The transition state of coupled folding and binding for a flexible β-finger

Journal of Molecular Biology

Volumn 417, Issue 3, 2012, Pages 253-261

  Karlsson, O Andreas ^a   Chi, Celestine N ^a   Engström, Åke ^a   Jemth, Per ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

binding kinetics; flexible proteins; intrinsically disordered proteins; PDZ domain; phi binding

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE; PDZ PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95;

ARTICLE; BINDING KINETICS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; HUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

EID: 84857653889     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.01.042     Document Type: Article

References (47)

1. Dyson H.J., and Wright P.E. Intrinsically unstructured proteins and their functions Nat. Rev., Mol. Cell Biol. 6 2005 197 208 (Pubitemid 40314921)
2. Dunker A.K., Silman I., Uversky V.N., and Sussman J.L. Function and structure of inherently disordered proteins Curr. Opin. Struct. Biol. 18 2008 756 764
3. Uversky V.N., and Dunker A.K. Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
4. Vuzman D., and Levy Y. Intrinsically disordered regions as affinity tuners in protein-DNA interactions Mol. Biosyst. 8 2012 47 57
5. Wright P.E., and Dyson H.J. Linking folding and binding Curr. Opin. Struct. Biol. 19 2009 31 38
6. Bernado P., and Svergun D.I. Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering Mol. Biosyst. 8 2012 151 167
7. Radhakrishnan I., Perez-Alvarado G.C., Parker D., Dyson H.J., Montminy M.R., and Wright P.E. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions Cell 91 1997 741 752 (Pubitemid 28007731)
8. Sugase K., Dyson H.J., and Wright P.E. Mechanism of coupled folding and binding of an intrinsically disordered protein Nature 447 2007 1021 1025 (Pubitemid 46975749)
9. Kjaergaard M., Teilum K., and Poulsen F.M. Conformational selection in the molten globule state of the nuclear coactivator binding domain of CBP Proc. Natl Acad. Sci. USA 107 2010 12535 12540
10. Tompa P. The interplay between structure and function in intrinsically unstructured proteins FEBS Lett. 579 2005 3346 3354 (Pubitemid 40804685)
11. Hilser V.J., and Thompson E.B. Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins Proc. Natl Acad. Sci. USA 104 2007 8311 8315 (Pubitemid 47175484)
12. Tompa P., Prilusky J., Silman I., and Sussman J.L. Structural disorder serves as a weak signal for intracellular protein degradation Proteins 71 2008 903 909 (Pubitemid 351430024)
13. Shoemaker B.A., Portman J.J., and Wolynes P.G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl Acad. Sci. USA 97 2000 8868 8873 (Pubitemid 30626639)
14. Trizac E., Levy Y., and Wolynes P.G. Capillarity theory for the fly-casting mechanism Proc. Natl Acad. Sci. USA 107 2010 2746 2750
15. Zhou H.X. Intrinsic disorder: signaling via highly specific but short-lived association Trends Biochem. Sci. 37 2012 43 48
16. Chemes L.B., Sanchez I.E., and de Prat-Gay G. Kinetic recognition of the retinoblastoma tumor suppressor by a specific protein target J. Mol. Biol. 412 2011 267 284
17. Narayanan R., Ganesh O.K., Edison A.S., and Hagen S.J. Kinetics of folding and binding of an intrinsically disordered protein: the inhibitor of yeast aspartic proteinase YPrA J. Am. Chem. Soc. 130 2008 11477 11485
18. Wang C.K., Pan L., Chen J., and Zhang M. Extensions of PDZ domains as important structural and functional elements Protein Cell 1 2010 737 751
19. Petit C.M., Zhang J., Sapienza P.J., Fuentes E.J., and Lee A.L. Hidden dynamic allostery in a PDZ domain Proc. Natl Acad. Sci. USA 106 2009 18249 18254
20. Zhang J., Petit C.M., King D.S., and Lee A.L. Phosphorylation of a PDZ domain extension modulates binding affinity and interdomain interactions in the PSD-95 MAGUK J. Biol. Chem. 286 2011 41776 41785
21. Tochio H., Mok Y.K., Zhang Q., Kan H.M., Bredt D.S., and Zhang M. Formation of nNOS/PSD-95 PDZ dimer requires a preformed β-finger structure from the nNOS PDZ domain J. Mol. Biol. 303 2000 359 370
22. Tochio H., Zhang Q., Mandal P., Li M., and Zhang M. Solution structure of the extended neuronal nitric oxide synthase PDZ domain complexed with an associated peptide Nat. Struct. Biol. 6 1999 417 421 (Pubitemid 29218008)
23. Wang P., Zhang Q., Tochio H., Fan J.S., and Zhang M. Formation of a native-like β-hairpin finger structure of a peptide from the extended PDZ domain of neuronal nitric oxide synthase in aqueous solution Eur. J. Biochem. 267 2000 3116 3122 (Pubitemid 30341137)
