Backbone nuclear relaxation characteristics and calorimetric investigation of the human Grb7-SH2/erbB2 peptide complex

Protein Science

Volumn 14, Issue 6, 2005, Pages 1556-1569

  Ivancic, Monika ^a,d   Spuches, Anne M ^b   Guth, Ethan C ^a   Daugherty, Margaret A ^a   Wilcox, Dean E ^b   Lyons, Barbara A ^c  

^a UNIVERSITY OF VERMONT   (United States)

^b Dartmouth College   (United States)

^c NEW MEXICO STATE UNIVERSITY   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; GROWTH FACTOR RECEPTOR BOUND PROTEIN 7; PEPTIDE DERIVATIVE; PROTEIN; PROTEIN SH2; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; ISOTHERMAL TITRATION CALORIMETRY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STEADY STATE; THERMODYNAMICS;

GRB7 ADAPTOR PROTEIN; HUMANS; MULTIPROTEIN COMPLEXES; PEPTIDES; PROTEINS; RECEPTOR, ERBB-2; SRC HOMOLOGY DOMAINS; THERMODYNAMICS;

EID: 22444439210     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041102305     Document Type: Article

References (67)

1. Barbato, G., Ikura, M., Kay, L.E., Pastor, R.W., and Bax, A. 1992. Backbone dynamics of calmodulin studied by 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible. Biochemistry 31: 5269-5278.
2. Bradshaw, J.M. and Waksman, G. 1998. Calorimetric investigation of proton linkage by monitoring both the enthalpy and association constant of binding: Application to the interaction of the Src SH2 domain with a high-affinity tyrosyl phosphopeptide. Biochemistry 37: 15400-15407.
3. _. 1999. Calorimetric examination of high-affinity Src SH2 domain-tyrosyl phosphopeptide binding: Dissection of the phosphopeptide sequence specificity and coupling energetics. Biochemistry 38: 5147-5154.
4. Brescia, P.J., Ivancic, M., and Lyons, B.A. 2002. Assignment of backbone 1H, 13C, and 15N resonances of human Grb7-SH2 domain in complex with a phosphorylated peptide ligand. J. Biomol. NMR 23: 77-78.
5. Cantor, C.R. and Schimmel, P.R. 1980. Techniques for the study of biological structure and function. In Biophysical chemistry. Freeman, San Francisco.
6. Chen, D., Xu, L.G., Chen, L., Li, L., Zhai, Z., and Shu, H.B. 2003. NIK is a component of the EGF/heregulin receptor signaling complexes. Oncogene 22: 4348-4355.
7. Chung, E., Henriques, D., Renzoni, D., Zvelebil, M., Bradshaw, J.M., Waksman, G., Robinson, C.V., and Ladbury, J.E. 1998. Mass spectrometric and thermodynamic studies reveal the role of water molecules in complexes formed between SH2 domains and tyrosyl phosphopeptides. Structure 6: 1141-1151.
8. Clore, G.M., Driscoll, P.C., Wingfield, P.T., and Gronenborn, A.M. 1990. Analysis of the backbone dynamics of interleukin-1 b using two-dimensional inverse detected heteronuclear 15N-1H NMR spectroscopy. Biochemistry 29: 7387-7401.
9. Cohn, E.J. and Edsall, J.T. 1943. Proteins, amino acids and peptides as ions and dipolar ions. Reinhold, New York.
10. Connelly, P.R. 1997. The cost of releasing site-specific, bound water molecules from proteins: Toward a quantitative guide for structure-based drug design. In Structure-based drug design: Thermodynamics, modeling, and strategy (eds. J.E. Ladbury and P.R. Connelly), pp. 143-157. Springer-Verlag, Berlin.
11. Coussens, L.M. and Werb, Z. 2002. Inflammation and cancer. Nature 420: 860-867.
12. Daly, R.J., Sanderson, G.M., Janes, P.W., and Sutherland, R.L. 1996. Cloning and characterization of GRB14, a novel member of the GRB7 gene family. J. Biol. Chem. 271: 12502-12510.
13. de Mol, N.J., Catalina, M.I., Fischer, M.J., Broutin, I., Maier, C.S., and Heck, A.J. 2004. Changes in structural dynamics of the Grb2 adaptor protein upon binding of phosphotyrosine ligand to its SH2 domain. Biochim. Biophys. Acta 1700: 53-64.
