Evidence for extended YFP-EGFR dimers in the absence of ligand on the surface of living cells

Physical Biology

Volumn 8, Issue 6, 2011, Pages

  Kozer, Noga ^a   Henderson, Christine ^a   Jackson, Jacob T ^b   Nice, Edouard C ^b   Burgess, Antony W ^b   Clayton, Andrew H A ^a  

^a SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HYBRID PROTEIN; LIGAND; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMAL; ARTICLE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; GENETICS; METABOLISM; MOUSE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; LIGANDS; LUMINESCENT PROTEINS; MICE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS;

EID: 82955195098     PISSN: 14783967     EISSN: 14783975     Source Type: Journal    
DOI: 10.1088/1478-3975/8/6/066002     Document Type: Article

References (67)

1. Alvarado D, Klein D E and Lemmon M A 2009 ErbB2 resembles an autoinhibited invertebrate epidermal growth factor receptor Nature 461 287-91
2. Alvarado D, Klein D E and Lemmon M A 2010 Structural basis for negative cooperativity in growth factor binding to an EGF receptor Cell 142 568-79
3. Ariotti N, Liang H, XU Y, Zhang Y, Yonekubo Y, Inder K, DU G, Parton R G, Hancock J F and Plowman S J 2010 Epidermal growth factor receptor activation remodels the plasma membrane lipid environment to induce nanocluster formation Mol. Cell. Biol. 30 3795-804
4. Bader A N, Hofman E G, Voortman J, EN Henegouwen P M and Gerritsen H C 2009 Homo-FRET imaging enables quantification of protein cluster sizes with subcellular resolution Biophys. J. 97 2613-22
5. Bagossi P, Horvath G, Vereb G, Szollosi J and Tozser J 2005 Molecular modeling of nearly full-length ErbB2 receptor Biophys. J. 88 1354-63 (Pubitemid 40975962)
6. Becker J W, Reeke G N Jr, Wang J L, Cunningham B A and Edelman G M 1975 The covalent and three-dimensional structure of concanavalin A: III. Structure of the monomer and its interactions with metals and saccharides J. Biol. Chem. 250 1513-24
7. Burgess A W, Cho H S, Eigenbrot C, Ferguson K M, Garrett T P, Leahy D J, Lemmon M A, Sliwkowski M X, Ward C W and Yokoyama S 2003 An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors Mol. Cell 12 541-52 (Pubitemid 37222478)
8. Burgess A W, Lloyd C J and Nice E C 1983 Murine epidermal growth factor: heterogeneity on high resolution ion-exchange chromatography Embo J. 2 2065-9
9. Canals F 1992 Signal transmission by epidermal growth factor receptor: coincidence of activation and dimerization Biochemistry 31 4493-501
10. Carraway K L 3rd, Koland J G and Cerione R A 1990 Location of the epidermal growth factor binding site on the EGF receptor: a resonance energy transfer study Biochemistry 29 8741-7 (Pubitemid 20302770)
11. Cho H S and Leahy D J 2002 Structure of the extracellular region of HER3 reveals an interdomain tether Science 297 1330-3 (Pubitemid 34913167)
12. Chung I, Akita R, Vandlen R, Toomre D, Schlessinger J and Mellman I 2010 Spatial control of EGF receptor activation by reversible dimerization on living cells Nature 464 783-7
13. Clayton A H 2008 The polarized AB plot for the frequency-domain analysis and representation of fluorophore rotation and resonance energy homotransfer J. Microsc. 232 306-12
14. Clayton A H, Hanley Q S, Arndt-Jovin D J, Subramaniam V and Jovin T M 2002 Dynamic fluorescence anisotropy imaging microscopy in the frequency domain (rFLIM) Biophys. J. 83 1631-49 (Pubitemid 34977734)
