Solution structure of the Grb2 SH2 domain complexed with a high-affinity inhibitor

Journal of Biomolecular NMR

Volumn 42, Issue 3, 2008, Pages 197-207

  Ogura, Kenji ^a   Shiga, Takanori ^a   Yokochi, Masashi ^a   Yuzawa, Satoru ^a   Burke Jr , Terrence R ^b   Inagaki, Fuyuhiko ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Inhibitor; Perdeuterated Grb2 SH2; Solution structure; Structure based drug design

Indexed keywords

GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; PHOSPHATE; PROTEIN INHIBITOR;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CRYSTAL STRUCTURE; GEL PERMEATION CHROMATOGRAPHY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

BINDING SITES; BIOMIMETICS; CHROMATOGRAPHY, GEL; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GLUTATHIONE TRANSFERASE; GRB2 ADAPTOR PROTEIN; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES, CYCLIC; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS; SRC HOMOLOGY DOMAINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 55649106334     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-008-9272-0     Document Type: Article

References (39)

1. Breeze AL (2000) Isotope-filtered NMR methods for the study of biomolecular structure and interactions. Prog NMR Spectrosc 36:323-372
2. Buday L, Downward J (1993) Epidermal growth factor regulates p21ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell 73:611-620
3. Burke TR Jr (2006) Development of Grb2 SH2 domain signaling antagonists: a potential new class of antiproliferative agents. Int J Pept Res Therapeutics 12:33-48
4. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289-302
5. Daly RJ, Binder MD, Sutherland RL (1994) Overexpression of the Grb2 gene in human breast cancer cell lines. Oncogene 9:2723-2727
6. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293
7. Domchek SM, Auger KR, Chatterjee S, Burke TR Jr, Shoelson SE (1992) Inhibition of SH2 domain/phosphoprotein association by a nonhydrolyzable phosphonopeptide. Biochemistry 31:9865-9870
8. Eck MJ, Atwell SK, Shoelson SE, Harrison SC (1994) Structure of the regulatory domains of the Src-family tyrosine kinase Lck. Nature 368:764-769
9. Furet P, Gay B, Garcia-Echeverria C, Rahuel J, Fretz H, Schoepfer J, Caravatti G (1997) Discovery of 3-aminobenzyloxycarbonyl as an N-terminal group conferring high affinity to the minimal phosphopeptide sequence recognized by the Grb2-SH2 domain. J Med Chem 40:3551-3556
10. Furet P, Gay B, Caravatti G, Garcia-Echeverria C, Rahuel J, Schoepfer J, Fretz H (1998) Structure-based design and synthesis of high affinity tripeptide ligands of the Grb2-SH2 domain. J Med Chem 41:3442-3449
11. Furet P, Garcia-Echeverria C, Gay B, Schoepfer J, Zeller M, Rahuel J (1999) Structure-based design, synthesis, and X-ray crystallography of a high-affinity antagonist of the Grb2-SH2 domain containing an asparagine mimetic. J Med Chem 42:2358-2363
12. Gale NW, Kaplan D, Lowenstein EJ, Schlessinger J, Bar-Sagi D (1993) Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature 363:88-92
13. Gao Y, Voigt J, Wu JX, Yang D, Burke TR Jr (2001a) Macrocyclization in the design of a conformationally constrained Grb2 SH2 domain inhibitor. Bioorg Med Chem Lett 11:1889-1892
14. Gao Y, Wei CQ, Burke TR Jr (2001b) Olefin metathesis in the design and synthesis of a globally constrained Grb2 SH2 domain inhibitor. Org Lett 3:1617-1620
15. 2. J Med Chem 41:1741-1744
16. Guntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278:353-378
17. Koradi R, Billeter M, Wuthrich K (1996) MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graph 14:51-55
18. Kuriyan J, Cowburn D (1997) Modular peptide recognition domains in eukaryotic signaling. Annu Rev Biophys Biomol Struct 26:259-288
19. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477-486
