Systematic analysis of the epidermal growth factor receptor by mass spectrometry reveals stimulation-dependent multisite phosphorylation

Molecular and Cellular Proteomics

Volumn 4, Issue 8, 2005, Pages 1107-1121

  Erba, Elisabetta Boeri ^a   Bergatto, Elena ^b   Cabodi, Sara ^b   Silengo, Lorenzo ^b   Tarone, Guido ^b   Defilippi, Paola ^b   Jensen, Ole N ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GRAPHITE; INTEGRIN; PERVANADATE; SERINE; THREONINE; TYROSINE;

AMINO ACID SEQUENCE; ARTICLE; CELL ADHESION; CHROMATOGRAPHY; CONTROLLED STUDY; CYTOLOGY; EXTRACELLULAR MATRIX; FEASIBILITY STUDY; GENE ACTIVATION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

CELL ADHESION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPIDERMAL GROWTH FACTOR; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; INTEGRINS; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 24044455639     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M500070-MCP200     Document Type: Article

References (41)

1. Carpenter, G. (2000) The EGF receptor: a nexus for trafficking and signaling. Bioessays 22, 697-707
2. Bishayee, S. (2000) Role of conformational alteration in the epidermal growth factor receptor (EGFR) function. Biochem. Pharmacol. 60, 1217-1223
3. Gschwind, A., Zwick, E., Prenzel, N., Leserer, M., and Ullrich, A. (2001) Cell communication networks: epidermal growth factor receptor transactivation as the paradigm for interreceptor signal transmission. Oncogene 20, 1594-1600
4. Assoian, R. K., and Schwartz, M. A. (2001) Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 11, 48-53
5. Moro, L., Venturino, M., Bozzo, C., Silengo, L., Altruda, F., Beguinot, L., Tarone, G., and Defilippi, P. (1998) Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. EMBO J. 17, 6622-6632
6. Moro, L., Dolce, L., Cabodi, S., Bergatto, E., Boeri Erba, E., Smeriglio, M., Turco, E., Retta, S. F., Giuffrida, M. G., Venturino, M., Godovac-Zimmermann, J., Conti, A., Schaefer, E., Beguinot, L., Tacchetti, C., Gaggini, P., Silengo, L., Tarone, G., and Defilippi, P. (2002) Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p13OCas and leads to phosphorylation of specific EGF receptor tyrosines. J. Biol. Chem. 277, 9405-9414
7. Marcoux, N., and Vuori, K. (2003) EGF receptor mediates adhesion-dependent activation of the Rac GTPase: a role for phosphatidylinositol 3-kinase and Vav2. Oncogene 22, 6100-6106
8. Cabodi, S., Moro, L., Bergatto, E., Boeri Erba, E., Di Stefano, P., Turco, E., Tarone, G., and Defilippi, P. (2004) Integrin regulation of epidermal growth factor (EGF) receptor and of EGF-dependent responses. Biochem. Soc. Trans. 32, 438-442
9. Mann, M., Ong, S. E., Gronborg, M., Steen, H., Jensen, O. N., and Pandey, A. (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 20, 261-268
10. McLachlin, D. T., and Chait, B. T. (2001) Analysis of phosphorylated proteins and peptides by mass spectrometry. Curr. Opin. Chem. Biol. 5, 591-602
11. Jensen, O. N. (2004) Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol. 8, 33-41
12. Medzihradszky, K. F., Campbell, J. M., Baldwin, M. A., Falick, A. M., Juhasz, P, Vestal, M. L., and Burlingame, A. L. (2000) The characteristics of peptide collision-induced dissociation using a high-performance MALDI-TOF/TOF tandem mass spectrometer. Anal. Chem. 72, 552-558
13. Shevchenko, A., Loboda, A., Ens, W., and Standing, K. G. (2000) MALDI quadrupole time-of-flight mass spectrometry: a powerful tool for proteomic research. Anal. Chem. 72, 2132-2141
14. Qin, J., and Chait, B. T. (1997) Identification and characterization of post-translational modifications of proteins by MALDI ion trap mass spectrometry. Anal. Chem. 69, 4002-4009
15. Bennett, K. L., Stensballe, A., Podtelejnikov, A. V., Moniatte, M., and Jensen, O. N. (2002) Phosphopeptide detection and sequencing by matrix-assisted laser desorption/ionization quadrupole time-of-flight tandem mass spectrometry. J. Mass Spectrom. 37, 179-190
16. Kjellström, S., and Jensen, O. N. (2004) Phosphoric acid as a matrix additive for MALDI MS analysis of phosphopeptides and phosphoproteins. Anal. Chem. 76, 5109-5117
17. Stensballe, A., and Jensen, O. N. (2004) Phosphoric acid enhances the performance of Fe(III) affinity chromatography and matrix-assisted laser desorption/ionization tandem mass spectrometry for recovery, detection and sequencing of phosphopeptides. Rapid Commun. Mass Spectrom. 18, 1721-1730
18. Stensballe, A., Andersen, S., and Jensen, O. N. (2001) Characterization of phosphoproteins from electrophoretic gels by nanoscale Fe(III) affinity chromatography with off-line mass spectrometry analysis. Proteomics 1, 207-222
