Predicting the impact of missense mutations on protein-protein binding affinity

Journal of Chemical Theory and Computation

Volumn 10, Issue 4, 2014, Pages 1770-1780

  Li, Minghui ^a   Petukh, Marharyta ^b   Alexov, Emil ^b   Panchenko, Anna R ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b CLEMSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84898455342     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct401022c     Document Type: Article

References (65)

1. Nooren, I. M. A.; Thornton, J. M. Structural Characterisation and Functional Significance of Transient Protein-Protein Interactions J. Mol. Biol. 2003, 325, 991-1018
2. Hashimoto, K.; Panchenko, A. R. Mechanisms of protein oligomerization, the critical role of insertions and deletions in maintaining different oligomeric states Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 20352-20357
3. Dahiyat, B. I.; Benjamin Gordon, D.; Mayo, S. L. Automated design of the surface positions of protein helices Protein Sci. 1997, 6, 1333-1337
4. Shifman, J. M.; Mayo, S. L. Exploring the origins of binding specificity through the computational redesign of calmodulin Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 13274-13279
5. Chen, T. S.; Keating, A. E. Designing specific protein-protein interactions using computation, experimental library screening, or integrated methods Protein Sci. 2012, 21, 949-963
6. Yin, H.; Slusky, J. S.; Berger, B. W.; Walters, R. S.; Vilaire, G.; Litvinov, R. I.; Lear, J. D.; Caputo, G. A.; Bennett, J. S.; DeGrado, W. F. Computational Design of Peptides That Target Transmembrane Helices Science 2007, 315, 1817-1822
7. Joachimiak, L. A.; Kortemme, T.; Stoddard, B. L.; Baker, D. Computational Design of a New Hydrogen Bond Network and at Least a 300-fold Specificity Switch at a Protein-Protein Interface J. Mol. Biol. 2006, 361, 195-208
8. Teng, S.; Madej, T.; Panchenko, A.; Alexov, E. Modeling Effects of Human Single Nucleotide Polymorphisms on Protein-Protein Interactions Biophys. J. 2009, 96, 2178-2188
9. Yates, C. M.; Sternberg, M. J. E. The Effects of Non-Synonymous Single Nucleotide Polymorphisms (nsSNPs) on Protein-Protein Interactions J. Mol. Biol. 2013, 425, 3949-3963
10. Nishi, H.; Tyagi, M.; Teng, S.; Shoemaker, B. A.; Hashimoto, K.; Alexov, E.; Wuchty, S.; Panchenko, A. R. Cancer Missense Mutations Alter Binding Properties of Proteins and Their Interaction Networks PLoS One 2013, 8, e66273
11. Wei, Q.; Wang, L.; Wang, Q.; Kruger, W. D.; Dunbrack, R. L. Testing computational prediction of missense mutation phenotypes: Functional characterization of 204 mutations of human cystathionine beta synthase Proteins: Struct., Funct., Bioinf. 2010, 78, 2058-2074
12. Chothia, C.; Janin, J. Principles of protein-protein recognition Nature 1975, 256, 705-708
13. Kastritis, P. L.; Bonvin, A. M. J. J. Molecular origins of binding affinity: seeking the Archimedean point Curr. Opin. Struct. Biol. 2013, 23, 868-877
14. Marsh, J. A.; Teichmann, S. A. Relative Solvent Accessible Surface Area Predicts Protein Conformational Changes upon Binding Structure 2011, 19, 859-867
15. Moal, I. H.; Agius, R.; Bates, P. A. Protein-protein binding affinity prediction on a diverse set of structures Bioinformatics 2011, 27, 3002-9
16. Kastritis, P. L.; Bonvin, A. M. J. J. Are Scoring Functions in Protein-Protein Docking Ready To Predict Interactomes? Clues from a Novel Binding Affinity Benchmark J. Proteome Res. 2010, 9, 2216-2225
17. Sharabi, O.; Dekel, A.; Shifman, J. M. Triathlon for energy functions: Who is the winner for design of protein-protein interactions? Proteins: Struct., Funct., Bioinf. 2011, 79, 1487-1498
18. Papoian, G. A.; Wolynes, P. G. The physics and bioinformatics of binding and folding - an energy landscape perspective Biopolymers 2003, 68, 333-349
19. Guerois, R.; Nielsen, J. E.; Serrano, L. Predicting Changes in the Stability of Proteins and Protein Complexes: A Study of More Than 1000 Mutations J. Mol. Biol. 2002, 320, 369-387
