary structure interactions Proc. Natl Acad. Sci. USA 98 2001 13008 13013
32. A.A. Adzhubei, and M.J. Sternberg Left-handed polyproline II helices commonly occur in globular proteins J. Mol. Biol. 229 1993 472 493
33. R. Carbo, and D. L. LCAO-MO similarity measures and taxonomy Int. J. Quant. Chem. 17 1987 517 545
34. C. Burt, and W.G. Richards The application of molecular similarity calculations J. Comput. Chem. 11 1990 1139 1146
35. E. Demchuk, T. Mueller, H. Oschkinat, W. Sebald, and R.C. Wade Receptor binding properties of four-helix-bundle growth factors deduced from electrostatic analysis Protein Sci. 3 1994 920 935
36. R.C. Wade, R.R. Gabdoulline, and B.A. Luty Species dependence of enzyme-substrate encounter rates for triose phosphate isomerases Proteins: Struct. Funct. Genet. 31 1998 406 416
37. R.C. Wade, R.R. Gabdoulline, S.K. Ludemann, and V. Lounnas Electrostatic steering and ionic tethering in enzyme-ligand binding: insights from simulations Proc. Natl Acad. Sci. USA 95 1998 5942 5949
38. G.M. Ullmann, M. Hauswald, A. Jensen, N.M. Kostic, and E.W. Knapp Comparison of the physiologically equivalent proteins cytochrome c6 and plastocyanin on the basis of their electrostatic potentials. Tryptophan 63 in cytochrome c6 may be isofunctional with tyrosine 83 in plastocyanin Biochemistry 36 1997 16187 16196
39. J. Felsenstein PHYLIP - phylogeny inference package (version 3.2) Cladistics 5 1989 164 166
40. W.D. Cornell, P. Cieplak, C.I. Payly, I.R. Gould, K.M. Merz, and D.M. Ferguson A second generation force field for the simulation of proteins, nucleic acids and organic molecules J. Am. Chem. Soc. 117 1995 5179 5197
41. G.T. Ibragimova, and R.C. Wade Stability of the beta-sheet of the WW domain: a molecular dynamics simulation study Biophys. J. 77 1999 2191 2198
42. J.C. Crane, E.K. Koepf, J.W. Kelly, and M. Gruebele Mapping the transition state of the WW domain beta-sheet J. Mol. Biol. 298 2000 283 292
43. M. Jager, H. Nguyen, J.C. Crane, J.W. Kelly, and M. Gruebele The folding mechanism of a beta-sheet: the WW domain J. Mol. Biol. 311 2001 373 393
44. H. Nguyen, M. Jager, A. Moretto, M. Gruebele, and J.W. Kelly Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation Proc. Natl Acad. Sci. USA 100 2003 3948 3953
45. A. Zarrinpar, and W.A. Lim Converging on proline: the mechanism of WW domain peptide recognition Nature Struct. Biol. 7 2000 611 613
46. M.P. Williamson The structure and function of proline-rich regions in proteins Biochem. J. 297 1994 249 260
47. J.P. Gallivan, and D.A. Doughtery Cation-pi interactions in structural biology Proc. Natl Acad. Sci. USA 96 1999 9459 9464
48. J. Schultz, F. Milpetz, P. Bork, and C.P. Ponting SMART, a simple modular architecture research tool: identification of signaling domains Proc. Natl Acad. Sci. USA 95 1998 5857 5864
49. I. Letunic, L. Goodstadt, N.J. Dickens, T. Doerks, J. Schultz, and R. Mott Recent improvements to the SMART domain-based sequence annotation resource Nucl. Acids Res. 30 2002 242 244
50. Y. Ho, A. Gruhler, A. Heilbut, G.D. Bader, L. Moore, and S.L. Adams Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry Nature 415 2002 180 183
51. A.C. Gavin, M. Bosche, R. Krause, P. Grandi, M. Marzioch, and A. Bauer Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 415 2002 141 147
52. T. Ito, T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, and Y. Sakaki A comprehensive two-hybrid analysis to explore the yeast protein interactome Proc. Natl Acad. Sci. USA 98 2001 4569 4574
53. L.J. Ball, T. Jarchau, H. Oschkinat, and U. Walter EVH1 domains: structure, function and interactions FEBS Letters 513 2002 45 52
54. R. Aasland, C. Abrams, C. Ampe, L.J. Ball, M.T. Bedford, and G. Cesareni Normalization of nomenclature for peptide motifs as ligands of modular protein domains FEBS Letters 513 2002 141 144
55. P.J. Goodford A computational procedure for determining energetically favorable binding sites on biologically important macromolecules J. Med. Chem. 28 1985 849 849
56. J.D. Madura, J.M. Briggs, R.C. Wade, M.E. Davis, B.A. Luty, and A. Ilin Electrostatics and diffusion of molecules in solution: simulations with the university of Houston Brownian dynamics program Comput. Phys. Commun. 91 1995 57 95
57. G. Vriend WHAT IF: a molecular modelling and drug design program J. Mol. Graph. 8 1990 52 56
58. R.W.W. Hooft, C. Sander, and G. Vriend Positioning hydrogen atoms by optimizing hydrogen bond networks in protein structures Proteins: Struct. Funct. Genet. 26 1996 363 376
59. E.E. Hodgkin, and W.G. Richards Molecular similarity based on electrostatic potential and electric field Int. J. Quant. Chem. Quant. Biol. Symp. 14 1987 105 110
60. M. Pastor, G. Cruciani, and S. Clementi Smart region definition: a new way to improve the predictive ability and interpretability of three-dimensional quantitative structure-activity relationships J. Med. Chem. 40 1997 1455 1464
61. C. Perez, M. Pastor, A.R. Ortiz, and F. Gago Comparative binding energy analysis of HIV-1 protease inhibitors: incorporation of solvent effects and validation as a powerful tool in receptor-based drug design J. Med. Chem. 41 1998 836 852
62. M. Baroni, G. Costantino, G. Cruciani, D. Riganelli, R. Valigi, and S. Clementi Generating optimal linear PLS estimations (GOLPE): an advanced chemometric tool for handling 3D-QSAR problems Quant. Struct.-Act. Relat. 12 1993 9 20
63. J.D. Thompson, T.J. Gibson, F. Plewniak, F. Jeanmougin, and D.G. Higgins The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucl. Acids Res. 25 1997 4876 4882
64. T. Wang, S. Tomic, R.R. Gabdoulline, and R.C. Wade How optimal are the binding energetics of barnase and barstar? Biophys. J. 12 2004 1563 1574