COMBINE analysis of the specificity of binding of Ras proteins to their effectors

Proteins: Structure, Function and Genetics

Volumn 67, Issue 2, 2007, Pages 435-447

  Tomić, Sanja ^a   Bertoša, Branimir ^a   Wang, Ting ^b,c   Wade, Rebecca C ^b  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b EML Research gGmbH   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Binding affinity; Binding specificity; Hot spots; Mutation; Poisson Boltzmann electrostatics; Quantitative structure activity relationship; Raf; RalGDS; Rap; Ras

Indexed keywords

AMINO ACID; ASPARTIC ACID; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; MUTANT PROTEIN; RAF PROTEIN; RAL PROTEIN; RAP PROTEIN; RAS PROTEIN; SERINE; TYROSINE;

AMINO ACID COMPOSITION; ARTICLE; BINDING AFFINITY; BINDING KINETICS; COMPLEX FORMATION; CONTROLLED STUDY; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

AMINO ACIDS; COMPUTATIONAL BIOLOGY; ELECTROSTATICS; GUANOSINE TRIPHOSPHATE; MODELS, MOLECULAR; PROTEIN BINDING; RAS PROTEINS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 33947408000     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21321     Document Type: Article

References (56)

1. Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 1990;348: 125-132.
2. Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 1991;349:117-127.
3. Rapp UR, Goldsborough MD, Mark GE, Bonner TI, Groffen J, Reynolds FH, Jr, Stephenson J. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc Natl Acad Sci USA 1983;80:4218-4222.
4. Hamad NM, Elconin JE, Karnoub AE, Bai W, Rich JN, Abraham RT, Der CJ, Counter CM. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev 2002;16: 2045-2057.
5. Singh A, Sowjanya AP, Ramakrishna G. The wild-type Ras: road ahead. FASEB J 2005;19:161-169.
6. Bos JL. All in the family? New insights and questions regarding interconnectivity of Ras, Rap and Ral. EMBO J 1998;17:6776-6782.
7. Wolthuis RM, Bos JL. Ras caught in another affair: the exchange factors for Ral. Curr Opin Genet Dev 1999;9:112-117.
8. Feig LA. The Ral GTPases: approaching their 15 minutes of fame. Trends Cell Biol 2003;13:419-425.
9. Hamad NM, Elconin JH, Karnoub AE, Bai W, Rich JN, Abraham RT, Der CJ, Counter CM. Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev 2002;16: 2045-2057.
10. Boettner B, Van Aelst L. The RASputin effect. Genes Dev 2002;16:2033-2038.
11. Agapova LS, Volodina JL, Chumakov PM, Kopnin BP. Activation of Ras-RalGDS pathway attenuates p53-independent DNA damage G2 checkpoint. J Biol Chem 2004;279:36382-36389.
12. Wittinghofer A, Herrmann C. Ras effector interactions, the problem of specificity. FEBS Lett 1995;369:52-56.
13. Nassar N, Horn G, Herrmann C, Scherer A, McCormick F, Wittinghofer A. The 2.2 Å crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf1 in complex with Rap1A and a GTP analogue. Nature 1995;375:554-560.
14. Nassar N, Horn G, Herrmann C, Block C, Janknecht R, Wittinghofer A. Ras/Rap effector specificity determined by charge reversal. Nat Struct Biol 1996;3:723-729.
15. Vetter IR, Linnemann T, Wohlgemuth S, Geyer M, Kalbitzer HR, Herrmann C, Wittinghofer A. Structural and biochemical analysis of Ras-effector signaling via RalGDS. FEBS Lett 1999;451:175-180.
16. Huang L, Hofer F, Martin GS, Kim SH. Structural basis for the interaction of Ras with RalGDS. Nat Struct Biol 1998;5:422-426.
17. Kigawa T, Yamaguchi-Nunokawa E, Kodama K, Matsuda T, Yabuki T, Matsuda N, Ishitani R, Nureki O, Yokoyama S. Selenomethionine incorporation into a protein by cell-free synthesis. J Struct Funct Genomics 2002;2:29-35.
