Structural insight into the binding diversity between the human Nck2 SH3 domains and proline-rich proteins

Biochemistry

Volumn 45, Issue 23, 2006, Pages 7171-7184

  Liu, Jingxian ^a   Li, Minfen ^b   Ran, Xiaoyuan ^a   Fan, Jing Song ^b   Song, Jianxing ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CELLS; CHEMICAL BONDS; CYTOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; TITRATION;

CYTOSKELETONAL DYNAMICS; HIGH-AFFINITY BINDINGS; HSQC TITRATIONS; LIGAND BINDING; SIGNALING NETWORKS;

PROTEINS;

ADAPTOR PROTEIN; PEPTIDE DERIVATIVE; PROTEIN NCK2; PROTEIN NOGO; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CALORIMETRY; CIRCULAR DICHROISM; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; ONCOGENE PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROPHOTOMETRY, ULTRAVIOLET; SRC HOMOLOGY DOMAINS; THERMODYNAMICS;

EID: 33745016248     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060091y     Document Type: Article

References (86)

1. Holder, N., and Klein, R. (1999) Eph receptors and ephrins: Effectors of morphogenesis, Development 126, 2033-2044.
2. Flanagan, J. G., and Vanderhaeghen, P. (1998) The ephrins and Eph receptors in neural development, Annu. Rev. Neurosci. 21, 309-345.
3. Poliakov, A., Cotrina, M., and Wilkinson, D. G. (2004) Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly, Dev. Cell 7, 465-480.
4. Murai, K. K., and Pasquale, E. B. (2003) 'Eph'ective signaling: Forward, reverse and crosstalk, J. Cell Sci. 116, 2823-2832.
5. Gauthier, L. R., and Robbins, S. M. (2003) Ephrin signaling: One raft to rule them all? One raft to sort them? One raft to spread their call and in signaling bind them? Life Sci. 74, 207-216.
6. Pasquale, E. B. (2005) Eph receptor signalling casts a wide net on cell behaviour, Nat. Rev. Mol. Cell Biol. 6, 462-475.
7. Cowan, C. A., and Henkemeyer, M. (2002) Ephrins in reverse, park and drive, Trends Cell Biol. 12, 339-346.
8. Himanen, J. P., and Nikolov, D. B. (2003) Eph signaling: A structural view, Trends Neurosci. 26, 46-51.
9. Murai, K. K., and Pasquale, E. B. (2002) Can Eph receptors stimulate the mind? Neuron 33, 159-162.
10. Fournier, A. E., and Strittmatter, S. M. (2001) Repulsive factors and axon regeneration in the CNS, Curr. Opin. Neurobiol. 11, 89-94.
11. Sandvig, A., Berry, M., Barrett, L. B., Butt, A., and Logan, A. (2004) Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: Expression, receptor signaling, and correlation with axon regeneration, Glia 46, 225-251.
12. Benson, M. D., Romero, M. I., Lush, M. E., Lu, Q. R., Henkemeyer, M., and Parada, L. F., (2005) Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth, Proc. Natl. Acad. Sci. U.S.A. 102, 10694-10699.
13. Battaglia, A. A., Sehayek, K., Grist, J., McMahon, S. B., and Gavazzi, I. (2003) EphB receptors and ephrin-B ligands regulate spinal sensory connectivity and modulate pain processing, Nat. Neurosci. 6, 339-340.
14. Dodelet, V. C., and Pasquale, E. B. (2000) Eph receptors and ephrin ligands: Embryogenesis to tumorigenesis, Oncogene 19, 5614-5619.
15. Surawska, H., Ma, P. C., and Salgia, R. (2004) The role of ephrins and Eph receptors in cancer, Cytokine Growth Factor Rev. 15, 419-433.
16. Bonaparte, M. I., Dimitrov, A. S., Bossart, K. N., Crameri, G., Mungall, B. A., Bishop, K. A., Choudhry, V., Dimitrov, D. S., Wang, L. F., Eaton, B. T., and Broder, C. C. (2005) Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus, Proc. Natl. Acad. Sci. U.S.A. 102, 10652-10657.
17. Negrete, O. A., Levroney, E. L., Aguilar, H. C., Bertolotti-Ciarlet, A., Nazarian, R., Tajyar, S., and Lee, B. (2005) EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus, Nature 436, 401-405.
18. Lu, Q., Sun, E. E., Klein, R. S., and Flanagan, J. G. (2001) Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction, Cell 105, 69-79.
