Electrostatic effects of mutations of Ras glutamine 61 measured using vibrational spectroscopy of a thiocyanate probe

Biochemistry

Volumn 51, Issue 13, 2012, Pages 2757-2767

  Stafford, Amy J ^a   Walker, David M ^a   Webb, Lauren J ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION ENERGIES; ACTIVE SITE; DISSOCIATION CONSTANT; ELECTROSTATIC EFFECT; ELECTROSTATIC ENVIRONMENTS; GTP HYDROLYSIS; GUANINE NUCLEOTIDE DISSOCIATION; GUANOSINE TRIPHOSPHATE; INTRINSIC MECHANISMS; MALIGNANT CELLS; NON-POLAR; ONCOPROTEINS; POLAR COMPONENTS; SIDE-CHAINS; SOLVENT ACCESSIBLE SURFACE AREAS; SPECTROSCOPIC PROBES; TRANSITION STATE; WATER MOLECULE; WILD TYPES;

CYANIDES; DISSOCIATION; ELECTROSTATICS; HYDROLYSIS; PROBES; VIBRATIONAL SPECTROSCOPY;

AMINO ACIDS;

CYSTEINE; DOCKING PROTEIN; GLUTAMINE; GUANOSINE TRIPHOSPHATE; MUTANT PROTEIN; NITRILE; PROLINE; PROTEIN P21; RAL PROTEIN; SOLVENT; THIOCYANATE; WATER;

ARTICLE; CANCER CELL; CHEMICAL LABELING; CONTROLLED STUDY; DISSOCIATION CONSTANT; ENERGY ABSORPTION; HUMAN; HYDRATION; HYDROLYSIS; MOLECULAR PROBE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN INTERACTION; SPECTROSCOPY; STATIC ELECTRICITY; WILD TYPE;

GLUTAMINE; MOLECULAR DYNAMICS SIMULATION; MUTATION; RAS PROTEINS; SPECTRUM ANALYSIS; STATIC ELECTRICITY; THIOCYANATES;

EID: 84859377876     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201225p     Document Type: Article

References (62)

