Conformation-directed catalysis and coupled enzyme-substrate dynamics in Pin1 phosphorylation-dependent cis-trans isomerase

Journal of Physical Chemistry B

Volumn 117, Issue 39, 2013, Pages 11509-11517

  Velazquez, Hector A ^a   Hamelberg, Donald ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; CONFORMATIONS; DISEASES; ENZYMES; ISOMERIZATION; MOLECULAR DYNAMICS; PHOSPHORYLATION; QUANTUM CHEMISTRY;

ACCELERATED MOLECULAR DYNAMICS; CATALYTIC DOMAINS; CATALYTIC MECHANISMS; CIS-TRANS ISOMERIZATION; ENZYME-SUBSTRATE INTERACTIONS; PHOSPHATE BINDING; PROTEIN SUBSTRATE; REGULATORY PATHWAY;

SUBSTRATES;

NIMA INTERACTING PEPTIDYLPROLYL ISOMERASE; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; PEPTIDYLPROLYL ISOMERASE;

ARTICLE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; HUMAN; ISOMERISM; MOLECULAR DYNAMICS; PROBABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; SOLUTION AND SOLUBILITY;

BIOCATALYSIS; CATALYTIC DOMAIN; HUMANS; ISOMERISM; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PEPTIDYLPROLYL ISOMERASE; PROBABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; SOLUTIONS; SUBSTRATE SPECIFICITY;

EID: 84885136834     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp405271s     Document Type: Article

References (65)