20. Li N, Batzer A, Daly R, Yajnik V, Skolnik E, Chadrin P, Bar-Sagi D, Margolis B, Schlessinger J (1993) Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363:85-88
21. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullrich A, Skolnik EY, Bar-Sagi D, Schlessinger J (1992) The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70:431-442
22. Marengere LE, Pawson T (1994) Structure and function of SH2 domains. J Cell Sci Suppl 18:97-104
23. Mikol V, Baumann G, Keller TH, Manning U, Zurini MG (1995) The crystal structures of the SH2 domain of p56lck complexed with two phosphonopeptides suggest a gated peptide binding site. J Mol Biol 246:344-355
24. Ogura K, Terasawa H, Inagaki F (1996) An improved double-tuned and isotope-filtered pulse scheme based on a pulsed field gradient and a wide-band inversion shaped pulse. J Biomol NMR 8:492-498
25. Ogura K, Tsuchiya S, Terasawa H, Yuzawa S, Hatanaka H, Mandiyan V, Schlessinger J, Inagaki F (1999) Solution structure of the SH2 domain of Grb2 complexed with the Shc-derived phosphotyrosine-containing peptide. J Mol Biol 289:439-445
26. Olejniczak ET, Xu RX, Fesik SW (1992) A 4D HCCH-TOCSY experiment for assigning the side chain 1H and 13C resonances of proteins. J Biomol NMR 2:655-659
27. Phan J, Shi ZD, Burke TR Jr, Waugh DS (2005) Crystal structures of a high-affinity macrocyclic peptide mimetic in complex with the Grb2 SH2 domain. J Mol Biol 353:104-115
28. Pronk GJ, de Vries-Smits AMM, Buday L, Downward J, Maassen JA, Medema RH, Bos JL (1994) Involvement of Shc in insulin- and epidermal growth factor-induced activation of p21ras. Mol Cell Biol 14:1575-1581
29. Rahuel J, Gay B, Erdmann D, Strauss A, Garcia-Echeverria C, Furet P, Caravatti G, Fretz H, Schoepfer J, Grutter MG (1996) Structural basis for specificity of GRB2-SH2 revealed by a novel ligand binding mode. Nat Struct Biol 3:586-589
30. Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W, Batzer A, Thomas S, Brugge J, Pelicci PG, Schlessinger J, Pawson T (1992) Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360:689-692
31. Schlaepfer DD, Hanks SK, Hunter T, van der Geer P (1994) Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 372:786-791
32. Schwarz-Linek U, Werner JM, Pickford AR, Gurusiddappa S, Kim JH, Pilka ES, Briggs JA, Gough TS, Höök M, Campbell ID, Potts JR (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423:177-181
33. Skolnik EY, Batzer A, Li N, Lee CH, Lowenstein LE, Mohammadi M, Margolis B, Schlessinger J (1993a) The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science 260:1953-1955
34. Skolnik EY, Lee CH, Batzer A, Vicentini LM, Zhou M, Daly R, Myers MJ Jr, Backer JM, Ullrich A, White MF, Schlessinger J (1993b) The SH2/SH3 domain-containing protein Grb2 interacts with tyrosine-phosphorylated IRS1 and Shc: Implications for insulin control of ras signaling. EMBO J 12:1929-1936
35. Songyang Z, Shoelson SE, McGlade J, Olivier P, Pawson T, Bustelo XR, Barbacid M, Sabe H, Hanafusa H, Yi T, Ren R, Baltimore D, Ratnofsky S, Feldman RA, Cantley LC (1994) Specific motifs recognized by the SH2 domains of Csk, 3BP2, fes/fps, Grb-2, SHPTP1, SHC, Syk and Vav. Mol Cell Biol 14:2777-2785
36. Thornton KH, Mueller WT, McConnell P, Zhu G, Saltiel AR, Thanabal V (1996) Nuclear magnetic resonance solution structure of the growth factor receptor-bound protein 2 Src homology 2 domain. Biochemistry 35:11852-11864
37. Tsuchiya S, Ogura K, Hatanaka H, Nagata K, Terasawa H, Mandiyan V, Schlessinger J, Aimoto S, Ohta H, Inagaki F (1999) Solution structure of SH2 domain of Grb2/Ash complexed with EGF receptor derived phosphotyrosine containing peptide. J Biochem 125:1145-1153
38. 2 symmetry. J Am Chem Soc 119:5958-5959
39. Yip SS, Crew AJ, Gee JM, Hui R, Blamey RW, Robertson JF, Nicholson RI, Sutherland RL, Daly RJ (2000) Up-regulation of the protein tyrosine phosphatase SHP-1 in human breast cancer and correlation with GRB2 expression. Int J Cancer 88:363-368