Live-cell fluorescence imaging reveals high stoichiometry of Grb2 binding to the EGF receptor sustained during endocytosis

Journal of Cell Science

Volumn 127, Issue 2, 2014, Pages 432-444

  Fortian, Arola ^a   Sorkin, Alexander ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

EGF receptor; Endocytosis; Endosome; Grb2

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; RHODAMINE; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FLUORESCENCE MICROSCOPY; HELA CELL; IMAGE ANALYSIS; INTERNALIZATION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; STOICHIOMETRY; THREE DIMENSIONAL IMAGING; TIME LAPSE IMAGING;

EGF RECEPTOR; ENDOCYTOSIS; ENDOSOME; GRB2;

BACTERIAL PROTEINS; CELL SURVIVAL; ENDOCYTOSIS; ENDOSOMES; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GRB2 ADAPTOR PROTEIN; HELA CELLS; HUMANS; KINETICS; LIGANDS; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING;

EID: 84892496733     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.137786     Document Type: Article

References (57)

1. 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.
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, 568-579.
3. Baass, P. C., Di Guglielmo, G. M., Authier, F., Posner, B. I. and Bergeron, J. J. (1995). Compartmentalized signal transduction by receptor tyrosine kinases. Trends Cell Biol. 5, 465-470.
4. Batzer, A. G., Rotin, D., Ureña, J. M., Skolnik, E. Y. and Schlessinger, J. (1994). Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol. Cell. Biol. 14, 5192-5201.
5. Brankatschk, B., Wichert, S. P., Johnson, S. D., Schaad, O., Rossner, M. J. and Gruenberg, J. (2012). Regulation of the EGF transcriptional response by endocytic sorting. Sci. Signal. 5, ra21.
6. Carpenter, G. and Cohen, S. (1979). Epidermal growth factor. Annu. Rev. Biochem. 48, 193-216.
7. Chen, Z., Gibson, T. B., Robinson, F., Silvestro, L., Pearson, G., Xu, B., Wright, A., Vanderbilt, C. and Cobb, M. H. (2001). MAP kinases. Chem. Rev. 101, 2449-2476.
8. Chook, Y. M., Gish, G. D., Kay, C. M., Pai, E. F. and Pawson, T. (1996). The Grb2-mSos1 complex binds phosphopeptides with higher affinity than Grb2. J. Biol. Chem. 271, 30472-30478.
9. Di Fiore, P. P. and De Camilli, P. (2001). Endocytosis and signaling. an inseparable partnership. Cell 106, 1-4.
10. Di Guglielmo, G. M., Baass, P. C., Ou, W.-J., Posner, B. I. and Bergeron, J. J. M. (1994). Compartmentalization of SHC, GRB2 and mSOS, and hyperphosphorylation of Raf-1 by EGF but not insulin in liver parenchyma. EMBO J. 13, 4269-4277.
11. Diwan, B. A., Ramakrishna, G., Anderson, L. M. and Ramljak, D. (2000). Overexpression of Grb2 in inflammatory lesions and preneoplastic foci and tumors induced by N-nitrosodimethylamine in Helicobacter hepaticus-infected and-noninfected A/J mice. Toxicol. Pathol. 28, 548-554.
12. Ebner, R. and Derynck, R. (1991). Epidermal growth factor and transforming growth factor-alpha: differential intracellular routing and processing of ligandreceptor complexes. Cell Regul. 2, 599-612.
13. Eden, E. R., Huang, F., Sorkin, A. and Futter, C. E. (2012). The role of EGF receptor ubiquitination in regulating its intracellular traffic. Traffic 13, 329-337.
14. French, A. R., Sudlow, G. P., Wiley, H. S. and Lauffenburger, D. A. (1994). Postendocytic trafficking of epidermal growth factor-receptor complexes is mediated through saturable and specific endosomal interactions. J. Biol. Chem. 269, 15749-15755.
15. French, A. R., Tadaki, D. K., Niyogi, S. K. and Lauffenburger, D. A. (1995). Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J. Biol. Chem. 270, 4334-4340.
16. Galperin, E., Verkhusha, V. V. and Sorkin, A. (2004). Three-chromophore FRET microscopy to analyze multiprotein interactions in living cells. Nat. Methods 1, 209-217.
17. Gillham, H., Golding, M. C., Pepperkok, R. and Gullick,W. J. (1999). Intracellular movement of green fluorescent protein-tagged phosphatidylinositol 3-kinase in response to growth factor receptor signaling. J. Cell Biol. 146, 869-880.
