Rapid and accurate ranking of binding affinities of epidermal growth factor receptor sequences with selected lung cancer drugs

Journal of the Royal Society Interface

Volumn 8, Issue 61, 2011, Pages 1114-1127

  Wan, Shunzhou ^a   Coveney, Peter V ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Binding free energy; Epidermal growth factor receptor; Molecular dynamics simulation; Molecular mechanics Poisson Boltzmann solvent area method

Indexed keywords

ATP-BINDING; BINDING AFFINITIES; BINDING FREE ENERGY; DRUG BINDING; DRUG SENSITIVITY; ENSEMBLE SIMULATION; EPIDERMAL GROWTH FACTOR RECEPTORS; GEFITINIB; HUMAN CANCER; KINASE DOMAINS; LUNG CANCER; LUNG CARCINOMA; MOLECULAR DYNAMICS SIMULATION; MOLECULAR DYNAMICS SIMULATIONS; PETA-SCALE COMPUTING; RELATIVE STRENGTH; TYROSINE KINASE; TYROSINE KINASE INHIBITOR;

AMINO ACIDS; BIOLOGICAL ORGANS; DISEASES; ENZYMES; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PEPTIDES;

BINDING ENERGY;

6 [4 (4 ETHYL 1 PIPERAZINYLMETHYL)PHENYL] 4 (ALPHA METHYLBENZYLAMINO) 7H PYRROLO[2,3 D]PYRIMIDINE; ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB;

ACCURACY; ARTICLE; BINDING AFFINITY; DRUG BINDING; DRUG SENSITIVITY; DRUG STRUCTURE; LUNG CANCER; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; SIMULATION;

COMPUTER SIMULATION; HUMANS; LUNG NEOPLASMS; MODELS, MOLECULAR; MUTATION; NEOPLASM PROTEINS; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; PURINES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 79960092299     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2010.0609     Document Type: Article

References (47)