1. Krauss, G. (2003) Biochemistry of Signal Transduction and Regulation, 3rd ed., Wiley-VCH Verlag, Weinheim, Germany.
2. Cox, A. D. and Der, C. J. (2003) The dark side of Ras: Regulation of apoptosis Oncogene 22, 8999-9006
3. Downward, J. (2002) Targeting Ras Signalling Pathways in Cancer Therapy Nat. Cancer Rev. 3, 11-22
4. Repasky, G. A., Chenette, E. J., and Der, C. J. (2004) Renewing the conspiracy theory debate: Does Raf function alone to mediate Ras oncogenesis? Trends Cell Biol. 14, 639-647
5. Shields, J. M., Pruitt, K., McFall, A., Shaub, A., and Der, C. J. (2000) Understanding Ras: 'it aint over til its over' Trends Cell Biol. 10, 147-154
6. Harvey, J. J. (1964) An Unidentified Virus which Causes the Rapid Production of Tumours in Mice Nature 204, 1104-1105
7. Bos, J. L. (1989) ras Oncogenes in Human Cancer: A Review Cancer Res. 49, 4682-4689
8. Eisenberg, S. and Henis, Y. I. (2008) Interactions of Ras proteins with the plasma membrane and their roles in signaling Cell. Signalling 20, 31-39
9. Pacold, M. E., Suire, S., Perisic, O., Lara-Gonzalez, S., Davis, C. T., Walker, E. H., Hawkins, P. T., Stephens, L., Eccleston, J. F., and Williams, R. L. (2000) Crystal Structure and Functional Analysis of Ras Binding to Its Effector Phosphoinositide 3-Kinase γ Cell 103, 931-943
10. Scheffzek, K., Ahmadian, M. R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997) The Ras-RasGAP Complex: Structural Basis for GTPase Activation and Its Loss in Oncogenic Ras Mutants Science 277, 333-338
11. Schweins, T., Geyer, M., Scheffzek, K., Warshel, A., Kalbitzer, H. R., and Wittinghofer, A. (1995) Substrate-assisted catalysis as a mechanism for GTP hydrolysis of p21ras and other GTP-binding proteins Nat. Struct. Biol. 2, 36-44
12. Ford, B., Hornak, V., Kleinman, H., and Nassar, N. (2006) Structure of a Transient Intermediate for GTP Hydrolysis by Ras Structure 14, 427-436
13. Buhrman, G., Holzapfel, G., Fetics, S., and Mattos, C. (2010) Allosteric modulation of Ras positions Q61 for a direct role in catalysis Proc. Natl. Acad. Sci. U.S.A. 107, 4931-4936
14. Frech, M., Darden, T. A., Pedersen, L. G., Foley, C. K., Charifson, P. S., Anderson, M. W., and Wittinghofer, A. (1994) Role of Glutamine-61 in the Hydrolysis of GTP by p21H-Ras; An Experimental and Theoretical Study Biochemistry 33, 3237-3244
15. Shurki, A. and Warshel, A. (2004) Why Does the Ras Switch "Break" by Oncogenic Mutations? Proteins 55, 1-10
16. Vogel, U. S., Dixon, R. A. F., Schaber, M. D., Diehl, R. E., Marshall, M. S., Scolnick, E. M., Sigal, I. S., and Gibbs, J. B. (1988) Cloning of bovine GAP and its interaction with oncogenic ras p21 Nature 335, 90-93
17. Pai, E. F., Krengel, U., Petsko, G. A., Goody, R. S., Kabsch, W., and Wittinghofer, A. (1990) Refined crystal structure of the triphosphate conformation of H-ras p21 at 1.35 Å resolution: Implications for the mechanism of GTP hydrolysis EMBO J. 9, 2351-2359
18. Krengel, U., Schlichting, I., Scherer, A., Schumann, R., Frech, M., John, J., Kabsch, W., Pai, E. F., and Wittinghofer, A. (1990) Three-Dimensional Structures of H-ras p21 Mutants: Molecular Basis for Their Inability to Function as Signal Sitch Molecules Cell 62, 539-548
19. Buhrman, G., Wink, G., and Mattos, C. (2007) Transformation Efficiency of RasQ61 Mutants Linked to Structural Features of the Switch Regions in the Presence of Raf Structure 15, 1618-1629
20. Thielges, M. C., Case, D. A., and Romesberg, F. E. (2008) Carbon-Deuterium Bonds as Probes of Dihydrofolate Reductase J. Am. Chem. Soc. 130, 6597-6603
21. Ye, S., Zaitseva, E., Caltabiano, G., Schertler, G. F. X., Sakmar, T. P., Deupi, X., and Vogel, R. (2010) Tracking G-protein-coupled receptor activation using genetically encoded infrared probes Nature 464, 1386-1391
22. Suydam, I. T. and Boxer, S. G. (2003) Vibrational Stark Effects Calibrate the Sensitivity of Vibrational Probes for Electric Fields in Proteins Biochemistry 42, 12050-12055
