Crystallographic and nuclear magnetic resonance evaluation of the impact of peptide binding to the second PDZ domain of protein tyrosine phosphatase 1E

Biochemistry

Volumn 49, Issue 43, 2010, Pages 9280-9291

  Zhang, Jun ^a   Sapienza, Paul J ^b   Ke, Hengming ^a   Chang, Aram ^c   Hengel, Sarah R ^d   Wang, Huanchen ^a   Phillips, George N ^c   Lee, Andrew L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b University of North Carolina   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d School of Health Science   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC MODEL; ALLOSTERY; ATOMIC COORDINATE; BIOPHYSICAL PROPERTIES; C-TERMINAL PEPTIDES; COMPLEX ENERGY LANDSCAPES; DATA SUPPORT; FUNCTIONAL TRANSITIONS; LIGAND BINDING; LOCK-AND-KEY; LONG-RANGE COMMUNICATIONS; LONG-RANGE PROPAGATION; NMR RELAXATION; NMR STRUCTURES; PDZ DOMAINS; PEPTIDE BINDING; PROTEIN-TYROSINE PHOSPHATASE; RELAXATION DISPERSION; RESIDUAL DIPOLAR COUPLINGS; SCAFFOLDING PROTEINS; SIDE-CHAIN DYNAMICS; STRUCTURAL CHANGE; TIME-AVERAGED; UBIQUITOUS PROTEIN; X RAY CRYSTAL STRUCTURES;

AMINO ACIDS; BINDING ENERGY; LIGANDS; MAGNETIC DOMAINS; NUCLEAR MAGNETIC RESONANCE; PEPTIDES; PHOSPHATASES; RESONANCE; SIGNAL TRANSDUCTION;

CRYSTAL ATOMIC STRUCTURE;

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR 2; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 13; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; CRYSTAL STRUCTURE; CRYSTALLIZATION; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HUMANS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; PDZ DOMAINS; PEPTIDES; PROTEIN BINDING; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 13;

EID: 78049307619     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101131f     Document Type: Article

References (87)