18. Spoerner M, Wittinghofer A, Kalbitzer HR. Perturbation of the conformational equilibria in Ras by selective mutations as studied by 31P NMR spectroscopy. FEBS Lett 2004;17;578:305-310.
19. Emerson SD, Madison VS, Palermo RE, Waugh DS, Scheffler JE, Tsao KL, Kiefer SE, Liu SP, Fry DC. Solution structure of the Ras-binding domain of c-Raf-1 and identification of its Ras interaction surface. Biochemistry 1995;34:6911-6918.
20. Huang L, Weng X, Hofer F, Martin GS, Kim SH. Three-dimensional structure of the Ras-interacting domain of RalGDS. Nat Struct Biol 1997;4:609-615.
21. Geyer M, Herrmann C, Wohlgemuth S, Wittinghofer A, Kalbitzer HR. Structure of the Ras-binding domain of RalGEF and implications for Ras binding and signaling. Nat Struct Biol 1997;4:694-699.
22. Walker EH, Perisic O, Ried C, Stephens L, Williams RL. Structural insights into phosphoinoside 3-kinase catalysis and signaling. Nature 1999;402:313-320.
23. Steiner G, Kremer W, Linnemann T, Herrmann C, Geyer M, Kalbitzer HR. Sequence-specific resonance assignment of the Ras-binding domain of AF6. J Biomol NMR 2000;18:73-74.
24. Gronwald W, Huber F, Grünewald P, Spörner M, Wohlgemuth S, Herrmann C, Kalbitzer HR. Solution structure of the Ras-binding domain of the protein kinase Byr2 from Schizosaccharomyces pombe. Structure 2001;9:1029-1041.
25. Scheffzeck K, Grünewald P, Wohlgemuth S, Kabsch W, Tu H, Wigler M, Wittinghofer A, Herrmann C. The Ras-Byr2RBD complex: structural basis for Ras effector recognition in yeast. Structure 2001;9:1043-1050.
26. Gohlke H, Kuhn LA, Case DA. Change in protein flexibility upon complex formation: analysis of Ras-Raf using molecular dynamics and a molecular framework approach. Proteins 2004;56:322-337.
27. Gohlke H, Case DA. Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf. J Comput Chem 2004;25:238-250.
28. Gohlke H, Kiel C, Case DA. Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes. J Mol Biol 2003;330:891-913.
29. Kiel C, Serrano L, Herrmann C. A detailed thermodynamic analysis of Ras/effector complex interfaces. J Mol Biol 2004;340: 1039-1058.
30. Muegge I, Schweins T, Warshel A. Electrostatic contributions to protein-protein binding affinities: application to Rap/Raf interaction. Proteins 1998;30:407-423.
31. Sheinerman FB, Honig B. On the role of electrostatic interactions in the design of protein-protein interfaces. J Mol Biol 2002;318:161-177.
32. Kiel C, Wohlgemuth S, Rousseau F, Schymkowitz J, Ferkingh-off-Borg J, Wittinghofer F, Serrano L. Recognizing and defining true ras binding domains II: in silico prediction based on homology modelling and energy calculations. J Mol Biol 2005;348:759-775.
33. Madura JD, Briggs JM, Wade RC, Davis ME, Luty BA, Ilin A, Antosiewicz J, Gilson MK, Bagheri B, Scott LR, McCammon JA. Electrostatics and diffusion of molecules in solution: simulations with the university of Houston brownian dynamics program. Comput Phys Commun 1995;91:57-95.
34. Ortiz AR, Pisabarro MT, Gago F, Wade RC. Prediction of drug binding affinities by comparative binding energy analysis. J Med Chem 1995;38:2681-2691.
35. Ortiz AR, Pastor M, Palomer A, Cruciani G, Gago F, Wade RC. 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 1997;40:1136-1148.
36. Wade RC, Henrich S, Wang T. Using 3D protein structures to derive 3D-QSARs Drug Discovery Today: Technologies 2004;1: 241-246.
37. Wade RC. Derivation of QSARs using 3D structural models of protein-ligand complexes by COMBINE analysis. In: Holtje HD,Sippl W, editors. Rational approaches to drug design: 13th European symposium on quantitative structure-activity relationships. Barcelona: Prous Science SA; 2001. pp 23-28.
