Preparation and characterization of Alexa Fluor 594-labeled epidermal growth factor for fluorescence -resonance energy transfer studies: Application to the epidermal growth factor receptor

Analytical Biochemistry

Volumn 324, Issue 2, 2004, Pages 227-236

  Whitson, Kristin B ^a   Beechem, Joseph M ^b,c   Beth, Albert H ^b   Staros, James V ^a,d  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MOLECULAR PROBES INC   (United States)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

Dimerization; EGF receptor; Epidermal growth factor; Fluorescence resonance energy transfer; Homo transfer; Oligomerization; Time resolved fluorescence spectroscopy

Indexed keywords

BINDING ENERGY; DIMERIZATION; EMISSION SPECTROSCOPY; ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; FORSTER RESONANCE ENERGY TRANSFER; LIGANDS; OLIGOMERIZATION; OLIGOMERS; RESONANCE;

EGF RECEPTOR; EPIDERMAL GROWTH FACTORS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HOMO TRANSFER; TIME-RESOLVED FLUORESCENCE SPECTROSCOPY;

X RAY CRYSTALLOGRAPHY;

DIMER; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; LIGAND; OLIGOMER;

ARTICLE; BINDING SITE; BIOLOGY; CELL LINE; CONTROLLED STUDY; CRYSTALLOGRAPHY; EXCITATION; EXPERIMENTAL MODEL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; LIGAND BINDING; MEMBRANE VESICLE; MOLECULAR PROBE; OLIGOMERIZATION; PHYSICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SYNTHESIS; TIME; X RAY CRYSTALLOGRAPHY;

ALEXA; HOMO; MURINAE;

EID: 0346362264     PISSN: 00032697     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ab.2003.09.023     Document Type: Article

References (70)