19. Cowan, C. A., and Henkemeyer, M. (2001) The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals, Nature 413, 174-179.
20. Song, J., Vranken, W., Xu, P., Gingras, R., Noyce, R. S., Yu, Z., Shen, S. H., and Ni, F. (2002) Solution structure and backbone dynamics of the functional cytoplasmic subdomain of human ephrin B2, a cell-surface ligand with bidirectional signaling properties, Biochemistry 41, 10942-10949.
21. Song, J. (2003) Tyrosine phosphorylation of the well packed ephrinB cytoplasmic β-hairpin for reverse signaling. Structural consequences and binding properties, J. Biol. Chem. 278, 24714-24720.
22. Ran, X., and Song, J. (2005) Structural insight into the binding diversity between the Tyr-phosphorylated human ephrinBs and Nck2 SH2 domain, J. Biol. Chem. 280, 19205-19212.
23. McCarty, J. H. (1998) The Nck SH2/SH3 adaptor protein: A regulator of multiple intracellular signal transduction events, BioEssays 20, 913-921.
24. Buday, L. (1999) Membrane-targeting of signalling molecules by SH2/SH3 domain-containing adaptor proteins, Biochim. Biophys. Acta 1422, 187-204.
25. Li, W., and She, H. (2000) The SH2 and SH3 adapter Nck: A two-gene family and a linker between tyrosine kinases and multiple signaling networks, Histol. Histopathol. 15, 947-955.
26. Li, W., Fan, J., and Woodley, D. T. (2001) Nck/Dock: An adapter between cell surface receptors and the actin cytoskeleton, Oncogene 20, 6403-6417.
27. Buday, L., Wunderlich, L., and Tamas, P. (2002) The Nck family of adapter proteins: Regulators of actin cytoskeleton, Cell Signalling 14, 723-731.
28. Braverman, L. E., and Quilliam, L. A. (1999) Identification of Grb4/Nckbeta, a src homology 2 and 3 domain-containing adapter protein having similar binding and biological properties to Nck, J. Biol. Chem. 274, 5542-5549.
29. Tu, Y., Li, F., and Wu, C. (1998) Nck-2, a novel Src homology2/3- containing adaptor protein that interacts with the LIM-only protein PINCH and components of growth factor receptor kinase-signaling pathways, Mol. Biol. Cell 9, 3367-3382.
30. Chen, M., She, H., Kim, A., Woodley, D. T., and Li, W. (2000) Nckβ adapter regulates actin polymerization in NIH 3T3 fibroblasts in response to platelet-derived growth factor bb, Mol. Cell. Biol. 20, 7867-7880.
31. Wei, Z., and Song, J. (2005) Molecular mechanism underlying the thermal stability and pH-induced unfolding of CHABII, J. Mol. Biol. 348, 205-218.
32. Braverman, L. E., and Quilliam, L. A. (1999) Identification of Grb4/Nckbeta, a src homology 2 and 3 domain-containing adapter protein having similar binding and biological properties to Nck, J. Biol. Chem. 274, 5542-5959.
33. Aspenstrom, P. (2002) The WASP-binding protein WIRE has a role in the regulation of the actin filament system downstream of the platelet-derived growth factor receptor, Exp. Cell Res. 279, 21-33.
34. Saras, J., Wollberg, P., and Aspenstrom, P. (2004) Wrch1 is a GTPase-deficient Cdc42-like protein with unusual binding characteristics and cellular effects, Exp. Cell Res. 299, 356-369.
35. Katoh, M. (2002) Molecular cloning and characterization of WRCH2 on human chromosome 15q15, Int. J. Oncol. 20, 977-982.
36. Aspenstrom, P., Fransson, A., and Saras, J. (2004) Rho GTPases have diverse effects on the organization of the actin filament system, Biochem. J. 377 (Part 2), 327-337.
37. Shutes, A., Berzat, A. C., Cox, A. D., and Der, C. J. (2004) Atypical mechanism of regulation of the Wrch-1 Rho family small GTPase, Curr. Biol. 14, 2052-2056.
38. Sattler, M., Schleucher, J., and Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients, Prog. NMR Spectrosc. 34, 93-158.
39. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
40. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
41. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology, J. Biomol. NMR 13, 289-302.
42. Guntert, P. (2004) Automated NMR structure calculation with CYANA, Methods Mol. Biol. 278, 353-378.
43. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse- Kunstleve, R. W., Jiang, J., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
44. Song, J., Gilquin, B., Jamin, N., Drakopoulou, E., Guenneugues, M., Dauplais, M., Vita, C., and Menez, A. (1997) NMR solution structure of a two-disulfide derivative of charybdotoxin: Structural evidence for conservation of scorpion toxin α/β motif and its hydrophobic side chain packing, Biochemistry 36, 3760-3766.
45. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Program for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-486.
46. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55.
47. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-137.
48. Renzoni, D. A., Pugh, D. J. R., Siligardi, G., Das, P., Rossi, C., Waterfield, M. D., Campbell, I. D., and Ladbury, J. E. (1996) Structural and thermodynamic characterization of the interaction of the SH3 domain from Fyn with the proline-rich binding site on the p85 subunit of PI3-kinase, Biochemistry 35, 15646-15653.
49. 15N NMR relaxation, Biochemistry 33, 5984-6003.
50. Yang, D., Mok, Y. K., Forman-Kay, J. D., Farrow, N. A., and Kay, L. E. (1997) Contributions to protein entropy and heat capacity from bond vector motions measured by NMR spin relaxation, J. Mol. Biol. 272, 790-804.
51. Mandel, A. M., Akke, M., and Palmer, A. G., III (1995) Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme, J. Mol. Biol. 246, 144-163.
52. Dosset, P., Hus, J. C., Blackledge, M., and Marion, D. (2000) Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data, J. Biomol. NMR 16, 23-28.
53. Fielding, L., Rutherford, S., and Fletcher, D. (2005) Determination of protein-ligand binding affinity by NMR: Observations from serum albumin model systems, Magn. Reson. Chem. 43, 463-470.
54. Kay, B. K., Williamson, M. P., and Sudol, M. (2000) The importance of being proline: The interaction of proline-rich motifs in signaling proteins with their cognate domains, FASEB J. 14, 231-241.
55. Mayer, B. J. (2001) SH3 domains: Complexity in moderation, J. Cell Sci. 114, 1253-1263.
56. Musacchio, A. (2002) How SH3 domains recognize proline, Adv. Protein Chem. 61, 211-268.
57. Zarrinpar, A., Bhattacharyya, R. P., and Lim, W. A. (2003) The structure and function of proline recognition domains, Sci. STKE 2003, RE8.
58. Cesareni, G., Panni, S., Nardelli, G., and Castagnoli, L. (2002) Can we infer peptide recognition specificity mediated by SH3 domains? FEBS Lett. 513, 38-44.
59. 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.
60. Li, S-C. (2005) Specificity and versatility of SH3 and other proline-recognition domains: Structural basis and implications for cellular signal transduction, Biochem. J. 390, 641-653.
61. Ball, L. J., Kuhne, R., Schneider-Mergener, J., and Oschkinat, H. (2005) Recognition of proline-rich motifs by protein-protein interaction domains, Angew. Chem., Int. Ed. 44, 2852-2869.
62. Venyaminov, S. Y., and Yang, J. T. (1996) Determination of protein secondary structure, in Circular Dichroism and the Conformational Analysis of Biomolecules (Fasman, G. D., Ed.) pp 69-107, Plenum Press, New York.
63. Farrow, N. A., Zhang, O., Forman-Kay, J. D., and Kay, L. E. (1995) Comparison of the backbone dynamics of a folded and an unfolded SH3 domain existing in equilibrium in aqueous buffer, Biochemistry 34, 868-878.
64. Wales, T. E., and Engen, J. R. (2006) Partial Unfolding of Diverse SH3 Domains on a Wide Timescale, J. Mol. Biol. 357, 1592-1604.
