Oligomerization-function relationship of EGFR on living cells detected by the coiled-coil labeling and FRET microscopy

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 6, 2015, Pages 1359-1366

  Yamashita, Hirotaka ^a   Yano, Yoshiaki ^a   Kawano, Kenichi ^a   Matsuzaki, Katsumi ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Dimerization; FRET; Live cell imaging

Indexed keywords

CHOLESTEROL; DIMER; EPIDERMAL GROWTH FACTOR RECEPTOR; MONOMER; MONOSIALOGANGLIOSIDE; MONOSIALOGANGLIOSIDE GM3; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR; MEMBRANE PROTEIN;

ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CELL LABELING; CELL MEMBRANE; CHO CELL LINE; CHO K1 CELL; COILED COIL TAG PROBE LABELING; CONCENTRATION (PARAMETERS); CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; INCUBATION TIME; INTRACELLULAR SIGNALING; LIGAND STIMULATION; MEASUREMENT ACCURACY; MOLECULAR DYNAMICS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RELIABILITY; SIMULATION; TIME SERIES ANALYSIS; WESTERN BLOTTING; ANIMAL; CELL SURVIVAL; CHEMISTRY; CRICETULUS; DRUG EFFECTS; HAMSTER; METABOLISM; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; RAT; TIME;

ANIMALS; CELL SURVIVAL; CHO CELLS; CRICETINAE; CRICETULUS; EPIDERMAL GROWTH FACTOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TIME FACTORS;

EID: 84925424845     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2015.03.004     Document Type: Article

References (50)