14. Dill, K.A. 1990. The meaning of hydrophobicity. Science 250: 297-298.
15. Eck, M.J., Shoelson, S.E., and Harrison, S.C. 1993. Recognition of a highaffinity phosphotyrosyl peptide by the Src homology-2 domain of p56lck. Nature 362: 87-91.
16. 15NNMR relaxation. Biochemistry 33: 5984-6003.
17. Griswold, I.J. and Dahlquist, F.W. 2002. The dynamic behavior of CheW from Thermotoga maritima in solution, as determined by nuclear magnetic resonance: Implications for potential protein-protein interaction sites. Biophys. Chem. 101-102: 359-373.
18. Han, D.C. and Guan, J.L. 1999. Association of focal adhesion kinase with Grb7 and its role in cell migration. J. Biol. Chem. 274: 24425-24430.
19. Han, D.C., Shen, T.L., and Guan, J.L. 2000. Role of Grb7 targeting to focal contacts and its phosphorylation by focal adhesion kinase in regulation of cell migration. J. Biol. Chem. 275: 28911-28917.
20. He, W., Rose, D.W., Olefsky, J.M., and Gustafson, T.A. 1998. Grb10 interacts differentially with the insulin receptor, insulin-like growth factor I receptor, and epidermal growth factor receptor via the Grb10 Src homology 2 (SH2) domain and a second novel domain located between the pleckstrin homology and SH2 domains. J. Biol. Chem. 273: 6860-6867.
21. Ivancic, M., Daly, R.J., and Lyons, B.A. 2003. Solution structure of the human Grb7-SH2 domain/erbB2 peptide complex and structural basis for Grb7 binding to ErbB2. J. Biomol. NMR 27: 205-219.
22. Jahn, T., Seipel, P., Urschel, S., Peschel, C., and Duyster, J. 2002. Role for the adaptor protein Grb10 in the activation of Akt. Mol. Cell Biol. 22: 979-991.
23. Janes, P.W., Lackmann, M., Church, W.B., Sanderson, G.M., Sutherland, R.L., and Daly, R.J. 1997. Structural determinants of the interaction between the erbB2 receptor and the Src homology 2 domain of Grb7. J. Biol. Chem. 272: 8490-8497.
24. Jin, D., Andrec, M., Montelione, G.T., and Levy, R.M. 1998. Propagation of experimental uncertainties using the Lipari-Szabo model-free analysis of protein dynamics. J. Biomol. NMR 12: 471-492.
25. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28: 8972-8979.
26. Kay, L.E., Nicholson, L.K., Delaglio, F., Bax, A., and Torchia, D.A. 1992. Pulse sequences for removal of the effects of cross-correlation between dipolar and chemical-shift anisotropy relaxation mechanism on the measurement of heteronuclear T1 and T2 values in proteins. J. Magn. Reson. 97: 359-375.
27. Ladbury, J.E., Lemmon, M.A., Zhou, M., Green, J., Botfield, M.C., and Schlessinger, J. 1995. Measurement of the binding of tyrosyl phosphopeptides to SH2 domains: A reappraisal. Proc. Natl. Acad. Sci. 92: 3199-3203.
28. Ladbury, J.E., Hensmann, M., Panayotou, G., and Campbell, I.D. 1996. Alternative modes of tyrosyl phosphopeptide binding to a Src family SH2 domain: Implications for regulation of tyrosine kinase activity. Biochemistry 35: 11062-11069.
29. Laue, T.M., Shaf, B.S., Ridgeway, T.M., and Pelletier, S.L. 1992. Computer-aided interpretation of analytical sedimentation data for proteins. In Analytical ultracentrifugation in biochemistry and polymer science, pp. 90-125. Royal Society of Chemistry, Cambridge, UK.
30. Lemmon, M.A. and Ladbury, J.E. 1994. Thermodynamic studies of tyrosyl-phosphopeptide binding to the SH2 domain of p56lck. Biochemistry 33: 5070-5076.
31. Li, Y.C. and Montelione, G.T. 1995. Human type-α transforming growth factor undergoes slow conformational exchange between multiple backbone conformations as characterized by nitrogen-15 relaxation measurements. Biochemistry 34: 2408-2423.
32. Lipari, G. and Szabo, A. 1982a. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104: 4546-4559.
