Two EGF molecules contribute additively to stabilization of the EGFR dimer

EMBO Journal

Volumn 16, Issue 2, 1997, Pages 281-294

  Lemmon, Mark A ^a,b   Bu, Zimei ^c   Ladbury, John E ^a,d   Zhou, Min ^a,e   Pinchasi, Dalia ^a   Lax, Irit ^a   Engelman, Donald M ^c   Schlessinger, Joseph ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c YALE UNIVERSITY   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e BRISTOL MYERS SQUIBB   (United States)

Author keywords

EGF receptor; Epidermal growth factor; Receptor dimerization; Titration calorimetry; X ray scattering

Indexed keywords

CYTOKINE RECEPTOR; DIMER; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA INTERFERON; RECEPTOR SUBUNIT;

ANIMAL CELL; ARTICLE; CALORIMETRY; CONTROLLED STUDY; LIGAND BINDING; MOLECULAR INTERACTION; MOLECULAR STABILITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TITRIMETRY; X RAY CRYSTALLOGRAPHY;

ANIMALS; CHO CELLS; CRICETINAE; EPIDERMAL GROWTH FACTOR; HUMANS; KINETICS; MODELS, CHEMICAL; PROTEIN CONFORMATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SCATTERING, RADIATION; STRUCTURE-ACTIVITY RELATIONSHIP;

ANIMALIA;

EID: 0031028273     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.2.281     Document Type: Article

References (71)

