Erlotinib binds both inactive and active conformations of the EGFR tyrosine kinase domain

Biochemical Journal

Volumn 448, Issue 3, 2012, Pages 417-423

  Park, Jin H ^a   Liu, Yingting ^b   Lemmon, Mark A ^a   Radhakrishnan, Ravi ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cancer; Epidermal growth factor receptor (EGFR); Erlotinib; Gefitinib; Inhibitor; Molecular dynamics; Receptor tyrosine kinase (RTK); X ray crystallography

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; LAPATINIB;

ARTICLE; COMPUTATIONAL FLUID DYNAMICS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DRUG RECEPTOR BINDING; ENZYME ACTIVE SITE; ENZYME CONFORMATION; GLIOBLASTOMA; HUMAN; LUNG NON SMALL CELL CANCER; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING;

ANIMALS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; HUMANS; INSECTS; PROTEIN CONFORMATION; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84870005636     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121513     Document Type: Article

References (41)

1. Sharma, S. V., Bell, D. W., Settleman, J. and Haber, D. A. (2007) Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 7, 169-181
2. Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455, 1061-1068
3. Vivanco, I., Robins, H. I., Rohle, D., Campos, C., Grommes, C., Nghiemphu, P. L., Kubek, S., Oldrini, B., Chheda, M. G., Yannuzzi, N. et al. (2012) Differential sensitivity of gliomaversus lung cancer-specific EGFR mutations to EGFR kinase inhibitors. Cancer Discovery 2, 458-471
4. Pao, W. and Chmielecki, J. (2010) Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat. Rev. Cancer 10, 760-774
5. Jänne, P. A., Gray, N. and Settleman, J. (2009) Factors underlying sensitivity of cancers to small-molecule kinase inhibitors. Nat. Rev. Drug Discovery 8, 709-723
6. Yoshikawa, S., Kukimoto-Niino, M., Parker, L., Handa, N., Terada, T., Fujimoto, T., Terazawa, Y., Wakiyama, M., Sato, M., Sano, S. et al. (2012) Structural basis for the altered drug sensitivities of non-small cell lung cancer-associated mutants of human epidermal growth factor receptor. Oncogene, doi:10.1038/onc.2012.21
7. Yun, C. H., Mengwasser, K. E., Toms, A. V., Woo, M. S., Greulich, H., Wong, K. K., Meyerson, M. and Eck, M. J. (2008) The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc. Natl. Acad. Sci. U.S.A. 105, 2070-2075 (Pubitemid 351439466)
8. Eck, M. J. and 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
9. Liu, Y. and Gray, N. S. (2006) Rational design of inhibitors that bind to inactive kinase conformations. Nat. Chem. Biol. 2, 358-364 (Pubitemid 43936934)
10. Stamos, J., Sliwkowski, M. X. and Eigenbrot, C. (2002) Structure of the epidermal growth factor receptor kinase domain alone and in complex with a 4-anilinoquinazoline inhibitor. J. Biol. Chem. 277, 46265-46272 (Pubitemid 35417619)
11. Yun, C. H., Boggon, T. J., Li, Y., Woo, M. S., Greulich, H., Meyerson, M. and 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 (Pubitemid 46349842)
12. Zhang, X., Gureasko, J., Shen, K., Cole, P. A. and Kuriyan, J. (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149 (Pubitemid 43866200)
13. Wood, E. R., Truesdale, A. T., McDonald, O. B., Yuan, D., Hassell, A., Dickerson, S. H., Ellis, B., Pennisi, C., Horne, E., Lackey, K. et al. (2004) 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, 6652-6659 (Pubitemid 39297926)
14. Fabian, M. A., Biggs, 3rd, W. H., Treiber, D. K., Atteridge, C. E., Azimioara, M. D., Benedetti, M. G., Carter, T. A., Ciceri, P., Edeen, P. T., Floyd, M. et al. (2005) A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23, 329-336 (Pubitemid 41094421)
15. Lu, C., Mi, L. Z., Schürpf, T., Walz, T. and Springer, T. A. (2012) Mechanisms for kinase-mediated dimerization of the EGF receptor. J. Biol. Chem., doi:10.1074/jbc.M112.414391
16. Wang, Z., Longo, P. A., Tarrant, M. K., Kim, K., Head, S., Leahy, D. J. and Cole, P. A. (2011) Mechanistic insights into the activation of oncogenic forms of EGF receptor. Nat. Struct. Mol. Biol. 18, 1388-1393
