Quantitation of the effect of ErbB2 on epidermal growth factor receptor binding and dimerization

Journal of Biological Chemistry

Volumn 287, Issue 37, 2012, Pages 31116-31125

  Li, Yu ^a   Macdonald Obermann, Jennifer ^a   Westfall, Corey ^a   Piwnica Worms, David ^a,b   Pike, Linda J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHOSPHORYLATION; COOPERATIVE BINDING; EPIDERMAL GROWTH FACTOR RECEPTORS; EPIDERMAL GROWTH FACTORS; HETERODIMERS; HOMODIMERS; KINASE ACTIVITY; SECOND LIGAND;

BIOCHEMISTRY; BIOMOLECULES; LIGANDS; PHOSPHORYLATION;

DIMERIZATION;

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HETERODIMER; HOMODIMER;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CONTROLLED STUDY; DIMERIZATION; DOWN REGULATION; ENZYME ACTIVITY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; RECEPTOR BINDING; STRUCTURE ACTIVITY RELATION;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; EPIDERMAL GROWTH FACTOR; MICE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2;

EID: 84866081605     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.373647     Document Type: Article

References (39)

1. Ullrich, A., Coussens, L., Hayflick, J. S., Dull, T. J., Gray, A., Tam, A. W., Lee, J., Yarden, Y., Libermann, T. A., Schlessinger, J., Downward, J., Mayes, E. L. V., Whittle, N., Waterfield, M. D., and Seeburg, P. H. (1984) Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309, 418-425
2. Ferguson, K. M. (2008) Structure-based view of epidermal growth factor receptor regulation. Annu. Rev. Biophys. 37, 353-373
3. Lemmon, M. A., and Schlessinger, J. (2010) Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134
4. Lemmon, M. A. (2009) Ligand-induced ErbB receptor dimerization. Exp. Cell Res. 315, 638-648
5. Wilson, K. J., Gilmore, J. L., Foley, J., Lemmon, M. A., and Riese, D. J., 2nd (2009) Functional selectivity of EGF family peptide growth factors. Implications for cancer. Pharmacol. Ther. 122, 1-8
6. 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, 39481-39489
7. 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, 684-698
8. Sako, Y., Minoghchi, S., and Yanagida, T. (2000) Single-molecule imaging of EGFR signalling on the surface of living cells. Nat. Cell Biol. 2, 168-172
9. Tao, R. H., and Maruyama, I. N. (2008) All EGF(ErbB) receptors have preformed homo- and heterodimeric structures in living cells. J. Cell Sci.121, 3207-3217
10. 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, 2547-2557
11. Yarden, Y., and Schlessinger, J. (1987) Self-phosphorylation of epidermal growth factor receptor. Evidence for a model of intermolecular allosteric activation. Biochemistry 26, 1434-1442
12. Graus-Porta, D., Beerli, R. R., Daly, J. M., and Hynes, N. E. (1997) ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 16, 1647-1655
13. Tzahar, E., Waterman, H., Chen, X., Levkowitz, G., Karunagaran, D., Lavi, S., Ratzkin, B. J., and Yarden, Y. (1996) A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16, 5276-5287
14. 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, 1137-1149
15. 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, 507-517
16. Garrett, T. P., 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., and Ward, C. W. (2002) Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor α. Cell 110, 763-773
17. Ogiso, H., Ishitani, R., Nureki, O., Fukai, S., Yamanaka, M., Kim, J. H., Saito, K., Sakamoto, A., Inoue, M., Shirouzu, M., and Yokoyama, S. (2002) Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 110, 775-787
18. Adak, S., DeAndrade, D., and Pike, L. J. (2011) The tethering arm of the EGF receptor is required for negative cooperativity and signal transduction. J. Biol. Chem. 286, 1545-1555
19. Lu, C., Mi, L. Z., Grey, M. J., Zhu, J., Graef, E., Yokoyama, S., and Springer, T. A. (2010) Structural evidence for loose linkage between ligand binding and kinase activation in the epidermal growth factor receptor. Mol. Cell. Biol. 30, 5432-5443