24. Hillier B.J., Christopherson K.S., Prehoda K.E., Bredt D.S., and Lim W.A. Unexpected modes of PDZ domain scaffolding revealed by structure of nNOS-syntrophin complex Science 284 1999 812 815 (Pubitemid 29291348)
25. DeLano W.L. The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA
26. Haq S.R., Chi C.N., Bach A., Dogan J., Engström Å., and Hultqvist G. Side-chain interactions form late and cooperatively in the binding reaction between disordered peptides and PDZ domains J. Am. Chem. Soc. 134 2012 599 605
27. Chi C.N., Gianni S., Calosci N., Travaglini-Allocatelli C., Engström Å., and Jemth P. A conserved folding mechanism for PDZ domains FEBS Lett. 581 2007 1109 1113 (Pubitemid 46385932)
28. Chi C.N., Bach A., Gottschalk M., Kristensen A.S., Strømgaard K., and Jemth P. Deciphering the kinetic binding mechanism of dimeric ligands using a potent plasma-stable dimeric inhibitor of postsynaptic density protein-95 as an example J. Biol. Chem. 285 2010 28252 28260
29. Chi C.N., Bach A., Engström Å., Wang H., Strømgaard K., Gianni S., and Jemth P. A sequential binding mechanism in a PDZ domain Biochemistry 48 2009 7089 7097
30. Gianni S., Walma T., Arcovito A., Calosci N., Bellelli A., and Engström Å. Demonstration of long-range interactions in a PDZ domain by NMR, kinetics and protein engineering Structure 14 2006 1801 1809 (Pubitemid 44855631)
31. Schreiber G., and Fersht A.R. Energetics of protein-protein interactions: analysis of the barnase-barstar interface by single mutations and double mutant cycles J. Mol. Biol. 248 1995 478 486
32. Fersht A. Structure and Mechanism in Protein Science 1999 W. H. Freeman and Co. New York, NY
33. Schreiber G., Haran G., and Zhou H.X. Fundamental aspects of protein-protein association kinetics Chem. Rev. 109 2009 839 860
34. Bachmann A., Wildemann D., Praetorius F., Fischer G., and Kiefhaber T. Mapping backbone and side-chain interactions in the transition state of a coupled protein folding and binding reaction Proc. Natl Acad. Sci. USA 108 2011 3952 3957
35. Fersht A.R., and Sato S. φ-Value analysis and the nature of protein-folding transition states Proc. Natl Acad. Sci. USA 101 2004 7976 7981 (Pubitemid 38698039)
36. Sanchez I.E., and Kiefhaber T. Origin of unusual φ-values in protein folding: evidence against specific nucleation sites J. Mol. Biol. 334 2003 1077 1085 (Pubitemid 37485690)
37. Leffler J.E. Parameters for the description of transition states Science 117 1953 340 341
38. Fersht A.R., Matouschek A., and Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding J. Mol. Biol. 224 1992 771 782
39. Itzhaki L.S., Otzen D.E., and Fersht A.R. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding J. Mol. Biol. 254 1995 260 288
40. Goldberg J.M., and Baldwin R.L. Kinetic mechanism of a partial folding reaction. 2. Nature of the transition state Biochemistry 37 1998 2556 2563 (Pubitemid 28119332)
41. Goldberg J.M., and Baldwin R.L. Kinetic mechanism of a partial folding reaction. 1. Properties of the reaction and effects of denaturants Biochemistry 37 1998 2546 2555 (Pubitemid 28119331)
42. Goldberg J.M., and Baldwin R.L. A specific transition state for S-peptide combining with folded S-protein and then refolding Proc. Natl Acad. Sci. USA 96 1999 2019 2024 (Pubitemid 29117860)
43. Hemsath L., Dvorsky R., Fiegen D., Carlier M.F., and Ahmadian M.R. An electrostatic steering mechanism of Cdc42 recognition by Wiskott-Aldrich syndrome proteins Mol. Cell 20 2005 313 324 (Pubitemid 41484175)
44. De Sancho D., and Best R.B. Modulation of an IDP binding mechanism and rates by helix propensity and non-native interactions: association of HIF1α with CBP Mol. Biosyst. 8 2012 256 267
45. Wang J., Wang Y., Chu X., Hagen S.J., Han W., and Wang E. Multi-scaled explorations of binding-induced folding of intrinsically disordered protein inhibitor IA3 to its target enzyme PLoS Comput. Biol. 7 2011 e1001118
46. Haq S.R., Jürgens M.C., Chi C.N., Koh C.S., Elfström L., and Selmer M. The plastic energy landscape of protein folding: a triangular folding mechanism with an equilibrium intermediate for a small protein domain J. Biol. Chem. 285 2010 18051 18059
47. Malatesta F. The study of bimolecular reactions under non-pseudo-first order conditions Biophys. Chem. 116 2005 251 256 (Pubitemid 40962453)