65. 15N Chemical Shift Anisotropy Relaxation Interference: Unambiguous Determination of Rotational Diffusion Tensors and Chemical Exchange Effects in Biological Macromolecules, J. Am. Chem. Soc. 120, 7905-7915.
66. 15N chemical shift anisotropies, J. Am. Chem. Soc. 123, 4567-4576.
67. Houtman, J. C., Barda-Saad, M., and Samelson, L. E. (2005) Examining multiprotein signaling complexes from all angles, FEBS Lett. 272, 5426-5435.
68. Vondriska, T. M., Pass, J. M., and Ping, P. (2004) Scaffold proteins and assembly of multiprotein signaling complexes, J. Mol. Cell. Cardiol. 37, 391-397.
69. Burack, W. R., Cheng, A. M., and Shaw, A. S. (2002) Scaffolds, adaptors and linkers of TCR signaling: theory and practice, Curr. Opin. Immunol. 14, 312-316.
70. Mayer, B. J. (1999) Protein-protein interactions in signaling cascades, Mol. Biotechnol. 13, 201-213.
71. Sudol, M. (1998) Physical and functional interactions between the transactivation domain of the hematopoietic transcription factor NF-E2 and WW domains, Oncogene 17, 1469-1474.
72. Pawson, T. (2004) SH2 and SH3 domains: From structure to function, Cell 116, 191-203.
73. Donaldson, L. W., Gish, G., Pawson, T., Kay, L. E., and Forman-Kay, J. D. (2002) Structure of a regulatory complex involving the Abl SH3 domain, the Crk SH2 domain, and a Crk-derived phosphopeptide, Proc. Natl. Acad. Sci. U.S.A. 99, 14053-14058.
74. Machida, K., and Mayer, B. J. (2005) Critical amino acid substitutions in the Src SH3 domain that convert c-Src to be oncogenic, Biochim. Biophys. Acta 1747, 1-25.
75. Mayer, B. J. (1998) Protein-protein interactions in signaling cascades, Methods Mol. Biol. 84, 33-48.
76. Manser, E., Leung, T., Salihuddin, H., Tan, L., and Lim, L. (1993) A non-receptor tyrosine kinase that inhibits the GTPase activity of p21cdc42, Nature 363, 364-367.
77. Zhao, Z. S., Manser, E., and Lim, L. (2000) Interaction between PAK and nck: A template for Nck targets and role of PAK autophosphorylation, Mol. Cell. Biol. 20, 3906-3917.
78. Velyvis, A., Vaynberg, J., Yang, Y., Vinogradova, O., Zhang, Y., Wu, C., and Qin, J. (2003) Structural and functional insights into PINCH LIM4 domain-mediated integrin signaling, Nat. Struct. Biol. 10, 558-564.
79. Vaynberg, J., Fukuda, T., Chen, K., Vinogradova, O., Velyvis, A., Tu, Y., Ng, L., Wu, C., and Qin, J. (2005) Structure of an ultraweak protein-protein complex and its crucial role in regulation of cell morphology and motility, Mol. Cell 17, 513-523.
80. Renzoni, D. A., Pugh, D. J., Siligardi, G., Das, P., Morton, C. J., Rossi, C., Waterfield, M. D., Campbell, I. D., and Ladbury, J. E. (1996) Structural and thermodynamic characterization of the interaction of the SH3 domain from Fyn with the proline-rich binding site on the p85 subunit of PI3-kinase, Biochemistry 35, 15646-15653.
81. Wang, C., Pawley, N. H., and Nicholson, L. K. (2001) The role of backbone motions in ligand binding to the c-Src SH3 domain, J. Mol. Biol. 313, 873-887.
82. Li, M., Shi, J., Wei, Z., Teng, F. Y., Tang, B. L., and Song, J. (2004) Structural characterization of the human Nogo-A functional domains. Solution structure of Nogo-40, a Nogo-66 receptor antagonist enhancing injured spinal cord regeneration, Eur. J. Biochem. 271, 3512-3522.
83. Koeberle, P. D., and Bahr, M. (2004) Growth and guidance cues for regenerating axons: Where have they gone? J. Neurobiol. 59, 162-180.
84. Oertle, T., and Schwab, M. E. (2003) Nogo and its paRTNers, Trends Cell Biol. 13 (4), 187-194.
85. Lee, D. H., Strittmatter, S. M., and Sah, D. W. (2003) Targeting the Nogo receptor to treat central nervous system injuries, Nat. Rev. Drug Discovery 2, 872-878.
86. Voeltz, G. K., Prinz, W. A., Shibata, Y., Rist, J. M., and Rapoport, T. A. (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum, Cell 124, 573-586.