1. Banner, D.W., D'Arcy, A., Janes, W., Gentz, R., Schoenfeld, H.-J., Broger, C., Loetscher, H. and Lesslauer, W. (1993) Crystal structure of the soluble human 55 kDa TNF receptor-human TNFβ complex: implications for TNF receptor activation. Cell, 73, 431-445.
2. Barbacci, E.G., Guarino, B.C., Stroh, J.G., Singleton, D.H., Rosnack, K.J., Moyer, J.D. and Andrews, G.C. (1995) The structural basis for the specificity of epidermal growth factor and heregulin binding. J. Biol. Chem., 270, 9585-9589.
3. Beerli, R.R. and Hynes, N.E. (1996) Epidermal growth factor-related peptides activate distinct subsets of erbB receptors and differ in their biological activities. J. Biol. Chem., 271, 6071-6076.
4. Berkers, J.A.M., van Bergen en Henegouwen, P.M.P. and Boonstra, J. (1991) Three classes of epidermal growth factor on HeLa cells. J. Biol. Chem., 266, 922-927.
5. Brown, P.M., Debanne, M.T. Grothe, S., Bergsma, D., Caron, M., Kay, C. and O'Connor-McCourt, M.D. (1994) The extracellular domain of the epidermal growth factor receptor. Studies on the affinity and stoichiometry of binding, receptor dimerization and a binding-domain mutant. Eur. J. Biochem., 225, 223-233.
6. Canals, F. (1992) Signal transmission by epidermal growth factor receptor: coincidence of activation and dimerization. Biochemistry, 31, 4493-4501.
7. Carraway, K.L.,III and Cantley, L.C. (1994) A Neu acquaintance for erbB3 and erbB4: a role for receptor heterodimerization in growth signaling. Cell, 78, 5-8.
8. Cohen, B.D., Green, J.M. Foy, L. and Fell, H.P. (1996) HER4-mediated biological and biochemical properties in NIH 3T3 cells: evidence for HER1-HER4 heterodimers. J. Biol. Chem., 271, 4813-4818.
9. Cunningham, B.C., Ultsch, M. de Vos, A.M., Mulkerrin, M.G., Clauser, K.R. and Wells, J.A. (1991) Dimerization of the extracellular domain of the human growth hormone receptor by a single hormone molecule. Science, 254, 821-825.
10. de Vos, A.M., Ultsch, M. and Kossiakoff, A.A. (1992) Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science, 255, 306-312.
11. Fretto, L.J., Snape, A.J., Tomlinson, J.E., Seroogy, J.J., Wolf, D.L., LaRochelle, W.J. and Giese, N.A. (1993) Mechanism of platelet-derived growth factor (PDGF) AA, AB and BB binding to α and β PDGF receptor. J. Biol. Chem., 268, 3625-3631.
12. Fuh, G., Cunningham, B.C., Fukunaga, R., Nagata, S., Goeddel, D.V. and Wells, J.A. (1992) Rational design of potent antagonists to the human growth hormone receptor. Science, 256, 1677-1680.
13. Greenfield, C., Hiles, I., Waterfield, M.D., Federwisch, M., Wollmer, A., Blundell, T.L. and McDonald, N. (1989) Epidermal growth factor binding induces a conformational change in the external domain of its receptor. EMBO J., 8, 4115-4123.
14. Günther, N., Betzel, C. and Weber, W. (1990) The secreted form of the epidermal growth factor receptor: characterization and crystallization of the receptor-ligand complex. J. Biol. Chem., 265, 22082-22085.
15. Heldin, C.-H. (1995) Dimerization of cell surface receptors in signal transduction. Cell, 80, 213-223.
16. Heldin, C.-H., Ernlund, A., Rorsman, C. and Rönnstrand, L. (1989) Dimerization of B-type platelet-derived growth factor receptors occurs after ligand binding and is closely associated with receptor kinase activation. J. Biol. Chem., 264, 8905-8912.
17. Higashiyama, S., Abraham, J.A., Miller, J., Fiddes, J.C. and Klagsbrun, M. (1991) A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF Science, 251, 936-939.
18. Honneger, A.M., Schmidt, A., Ullrich, A. and Schlessinger, J. (1990) Evidence for epidermal growth factor (EGF)-induced intermolecular autophosphorylation in living cells. Mol. Cell. Biol., 10, 4035-4044.
19. Horan, T., Wen, J., Arakawa, T., Liu, N., Brankow, D., Hu, S., Ratzkin, B. and Philo, J.S. (1995) Binding of Neu differentiation factor with the extracellular domain of Her2 and Her3. J. Biol. Chem., 270, 24604-24608.
20. Horan, T., Wen, J., Narhi, L., Parker, V., Garcia, A., Arakawa, T. and Philo, J. (1996) Dimerization of the extracellular domain of granulocyte-colony stimulating factor receptor by ligand binding: a monovalent ligand induces 2:2 complexes. Biochemistry, 35, 4886-4896.
21. Hubbard, S.R., Wei, L., Ellis, L. and Hendrickson, W.A. (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature, 372, 746-754.
22. Hurwitz, D.R., Emanuel, S.L., Nathan, M.H., Sarver, N., Ullrich, A., Felder, S., Lax, I. and Schlessinger, J. (1991) EGF induces increased ligand binding affinity and dimerization of soluble epidermal growth factor (EGF) receptor extracellular domain. J. Biol. Chem., 266, 22035-22043.
23. Hynes, N.E. and Stern, D.F. (1994) The biology of erbB-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta, 1198, 165-184.
24. Karunagaran, D., Tzahar, E., Liu, N., Wen, D. and Yarden, Y. (1995) Neu differentiation factor inhibits EGF binding. J. Biol. Chem., 270, 9982-9990.
