Molecular dynamics of the asymmetric dimers of EGFR: Simulations on the active and inactive conformations of the kinase domain

Journal of Molecular Graphics and Modelling

Volumn 58, Issue , 2015, Pages 16-29

  Songtawee, Napat ^a   Bevan, David R ^b   Choowongkomon, Kiattawee ^a  

^a KASETSART UNIVERSITY   (Thailand)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Asymmetric dimers; EGFR; Essential dynamics; Intermolecular interactions; Kinase domain; Molecular dynamics

Indexed keywords

CHEMICAL ACTIVATION; CONFORMATIONS; DISEASES; ENZYMES; MOLECULAR DYNAMICS; PROTEINS;

ASYMMETRIC DIMERS; EGFR; ESSENTIAL DYNAMICS; INTERMOLECULAR INTERACTIONS; KINASE DOMAINS;

DIMERS;

DIMER; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE; EGFR PROTEIN, HUMAN;

ALLOSTERISM; ALPHA HELIX; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DIMERIZATION; HUMAN; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84925332963     PISSN: 10933263     EISSN: 18734243     Source Type: Journal    
DOI: 10.1016/j.jmgm.2015.03.002     Document Type: Article

References (59)

1. F.R. Hirsch, M. Varella-Garcia, P.A. Bunn Jr., M.V. Di Maria, R. Veve, R.M. Bremmes, et al. Epidermal growth factor receptor in non-small-cell lung carcinomas: correlation between gene copy number and protein expression and impact on prognosis J. Clin. Oncol. 21 2003 3798 3807
2. M.A. Lemmon, and J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 141 2010 1117 1134
3. N.E. Hynes, and H.A. Lane ERBB receptors and cancer: the complexity of targeted inhibitors Nat. Rev. Cancer 5 2005 341 354
4. K.M. Ferguson Structure-based view of epidermal growth factor receptor regulation Annu. Rev. Biophys. 37 2008 353 373
5. G.M. Walton, W.S. Chen, M.G. Rosenfeld, and G.N. Gill Analysis of deletions of the carboxyl terminus of the epidermal growth factor receptor reveals self-phosphorylation at tyrosine 992 and enhanced in vivo tyrosine phosphorylation of cell substrates J. Biol. Chem. 265 1990 1750 1754
6. Y. Yarden, and M.X. Sliwkowski Untangling the ErbB signalling network Nat. Rev. Mol. Cell Biol. 2 2001 127 137
7. J. Stamos, M.X. Sliwkowski, and C. Eigenbrot Structure of the epidermal growth factor receptor kinase domain alone and in complex with a 4-anilinoquinazoline inhibitor J. Biol. Chem. 277 2002 46265 46272
8. E.R. Wood, A.T. Truesdale, O.B. McDonald, D. Yuan, A. Hassell, S.H. Dickerson, et al. A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib): relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells Cancer Res. 64 2004 6652 6659
9. X. Zhang, J. Gureasko, K. Shen, P.A. Cole, and J. Kuriyan An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor Cell 125 2006 1137 1149
10. X. Zhang, K.A. Pickin, R. Bose, N. Jura, P.A. Cole, and J. Kuriyan Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface Nature 450 2007 741 744
11. N. Jura, N.F. Endres, K. Engel, S. Deindl, R. Das, M.H. Lamers, et al. Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment Cell 137 2009 1293 1307
12. M. Red Brewer, S.H. Choi, D. Alvarado, K. Moravcevic, A. Pozzi, M.A. Lemmon, et al. The juxtamembrane region of the EGF receptor functions as an activation domain Mol. Cell 34 2009 641 651
13. E.R. Wood, L.M. Shewchuk, B. Ellis, P. Brignola, R.L. Brashear, T.R. Caferro, et al. 6-Ethynylthieno[3,2-d]- and 6-ethynylthieno[2,3-d]pyrimidin-4-anilines as tunable covalent modifiers of ErbB kinases Proc. Natl. Acad. Sci. U. S. A. 105 2008 2773 2778
14. N. Jura, X. Zhang, N.F. Endres, M.A. Seeliger, T. Schindler, and J. Kuriyan Catalytic control in the EGF receptor and its connection to general kinase regulatory mechanisms Mol. Cell 42 2011 9 22
15. B. Liu, B. Bernard, and J.H. Wu Impact of EGFR point mutations on the sensitivity to gefitinib: insights from comparative structural analyses and molecular dynamics simulations Proteins 65 2006 331 346
16. T.E. Balius, and R.C. Rizzo Quantitative prediction of fold resistance for inhibitors of EGFR Biochemistry. 48 2009 8435 8448
17. A. Dixit, and G.M. Verkhivker 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 2009 e1000487
18. S. Wan, and P.V. Coveney Rapid and accurate ranking of binding affinities of epidermal growth factor receptor sequences with selected lung cancer drugs J. R. Soc. Interface. 8 2011 1114 1127
19. O. Sawatdichaikul, S. Hannongbua, C. Sangma, P. Wolschann, and K. Choowongkomon In silico screening of epidermal growth factor receptor (EGFR) in the tyrosine kinase domain through a medicinal plant compound database J. Mol. Model. 18 2012 1241 1254
20. A. Papakyriakou, D. Vourloumis, F. Tzortzatou-Stathopoulou, and M. Karpusas Conformational dynamics of the EGFR kinase domain reveals structural features involved in activation Proteins 76 2009 375 386
21. S.E. Telesco, and R. Radhakrishnan Atomistic insights into regulatory mechanisms of the HER2 tyrosine kinase domain: a molecular dynamics study Biophys. J. 96 2009 2321 2334
22. M. Mustafa, A. Mirza, and N. Kannan Conformational regulation of the EGFR kinase core by the juxtamembrane and C-terminal tail: a molecular dynamics study Proteins 79 2011 99 114
