Structure and Dynamics of Pin1 During Catalysis by NMR

Journal of Molecular Biology

Volumn 367, Issue 5, 2007, Pages 1370-1381

  Labeikovsky, Wladimir ^a   Eisenmesser, Elan Z ^a   Bosco, Daryl A ^a   Kern, Dorothee ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

catalysis; NMR spectroscopy; peptidylprolyl isomerase; protein dynamics

Indexed keywords

NITROGEN 15; PEPTIDE FRAGMENT; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN SUBUNIT; SERYLPROLINE; TAU PROTEIN; THREONYLPROLINE; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ISOMERIZATION; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN FAMILY; STRUCTURE ACTIVITY RELATION;

EID: 33947144085     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.01.049     Document Type: Article

References (60)

1. Fersht A. Structure and Mechanism in Protein Science (2000), W.H. Freeman, New York
2. Kay L. NMR studies of protein structure and dynamics. J. Magn. Reson. 173 (2005) 193-207
3. Palmer A. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104 (2004) 3623-3640
4. Kern D., Eisenmesser E., and Wolf-Watz M. Enzyme dynamics during catalysis measured by NMR spectroscopy. Methods Enzymol. 394 (2005) 507-524
5. Boehr D., McElheny D., Dyson H., and Wright P. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313 (2006) 1638-1642
6. Boehr D., Dyson H., and Wright P. An NMR perspective on enzyme dynamics. Chem. Rev. 106 (2006) 3055-3079
7. Massi F., Wang C., and Palmer A. Solution NMR and computer simulation studies of active site loop motion in triosephosphate isomerase. Biochemistry 45 (2006) 10787-10794
8. Butterwick J., and Palmer A. An inserted Gly residue fine tunes dynamics between mesophilic and thermophilic ribonucleases H. Protein Sci. 15 (2006) 2697-2707
9. Tugarinov V., and Kay L. Quantitative 13C and 2H NMR relaxation studies of the 723-residue enzyme malate synthase G reveal a dynamic binding interface. Biochemistry 44 (2005) 15970-15977
10. Tugarinov V., and Kay L. Relaxation rates of degenerate 1H transitions in methyl group of proteins as reporters of side-chain dynamics. J. Am. Chem. Soc. 128 (2006) 7299-7308
11. Vallurupalli P., and Kay L. Complementarity of ensemble and single-molecule measures of protein motion: a relaxation dispersion NMR study of an enzyme complex. Proc. Natl Acad. Sci. USA 103 (2006) 11910-11915
12. Stevens S., Sanker S., Kent C., and Zuiderweg E. Delineation of the allosteric mechanism of a cytidyltransferase exhibiting negative cooperativity. Nat. Mol. Biol. 8 (2001) 947-952
13. Davis J., and Agard D. Relationship between enzyme specificity and the backbone dynamics of free and inhibited alpha-lytic protease. Biochemistry 37 (1998) 7696-7707
14. Rozovsky S., Jogl G., Tong L., and McDermott A. Solution-state NMR investigations of triosephosphate isomerase active site loop motion: ligand release in relation to active site loop dynamics. J. Mol. Biol. 310 (2001) 271-280
15. Williams J., and McDermott A. Dynamics of the flexible loop of triosephosphate isomerase: the loop motion is not ligand gated. Biochemistry 34 (1995) 8309-8319
16. Falzone C., Wright P., and Benkovic S. Dynamics of a flexible loop in dihydrofolate reductase from E. coli and its implication for catalysis. Biochemistry 33 (1994) 439-442
17. Osborne M., Schnell J., Benkovic S., Dyson H., and Wright P. Backbone dynamics in dihydrofolate reductase complexes: role of loop flexibility in the catalytic mechanism. Biochemistry 40 (2001) 9846-9859
18. Schnell J., Dyson H., and Wright P. Structure, dynamics and catalytic function of dihydrofolate reductase. Annu. Rev. Biophys. Biomol. Struct. 33 (2004) 119-140
19. Ishima R., Freedberg D., Wang Y., Louis J., and Torchia D. Flap opening and dimer interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function. Structure 7 (1999) 1047-1055
20. Lukin J., Kontaxis G., Simplaceanu V., Yuan Y., Bax A., and Ho C. Quaternary structure of hemoglobin in solution. Proc. Natl Acad. Sci. USA 100 (2003) 517-520
21. Wang L., Pang Y., Holder T., Brender J., Kurochkin A., and Zuiderweg E. Functional dynamics in the active site of the ribonuclease binase. Proc. Natl Acad. Sci. USA 98 (2001) 7684-7689
22. Cole R., and Loria J. Evidence for flexibility in the function of ribonuclease A. Biochemistry 42 (2002) 6072-6081
23. Beach H., Cole R., Gill M., and Loria J. Conservation of μs-ms enzyme motions in the apo- and substrate-mimicked state. J. Am. Chem. Soc. 127 (2005) 9167-9176
24. Farrow N., Muhandiram R., Singer A., Pascal S., Kay C., Gish G., et al. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
25. Palmer A., Kroenke C., and Loria J. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 339 (2001) 204-238
26. Loria J., Rance M., and Palmer A. A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J. Biomol. NMR 15 (1999) 151-155
27. Carver J., and Richards R. A general two-site solution for the chemical exchange produced dependence of T2 upon the Carr-Purcell pulse separation. J. Magn. Reson. 6 (1972) 89-105
28. Tollinger M., Skrynnikov N., Mulder F., Forman-Kay J., and Kay L. Slow dynamics in folded and unfolded states of an SH3 domain. J. Am. Chem. Soc. 123 (2001) 11341-11352
29. Gothel S., and Marahiel M. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 55 (1999) 423-436