33. _. 1982b. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104: 4559-4570.
34. Loh, A.P., Guo, W., Nicholson, L.K., and Oswald, R.E. 1999. Backbone dynamics of inactive, active, and effector-bound Cdc42Hs from measurements of (15)N relaxation parameters at multiple field strengths. Biochemistry 38: 12547-12557.
35. Loh, A.P., Pawley, N., Nicholson, L.K., and Oswald, R.E. 2001. An increase in side chain entropy facilitates effector binding: NMR characterization of the side chain methyl group dynamics in Cdc42Hs. Biochemistry 40: 4590-4600.
36. Mandiyan, V., O'Brien, R., Zhou, M., Margolis, B., Lemmon, M.A., Sturtevant, J.M., and Schlessinger, J. 1996. Thermodynamic studies of SHC phosphotyrosine interaction domain recognition of the NPXpY motif. J. Biol. Chem. 271: 4770-4775.
37. Margolis, B. 1994. The GRB family of SH2 domain proteins. Prog. Biophys. Mol. Biol. 62: 223-244.
38. Margolis, B., Silvennoinen, O., Comoglio, F., Roonprapunt, C., Skolnik, E., Ullrich, A., and Schlessinger, J. 1992. High-efficiency expression/cloning of epidermal growth factor-receptor-binding proteins with Src homology 2 domains. Proc. Natl. Acad. Sci. 89: 8894-8898.
39. McNemar, C., Snow, M.E., Windsor, W.T., Prongay, A., Mui, P., Zhang, R., Durkin, J., Le, H.V., and Weber, P.C. 1997. Thermodynamic and structural analysis of phosphotyrosine polypeptide binding to Grb2-SH2. Biochemistry 36: 10006-10014.
40. Mercier, P., Spyracopoulos, L., and Sykes, B.D. 2001. Structure, dynamics, and thermodynamics of the structural domain of troponin C in complex with the regulatory peptide 1-40 of troponin I. Biochemistry 40: 10063-10077.
41. Mittag, T., Schaffhausen, B., and Gunther, U.L. 2003. Direct observation of protein-ligand interaction kinetics. Biochemistry 42: 11128-11136.
42. Morrione, A., Plant, P., Valentinis, B., Staub, O., Ku, S., Rotin, D., and Baserga, R. 1999. mGrb10 interacts with Nedd4. J. Biol. Chem. 274: 24094-24099.
43. Nantel, A., Mohammad-Ali, K., Sherk, J., Posner, B.I., and Thomas, D.Y. 1998. Interaction of the Grb10 adapter protein with the Raf1 and MEK1 kinases. J. Biol. Chem. 273: 10475-10484.
44. Nicholson, L.K., Yamazaki, T., Torchia, D.A., Grzesiek, S., Bax, A., Stahl, S.J., Kaufman, J.D., Wingfield, P.T., Lam, P.Y., Jadhav, P.K., et al. 1995. Flexibility and function in HIV-1 protease. Nat. Struct. Biol. 2: 274-280.
45. Nioche, P., Liu, W.Q., Broutin, I., Charbonnier, F., Latreille, M.T., Vidal, M., Roques, B., Garbay, C., and Ducruix, A. 2002. Crystal structures of the SH2 domain of Grb2: Highlight on the binding of a new high-affinity inhibitor. J. Mol. Biol. 315: 1167-1177.
46. O'Brien, R., Rugman, P., Renzoni, D., Layton, M., Handa, R., Hilyard, K., Waterfield, M.D., Driscoll, P.C., and Ladbury, J.E. 2000. Alternative modes of binding of proteins with tandem SH2 domains. Protein Sci. 9: 570-579.
47. Ogura, K., Tsuchiya, S., Terasawa, H., Yuzawa, S., Hatanaka, H., Mandiyan, V., Schlessinger, J., and 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.
48. Orekhov, V.Y., Nolde, D.E., Golovanov, A.P., Korzhnev, D.M., and Arseniev, A.S. 1995. Processing of heteronuclear NMR relaxation with the new software DASHA. Appl. Magn. Reson. 9: 581-588.
49. Panayotou, G., Gish, G., End, P., Truong, O., Gout, I., Dhand, R., Fry, M.J., Hiles, I., Pawson, T., and Waterfield, M.D. 1993. Interactions between SH2 domains and tyrosine-phosphorylated platelet-derived growth factor β-receptor sequences: Analysis of kinetic parameters by a novel biosensor-based approach. Mol. Cell Biol. 13: 3567-3576.
