Thermodynamic, dynamic and solvational properties of PDEδ binding to farnesylated cystein: A model study for uncovering the molecular mechanism of PDEδ interaction with prenylated proteins

Journal of Physical Chemistry B

Volumn 118, Issue 4, 2014, Pages 966-975

  Suladze, S ^a   Ismail, S ^b   Winter, R ^a  

^a TU DORTMUND UNIVERSITY   (Germany)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROPHOBICITY;

BIOLOGICAL FUNCTIONS; HYDROPHOBIC LIGAND; HYDROPHOBIC POCKETS; INTERACTING SPECIES; MOLECULAR DESIGN; MOLECULAR MECHANISM; SOLVENT ACCESSIBLE SURFACE AREAS; VOLUME FLUCTUATIONS;

PROTEINS;

CYSTEINE; DRUG DERIVATIVE; PHOSPHODIESTERASE VI; RAS PROTEIN;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN PRENYLATION; SOLUBILITY; THERMODYNAMICS;

BINDING SITES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; CYSTEINE; MODELS, MOLECULAR; PROTEIN PRENYLATION; RAS PROTEINS; SOLUBILITY; THERMODYNAMICS;

EID: 84893483116     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp411466r     Document Type: Article

References (54)

1. Ismail, S. A.; Chen, Y. X.; Rusinova, A.; Chandra, A.; Bierbaum, M.; Gremer, L.; Triola, G.; Waldmann, H.; Bastiaens, P. I.; Wittinghofer, A. Arl2-GTP and Arl3-GTP Regulate a GDI-Like Transport System for Farnesylated Cargo Nat. Chem. Biol. 2011, 7 (12) 942-949
2. Zimmermann, G.; Papke, B.; Ismail, S.; Vartak, N.; Chandra, A.; Hoffmann, M.; Hahn, S. A.; Triola, G.; Wittinghofer, A.; Bastiaens, P. I. Small Molecule Inhibition of the KRas-PDEδ Interaction Impairs Oncogenic KRas Signalling Nature 2013, 497 (7451) 638-642
3. Baker, N. M.; Der, C. J. Cancer: Drug for an 'Undruggable' Protein Nature 2013, 497 (7451) 577-578
4. Chandra, A.; Grecco, H. E.; Pisupati, V.; Perera, D.; Cassidy, L.; Skoulidis, F.; Ismail, S. A.; Hedberg, C.; Hanzal-Bayer, M.; Venkitaraman, A. R. The GDI-Like Solubilizing Factor PDEδ Sustains the Spatial Organization and Signalling of Ras Family Proteins Nat. Cell Biol. 2011, 14 (2) 148-158
5. Weise, K.; Kapoor, S.; Werkmuller, A.; Mobitz, S.; Zimmermann, G.; Triola, G.; Waldmann, H.; Winter, R. Dissociation of the K-Ras4B/PDEδ Complex upon Contact with Lipid Membranes: Membrane Delivery Instead of Extraction J. Am. Chem. Soc. 2012, 134 (28) 11503-11510
6. Iwig, J. S.; Kuriyan, J. Fixing a Hole Where the Ras Gets In Cell 2013, 153 (6) 1191-1193
7. Frett, B.; Wang, Y.; Li, H. Y. Targeting the K-Ras/PDEδ Protein-Protein Interaction: The Solution for Ras-Driven Cancers or Just Another Therapeutic Mirage? ChemMedChem 2013, 8, 1620-1622
8. Zhang, H.; Liu, X. H.; Zhang, K.; Chen, C. K.; Frederick, J. M.; Prestwich, G. D.; Baehr, W. Photoreceptor cGMP Phosphodiesterase Delta Subunit (PDEδ) Functions as a Prenyl-binding Protein J. Biol. Chem. 2004, 279 (1) 407-413
9. Lopez, M. M.; Makhatadze, G. I. Isothermal Titration Calorimetry Methods Mol. Biol. 2002, 173, 121-126
10. Wiseman, T.; Williston, S.; Brandts, J. F.; Lin, L. N. Rapid Measurement of Binding Constants and Heats of Binding Using a New Titration Calorimeter Anal. Biochem. 1989, 179 (1) 131-137
11. Makhatadze, G. I. Measuring Protein Thermostability by Differential Scanning Calorimetry Curr. Protoc. Protein Sci. 2001, 7.9.1-7.9.14
12. Makhatadze, G. I.; Privalov, P. L. Heat Capacity of Proteins. I. Partial Molar Heat Capacity of Individual Amino Acid Residues in Aqueous Solution: Hydration effect J. Mol. Biol. 1990, 213 (2) 375-384
13. Zhai, Y.; Okoro, L.; Cooper, A.; Winter, R. Applications of Pressure Perturbation Calorimetry in Biophysical Studies Biophys. Chem. 2011, 156 (1) 13-23
