Quantifying intramolecular binding in multivalent interactions: A Structure-Based synergistic study on Grb2-Sos1 complex

PLoS Computational Biology

Volumn 7, Issue 10, 2011, Pages

  Sethi, Anurag ^a,b   Goldstein, Byron ^a   Gnanakaran, S ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b CENTER FOR NONLINEAR STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CELL MEMBRANES; CELL SIGNALING; MOLECULAR DYNAMICS; PROTEINS; STOICHIOMETRY; THERMOANALYSIS;

BINDING CONSTANT; EQUILIBRIA CONSTANTS; GROWTH FACTOR RECEPTOR-BOUND PROTEIN 2; INTRAMOLECULAR BINDING; MULTIVALENT BINDING; MULTIVALENT INTERACTIONS; POLYPROLINE; SIGNALLING PROTEINS; SON OF SEVENLESS; STRUCTURE-BASED;

EQUILIBRIUM CONSTANTS;

GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; PROTEIN SH3; RAS PROTEIN; SOS PROTEIN;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; CROSS LINKING; CYTOSOL; DISSOCIATION CONSTANT; EQUILIBRIUM CONSTANT; HYDROGEN BOND; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PROLINE RICH PROTEIN DOMAIN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; STOICHIOMETRY; THEORETICAL STUDY; THERMODYNAMICS; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PROBABILITY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; GRB2 ADAPTOR PROTEIN; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PROBABILITY; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; SOS1 PROTEIN;

EID: 80055072274     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002192     Document Type: Article

References (60)

1. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, et al. (1992) The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70: 431-442.
2. Yuzawa S, Yokochi M, Hatanaka H, Ogura K, Kataoka M, et al. (2001) Solution structure of Grb2 reveals extensive exibility necessary for target recognition. J Mol Biol 306: 527-37.
3. Nimnual AS, Yatsula BA, Bar-Sagi D, (1998) Coupling of ras and rac guanosine triphosphatases through the ras exchanger Sos. Science 279: 560-563.
4. Vetter IR, Wittinghofer A, (2001) The guanine nucleotide-binding switch in three dimensions. Science 294: 1299-1304.
5. Bunnell SC, Hong DI, Kardon JR, Yamazaki T, McGlade CJ, et al. (2002) T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J Cell Biol 158: 1263-1275.
6. Houtman JCD, Yamaguchi H, Barda-Saad M, Braiman A, Bowden B, et al. (2006) Oligomerization of signaling complexes by the multipoint binding of GRB2 to both LAT and SOS1. Nat Struct Mol Biol 13: 798-805.
7. Wilson BS, Pfeiffer JR, Surviladze Z, Gaudet EA, Oliver JM, (2001) High resolution mapping of mast cell membranes reveals primary and secondary domains of FcεRI and LAT. J Cell Biol 154: 645-658.
8. Nag A, Monine MI, Faeder JR, Goldstein B, (2009) Aggregation of membrane proteins by cytosolic cross-linkers: theory and simulation of the LAT-Grb2-SOS1 system. Biophys J 96: 2604-2623.
9. Tomlinson MG, Lin J, Weiss A, (2000) Lymphocytes with a complex: adapter proteins in antigen receptor signaling. Immunol Today 21: 584-591.
10. Simon JA, Schreiber SL, (1995) Grb2 SH3 binding to peptides from Sos: evaluation of a general model for SH3-ligand interactions. Chem Biol 2: 53-60.
11. Sparks AB, Rider JE, Hoffman NG, Fowlkes DM, Quillam LA, et al. (1996) Distinct ligand preferences of Src homology 3 domains from Src, Yes, Abl, Cortactin, p53bp2, PLC, Crk, and Grb2. Proc Natl Acad Sci U S A 93: 1540-4.
12. McDonald CB, Seldeen KL, Deegan BJ, Farooq A, (2008) Structural basis of the differential binding of the SH3 domains of Grb2 adaptor to the guanine nucleotide exchange factor Sos1. Arch Biochem Biophys 479: 52-62.
13. McDonald CB, Seldeen KL, Deegan BJ, Farooq A, (2009) SH3 domains of Grb2 adaptor bind to PXψPXR motifs within the Sos1 nucleotide exchange factor in a discriminate manner. Biochemistry 48: 4074-85.
14. Feng S, Chen JK, Yu H, Simon JA, Schreiber SL, (1994) Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266: 1241-1247.
15. Fernandez-Ballester G, Blanes-Mira C, Serrano L, (2004) The tryptophan switch: changing ligand-binding specificity from type I to type II in SH3 domains. J Mol Biol 335: 619-29.
16. Vidal M, Goudreau N, Cornille F, Cussac D, Gincel E, et al. (1999) Molecular and cellular analysis of Grb2 SH3 domain mutants: interaction with Sos and dynamin. J Mol Biol 290: 717-30.
17. Yang SS, Van Aelst L, Bar-Sagi D, (1995) Differential interactions of human Sos1 and Sos2 with Grb2. J Biol Chem 270: 18212-18215.
18. Raabe T, Olivier JP, Dickson B, Liu X, Gish GD, et al. (1995) Biochemical and genetic analysis of the Drk SH2/SH3 adaptor protein of Drosophila. EMBO J 14: 2509-2518.
19. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, et al. (2009) AutoDock4 and AutoDockTools4: Automated docking with selective receptor exibility. J Comput Chem 30: 2785-91.
20. Morris GM, Goodsell DS, Pique ME, Lindstrom W, Huey R, et al. (2009) Autodock version 4.2 userguide. http://autodockscrippsedu/faqs-help/manual/autodock-4-2-userguide/AutoDock42_UserGuidepdf.
21. Kohda D, Terasawa H, Ichikawa S, Ogura K, Hatanaka H, et al. (1994) Solution structure and ligand-binding site of the carboxy-terminal SH3 domain of GRB2. Structure 2: 1029-40.
22. Amaro RE, Baron R, McCammon JA, (2008) An improved relaxed complex scheme for receptor exibility in computer-aided drug design. J Comput Aided Mol Des 22: 693-705.
23. Kim R, Skolnick J, (2008) Assessment of programs for ligand binding affinity prediction. J Comput Chem 29: 1316-1331.
24. Musacchio A, Saraste M, Wilmanns M, (1994) High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat Struct Biol 1: 546-551.
25. Wu X, Knudsen B, Feller SM, Zheng J, Sali A, et al. (1995) Structural basis for the specific interaction of lysine-containing proline-rich peptides with the N-terminal SH3 domain of c-Crk. Structure 3: 215-226.
26. Zhou HX, (2006) Quantitative relation between intermolecular and intramolecular binding of pro-rich peptides to SH3 domains. Biophys J 91: 3170-81.
27. Van Valen D, Haataja M, Phillips R, (2009) Biochemistry on a leash: the roles of tether length and geometry in signal integration proteins. Biophys J 96: 1275-92.
28. Kratky O, Porod G, (1949) Röntgenuntersuchung gelöster fadenmoleküle. Rec Trav Chim Pays-Bas 68: 1106-1123.