1. Kim, E. and Sheng, M. (2004) PDZ domain proteins of synapses Nat. Rev. Neurosci. 5, 771-781
2. Sheng, M. and Sala, C. (2001) PDZ domains and the organization of supramolecular complexes Annu. Rev. Neurosci. 24, 1-29
3. Ponting, C. P. (1997) Evidence for PDZ domains in bacteria, yeast, and plants Protein Sci. 6, 464-468
4. van Ham, M. and Hendriks, W. (2003) PDZ domains: Glue and guide Mol. Biol. Rep. 30, 69-82
5. Peterson, F. C., Penkert, R. R., Volkman, B. F., and Prehoda, K. E. (2004) Cdc42 regulates the Par-6 PDZ domain through an allosteric CRIB-PDZ transition Mol. Cell 13, 665-676
6. Sohn, J., Grant, R. A., and Sauer, R. T. (2007) Allosteric activation of DegS, a stress sensor PDZ protease Cell 131, 572-583
7. Zhang, M. (2007) Scaffold proteins as dynamic switches Nat. Chem. Biol. 3, 756-757
8. van den Berk, L. C., Landi, E., Walma, T., Vuister, G. W., Dente, L., and Hendriks, W. J. (2007) An allosteric intramolecular PDZ-PDZ interaction modulates PTP-BL PDZ2 binding specificity Biochemistry 46, 13629-13637
9. Petit, C. M., Zhang, J., Sapienza, P. J., Fuentes, E. J., and Lee, A. L. (2009) Hidden dynamic allostery in a PDZ domain Proc. Natl. Acad. Sci. U.S.A. 106, 18249-18254
10. Yan, J., Pan, L., Chen, X., Wu, L., and Zhang, M. (2010) The structure of the harmonin/sans complex reveals an unexpected interaction mode of the two Usher syndrome proteins Proc. Natl. Acad. Sci. U.S.A. 107, 4040-4045
11. Qian, Y. and Prehoda, K. E. (2006) Interdomain interactions in the tumor suppressor discs large regulate binding to the synaptic protein GukHolder J. Biol. Chem. 281, 35757-35763
12. Li, J., Callaway, D. J., and Bu, Z. (2009) Ezrin induces long-range interdomain allostery in the scaffolding protein NHERF1 J. Mol. Biol. 392, 166-180
13. Bezprozvanny, I. and Maximov, A. (2001) PDZ domains: More than just a glue Proc. Natl. Acad. Sci. U.S.A. 98, 787-789
14. Mishra, P., Socolich, M., Wall, M. A., Graves, J., Wang, Z., and Ranganathan, R. (2007) Dynamic scaffolding in a G protein-coupled signaling system Cell 131, 80-92
15. Lockless, S. W. and Ranganathan, R. (1999) Evolutionarily conserved pathways of energetic connectivity in protein families Science 286, 295-299
16. Fuentes, E. J., Der, C. J., and Lee, A. L. (2004) Ligand-dependent dynamics and intramolecular signaling in a PDZ domain J. Mol. Biol. 335, 1105-1115
17. Fuentes, E. J., Gilmore, S. A., Mauldin, R. V., and Lee, A. L. (2006) Evaluation of energetic and dynamic coupling networks in a PDZ domain protein J. Mol. Biol. 364, 337-351
18. Gianni, S., Walma, T., Arcovito, A., Calosci, N., Bellelli, A., Engstrom, A., Travaglini-Allocatelli, C., Brunori, M., Jemth, P., and Vuister, G. W. (2006) Demonstration of long-range interactions in a PDZ domain by NMR, kinetics, and protein engineering Structure 14, 1801-1809
19. Ota, N. and Agard, D. A. (2005) Intramolecular signaling pathways revealed by modeling anisotropic thermal diffusion J. Mol. Biol. 351, 345-354
20. Sharp, K. and Skinner, J. J. (2006) Pump-probe molecular dynamics as a tool for studying protein motion and long range coupling Proteins 65, 347-361
21. Ho, B. K. and Agard, D. A. (2009) Probing the flexibility of large conformational changes in protein structures through local perturbations PLoS Comput. Biol. 5, e1000343
22. Kong, Y. and Karplus, M. (2009) Signaling pathways of PDZ2 domain: A molecular dynamics interaction correlation analysis Proteins 74, 145-154
23. Ho, B. K. and Agard, D. A. (2010) Conserved tertiary couplings stabilize elements in the PDZ fold, leading to characteristic patterns of domain conformational flexibility Protein Sci. 19, 398-411
24. Doyle, D. A., Lee, A., Lewis, J., Kim, E., Sheng, M., and MacKinnon, R. (1996) Crystal structures of a complexed and peptide-free membrane protein-binding domain: Molecular basis of peptide recognition by PDZ Cell 85, 1067-1076
25. Cooper, A. and Dryden, D. T. (1984) Allostery without conformational change. A plausible model Eur. Biophys. J. 11, 103-109
26. Kozlov, G., Gehring, K., and Ekiel, I. (2000) Solution structure of the PDZ2 domain from human phosphatase hPTP1E and its interactions with C-terminal peptides from the Fas receptor Biochemistry 39, 2572-2580
27. Kozlov, G., Banville, D., Gehring, K., and Ekiel, I. (2002) Solution structure of the PDZ2 domain from cytosolic human phosphatase hPTP1E complexed with a peptide reveals contribution of the β2-β3 loop to PDZ domain-ligand interactions J. Mol. Biol. 320, 813-820
28. Walma, T., Spronk, C. A., Tessari, M., Aelen, J., Schepens, J., Hendriks, W., and Vuister, G. W. (2002) Structure, dynamics and binding characteristics of the second PDZ domain of PTP-BL J. Mol. Biol. 316, 1101-1110
29. Niv, M. Y. and Weinstein, H. (2005) A flexible docking procedure for the exploration of peptide binding selectivity to known structures and homology models of PDZ domains J. Am. Chem. Soc. 127, 14072-14079
