A sequential binding mechanism in a PDZ domain

Biochemistry

Volumn 48, Issue 30, 2009, Pages 7089-7097

  Chi, Celestine N ^a   Bach, Anders ^b   Engström, Åke ^a   Wang, Huiqun ^a   Strømgaard, Kristian ^b   Gianni, Stefano ^c   Jemth, Per ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC PROTEINS; BINDING MECHANISMS; BINDING RATE CONSTANTS; BIPHASIC KINETICS; CONFORMATIONAL CHANGE; CONFORMATIONAL SELECTION; CONTINUOUS-FLOW; INDUCED FIT; INDUCED-FIT MECHANISM; LIGAND BINDING; MULTIPLE CONFORMATIONS; PDZ DOMAINS; PEPTIDE LIGAND; SINGLE-DOMAIN PROTEINS; STOPPED-FLOW TECHNIQUES; TWO-STEP PROCESS; UBIQUITIN;

AMINES; LIGANDS; PROTEINS;

RATE CONSTANTS;

MEMBRANE PROTEIN; PROTEIN SAP97; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FLUOROMETRY; KINETICS; LIGAND BINDING; MOLECULAR MECHANICS; MUTAGENESIS; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; BINDING SITES; DNA-BINDING PROTEINS; HUMANS; LIGANDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS, VIRAL; PDZ DOMAINS; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 68049085520     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900559k     Document Type: Article

References (46)