1. Deribe, Y. L.; Pawson, T.; Dikic, I. Post-Translational Modifications in Signal Integration Nat. Struct. Mol. Biol. 2010, 17, 666-672
2. Goodey, N. M.; Benkovic, S. J. Allosteric Regulation and Catalysis Emerge via a Common Route Nat. Chem. Biol. 2008, 4, 474-482
3. Kuriyan, J.; Eisenberg, D. The Origin of Protein Interactions and Allostery in Colocalization Nature 2007, 450, 983-990
4. Ha, J.-H.; Loh, S. N. Protein Conformational Switches: From Nature to Design Chem.-Eur. J. 2012, 18, 7984-7999
5. Tsai, C. J.; del Sol, A.; Nussinov, R. Allostery: Absence of a Change in Shape Does Not Imply That Allostery Is Not at Play J. Mol. Biol. 2008, 378, 1-11
6. Kun Ping, L.; Finn, G.; Tae, Ho, L.; Nicholson, L. K. Prolyl Cis-Trans Isomerization as a Molecular Timer Nat. Chem. Biol. 2007, 3, 619-629
7. Theuerkorn, M.; Fischer, G.; Schiene-Fischer, C. Prolyl Cis/Trans Isomerase Signalling Pathways in Cancer Curr. Opin. Pharmacol. 2011, 11, 281-287
8. Lu, K. P.; Zhou, X. Z. The Prolyl Isomerase Pin1: A Pivotal New Twist in Phosphorylation Signalling and Disease Nat. Rev. Mol. Cell Biol. 2007, 8, 904-916
9. Zhou, X. Z.; Kops, O.; Werner, A.; Lu, P. J.; Shen, M.; Stoller, G.; Kullertz, G.; Stark, M.; Fischer, G.; Lu, K. P. Pin1-Dependent Prolyl Isomerization Regulates Dephosphorylation of Cdc25c and Tau Proteins Mol. Cell 2000, 6, 873-883
10. Werner-Allen, J. W.; Lee, C. J.; Liu, P.; Nicely, N. I.; Wang, S.; Greenleaf, A. L.; Zhou, P. Cis-Proline-Mediated Ser(P)5 Dephosphorylation by the RNA Polymerase II C-Terminal Domain Phosphatase Ssu72 J. Biol. Chem. 2011, 286, 5717-5726
11. Lu, K.; Hanes, S.; Hunter, T. A Human Peptidyl-Prolyl Isomerase Essential for Regulation of Mitosis Nature 1996, 380, 544-547
12. Ryo, A.; Liou, Y.-C.; Lu, K. P.; Wulf, G. Prolyl Isomerase Pin1: A Catalyst for Oncogenesis and a Potential Therapeutic Target in Cancer J. Cell Sci. 2003, 116, 773-783
13. Finn, G.; Lu, K. P. Phosphorylation-Specific Prolyl Isomerase Pin1 as a New Diagnostic and Therapeutic Target for Cancer Curr. Cancer Drug Targets 2008, 8, 223-229
14. Bulbarelli, A.; Lonati, E.; Cazzaniga, E.; Gregori, M.; Masserini, M. Pin1 Affects Tau Phosphorylation in Response to a Beta Oligomers Mol. Cell. Neurosci. 2009, 42, 75-80
15. Pei-Jung, L.; Wulf, G.; Zhou, X.; Davies, P.; Lu, K. The Prolyl Isomerase Pin1 Restores the Function of Alzheimer-Associated Phosphorylated Tau Protein Nature 1999, 399, 784-788
16. Pastorino, L.; Sun, A.; Lu, P. J.; Zhou, X. Z.; Balastik, M.; Finn, G.; Wulf, G.; Lim, J.; Li, S. H.; Li, X. The Prolyl Isomerase Pin1 Regulates Amyloid Precursor Protein Processing and Amyloid-Beta Production Nature 2006, 440, 528-34
17. Lim, Y.-S.; Tran, H. T. L.; Park, S.-J.; Yim, S.-A.; Hwang, S. B. Peptidyl-Prolyl Isomerase Pin1 Is a Cellular Factor Required for Hepatitis C Virus Propagation J. Virol. 2011, 85, 8777-8788
18. Mori, T.; Hidaka, M.; Lin, Y.-C.; Yoshizawa, I.; Okabe, T.; Egashira, S.; Kojima, H.; Nagano, T.; Koketsu, M.; Takamiya, M. A Dual Inhibitor against Prolyl Isomerase Pin1 and Cyclophilin Discovered by a Novel Real-Time Fluorescence Detection Method Biochem. Biophys. Res. Commun. 2011, 406, 439-443
19. Potter, A. J.; Ray, S.; Gueritz, L.; Nunns, C. L.; Bryant, C. J.; Scrace, S. F.; Matassova, N.; Baker, L.; Dokurno, P.; Robinson, D. A. Structure-Guided Design of A-Amino Acid-Derived Pin1 Inhibitors Bioorg. Med. Chem. Lett. 2010, 20, 586-590
20. Wang, X. D. J.; Xu, B. L.; Mullins, A. B.; Neiler, F. K.; Etzkorn, F. A. Conformationally Locked Isostere of Phosphoser- cis -Pro Inhibits Pin1 23-Fold Better Than Phosphoser- trans -Pro Isostere J. Am. Chem. Soc. 2004, 126, 15533-15542
21. Liu, T.; Liu, Y.; Kao, H.-Y.; Pei, D. Membrane Permeable Cyclic Peptidyl Inhibitors against Human Peptidylprolyl Isomerase Pin1 J. Med. Chem. 2010, 53, 2494-2501
22. Wildemann, D.; Erdmann, F.; Alvarez, B. H.; Stoller, G.; Zhou, X. Z.; Fanghänel, J.; Schutkowski, M.; Lu, K. P.; Fischer, G. Nanomolar Inhibitors of the Peptidyl Prolyl Cis/Trans Isomerase Pin1 from Combinatorial Peptide Libraries J. Med. Chem. 2006, 49, 3430-3430
