Energetics of peptide recognition by the second PDZ domain of human protein tyrosine phosphatase 1E

Biochemistry

Volumn 46, Issue 4, 2007, Pages 1064-1078

  Milev, Stoyan ^a   Bjelić, Saša ^a   Georgiev, Oleg ^a   Jelesarov, Ilian ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL STRUCTURE; EVOLUTIONARY PRESSURE; PDZ DOMAINS; TUMOR SUPPRESSOR;

AMINO ACIDS; CALORIMETRY; ENTHALPY; ENTROPY; MOLECULAR STRUCTURE; SURFACE PLASMON RESONANCE; THERMODYNAMICS; TUMORS;

ENZYMES;

APC PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR RA GEF2; PDZ PROTEIN; PENTADECAPEPTIDE; PROTEIN TYROSINE PHOSPHATASE 1E; PROTEIN TYROSINE PHOSPHATASE EPSILON; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CALORIMETRY; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; ENTHALPY; ENTROPY; HUMAN; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN MOTIF; SIMULATION; SURFACE PLASMON RESONANCE; THERMODYNAMICS; TUMOR SUPPRESSOR GENE;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; DNA, COMPLEMENTARY; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE-PHOSPHATASE; RECOMBINANT PROTEINS; THERMODYNAMICS;

EID: 33846582419     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061869i     Document Type: Article

References (87)