20. Macdonald, J. L., and Pike, L. J. (2008) Heterogeneity in EGF-binding affinities arises from negative cooperativity in an aggregating system. Proc. Natl. Acad. Sci. U.S.A. 105, 112-117
21. Macdonald-Obermann, J. L., and Pike, L. J. (2009) The intracellular juxtamembrane domain of the epidermal growth factor (EGF) receptor is responsible for the allosteric regulation of EGF binding. J. Biol. Chem. 284, 13570-13576
22. Karunagaran, D., Tzahar, E., Beerli, R. R., Chen, X., Graus-Porta, D., Ratzkin, B. J., Seger, R., Hynes, N. E., and Yarden, Y. (1996) ErbB-2 is a common auxiliary subunit of NDF and EGF receptors. Implications for breast cancer. EMBO J. 15, 254-264
23. Macdonald-Obermann, J. L., Piwnica-Worms, D., and Pike, L. J. (2012) Mechanics of EGF receptor/ErbB2 kinase activation revealed by luciferase fragment complementation imaging. Proc. Natl. Acad. Sci. U.S.A. 109, 137-142
24. Contreras, M. A., Bale, W. F., and Spar, I. L. (1983) Iodine monochloride (IC1) iodination techniques. Methods Enzymol. 92, 277-292
25. Yang, K. S., Macdonald-Obermann, J. L., Piwnica-Worms, D., and Pike, L. J. (2010) Asp-960/Glu-961 controls the movement of the C-terminal tail of the epidermal growth factor receptor to regulate asymmetric dimer formation. J. Biol. Chem. 285, 24014-24022
26. Yang, K. S., Ilagan, M. X., Piwnica-Worms, D., and Pike, L. J. (2009) Luciferase fragment complementation imaging of conformational changes in the epidermal growth factor receptor. J. Biol. Chem. 284, 7474-7482
27. Sarup, J. C., Johnson, R. M., King, K. L., Fendly, B. M., Lipari, M. T., Napier, M. A., Ullrich, A., and Shepard, H. M. (1991) Characterization of an antip185HER2 monoclonal antibody that stimulates receptor function and inhibits tumor cell growth. Growth Regul. 1, 72-82
28. Cho, H. S., Mason, K., Ramyar, K. X., Stanley, A. M., Gabelli, S. B., Denny, D. W., Jr., and Leahy, D. J. (2003) Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab. Nature 421, 756-760
29. Garrett, T. P., 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., and Ward, C. W. (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
30. Adak, S., Yang, K. S., Macdonald-Obermann, J., and Pike, L. J. (2011) The membrane-proximal intracellular domain of the epidermal growth factor receptor underlies negative cooperativity in ligand binding. J. Biol. Chem. 286, 45146-45155
31. Chantry, A. (1995) The kinase domain and membrane localization determine intracellular interactions between epidermal growth factor receptors. J. Biol. Chem. 270, 3068-3073
32. 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, 30392-30399
33. 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, 2415-2427
34. Luker, K. E., Smith, M. C., Luker, G. D., Gammon, S. T., Piwnica-Worms, H., and Piwnica-Worms, D. (2004) Kinetics of regulated protein-protein interactions revealed with firefly luciferase complementation imaging in cells and living animals. Proc. Natl. Acad. Sci. U.S.A. 101, 12288-12293
35. Offterdinger, M., and Bastiaens, P. I. (2008) Prolonged EGFR signaling by ERBB2-mediated sequestration at the plasma membrane. Traffic 9, 147-155
36. Wang, Z., Zhang, L., Yeung, T. K., and Chen, X. (1999) Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol. Biol. Cell 10, 1621-1636
37. Wada, T., Qian, X. L., and Greene, M. I. (1990) Intermolecular association of the p185neu protein and EGF receptor modulates EGF receptor function. Cell 61, 1339-1347
38. 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, 568-579
39. Liu, P., Cleveland, T. E., 4th, Bouyain, S., Byrne, P. O., Longo, P. A., and Leahy, D. J. (2012) A single ligand is sufficient to activate EGFR dimers. Proc. Natl. Acad. Sci. U.S.A. 109, 10861-10866