23. Webb, L. J. and Boxer, S. G. (2008) Electrostatic Fields Near the Active Site of Human Aldose Reductase: 1. New Inhibitors and Vibrational Stark Effect Measurements Biochemistry 47, 1588-1598
24. Waegele, M. M., Culik, R. M., and Gai, F. (2011) Site-Specific Spectroscopic Reporters of the Local Electric Field, Hydration, Structure, and Dynamics of Biomolecules J. Phys. Chem. Lett. 2, 2598-2609
25. Gunner, M. R., Nicholls, A., and Honig, B. (1996) Electrostatic Potentials in Rhodopseudomonas viridis Reaction Centers: Implications for the Driving Force and Directionality of Electron Transfer J. Phys. Chem. 100, 4277-4291
26. Honig, B. and Nicholls, A. (1995) Classical Electrostatics in Biology and Chemistry Science 268, 1144-1149
27. Lee, L. P. and Tidor, B. (2001) Optimization of Binding Electrostatics: Charge Complementarity in the Barnase-Barstar Protein Complex Protein Sci. 10, 362-377
28. Simonson, T. (2001) Macromolecular electrostatics: Continuum models and their growing pains Curr. Opin. Struct. Biol. 11, 243-252
29. Villa, J. and Warshel, A. (2001) Energetics and Dynamics of Enzymatic Reactions J. Phys. Chem. B 105, 7887-7907
30. Warshel, A. and Papazyan, A. (1998) Electrostatic effects in macromolecules: Fundamental concepts and practical modeling Curr. Opin. Struct. Biol. 8, 211-217
31. Sigala, P. A., Fafarman, A. T., Bogard, P. E., Boxer, S. G., and Herschlag, D. (2007) Do Ligand Binding and Solvent Exclusion Alter the Electrostatic Character within the Oxyanion Hole of an Enzymatic Active Site J. Am. Chem. Soc. 129, 12104-12105
32. Fafarman, A. T., Sigala, P. A., Herschlag, D., and Boxer, S. G. (2010) Decomposition of Vibrational Shifts of Nitriles into Electrostatic and Hydrogen-Bonding Effects J. Am. Chem. Soc. 132, 12811-12813
33. Baran, K. L., Chimenti, M. S., Schlessman, J. L., Fitch, C. A., Herbst, K. J., and Garcia-Moreno, B. E. (2008) Electrostatic Effects in a Network of Polar and Ionizable Groups in Staphylococcal Nuclease J. Mol. Biol. 379, 1045-1062
34. Castaneda, C. A., Fitch, C. A., Majumdar, A., Khangulov, V., Schlessman, J. L., and Garcia-Moreno, B. E. (2009) Molecular determinants of the pHa values of Asp and Glu residues in staphylococcal nuclease Proteins 77, 570-588
35. 19F NMR To Probe Protein Structure and Conformational Changes Annu. Rev. Biophys. Biomol. Struct. 25, 163-195
36. Forsyth, W. R., Antosiewicz, J. M., and Robertson, A. D. (2002) Empirical Relationships Between Protein Structure and Carboxyl pKa Values in Proteins Proteins 48, 388-403
37. Harms, M. J., Castaneda, C. A., Schlessman, J. L., Sue, G. R., Isom, D. G., Cannon, B. R., and Garcia-Moreno, B. E. (2009) The pKa Values of Acidic and Basic Residues Buried at the Same Internal Location in a Protein Are Governed by Different Factors J. Mol. Biol. 389, 34-47
38. Matousek, W. M., Ciani, B., Fitch, C. A., Garcia-Moreno, B. E., Kammerer, R. A., and Alexandrescu, A. T. (2007) Electrostatic Contributions to the Stability of the GCN4 Leucine Zipper Structure J. Mol. Biol. 374, 206-219
39. Pearson, J. G., Oldfield, E., Lee, F. S., and Warshel, A. (1993) Chemical Shifts in Proteins: A Shielding Trajectory Analysis of the Fluorine Nuclear Magnetic Resonance Spectrum of the Escherichia coli Galactose Binding Protein Using a Multipole Shielding Polarizability-Local Reaction Field-Molecular Dynamics Approach J. Am. Chem. Soc. 115, 6851-6862
40. Schutz, C. N. and Warshel, A. (2001) What are Dielectric "Constants" of Proteins and How to Validate Electrostatic Models? Proteins 44, 400-417
41. Thurlkill, R. L., Grimsley, G. R., Scholtz, J. M., and Pace, C. N. (2006) Hydrogen Bonding Markedly Reduces the pKa of Buried Carboxyl Groups in Proteins J. Mol. Biol. 362, 594-604