50. Pandey, A., Duan, H., Di Fiore, P.P., and Dixit, V.M. 1995. The Ret receptor protein tyrosine kinase associates with the SH2-containing adapter protein Grb10. J. Biol. Chem. 270: 21461-21463.
51. Pascal, S.M., Singer, A.U., Gish, G., Yamazaki, T., Shoelson, S.E., Pawson, T., Kay, L.E., and Forman-Kay, J.D. 1994. Nuclear magnetic resonance structure of an SH2 domain of phospholipase C-γ 1 complexed with a high affinity binding peptide. Cell 77: 461-472.
52. Pawley, N.H., Koide, S., and Nicholson, L.K. 2002. Backbone dynamics and thermodynamics of Borrelia outer surface protein A. J. Mol. Biol. 324: 991-1002.
53. Philo, J.S. 2000. A method for directly fitting the timer derivative of sedimentation velocity data and an alternative algorithm for calculating sedimentation coefficient distribution functions. Anal. Biochem. 279: 151-163.
54. Privalov, P.L., Gill, S.J., and Murphy, K.P. 1990. The meaning of hydrophobicity: Response to Dill. Science 250: 297-298.
55. Rahuel, J., Garcia-Echeverria, C., Furet, P., Strauss, A., Caravatti, G., Fretz, H., Schoepfer, J., and Gay, B. 1998. Structural basis for the high affinity of amino-aromatic SH2 phosphopeptide ligands. J. Mol. Biol. 279: 1013-1022.
56. Schneider, D.M., Dellwo, M.J., and Wand, A.J. 1992. Fast internal mainchain dynamics of human ubiquitin. Biochemistry 31: 3645-3652.
57. Shen, T.L. and Guan, J.L. 2001. Differential regulation of cell migration and cell cycle progression by FAK complexes with Src, PI3K, Grb7 and Grb2 in focal contacts. FEBS Lett. 499: 176-181.
58. Stein, D., Wu, J., Fuqua, S.A., Roonprapunt, C., Yajnik, V., D'Eustachio, P., Moskow, J.J., Buchberg, A.M., Osborne, C.K., and Margolis, B. 1994. The SH2 domain protein GRB-7 is co-amplified, overexpressed and in a tight complex with HER2 in breast cancer. EMBO J. 13: 1331-1340.
59. Stein, E.G., Ghirlando, R., and Hubbard, S.R. 2003. Structural basis for dimerization of the Grb10 Src homology 2 domain. Implications for ligand specificity. J. Biol. Chem. 278: 13257-13264.
60. 15N NMR relaxation measurements. Biochemistry 31: 4394-4406.
61. Suenaga, A., Hatakeyama, M., Ichikawa, M., Yu, X., Futatsugi, N., Narumi, T., Fukui, K., Terada, T., Taiji, M., Shirouzu, M., et al. 2003. Molecular dynamics, free energy, and SPR analyses of the interactions between the SH2 domain of Grb2 and ErbB phosphotyrosyl peptides. Biochemistry 42: 5195-5200.
62. Venable, R.M. and Pastor, R.W. 1988. Frictional models for stochastic simulations of proteins. Biopolymers 27: 1001-1014.
63. Waksman, G., Shoelson, S.E., Pant, N., Cowburn, D., and Kuriyan, J. 1993. Binding of a high affinity phosphotyrosyl peptide to the Src SH2 domain: Crystal structures of the complexed and peptide-free forms. Cell 72: 779-790.
64. Wang, J., Dai, H., Yousaf, N., Moussaif, M., Deng, Y., Boufelliga, A., Swamy, O.R., Leone, M.E., and Riedel, H. 1999. Grb10, a positive, stimulatory signaling adapter in platelet-derived growth factor BB-, insulin-like growth factor I-, and insulin-mediated mitogenesis. Mol. Cell Biol. 19: 6217-6228.
65. Wiseman, T., Williston, S., Brandts, J.F., and Lin, L.N. 1989. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179: 131-137.
66. Wojcik, J., Girault, J.A., Labesse, G., Chomilier, J., Mornon, J.P., and Callebaut, I. 1999. Sequence analysis identifies a ras-associating (RA)-like domain in the N-termini of band 4.1/JEF domains and in the Grb7/10/14 adapter family. Biochem. Biophys. Res. Commun. 259: 113-120.
67. Zhang, Y., Akilesh, S., and Wilcox, D.E. 2000. Isothermal titration calorimetry measurements of Ni(II) and Cu(II) binding to His, GlyGlyHis, HisGlyHis, and bovine serum albumin: A critical evaluation. Inorg. Chem. 39: 3057-3064.