20. Schymkowitz, J. W. H.; Rousseau, F.; Martins, I. C.; Ferkinghoff-Borg, J.; Stricher, F.; Serrano, L. Prediction of water and metal binding sites and their affinities by using the Fold-X force field Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 10147-10152
21. Dehouck, Y.; Kwasigroch, J. M.; Rooman, M.; Gilis, D. BeAtMuSiC: prediction of changes in protein-protein binding affinity on mutations Nucleic Acids Res. 2013, 41, W333-W339
22. Benedix, A.; Becker, C. M.; de Groot, B. L.; Caflisch, A.; Bockmann, R. A. Predicting free energy changes using structural ensembles Nat. Methods 2009, 6, 3-4
23. Kuhn, B.; Gerber, P.; Schulz-Gasch, T.; Stahl, M. Validation and Use of the MM-PBSA Approach for Drug Discovery J. Med. Chem. 2005, 48, 4040-4048
24. Rastelli, G.; Rio, A. D.; Degliesposti, G.; Sgobba, M. Fast and accurate predictions of binding free energies using MM-PBSA and MM-GBSA J. Comput. Chem. 2010, 31, 797-810
25. Okimoto, N.; Futatsugi, N.; Fuji, H.; Suenaga, A.; Morimoto, G.; Yanai, R.; Ohno, Y.; Narumi, T.; Taiji, M. High-Performance Drug Discovery: Computational Screening by Combining Docking and Molecular Dynamics Simulations PLoS Comput. Biol. 2009, 5, e1000528
26. Zhang, Z.; Wang, L.; Gao, Y.; Zhang, J.; Zhenirovskyy, M.; Alexov, E. Predicting folding free energy changes upon single point mutations Bioinformatics 2012, 28, 664-671
27. Spassov, V. Z.; Yan, L. pH-selective mutagenesis of protein-protein interfaces: In silico design of therapeutic antibodies with prolonged half-life Proteins: Struct., Funct., Bioinf. 2013, 81, 704-714
28. Weinkam, P.; Chen, Y. C.; Pons, J.; Sali, A. Impact of Mutations on the Allosteric Conformational Equilibrium J. Mol. Biol. 2013, 425, 647-661
29. Massova, I.; Kollman, P. A. Computational Alanine Scanning To Probe Protein-Protein Interactions: A Novel Approach To Evaluate Binding Free Energies J. Am. Chem. Soc. 1999, 121, 8133-8143
30. Huo, S.; Massova, I.; Kollman, P. A. Computational alanine scanning of the 1:1 human growth hormone-receptor complex J. Comput. Chem. 2002, 23, 15-27
31. Moreira, I. S.; Fernandes, P. A.; Ramos, M. J. Unraveling the Importance of Protein-Protein Interaction: Application of a Computational Alanine-Scanning Mutagenesis to the Study of the IgG1 Streptococcal Protein G (C2 Fragment) Complex J. Phys. Chem. B 2006, 110, 10962-10969
32. Gohlke, H.; Kiel, C.; Case, D. A. 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
33. Zhang, Z.; Teng, S.; Wang, L.; Schwartz, C. E.; Alexov, E. Computational analysis of missense mutations causing Snyder-Robinson syndrome Hum. Mutat. 2010, 31, 1043-1049
34. Moal, I. H.; Fernández-Recio, J. SKEMPI: a Structural Kinetic and Energetic database of Mutant Protein Interactions and its use in empirical models Bioinformatics 2012, 28, 2600-2607
35. Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics J. Mol. Graph. 1996, 14 (33-8) 27-8
36. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable molecular dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-802
37. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28, 235-242
38. Foloppe, N.; MacKerell, A. D. All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data J. Comput. Chem. 2000, 21, 86-104
39. Tanner, D. E.; Chan, K.-Y.; Phillips, J. C.; Schulten, K. Parallel Generalized Born Implicit Solvent Calculations with NAMD J. Chem. Theory Comput. 2011, 7, 3635-3642
40. Lee, M. S.; Olson, M. A. Calculation of Absolute Protein-Ligand Binding Affinity Using Path and Endpoint Approaches Biophys. J. 2006, 90, 864-877
41. Bradshaw, R. T.; Patel, B. H.; Tate, E. W.; Leatherbarrow, R. J.; Gould, I. R. Comparing experimental and computational alanine scanning techniques for probing a prototypical protein-protein interaction Protein Eng. Des. Sel. 2011, 24, 197-207
42. Li, M.; Zheng, W. Probing the Structural and Energetic Basis of Kinesin-Microtubule Binding Using Computational Alanine-Scanning Mutagenesis Biochemistry (Moscow) 2011, 50, 8645-8655