25. King, C.R., Borrello, I., Bellot, F., Comoglio, P. and Schlessinger, J. (1988) EGF binding to its receptor triggers a rapid tyrosine phosphorylation of the erbB-2 protein in the mammary tumor cell line SK-BR-3. EMBO J., 7, 1647-1651.
26. Kishimoto, T. Taga, T. and Akira, S. (1994) Cytokine signal transduction. Cell, 76, 252-262.
27. Kohda, D., Odaka, M., Lax, I., Kawasaki, H., Suzuki, K., Ullrich, A., Schlessinger, J. and Inagaki, F. (1993) A 40-kDa epidermal growth factor/transforming growth factor α-binding domain produced by limited proteolysis of the extracellular domain of the epidermal growth factor receptor. J. Biol. Chem., 268, 1976-1981.
28. Kossiakoff, A.A., Somers, W., Ultsch, M., Andow, K., Muller, Y.A. and De Vos, A.M. (1994) Comparison of the intermediate complexes of human growth hormone bound to the human growth hormone and prolactin receptors. Protein Sci., 3, 1697-1705.
29. Lax, I., Burgess, W.H., Bellot, F., Ullrich, A., Schlessinger, J. and Givol, D. (1988a) Localization of a major receptor-binding domain for epidermal growth factor by affinity labeling. Mol. Cell. Biol., 8, 1831-1834.
30. Lax, I., Johnson, A., Howk, R., Sap, J., Bellot, F., Winkler, M., Ullrich, A., Vennstrom, B., Schlessinger, J. and Givol, D. (1988b) Chicken epidermal growth factor (EGF) receptor: cDNA cloning, expression in mouse cells and differential binding of EGF and transforming growth factor alpha. Mol. Cell Biol., 8, 1970-1978.
31. Lax, I., Bellot, F., Howk, R., Ullrich, A., Givol, D. and Schlessinger, J. (1989) Functional analysis of the ligand binding site of EGF-receptor utilizing chicken/human receptor molecules. EMBO J., 8, 421-427.
32. Lax, I., Bellot, F. Honegger, A.M., Schmidt, A., Ullrich, A., Givol, D. and Schlessinger, J (1990) Domain deletion in the extracellular portion of the EGF-receptor reduces ligand binding and impairs cell surface expression.Cell Regulation, 1, 173-188.
33. Lax, I., Mitra, A.K., Ravera, C., Hurwitz, D.R., Rubinstein, M., Ullrich, A., Stroud, R.M. and Schlessinger, J. (1991a) Epidermal growth factor (EGF) induces oligomerization of soluble, extracellular, ligand-binding domain of EGF receptor. J. Biol. Chem., 266, 13828-13833.
34. Lax, I., Rischer, R., Ng, C, Segre, J., Ullrich, A., Givol, D. and Schlessinger, J. (1991b) Noncontiguous regions in the extracellular domain of EGF receptor define ligand-binding specificity. Cell Regulation, 2, 337-345.
35. Lemmon, M.A. and Schlessinger, J. (1994) Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem. Sci., 19, 459-463.
36. Lemmon, M.A., Pinchasi, D., Zhou, M., Lax, I. and Schlessinger, J. (1997) Kit receptor dimerization is driven by bivalent binding of stem cell factor. J. Biol. Chem., in press.
37. Lev, S., Yarden, Y. and Givol, D. (1992) A recombinant ectodomain of the receptor for the stem cell factor (SCF) retains ligand-induced receptor dimerization and antagonizes SCF-stimulated cellular responses. J. Biol. Chem., 267, 10866-10873.
38. Levitzki, A. and Schlessinger, J. (1974) Cooperativity in associating proteins. Monomer-dimer equilibrium coupled to ligand binding. Biochemistry, 13, 5214-5219.
39. Mohammadi, M., Schlessinger, J. and Hubbard, S.J. (1996) Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell. 86, 577-587.
40. Philo, J., Talvenheimo, J., Wen, J., Rosenfeld, R., Welcher, A. and Arakawa, T. (1994) Interactions of neurotrophin-3 (NT-3), brain-derived neurotrophic factor (BDNF) and the NT-3:BDNF heterodimer with the extracellular domains of the TrkB and TrkC receptors. J. Biol. Chem., 269, 27840-27846.
41. Philo, J.S., Aoki, K.H., Arakawa, T., Narhi, L.O. and Wen, J. (1996a) Dimerization of the extracellular domain of the erythropoietin (EPO) receptor by EPO: one high-affinity and one low-affinity interaction. Biochemistry, 35, 1681-1691.
42. Philo, J.S., Wen, J., Schwartz, M.G., Mendiaz, E.A. and Langley, K.E. (1996b) Human stem cell factor dimer forms a complex with two molecules of the extracellular domain of its receptor. Kit. J. Biol. Chem., 271, 6895-6902.
43. Plowman, G.D., Green, J.M., McDonald, V.L., Neubauer, M.G., Disteche, C.M., Todaro, G.J. and Shoyab, M. (1990) The amphiregulin gene encodes a novel epidermal growth factor-related protein with tumor-inhibitory activity. Mol. Cell. Biol., 10, 1969-1981.
44. c-neu and epidermal growth factor receptor associate into a structure composed of activated kinases. Proc. Natl Acad. Sci. USA, 89, 13330-13345.
45. Riese, D.J.,II, van Raaij, T.M., Plowman, G.D., Andrews, G.C. and Stern, D.F. (1995) The cellular response to neuregulins is governed by complex interactions of the erbB receptor family. Mol. Cell. Biol., 15, 5770-5776.
