Emerging concepts in the regulation of the EGF receptor and other receptor tyrosine kinases

Trends in Biochemical Sciences

Volumn 39, Issue 10, 2014, Pages 437-446

  Endres, Nicholas F ^a,b   Barros, Tiago ^a,b   Cantor, Aaron J ^a,b   Kuriyan, John ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Allostery; Epidermal growth factor receptor; Receptor tyrosine kinases; Signal transduction

Indexed keywords

EPHRIN A4; EPHRIN A5; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE; EPIDERMAL GROWTH FACTOR DERIVATIVE; LIGAND;

CELL MEMBRANE; DIMERIZATION; ENZYME ACTIVATION; ENZYME CONFORMATION; ENZYME INHIBITION; ENZYME REGULATION; GENE MUTATION; LIGAND BINDING; MEMBRANE BINDING; MOLECULAR DYNAMICS; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

METAZOA;

CELL MEMBRANE; EGF FAMILY OF PROTEINS; ENZYME ACTIVATION; HUMANS; LIGANDS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84914142936     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2014.08.001     Document Type: Review

References (92)

1. Hubbard S.R. Structural analysis of receptor tyrosine kinases. Prog. Biophys. Mol. Biol. 1999, 71:343-358.
2. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
3. Heldin C-H. Dimerization of cell surface receptors in signal transduction. Cell 1995, 80:213-223.
4. Yarden Y., Schlessinger J. Epidermal growth factor induces rapid, reversible aggregation of the purified epidermal growth factor receptor. Biochemistry 1987, 26:1443-1451.
5. Yarden Y., Schlessinger J. Self-phosphorylation of epidermal growth factor receptor: evidence for a model of intermolecular allosteric activation. Biochemistry 1987, 26:1434-1442.
6. Burgess A.W., et al. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell 2003, 12:541-552.
7. Wiesmann C., et al. Crystal structure of nerve growth factor in complex with the ligand-binding domain of the TrkA receptor. Nature 1999, 401:184-188.
8. Jura N., et al. Catalytic control in the EGF receptor and its connection to general kinase regulatory mechanisms. Mol. Cell 2011, 42:9-22.
9. Hubbard S.R., Till J.H. Protein tyrosine kinase structure and function. Annu. Rev. Biochem. 2000, 69:373-398.
10. Nolen B., et al. Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 2004, 15:661-675.
11. Hubbard S.R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 1997, 16:5572-5581.
12. Wybenga-Groot L.E., et al. Structural basis for autoinhibition of the Ephb2 receptor tyrosine kinase by the unphosphorylated juxtamembrane region. Cell 2001, 106:745-757.
13. Griffith J., et al. The structural basis for autoinhibition of FLT3 by the juxtamembrane domain. Mol. Cell 2004, 13:169-178.
14. Hubbard S.R. Juxtamembrane autoinhibition in receptor tyrosine kinases. Nat. Rev. Mol. Cell Biol. 2004, 5:464-471.
15. Shewchuk L.M., et al. Structure of the Tie2 RTK domain: self-inhibition by the nucleotide binding loop, activation loop, and C-terminal tail. Structure 2000, 8:1105-1113.
16. Zhang X., et al. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 2006, 125:1137-1149.
17. Huse M., Kuriyan J. The conformational plasticity of protein kinases. Cell 2002, 109:275-282.
18. Kornev A.P., Taylor S.S. Defining the conserved internal architecture of a protein kinase. Biochim. Biophys. Acta 2010, 1804:440-444.
19. Hubbard S.R., et al. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 1994, 372:746-754.
20. Chen H., et al. A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol. Cell 2007, 27:717-730.
21. Yun C-H., et al. Structures of lung cancer-derived EGFR mutants and inhibitor complexes: Mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 2007, 11:217-227.
22. Yun C-H., et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2070-2075.
23. Dixit A., et al. Sequence and structure signatures of cancer mutation hotspots in protein kinases. PLoS ONE 2009, 4:e7485.
24. Shaw D.E., et al. Millisecond-scale molecular dynamics simulations on Anton. Presented at the Proceedings of the Conference on High Performance Computing Networking, Storage and Analysis 2009, 65:1-65:11. 10.1145/1654059.1654126.
25. Arkhipov A., et al. Architecture and membrane interactions of the EGF receptor. Cell 2013, 152:557-569.
26. Arkhipov A., et al. Her2 activation mechanism reflects evolutionary preservation of asymmetric ectodomain dimers in the human EGFR family. Elife 2013, 2:e00708.
27. Shan Y., et al. Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 2012, 149:860-870.
28. Shan Y., et al. Transitions to catalytically inactive conformations in EGFR kinase. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7270-7275.
29. Gajiwala K.S., et al. Insights into the aberrant activity of mutant EGFR kinase domain and drug recognition. Structure 2013, 21:209-219.