23. Potter, A.; Oldfield, V.; Nunns, C.; Fromont, C.; Ray, S.; Northfield, C. J.; Bryant, C. J.; Scrace, S. F.; Robinson, D.; Matossova, N. Discovery of Cell-Active Phenyl-Imidazole Pin1 Inhibitors by Structure-Guided Fragment Evolution Bioorg. Med. Chem. Lett. 2010, 20, 6483-6488
24. Lv, L.; Zhou, Z.; Huang, X.; Zhao, Y.; Zhang, L.; Shi, Y.; Sun, M.; Zhang, J. Inhibition of Peptidyl-Prolyl Cis/Trans Isomerase Pin1 Induces Cell Cycle Arrest and Apoptosis in Vascular Smooth Muscle Cells Apoptosis 2010, 15, 41-54
25. Hennig, L.; Christner, C.; Kipping, M.; Schelbert, B.; Rücknagel, K. P.; Grabley, S.; Küllertz, G.; Fischer, G. Selective Inactivation of Parvulin-Like Peptidyl-Prolyl cis / trans Isomerases by Juglone Biochemistry 1998, 37, 5953-5960
26. Zhu, L.; Jin, J.; Liu, C.; Zhang, C.; Sun, Y.; Guo, Y.; Fu, D.; Chen, X.; Xu, B. Synthesis and Biological Evaluation of Novel Quinazoline-Derived Human Pin1 Inhibitors Biorg. Med. Chem. 2011, 19, 2797-2807
27. Ranganathan, R.; Lu, K. P.; Hunter, T.; Noel, J. P. Structural and Functional Analysis of the Mitotic Rotamase Pin1 Suggests Substrate Recognition Is Phosphorylation Dependent Cell 1997, 89, 875-886
28. Daum, S.; Fanghänel, J.; Wildemann, D.; Schiene-Fischer, C. Thermodynamics of Phosphopeptide Binding to the Human Peptidyl Prolyl cis / trans Isomerase Pin1 Biochemistry 2006, 45, 12125-12135
29. Greenwood, A. I.; Rogals, M. J.; De, S.; Lu, K. P.; Kovrigin, E. L.; Nicholson, L. K. Complete Determination of the Pin1 Catalytic Domain Thermodynamic Cycle by NMR Lineshape Analysis J. Biomol. NMR 2011, 51, 21-34
30. Fanghanel, J.; Fischer, G. Insights into the Catalytic Mechanism of Peptidyl Prolyl Cis/Trans Isomerases Front. Biosci. 2004, 9, 3453-3478
31. Behrsin, C. D.; Bailey, M. L.; Bateman, K. S.; Hamilton, K. S.; Wahl, L. M.; Brandl, C. J.; Shilton, B. H.; Litchfield, D. W. Functionally Important Residues in the Peptidyl-Prolyl Isomerase Pin1 Revealed by Unigenic Evolution J. Mol. Biol. 2007, 365, 1143-1162
32. Xu, G. Y. G.; Zhang, Y.; Mercedes-Camacho, A. Y.; Etzkorn, F. A. A Reduced-Amide Inhibitor of Pin1 Binds in a Conformation Resembling a Twisted-Amide Transition State Biochemistry 2011, 50, 9545-9550
33. Schutkowski, M.; Bernhardt, A.; Zhou, X. Z.; Shen, M.; Reimer, U.; Rahfeld, J.-U.; Lu, K. P.; Fischer, G. Role of Phosphorylation in Determining the Backbone Dynamics of the Serine/Threonine-Proline Motif and Pin1 Substrate Recognition Biochemistry 1998, 37, 5566-5575
34. Vöhringer-Martinez, E.; Duarte, F.; Toro-Labbe, A. How Does Pin1 Catalyze the Cis-Trans Prolyl Peptide Bond Isomerization? A QM/MM and Mean Reaction Force Study J. Phys. Chem. B 2012, 116, 12972-12979
35. Mueller, J. W.; Link, N. M.; Matena, A.; Hoppstock, L.; Ruppel, A.; Bayer, P.; Blankenfeldt, W. Crystallographic Proof for an Extended Hydrogen-Bonding Network in Small Prolyl Isomerases J. Am. Chem. Soc. 2011, 133, 20096-20099
36. Bailey, M. L.; Shilton, B. H.; Brandl, C. J.; Litchfield, D. W. The Dual Histidine Motif in the Active Site of Pin1 Has a Structural Rather Than Catalytic Role Biochemistry 2008, 47, 11481-11489
37. Velazquez, H. A.; Hamelberg, D. Conformational Selection in the Recognition of Phosphorylated Substrates by the Catalytic Domain of Human Pin1 Biochemistry 2011, 50, 9605-9615
38. McGowan, Lauren, C.; Hamelberg, D. Conformational Plasticity of an Enzyme During Catalysis: Intricate Coupling between Cyclophilin a Dynamics and Substrate Turnover Biophys. J. 2013, 104, 216-226
39. Hamelberg, D.; Mongan, J.; McCammon, J. A. Accelerated Molecular Dynamics: A Promising and Efficient Simulation Method for Biomolecules J. Chem. Phys. 2004, 120, 11919-11929
40. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W. Calculating Structures and Free Energies of Complex Molecules: Combining Molecular Mechanics and Continuum Models Acc. Chem. Res. 2000, 33, 889-897