1. Parkin, D. M., Bray, F., Ferlay, J. & Pisani, P. 2005 Global cancer statistics, 2002. Ca Cancer J. Clin. 55, 74-108. (doi:10.3322/canjclin.55.2.74)
2. Skarin, A. T. 2000 Multimodality treatment of lung cancer. New York, NY: Marcel Dekker.
3. Sawyers, C. 2004 Targeted cancer therapy. Nature 432, 294-297. (doi:10.1038/nature03095)
4. Sharma, S. V., Bell, D. W., Settleman, J. & Haber, D. A. 2007 Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 7, 169-181. (doi:10.1038/nrc2088)
5. Zhang, X. W., Gureasko, J., Shen, K., Cole, P. A. & Kuriyan, J. 2006 An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149. (doi:10.1016/j.cell.2006.05.013)
6. Imai, K. & Takaoka, A. 2006 Comparing antibody and small-molecule therapies for cancer. Nat. Rev. Cancer 6, 714-727. (doi:10.1038/nrc1913)
7. Zhang, J. M., Yang, P. L. & Gray, N. S. 2009 Targeting cancer with small molecule kinase inhibitors. Nat. Rev. Cancer 9, 28-39. (doi:10.1038/nrc2559)
8. Traxler, P. et al. 2004 AEE788: a dual family epidermal growth factor receptor/ErbB2 and vascular endothelial growth factor receptor tyrosine kinase inhibitor with antitumor and antiangiogenic activity. Cancer Res. 64, 4931-4941. (doi:10.1158/0008-5472.CAN-03-3681)
9. Byers, L. A. & Heymach, J. V. 2007 Dual targeting of the vascular endothelial growth factor and epidermal growth factor receptor pathways: rationale and clinical applications for non-small-cell lung cancer. Clin. Lung Cancer 8, S79-S85. (doi:10.3816/CLC.2007.s.006)
10. Yun, C. H., Mengwasser, K. E., Toms, A. V., Woo, M. S., Greulich, H., Wong, K. K., Meyerson, M. & Eck, M. J. 2008 The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc. Natl Acad. Sci. USA 105, 2070-2075. (doi:10.1073/pnas.0709662105)
11. Sloot, P. M., Coveney, P. V., Ertaylan, G., Muller, V., Boucher, C. A. & Bubak, M. 2009 HIV decision support: from molecule to man. Phil. Trans. R. Soc. A 367, 2691-2703. (doi:10.1098/rsta.2009.0043)
12. Coveney, P. V. & Fowler, P. W. 2005 Modelling biological complexity: a physical scientist's perspective. J. R. Soc. Interface 2, 267-280. (doi:10.1098/rsif.2005.0045)
13. Sadiq, S. K., Wright, D., Watson, S. J., Zasada, S. J., Stoica, I. & Coveney, P. V. 2008 Automated molecular simulation based binding affinity calculator for ligand-bound HIV-1 proteases. J. Chem. Info. Model. 48, 1909-1919. (doi:10.1021/ci8000937)
14. Saksena, R. S. et al. 2009 Real science at the petascale. Phil. Trans. R. Soc. A 367, 2557-2571. (doi:10.1098/rsta.2009.0049)
15. Zasada, S. J. & Coveney, P. V. 2009 Virtualizing access to scientific applications with the application hosting environment. Comput. Phys. Commun. 180, 2513-2525. (doi:10.1016/j.cpc.2009.06.008)
16. Balius, T. E. & Rizzo, R. C. 2009 Quantitative prediction of fold resistance for inhibitors of EGFR. Biochemistry 48, 8435-8448. (doi:10.1021/bi900729a)
17. Dixit, A., Torkamani, A., Schork, N. J. & Verkhivker, G. 2009 Computational modeling of structurally conserved cancer mutations in the RET and MET kinases: the impact on protein structure, dynamics, and stability. Biophys. J. 96, 858-874. (doi:10.1016/j.bpj.2008.10.041)
18. Hatti, K. S., Chandregowda, V., Rao, G. V., Kush, A. & Reddy, G. C. 2009 In-silico interaction studies of quinazoline derivatives for their inhibitory action on both wild and mutant EGFRs. J. Proteomics Bioinform. 2, 126-130. (doi:10.4172/jpb.1000069)
19. Hou, T. J., Zhu, L. L., Chen, L. R. & Xu, X. J. 2003 Mapping the binding site of a large set of quinazoline type EGF-R inhibitors using molecular field analyses and molecular docking studies. J. Chem. Info. Comput. Sci. 43, 273-287. (doi:10.1021/ci025552a)
20. Verkhivker, G. M. 2007 Exploring sequence-structure relationships in the tyrosine kinome space: functional classification of the binding specificity mechanisms for cancer therapeutics. Bioinformatics 23, 1919-1926. (doi:10.1093/bioinformatics/btm277)
21. Srinivasan, J., Cheatham, T. E., Cieplak, P., Kollman, P. A. & Case, D. A. 1998 Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate - DNA helices. J. Am. Chem. Soc. 120, 9401-9409. (doi:10.1021/ja981844+)
22. Perez, D., Uberuaga, B. P., Shim, Y., Amar, J. G. & Voter, A. F. 2009 Accelerated molecular dynamics methods: introduction and recent developments. Annu. Rep. Comput. Chem. 5, 79-98. (doi:10.1016/S1574-1400(09)00504-0)
23. Caves, L. S. D., Evanseck, J. D. & Karplus, M. 1998 Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin. Protein Sci. 7, 649-666. (Pubitemid 28130887)
24. Sadiq, S. K. et al. 2008 Patient-specific simulation as a basis for clinical decision-making. Phil. Trans. R. Soc. A 366, 3199-3219. (doi:10.1098/rsta.2008.0100)