19. Larsen, M. R., Graham, M. E., Robinson, P. J., and Roepstorff, P. (2004) Improved detection of hydrophilic phosphopeptides using graphite powder microcolumns and mass spectrometry: evidence for in vivo doubly phosphorylated dynamin I and dynamin III. Mol. Cell. Proteomics 3, 456-465
20. Gobom, J., Nordhoff, E., Mirgorodskaya, E., Ekman, R., and Roepstorff, P. (1999) Sample purification and preparation technique based on nanoscale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J. Mass Spectrom. 34, 105-116
21. Loughrey Chen, S., Huddleston, M. J., Shou, W., Deshaies, R. J., Annan, R. S., and Carr, S. A. (2002) Mass spectrometry-based methods for phosphorylation site mapping of hyperphosphorylated proteins applied to Net1, a regulator of exit from mitosis in yeast. Mol. Cell. Proteomics 1, 186-196
22. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacryiamide gels. Anal. Chem. 68, 850-858
23. Neubauer, G., and Mann, M. (1999) Mapping of phosphorylation sites of gel-isolated proteins by nanoelectrospray tandem mass spectrometry: potentials and limitations. Anal. Chem. 71, 235-242
24. Larsen, M. R., Cordwell, S. J., and Roepstorff, P. (2002) Graphite powder as an alternative or supplement to reversed-phase material for desalting and concentration of peptide mixtures prior to matrix-assisted laser desorption/ionization-mass spectrometry. Proteomics 2, 1277-1287
25. Deleted in proof
26. Sato, K., Sato, A., Aoto, M., and Fukami, Y. (1995) c-Src phosphorylates epidermal growth factor receptor on tyrosine 845. Biochem. Biophys. Res. Commun. 5, 1078-1087
27. 1101 is associated with modulation of receptor function. J. Biol. Chem. 274, 8335-8343
28. Stover, D. R., Becker, M., Liebetanz, J., and Lydon, N. B. (1995) Src phosphorylation of the epidermal growth factor receptor at novel sites mediates receptor interaction with Src and P85α. J. Biol. Chem. 270, 15591-15597
29. Nuhse, T. S., Stensballe, A., Jensen, O. N., and Peck, S. C. (2003). Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. Mol. Cell. Proteomics 2, 1234-1243
30. Gruhler, A., Olsen, J. V., Mohammed, S., Mortensen, P., Faergeman, N. F., Mann, M., and Jensen, O. N. (2005). Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell Proteomics. 4, 310-327
31. Boeri Erba, E., Bergatto, E., Cabodi, S., Silengo, L., Tarone, G., Defilippi, P., and Jensen, O. N. (2004) Adhesion-dependent differential phosphorylation of EGF receptor determined by MALDI-Q-TOF tandem mass spectrometry, in 52nd American Society for Mass Spectrometry Conference of Mass Spectrometry, Nashville, May 23-27, 2004, poster number TPQ337, American Society for Mass Spectrometry, Santa Fe, NM
32. Margolis, B. L., Lax, I., Kris, R., Dombalagian, M., Honegger, A. M., Howk, R., Givol, D., Ullrich, A., and Schlessinger, J. (1989) All autophosphorylation sites of epidermal growth factor (EGF) receptor and HER2/neu are located in their carboxyl-terminal tails. Identification of a novel site in EGF receptor. Cell 57, 1101-1107
33. 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
34. Defilippi, P., Retta, S. F., Olivo, C., Palmieri, M., Venturino, M., Silengo, L., and Tarone, G. (1995) p125FAK tyrosine phosphorylation and focal adhesion assembly: studies with phosphotyrosine phosphatase inhibitors. Exp. Cell Res. 221, 141-152
35. Oksvold, M. P., Thien, C. B., Widerberg, J., Chantry, A., Huitfeldt, H. S., and Langdon, W. Y. (2003) Serine mutations that abrogate ligand-induced ubiquitination and internalization of the EGF receptor do not affect c-Cbl association with the receptor. Oncogene. 22, 8509-8518
36. Salek, M., Alonso, A., Pipkorn, R., and Lehmann, W. D. (2003) Neutral loss of amino acid residues from protonated peptides in collision-induced dissociation generates N- or C-terminall sequence ladders. J. Mass Spectrom. 38, 1143-1149
37. Steen, H., Fernandez, M., Ghaffari, S., Pandey, A., and Mann, M. (2003) Phosphotyrosine mapping in Bcr/Abl oncoprotein using phosphotyrosine-specific immonium ion scanning. Mol. Cell. Proteomics 2, 138-145
38. 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
39. Thelemann, A., Petti, F., Griffin, G., Iwata, K., Hunt, T., Settinari, T., Fenyo, D., Gibson, N., and Haley, J. D. (2005) Phosphotyrosine signaling networks in epidermal growth factor receptor overexpressing squamous carcinoma cells. Mol. Cell. Proteomics 4, 356-376
40. Ballif, B. A., Roux, P. P., Gerber, S. A., MacKeigan, J. P., Blenis, J., and Gygi, S. P. (2005) Quantitative phosphorylation profiling of the ERK/p90 ribosomal S6 kinase-signaling cassette and its targets, the tuberous sclerosis tumor suppressors. Proc. Natl. Acad. Sci. U. S. A. 102, 667-672
41. Uhlen, M., and Ponten, F. (2005). Antibody-based proteomics for human tissue profiling. Mol. Cell. Proteomics 4, 384-393