Structural characterization of Lyn-SH3 domain in complex with a herpesviral protein reveals an extended recognition motif that enhances binding affinity

Protein Science

Volumn 14, Issue 10, 2005, Pages 2487-2498

  Bauer, Finn ^a,b   Schweimer, Kristian ^a   Meiselbach, Heike ^b   Hoffmann, Silke ^a,c,d   Rösch, Paul ^a   Sticht, Heinrich ^b  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Complex; Docking proteins; Extended binding motif; Fluorescence; Ligand affinity; Lyn; NMR; NMR spectroscopy; SH3 domain; Structure

Indexed keywords

LEUCINE; PROLINE; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; VIRUS PROTEIN;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; ENHANCER REGION; HYDROPHOBICITY; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SRC HOMOLOGY DOMAIN; STRUCTURE ANALYSIS;

MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES; VIRAL PROTEINS;

EID: 25844525760     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.051563605     Document Type: Article

References (45)

1. Arold, S., Franken, P., Strub, M.P., Hoh, F., Benichou, S., Benarous, R., and Dumas, C. 1997. The crystal structure of HIV-1 Nef protein bound to the Fyn kinase SH3 domain suggests a role for this complex in altered T cell receptor signaling. Structure 5: 1361-1372.
2. Bauer, F., Hofinger, E., Hoffmann, S., Rösch, P., Schweimer, K., and Sticht, H. 2004. Characterization of Lck-binding elements in the herpesviral regulatory Tip protein. Biochemistry 43: 14932-14939.
3. Bax, A., Kontaxis, G., and Tjandra, N. 2001. Dipolar couplings in macromolecular structure determination. Methods Enzymol. 339: 127-174.
4. Cavanagh, J., Fairbrother, W.J., Palmer III, A.G., and Skelton, N.J. 1996. Protein NMR spectroscopy. Academic Press, New York.
5. Chakrabartty, A., Doig, A.J., and Baldwin, R.L. 1993. Helix capping propensities in peptides parallel those in proteins. Proc. Natl. Acad. Sci. 90: 11332-11336.
6. Clore, G.M., Gronenborn, A.M., Nilges, M., and Ryan, C.A. 1987. Three-dimensional structure of potato carboxypeptidase inhibitor in solution. A study using nuclear magnetic resonance, distance geometry, and restrained molecular dynamics. Biochemistry 26: 8012-8023.
7. 13C-edited nuclear Overhauser enhancement spectroscopy of a protein in solution: Application to interleukin 1 β. Biochemistry 30: 12-18.
8. 1H groups with pulsed-field gradients and preservation of coherence pathways. J. Magn. Reson. 111: 121-126.
9. Dutta, K., Shi, H., Cruz-Chu, E.R., Kami, K., and Ghose, R. 2004. Dynamic influences on a high-affinity, high-specificity interaction involving the C-terminal SH3 domain of p67phox. Biochemistry 43: 8094-8106.
10. Fazi, B., Cope, M.J., Douangamath, A., Ferracuti, S., Schirwitz, K., Zucconi, A., Drubin, D.G., Wilmanns, M., Cesareni, G., and Castagnoli, L. 2002. Unusual binding properties of the SH3 domain of the yeast actin-binding protein Abp1: Structural and functional analysis. J. Biol. Chem. 277: 5290-5298.
11. Feng, S., Chen, J.K., Yu, H., Simon, J.A., and Schreiber, S.L. 1994. Two binding orientations for peptides to the Src SH3 domain: Development of a general model for SH3-ligand interactions. Science 266: 1241-1247.
12. Feng, S., Kasahara, C., Rickles, R.J., and Schreiber, S.L. 1995. Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc. Natl. Acad. Sci. 92: 12408-12415.
13. Folmer, R.H., Hilbers, C.W., Konings, R.N., and Nilges, M. 1997. Floating stereospecific assignment revisited: Application to an 18 kDa protein and comparison with J-coupling data. J. Biomol. NMR 9: 245-258.
14. Ghose, R., Shekhtman, A., Goger, M.J., Ji, H., and Cowburn, D. 2001. A novel, specific interaction involving the Csk SH3 domain and its natural ligand. Nat. Struct. Biol. 8: 998-1004.
15. 2O in protein NMR. Application to sensitivity enhancement and NOE measurements. J. Am. Chem. Soc. 115: 12593-12594.
16. Hutchinson, E.G. and Thornton, J.M. 1996. PROMOTIF - A program to identify and analyze structural motifs in proteins. Protein Sci. 5: 212-220.
17. Kabsch, W. and Sander, C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
18. Karplus, M. 1959. Contact electron-spin coupling of nuclear magnetic moments. J. Chem. Phys. 30: 11-15.
19. Kay, L.E., Clore, G.M., Bax, A., and Gronenborn, A.M. 1990. Four-dimensional heteronuclear triple-resonance NMR spectroscopy of interleukin-1 β in solution. Science 249: 411-414.