41. Case, D. A.; Cheatham, T. E., III; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M., Jr.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber Biomolecular Simulation Programs J. Comput. Chem. 2005, 26, 1668-1688
42. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of Multiple Amber Force Fields and Development of Improved Protein Backbone Parameters Proteins: Struct., Funct., Bioinf. 2006, 65, 712-725
43. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules J. Am. Chem. Soc. 1995, 117, 5179-5197
44. J. Am. Chem. Soc. 1996, 118, 2309-2309.
45. Doshi, U.; Hamelberg, D. Reoptimization of the Amber Force Field Parameters for Peptide Bond (Omega) Torsions Using Accelerated Molecular Dynamics J. Phys. Chem. B 2009, 113, 16590-16595
46. Homeyer, N.; Horn, A.; Lanig, H.; Sticht, H. Amber Force-Field Parameters for Phosphorylated Amino Acids in Different Protonation States: Phosphoserine, Phosphothreonine, Phosphotyrosine, and Phosphohistidine J. Mol. Model. 2006, 12, 281-289
47. Zhang, Y.; Daum, S.; Wildemann, D.; Zhou, X. Z.; Verdecia, M. A.; Bowman, M. E.; Lücke, C.; Hunter, T.; Lu, K.-P.; Fischer, G. Structural Basis for High-Affinity Peptide Inhibition of Human Pin1 ACS Chem. Biol. 2007, 2, 320-328
48. Jorgensen, W. L. Revised Tips for Simulations of Liquid Water and Aqueous Solutions J. Chem. Phys. 1982, 77, 4156-4163
49. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of N-Alkanes J. Comput. Phys. 1977, 23, 327-341
50. Izaguirre, J. A.; Catarello, D. P.; Wozniak, J. M.; Skeel, R. D. Langevin Stabilization of Molecular Dynamics J. Chem. Phys. 2001, 114, 2090
51. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A Smooth Particle Mesh Ewald Method J. Chem. Phys. 1995, 103, 8577-8593
52. Shen, T.; Hamelberg, D. A Statistical Analysis of the Precision of Reweighting-Based Simulations J. Chem. Phys. 2008, 129, 034103/1-034103/9
53. Doshi, U.; Hamelberg, D. Improved Statistical Sampling and Accuracy with Accelerated Molecular Dynamics on Rotatable Torsions J. Chem. Theory Comput. 2012, 8, 4004-4012
54. Wolfenden, R.; Snider, M. J. The Depth of Chemical Time and the Power of Enzymes as Catalysts Acc. Chem. Res. 2001, 34, 938-945
55. Wolfenden, R. Thermodynamic and Extrathermodynamic Requirements of Enzyme Catalysis Biophys. Chem. 2003, 105, 559-572
56. Wolfenden, R. Enzyme Catalysis: Conflicting Requirements of Substrate Access and Transition State Affinity Mol. Cell. Biochem. 1974, 3, 207-211
57. Ma, B.; Nussinov, R. Enzyme Dynamics Point to Stepwise Conformational Selection in Catalysis Curr. Opin. Chem. Biol. 2010, 14, 652-659
58. Fraser, J. S.; Clarkson, M. W.; Degnan, S. C.; Erion, R.; Kern, D.; Alber, T. Hidden Alternative Structures of Proline Isomerase Essential for Catalysis Nature 2009, 462, 669-673
59. Namanja, A. T.; Wang, X. J.; Xu, B.; Mercedes-Camacho, A. Y.; Wilson, K. A.; Etzkorn, F. A.; Peng, J. W. Stereospecific Gating of Functional Motions in Pin1 Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 12289-12294
60. Doshi, U.; McGowan, L. C.; Ladani, S. T.; Hamelberg, D. Resolving the Complex Role of Enzyme Conformational Dynamics in Catalytic Function Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 5699-5704
61. Fischer, S.; Dunbrack, R. L.; Karplus, M. Cis-Trans Imide Isomerization of the Proline Dipeptide J. Am. Chem. Soc. 1994, 116, 11931-11937
62. Hamelberg, D.; McCammon, J. A. Mechanistic Insight into the Role of Transition-State Stabilization in Cyclophilin A J. Am. Chem. Soc. 2008, 131, 147-152
63. Ladani, S. T.; Hamelberg, D. Entropic and Surprisingly Small Intramolecular Polarization Effects in the Mechanism of Cyclophilin A J. Phys. Chem. B 2012, 116, 10771-10778
64. Yaffe, M. B.; Schutkowski, M.; Shen, M.; Zhou, X. Z.; Stukenberg, P. T.; Rahfeld, J. U.; Xu, J.; Kuang, J.; Kirschner, M. W.; Fischer, G. Sequence-Specific and Phosphorylation-Dependent Proline Isomerization: A Potential Mitotic Regulatory Mechanism Science 1997, 278, 1957-1960
65. Zhou, P.; Tian, F.; Lv, F.; Shang, Z. Geometric Characteristics of Hydrogen Bonds Involving Sulfur Atoms in Proteins Proteins: Struct., Funct., Bioinf. 2009, 76, 151-163