1. Monod, J., Wyman, J., and Changeux, J. P. (1965) On the Nature of Allosteric Transitions: A Plausible Model. J. Mol. Biol. 12, 88-118.
2. Koshland, D. E.Jr., Nemethy, G., and Filmer, D. (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385.
3. Lange, O. F., Lakomek, N.-A., Fares, C., Schroder, G. F., Walter, K. F. A., Becker, S., Meiler, J., Grubmuller, H., Griesinger, C., and de Groot, B. L. (2008) Recognition Dynamics Up to Microseconds Revealed from an RDC-Derived Ubiquitin Ensemble in Solution. Science 320, 1471-1475. (Pubitemid 351929422)
4. Lancet, D., and Pecht, I. (1976) Kinetic evidence for hapten-induced conformational transition in immunoglobin MOPC 460. Proc. Natl. Acad. Sci. U.S.A. 73, 3549-3553.
5. Berger, C., Weber-Bornhauser, S., Eggenberger, J., Hanes, J., Pluckthun, A., and Bosshard, H. R. (1999) Antigen recognition by conformational selection. FEBS Lett. 450, 149-153.
6. Foote, J., and Milstein, C. (1994) Conformational isomerism and the diversity of antibodies. Proc. Natl. Acad. Sci. U.S.A. 91, 10370-10374.
7. Leopold, P. E., Montal, M., and Onuchic, J. N. (1992) Protein folding funnels: A kinetic approach to the sequence-structure relationship. Proc. Natl. Acad. Sci. U.S.A. 89, 8721-8725.
8. Boehr, D. D., and Wright, P. E. (2008) How do proteins interact?. Science 320, 1429-1430.
9. Stevens, F. J., Chang, C. H., and Schiffer, M. (1988) Dual conformations of an immunoglobulin light-chain dimer: Heterogeneity of antigen specificity and idiotope profile may result from multiple variable-domain interaction mechanisms. Proc. Natl. Acad. Sci. U.S. A. 85, 6895-6899.
10. Wilson, I. A., and Stanfield, R. L. (1994) Antibody-antigen interactions: New structures and new conformational changes. Curr. Opin. Struct. Biol. 4, 857-867.
11. Gsponer, J., Christodoulou, J., Cavalli, A., Bui, J. M., Richter, B., Dobson, C. M., and Vendruscolo, M. (2008) A Coupled Equilibrium Shift Mechanism in Calmodulin-Mediated Signal Transduction. Structure 16, 736-746. (Pubitemid 351615020)
12. Bennett, W. S.Jr., and Steitz, T. A. (1978) Glucose-induced conformational change in yeast hexokinase. Proc. Natl. Acad. Sci. U.S.A. 75, 4848-4852.
13. 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. (Pubitemid 44855631)
14. James, L. C., Roversi, P., and Tawfik, D. S. (2003) Antibody multispecificity mediated by conformational diversity. Science 299, 1362-1367. (Pubitemid 36254643)
15. Pan, H., Lee, J. C., and Hilser, V. J. (2000) Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble. Proc. Natl. Acad. Sci. U.S.A. 97, 12020-12025.
16. Cooper, A., and Dryden, D. T. (1984) Allostery without conformational change. A plausible model. Eur. Biophys. J. 11, 103-109.
17. Lee, A. L., Kinnear, S. A., and Wand, A. J. (2000) Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex. Nat. Struct. Biol. 7, 72-77.
18. Gunasekaran, K., Ma, B., and Nussinov, R. (2004) Is allostery an intrinsic property of all dynamic proteins?. Proteins 57, 433-443. (Pubitemid 39390799)
19. Henzler-Wildman, K. A., Lei, M., Thai, V., Kerns, S. J., Karplus, M., and Kern, D. (2007) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450, 913-916. (Pubitemid 350231333)
20. Jemth, P., and Gianni, S. (2007) PDZ domains: Folding and binding. Biochemistry 46, 8701-8708.
21. 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.
22. Saro, D., Li, T., Rupasinghe, C., Paredes, A., Caspers, N., and Spaller, M. R. (2007) A thermodynamic ligand binding study of the third PDZ domain (PDZ3) from the mammalian neuronal protein PSD-95. Biochemistry 46, 6340-6352. (Pubitemid 46842877)
23. 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.
24. 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.
25. Bach, A., Chi, C. N., Olsen, B. T., Pedersen, W. S., Roder, U. M., Pang, F. G., Clausen, P. R., Jemth, P., and Strømgaard, K. (2008) Modified Peptides as Potent Inhibitors of the PSD-95/NMDA Receptor Interaction. J. Med. Chem. 51, 6450-6459.
26. Chi, C. N., Engström, Å., Gianni, S., Larsson, M., and Jemth, P. (2006) Two conserved residues govern the salt and pH dependencies of the binding reaction of a PDZ domain. J. Biol. Chem. 281, 36811-36818.
27. Fersht, A. (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding, W. H. Freeman and Co., New York.
28. Chi, C. N., Elfström, L., Shi, Y., Snäll, T., Engström, Å., and Jemth, P. (2008) Reassessing a sparse energetic network within a single protein domain. Proc. Natl. Acad. Sci. U.S.A. 105, 4679-4684.
29. Malatesta, F. (2005) The study of bimolecular reactions under non-pseudo-first order conditions. Biophys. Chem. 116, 251-256.
30. Zhang, Y., Dasgupta, J., Ma, R. Z., Banks, L., Thomas, M., and Chen, X. S. (2007) Structures of a human papillomavirus (HPV) E6 polypeptide bound to MAGUK proteins: Mechanisms of targeting tumor suppressors by a high-risk HPV oncoprotein. J. Virol. 81, 3618-3626. (Pubitemid 46456670)
31. Liu, Y., Henry, G. D., Hegde, R. S., and Baleja, J. D. (2007) Solution structure of the hDlg/SAP97 PDZ2 domain and its mechanism of interaction with HPV-18 papillomavirus E6 protein. Biochemistry 46, 10864-10874. (Pubitemid 47463038)
32. von Ossowski, I., Oksanen, E., von Ossowski, L., Cai, C., Sundberg, M., Goldman, A., and Keinänen, 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. (Pubitemid 44673309)
33. Grembecka, J., Cierpicki, T., Devedjiev, Y., Derewenda, U., Kang, B. S., Bushweller, J. H., and Derewenda, Z. S. (2006) The binding of the PDZ tandem of syntenin to target proteins. Biochemistry 45, 3674-3683.
34. Kang, B. S., Cooper, D. R., Devedjiev, Y., Derewenda, U., and Derewenda, Z. S. (2003) Molecular Roots of Degenerate Specificity in Syntenin's PDZ2 Domain: Reassessment of the PDZ Recognition Paradigm. Structure 11, 845-853. (Pubitemid 36833270)
35. Tungteakkhun, S. S., and Duerksen-Hughes, P. J. (2008) Cellular binding partners of the human papillomavirus E6 protein. Arch. Virol. 153, 397-408.
36. Olson, S. T., Srinivasan, K. R., Bjork, I., and Shore, J. D. (1981) Binding of high affinity heparin to antithrombin III. Stopped flow kinetic studies of the binding interaction. J. Biol. Chem. 256, 11073-11079.
37. Cui, Q., and Karplus, M. (2008) Allostery and cooperativity revisited. Protein Sci. 17, 1295-1307.
38. 15N NMR relaxation. Biochemistry 32, 9832-9844.
39. Malmendal, A., Evenas, J., Forsen, S., and Akke, M. (1999) Structural dynamics in the C-terminal domain of calmodulin at low calcium levels. J. Mol. Biol. 293, 883-899.
40. Bracken, C., Carr, P. A., Cavanagh, J., and Palmer, A. G.III (1999) Temperature dependence of intramolecular dynamics of the basic leucine zipper of GCN4: Implications for the entropy of association with DNA. J. Mol. Biol. 285, 2133-2146.
41. Mittermaier, A., and Kay, L. E. (2006) New tools provide new insights in NMR studies of protein dynamics. Science 312, 224-228.
42. Freund, S. M., Johnson, C. M., Jaulent, A., and Ferguson, N. (2008) Moving towards High-Resolution Descriptions of the Molecular Interactions and Structural Rearrangements of the Human Hepatitis B Core Protein. J. Mol. Biol. 384, 1301-1313.
43. Clarkson, M. W., and Lee, A. L. (2004) Long-range dynamic effects of point mutations propagate through side chains in the serine protease inhibitor eglin c. Biochemistry 43, 12448-12458.
44. 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.
45. 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. (Pubitemid 26231173)
46. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.