Different Epidermal Growth Factor Receptor (EGFR) agonists produce unique signatures for the recruitment of downstream signaling proteins

Journal of Biological Chemistry

Volumn 291, Issue 11, 2016, Pages 5528-5540

  Ronan, Tom ^a   Macdonald Obermann, Jennifer L ^a   Huelsmann, Lorel ^a,c   Bessman, Nicholas J ^b,d   Naegle, Kristen M ^a   Pike, Linda J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; LIGANDS; PRINCIPAL COMPONENT ANALYSIS; PROTEINS;

BIOLOGICAL EFFECTS; ENSEMBLE CLUSTERING; EPIDERMAL GROWTH FACTOR RECEPTORS; FRAGMENT COMPLEMENTATION; HEPARIN BINDING; NETWORK INTERACTION; RECEPTOR LIGANDS; SIGNALING PROTEINS;

CELL SIGNALING;

AMPHIREGULIN; BETACELLULIN; CBL PROTEIN; CRK LIKE PROTEIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR AGONIST; EPIGEN; EPIREGULIN; ERLOTINIB; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; LAPATINIB; LIGAND; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN GAB1; PROTEIN P52 SHC; PROTEIN P66 SHC; PROTEIN TYROSINE PHOSPHATASE SHP 2; SIGNALING PROTEIN; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CHO CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RECRUITMENT; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; PROTEIN-FRAGMENT COMPLEMENTATION ASSAY; AGONISTS; ANIMAL; CRICETULUS; DRUG EFFECTS; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CHO CELLS; CRICETULUS; EPIDERMAL GROWTH FACTOR; LIGANDS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84973345879     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.710087     Document Type: Article

References (44)

