Tyrosine phosphorylation of Mig6 reduces its inhibition of the epidermal growth factor receptor

ACS Chemical Biology

Volumn 8, Issue 11, 2013, Pages 2373-2376

  Wang, Zhihong ^a   Raines, Lily L ^a   Hooy, Richard M ^a   Roberson, Heather ^a   Leahy, Daniel J ^a   Cole, Philip A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; MIG6 PROTEIN; NANODISC; PROTEIN; UNCLASSIFIED DRUG; MIG-6 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; TYROSINE;

ARTICLE; BILAYER MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME KINETICS; FEEDBACK SYSTEM; GEL PERMEATION CHROMATOGRAPHY; LIPID BILAYER; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REDUCTION; SOLUBILIZATION; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; BIOASSAY; BIOLOGICAL MODEL; CHEMISTRY; HUMAN; METABOLISM; MUTATION; PHOSPHORYLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; BIOLOGICAL ASSAY; HUMANS; MODELS, BIOLOGICAL; MUTATION; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR SUPPRESSOR PROTEINS; TYROSINE;

EID: 84887939326     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb4005707     Document Type: Article

References (31)

1. Lemmon, M. A. and Schlessinger, J. (2010) Cell signaling by receptor tyrosine kinases Cell 141, 1117-1134
2. Hynes, N. E. and Lane, H. A. (2005) ERBB receptors and cancer: the complexity of targeted inhibitors Nat. Rev. Cancer 5, 341-354
3. 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
4. Paez, J. G., Janne, P. A., Lee, J. C., Tracy, S., Greulich, H., Gabriel, S., Herman, P., Kaye, F. J., Lindeman, N., Boggon, T. J., Naoki, K., Sasaki, H., Fujii, Y., Eck, M. J., Sellers, W. R., Johnson, B. E., and Meyerson, M. (2004) EGFR mutations in lung cancer: Correlation with clinical response to gefitinib therapy Science 304, 1497-1500
5. Pao, W., Miller, V., Zakowski, M., Doherty, J., Politi, K., Sarkaria, I., Singh, B., Heelan, R., Rusch, V., Fulton, L., Mardis, E., Kupfer, D., Wilson, R., Kris, M., and Varmus, H. (2004) EGF receptor gene mutations are common in lung cancers from ″never smokers″ and are associated with sensitivity of tumors to gefitinib and erlotinib Proc. Natl. Acad. Sci. U.S.A. 101, 13306-13311
6. Ferby, I., Reschke, M., Kudlacek, O., Knyazev, P., Pante, G., Amann, K., Sommergruber, W., Kraut, N., Ullrich, A., Fassler, R., and Klein, R. (2006) Mig6 is a negative regulator of EGF receptor-mediated skin morphogenesis and tumor formation Nat. Med. 12, 568-573
7. Anastasi, S., Baietti, M. F., Frosi, Y., Alema, S., and Segatto, O. (2007) The evolutionarily conserved EBR module of RALT/MIG6 mediates suppression of the EGFR catalytic activity Oncogene 26, 7833-7846
8. Zhang, X. W., Pickin, K. A., Bose, R., Jura, N., Cole, P. A., and Kuriyan, J. (2007) Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface Nature 450, 741-745
9. Wang, Z. H., Longo, P. A., Tarrant, M. K., Kim, K., Head, S., Leahy, D. J., and Cole, P. A. (2011) Mechanistic insights into the activation of oncogenic forms of EGF receptor Nat. Struct. Mol. Biol. 18, 1388-1393
10. Guha, U., Chaerkady, R., Marimuthu, A., Patterson, A. S., Kashyap, M. K., Harsha, H. C., Sato, M., Bader, J. S., Lash, A. E., Minna, J. D., Pandey, A., and Varmus, H. E. (2008) Comparisons of tyrosine phosphorylated proteins in cells expressing lung cancer-specific alleles of EGFR and KRAS Proc. Natl. Acad. Sci. U.S.A. 105, 14112-14117
11. Wolf-Yadlin, A., Kumar, N., Zhang, Y., Hautaniemi, S., Zaman, M., Kim, H. D., Grantcharova, V., Lauffenburger, D. A., and White, F. M. (2006) Effects of HER2 overexpression on cell signaling networks governing proliferation and migration Mol. Syst. Biol. 2, 54
12. Muir, T. W., Sondhi, D., and Cole, P. A. (1998) Expressed protein ligation: a general method for protein engineering Proc. Natl. Acad. Sci. U.S.A. 95, 6705-6710