15. Clayton A H, Hanley Q S and Verveer P J 2004 Graphical representation and multicomponent analysis of single-frequency fluorescence lifetime imaging microscopy data J. Microsc. 213 1-5 (Pubitemid 38161145)
16. Clayton A H, Orchard S G, Nice E C, Posner R G and Burgess A W 2008 Predominance of activated EGFR higher-order oligomers on the cell surface Growth Factors 26 316-24 (Pubitemid 352781844)
17. Clayton A H, Walker F, Orchard S G, Henderson C, Fuchs D, Rothacker J, Nice E C and Burgess A W 2005 Ligand-induced dimer-tetramer transition during the activation of the cell surface epidermal growth factor receptor-A multidimensional microscopy analysis J. Biol. Chem. 280 30392-9 (Pubitemid 41216222)
18. Dewey T G and Hammes G G 1980 Calculation on fluorescence resonance energy transfer on surfaces Biophys. J. 32 1023-35 (Pubitemid 11195960)
19. Digman M A, Caiolfa V R, Zamai M and Gratton E 2008 The phasor approach to fluorescence lifetime imaging analysis Biophys. J. 94 L14-6
20. Elleman T C et al 2001 Identification of a determinant of epidermal growth factor receptor ligand-binding specificity using a truncated, high-affinity form of the ectodomain Biochemistry 40 8930-9 (Pubitemid 32709526)
21. Ferguson K M, Berger M B, Mendrola J M, Cho H S, Leahy D J and Lemmon M A 2003 EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization Mol. Cell 11 507-17 (Pubitemid 36297057)
22. Gadella T W Jr and Jovin T M 1995 Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy: a stereochemical model for tyrosine kinase receptor activation J. Cell. Biol. 129 1543-58
23. Gan H K, Walker F, Burgess A W, Rigopoulos A, Scott A M and Johns T G 2007 The epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor AG1478 increases the formation of inactive untethered EGFR dimers: implications for combination therapy with monoclonal antibody 806 J. Biol. Chem. 282 2840-50 (Pubitemid 47084315)
24. Garrett T P et al 2002 Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor alpha Cell 110 763-73 (Pubitemid 35283965)
25. Garrett T P et al 2003 The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors Mol. Cell. 11 495-505 (Pubitemid 36293841)
26. Gautier I, Tramier M, Durieux C, Coppey J, Pansu R B, Nicolas J C, Kemnitz K and Coppey-Moisan M 2001 Homo-FRET microscopy in living cells to measure monomer-dimer transition of GFP-tagged proteins Biophys. J. 80 3000-8 (Pubitemid 32536682)
27. Hofman E G, Bader A N, Voortman J, Van Den Heuvel D J, Sigismund S, Verkleij A J, Gerritsen H C and Van Bergen EN Henegouwen P M 2010 Ligand-induced EGF receptor oligomerization is kinase-dependent and enhances internalization J. Biol. Chem. 285 39481-9
28. Honegger A M, Schmidt A, Ullrich A and Schlessinger J 1990 Evidence for epidermal growth factor (EGF)-induced intermolecular autophosphorylation of the EGF receptors in living cells Mol. Cell. Biol. 10 4035-44
29. Ichinose J, Murata M, Yanagida T and Sako Y 2004 EGF signalling amplification induced by dynamic clustering of EGFR Biochem. Biophys. Res. Commun. 324 1143-9 (Pubitemid 39361628)
30. Jorissen R N, Walker F, Pouliot N, Garrett T P J, Ward C W and Burgess A W 2003 Epidermal growth factor receptor: mechanisms of activation and signalling Exp. Cell Res. 284 31-53 (Pubitemid 36331965)
31. Jung G, MA Y, Prall B S and Fleming G R 2005 Ultrafast fluorescence depolarisation in the yellow fluorescent protein due to its dimerisation Chemphyschem 6 1628-32 (Pubitemid 41187247)