29. Flory P, (1969) Statistical Mechanics of Chain Molecules Appendix G. John Wiley and Sons.
30. Zhou H, (2001) Loops in proteins can be modeled as worm-like chains. Journal of Physical Chemistry B 105: 6763-6766.
31. Ohashi T, Galiacy SD, Briscoe G, Erickson HP, (2007) An experimental study of GFPbased FRET, with application to intrinsically unstructured proteins. Protein Sci 16: 1429-1438.
32. Rawat N, Biswas P, (2009) Size, shape, and exibility of proteins and DNA. J Chem Phys 131: 165104.
33. Kim YC, Hummer G, (2008) Coarse-grained models for simulations of multiprotein complexes: application to ubiquitin binding. J Mol Biol 375: 1416-1433.
34. Chook YM, Gish GD, Kay CM, Pai EF, Pawson T, (1996) The Grb2-mSos1 complex binds phosphopeptides with higher affinity than Grb2. J Biol Chem 271: 30472-8.
35. Feng S, Kasahara C, Rickles RJ, Schreiber SL, (1995) Specific interactions outside the proline-rich core of two classes of src homology 3 ligands. Proc Natl Acad Sci U S A 92: 12408-12415.
36. Musacchio A, (2002) How SH3 domains recognize proline. Adv Protein Chem 61: 211-268.
37. Houtman JCD, Brown PH, Bowden B, Yamaguchi H, Appella E, et al. (2007) Studying multisite binary and ternary protein interactions by global analysis of isothermal titration calorimetry data in SEDPHAT: application to adaptor protein complexes in cell signaling. Protein Sci 16: 30-42.
38. Houtman JCD, Houghtling RA, Barda-Saad M, Toda Y, Samelson LE, (2005) Early phosphorylation kinetics of proteins involved in proximal TCR-mediated signaling pathways. J Immunol 175: 2449-2458.
39. Houtman JCD, Higashimoto Y, Dimasi N, Cho S, Yamaguchi H, et al. (2004) Binding specificity of multiprotein signaling complexes is determined by both cooperative interactions and affinity preferences. Biochemistry 43: 4170-4178.
40. Mathai Mammen GMW Seok-Ki Choi (1998) Polyvalent interactions in biological systems: Implications for design and use of multivalent ligands and inhibitors. Angewandte Chemie 37: 2754-2794.
41. Lundquist JJ, Debenham SD, Toone EJ, (2000) Multivalency effects in protein- carbohydrate interaction: the binding of the shiga-like toxin 1 binding subunit to multivalent c-linked glycopeptides. J Org Chem 65: 8245-50.
42. Zhou HX, (2001) The affinity-enhancing roles of exible linkers in two-domain DNAbinding proteins. Biochemistry 40: 15069-15073.
43. Zhou HX, (2003) Quantitative account of the enhanced affinity of two linked scFvs specific for different epitopes on the same antigen. J Mol Biol 329: 1-8.
44. Barua D, Faeder JR, Haugh JM, (2008) Computational models of tandem src homology 2 domain interactions and application to phosphoinositide 3-kinase. J Biol Chem 283: 7338-7345.
45. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
46. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
47. Sethi A, O'Donoghue P, Luthey-Schulten Z, (2005) Evolutionary profiles from the QR factorization of multiple sequence alignments. Proc Natl Acad Sci U S A 102: 4045-4050.
48. Roberts E, Eargle J, Wright D, Luthey-Schulten Z, (2006) Multiseq: unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics 7: 382.
49. William Humphrey AD, Schulten K, (1996) Vmd: Visual molecular dynamics. J Mol Graph 14: 33-38.
50. Krivov GG, Shapovalov MV, Dunbrack RLJ, (2009) Improved prediction of protein sidechain conformations with scwrl4. Proteins 77: 778-795.
51. Maignan S, Guilloteau JP, Fromage N, Arnoux B, Becquart J, et al. (1995) Crystal structure of the mammalian Grb2 adaptor. Science 268: 291-3.
52. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al. (2007) Comparative protein structure modeling using modeller. Curr Protoc Protein Sci Chapter 2: Unit 2.9.
53. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with namd. J Comput Chem 26: 1781-1802.
54. MacKerell JA, (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
55. Mark P, Nilsson L, (2001) Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 k. J Phys Chem A 105: 9954-9960.
56. Bas DC, Rogers DM, Jensen JH, (2008) Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins 73: 765-783.
57. Eargle J, Black AA, Sethi A, Trabuco LG, Luthey-Schulten Z, (2008) Dynamics of recognition between tRNA and elongation factor Tu. J Mol Biol 377: 1382-1405.
58. Darden T, York D, Pedersen L, (1993) Particle mesh Ewald: An nlog(n) method for Ewald sums in large systems. J Chem Phys 98: 10089.
59. Anderson H, (1983) Rattle: A "velocity" version of the shake algorithm for molecular dynamics calculations. J Comput Phys 52: 24-34.
60. Miyamoto S, Kollman PA, (1992) Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 13: 952-962.