20. Kollman, P.A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., et al. 2000. Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Acc. Chem. Res. 33: 889-897.
21. Koradi, R., Billeter, M., and Wuthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14: 51-55, 29-32.
22. Larson, S.M. and Davidson, A.R. 2000. The identification of conserved interactions within the SH3 domain by alignment of sequences and structures. Protein Sci. 9: 2170-2180.
23. Laskowski, R.A., Rullmann, J.A., MacArthur, M.W., Kaptein, R., and Thornton, J.M. 1996. AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8: 477-486.
24. Lee, C.H., Saksela, K., Mirza, U.A., Chait, B.T., and Kuriyan, J. 1996. Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell 85: 931-942.
25. Lim, W.A., Richards, F.M., and Fox, R.O. 1994. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature 372: 375-379.
26. Morton, C.J. and Campbell, I.D. 1994. SH3 domains. Molecular "Velcro." Curr. Biol. 4: 615-617.
27. Nilges, M. and O'Donoghue, S.I. 1998. Ambiguous NOEs and automated NOE assignment. Prog. Nucl. Mag. Res. Sp. 32: 107-139.
28. HN α for identification of helical secondary structure. J. Mol. Biol. 180: 741-751.
29. Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham 3rd, T.E., DeBolt, S., Ferguson, D., Seibel, G., and Kollman, P. 1995. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun. 91: 1-41.
30. Pisabarro, M.T. and Serrano, L. 1996. Rational design of specific high-affinity peptide ligands for the Abl-SH3 domain. Biochemistry 35: 10634-10640.
31. Pisabarro, M.T., Serrano, L., and Wilmanns, M. 1998. Crystal structure of the abl-SH3 domain complexed with a designed high-affinity peptide ligand: Implications for SH3-ligand interactions. J. Mol. Biol. 281: 513-521.
32. Posern, G., Zheng, J., Knudsen, B.S., Kardinal, C., Muller, K.B., Voss, J., Shishido, T., Cowburn, D., Cheng, G., Wang, B., et al. 1998. Development of highly selective SH3 binding peptides for Crk and CRKL which disrupt Crk-complexes with DOCK180, SoS and C3G. Oncogene 16: 1903-1912.
33. Reiss, C., Niedobitek, G., Hör, S., Lisner, R., Friedrich, U., Bodemer, W., and Biesinger, B. 2002. Peripheral T-cell lymphoma in herpesvirus saimiri-infected tamarins: Tumor cell lines reveal subgroup-specific differences. Virology 294: 31-46.
34. Rocchia, W., Alexov, E., and Honig, B. 2001. Extending the applicability of the nonlinear Poisson-Boltzmann equation: Multiple dielectric constants and multivalent ions. J. Phys. Chem. 105: 6507-6514.
35. Rocchia, W., Sridharan, S., Nicholls, A., Alexov, E., Chiabrera, A., and Honig, B. 2002. Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: Applications to the molecular systems and geometric objects. J. Comput. Chem. 23: 128-137.
36. Sattler, M., Schleucher, J., and Griesinger, C. 1999. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field grandients. Prog. Nucl. Mag. Res. Sp. 34: 93-158.
37. Schweimer, K., Hoffmann, S., Bauer, F., Friedrich, U., Kardinal, C., Feller, S.M., Biesinger, B., and Sticht, H. 2002. Structural investigation of the binding of a herpesviral protein to the SH3 domain of tyrosine kinase Lck. Biochemistry 41: 5120-5130.
38. Schwieters, C.D., Kuszewski, J.J., Tjandra, N., and Clore, G.M. 2003. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160: 65-73.
39. Srinivasan, J., Cheatham III, T.E., Cieplak, P., Kollman, P.A., and Case, D.A. 1998. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices. J. Am. Chem. Soc. 120: 9401-9409.
40. Talluri, S. and Wagner, G. 1996. An optimized 3D NOESY-HSQC. J. Magn. Reson. 112: 200-205.
41. 13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nat. Struct. Biol. 4: 732-738.
42. Wallace, A.C., Laskowski, R.A., and Thornton, J.M. 1995. LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8: 127-134.
43. Wang, W., Lim, W.A., Jakalian, A., Wang, J., Wang, J., Luo, R., Bayly, C.I., and Kollman, P.A. 2001. An analysis of the interactions between the Sem-5 SH3 domain and its ligands using molecular dynamics, free energy calculations, and sequence analysis. J. Am. Chem. Soc. 123: 3986-3994.
44. Wartha, F., Horn, A.H.C., Meiselbach, H., and Sticht H. 2005. Molecular dynamics simulations of HIV-1 protease suggest different mechanisms contributing to drug resistance. J. Chem. Theory Comput. 1: 315-324.
45. Yu, H., Chen, J.K., Feng, S., Dalgarno, D.C., Brauer, A.W., and Schreiber, S.L. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76: 933-945.