42. Fafarman, A. T., Webb, L. J., Chuang, J. I., and Boxer, S. G. (2006) Site-Specific Conversion of Cysteine Thiols into Thiocyanate Creates an IR Probe for Electric Fields in Proteins J. Am. Chem. Soc. 128, 13356-13357
43. Stafford, A. J., Ensign, D. L., and Webb, L. J. (2010) Vibrational Stark Effect Spectroscopy at the Interface of Ras and Rap1A Bound to the Ras Binding Domain of RalGDS Reveals an Electrostatic Mechanism for Protein-Protein Interaction J. Phys. Chem. B 114, 15331-15344
44. Suydam, I. T., Snow, C. D., Pande, V. S., and Boxer, S. G. (2006) Electric Fields at the Active Site of an Enzyme: Direct Comparison of Experiment with Theory Science 313, 200-204
45. Ensign, D. L. and Webb, L. J. (2011) Factors Determining Electrostatic Fields at the Ras/Effector Interface Proteins 79, 3511-3524
46. Huang, L., Hofer, F., Martin, G. S., and Kim, S. H. (1998) Structural basis for the interaction of Ras with RalGDS Nat. Struct. Biol. 5, 422-426
47. Rudolph, M. G., Linnemann, T., Grunewald, P., Wittinghofer, A., Vetter, I. R., and Herrmann, C. (2001) Thermodynamics of Ras/Effector and Cdc42/Effector Interactions Probed by Isothermal Titration Calorimetry J. Biol. Chem. 276, 23914-23921
48. Kapust, R. B., Tozser, J., Fox, J. D., Anderson, D. E., Cherry, S., Copeland, T. D., and Waugh, D. S. (2001) Tobacco etch virus protease: Mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency Protein Eng. 14, 993-1000
49. Boriack-Sjodin, P. A., Margarit, S. M., Bar-Sagi, D., and Kuriyan, J. (1998) The structural basis of the activation of Ras by Sos Nature 394, 337-343
50. Herrmann, C., Horn, G., Spaargaren, M., and Wittinghofer, A. (1996) Differential Interactions of the Ras Family of GTP-binding Proteins H-Ras, Rap1A, and R-Ras with the Putative Effector Molecules Raf Kinase and Ral-Guanine Nucleotide Exchange Factor J. Biol. Chem. 271, 6794-6800
51. Choi, J. H., Oh, K. I., Lee, H., Lee, C., and Cho, M. (2008) Nitrile and thiocyanate IR probes: Quantum chemistry calculation studies and multivariate least-square fitting analysis J. Chem. Phys. 128, 134506
52. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T., Caldwell, J. W., Wang, J., and Kollman, P. A. (2003) A Point-Charge Force Field for Molecular Mechanics Simulations of Proteins Based on Condensed-Phase Quantum Mechanical Calculations J. Comput. Chem. 24, 1999-2012
53. van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. C. (2005) GROMACS: Fast, Flexible, and Free J. Comput. Chem. 26, 1701-1718
54. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
55. Gallicchio, E., Andrec, M., Felts, A. K., and Levy, R. M. (2005) Temperature Weighted Histogram Analysis Method, Replica Exchange, and Transition Paths J. Phys. Chem. B 109, 6722-6731
56. Roux, B. (1995) The calculation of the potential of mean force using computer simulations Comput. Phys. Commun. 91, 275-282
57. Wimley, W. C., Creamer, T. P., and White, S. H. (1996) Solvation Energies of Amino Acid Side Chains and Backbone in a Family of Host-Guest Pentapeptides Biochemistry 35, 5109-5124
58. Wolfenden, R., Andersson, L., Cullis, P. M., and Southgate, C. C. B. (1981) Affinities of Amino Acid Side Chains for Solvent Water Biochemistry 20, 849-855
59. John, J., Frech, M., and Wittinghofer, A. (1988) Biochemical Properties of Ha-ras Encoded p21 Mutants and Mechanis of the Autophosphorylation Reaction J. Biol. Chem. 263, 11792-11799
60. Leupold, C. M., Goody, R. S., and Wittinghofer, A. (1983) Stereochemistry of the elongation factor Tu-GTP complex Eur. J. Biochem. 135, 237-241
61. Reinstein, J., Schlichting, I., Frech, M., Goody, R. S., and Wittinghofer, A. (1991) p21 with a Phenylalanine 28 to Leucine Mutation Reacts Normally with the GTPase Activating Protein GAP but Nevertheless Has Transforming Properties J. Biol. Chem. 266, 17700-17706
62. Der, C. J., Finkel, T., and Cooper, G. M. (1986) Biological and Biochemical Properties of Human rasH Genes Mutated at Codon 61 Cell 44, 167-176