1. K. Sakaguchi, Y. Okabayashi, Y. Kido, S. Kimura, Y. Matsumura, K. Inushima, and M. Kasuga Shc phosphotyrosine-binding domain dominantly interacts with epidermal growth factor receptors and mediates Ras activation in intact cells Mol. Endocrinol. 12 1998 536 543
2. J. Mendelsohn, and J. Baselga The EGF receptor family as targets for cancer therapy Oncogene 19 2000 6550 6565
3. I. Okamoto Epidermal growth factor receptor in relation to tumor development: EGFR-targeted anticancer therapy FEBS J. 277 2010 309 315
4. W.A. Franklin, R. Veve, F.R. Hirsch, B.A. Helfrich, and P.A. Bunn Jr. Epidermal growth factor receptor family in lung cancer and premalignancy Semin. Oncol. 29 2002 3 14
5. M.A. Lemmon Ligand-induced ErbB receptor dimerization Exp. Cell Res. 315 2009 638 648
6. K.M. Ferguson Structure-based view of epidermal growth factor receptor regulation Annu. Rev. Biophys. 37 2008 353 373
7. 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
8. K.M. Ferguson, M.B. Berger, J.M. Mendrola, H.S. Cho, D.J. Leahy, and M.A. Lemmon EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization Mol. Cell 11 2003 507 517
9. H. Ogiso, R. Ishitani, O. Nureki, S. Fukai, M. Yamanaka, J.H. Kim, K. Saito, A. Sakamoto, M. Inoue, M. Shirouzu, and S. Yokoyama Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains Cell 110 2002 775 787
10. T.P. Garrett, N.M. McKern, M. Lou, T.C. Elleman, T.E. Adams, G.O. Lovrecz, H.J. Zhu, F. Walker, M.J. Frenkel, P.A. Hoyne, R.N. Jorissen, E.C. Nice, A.W. Burgess, and C.W. Ward Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor alpha Cell 110 2002 763 773
11. R. Zidovetzki, D.A. Johnson, D.J. Arndt-Jovin, and T.M. Jovin Rotational mobility of high-affinity epidermal growth factor receptors on the surface of living A431 cells Biochemistry 30 1991 6162 6166
12. C. Wofsy, B. Goldstein, K. Lund, and H.S. Wiley Implications of epidermal growth factor (EGF) induced egf receptor aggregation Biophys. J. 63 1992 98 110
13. L.J. Pike Negative co-operativity in the EGF receptor Biochem. Soc. Trans. 40 2012 15 19
14. T. Moriki, H. Maruyama, and I.N. Maruyama Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain J. Mol. Biol. 311 2001 1011 1026
15. A.H. Clayton, F. Walker, S.G. Orchard, C. Henderson, D. Fuchs, J. Rothacker, E.C. Nice, and A.W. Burgess Ligand-induced dimer-tetramer transition during the activation of the cell surface epidermal growth factor receptor-A multidimensional microscopy analysis J. Biol. Chem. 280 2005 30392 30399
16. E.G. Hofman, A.N. Bader, J. Voortman, D.J. van den Heuvel, S. Sigismund, A.J. Verkleij, H.C. Gerritsen, and P.M. van Bergen en Henegouwen Ligand-induced EGF receptor oligomerization is kinase-dependent and enhances internalization J. Biol. Chem. 285 2010 39481 39489
17. N. Kawashima, K. Nakayama, K. Itoh, T. Itoh, M. Ishikawa, and V. Biju Reversible dimerization of EGFR revealed by single-molecule fluorescence imaging using quantum dots Chemistry 16 2010 1186 1192
18. A. Salahpour, and B. Masri Experimental challenge to a 'rigorous' BRET analysis of GPCR oligomerization Nat. Methods 4 2007 599 600 (author reply 601)
19. Y. Yano, A. Yano, S. Oishi, Y. Sugimoto, G. Tsujimoto, N. Fujii, and K. Matsuzaki Coiled-coil tag-probe system for quick labeling of membrane receptors in living cell ACS Chem. Biol. 3 2008 341 345
20. K. Kawano, Y. Yano, K. Omae, S. Matsuzaki, and K. Matsuzaki Stoichiometric analysis of oligomerization of membrane proteins on living cells using coiled-coil labeling and spectral imaging Anal. Chem. 85 2013 3454 3461
21. Y. Yano, and K. Matsuzaki Fluorescence ratiometric detection of ligand-induced receptor internalization using extracellular coiled-coil tag-probe labeling FEBS Lett. 585 2011 2385 2388
22. A.W. Krug, C. Schuster, B. Gassner, R. Freudinger, S. Mildenberger, J. Troppmair, and M. Gekle Human epidermal growth factor receptor-1 expression renders Chinese hamster ovary cells sensitive to alternative aldosterone signaling J. Biol. Chem. 277 2002 45892 45897
23. E. Tzahar, H. Waterman, X. Chen, G. Levkowitz, D. Karunagaran, S. Lavi, B.J. Ratzkin, and Y. Yarden A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor Mol. Cell. Biol. 16 1996 5276 5287
24. A.R. Zurita, P.M. Crespo, N.P. Koritschoner, and J.L. Daniotti Membrane distribution of epidermal growth factor receptors in cells expressing different gangliosides Eur. J. Biochem. 271 2004 2428 2437
25. R.H. Tao, and I.N. Maruyama All EGF(ErbB) receptors have preformed homo- and heterodimeric structures in living cells J. Cell Sci. 121 2008 3207 3217
26. B.H. Meyer, J.M. Segura, K.L. Martinez, R. Hovius, N. George, K. Johnsson, and H. Vogel FRET imaging reveals that functional neurokinin-1 receptors are monomeric and reside in membrane microdomains of live cells Proc. Natl. Acad. Sci. U. S. A. 103 2006 2138 2143