30. Yaffe M., Schutkowski M., Shen M., Zhou X., Stukenberg P., Rahfeld J., et al. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278 (1997) 1957-1960
31. Zhou X., Lu P., Wulf G., and Lu K. Phosphorylation-dependent prolyl isomerization: a novel signaling regulatory mechanism. Cell. Mol. Life Sci. 56 (1999) 788-806
32. Zhou X., Kops O., Werner A., Lu P., Shen M., Stoller G., et al. Pin1-dependent prolyl isomerization regulates dephosphorylation of cdc25C and tau proteins. Mol. Cell 6 (2000) 873-883
33. Weiwad M., Werner A., Rücknagel P., Schierhorn A., Küllertz G., and Fischer G. Catalysis of proline-directed protein phosphorylation by peptidyl-prolyl cis/trans isomerases. J. Mol. Biol. 339 (2004) 635-646
34. Shen M., Stukenberg P., Kirschner M., and Lu K. The essential mitotic peptidylprolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins. Genes Dev. 12 (1998) 706-720
35. Lu K., Liou Y., and Vincent I. Proline-directed phosphorylation and isomerization in mitotic regulation and in Alzheimer's disease. Bioessays 25 (2003) 174-181
36. Bayer E., Goettsch S., Mueller J., Griewel B., Guiberman E., Mayr L., and Bayer P. Structural analysis of the mitotic regulator hPin1 in solution: insights into domain architecture and substrate binding. J. Biol. Chem. 278 (2003) 26183-26193
37. Ranganathan R., Lu K., Hunter T., and Noel J. Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89 (1997) 875-886
38. Fischer G., Wittmann-Liebold B., Lang K., Kiefhaber T., and Schmid F. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337 (1989) 476-478
39. Wider G., Weber C., and Wuthrich K. Proton-proton overhouser effects of receptor-bound cyclosporin A observed with the use of a heteronuclear-resolved half-filter experiment. J. Am. Chem. Soc. 113 (1991) 4676-4678
40. Ikura M., and Bax A. Isotope-filtered 2D NMR of a protein-peptide complex: study of a skeletal muscle myosin light chain kinase fragment bound to calmodulin. J. Am. Chem. Soc. 114 (1992) 2433-2440
41. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., and Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comp. Chem. 4 (1983) 187-217
42. Jorgensen W., Chandrasekhar J., Madura J., Impey R., and Klein M. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983) 926-935
43. Eisenmesser E., Bosco D., Akke M., and Kern D. Enzyme dynamics during catalysis. Science 295 (2002) 1520-1523
44. McConnell H. Reaction rates by nuclear magnetic resonance. J. Chem. Phys. 28 (1958) 430-431
45. Millet O., Loria J., Kroenke C., Pons M., and Palmer A. The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122 (2000) 2867-2877
46. Ishima R., and Torchia D. Error estimation and global fitting in transverse-relaxation dispersion experiments to determine chemical-exchange parameters. J. Biomol. NMR 32 (2005) 41-54
47. Korzhnev D., Karlsson B., Orekhov V., and Billeter M. NMR detection of multiple transitions to low-populated states in azurin. Protein Sci. 12 (2003) 56-65
48. Eisenmesser E., Millet O., Labeikovsky W., Korzhnev D., Wolf-Watz M., Bosco D., et al. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438 (2005) 117-121
49. Wolf-Watz M., Thai V., Henzler-Wildman K., Hadjipavlou G., Eisenmesser E., and Kern D. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat. Struct. Mol. Biol. 11 (2004) 945-949
50. Zhang Y., Fussel S., Reimer U., Schutkowski M., and Fischer G. Substrate-based design of reversible Pin1 inhibitors. Biochemistry 41 (2002) 11868-11877
51. Wittekind M., and Mueller L. HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J. Magn. Reson., Ser. B 101 (1993) 201-205
52. Grzesiek S., and Bax A. Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114 (1992) 6291-6293
53. Grzesiek S., Anglister J., and Bax A. Correlation of backbone amide and aliphatic side-chain resonances in 13C/15N-enriched proteins by isotropic mixing of 13C magnetization. J. Magn. Reson., Ser. B 101 (1993) 114-119
54. Lyons B.A., and Montelione G.T. An HCCNH triple-resonance experiment using carbon-13 isotropic mixing for correlating backbone amide and side-chain aliphatic resonances in isotopically enriched proteins. J. Magn. Reson., Ser. B 101 (1993) 206-209
55. Kay L.E., Xu G.Y., Singer A.U., Muhandiram R., and Forman-Kay J.D. A gradient-enhanced HCCH-TOCSY experiment for recording side-chain 1H and 13C correlations in H2O samples of proteins. J. Magn. Reson., Ser. B 101 (1993) 333-337
56. Zhang O., Kay L.E., Olivier J.P., and Forman-Kay J. Backbone 1H and 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J. Biomol. NMR 4 (1994) 845-858
57. 2O saturation. J. Magn. Reson., Ser. A 109 (1994) 129-133
58. Eichmüller C., Schüler W., Konrat R., and Krautler B. Simultaneous measurement of intra- and intermolecular NOEs in differentially labeled protein-ligand complexes. J. Biomol. NMR 21 (2001) 107-116
59. Eichmüller C., Tollinger M., Krautler B., and Konrat R. Mapping the ligand binding site at protein side-chains in protein-ligand complexes through NOE difference spectroscopy. J. Biomol. NMR 20 (2001) 195-202
60. Pervushin K., Riek R., Wider G., and Wuthrich K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biomolecular structures in solution. Proc. Natl Acad. Sci. USA 94 (1997) 12366-12371