Engineering NGF receptors to bind Grb2 directly uncovers differences in signaling ability between Grb2- and ShcA-binding sites

FEBS Letters

Volumn 586, Issue 20, 2012, Pages 3658-3664

  Oku, Shinichiro ^a   Van Der Meulen, Talitha ^a   Copp, Jeremy ^a   Glenn, Gary ^a   Van Der Geer, Peter ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Akt; DNA synthesis; Erk; Protein tyrosine kinase; Signal transduction; TrkA

Indexed keywords

BINDING PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAS PROTEIN; SHCA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVATION; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN MOTIF; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; DNA; GRB2 ADAPTOR PROTEIN; HUMANS; MICE; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BINDING; PROTEIN ENGINEERING; PROTO-ONCOGENE PROTEINS C-AKT; RAS PROTEINS; RECEPTOR, NERVE GROWTH FACTOR; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84867576685     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.08.021     Document Type: Article

References (31)

1. R. Perona Cell signalling: growth factors and tyrosine kinase receptors Clin. Transl. Oncol. 8 2006 77 82
2. W.C. Forrester The Ror receptor tyrosine kinase family Cell. Mol. Life. Sci. 59 2002 83 96
3. T.A. Gustafson, S.A. Moodie, and B.E. Lavan The insulin receptor and metabolic signaling Rev. Physiol. Biochem. Pharmacol. 137 1999 71 190
4. J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 103 2000 211 225
5. S.R. Hubbard, and W.T. Miller Receptor tyrosine kinases: mechanisms of activation and signaling Curr. Opin. Cell Biol. 19 2007 117 123
6. T. Pawson Protein modules and signalling networks Nature 373 1995 573 580
7. T. Pawson, G.D. Gish, and P. Nash SH2 domains, interaction modules and cellular wiring Trends Cell Biol. 11 2001 504 511
8. E.J. Lowenstein The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling Cell 70 1992 431 442
9. Z. Songyang Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav Mol. Cell. Biol. 14 1994 2777 2785
10. M. Rozakis-Adcock, R. Fernley, J. Wade, T. Pawson, and D. Bowtell The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1 Nature 363 1993 83 85
11. G. Pelicci A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction Cell 70 1992 93 104
12. W.M. Kavanaugh, and L.T. Williams An alternative to SH2 domains for binding tyrosine-phosphorylated proteins Science 266 1994 1862 1865
13. P. van der Geer, S. Wiley, G.D. Gish, V.K. Lai, R. Stephens, M.F. White, D. Kaplan, and T. Pawson Identification of residues that control specific binding of the Shc phosphotyrosine-binding domain to phosphotyrosine sites Proc. Natl. Acad. Sci. U S A 93 1996 963 968
14. P. van der Geer, S. Wiley, G.D. Gish, and T. Pawson The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions Curr. Biol. 6 1996 1435 1444
15. M. Rozakis-Adcock Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in the activation of the Ras pathway by tyrosine kinases Nature 360 1992 689 692
16. C. Cordon-Cardo The trk tyrosine protein kinase mediates the mitogenic properties of nerved growth factor and neurotrophin-3 Cell 66 1991 173 183
17. P. van der Geer A conserved amino-terminal Shc domain binds to phosphotyrosine motifs in activated growth factor receptors and phosphopeptides Curr. Biol. 5 1995 404 412
18. C.A. Schneider, W.S. Rasband, and K.W. Eliceiri NIH Image to ImageJ: 25 years of image analysis Nat. Methods 9 2012 671 675
19. R.M. Stephens, D.M. Loeb, T.D. Copeland, T. Pawson, L.A. Greene, and D.R. Kaplan Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma 1 to mediate NGF responses Neuron 12 1994 691 705
20. W.-S. Wu Protein kinase C [alpha] trigger Ras and Raf-independent MEK/ERK activation for TPA-induced growth inhibition of human hepatoma cell HepG2 Cancer Lett. 239 2006 27 35
21. M. Holgado-Madruga, D.R. Emlet, D.K. Moscatello, A.K. Godwin, and A.J. Wong A Grb2-associated docking protein in EGF- and insulin-receptor signalling Nature 379 1996 560 564
22. E.D. Fixman, M. Holgado-Madruga, L. Nguyen, D.M. Kamikura, T.M. Fournier, A.J. Wong, and M. Park Efficient cellular transformation by the Met oncoprotein requires a functional Grb2 binding site and correlates with phosphorylation of the Grb2-associated proteins, Cbl and Gab1 J. Biol. Chem. 272 1997 20167 20172
23. B. Margolis, and E.Y. Skolnik Activation of Ras by receptor tyrosine kinases J. Am. Soc. Nephrol. 5 1994 1288 1299
24. C.J. Marshall Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation Cell 80 1995 179 185
25. X. Qian, A. Riccio, Y. Zhang, and D.D. Ginty Identification and characterization of novel substrates of Trk receptors in developing neurons Neuron 21 1998 1017 1029
26. P.J. Coffer, J. Jin, and J.R. Woodgett Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation Biochem. J. 335 1998 1 13
27. S.O. Meakin, J.I. MacDonald, E.A. Gryz, C.J. Kubu, and J.M. Verdi The signaling adapter FRS-2 competes with Shc for binding to the nerve growth factor receptor TrkA. A model for discriminating proliferation and differentiation J. Biol. Chem. 274 1999 9861 9870
28. G. Zeng, and S.O. Meakin Overexpression of the signaling adapter FRS2 reconstitutes the cell cycle deficit of a nerve growth factor non-responsive TrkA receptor mutant J. Neurochem. 81 2002 820 831
29. S.H. Ong, G.R. Guy, Y.R. Hadari, S. Laks, N. Gotoh, J. Schlessinger, and I. Lax FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors Mol. Cell. Biol. 20 2000 979 989
30. C. Dhalluin Structural basis of SNT PTB domain interactions with distinct neurotrophic receptors Molecular Cell 6 2000 921 929
31. N. Jones, W.R. Hardy, M.B. Friese, C. Jorgensen, M.J. Smith, N.M. Woody, S.J. Burden, and T. Pawson Analysis of a Shc family adaptor protein, ShcD/Shc4, that associates with muscle-specific kinase Mol. Cell. Biol. 27 2007 4759 4773