43. MacKerell, A. D.; Bashford, D.; Bellott, M.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T. K.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, W. E.; Roux, B.; Schlenkrich, M.; Smith, J. C.; Stote, R.; Straub, J.; Watanabe, M.; Wiorkiewicz-Kuczera, J.; Yin, D.; Karplus, M. All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 1998, 102, 3586-3616
44. Deserno, M.; Holm, C. How to mesh up Ewald sums. I. A theoretical and numerical comparison of various particle mesh routines J. Chem. Phys. 1998, 109, 7678-7693
45. Hoover, W. G. Canonical dynamics: Equilibrium phase-space distributions Phys. Rev. A 1985, 31, 1695-1697
46. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Cieplak, P.; Srinivasan, J.; Case, D. A.; Cheatham, T. E. Calculating Structures and Free Energies of Complex Molecules: Combining Molecular Mechanics and Continuum Models Acc. Chem. Res. 2000, 33, 889-897
47. Russell, S. T.; Warshel, A. Calculations of electrostatic energies in proteins: The energetics of ionized groups in bovine pancreatic trypsin inhibitor J. Mol. Biol. 1985, 185, 389-404
48. Im, W.; Beglov, D.; Roux, B. Continuum Solvation Model: computation of electrostatic forces from numerical solutions to the Poisson-Boltzmann equation Comput. Phys. Commun. 1998, 111, 59-75
49. Jo, S.; Vargyas, M.; Vasko-Szedlar, J.; Roux, B.; Im, W. PBEQ-Solver for online visualization of electrostatic potential of biomolecules Nucleic Acids Res. 2008, 36, W270-W275
50. Connolly, M. Analytical molecular surface calculation J. Appl. Crystallogr. 1983, 16, 548-558
51. Olson, M. A.; Reinke, L. T. Modeling implicit reorganization in continuum descriptions of protein-protein interactions Proteins 2000, 38, 115-9
52. Gilson, M. K.; Honig, B. H. The dielectric constant of a folded protein Biopolymers 1986, 25, 2097-119
53. Sharp, K. A.; Honig, B. Electrostatic interactions in macromolecules: theory and applications Annu. Rev. Biophys. Biophys. Chem. 1990, 19, 301-32
54. Sharp, K. A.; Honig, B. Calculating Total Electrostatic Energies with the Nonlinear Poisson-Boltzmann Equation J. Phys. Chem. 1990, 94, 7684-7692
55. Roux, B. Influence of the membrane potential on the free energy of an intrinsic protein Biophys. J. 1997, 73, 2980-9
56. Nina, M.; Beglov, D.; Roux, B. Atomic radii for continuum electrostatics calculations based on molecular dynamics free energy simulations J. Phys. Chem. B 1997, 101, 5239-5248
57. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. Charmm-a Program for Macromolecular Energy, Minimization, and Dynamics Calculations J. Comput. Chem. 1983, 4, 187-217
58. Dehouck, Y.; Gilis, D.; Rooman, M. A New Generation of Statistical Potentials for Proteins Biophys. J. 2006, 90, 4010-4017
59. Hashimoto, K.; Rogozin, I. B.; Panchenko, A. R. Oncogenic potential is related to activating effect of cancer single and double somatic mutations in receptor tyrosine kinases Hum. Mutat. 2012, 33, 1566-1575
60. Li, M.; Shoemaker, B. A.; Thangudu, R. R.; Ferraris, J. D.; Burg, M. B.; Panchenko, A. R. Mutations in DNA-Binding Loop of NFAT5 Transcription Factor Produce Unique Outcomes on Protein-DNA Binding and Dynamics J. Phys. Chem. B 2013, 117, 13226-13234
61. Levy, E. D. A Simple Definition of Structural Regions in Proteins and Its Use in Analyzing Interface Evolution J. Mol. Biol. 2010, 403, 660-670
62. Weis, A.; Katebzadeh, K.; Söderhjelm, P.; Nilsson, I.; Ryde, U. Ligand Affinities Predicted with the MM/PBSA Method: Dependence on the Simulation Method and the Force Field J. Med. Chem. 2006, 49, 6596-6606
63. Reichmann, D.; Rahat, O.; Albeck, S.; Meged, R.; Dym, O.; Schreiber, G. The modular architecture of protein-protein binding interfaces Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 57-62
64. Chopra, G.; Summa, C. M.; Levitt, M. Solvent dramatically affects protein structure refinement Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 20239-20244
65. Kellogg, E. H.; Leaver-Fay, A.; Baker, D. Role of conformational sampling in computing mutation-induced changes in protein structure and stability Proteins: Struct., Funct., Bioinf. 2011, 79, 830-838