30. Sutto L., Gervasio F.L. Effects of oncogenic mutations on the conformational free-energy landscape of EGFR kinase. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:10616-10621.
31. Wood E.R., 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. 2004, 64:6652-6659.
32. Wang Z., et al. Mechanistic insights into the activation of oncogenic forms of EGF receptor. Nat. Struct. Mol. Biol. 2011, 10.1038/nsmb.2168.
33. Zhang X., et al. Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 2007, 450:741-744.
34. Red Brewer M., et al. Mechanism for activation of mutated epidermal growth factor receptors in lung cancer. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E3595-E3604.
35. Chen H., et al. Cracking the molecular origin of intrinsic tyrosine kinase activity through analysis of pathogenic gain-of-function mutations. Cell Rep. 2013, 4:376-384.
36. Dixit A., Verkhivker G.M. The energy landscape analysis of cancer mutations in protein kinases. PLoS ONE 2011, 6:e26071.
37. Schlessinger J. Signal transduction by allosteric receptor oligomerization. Trends Biochem. Sci. 1988, 13:443-447.
38. Nagy P., et al. Distribution of resting and ligand-bound ErbB1 and ErbB2 receptor tyrosine kinases in living cells using number and brightness analysis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16524-16529.
39. Ogiso H., et al. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 2002, 110:775-787.
40. Garrett T.P.J., et al. Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor alpha. Cell 2002, 110:763-773.
41. Ferguson K.M., et al. EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol. Cell 2003, 11:507-517.
42. Kalinina J., et al. The alternatively spliced acid box region plays a key role in FGF receptor autoinhibition. Structure 2012, 20:77-88.
43. Pines G., et al. EGFRvIV: a previously uncharacterized oncogenic mutant reveals a kinase autoinhibitory mechanism. Oncogene 2010, 29:5850-5860.
44. Jura N., et al. Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 2009, 137:1293-1307.
45. Red Brewer M., et al. The juxtamembrane region of the EGF receptor functions as an activation domain. Mol. Cell 2009, 34:641-651.
46. Endres N.F., et al. Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 2013, 152:543-556.
47. McLaughlin S., et al. An electrostatic engine model for autoinhibition and activation of the epidermal growth factor receptor (EGFR/ErbB) family. J. Gen. Physiol. 2005, 126:41-53.
48. Bryant K.L., et al. Mutations in the polybasic juxtamembrane sequence of both plasma membrane- and endoplasmic reticulum-localized epidermal growth factor receptors confer ligand-independent cell transformation. J. Biol. Chem. 2013, 288:34930-34942.
49. Blume-Jensen P., Hunter T. Oncogenic kinase signalling. Nature 2001, 411:355-365.
50. de Gunst M.M., et al. Functional analysis of cancer-associated EGFR mutants using a cellular assay with YFP-tagged EGFR intracellular domain. Mol. Cancer 2007, 6:56.
51. Chung I., et al. Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 2010, 464:783-787.
52. Low-Nam S.T., et al. ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding. Nat. Struct. Mol. Biol. 2011, 18:1244-1249.
53. Yamakawa D., et al. Ligand-independent Tie2 dimers mediate kinase activity stimulated by high dose angiopoietin-1. J. Biol. Chem. 2013, 288:12469-12477.
54. Wei X., et al. Uncoupling ligand-dependent and -independent mechanisms for mitogen-activated protein kinase activation by the murine Ron receptor tyrosine kinase. J. Biol. Chem. 2005, 280:35098-35107.
55. Dietz M.S., et al. Single-molecule photobleaching reveals increased MET receptor dimerization upon ligand binding in intact cells. BMC Biophys. 2013, 6:6.
56. Mihai C., et al. Mapping of DDR1 distribution and oligomerization on the cell surface by FRET microscopy. J. Mol. Biol. 2009, 385:432-445.
57. Shen J., Maruyama I.N. Nerve growth factor receptor TrkA exists as a preformed, yet inactive, dimer in living cells. FEBS Lett. 2011, 585:295-299.
58. Seiradake E., et al. An extracellular steric seeding mechanism for Eph-ephrin signaling platform assembly. Nat. Struct. Mol. Biol. 2010, 17:398-402.
59. Himanen J.P., et al. Architecture of Eph receptor clusters. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:10860-10865.
60. Wimmer-Kleikamp S.H., et al. Recruitment of Eph receptors into signaling clusters does not require ephrin contact. J. Cell Biol. 2004, 164:661-666.
61. Xu K., et al. Insights into Eph receptor tyrosine kinase activation from crystal structures of the EphA4 ectodomain and its complex with ephrin-A5. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:14634-14639.
62. Saffarian S., et al. Oligomerization of the EGF receptor investigated by live cell fluorescence intensity distribution analysis. Biophys. J. 2007, 93:1021-1031.