30. Basdevant, N., Weinstein, H., and Ceruso, M. (2006) Thermodynamic basis for promiscuity and selectivity in protein-protein interactions: PDZ domains, a case study J. Am. Chem. Soc. 128, 12766-12777
31. Gerek, Z. N., Keskin, O., and Ozkan, S. B. (2009) Identification of specificity and promiscuity of PDZ domain interactions through their dynamic behavior Proteins 77, 796-811
32. Gerek, Z. N. and Ozkan, S. B. (2010) A flexible docking scheme to explore the binding selectivity of PDZ domains Protein Sci. 19, 914-928
33. Stiffler, M. A., Chen, J. R., Grantcharova, V. P., Lei, Y., Fuchs, D., Allen, J. E., Zaslavskaia, L. A., and MacBeath, G. (2007) PDZ domain binding selectivity is optimized across the mouse proteome Science 317, 364-369
34. Dev, K. K. (2004) Making protein interactions druggable: Targeting PDZ domains Nat. Rev. Drug Discovery 3, 1047-1056
35. Wang, N. X., Lee, H. J., and Zheng, J. J. (2008) Therapeutic use of PDZ protein-protein interaction antagonism Drug News Perspect. 21, 137-141
36. Jemth, P. and Gianni, S. (2007) PDZ domains: Folding and binding Biochemistry 46, 8701-8708
37. Gianni, S., Geierhaas, C. D., Calosci, N., Jemth, P., Vuister, G. W., Travaglini-Allocatelli, C., Vendruscolo, M., and Brunori, M. (2007) A PDZ domain recapitulates a unifying mechanism for protein folding Proc. Natl. Acad. Sci. U.S.A. 104, 128-133
38. Calosci, N., Chi, C. N., Richter, B., Camilloni, C., Engstrom, A., Eklund, L., Travaglini-Allocatelli, C., Gianni, S., Vendruscolo, M., and Jemth, P. (2008) Comparison of successive transition states for folding reveals alternative early folding pathways of two homologous proteins Proc. Natl. Acad. Sci. U.S.A. 105, 19241-19246
39. Milev, S., Bjelic, S., Georgiev, O., and Jelesarov, I. (2007) Energetics of peptide recognition by the second PDZ domain of human protein tyrosine phosphatase 1E Biochemistry 46, 1064-1078
40. Rao, F. and Karplus, M. (2010) Protein dynamics investigated by inherent structure analysis Proc. Natl. Acad. Sci. U.S.A. 107, 9152-9157
41. De Los Rios, P., Cecconi, F., Pretre, A., Dietler, G., Michielin, O., Piazza, F., and Juanico, B. (2005) Functional dynamics of PDZ binding domains: A normal-mode analysis Biophys. J. 89, 14-21
42. Dhulesia, A., Gsponer, J., and Vendruscolo, M. (2008) Mapping of two networks of residues that exhibit structural and dynamical changes upon binding in a PDZ domain protein J. Am. Chem. Soc. 130, 8931-8939
43. Dreier, L. and Wider, G. (2006) Concentration measurements by PULCON using X-filtered or 2D NMR spectra Magn. Reson. Chem. 44 ((Spec. No.)) S206-S212
44. Wider, G. and Dreier, L. (2006) Measuring protein concentrations by NMR spectroscopy J. Am. Chem. Soc. 128, 2571-2576
45. Dick, F. (1994) Acid cleavage/deprotection in Fmoc/tBu solid-phase peptide synthesis Methods Mol. Biol. 35, 63-72
46. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
47. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
48. Collaborative Computational Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
49. von Ossowski, I., Oksanen, E., von Ossowski, L., Cai, C., Sundberg, M., Goldman, A., and Keinanen, K. (2006) Crystal structure of the second PDZ domain of SAP97 in complex with a GluR-A C-terminal peptide FEBS J. 273, 5219-5229
50. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
51. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
52. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
53. Painter, J. and Merritt, E. A. (2006) TLSMD web server for the generation of multi-group TLS models J. Appl. Crystallogr. 39, 109-111
54. 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
55. Johnson, B. A. and Blevins, R. A. (1994) NMR View: A computer program for the visualization and analysis of NMR data J. Biomol. NMR 4, 603-614
56. Ottiger, M., Delaglio, F., and Bax, A. (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra J. Magn. Reson. 131, 373-378
57. Sass, H. J., Musco, G., Stahl, S. J., Wingfield, P. T., and Grzesiek, S. (2000) Solution NMR of proteins within polyacrylamide gels: Diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes J. Biomol. NMR 18, 303-309
58. Valafar, H. and Prestegard, J. H. (2004) REDCAT: A residual dipolar coupling analysis tool J. Magn. Reson. 167, 228-241
59. Loria, J. P., Rance, M., and Palmer, A. G., III (1999) A TROSY CPMG sequence for characterizing chemical exchange in large proteins J. Biomol. NMR 15, 151-155
60. Mauldin, R. V., Carroll, M. J., and Lee, A. L. (2009) Dynamic dysfunction in dihydrofolate reductase results from antifolate drug binding: Modulation of dynamics within a structural state Structure 17, 386-394
61. Palmer, A. G., III, Kroenke, C. D., and Loria, J. P. (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules Methods Enzymol. 339, 204-238
62. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease Biochemistry 28, 8972-8979
63. Gao, X., Satoh, T., Liao, Y., Song, C., Hu, C. D., Kariya, K., and Kataoka, T. (2001) Identification and characterization of RA-GEF-2, a Rap guanine nucleotide exchange factor that serves as a downstream target of M-Ras J. Biol. Chem. 276, 42219-42225
64. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797
65. Krojer, T., Garrido-Franco, M., Huber, R., Ehrmann, M., and Clausen, T. (2002) Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine Nature 416, 455-459
66. Andrec, M., Snyder, D. A., Zhou, Z., Young, J., Montelione, G. T., and Levy, R. M. (2007) A large data set comparison of protein structures determined by crystallography and NMR: Statistical test for structural differences and the effect of crystal packing Proteins 69, 449-465
67. Wang, J., Zuo, X., Yu, P., Byeon, I. J., Jung, J., Wang, X., Dyba, M., Seifert, S., Schwieters, C. D., Qin, J., Gronenborn, A. M., and Wang, Y. X. (2009) Determination of multicomponent protein structures in solution using global orientation and shape restraints J. Am. Chem. Soc. 131, 10507-10515
68. Bax, A. (2003) Weak alignment offers new NMR opportunities to study protein structure and dynamics Protein Sci. 12, 1-16
69. Cornilescu, G. and Bax, A. (1998) Validation of Protein Structure from Anisotropic Carbonyl Chemical Shifts in a Dilute Liquid Crystalline Phase J. Am. Chem. Soc. 120, 6836-6837
70. Cornilescu, G. and Bax, A. (2000) Measurement of Proton, Nitrogen, and Carbonyl Chemical Shielding Anisotropies in a Protein Dissolved in a Dilute Liquid Crystalline Phase J. Am. Chem. Soc. 122, 10143-10154
71. Stacklies, W., Vega, M. C., Wilmanns, M., and Grater, F. (2009) Mechanical network in titin immunoglobulin from force distribution analysis PLoS Comput. Biol. 5, e1000306
72. Stacklies, W., Xia, F., and Grater, F. (2009) Dynamic allostery in the methionine repressor revealed by force distribution analysis PLoS Comput. Biol. 5, e1000574
73. Whitley, M. J. and Lee, A. L. (2009) Frameworks for understanding long-range intra-protein communication Curr. Protein Pept. Sci. 10, 116-127
74. Erdmann, K. S., Kuhlmann, J., Lessmann, V., Herrmann, L., Eulenburg, V., Muller, O., and Heumann, R. (2000) The Adenomatous Polyposis Coli-protein (APC) interacts with the protein tyrosine phosphatase PTP-BL via an alternatively spliced PDZ domain Oncogene 19, 3894-3901
75. Smock, R. G. and Gierasch, L. M. (2009) Sending signals dynamically Science 324, 198-203
76. Wand, A. J. (2001) Dynamic activation of protein function: A view emerging from NMR spectroscopy Nat. Struct. Biol. 8, 926-931
77. Tsai, C. J., del Sol, A., and Nussinov, R. (2008) Allostery: Absence of a change in shape does not imply that allostery is not at play J. Mol. Biol. 378, 1-11
78. Mittermaier, A. and Kay, L. E. (2006) New tools provide new insights in NMR studies of protein dynamics Science 312, 224-228
79. Loria, J. P., Berlow, R. B., and Watt, E. D. (2008) Characterization of enzyme motions by solution NMR relaxation dispersion Acc. Chem. Res. 41, 214-221
80. Mittag, T., Schaffhausen, B., and Gunther, U. L. (2003) Direct observation of protein-ligand interaction kinetics Biochemistry 42, 11128-11136
81. Mittag, T., Schaffhausen, B., and Gunther, U. L. (2004) Tracing kinetic intermediates during ligand binding J. Am. Chem. Soc. 126, 9017-9023
82. 15N NMR relaxation dispersion spectroscopy: Binding of an antithrombin peptide to human prothrombin J. Am. Chem. Soc. 125, 12432-12442
83. Hansen, D. F., Vallurupalli, P., Lundstrom, P., Neudecker, P., and Kay, L. E. (2008) Probing chemical shifts of invisible states of proteins with relaxation dispersion NMR spectroscopy: How well can we do? J. Am. Chem. Soc. 130, 2667-2675
84. Niu, X., Chen, Q., Zhang, J., Shen, W., Shi, Y., and Wu, J. (2007) Interesting structural and dynamical behaviors exhibited by the AF-6 PDZ domain upon Bcr peptide binding Biochemistry 46, 15042-15053
85. McElheny, D., Schnell, J. R., Lansing, J. C., Dyson, H. J., and Wright, P. E. (2005) Defining the role of active-site loop fluctuations in dihydrofolate reductase catalysis Proc. Natl. Acad. Sci. U.S.A. 102, 5032-5037
86. Namanja, A. T., Wang, X. J., Xu, B., Mercedes-Camacho, A. Y., Wilson, B. D., Wilson, K. A., Etzkorn, F. A., and Peng, J. W. (2010) Toward flexibility-activity relationships by NMR spectroscopy: Dynamics of Pin1 ligands J. Am. Chem. Soc. 132, 5607-5609
87. Korzhnev, D. M., Neudecker, P., Mittermaier, A., Orekhov, V. Y., and Kay, L. E. (2005) Multiple-site exchange in proteins studied with a suite of six NMR relaxation dispersion experiments: An application to the folding of a Fyn SH3 domain mutant J. Am. Chem. Soc. 127, 15602-15611