1. Sheng, M., and Sala, C. (2001) PDZ domains and the organization of supramolecular complexes, Annu. Rev. Neurosci. 24, 1-29.
2. Bezprozvanny, I., and Maximov, A. (2001) PDZ domains: More than just a glue, Proc. Natl. Acad. Sci. U.S.A. 98, 787-789.
3. Hung, A. Y., and Sheng, M. (2002) PDZ domains: Structural modules for protein complex assembly, J. Biol. Chem. 277, 5699-5702.
4. Montell, C. (2000) A PDZ protein ushers in new links, Nat. e Genet. 26, 6-7.
5. Nourry, C., Grant, S. G. N., and Borg, J.-P. (2003) PDZ domain proteins: Plug and play!, Sci. STKE 2003, re7.
6. Sherman, D. L., Fabrizi, C., Gillespie, C. S., and Brophy, P. J. (2001) Specific disruption of a Schwann cell dystrophin-related protein complex in a demyelinating neuropathy, Neuron 30, 677-687.
7. Verpy, E., Leibovici, M., Zwaenepoel, I., Liu, X. Z., Gal, A., Salem, N., Mansour, A., Blanchard, S., Kobayashi, I., Keats, B. J. B., Slim, R., and Petit, C. (2000) A defect in harmonin, a PDZ domain-containing protein expressed in the inner ear sensory hair cells, underlies Usher syndrome type 1C, Nat. Genet. 26, 51-55.
8. Bezprozvanny, I., and Maximov, A. (2001) Classification of PDZ domains, FEBS Lett. 509, 457-462.
9. Birrane, G., Chung, J., and Ladias, J. A. A. (2003) Novel mode of ligand recognition by the erbin PDZ domain, J. Biol. Chem. 278, 1399-1402.
10. 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 beta 2-beta 3 loop to PDZ domain-ligand interactions, J. Mol. Biol. 320, 813-820.
11. 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 receptors, Biochemistry 39, 2572-2580.
12. Skelton, N. J., Koehler, M. F. T., Zobel, K., Wong, W. L., Yeh, S., Pisabarro, M. T., Yin, J. P., Lasky, L. A., and Sidhu, S. S. (2003) Origins of PDZ domain ligand specificity: structure determination and mutagenesis of the Erbin PDZ domain, J. Biol. Chem. 278, 7645-7654.
13. Tochio, H., Hung, F., Li, M., Bredt, D. S., and Zhang, M. J. (2000) Solution structure and backbone dynamics of the second PDZ domain of postsynaptic density-95, J. Mol. Biol. 297, 830-830.
14. 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.
15. 2+ ATPase isoform 4b binds to membrane-associated guanylate kinase (MAGUK) proteins via their PDZ (PSD-95/Dlg/ZO-1) domains, J. Biol. Chem. 273, 1591-1595.
16. Songyang, Z., Fanning, A. S., Fu, C., Xu, J., Marfatia, S. M., Chishti, A. H., Crompton, A., Chan, A. C., Anderson, J. M., and Cantley, L. C. (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains, Science 275, 73-77.
17. Ekiel, I., Banville, D., Shen, S. H., and Gehring, K. (1998) Effect of peptide binding on amide proton exchange rates in the PDZ2 domain from human phosphatase hPTP1E, Biochem. Cell. Biol. 76, 334-340.
18. 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.
19. Kang, B. S., Cooper, D. R., Jelen, F., Devedjiev, Y., Derewenda, U., Dauter, Z., Otlewski, J., and Derewenda, Z. S. (2003) PDZ tandem of human syntenin: Crystal structure and functional properties, Structure 11, 459-468.
20. Niethammer, M., Valtschanoff, J. G., Kapoor, T. M., Allison, D. W., Weinberg, R. J., Craig, A. M., and Sheng, M. (1998) CRIPT, a novel postsynaptic protein that binds to the third PDZ domain of PSD-95/SAP90, Neuron 20, 693-707.
21. Lu, J., Li, H., Wang, Y., Sudhof, T. C., and Rizo, J. (2005) Solution structure of the RIM1[alpha] PDZ domain in complex with an ELKS1b C-terminal peptide, J. Mol. Biol. 352, 455-466.
22. Freiss, G., and Vignon, F. (2004) Protein tyrosine phosphatases and breast cancer, CRC Oncol. Hematol. 52, 9-17.
23. Palmer, A., Zimmer, M., Erdmann, K. S., Eulenburg, V., Porthin, A., Heumann, R., Deutsch, U., and Klein, R. (2002) EphrinB phosphorylation and reverse signaling: Regulation by Src kinases and PTP-BL phosphatase, Mol. Cell 9, 725-737.
24. Sato, T., Irie, S., Kitada, S., and Reed, J. C. (1995) FAP-1: a protein tyrosine phosphatase that associates with Fas, Science 268, 411-415.
25. Murthy, K. K., Clark, K., Fortin, Y., Shen, S.-H., and Banville, D. (1999) ZRP-1, a zyxin-related protein, interacts with the second PDZ domain of the cytosolic protein tyrosine phosphatase hPTP1E, J. Biol. Chem. 274, 20679-20687.
26. Gao, X., Satoh, T., Liao, Y., Song, C., Hu, C.-D., Kariya, K.-i., 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.
27. Plotnikov, V. V., Brandts, J. M., Lin, L. N., and Brandts, J. F. (1997) A new ultrasensitive scanning calorimeter, Anal. Biochem. 250, 237-244.
28. Freire, E. (1995) Thermal denaturation methods in the study of protein folding, Methods Enzymol. 259, 144-169.
29. Freire, E., and Biltonen, R. L. (1978) Statistical mechanical deconvolution of thermal transitions in macromolecules. I. Theory and application to homogeneous systems, Biopolymers 17, 463-479.
30. Privalov, P. L., and Potekhin, S. A. (1986) Scanning microcalorimetry in studying temperature-induced changes in proteins, Methods Enzymol. 131, 4-51.
31. Privalov, P. L., and Makhatadze, G. I. (1990) Heat capacity of proteins. II. Partial molar heat capacity of the unfolded polypeptide chain of proteins: Protein unfolding effects, J. Mol. Biol. 213, 385-391.