17. Barkovich, K. J., Hariono, S., Garske, A. L., Zhang, J., Blair, J. A., Fan, Q. W., Shokat, K. M., Nicolaides, T. and Weiss, W. A. (2012) Kinetics of inhibitor cycling underlie therapeutic disparities between EGFR-driven lung and brain cancers. Cancer Discovery 2, 450-457
18. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
19. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
20. Jura, N., Endres, N. F., Engel, K., Deindl, S., Das, R., Lamers, M. H., Wemmer, D. E., Zhang, X. and Kuriyan, J. (2009) Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 137, 1293-1307
21. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
22. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F. and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. Sect. D Biol. Crystallogr. 67, 355-367
23. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S. et al. (1998) Crystallography &NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 54, 905-921
24. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 213-221
25. Winn, M. D., Isupov, M. N. and Murshudov, G. N. (2001) Use of TLS anisotropic displacements in macromolecular refinement. Acta Crystallogr. Sect. D Biol. Crystallogr. 57, 122-133 (Pubitemid 32062682)
26. Schüttelkopf, A. W. and van Aalten, D. M. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 1355-1363 (Pubitemid 41079731)
27. Reference deleted
28. Reference deleted
29. Reference deleted
30. Jorgensen, W. L. and Tiradorives, J. (1988) The OPLS potential functions for proteins: energy minimizations for crystals of cyclic-peptides and crambin. J. Am. Chem. Soc. 110, 1657-1666
31. Sherman, W., Day, T., Jacobson, M. P., Friesner, R. A. and Farid, R. (2006) Novel procedure for modeling ligand/receptor induced fit effects. J. Med. Chem. 49, 534-553 (Pubitemid 43157487)
32. Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C. and Mainz, D. T. (2006) Extra Precision Glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J. Med. Chem. 49, 6177-6196 (Pubitemid 44595196)
33. Jacobson, M. P., Pincus, D. L., Rapp, C. S., Day, T. J. F., Honig, B., Shaw, D. E. and Friesner, R. A. (2004) A hierarchical approach to all-atom protein loop prediction. Proteins 55, 351-367 (Pubitemid 38437493)
34. Foloppe, N. and MacKerell, A. D. (2000) All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J. Comput. Chem. 21, 86-104
35. Wang, J., Morin, P., Wang, W. and Kollman, P. A. (2001) Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MM-PBSA. J. Am. Chem. Soc. 123, 5221-5230 (Pubitemid 32910665)
36. Swanson, J. M. J., Henchman, R. H. and McCammon, J. A. (2004) Revisiting free energy calculations: a theoretical connection between MM/PBSA and direct calculation of the association free energy. Biophys. J. 86, 67-74 (Pubitemid 38067436)
37. Im, W., Beglov, D. and Roux, B. (1998) Continuum Solvation Model: computation of electrostatic forces from numerical solutions to the Poisson-Boltzmann equation. Comput. Phys. Commun. 111, 59-75 (Pubitemid 128400465)
38. Sanner, M. F., Olson, A. J. and Spehner, J. C. (1996) Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38, 305-320
39. Zhang, X., Pickin, K. A., Bose, R., Jura, N., Cole, P. A. and Kuriyan, J. (2007) Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 450, 741-744 (Pubitemid 350207680)
40. Anido, J., Matar, P., Albanell, J., Guzmán, M., Rojo, F., Arribas, J., Averbuch, S. and Baselga, J. (2003) ZD1839, a specific epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor, induces the formation of inactive EGFR/HER2 and EGFR/HER3 heterodimers and prevents heregulin signaling in HER2-overexpressing breast cancer cells. Clin. Cancer Res. 9, 1274-1283 (Pubitemid 36418377)
41. Mi, L. Z., Lu, C., Li, Z., Nishida, N., Walz, T. and Springer, T. A. (2011) Simultaneous visualization of the extracellular and cytoplasmic domains of the epidermal growth factor receptor. Nat. Struct. Mol. Biol. 18, 984-989