1. 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 cell surface epidermal growth factor receptor. A multidimensional microscopy analysis. J. Biol. Chem. 280, 30392-30399
2. 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 epidermal growth factor receptor (EGFR) oligomerization is kinase-dependent and enhances internalization. J. Biol. Chem. 285, 39481-39489
3. 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, 1011-1026
4. 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, 1021-1031
5. 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
6. 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
7. 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
8. 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
9. Citri, A., and Yarden, Y. (2006) EGF-ErbB signalling: toward the systems level. Nat. Rev. Mol. Cell Biol. 7, 505-516
10. Pawson, T. (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191-203
11. Levkowitz, G., Waterman, H., Ettenberg, S. A., Katz, M., Tsygankov, A. Y., Alroy, I., Lavi, S., Iwai, K., Reiss, Y., Ciechanover, A., Lipkowitz, S., and Yarden, Y. (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4, 1029-1040
12. Holgado-Madruga, M., Emlet, D. R., Moscatello, D. K., Godwin, A. K., and Wong, A. J. (1996) A Grb2-associated docking protein in EGF- and insulin-receptor signalling. Nature 379, 560-564
13. Gu, H., and Neel, B. G. (2003) The 'Gab' in signal transduction. Trends Cell Biol. 13, 122-130
14. Rodrigues, G. A., Falasca, M., Zhang, Z., Ong, S. H., and Schlessinger, J. (2000) A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol. Cell. Biol. 20, 1448-1459
15. Simister, P. C., and Feller, S. M. (2012) Order and disorder in large multisite docking proteins of the Gab family-implications for signalling complex formation and inhibitor design strategies. Mol. Biosyst. 9, 33-46
16. Wang, W., Xu, S., Yin, M., and Jin, Z. G. (2015) Essential roles of Gab1 tyrosine phosphorylation in growth factor-mediated signaling and angiogenesis. Int. J. Cardiol. 181, 180-184
17. 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
18. Saito, T., Okada, S., Ohshima, K., Yamada, E., Sato, M., Uehara, Y., Shimizu, H., Pessin, J. E., and Mori, M. (2004) Differential activation of epidermal growth factor (EGF) receptor downstream signaling pathways by betacellulin and EGF. Endocrinology 145, 4232-4243
19. Shin, H. S., Lee, H. J., Nishida, M., Lee, M.-S., Tamura, R., Yamashita, S., Matsuzawa, Y., Lee, I.-K., and Koh, G. Y. (2003) Betacellulin and amphiregulin induce upregulation of cyclin D1 and DNA synthesis activity through differential signaling pathways in vascular smooth muscle cells. Circ. Res. 93, 302-310
20. Streicher, K. L., Willmarth, N. E., Garcia, J., Boerner, J. L., Dewey, T. G., and Ethier, S. P. (2007) Activation of a nuclear factor-oκB/interleukin-1 positive feedback loop by amphiregulin in human breast cancer cells. Mol. Cancer Res. 5, 847-861
21. Wilson, K. J., Mill, C., Lambert, S., Buchman, J., Wilson, T. R., Hernandez-Gordillo, V., Gallo, R. M., Ades, L. M., Settleman, J., and Riese, D. J., 2nd (2012) EGFR ligands exhibit functional differences in models of paracrine and autocrine signaling. Growth Factors 30, 107-116
22. Macdonald-Obermann, J. L., Adak, S., Landgraf, R., Piwnica-Worms, D., and Pike, L. J. (2013) Dynamic analysis of the epidermal growth factor (EGF) receptor-ErbB2-ErbB3 protein network by luciferase fragment complementation imaging. J. Biol. Chem. 288, 30773-30784
23. Macdonald-Obermann, J. L., and Pike, L. J. (2014) Different epidermal growth factor (EGF) ligands show distinct kinetics and biased or partial agonism for homodimer and heterodimer formation. J. Biol. Chem. 289, 26178-26188
24. Yang, K. S., Ilagan, M. X., Piwnica-Worms, D., and Pike, L. J. (2009) Luciferase fragment complementation imaging of conformational changes in the EGF receptor. J. Biol. Chem. 284, 7474-7482
25. Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Prettenhofer, P., Weiss, R., Dubourg, V., Vanderplas, J., Passos, A., Cournapeau, D., Brucher, M., Perrot, M., and Duchesnay, E. (2011) Scikit-learn: machine learning in Python. J. Mach. Learn. Res. 12, 2825-2830
26. 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
27. Zheng, Y., Zhang, C., Croucher, D. R., Soliman, M. A., St.-Denis, N., Pasculescu, A., Taylor, L., Tate, S. A., Hardy, W. R., Colwill, K., Dai, A. Y., Bagshaw, R., Dennis, J. W., Gingras, A.-C., Daly, R. J., and Pawson, T. (2013) Temporal regulation of EGF signalling networks by the scaffold protein Shc1. Nature 499, 166-173
28. Beguinot, L., Lyall, R. M., Willingham, M. C., and Pastan, I. (1984) Down-regulation of the epidermal growth factor receptor in KB cells is due to receptor internalization and subsequent degradation in lysosomes. Proc. Natl. Acad. Sci. U.S.A. 81, 2384-2388
29. Knudsen, S. L., Mac, A. S., Henriksen, L., van Deurs, B., and Grøvdal, L. M. (2014) EGFR signaling patterns are regulated by its different ligands. Growth Factors 32, 155-163
30. Gilmore, J. L., Scott, J. A., Bouizar, Z., Robling, A., Pitfield, S. E., Riese, D. J., 2nd, and Foley, J. (2008) Amphiregulin-EGFR signaling regulates PTHrP gene expression in breast cancer cells. Breast Cancer Res. Treat. 110, 493-505
31. Curran, T. G., Zhang, Y., Ma, D. J., Sarkaria, J. N., and White, F. M. (2015) A multiplex method for absolute quantification of peptides and posttranslational modifications. Nat. Commun. 6, 5924
32. Guo, L., Kozlosky, C. J., Ericsson, L. H., Daniel, T. O., Cerretti, D. P., and Johnson, R. S. (2003) Studies of ligand-induced site-specific phosphorylation of epidermal growth factor receptor. J. Am. Soc. Mass Spectrom. 14, 1022-1031
33. Grayson, L. S., Hansbrough, J. F., Zapata-Sirvent, R. L., Dore, C. A., Morgan, J. L., and Nicolson, M. A. (1993) Quantitation of cytokine levels in skin graft donor site wound fluid. Burns 19, 401-405
34. Lemos-González, Y., Rodríguez-Berrocal, F. J., Cordero, O. J., Gómez, C., and Páez de la Cadena, M. (2007) Alteration of the serum levels of the epidermal growth factor receptor and its ligands in patients with nonsmall cell lung cancer and head and neck carcinoma. Br. J. Cancer 96, 1569-1578
35. Marti, U., Burwen, S. J., and Jones, A. L. (1989) Biological effects of epidermal growth factor, with emphasis on the gastrointestinal tract and liver: an update. Hepatology 9, 126-138
36. Blagoev, B., Ong, S.-E., Kratchmarova, I., and Mann, M. (2004) Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat. Biotechnol. 22, 1139-1145
37. Dengjel, J., Akimov, V., Olsen, J. V., Bunkenborg, J., Mann, M., Blagoev, B., and Andersen, J. S. (2007) Quantitative proteomic assessment of very early cellular signaling events. Nat. Biotechnol. 25, 566-568
38. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648
39. Zhang, Y., Wolf-Yadlin, A., Ross, P. L., Pappin, D. J., Rush, J., Lauffenburger, D. A., and White, F. M. (2005) Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol. Cell. Proteomics 4, 1240-1250
40. Steen, H., Kuster, B., Fernandez, M., Pandey, A., and Mann, M. (2002) Tyrosine phosphorylation mapping of the epidermal growth factor receptor signaling pathway. J. Biol. Chem. 277, 1031-1039
41. Kyono, W. T., de Jong, R., Park, R. K., Liu, Y., Heisterkamp, N., Groffen, J., and Durden, D. (1998) Differential interaction of CrkL with Cbl or C3G, Hef-1 and γ subunit immunoreceptor tyrosine-based activation motif in signaling of myeloid high affinity Fc receptor for IgG (FcγRI). J. Immunol. 161, 5555-5563
42. Sattler, M., Salgia, R., Shrikhande, G., Verma, S., Uemura, N., Law, S. F., Golemis, E. A., and Griffin, J. D. (1997) Differential signaling after β1 integrin ligation is mediated through binding of CrkL to p120Cbl and p110HEF1. J. Biol. Chem. 272, 14320-14326
43. Ingham, R. J., Holgado-Madruga, M., Siu, C., Wong, A. J., and Gold, M. R. (1998) The Gab1 protein is a docking site for multiple proteins involved in signaling by the B cell antigen receptor. J. Biol. Chem. 273, 30630-30637
44. Lecoq-Lafon, C., Verdier, F., Fichelson, S., Chrétien, S., Gisselbrecht, S., Lacombe, C., and Mayeux, P. (1999) Erythropoietin induces the tyrosine phosphorylation of Gab1 and its association with Shc, Shp2, SHIP and phosphatidylinositol 3-kinase. Blood 93, 2578-2585