32. Milev, S., Gorfe, A. A., Karshikoff, A., Clubb, R. T., Bosshard, H. R., and Jelesarov, I. (2003) Energetics of sequence-specific protein-DNA association: Binding of integrase Tn916 to its target DNA, Biochemistry 42, 34813491.
33. Brandts, J. F., and Lin, L. N. (1990) Study of strong to ultratight protein interactions using differential scanning calorimetry, Biochemistry 29, 6927-6940.
34. Bashford, D. (2004) Macroscopic electrostatic models for protonation states in proteins, Front. Biosci. 9, 1082-1099.
35. Lindahl, E., Hess, B., and van der Spoel, D. (2001) GROMACS 3.0: a package for molecular simulation and trajectory analysis, J. Mol. Model. 7, 306-317.
36. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water, J. Chem. Phys. 79, 926-935.
37. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations. J. Comp. Chem. 18, 1463-1472.
38. Miyamoto, S., and Kollman, P. A. (1992) Settle - an analytical version of the shake and rattle algorithm for rigid water models, J. Comput. Chem. 13, 952-962.
39. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald-an N.Log(N) method for Ewald sums in large systems, J. Chem. Phys. 98, 10089-10092.
40. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., and Haak, J. R. (1984) Molecular-dynamics with coupling to an external bath, J. Chem. Phys. 81, 3684-3690.
41. Baker, B. M., and Murphy, K. P. (1998) Prediction of binding energetics from structure using empirical parameterization, Methods Enzymol. 295, 294-315.
42. Luque, I., and Freire, E. (1998) Structure-based prediction of binding affinities and molecular design of peptide ligands, Methods Enzymol. 295, 100-127.
43. Hubbard, S. J., and Thornton, J. M. (1993) NACCESS, Computer Program, Department of Biochemistry and Molecular Biology, University College, London.
44. Yu, Y. B., Privalov, P. L., and Hodges, R. S. (2001) Contribution of translational and rotational motions to molecular association in aqueous solution, Biophys. J. 81, 1632-1642.
45. Antonsson, P., Kammerer, R. A., Schulthess, T., Hanisch, G., and Engel, J. (1995) Stabilization of the alpha-helical coiled-coil domain in laminin by C-terminal disulfide bonds, J. Mol. Biol. 250, 74-79.
46. Bardi, J. S., Luque, I., and Freire, E. (1997) Structure-based thermodynamic analysis of HIV-1 protease inhibitors, Biochemistry 36, 6588-6596.
47. Gomez, J., Hilser, V. J., Xie, D., and Freire, E. (1995) The heat capacity of proteins, Proteins: Struct., Funct., Genet. 22, 404-412.
48. Gianni, S., Calosci, N., Aelen, J. M. A., Vuister, G. W., Brunori, M., and Travaglini-Allocatelli, C. (2005) Kinetic folding mechanism of PDZ2 from PTP-BL, Protein Eng., Des. Sci. 18, 389-395.
49. Makhatadze, G. I., and Privalov, P. L. (1995) Energetics of protein structure, Adv. Protein Chem. 47, 307-425.
50. Robertson, A. D., and Murphy, K. P. (1997) Protein structure and the energetics of protein stability, Chem. Rev. 97, 1251-1267.
51. Haynie, D. T., and Freire, E. (1994) Estimation of the folding/unfolding energetics of marginally stable proteins using differential scanning calorimetry, Anal. Biochem. 216, 33-41.
52. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m-values and heat-capacity changes-relation to changes in accessible surface-areas of protein unfolding, Protein Sci. 4, 2138-2148.
53. Gianni, S., Engstrom, A., Larsson, M., Calosci, N., Malatesta, F., Eklund, L., Ngang, C. C., Travaglini-Allocatelli, C., and Jemth, P. (2005) The kinetics of PDZ domain-ligand interactions and implications for the binding mechanism, J. Biol. Chem. 280, 34805-34812.
54. Saro, D., Klosi, E., Paredes, A., and Spaller, M. R. (2004) Thermodynamic analysis of a hydrophobic binding site: Probing the PDZ domain with nonproteinogenic peptide ligands, Org. Lett. 6, 3429-3432.
55. Marfatia, S. M., MoraisCabral, J. H., Kim, A. C., Byron, O., and Chishti, A. H. (1997) The PDZ domain of human erythrocyte p55 mediates its binding to the cytoplasmic carboxyl terminus of glycophorin C-Analysis of the binding interface by in vitro mutagenesis, J. Biol. Chem. 272, 24191-24197.
56. Gopalakrishnan, M., Forsten-Williams, K., Cassino, T., Padro, L., Ryan, T., and Tãuber, U. (2005) Ligand rebinding: self-consistent mean-field theory and numerical simulations applied to surface plasmon resonance studies, Eur. Biophys. J. 34, 943-958.
57. Nieba, L., Krebber, A., and Pluckthun, A. (1996) Competition BIAcore for measuring true affinities: Large differences from values determined from binding kinetics, Anal. Biochem. 234, 155-165.
58. Carra, J. H., and Privalov, P. L. (1997) Energetics of folding and DNA binding of the MAT alpha homeodomain, Biochemistry 36, 526-535.
59. Celej, M. S., Dassie, S. A., Gonzalez, M., Bianconi, M. L., and Fidelio, G. D. (2006) Differential scanning calorimetry as a tool to estimate binding parameters in multiligand binding proteins, Anal. Biochem. 350, 277-284.
60. Mitkevich, V. A., Schulga, A. A., Ermolyuk, Y. S., Lobachov, V. M., Chekhov, V. O., Yakovlev, G. I., Hartley, R. W., Nick, Pace, C., Kirpichnikov, M. P., and Makarov, A. A. (2003) Thermodynamics of denaturation of complexes of barnase and binase with barstar, Biophys. Chem. 105, 383-390.