27. K. Kawano, Y. Yano, and K. Matsuzaki A dimer is the minimal proton-conducting unit of the influenza a virus m2 channel J. Mol. Biol. 426 2014 2679 2691
28. T. Ha, A.Y. Ting, J. Liang, W.B. Caldwell, A.A. Deniz, D.S. Chemla, P.G. Schultz, and S. Weiss Single-molecule fluorescence spectroscopy of enzyme conformational dynamics and cleavage mechanism Proc. Natl. Acad. Sci. U. S. A. 96 1999 893 898
29. L.J. Pike, and L. Casey Cholesterol levels modulate EGF receptor-mediated signaling by altering receptor function and trafficking Biochemistry 41 2002 10315 10322
30. Q. Zhou, S. Hakomori, K. Kitamura, and Y. Igarashi GM3 directly inhibits tyrosine phosphorylation and de-N-acetyl-GM3 directly enhances serine phosphorylation of epidermal growth factor receptor, independently of receptor-receptor interaction J. Biol. Chem. 269 1994 1959 1965
31. A.H.A. Clayton, M.L. Tavarnesi, and T.G. Johns Unligated epidermal growth factor receptor forms higher order oligomers within microclusters on A431 cells that are sensitive to tyrosine kinase inhibitor binding Biochemistry 46 2007 4589 4597
32. S. Saffarian, Y. Li, E.L. Elson, and L.J. Pike Oligomerization of the EGF receptor investigated by live cell fluorescence intensity distribution analysis Biophys. J. 93 2007 1021 1031
33. N.F. Endres, R. Das, A.W. Smith, A. Arkhipov, E. Kovacs, Y. Huang, J.G. Pelton, Y. Shan, D.E. Shaw, D.E. Wemmer, J.T. Groves, and J. Kuriyan Conformational coupling across the plasma membrane in activation of the EGF receptor Cell 152 2013 543 556
34. J.L. Macdonald-Obermann, and L.J. Pike The intracellular juxtamembrane domain of the epidermal growth factor (EGF) receptor is responsible for the allosteric regulation of EGF binding J. Biol. Chem. 284 2009 13570 13576
35. S.T. Low-Nam, K.A. Lidke, P.J. Cutler, R.C. Roovers, P.M. van Bergen en Henegouwen, B.S. Wilson, and D.S. Lidke ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding Nat. Struct. Mol. Biol. 18 2011 1244 1249
36. Y. Teramura, J. Ichinose, H. Takagi, K. Nishida, T. Yanagida, and Y. Sako Single-molecule analysis of epidermal growth factor binding on the surface of living cells EMBO J. 25 2006 4215 4222
37. H.S. Wiley, B.J. Walsh, and K.A. Lund Global modulation of the epidermal growth factor receptor is triggered by occupancy of only a few receptors J. Biol. Chem. 264 1989 18912 18920
38. O.G. Berg, and P.H. von Hippel Diffusion-controlled macromolecular interactions Annu. Rev. Biophys. Biophys. Chem. 14 1985 131 160
39. M. Korc, L.M. Matrisian, S.R. Planck, and B.E. Magun Binding of epidermal growth factor in rat pancreatic acini Biochem. Biophys. Res. Commun. 111 1983 1066 1073
40. K.W. Ng, N.C. Partridge, M. Niall, and T.J. Martin Epidermal growth factor receptors in clonal lines of a rat osteogenic sarcoma and in osteoblast-rich rat bone cells Calcif. Tissue Int. 35 1983 298 303
41. P.B. Jones, T.H. Welsh Jr., and A.J. Hsueh Regulation of ovarian progestin production by epidermal growth factor in cultured rat granulosa cells J. Biol. Chem. 257 1982 11268 11273
42. L. Raaberg, E. Nexo, S. Buckley, W. Luo, M.L. Snead, and D. Warburton Epidermal growth factor transcription, translation, and signal transduction by rat type II pneumocytes in culture Am. J. Respir. Cell Mol. Biol. 6 1992 44 49
43. N. Matsuda, N.M. Kumar, P.R. Ramakrishnan, W.L. Lin, R.J. Genco, and M.I. Cho Evidence for up-regulation of epidermal growth-factor receptors on rat periodontal ligament fibroblastic cells associated with stabilization of phenotype in vitro Arch. Oral Biol. 38 1993 559 569
44. B.N. Kholodenko, O.V. Demin, M. Gisela, and J.B. Hoek Quantification of short term singnaling by the epidermal growth factor receptor J. Biol. Chem. 274 1999 30169 30181
45. P.J. Bertics, W.S. Chen, L. Hubler, C. Lazar, M.G. Rosenfeld, and G.N. Gill Alteration of epidermal growth factor receptor activity by mutation of its primary carboxy-terminal site of tyrosine self-phosphorylation J. Biol. Chem. 263 1988 3610 3617
46. P.J. Verveer, F.S. Wouters, A.R. Reynolds, and P.H.I. Bastians Quantitative imaging of lateral ErbB1 receptor signal propagation in the plasma membrane Science 290 2000 1567 1570
47. N.J. Bessman, D.M. Freed, and M.A. Lemmon Putting together structures of epidermal growth factor reeptors Curr. Opin. Struct. Biol. 29 2014 95 101
48. P. Liu, T.E. Cleveland IV, S. Bouyain, P.O. Byrne, P.A. Longo, and D.J. Leahy A single ligand is sufficient to activate EGFR dimers Proc. Natl. Acad. Sci. U. S. A. 109 2012 10861 10866
49. H. Haigler, J.F. Ash, S.J. Singer, and S. Cohen Visualization by fluorescence of the binding and internalization of epidermal growth factor in human carcinoma cells A-431 Proc. Natl. Acad. Sci. U. S. A. 75 1978 3317 3321
50. C.T. Kuan, C.J. Wikstrand, and D.D. Bigner EGF mutant receptor vIII as a molecular target in cancer therapy Endocr. Relat. Cancer 8 2001 83 96