18. Goh, L. K., Huang, F., Kim, W., Gygi, S. and Sorkin, A. (2010). Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J. Cell Biol. 189, 871-883.
19. Haugh, J. M. and Meyer, T. (2002). Active EGF receptors have limited access to PtdIns(4,5)P(2) in endosomes: implications for phospholipase C and PI 3-kinase signaling. J. Cell Sci. 115, 303-310.
20. Huang, F. and Sorkin, A. (2005). Growth factor receptor binding protein 2-mediated recruitment of the RING domain of Cbl to the epidermal growth factor receptor is essential and sufficient to support receptor endocytosis. Mol. Biol. Cell 16, 1268-1281.
21. Imai, Y., Leung, C. K., Friesen, H. G. and Shiu, R. P. (1982). Epidermal growth factor receptors and effect of epidermal growth factor on growth of human breast cancer cells in long-term tissue culture. Cancer Res. 42, 4394-4398.
22. Jiang, X. and Sorkin, A. (2002). Coordinated traffic of Grb2 and Ras during epidermal growth factor receptor endocytosis visualized in living cells. Mol. Biol. Cell 13, 1522-1535.
23. Jiang, X., Huang, F., Marusyk, A. and Sorkin, A. (2003). Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 14, 858-870.
24. Johannessen, L. E., Haugen, K. E., Østvold, A. C., Stang, E. and Madshus, I. H. (2001). Heterodimerization of the epidermal-growth-factor (EGF) receptor and ErbB2 and the affinity of EGF binding are regulated by different mechanisms. Biochem. J. 356, 87-96.
25. Kranenburg, O., Verlaan, I. and Moolenaar, W. H. (1999). Dynamin is required for the activation of mitogen-activated protein (MAP) kinase by MAP kinase kinase. J. Biol. Chem. 274, 35301-35304.
26. Lemmon, M. A. and Schlessinger, J. (2010). Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134.
27. Lemmon, M. A., Ladbury, J. E., Mandiyan, V., Zhou, M. and Schlessinger, J. (1994). Independent binding of peptide ligands to the SH2 and SH3 domains of Grb2. J. Biol. Chem. 269, 31653-31658.
28. Low-Nam, S. T., Lidke, K. A., Cutler, P. J., Roovers, R. C., van Bergenen Henegouwen, P. M., Wilson, B. S. and Lidke, D. S. (2011). ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding. Nat. Struct. Mol. Biol. 18, 1244-1249.
29. Lowenstein, E. J., Daly, R. J., Batzer, A. G., Li, W., Margolis, B., Lammers, R., Ullrich, A., Skolnik, E. Y., Bar-Sagi, D. and Schlessinger, J. (1992). The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70, 431-442.
30. Matsuda, M., Paterson, H. F., Rodriguez, R., Fensome, A. C., Ellis, M. V., Swann, K. and Katan, M. (2001). Real time fluorescence imaging of PLC gamma translocation and its interaction with the epidermal growth factor receptor. J. Cell Biol. 153, 599-612.
31. Miaczynska, M., Pelkmans, L. and Zerial, M. (2004). Not just a sink: endosomes in control of signal transduction. Curr. Opin. Cell Biol. 16, 400-406.
32. Morimatsu, M., Takagi, H., Ota, K. G., Iwamoto, R., Yanagida, T. and Sako, Y. (2007). Multiple-state reactions between the epidermal growth factor receptor and Grb2 as observed by using single-molecule analysis. Proc. Natl. Acad. Sci. USA 104, 18013-18018.
33. Nag, A., Monine, M. I., Faeder, J. R. and Goldstein, B. (2009). Aggregation of membrane proteins by cytosolic cross-linkers: theory and simulation of the LATGrb2-SOS1 system. Biophys. J. 96, 2604-2623.
34. Nexø, E. and Hansen, H. F. (1985). Binding of epidermal growth factor from man, rat and mouse to the human epidermal growth factor receptor. Biochim. Biophys. Acta 843, 101-106.
35. Okabayashi, Y., Kido, Y., Okutani, T., Sugimoto, Y., Sakaguchi, K. and Kasuga, M. (1994). Tyrosines 1148 and 1173 of activated human epidermal growth factor receptors are binding sites of Shc in intact cells. J. Biol. Chem. 269, 18674-18678.