23. S. Wan, and P.V. Coveney Molecular dynamics simulation reveals structural and thermodynamic features of kinase activation by cancer mutations within the epidermal growth factor receptor J. Comput. Chem. 32 2011 2843 2852
24. Y. Shan, M.P. Eastwood, X. Zhang, E.T. Kim, A. Arkhipov, R.O., et al. Dror Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization Cell 149 2012 860 870
25. N. Songtawee, M.P. Gleeson, and K. Choowongkomon Computational study of EGFR inhibition: molecular dynamics studies on the active and inactive protein conformations J. Mol. Model. 19 2013 497 509
26. Y. Shan, A. Arkhipov, E.T. Kim, A.C. Pan, and D.E. Shaw Transitions to catalytically inactive conformations in EGFR kinase Proc. Natl. Acad. Sci. U.S.A. 110 2013 7270 7275
27. A. Arkhipov, Y. Shan, R. Das, N.F. Endres, M.P. Eastwood, D.E. Wemmer, et al. Architecture and membrane interactions of the EGF receptor Cell 152 2013 557 569
28. N. Guex, and M.C. Peitsch SWISS-MODEL the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18 1997 2714 2723
29. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
30. A. Fiser, and A. Sali ModLoop: automated modeling of loops in protein structures Bioinformatics 19 2003 2500 2501
31. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
32. C. Oostenbrink, A. Villa, A.E. Mark, and W.F. van Gunsteren A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 25 2004 1656 1676
33. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, and J. Hermans Interaction models for water in relation to protein hydration B. Pullman, Intermolecular Forces 1981 Reidel Dordrecht, The Netherlands 331 342
34. D. Van Der Spoel, E. Lindahl, B. Hess, G. Groenhof, A.E. Mark, and H.J. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718
35. S. Pronk, S. Pall, R. Schulz, P. Larsson, P. Bjelkmar, R. Apostolov, et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 29 2013 845 854
36. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, A. DiNola, and J.R. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
37. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101
38. M. Parrinello, and A. Rahman Polymorphic transitions in single crystals: a new molecular dynamics method J. Appl. Phys. 52 1981 7182 7190
39. S. Nosé, and M.L. Klein Constant pressure molecular dynamics for molecular systems Mol. Phys. 50 1983 1055 1076
40. S. Nosé A molecular dynamics method for simulations in the canonical ensemble Mol. Phys. 52 1984 255 268
41. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
42. B. Hess, H. Bekker, H.J.C. Berendsen, and J.G.E.M. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472
43. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an N • log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
44. U. Essmann, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, and L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
45. D. van der Spoel, E. Lindahl, B. Hess, A.R. van Buuren, E. Apol, P.J. Meulenhoff, et al. Gromacs User Manual Version 4.5.4 2010 www.gromacs.org
46. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
47. K.G. Tina, R. Bhadra, and N. Srinivasan PIC: protein interactions calculator Nucleic Acids Res. 35 2007 W473 W476
48. P.J. Turner Grace 2008 Center for Coastal and Land-Margin Research Oregon Graduate Institute of Science and Technology Beaverton, OR, USA
49. W.L. DeLano The PyMOL Molecular Graphics System, Version 1.3r1 2010 Schrödinger, LLC
50. A. Amadei, A.B. Linssen, and H.J. Berendsen Essential dynamics of proteins Proteins 17 1993 412 425
51. S. Hayward, and B.L. de Groot Normal modes and essential dynamics Methods Mol. Biol. 443 2008 89 106
52. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
53. A.J. Shih, S.E. Telesco, S.H. Choi, M.A. Lemmon, and R. Radhakrishnan Molecular dynamics analysis of conserved hydrophobic and hydrophilic bond-interaction networks in ErbB family kinases Biochem. J. 436 2011 241 251
54. D.M. van Aalten, D.A. Conn, B.L. de Groot, H.J. Berendsen, J.B. Findlay, and A. Amadei Protein dynamics derived from clusters of crystal structures Biophys. J. 73 1997 2891 2896
55. B.L. de Groot, S. Hayward, D.M. van Aalten, A. Amadei, and H.J. Berendsen Domain motions in bacteriophage T4 lysozyme: a comparison between molecular dynamics and crystallographic data Proteins 31 1998 116 127
56. A. Ivetac, and J.A. McCammon Elucidating the inhibition mechanism of HIV-1 non-nucleoside reverse transcriptase inhibitors through multicopy molecular dynamics simulations J. Mol. Biol. 388 2009 644 658
57. N. Narayana, S. Cox, X. Nguyen-huu, L.F. Ten Eyck, and S.S. Taylor A binary complex of the catalytic subunit of cAMP-dependent protein kinase and adenosine further defines conformational flexibility Structure 5 1997 921 935
58. M. Landau, and N. Ben-Tal Dynamic equilibrium between multiple active and inactive conformations explains regulation and oncogenic mutations in ErbB receptors Biochim. Biophys. Acta 1785 2008 12 31
59. R. Bose, and X. Zhang The ErbB kinase domain: structural perspectives into kinase activation and inhibition Exp. Cell Res. 315 2009 649 658