32. Jura N, Endres N F, Engel K, Deindl S, Das R, Lamers M H, Wemmer D E, Zhang X and Kuriyan J 2009a Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment Cell 137 1293-307
33. Jura N, Shan Y, Cao X, Shaw D E and Kuriyan J 2009b Structural analysis of the catalytically inactive kinase domain of the human EGF receptor 3 Proc. Natl Acad. Sci. USA 106 21608-13
34. Kastner J, Loeffler H H, Roberts S K, Martin-Fernandez M L and Winn M D 2009 Ectodomain orientation, conformational plasticity and oligomerization of ErbB1 receptors investigated by molecular dynamics J. Struct. Biol. 167 117-28
35. Kawashima N, Nakayama K, Itoh K, Itoh T, Ishikawa M and Biju V 2010 Reversible dimerization of EGFR revealed by single-molecule fluorescence imaging using quantum dots Chemistry 16 1186-92
36. Kozer N, Henderson C, Bailey M F, Rothacker J, Nice E C, Burgess A W and Clayton A H 2010 Creation and biophysical characterization of a high-affinity, monomeric EGF receptor ectodomain using fluorescent proteins Biochemistry 49 7459-66
37. Lidke D S, Nagy P, Barisas B G, Heintzmann R, Post J N, Lidke K A, Clayton A H, Arndt-Jovin D J and Jovin T M 2003 Imaging molecular interactions in cells by dynamic and static fluorescence anisotropy (rFLIM and emFRET) Biochem. Soc. Trans. 31 1020-7 (Pubitemid 37305039)
38. Liu P, Sudhaharan T, Koh R M, Hwang L C, Ahmed S, Maruyama I N and Wohland T 2007 Investigation of the dimerization of proteins from the epidermal growth factor receptor family by single wavelength fluorescence cross-correlation spectroscopy Biophys. J. 93 684-98 (Pubitemid 47057833)
39. MA X, Ahmed S and Wohland T 2011 EGFR activation monitored by SW-FCCS in live cells Frontiers Biosci. (Elite Ed) 3 22-32
40. Magde D, Wong R and Seybold P G 2002 Fluorescence quantum yields and their relation to lifetimes of rhodamine 6G and fluorescein in nine solvents: improved absolute standards for quantum yields Photochem. Photobiol. 75 327-34
41. Martin-Fernandez M, Clarke D T, Tobin M J, Jones S V and Jones G R 2002 Preformed oligomeric epidermal growth factor receptors undergo an ectodomain structure change during signaling Biophys. J. 82 2415-27 (Pubitemid 34441281)
42. Mattoon D, Klein P, Lemmon M A, Lax I and Schlessinger J 2004 The tethered configuration of the EGF receptor extracellular domain exerts only a limited control of receptor function Proc. Natl Acad. Sci. USA 101 923-8 (Pubitemid 38160560)
43. Moriki T, Maruyama H and Maruyama I N 2001 Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain J. Mol. Biol. 311 1011-26 (Pubitemid 32803717)
44. Morris C F, Young I G and Hapel A J 1990 Molecular and cellular biology of interleukin-3 Immunol. Ser. 49 177-214
45. Nagy P, Claus J, Jovin T M and Arndt-Jovin D J 2010 Distribution of resting and ligand-bound ErbB1 and ErbB2 receptor tyrosine kinases in living cells using number and brightness analysis Proc. Natl Acad. Sci. USA 107 16524-9
46. Ogiso H et al 2002 Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains Cell 110 775-87 (Pubitemid 35291060)
47. Patterson G H, Piston D W and Barisas B G 2000 Förster distances between green fluorescent protein pairs Anal. Biochem. 284 438-40
48. Pham E, Chiang J, LI I, Shum W and Truong K 2007 A computational tool for designing FRET protein biosensors by rigid-body sampling of their conformational space Structure 15 515-23 (Pubitemid 46702683)
49. Redford G I and Clegg R M 2005 Polar plot representation for frequency-domain analysis of fluorescence lifetimes J. Fluoresc. 15 805-15 (Pubitemid 41795606)