1. Savage C.R. Jr., Inagami T., Cohen S. The primary structure of epidermal growth factor. J. Biol. Chem. 247:1972;7612-7621.
2. Jorissen R.N., Walker F., Pouliot N., Garrett T.P.J., Ward C.W., Burgess A.W. Epidermal growth factor receptor: mechanisms of activation and signaling. Exp. Cell Res. 284:2003;31-53.
3. Hackel P.O., Zwick E., Prenzel N., Ullrich A. Epidermal growth factor receptors: critical mediators of multiple receptor pathways. Curr. Opin. Cell Biol. 11:1999;184-189.
4. Stein R.A., Staros J.V. Evolutionary analysis of the ErbB receptor and ligand families. J. Mol. Evol. 50:2000;397-412.
5. Schechter A.L., Hung M.C., Vaidyanathan L., Weinberg R.A., Yang-Feng T.L., Francke U., Ullrich A., Coussens L. The neu gene: an erbB-homologous gene distinct from and unlinked to the gene encoding the EGF receptor. Science. 229:1985;976-978.
6. Kraus M.H., Issing W., Miki T., Popescu N.C., Aaronson S.A. Isolation and characterization of ERBB3, a third member of the ERBB/epidermal growth factor receptor family: evidence for overexpression in a subset of human mammary tumors. Proc. Natl. Acad. Sci. USA. 86:1989;9193-9197.
7. Plowman G.D., Culouscou J.M., Whitney G.S., Green J.M., Carlton G.W., Foy L., Neubauer M.G., Shoyab M. Ligand-specific activation of HER4/p180erbB4, a fourth member of the epidermal growth factor receptor family. Proc. Natl. Acad. Sci. USA. 90:1993;1746-1750.
8. Cho H-S., Leahy D.J. Structure of the extracellular region of HER3 reveals an interdomain tether. Science. 297:2002;1330-1333.
9. Ferguson K.M., Berger M.B., Mendrola J.M., Cho H-S., Leahy D.J., Lemmon M.A. EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol. Cell. 11:2003;507-517.
10. Garrett T.P.J., McKern N.M., Lou M., Elleman T.C., Adams T.E., Lovrecz G.O., Kofler M., Jorissen R.N., Nice E.C., Burgess A.W., Ward C.W. The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors. Mol. Cell. 11:2003;495-505.
11. Ogiso H., Ishitani R., Nureki O., Fukai S., Yamanaka M., Kim J-H., Saito K., Sakamoto A., Inoue M., Shirouzu M., Yokoyama S. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell. 110:2002;775-787.
12. Garrett T.P.J., McKern N.M., Lou M., Elleman T.C., Adams T.E., Lovrecz G.O., Zhu H.-J., Walker F., Frenkel M.J., Hoyne P.A., Jorissen R.N., Nice E.C., Burgess A.W., Ward C.W. Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor α Cell. 110:2002;763-773.
13. Stamos J., Sliwkowski M.X., Eigenbrot C. Structure of the epidermal growth factor receptor kinase domain alone and in complex with a 4-anilinoquinazoline inhibitor. J. Biol. Chem. 277:2002;46265-46272.
14. Lemmon M.A., Bu Z., Ladbury J.E., Zhou M., Pinchasi D., Lax I., Engelman D.M., Schlessinger J. Two EGF molecules contribute additively to stabilization of the EGFR dimer. EMBO J. 16:1997;281-294.
15. Ferguson K.M., Darling P.J., Mohan M.J., Macatee T.L., Lemmon M.A. Extracellular domains drive homo- but not hetero-dimerization of erbB receptors. EMBO J. 19:2000;4632-4643.
16. Fanger B.O., Austin K.S., Earp H.S., Cidlowski J.A. Cross-linking of epidermal growth factor receptors in intact cells: detection of initial stages of receptor clustering and determination of molecular weight of high affinity receptors. Biochemistry. 25:1986;6414-6420.
17. Cochet C., Kashles O., Chambaz E.M., Borrello I., King C.R., Schlessinger J. Demonstration of epidermal growth factor-induced receptor dimerization in living cells using a chemical covalent cross-linking agent. J. Biol. Chem. 263:1988;3290-3295.
18. Lemmon M.A., Schlessinger J. Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem. Sci. 19:1994;459-463.
19. Fanger B.O., Stephens J.E., Staros J.V. High-yield trapping of EGF-induced receptor dimers by chemical cross-linking. FASEB J. 3:1989;71-75.
20. Brennan P.J., Kumogai T., Berezov A., Murali R., Greene M.I. HER2/Neu: mechanisms of dimerization/oligomerization. Oncogene. 19:2000;6093-6101.
21. van Belzen N., Rijken P.J., Hage W.J., de Laat S.W., Verkleij A.J., Boonstra J. Direct visualization and quantitative analysis of epidermal growth factor-induced receptor clustering. J. Cell Physiol. 134:1988;413-420.
22. Stein R.A., Wilkinson J.C., Guyer C.A., Staros J.V. An analytical approach to the measurement of equilibrium binding constants: application to EGF binding to EGF receptors in intact cells measured by flow cytometry. Biochemistry. 40:2001;6142-6154.
23. Pramanik A., Rigler R. Ligand-receptor interactions in the membrane of cultured cells monitored by fluorescence correlation spectroscopy. Biol. Chem. 382:2001;371-378.