46. Riese, D.J.,II, Bermingham, Y., van Raaij, T.M., Buckley, S., Plowman, G.D. and Stem, D.F. (1996) Betacellulin activates the epidermal growth factor and erbB4 and induces cellular response patterns distinct from those stimulated by epidermal growth factor or neuregulin-β. Oncogene, 12, 345-353.
47. Schlessinger, J. (1979) Receptor aggregation as a mechanism for transmembrane signaling: Models for hormone action. In De Lisi, C. and Blumenthal, R. (eds). Physical Chemistry of Cell Surface Events in Cellular Regulation. Elsevier, pp. 89-118.
48. Schlessinger, J. (1988) The epidermal growth factor receptor as a multifunctional allosteric protein. Biochemistry, 27, 3119-3123.
49. Schlessinger, J. and Ullrich, A. (1992) Growth factor signaling by receptor tyrosine kinases. Neuron, 9, 383-391.
50. Schlessinger, J., Lax, I. and Lemmon, M.A. (1995) Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell, 83, 357-360.
51. Semenyuk, A.V. and Svergun, I. (1991) GNOM - a program package for small-angle scattering data processing. J. Appl. Crystallogr., 24, 537-540.
52. Sherrill, J.M. and Kyte, J. (1996) Activation of epidermal growth factor receptor by epidermal growth factor. Biochemistry, 35, 5705-5718.
53. Shing, Y., Christofori, G., Hanahan, D., Ono, Y., Sasada, R., Igarashi, K. and Folkman, J. (1993) Betacellulin: a mitogen from pancreatic beta cell tumors. Science, 259, 1604-1607.
54. Soltoff, S.R. Carraway, K.L.,III, Prigent, S.A., Gullick, W.G. and Cantley, L.C. (1994) ErbB3 is involved in activation of phosphatidyl-inositol 3-kinase by epidermal growth factor. Mol. Cell. Biol., 14, 3550-3558.
55. Spivak-Kroizman, T., Rotin, D., Pinchasi, D., Ullrich, A., Schlessinger, J. and Lax, I. (1992) Heterodimerization of c-erbB2 with different epidermal growth factor receptor mutants elicits stimulatory or inhibitory responses. J. Biol. Chem., 267, 8056-8063.
56. Spivak-Kroizman, T. et al. (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation and cell proliferation. Cell, 79, 1015-1024.
57. Sprang, S.R. and Bazan, J.F. (1993) Cytokine structural taxonomy and mechanisms of receptor engagement. Curr. Opin. Struct. Biol., 3, 815-827.
58. Stern, D.F. and Kamps, M.P. (1988) EGF-stimulated tyrosine phosphorylation of p185neu: a potential model for receptor interactions. EMBO J., 7, 995-1001.
59. Toyoda, H., Komurasaki, T., Uchida, D., Takayama, Y. Isobe, T., Okuyama, T. and Hanada, K. (1995) Epiregulin. A novel epidermal growth factor with mitogenic activity for rat primary hepatocytes. J. Biol. Chem., 270, 7495-7500.
60. Walter, M.R., Windsor, W.T., Nagabhushan, T.L., Lundell, D.J., Lunn, C.A., Zauodny, P.J. and Narula, S.K. (1995) Crystal structure of a complex between interferon-γ and its soluble high-affinity receptor. Nature, 376, 230-235.
61. Ward, C.W., Hoyne, P.A. and Flegg, R.H. (1995) Insulin and epidermal growth factor receptors contain the cysteine repeat motif found in the tumor necrosis factor receptor. Proteins: Structure, Funct. Genet., 22, 141-153.
62. Weber, W., Bertics, P.J. and Gill, G.N. (1984) Immunoaffinity purification of the epidermal growth factor receptor: stoichiometry of binding and kinetics of self-phosphorylation. J. Biol. Chem., 259, 14631-14636.
63. Wells, J.A. (1996) Binding in the growth hormone receptor complex. Proc. Natl Acad. Sci. USA, 93, 1-6.
64. Wiseman, T., Williston, S., Brandts, J.F. and Lin, L.-N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem., 179, 131-137.
65. Wofsy, C. Goldstein, B., Lund, K. and Wiley, H.S. (1992) Implications of epidermal growth factor (EGF) induced EGF receptor aggregation. Biophys. J., 63, 98-100.
66. Woltjer, R.L., Lukas, T.L. and Staros, J.V. (1992) Direct identification of residues of the epidermal growth factor receptor in close proximity to the amino terminus of bound epidermal growth factor. Proc. Natl Acad. Sci. USA, 89, 7801-7805.
67. Wu, D.G., Wang, L.H., Chi, Y., Sato, G.H. and Sato, J.D. (1990) Human epidermal growth factor receptor residue covalently cross-linked to epidermal growth factor. Proc. Natl Acad. Sci. USA, 87, 3151-3155.
68. Yarden, Y. and Schlessinger, J. (1987a) Self-phosphorylation of epidermal growth factor receptor: evidence for a model of intermolecular allosteric activation. Biochemistry, 26, 1434-1442.
69. Yarden, Y. and Schlessinger, J. (1987b) Epidermal growth factor induces rapid, reversible aggregation of the purified epidermal growth factor receptor. Biochemistry, 26, 1443-1451.
70. Yarden, Y. Harari, I. and Schlessinger, J. (1985) Purification of an active EGF receptor kinase with monoclonal antireceptor antibodies. J. Biol. Chem., 260, 315-319.
71. Zhou, M. Felder, S., Rubinstein, M., Hurwitz, D.R., Ullrich, A., Lax, I. and Schlessinger, J. (1993) Real-time measurements of kinetics of EGF binding to soluble EGF receptor monomers and dimers support the dimerization model for receptor activation. Biochemistry, 32, 8193-8198.