38. Pastor M, Gago F, Cruciani G. Comparative binding energy (COMBINE) analysis on a series of glycogen phosphorylase inhibitors: comparison with GRID/GOLPE methods. In: Gundertofter K, Jorgensen FS, editors. Molecular modeling and prediction of bioactivity. New York: Kluwer; 2000. pp 329-330.
39. Wang T, Wade RC. Comparative binding energy (COMBINE) analysis of influenza neuraminidase-inhibitor complexes. J Med Chem 2001;44:961-671.
40. Lozano JJ, Pastor M, Cruciani G, Gaedt K, Centeno NB, Gago F, Sanz F. 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 2000;14:341-353.
41. Tomic S, Kojic-Prodic B. A quantitative model for predicting enzyme enantioselectivity: application to burkholderia cepacia lipase and 3-(aryloxy)-1,2-propanediol derivatives. J Mol Graph Model 2002;21:241-252.
42. Tomić S, Bertoša B, Kojić-Prodić B, Kolosvary I. Stereoselectivity of Burkholderia cepacia lipase towards secondary alcohols: molecular modelling and 3D QSAR approach. Tetrahedron Asymmetry 2004;15:1163-1172.
43. Tomić S. Enantioselectivity of burkholderia cepacia lipase towards primary and secondary alcohols: molecular modelling and 3D QSAR analysis. In: Ford M, Livingstone D, Dearden J, vande Waterbeemd H, editors. Designing drugs and crop protectants: processes, problems and solutions. Oxford, UK: Blackwell; 2003. pp 326-328.
44. Wang T, Wade RC. Comparative binding energy (COMBINE) analysis of OppA-peptide complexes to relate structure to binding thermodynamics. J Med Chem 2002;45:4828-4837.
45. Tomic S, Nilsson L, Wade RC. Nuclear receptor-DNA binding specificity: a COMBINE and free-Wilson QSAR analysis. J Med Chem 2000;45:1780-1792.
46. Tomić S, Wade RC. COMBINE analysis of nuclear receptor-DNA binding specificity: comparison of two datasets. Croatica Chemica Acta 2001;74:295-314.
47. Wang T, Tomić S, Gabdoulline R, Wade RC. How optimal are the binding energetics of barnase and barstar? Biophys J 2004;12: 1563-1574.
48. InsightII version 2000. San Diego, CA: Accelrys, Inc.
49. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comp Chem 2003;24:1999-1994.
50. Vriend G. WHAT IF: a molecular modelling and drug design program. J Mol Graph 1990;8:52-56
51. Hooft RW, Sander C, Vriend G. Positioning hydrogen atoms by optimizing hydrogen bond networks in protein structures. Proteins 1996;26:363-376.
52. Madura JD, Briggs JM, Wade RC, Davis ME, Luty BA, Ilin A, Antosiewicz J, Gilson MK, Bagheri B, Scott LR. Electrostatics and diffusion of molecules in solution: simulations with the university of Houston Brownian dynamics program. Comput Phys Commun 1995;91:57-95.
53. Perez C, Pastor M, Ortiz AR, Gago F. 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 1998;41:836-852.
54. Baroni M, Costantino G, Cruciani G, Riganelli D, Valigi R, Clementi S. Generating optimal linear PLS estimations (GOLPE): an advanced chemometric tool for handling 3D-QSAR problems. Quant Struct Act Rel 1993;12:9-20.
55. Kiel C, Selzer T, Shaul Y, Schreiber G, Herrmann C. Electrostatically optimized Ras-binding Ral guanine dissociation stimulator mutants increase the rate of association by stabilizing the encounter complex. PNAS 2004;101:9223-9228.
56. Trosset J-Y, Dalvit C, Knapp S, Fasolini M, Veronesi M, Mantegani S, Gianellini LM, Catana C, Sundström M, FW, Stouten PFW, Jürgen K, Moll JK. Inhibition of protein-protein interactions: the discovery of druglike β-catenin inhibitors by combining virtual and biophysical screening biophysical screening. Proteins 2006;64:60-67.