13. Szewczuk, L. M., Tarrant, M. K., and Cole, P. A. (2009) Protein phosphorylation by semisynthesis: from paper to practice Methods Enzymol. 462, 1-24
14. Vila-Perello, M. and Muir, T. W. (2010) Biological applications of protein splicing Cell 143, 191-200
15. Hackenberger, C. P. and Schwarzer, D. (2008) Chemoselective ligation and modification strategies for peptides and proteins Angew. Chem., Int. Ed. 47, 10030-10074
16. Qiu, C., Tarrant, M. K., Boronina, T., Longo, P. A., Kavran, J. M., Cole, R. N., Cole, P. A., and Leahy, D. J. (2009) In vitro enzymatic characterization of near full length EGFR in activated and inhibited states Biochemistry 48, 6624-6632
17. Bayburt, T. H. and Sligar, S. G. (2010) Membrane protein assembly into nanodiscs FEBS Lett. 584, 1721-1727
18. Kim, K. and Cole, P. A. (1998) Kinetic analysis of a protein tyrosine kinase reaction transition state in the forward and reverse directions J. Am. Chem. Soc. 120, 6851-6858
19. Cook, P. F., Neville, M. E., Jr., Vrana, K. E., Hartl, F. T., and Roskoski, R., Jr. (1982) Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: kinetic mechanism for the bovine skeletal muscle catalytic subunit Biochemistry 21, 5794-5799
20. Qiao, Y., Molina, H., Pandey, A., Zhang, J., and Cole, P. A. (2006) Chemical rescue of a mutant enzyme in living cells Science 311, 1293-1297
21. Kleiman, L. B., Maiwald, T., Conzelmann, H., Lauffenburger, D. A., and Sorger, P. K. (2011) Rapid phospho-turnover by receptor tyrosine kinases impacts downstream signaling and drug binding Mol. Cell 43, 723-737
22. Xia, F., Li, J., Hickey, G. W., Tsurumi, A., Larson, K., Guo, D., Yan, S. J., Silver-Morse, L., and Li, W. X. (2008) Raf activation is regulated by tyrosine 510 phosphorylation in Drosophila PLoS Biol. 6, 1115-1129
23. Tamada, M., Farrell, D. L., and Zallen, J. A. (2012) Abl regulates planar polarized junctional dynamics through beta-catenin tyrosine phosphorylation Dev. Cell 22, 309-319
24. Red Brewer, M., Choi, S. H., Alvarado, D., Moravcevic, K., Pozzi, A., Lemmon, M. A., and Carpenter, G. (2009) The juxtamembrane region of the EGF receptor functions as an activation domain Mol. Cell 34, 641-651
25. Scheck, R. A., Lowder, M. A., Appelbaum, J. S., and Schepartz, A. (2012) Bipartite tetracysteine display reveals allosteric control of ligand-specific EGFR activation ACS Chem. Biol. 7, 1367-1376
26. Endres, N. F., Das, R., Smith, A. W., Arkhipov, A., Kovacs, E., Huang, Y. J., Pelton, J. G., Shan, Y. B., Shaw, D. E., Wemmer, D. E., Groves, J. T., and Kuriyan, J. (2013) Conformational coupling across the plasma membrane in activation of the EGF receptor Cell 152, 543-556
27. 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
28. Hackeng, T. M., Griffin, J. H., and Dawson, P. E. (1999) Protein synthesis by native chemical ligation: expanded scope by using straightforward methodology Proc. Natl. Acad. Sci. U.S.A. 96, 10068-10073
29. Tarrant, M. K., Rho, H. S., Xie, Z., Jiang, Y. L., Gross, C., Culhane, J. C., Yan, G., Qian, J., Ichikawa, Y., Matsuoka, T., Zachara, N., Etzkorn, F. A., Hart, G. W., Jeong, J. S., Blackshaw, S., Zhu, H., and Cole, P. A. (2012) Regulation of CK2 by phosphorylation and O-GlcNAcylation revealed by semisynthesis Nat. Chem. Biol. 8, 262-269
30. Ritchie, T. K., Grinkova, Y. V., Bayburt, T. H., Denisov, I. G., Zolnerciks, J. K., Atkins, W. M., and Sligar, S. G. (2009) Chapter 11: Reconstitution of membrane proteins in phospholipid bilayer nanodiscs Methods Enzymol. 464, 211-231
31. Mi, L. Z., Grey, M. J., Nishida, N., Walz, T., Lu, C., and Springer, T. A. (2008) Functional and structural stability of the epidermal growth factor receptor in detergent micelles and phospholipid nanodiscs Biochemistry 47, 10314-10323