63. Salaita K., Groves J.T. Roles of the cytoskeleton in regulating EphA2 signals. Commun. Integr. Biol. 2010, 3:454-457.
64. Casaletto J.B., McClatchey A.I. Spatial regulation of receptor tyrosine kinases in development and cancer. Nat. Rev. Cancer 2012, 12:387-400.
65. Ariotti N., et al. Epidermal growth factor receptor activation remodels the plasma membrane lipid environment to induce nanocluster formation. Mol. Cell. Biol. 2010, 30:3795-3804.
66. Salaita K., et al. Restriction of receptor movement alters cellular response: physical force sensing by EphA2. Science 2010, 327:1380-1385.
67. Clayton A.H.A., et al. Predominance of activated EGFR higher-order oligomers on the cell surface. Growth Factors 2008, 26:316-324.
68. McKern N.M., et al. Structure of the insulin receptor ectodomain reveals a folded-over conformation. Nature 2006, 443:218-221.
69. Whittaker J., et al. α-Helical element at the hormone-binding surface of the insulin receptor functions as a signaling element to activate its tyrosine kinase. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:11166-11171.
70. Menting J.G., et al. How insulin engages its primary binding site on the insulin receptor. Nature 2013, 493:241-245.
71. Smith B.J., et al. Structural resolution of a tandem hormone-binding element in the insulin receptor and its implications for design of peptide agonists. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:6771-6776.
72. Verstraete K., Savvides S.N. Extracellular assembly and activation principles of oncogenic class III receptor tyrosine kinases. Nat. Rev. Cancer 2012, 12:753-766.
73. Carafoli F., et al. Structure of the discoidin domain receptor 1 extracellular region bound to an inhibitory Fab fragment reveals features important for signaling. Structure 2012, 20:688-697.
74. Janes P.W., et al. Cytoplasmic relaxation of active Eph controls ephrin shedding by ADAM10. PLoS Biol. 2009, 7:e1000215.
75. Reshetnyak A.V., et al. Structural basis for KIT receptor tyrosine kinase inhibition by antibodies targeting the D4 membrane-proximal region. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:17832-17837.
76. Li E., Hristova K. Receptor tyrosine kinase transmembrane domains: function, dimer structure and dimerization energetics. Cell Adh. Migr. 2010, 4:249-254.
77. Bocharov E.V., et al. Structural and thermodynamic insight into the process of "weak" dimerization of the ErbB4 transmembrane domain by solution NMR. Biochim. Biophys. Acta 2012, 1818:2158-2170.
78. Fleishman S.J., et al. A putative molecular-activation switch in the transmembrane domain of erbB2. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:15937-15940.
79. He L., Hristova K. Consequences of replacing EGFR juxtamembrane domain with an unstructured sequence. Sci. Rep. 2012, 2:854.
80. Scheck R.A.R., et al. Bipartite tetracysteine display reveals allosteric control of ligand-specific EGFR activation. ACS Chem. Biol. 2012, 7:1367-1376.
81. Lu C., et al. Structural evidence for loose linkage between ligand binding and kinase activation in the epidermal growth factor receptor. Mol. Cell. Biol. 2010, 30:5432-5443.
82. Finger C., et al. The single transmembrane domains of human receptor tyrosine kinases encode self-interactions. Sci. Signal. 2009, 2:ra56.
83. Bocharov E.V., et al. Structure of FGFR3 transmembrane domain dimer: implications for signaling and human pathologies. Structure 2013, 21:2087-2093.
84. Reddy T., et al. Primary and secondary dimer interfaces of the fibroblast growth factor receptor 3 transmembrane domain: characterization via multiscale molecular dynamics simulations. Biochemistry 2014, 53:323-332.
85. Dosch D.D., Ballmer-Hofer K. Transmembrane domain-mediated orientation of receptor monomers in active VEGFR-2 dimers. FASEB J. 2010, 24:32-38.
86. Yu X., et al. Structural basis for angiopoietin-1-mediated signaling initiation. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7205-7210.
87. Seegar T.C.M., et al. Tie1-Tie2 interactions mediate functional differences between angiopoietin ligands. Mol. Cell 2010, 37:643-655.
88. Alvarado D., et al. Structural basis for negative cooperativity in growth factor binding to an EGF receptor. Cell 2010, 142:568-579.
89. Liu P., et al. A single ligand is sufficient to activate EGFR dimers. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:10861-10866.
90. Macdonald J.L., Pike L.J. Heterogeneity in EGF-binding affinities arises from negative cooperativity in an aggregating system. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:112-117.
91. Krall J.A., et al. High- and low-affinity epidermal growth factor receptor-ligand interactions activate distinct signaling pathways. PLoS ONE 2011, 6:e15945.
92. Grecco H.E., et al. Signaling from the living plasma membrane. Cell 2011, 144:897-909.