Palmitoylation of the EGF receptor impairs signal transduction and abolishes high-affinity ligand binding

Biochemistry

Volumn 48, Issue 11, 2009, Pages 2505-2513

  Macdonald Obermann, Jennifer L ^a   Pike, Linda J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AS-LIGANDS; AUTO PHOSPHORYLATIONS; CYTOPLASMIC JUXTAMEMBRANE; EXTRACELLULAR LIGANDS; HIGH-AFFINITY LIGAND BINDINGS; JUXTAMEMBRANE DOMAINS; LIGAND BINDINGS; LIPID RAFTS; PALMITOYLATION; SCATCHARD PLOTS; TYROSINE KINASE; WILD TYPES;

AMINO ACIDS; BIOCHEMISTRY; ENZYME ACTIVITY; SIGNAL TRANSDUCTION;

LIGANDS;

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; PALMITIC ACID;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CONTROLLED STUDY; CYTOPLASM; LIGAND BINDING; LIPID RAFT; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; EPIDERMAL GROWTH FACTOR; KINETICS; LIGANDS; LIPOYLATION; MICE; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 64849084821     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi802249x     Document Type: Article

References (36)

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., 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.
3. Garrett, T. P. J., 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 R. Cell 110, 763-773.
4. 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.
5. Citri, A., and Yarden, Y. (2006) EGF-ErbB Signalling: Towards the Systems Level. Nat. Rev. Mol. Cell Biol. 7, 505-516.
6. 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.
7. 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.
8. Thiel, K. W., and Carpenter, G. (2007) Epidermal Growth Factor Receptor Juxtamembrane Region Regulates Allosteric Tyrosine Kinase Activation. Proc. Natl. Acad. Sci. U.S.A. 104, 19238-19243.
9. Mendrola, J. M., Berger, M. B., King, M. C., and Lemmon, M. A. (2002) The Single Transmembrane Domains of ErbB Receptors Self-associate in Cell Membranes. J. Biol. Chem. 277, 4704-4712.
10. Duneau, J.-P., Vegh, A. P., and Sturgis, J. N. (2007) A Dimerization Hierarchy in the Transmembrane Domains of the HER Receptor Family. Biochemistry 46, 2010-2019.
11. Moriki, T., Maruyama, H., and Maruyama, I. N. (2001) Activation of Preformed EGF Receptor Dimers by Ligandinduced Rotation of the Transmembrane Domain. J. Mol. Biol. 311, 1011-1026.
12. Doran, D. M., and Spar, I. L. (1980) Oxidative Iodine Monochloride Iodination Technique. J. Immunol. Methods 39, 155-163.
13. Macdonald, J. L., and Pike, L. J. (2005) A Simplified Method for the Preparation of Detergent-free Lipid Rafts. J. Lipid Res. 46, 1061-1067.
14. Resh, M. D. (2006) Palmitoylation of Ligands, Receptors and Intracellular Signaling Molecules. Sci. STKE 359, 1-14.
15. Smotrys, J. E., and Linder, M. E. (2004) Palmitoylation of Intracellular Signaling Proteins. Regulation and Function. Annu. Rev. Biochem. 73, 559-587.
16. Walker, F., Orchard, S. G., Jorissen, R. N., Hall, N. E., Zhang, H.-H., Hoyne, P. A., Adams, T. E., Johns, T. G., Ward, C. W., Nice, E. C., and Burgess, A. W. (2004) CR1/CR2 Interactions Modulate the Functions of the Cell Surface Epidermal Growth Factor Receptor. J. Biol. Chem. 279, 22387-22398.
17. Webb, Y., Hermida-Matsumoto, L., and Resh, M. D. (2000) Inhibition of Protein Palmitoylation, Raft Localization, and T Cell Signaling by 2-Bromopalmitate and Polyunsaturated Fatty Acids. J. Biol. Chem. 275, 261-270.
18. Mineo, C., James, G. L., Smart, E. J., and Anderson, R. G. W. (1996) Localization of Epidermal Growth Factor-stimulated Ras/ Raf-1 Interaction to Caveolae Membrane. J. Biol. Chem. 271, 11930-11935.
19. Pike, L. J., and Miller, J. M. (1998) Cholesterol Depletion Delocalizes PIP2 and Inhibits Hormone-Stimulated Phosphatidylinositol Turnover. J. Biol. Chem. 273, 22298-22304.