50. Saffarian S, LI Y, Elson E L and Pike L J 2007 Oligomerization of the EGF receptor investigated by live cell fluorescence intensity distribution analysis Biophys. J. 93 1021-31 (Pubitemid 47219793)
51. Sako Y, Minoghchi S and Yanagida T 2000 Single-molecule imaging of EGFR signalling on the surface of living cells Nat. Cell. Biol. 2 168-72
52. Schlessinger J 2002 Ligand-induced, receptor-mediated dimerization and activation of EGF receptor Cell 110 669-72 (Pubitemid 35283957)
53. Sorokin A, Lemmon M A, Ullrich A and Schlessinger J 1994 Stabilization of an active dimeric form of the epidermal growth factor receptor by introduction of an inter-receptor disulfide bond J. Biol. Chem. 269 9752-9 (Pubitemid 24196580)
54. Tramier M and Coppey-Moisan M 2008 Fluorescence anisotropy imaging microscopy for homo-FRET in living cells Methods Cell Biol. 85 395-414
55. Ullrich A et al 1984 Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells Nature 309 418-25 (Pubitemid 14102443)
56. Van Munster E B and Gadella T W JR 2004 Suppression of photobleaching-induced artifacts in frequency-domain FLIM by permutation of the recording order Cytometry A 58 185-94 (Pubitemid 38509180)
57. Vieira A V, Lamaze C and Schmid S L 1996 Control of EGF receptor signaling by clathrin-mediated endocytosis Science 274 2086-9 (Pubitemid 27020702)
58. Walker F, Hibbs M L, Zhang H H, Gonez L J and Burgess A W 1998 Biochemical characterization of mutant EGF receptors expressed in the hemopoietic cell line BaF/3 Growth Factors 16 53-67 (Pubitemid 28499711)
59. Walker F et al 2004 CR1/CR2 interactions modulate the functions of the cell surface epidermal growth factor receptor J. Biol. Chem. 279 22387-98 (Pubitemid 38679436)
60. Webb S E, Roberts S K, Needham S R, Tynan C J, Rolfe D J, Winn M D, Clarke D T, Barraclough R and Martin-Fernandez M L 2008 Single-molecule imaging and fluorescence lifetime imaging microscopy show different structures for high- and low-affinity epidermal growth factor receptors in A431 cells Biophys. J. 94 803-19 (Pubitemid 351162449)
61. Whitson K B, Beechem J M, Beth A H and Staros J V 2004 Preparation and characterization of Alexa Fluor 594-labeled epidermal growth factor for fluorescence resonance energy transfer studies: application to the epidermal growth factor receptor Anal. Biochem. 324 227-36 (Pubitemid 38019013)
62. Yarden Y and Schlessinger J 1987 Self-phosphorylation of epidermal growth factor receptor: evidence for a model of intermolecular allosteric activation Biochemistry 26 1434-42 (Pubitemid 17045874)
63. Yarden Y and Sliwkowski M X 2001 Untangling the ErbB signalling network Nat. Rev. Mol. Cell. Biol. 2 127-37 (Pubitemid 33674041)
64. Yeow E K and Clayton A H 2007 Enumeration of oligomerization states of membrane proteins in living cells by homo-FRET spectroscopy and microscopy: theory and application Biophys. J. 92 3098-104 (Pubitemid 46684571)
65. Yu X, Sharma K D, Takahashi T, Iwamoto R and Mekada E 2002 Ligand-independent dimer formation of epidermal growth factor receptor (EGFR) is a step separable from ligand-induced EGFR signaling Mol. Biol. Cell 13 2547-57 (Pubitemid 34831354)
66. Zacharias D A, Violin J D, Newton A C and Tsien R Y 2002 Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells Science 296 913-6 (Pubitemid 34464897)
67. 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 1137-49 (Pubitemid 43866200)