14. Lin, L. N.; Brandts, J. F.; Brandts, J. M.; Plotnikov, V. Determination of the Volumetric Properties of Proteins and Other Solutes Using Pressure Perturbation Calorimetry Anal. Biochem. 2002, 302 (1) 144-160
15. Krivanek, R.; Okoro, L.; Winter, R. Effect of Cholesterol and Ergosterol on the Compressibility and Volume Fluctuations of Phospholipid-Sterol Bilayers in the Critical Point Region: A Molecular Acoustic and Calorimetric Study Biophys. J. 2008, 94 (9) 3538-3548
16. Kratky, O.; Leopold, H.; Stabinger, H. The Determination of the Partial Specific Volume of Proteins by the Mechanical Oscillator Technique Methods Enzymol. 1973, 27, 98-110
17. Barnartt, S. The Velocity of Sound in Electrolytic Solutions J. Chem. Phys. 1952, 20 (2) 278
18. Taulier, N.; Chalikian, T. V. Compressibility of Protein Transitions Biochim. Biophys. Acta 2002, 1595, 48-70
19. Sarvazyan, A. P. Ultrasonic Velocimetry of Biological Compounds Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 321-342
20. Chalikian, T. V.; Totrov, M.; Abagyan, R.; Breslauer, K. J. The Hydration of Globular Proteins as Derived from Volume and Compressibility Measurements: Cross Correlating Thermodynamic and Structural Data J. Mol. Biol. 1996, 260 (4) 588-603
21. Blandamer, M. J.; Davis, M. I.; Douheret, G.; Reis, J. C. R. Apparent Molar Isentropic Compressions and Expansions of Solutions Chem. Soc. Rev. 2001, 30 (1) 8-15
22. Delano, W. The PyMOL Molecular Graphics System, version 1.5.0.4; Schrödinger, LLC: Portland, OR, 2002.
23. Richards, F. M. Areas, Volumes, Packing and Protein Structure Annu. Rev. Biophys. Bioeng. 1977, 6, 151-176
24. Voss, N. R.; Gerstein, M. 3V: Cavity, Channel and Cleft Volume Calculator and Extractor Nucleic. Acids. Res. 2010, 38, W555-62 (Web Server issue)
25. Gerstein, M.; Tsai, J.; Levitt, M. The Volume of Atoms on the Protein Surface: Calculated from Simulation, using Voronoi Polyhedra J. Mol. Biol. 1995, 249 (5) 955-966
26. Alexander, M.; Gerauer, M.; Pechlivanis, M.; Popkirova, B.; Dvorsky, R.; Brunsveld, L.; Waldmann, H.; Kuhlmann, J. Mapping the Isoprenoid Binding Pocket of PDEδ by a Semisynthetic, Photoactivatable N-Ras Lipoprotein ChemBioChem 2009, 10 (1) 98-108
27. Chen, Y. X.; Koch, S.; Uhlenbrock, K.; Weise, K.; Das, D.; Gremer, L.; Brunsveld, L.; Wittinghofer, A.; Winter, R.; Triola, G. Synthesis of the Rheb and K-Ras4B GTPases Angew. Chem., Int. Ed. Engl. 2010, 49 (35) 6090-6095
28. Williams, D. H.; Stephens, E.; O'Brien, D. P.; Zhou, M. Understanding Noncovalent Interactions: Ligand Binding Energy and Catalytic Efficiency from Ligand-Induced Reductions in Motion within Receptors and Enzymes Angew. Chem., Int. Ed. Engl. 2004, 43 (48) 6596-6616
29. Barratt, E.; Bingham, R. J.; Warner, D. J.; Laughton, C. A.; Phillips, S. E. V; Homans, S. W. van der Waals Interactions Dominate Ligand-Protein Association in a Protein Binding Site Occluded from Solvent Water J. Am. Chem. Soc. 2005, 127 (33) 11827-11834
30. Dunitz, J. D. Win Some, Lose Some: Enthalpy-Entropy Compensation in Weak Intermolecular Interactions Chem. Biol. 1995, 2 (11) 709-712
31. Brokx, R. D.; Lopez, M. M.; Vogel, H. J.; Makhatadze, G. I. Energetics of Target Peptide Binding by Calmodulin Reveals Different Modes of Binding J. Biol. Chem. 2001, 276 (17) 14083-14091
32. Makhatadze, G. I. Heat Capacities of Amino Acids, Peptides and Proteins Biophys. Chem. 1998, 71 (2-3) 133-156