25. Sadiq, S. K., Wright, D. W., Kenway, O. A. & Coveney, P. V. 2010 Accurate ensemble molecular dynamics binding free energy ranking of multidrug-resistant HIV-1 proteases. J. Chem. Info. Model. 50, 890-905. (doi:10.1021/ci100007w)
26. Stoica, I., Sadiq, S. K. & Coveney, P. V. 2008 Rapid and accurate prediction of binding free energies for saquinavir-bound HIV-1 proteases. J. Am. Chem. Soc. 130, 2639-2648. (doi:10.1021/ja0779250)
27. Wan, S. Z., Coveney, P. V. & Flower, D. R. 2005 Peptide recognition by the T cell receptor: comparison of binding free energies from thermodynamic integration, Poisson-Boltzmann and linear interaction energy approximations. Phil. Trans. R. Soc. A 363, 2037-2053. (doi:10.1098/rsta.2005.1627)
28. Yun, C. H., Boggon, T. J., Li, Y. Q., Woo, M. S., Greulich, H., Meyerson, M. & Eck, M. J. 2007 Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 11, 217-227. (doi:10.1016/j.ccr.2006.12.017)
29. Frisch, M. J. et al. 2004 Gaussian 03, Revision B.03. USA: Gaussian, Inc.
30. Case, D. A. et al. 2005 The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688. (doi:10.1002/jcc.20290)
31. Shan, Y. B., Seeliger, M. A., Eastwood, M. P., Frank, F., Xu, H. F., Jensen, M. O., Dror, R. O., Kuriyan, J. & Shaw, D. E. 2009 A conserved protonation-dependent switch controls drug binding in the Abl kinase. Proc. Natl Acad. Sci. USA 106, 139-144. (doi:10.1073/pnas.0811223106)
32. Liu, B., Bernard, B. & Wu, J. H. 2006 Impact of EGFR point mutations on the sensitivity to gefitinib: insights from comparative structural analyses and molecular dynamics simulations. Proteins Struct. Funct. Bioinformatics 65, 331-346. (doi:10.1002/prot.21111)
33. Wang, J. M., Wolf, R. M., Caldwell, J. W., Kollman, P. A. & Case, D. A. 2004 Development and testing of a general amber force field. J. Comput. Chem. 25, 1157-1174. (doi:10.1002/jcc.20035)
34. Duan, Y. et al. 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. (doi:10.1002/jcc.10349)
35. Phillips, J. C. et al. 2005 Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802. (doi:10.1002/jcc.20289)
36. van Gunsteren, W. F. & Mark, A. E. 1998 Validation of molecular dynamics simulation. J. Chem. Phys. 108, 6109-6116. (doi:10.1063/1.476021)
37. Humphrey, W., Dalke, A. & Schulten, K. 1996 VMD: Visual molecular dynamics. J. Mol. Graph. 14, 33-38. (doi:10.1016/0263-7855(96)00018-5)
38. Andrec, M., Snyder, D. A., Zhou, Z. Y., Young, J., Montellone, G. T. & Levy, R. M. 2007 A large data set comparison of protein structures determined by crystallography and NMR: statistical test for structural differences and the effect of crystal packing. Proteins Struct. Funct. Bioinformatics 69, 449-465. (doi:10.1002/prot.21507)
39. Fabian, M. A. et al. 2005 A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23, 329-336. (doi:10.1038/nbt1068)
40. Rastelli, G., Rio, A. D., Degliesposti, G. & Sgobba, M. 2009 Fast and accurate predictions of binding free energies using MM-PBSA and MM-GBSA. J. Comput. Chem. 31, 797-810.
41. Kancha, R. K., von Bubnoff, N., Peschel, C. & Duyster, J. 2009 Functional analysis of epidermal growth factor receptor (EGFR) mutations and potential implications for EGFR targeted therapy. Clin. Cancer Res. 15, 460-467. (doi:10.1158/1078-0432.CCR-08-1757)
42. Azam, M., Seeliger, M. A., Gray, N. S., Kuriyan, J. & Daley, G. Q. 2008 Activation of tyrosine kinases by mutation of the gatekeeper threonine. Nat. Struct. Mol. Biol. 15, 1109-1118. (doi:10.1038/nsmb.1486)
43. Eck, M. J. & Yun, C. H. 2010 Structural and mechanistic underpinnings of the differential drug sensitivity of EGFR mutations in non-small cell lung cancer. Biochim. Biophys. Acta 1804, 559-566. (doi:10.1016/j.bbapap.2009.12.010)
44. Dixit, A. & Verkhivker, G. M. 2009 Hierarchical modeling of activation mechanisms in the ABL and EGFR kinase domains: thermodynamic and mechanistic catalysts of kinase activation by cancer mutations. PLoS Comput. Biol. 5, e1000487. (doi:10.1371/journal.pcbi.1000487)
45. La Motta, C., Sartini, S., Tuccinardi, T., Nerini, E., Da Settimo, F. & Martinelli, A. 2009 Computational studies of epidermal growth factor receptor: docking reliability, three-dimensional quantitative structure-activity relationship analysis, and virtual screening studies. J. Med. Chem. 52, 964-975. (doi:10.1021/jm800829v)
46. Shawver, L. K., Slamon, D. & Ullrich, A. 2002 Smart drugs: tyrosine kinase inhibitors in cancer therapy. Cancer Cell 1, 117-123. (doi:10.1016/S1535-6108(02)00039-9)
47. Juul, N. et al. 2010 Assessment of an RNA interference screen-derived mitotic and ceramide pathway metagene as a predictor of response to neoadjuvant paclitaxel for primary triple-negative breast cancer: a retrospective analysis of five clinical trials. Lancet Oncol. 11, 358-365. (doi:10.1016/S1470-2045(10) 70018-8)