20. Moffett, S., Brown, D. A., and Linder, M. E. (2000) Lipiddependent Targeting of G Proteins into Rafts. J. Biol. Chem. 275, 2191-2198.
21. Melkonian, K. A., Ostermeyer, A. G., Chen, J. Z., Roth, M. G., and Brown, D. A. (1999) Role of Lipid Modifications in Targeting Proteins to Detergent-resistant Membrane Rafts. J. Biol. Chem. 274, 3910-3917.
22. Zacharias, D. A., Violin, J. D., Newton, A. C., and Tsien, R. Y. (2002) Partitioning of Lipid-Modified Monomeric GFPs into Membrane Microdomains of Live Cells. Science 296, 913-916.
23. Roepstorff, K., Thomsen, P., Sandvig, K., and van Deurs, B. (2002) Sequestration of EGF Receptors in Non-caveolar Lipid Rafts Inhibits Ligand Binding. J. Biol. Chem. 277, 18954-18960.
24. Pike, L. J., and Casey, L. (2002) Cholesterol Levels Modulate EGF Receptor-Mediated Signaling by Altering Receptor Function and Trafficking. Biochemistry 41, 10315-10322.
25. Westover, E. J., Covey, D. F., Brockman, H. L., Brown, R. E., and Pike, L. J. (2003) Cholesterol Depletion Results in Site-Specific Increases in EGF Receptor Phosphorylation Due to Membrane Level Effects: Studies with Cholesterol Enantiomers. J. Biol. Chem. 278, 51125-51133.
26. Yamane, K., Toyoshima, C., and Nishimura, S. (1992) Ligand- Induced Functions of the Epidermal Growth Factor Receptor Require the Positively Charged Region Asymmetrically Distributed Across the Plasma Membrane. Biochem. Biophys. Res. Commun. 184, 1301-1310.
27. Aifa, S., Aydin, J., Nordvall, G., Lundstrom, I., Svensson, S. P. S., and Hermanson, O. (2005) A Basic Peptide Within the Juxtamembrane Region is Required for EGF Receptor Dimerization. Exp. Cell Res. 302, 108-114.
28. Aifa, S., Miled, N., Frikha, F., Aniba, M. R., Svensson, S. P. S., and Rebai, A. (2006) Electrostatic Interactions of Peptides Flanking the Tyrosine Kinase Domain in the Epidermal Growth Factor Receptor Provides a Model for Intracellular Dimerization and Autophosphorylation. Proteins 62, 1036-1043.
29. McLaughlin, S., Smith, S. O., Hayman, M. J., and Murray, D. (2005) An Electrostatic Engine Model For Autoinhibition and Activation of the Epidermal Growth Factor Receptor (EGFR/ErbB) Family. J. Gen. Physiol. 126, 41-53.
30. Li, H., Ruano, M. J., and Villalobo, A. (2004) Endogenous Calmodulin Interacts with the Epidermal Growth Factor Receptor in Living Cells. FEBS Lett. 559, 175-180.
31. Bell, C. A., Tynan, J. A., Hart, K. C., Meyer, A. N., Robertson, S. C., and Donoghue, D. J. (2000) Rotational Coupling of the Transmembrane and Kinase Domains of the Neu Receptor Tyrosine Kinase. Mol. Biol. Cell 11, 3589-3599.
32. Joseph, M., and Nagaraj, R. (1995) Interactions of Peptides Corresponding to Fatty Acylation Sites in Proteins with Model Membranes. J. Biol. Chem. 270, 16749-16765.
33. Prywes, R., Livneh, E., Ullrich, A., and Schlessinger, J. (1986) Mutations in the Cytoplasmic Domain of EGF Receptor Affect EGF Binding and Receptor Internalization. EMBO J. 5, 2179-2190.
34. Kashles, O., Yarden, Y., Fischer, R., Ullrich, A., and Schlessinger, J. (1991) A Dominant Negative Mutation Suppresses the Function of Normal Epidermal Growth Factor Receptors by Heterodimerization. Mol. Cell. Biol. 11, 1454-1463.
35. Mineo, C., Gill, G. N., and Anderson, R. G. W. (1999) Regulated Migration of Epidermal Growth Factor Receptor from Caveolae. J. Biol. Chem. 274, 30636-30643.
36. Ringerike, T., Glystad, F. D., Levy, F. O., Madshus, I. H., and Stang, E. (2002) Cholesterol is Important in Control of EGF Receptor Kinase Activity but EGF Receptors are Not Concentrated in Caveolae. J. Cell Sci. 115, 1331-1340.