61. Plotnikov, V., Rochalski, A., Brandts, M., Brandts, J. F., Williston, S., Frasca, V., and Lin, L. N. (2002) An autosampling differential scanning salorimeter instrument for studying molecular interactions, Assay Drug Dev. Technol. 1 (Part 1), 83-90.
62. Waldron, T. T., and Murphy, K. P. (2003) Stabilization of proteins by ligand binding: Application to drug screening and determination of unfolding energetics, Biochemistry 42, 5058-5064.
63. Rupasinghe, C. N., and Spaller, M. R. (2006) The interplay between structure-based design and combinatorial chemistry, Curr. Opin. Struct. Biol. 10, 1-6.
64. Wiedemann, U., Boisguerin, P., Leben, R., Leitner, D., Krause, G., Moelling, K., Volkmer-Engert, R., and Oschkinat, H. (2004) Quantification of PDZ domain specificity, prediction of ligand affinity and rational design of super-binding peptides, J. Mol. Biol. 343, 703-718.
65. Ruben, A. J., Kiso, Y., and Freire, E. (2006) Overcoming roadblocks in lead optimization: A thermodynamic perspective, Chem. Biol. Drug Des. 67, 2-4.
66. Cummings, M. D., Hart, T. N., and Read, R. J. (1995) Atomic solvation parameters in the analysis of protein-protein docking results, Protein Sci. 4, 2087-2099.
67. Horton, N., and Lewis, M. (1992) Calculation of the free-energy of association for protein complexes, Protein Sci. 1, 169-181.
68. Krystek, S., Stouch, T., and Novotny, J. (1993) Affinity and specificity of serine endopeptidase protein inhibitor interactions-Empirical free-energy calculations based on X-ray crystallographic structures, J. Mol. Biol. 234, 661-679.
69. Luque, I., and Freire, E. (2002) Structural parameterization of the binding enthalpy of small ligands, Proteins: Struct., Funct., Genet. 49, 181-190.
70. Williams, D. H., Cox, J. P. L., Doig, A. J., Gardner, M., Gerhard, U., Kaye, P. T., Lal, A. R., Nicholls, I. A., Salter, C. J., and Mitchell, R. C. (1991) Toward the semiquantitative estimation of binding constants-Guides for peptide peptide binding in aqueous solution, J. Am. Chem. Soc. 113, 7020-7030.
71. Walma, T., Spronk, C. A. E. M., 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.
72. Baker, B. M., and Murphy, K. P. (1997) Dissecting the energetics of a protein-protein interaction: the binding of ovomucoid third domain to elastase, J. Mol. Biol. 268, 557-569.
73. Lavigne, P., Bagu, J. R., Boyko, R., Willard, L., Holmes, C. F., and Sykes, B. D. (2000) Structure-based thermodynamic analysis of the dissociation of protein phosphatase-1 catalytic subunit and microcystin-LR docked complexes, Protein Sci. 9, 252-264.
74. Sturtevant, J. M. (1977) Heat-capacity and entropy changes in processes involving proteins, Proc. Natl. Acad. Sci. U.S.A. 74, 2236-2240.
75. Eftink, M., and Biltonen, R. L. (1980) Thermodynamics of interaction biological systems., in Biological Microcalorimetry (Beezer, A. E., Ed.) pp 343-412, Academic Press, San Diego, CA.
76. Cooper, A., Johnson, C. M., Lakey, J. H., and Nollmann, M. (2001) Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions, Biophys. Chem. 93, 215-230.
77. Privalov, G. P., and Privalov, P. L. (2000) Problems and prospects in microcalorimetry of biological macromolecules, Methods Enzymol. 323, 31-62.
78. Cooper, A. (2005) Heat capacity effects in protein folding and ligand binding: A re-evaluation of the role of water in biomolecular thermodynamics, Biophys. Chem. 115, 89-97.
79. Morton, C. J., and Ladbury, J. E. (1996) Water mediated protein-DNA interactions: The relationship of thermodynamics to structural detail, Protein Sci. 5, 2115-2118.
80. Connelly, P. R. (1997) The Cost of Releasing Site-Specific, Bound Water Molecules from Protein: Towards a Quantitative Guide for Structure-Based Drug Design, Springer, Berlin.
81. Hilser, V. J., Gomez, J., and Freire, E. (1996) Enthalpy change in protein folding and binding: Refinement of parameters for structure-based calculations, Proteins: Struct., Funct., Genet. 26, 123-133.
82. Holdgate, G. A., Tunnicliffe, A., Ward, W. H. J., Weston, S. A., Rosenbrock, G., Barth, P. T., Taylor, I. W. F., Pauptit, R. A., and Timms, D. (1997) The entropic penalty of ordered water accounts for weaker binding of the antibiotic novobiocin to a resistant mutant of DNA gyrase: A thermodynamic and crystallographic study, Biochemistry 36, 9663-9673.
83. Cooper, A., and Dryden, D. T. F. (1984) Allostery without conformational change. A plausible model, Eur. Biophys. J. 11, 103-109.
84. Williams, D. H., Stephens, E., O'Brien, D. P., and Zhou, M. (2004) Understanding noncovalent interactions: Ligand binding energy and catalytic efficiency from ligand-induced reductions in motion within receptors and enzymes, Angew. Chem., Int. Ed. 43, 6596-6616.
85. 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.
86. Sharp, K., and Skinner, J. J. (2006) Pump-probe molecular dynamics as a tool for studying protein motion and long range coupling, Proteins: Struct., Funct., Bioinf. 65, 347-361.
87. Lockless, S. W., and Ranganathan, R. (1999) Evolutionarily conserved pathways of energetic connectivity in protein families, Science 286, 295-299.