36. Oksvold, M. P., Skarpen, E., Wierød, L., Paulsen, R. E. and Huitfeldt, H. S. (2001). Re-localization of activated EGF receptor and its signal transducers to multivesicular compartments downstream of early endosomes in response to EGF. Eur. J. Cell Biol. 80, 285-294.
37. Okutani, T., Okabayashi, Y., Kido, Y., Sugimoto, Y., Sakaguchi, K., Matuoka, K., Takenawa, T. and Kasuga, M. (1994). Grb2/Ash binds directly to tyrosines 1068 and 1086 and indirectly to tyrosine 1148 of activated human epidermal growth factor receptors in intact cells. J. Biol. Chem. 269, 31310-31314.
38. Roepstorff, K., Grandal, M. V., Henriksen, L., Knudsen, S. L., Lerdrup, M., Grøvdal, L., Willumsen, B. M. and van Deurs, B. (2009). Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 10, 1115-1127.
39. Sato, K., Kimoto, M., Kakumoto, M., Horiuchi, D., Iwasaki, T., Tokmakov, A. A. and Fukami, Y. (2000). Adaptor protein Shc undergoes translocation and mediates up-regulation of the tyrosine kinase c-Src in EGF-stimulated A431 cells. Genes Cells 5, 749-764.
40. Scaltriti, M. and Baselga, J. (2006). The epidermal growth factor receptor pathway: a model for targeted therapy. Clin. cancer res. 12, 5268-5272.
41. Schulze, W. X., Deng, L. and Mann, M. (2005). Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst. Biol. 1, 0008.
42. Scita, G. and Di Fiore, P. P. (2010). The endocytic matrix. Nature 463, 464-473.
43. Sibilia, M., Kroismayr, R., Lichtenberger, B. M., Natarajan, A., Hecking, M. and Holcmann, M. (2007). The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75, 770-787.
44. Sorkin, A. and Duex, J. E. (2010). Quantitative analysis of endocytosis and turnover of epidermal growth factor (EGF) and EGF receptor. Curr. Protoc. Cell Biol. 46, 15.14.1-15.14.20.
45. Sorkin, A. and Goh, L. K. (2009). Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 315, 683-696.
46. Sorkin, A. and von Zastrow, M. (2002). Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 3, 600-614.
47. Sorkin, A. and von Zastrow, M. (2009). Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622.
48. Sorkin, A., Waters, C. M., Overholser, K. A. and Carpenter, G. (1991). Multiple autophosphorylation site mutations of the epidermal growth factor receptor. Analysis of kinase activity and endocytosis. J. Biol. Chem. 266, 8355-8362.
49. Sorkin, A., McClure, M., Huang, F. and Carter, R. (2000). Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr. Biol. 10, 1395-1398.
50. Sousa, L. P., Lax, I., Shen, H., Ferguson, S. M., De Camilli, P. and Schlessinger, J. (2012). Suppression of EGFR endocytosis by dynamin depletion reveals that EGFR signaling occurs primarily at the plasma membrane. Proc. Natl. Acad. Sci. USA 109, 4419-4424.
51. Verbeek, B. S., Adriaansen-Slot, S. S., Rijksen, G. and Vroom, T. M. (1997). Grb2 overexpression in nuclei and cytoplasm of human breast cells: a histochemical and biochemical study of normal and neoplastic mammary tissue specimens. J. Pathol. 183, 195-203.
52. Vieira, A. V., Lamaze, C. and Schmid, S. L. (1996). Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274, 2086-2089.
53. Vlodavsky, I., Brown, K. D. and Gospodarowicz, D. (1978). A comparison of the binding of epidermal growth factor to cultured granulosa and luteal cells. J. Biol. Chem. 253, 3744-3750.
54. Waterman, H., Katz, M., Rubin, C., Shtiegman, K., Lavi, S., Elson, A., Jovin, T. and Yarden, Y. (2002). A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J. 21, 303-313.
55. Wells, A., Welsh, J. B., Lazar, C. S., Wiley, H. S., Gill, G. N. and Rosenfeld, M. G. (1990). Ligand-induced transformation by a noninternalizing epidermal growth factor receptor. Science 247, 962-964.
56. Wiley, H. S. and Cunningham, D. D. (1982). The endocytotic rate constant. A cellular parameter for quantitating receptor-mediated endocytosis. J. Biol. Chem. 257, 4222-4229.
57. Wouters, F. S. and Bastiaens, P. I. (1999). Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells. Curr. Biol. 9, 1127-1130.