Transitions to catalytically inactive conformations in EGFR kinase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 18, 2013, Pages 7270-7275

  Shan, Yibing ^a   Arkhipov, Anton ^a   Kim, Eric T ^a   Pan, Albert C ^a   Shawa, David E ^a,b  

^a D E SHAW RESEARCH   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Activation loop conformations; High entropy transition state; Hinge unfolding; Molten globule intermediate state

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DEUTERIUM HYDROGEN EXCHANGE; ENZYME CONFORMATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL;

AMINO ACID MOTIFS; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; DEUTERIUM EXCHANGE MEASUREMENT; ENZYME ACTIVATION; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, EPIDERMAL GROWTH FACTOR; SRC-FAMILY KINASES;

EID: 84876902448     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220843110     Document Type: Article

References (47)

1. Yarden Y, Sliwkowski MX (2001) Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2(2):127-137. (Pubitemid 33674041)
2. Lurje G, Lenz H-J (2009) EGFR signaling and drug discovery. Oncology 77(6):400-410.
3. Stamos J, Sliwkowski MX, 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(48):46265-46272. (Pubitemid 35417619)
4. Wood ER, 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(18):6652-6659. (Pubitemid 39297926)
5. Zhang XW, Gureasko J, Shen K, Cole PA, Kuriyan J (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125(6):1137-1149. (Pubitemid 43866200)
6. Huse M, Kuriyan J (2002) The conformational plasticity of protein kinases. Cell 109(3):275-282. (Pubitemid 34606870)
7. Huang H, Ozkirimli E, Post CB (2009) Comparison of three perturbation molecular dynamics methods for modeling conformational transitions. J Chem Theory Comput 5(5):1301-1314.
8. Lovera S, et al. (2012) The different flexibility of c-Src and c-Abl kinases regulates the accessibility of a druggable inactive conformation. J Am Chem Soc 134(5):2496-2499.
9. Lu B, Wong CF, McCammon JA (2005) Release of ADP from the catalytic subunit of protein kinase A: A molecular dynamics simulation study. Protein Sci 14(1):159-168. (Pubitemid 40054127)
10. Ozkirimli E, Post CB (2006) Src kinase activation: A switched electrostatic network. Protein Sci 15(5):1051-1062.
11. Wan S, Wright DW, Coveney PV (2012) Mechanism of drug efficacy within the EGF receptor revealed by microsecond molecular dynamics simulation. Mol Cancer Ther 11(11):2394-2400.
12. Yang S, Banavali NK, Roux B (2009) Mapping the conformational transition in Src activation by cumulating the information from multiple molecular dynamics trajectories. Proc Natl Acad Sci USA 106(10):3776-3781.
13. Frembgen-Kesner T, Elcock AH (2006) Computational sampling of a cryptic drug binding site in a protein receptor: Explicit solvent molecular dynamics and inhibitor docking to p38 MAP kinase. J Mol Biol 359(1):202-214. (Pubitemid 44287824)
14. Gajiwala KS, et al. (2013) Insights into the aberrant activity of mutant EGFR kinase domain and drug recognition. Structure 21(2):209-219.
15. Zhang X, et al. (2007) Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 450(7170):741-744. (Pubitemid 350207680)
16. Shan Y, et al. (2012) Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 149(4):860-870.
17. Miyashita O, Onuchic JN, Wolynes PG (2003) Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc Natl Acad Sci USA 100(22):12570-12575. (Pubitemid 37339939)
18. Wolf-Watz M, et al. (2004) Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat Struct Mol Biol 11(10):945-949. (Pubitemid 39315297)
19. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254(5038):1598-1603. (Pubitemid 21917496)
20. Hyeon C, Jennings PA, Adams JA, Onuchic JN (2009) Ligand-induced global transitions in the catalytic domain of protein kinase A. Proc Natl Acad Sci USA 106(9):3023-3028.
21. Whitford PC, Miyashita O, Levy Y, Onuchic JN (2007) Conformational transitions of adenylate kinase: Switching by cracking. J Mol Biol 366(5):1661-1671. (Pubitemid 46215597)
22. Brokaw JB, Chu JW (2010) On the roles of substrate binding and hinge unfolding in conformational changes of adenylate kinase. Biophys J 99(10):3420-3429.
23. Whitford PC, Sanbonmatsu KY, Onuchic JN (2012) Biomolecular dynamics: Order-disorder transitions and energy landscapes. Rep Prog Phys 75(7):076601.
24. Shan Y, et al. (2009) A conserved protonation-dependent switch controls drug binding in the Abl kinase. Proc Natl Acad Sci USA 106(1):139-144.
25. Levinson NM, et al. (2006) A Src-like inactive conformation in the abl tyrosine kinase domain. PLoS Biol 4(5):e144.
26. as and adding missing hydrogens to macromolecules. Nucleic Acids Res 33(Web Server issue):W368-W371.
27. Onufriev A, Bashford D, Case DA (2000) Modification of the generalized Born model suitable for macromolecules. J Phys Chem B 104(15):3712-3720.
28. Hubbard SR, Wei L, Ellis L, Hendrickson WA (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372(6508):746-754.
29. Pike ACW, et al. (2008) Activation segment dimerization: A mechanism for kinase autophosphorylation of non-consensus sites. EMBO J 27(4):704-714. (Pubitemid 351273130)
30. Li Y, Palmer AG (2009) Domain swapping in the kinase superfamily: OSR1 joins the mix. Protein Sci 18(4):678-681.
31. Piana S, Lindorff-Larsen K, Shaw DE (2011) How robust are protein folding simulations with respect to force field parameterization? Biophys J 100(9):L47-L49.
32. Hornak V, et al. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65(3):712-725. (Pubitemid 44583220)
33. Lindorff-Larsen K, et al. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78(8):1950-1958.
34. Adams JA (2001) Kinetic and catalytic mechanisms of protein kinases. Chem Rev 101(8):2271-2290.
35. Nagar B, et al. (2003) Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112(6):859-871. (Pubitemid 36378887)
36. Sicheri F, MoarefiI, Kuriyan J (1997) Crystal structure of the Src family tyrosine kinase Hck. Nature 385(6617):602-609. (Pubitemid 27087567)
37. Xu W, Harrison SC, Eck MJ (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385(6617):595-602. (Pubitemid 27087566)
38. Young MA, Gonfloni S, Superti-Furga G, Roux B, Kuriyan J (2001) Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105(1):115-126. (Pubitemid 32323921)
39. Chen H, et al. (2007) A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol Cell 27(5):717-730. (Pubitemid 47333217)
40. Deindl S, et al. (2007) Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Cell 129(4):735-746. (Pubitemid 46802380)
41. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79(2):926-935.
42. MacKerell AD, Jr., et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102(18):3586-3616.
43. Shaw DE, et al. (2009) Millisecond-scale molecular dynamics simulations on Anton. Proceedings of the Conference on High Performance Computing, Networking, Storage and Analysis (SC09) (Association for Computing Machinery, New York), 10.1145/1654059.1654099.
44. Berendsen HJC, Postma JPM, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81(8):3684-3690.
45. Krautler V, van Gunsteren WF, Hunenberger PH (2001) A fast SHAKE algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. J Comput Chem 22(5):501-508. (Pubitemid 32291686)
46. Shan Y, Klepeis JL, Eastwood MP, Dror RO, Shaw DE (2005) Gaussian split Ewald: A fast Ewald mesh method for molecular simulation. J Chem Phys 122(5):54101.
47. Tuckerman M, Berne BJ, Martyna GJ (1992) Reversible multiple time scale molecular dynamics. J Chem Phys 97(3):1990-2001.