33. Pierce, M. M.; Raman, C. S.; Nall, B. T. Isothermal Titration Calorimetry of Protein-Protein Interactions Methods 1999, 19 (2) 213-221
34. Head-Gordon, T. Is Water Structure Around Hydrophobic Groups Clathrate-Like? Proc. Natl. Acad. Sci. U. S. A. 1995, 92 (18) 8308-8312
35. Munson, M.; Balasubramanian, S.; Fleming, K. G.; Nagi, A. D.; O'Brien, R.; Sturtevant, J. M.; Regan, L. What Makes a Protein a Protein? Hydrophobic Core Designs that Specify Stability and Structural Properties Protein Sci. 1996, 5 (8) 1584-1593
36. Celej, M. S.; Montich, G. G.; Fidelio, G. D. Protein Stability Induced by Ligand Binding Correlates with Changes in Protein Flexibility Protein Sci. 2003, 12 (7) 1496-1506
37. Jaenicke, R. Stability and Stabilization of Globular Proteins in Solution J. Biotechnol. 2000, 79 (3) 193-203
38. Chalikian, T. V.; Bresiauer, K. J. On Volume Changes Accompanying Conformational Transitions of Biopolymers Biopolymers 1996, 39 (5) 619-626
39. Ravindra, R.; Winter, R. Pressure Perturbation Calorimetry: A New Technique Provides Surprising Results on the Effects of Co-solvents on Protein Solvation and Unfolding Behavior ChemPhysChem 2004, 5 (4) 566-571
40. Schweiker, K. L.; Fitz, V. W.; Makhatadze, G. I. Universal Convergence of the Specific Volume Changes of Globular Proteins upon Unfolding Biochemistry 2009, 48 (46) 10846-10851
41. Mitra, L.; Smolin, N.; Ravindra, R.; Royer, C.; Winter, R. Pressure Perturbation Calorimetric Studies of the Solvation Properties and the Thermal Unfolding of Proteins in Solution-Experiments and Theoretical Interpretation Phys. Chem. Chem. Phys. 2006, 8 (11) 1249-1265
42. Gekko, K.; Noguchi, H. Compressibility of Globular Proteins in Water at 25 C J. Phys. Chem. 1979, 83 (21) 2706-2714
43. Gekko, K. Compressibility Gives New Insight into Protein Dynamics and Enzyme Function Biochim. Biophys. Acta 2002, 1595 (1-2) 382-386
44. Kharakoz, D. P.; Sarvazyan, A. P. Hydrational and Intrinsic Compressibilities of Globular Proteins Biopolymers 1993, 33 (1) 11-26
45. Son, I.; Shek, Y. L.; Dubins, D. N.; Chalikian, T. V. Volumetric Characterization of Tri- N -acetylglucosamine Binding to Lysozyme Biochemistry 2012, 51 (29) 5784-5790
46. Son, I.; Selvaratnam, R.; Dubins, D. N.; Melacini, G.; Chalikian, T. V. Ultrasonic and Densimetric Characterization of the Association of Cyclic AMP with the cAMP-Binding Domain of the Exchange Protein EPAC1 J. Phys. Chem. B 2013, 117, 10779-10784
47. Lee, B.; Richards, F. M. The Interpretation of Protein Structures: Estimation of Static Accessibility J. Mol. Biol. 1971, 55 (3) 379-400
48. Patel, N.; Dubins, D. N.; Pomes, R.; Chalikian, T. V. Size Dependence of Cavity Volume: A Molecular Dynamics Study Biophys. Chem. 2012, 161, 46-49
49. Kauzmann, W. Some Factors in the Interpretation of Protein Denaturation Adv. Protein Chem. 1959, 14, 1-63
50. Gerstein, M.; Chothia, C. Packing at the Protein-Water Interface Proc. Natl. Acad. Sci. U. S. A. 1996, 93 (19) 10167-10172
51. Chalikian, T. V. Structural Thermodynamics of Hydration J. Phys. Chem. B 2001, 105 (50) 12566-12578
52. Luque, I.; Freire, E. Structure-Based Prediction of Binding Affinities and Molecular Design of Peptide Ligands Methods Enzymol. 1998, 295, 100-127
53. Makhatadze, G. I.; Privalov, P. L. Energetics of Protein Structure Adv. Protein Chem. 1995, 47, 307-425
54. Dubins, D. N.; Filfil, R.; Macgregor, R. B.; Chalikian, T. V. Role of Water in Protein-Ligand Interactions: Volumetric Characterization of the Binding of 2′-CMP and 3′-CMP to Ribonuclease A J. Phys. Chem. B 2000, 104 (2) 390-401