24. Carraway 3rd K.L., Cerione R.A. Fluorescent-labeled growth factor molecules serve as probes for receptor binding and endocytosis. Biochemistry. 32:1993;12039-12045.
25. Rousseau D.L. Jr., Staros J.V., Beechem J.M. The interaction of epidermal growth factor with its receptor in A431 cell membranes: a stopped-flow fluorescence anisotropy study. Biochemistry. 34:1995;14508-14518.
26. Chung J.C., Sciaky N., Gross D.J. Heterogeneity of epidermal growth factor binding kinetics on individual cells. Biophys. J. 73:1997;1089-1102.
27. Wilkinson J.C., Stein R.A., Guyer C.A., Beechem J.M., Staros J.V. Real-time kinetics of ligand/cell surface receptor interactions in living cells: binding of epidermal growth factor to the epidermal growth factor receptor. Biochemistry. 40:2001;10230-10242.
28. Hillman G.M., Schlessinger J. Lateral diffusion of epidermal growth factor complexed to its surface receptors does not account for the thermal sensitivity of patch formation and endocytosis. Biochemistry. 21:1982;1667-1672.
29. Haigler H., Ash J.F., Singer S.J., Cohen S. Visualization by fluorescence of the binding and internalization of epidermal growth factor in human carcinoma cells A-431. Proc. Natl. Acad. Sci. USA. 75:1978;3317-3321.
30. Martin-Fernandez M.L., Clarke D.T., Tobin M.J., Jones G.R. Real-time studies of the interactions between epidermal growth factor and its receptor during endocytic trafficking. Cell. Mol. Biol. 46:2000;1103-1112.
31. Sako Y., Minoghchi S., Yanagida T. Single-molecule imaging of EGFR signaling on the surface of living cells. Nat. Cell Biol. 2:2000;168-172.
32. Carraway 3rd K.L., Koland J.G., Cerione R.A. Visualization of epidermal growth factor (EGF) receptor aggregation in plasma membranes by fluorescence resonance energy transfer. J. Biol. Chem. 264:1989;8699-8707.
33. Carraway 3rd K.L., Cerione R.A. Comparison of epidermal growth factor (EGF) receptor-receptor interactions in intact A431 cells and isolated plasma membranes. J. Biol. Chem. 266:1991;8899-8906.
34. Gadella T.W.J., Jovin T.M. 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. 129:1995;1543-1558.
35. Martin-Fernandez M., Clarke D.T., Tobin M.J., Jones S.V., Jones G.R. Preformed oligomeric epidermal growth factor receptors undergo an ectodomain structure change during signaling. Biophys. J. 82:2002;2415-2427.
36. Wilkinson J.C., Beechem J.M., Staros J.V. A stopped-flow fluorescence anisotropy method for measuring hormone binding and dissociation kinetics with cell-surface receptors in living cells. J. Recept. Signal Transduct. Res. 22:2002;357-371.
37. Savage C.R., Cohen S. Epidermal growth factor and a new derivative. Rapid isolation procedures and biological and chemical characterization. J. Biol. Chem. 247:1972;7609-7611.
38. Cohen S., Ushiro H., Stoscheck C., Chinkers M. A native 170,000 epidermal growth factor receptor-kinase complex from shed plasma membrane vesicles. J. Biol. Chem. 257:1982;1523-1531.
39. Woltjer R.L., Staros J.V. Effects of sulfhydryl modification reagents on the kinase activity of the epidermal growth factor receptor. Biochemistry. 36:1997;9911-9916.
40. Lakowicz J.R. Principles of Fluorescence Spectroscopy. second ed. 1999;Kluwer Academic Publishers, New York.
41. ′ -nearest neighbors on the insertion kinetics of the fluorescent nucleotide analog 2-aminopurine by Klenow fragment Biochemistry. 32:1993;11247-11258.
42. Perez-Howard G.M., Weil P.A., Beechem J.M. Yeast TATA binding protein interaction with DNA: fluorescence determination of oligomeric state, equilibrium binding, on-rate, and dissociation kinetics. Biochemistry. 34:1995;8005-8017.
43. Beechem J.M., Gratton E., Ameloot M., Knutson J.R., Brand L. Lakowicz J.R. Topics of Fluorescence Spectroscopy. vol. 2:1991;241-301 Plenum Press, New York.
44. Cullander C. Imaging in the far-red with electronic light microscopy: requirements and limitations. J. Microsc. 176:1994;281-286.
45. Haigler H.T., McKanna J.A., Cohen S. Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J. Cell Biol. 81:1979;382-395.
46. Woltjer R.L., Weclas-Henderson L., Papayannopoulos I.A., Staros J.V. High-yield covalent attachment of epidermal growth factor to its receptor by kinetically controlled, stepwise affinity cross-linking. Biochemistry. 31:1992;7341-7346.
47. Rousseau D.L. Jr., Guyer C.A., Beth A.H., Papayannopoulos I.A., Wang B., Wu R., Mroczkowski B., Staros J.V. Preparation and characterization of a bifunctionally spin-labeled mutant of murine epidermal growth factor for saturation-transfer electron paramagnetic resonance studies of the growth factor/receptor complex. Biochemistry. 32:1993;7893-7903.
48. Lillo M.P., Szpikowska B.K., Mas M.T., Sutin J.D., Beechem J.M. Real-time measurement of multiple intramolecular distances during protein folding reactions: a multisite stopped-flow fluorescence energy-transfer study of yeast phosphoglycerate kinase. Biochemistry. 36:1997;11273-11281.
49. Gregory H. Isolation and structure of urogastrone and its relationship to epidermal growth factor. Nature. 257:1975;325-327.
50. Der-Balian G.P., Kameda N., Rowley G.L. Fluorescein labeling of Fab' while preserving single thiol. Anal. Biochem. 173:1988;59-63.
51. Haugland R.P. Handbook of Fluorescent Probes and Research Chemicals. sixth ed. 1996;Molecular Probes, Eugene, OR.
52. Panchuk-Voloshina N., Haugland R.P., Bishop-Stewart J., Bhalgat M.K., Millard P.J., Mao F., Leung W-Y., Haugland R.P. Alexa Dyes, a series of new fluorescent dyes that yield exceptionally bright, photostable conjugates. J. Histol. Cytochem. 47:1999;1179-1188.
53. Montelione G.T., Wuthrich K., Nice E.C., Burgess A.W., Scheraga H.A. Solution structure of murine epidermal growth factor: determination of the polypeptide backbone chain-fold by nuclear magnetic resonance and distance geometry. Proc. Natl. Acad. Sci. USA. 84:1987;5226-5230.
54. Ghiron C.A., Eftink M.R., Engler D.A., Niyogi S.K. Fluorescence studies with human epidermal growth factor. Photochem. Photobiol. 55:1992;29-34.
55. Blackman S.M., Piston D.W., Beth A.H. Oligomeric state of human erythrocyte band 3 measured by fluorescence resonance energy homotransfer. Biophys. J. 75:1998;1117-1130.
56. McVey M., Ramsay D., Kellett E., Rees S., Wilson S., Pope A.J., Milligan G. Monitoring receptor oligomerization using time-resolved fluorescence resonance energy transfer and bioluminescence resonance energy transfer. The human delta-opioid receptor displays constitutive oligomerization at the cell surface, which is not regulated by receptor occupancy. J. Biol. Chem. 276:2001;14092-14099.
57. Pierce J.H., Ruggiero M., Fleming T.P., Di Fiore P.P., Greenberger J.S., Varticovski L., Schlessinger J., Rovera G., Aaronson S.A. Signal transduction through the EGF receptor transfected in IL-3-dependent hematopoietic cells. Science. 239:1988;628-631.
58. Wang L.M., Kuo A., Alimandi M., Veri M.C., Lee C.C., Kapoor V., Ellmore N., Chen X.H., Pierce J.H. ErbB2 expression increases the spectrum and potency of ligand-mediated signal transduction through ErbB4. Proc. Natl. Acad. Sci. USA. 95:1998;6809-6814.
59. Sorkin A., Krolenko S., Kudrjavtceva N., Lazebnik J., Teslenko L., Soderquist A., Nikolsky N. Recycling of epidermal growth factor-receptor complexes in A431 cells: identification of dual pathways. J. Cell Biol. 112:1991;55-63.
60. Tanaka F., Mataga N. Theory of time-dependent photo-selection in interacting fixed media. Photochem. Photobiol. 29:1979;1091-1097.
61. Lu H.S., Chai J.J., Li M., Huang B.R., He C.H., Bi R.C. Crystal structure of human epidermal growth factor and its dimerization. J. Biol. Chem. 276:2001;34913-34917.
62. Canals F. Signal transmission by epidermal growth factor receptor: coincidence of activation and dimerization. Biochemistry. 31:1992;4493-4501.
63. Honegger A.M., Kris R.M., Ullrich A., Schlessinger J. Evidence that autophosphorylation of solubilized receptors for epidermal growth factor is mediated by intermolecular cross-phosphorylation. Proc. Natl. Acad. Sci. USA. 86:1989;925-929.
64. Lammers R., Van Obberghen E., Ballotti R., Schlessinger J., Ullrich A. Transphosphorylation as a possible mechanism for insulin and epidermal growth factor receptor activation. J. Biol. Chem. 265:1990;16886-16890.
65. Kashles O., Yarden Y., Fischer R., Ullrich A., Schlessinger J. A dominant negative mutation suppresses the function of normal epidermal growth factor receptors by heterodimerization. Mol. Cell Biol. 11:1991;1454-1463.
66. Moriki T., Maruyama H., Maruyama I.N. Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain. J. Mol. Biol. 311:2001;1011-1026.
67. Sorkin A., Carpenter G. Interaction of activated EGF receptors with coated pit adaptins. Science. 261:1993;612-615.
68. Sorkin A. Endocytosis and intracellular sorting of receptor tyrosine kinases. Front. Biosci. 3:1998;d729-d738.
69. Carpenter G. The EGF receptor: a nexus for trafficking and signaling. Bioessays. 22:2000;697-707.
70. Pike L.J., Miller J.M. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J. Biol. Chem. 273:1998;22298-22304.