Protein conformational populations and functionally relevant substates

Accounts of Chemical Research

Volumn 47, Issue 1, 2014, Pages 149-156

  Ramanathan, Arvind ^a   Savol, Andrej ^b,c   Burger, Virginia ^b,c   Chennubhotla, Chakra S ^c   Agarwal, Pratul K ^a,d  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d Annavitas Biosciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN A; PROTEIN;

ARTICLE; BIOCATALYSIS; BIOLOGY; CHEMISTRY; HUMAN; METABOLISM; PROTEIN CONFORMATION;

BIOCATALYSIS; COMPUTATIONAL BIOLOGY; CYCLOPHILIN A; HUMANS; PROTEIN CONFORMATION; PROTEINS;

EID: 84892691978     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400084s     Document Type: Article

References (54)

1. Fischer, E. Einfluss der Configuration auf die Wirkung den Enzyme Ber. Dtsch. Chem. Ges. 1894, 27, 2985-2993
2. Henzler-Wildman, K. A.; Lei, M.; Thai, V.; Kerns, S. J.; Karplus, M.; Kern, D. A Hierarchy of Timescales in Protein Dynamics Is Linked to Enzyme Catalysis Nature 2007, 450, 913-916
3. Hammes, G. G.; Benkovic, S. J.; Hammes-Schiffer, S. Flexibility, Diversity, and Cooperativity: Pillars of Enzyme Catalysis Biochemistry 2011, 50, 10422-10430
4. Ramanathan, A.; Agarwal, P. K. Evolutionarily Conserved Linkage between Enzyme Fold, Flexibility, and Catalysis PLoS Biol. 2011, 9 e1001193
5. Ramanathan, A.; Savol, A. J.; Langmead, C. J.; Agarwal, P. K.; Chennubhotla, C. S. Discovering Conformational Sub-States Relevant to Protein Function PLoS ONE 2011, 6 e15827
6. Senet, P.; Maisuradze, G. G.; Foulie, C.; Delarue, P.; Scheraga, H. A. How Main-Chains of Proteins Explore the Free-Energy Landscape in Native States Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 19708-19713
7. Agarwal, P. K. Enzymes: An Integrated View of Structure, Dynamics and Function Microb. Cell Fact. 2006, 5, 2
8. Bowman, G. R.; Pande, V. S. Protein Folded States Are Kinetic Hubs Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 10890-10895
9. Boehr, D. D.; McElheny, D.; Dyson, H. J.; Wright, P. E. The Dynamic Energy Landscape of Dihydrofolate Reductase Catalysis Science 2006, 313, 1638-1642
10. Savol, A. J.; Burger, V. M.; Agarwal, P. K.; Ramanathan, A.; Chennubhotla, C. S. QAARM: Quasi-anharmonic Autoregressive Model Reveals Molecular Recognition Pathways in Ubiquitin Bioinformatics 2011, 27, I52-I60
11. Ramanathan, A.; Savol, A. J.; Agarwal, P. K.; Chennubhotla, C. S. Event Detection and Sub-state Discovery from Biomolecular Simulations Using Higher-Order Statistics: Application to Enzyme Adenylate Kinase Proteins 2012, 80, 2536-2551
12. Boehr, D. D.; Nussinov, R.; Wright, P. E. The Role of Dynamic Conformational Ensembles in Biomolecular Recognition Nat. Chem. Biol. 2009, 5, 789-796
13. Kar, G.; Keskin, O.; Gursoy, A.; Nussinov, R. Allostery and Population Shift in Drug Discovery Curr. Opin. Pharmacol. 2010, 10, 715-722
14. 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
15. Boehr, D. D.; McElheny, D.; Dyson, H. J.; Wright, P. E. Millisecond Timescale Fluctuations in Dihydrofolate Reductase Are Exquisitely Sensitive to the Bound Ligands Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 1373-1378
16. Akke, M. Conformational Dynamics and Thermodynamics of Protein-Ligand Binding Studied by NMR Relaxation Biochem. Soc. Trans. 2012, 40, 419-423
17. Homouz, D.; Sanabria, H.; Waxham, M. N.; Cheung, M. S. Modulation of Calmodulin Plasticity by the Effect of Macromolecular Crowding J. Mol. Biol. 2009, 391, 933-943
18. Mehmood, S.; Domene, C.; Forest, E.; Jault, J. M. Dynamics of a Bacterial Multidrug ABC Transporter in the Inward- And Outward-Facing Conformations Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 10832-10836
19. Borreguero, J. M.; He, J. H.; Meilleur, F.; Weiss, K. L.; Brown, C. M.; Myles, D. A.; Herwig, K. W.; Agarwal, P. K. Redox-Promoting Protein Motions in Rubredoxin J. Phys. Chem. B 2011, 115, 8925-8936
20. Schiro, G.; Vetri, V.; Frick, B.; Militello, V.; Leone, M.; Cupane, A. Neutron Scattering Reveals Enhanced Protein Dynamics in Concanavalin A Amyloid Fibrils J. Phys. Chem. Lett. 2012, 3, 992-996
21. Markwick, P. R. L.; Bouvignies, G.; Blackledge, M. Exploring Multiple Timescale Motions in Protein GB3 Using Accelerated Molecular Dynamics and NMR Spectroscopy J. Am. Chem. Soc. 2007, 129, 4724-4730
22. Boehr, D. D.; Dyson, H. J.; Wright, P. E. An NMR Perspective on Enzyme Dynamics Chem. Rev. 2006, 106, 3055-3079
23. Lange, O. F.; Lakomek, N. A.; Fares, C.; Schroder, G. F.; Walter, K. F. A.; Becker, S.; Meiler, J.; Grubmuller, H.; Griesinger, C.; de Groot, B. L. Recognition Dynamics up to Microseconds Revealed from an RDC-Derived Ubiquitin Ensemble in Solution Science 2008, 320, 1471-1475
24. Ban, D.; Funk, M.; Gulich, R.; Egger, D.; Sabo, T. M.; Walter, K. F. A.; Fenwick, R. B.; Giller, K.; Pichierri, F.; de Groot, B. L.; Lange, O. F.; Grubmuller, H.; Salvatella, X.; Wolf, M.; Loidl, A.; Kree, R.; Becker, S.; Lakomek, N. A.; Lee, D.; Lunkenheimer, P.; Griesinger, C. Kinetics of Conformational Sampling in Ubiquitin Angew. Chem., Int. Ed. 2011, 50, 11437-11440
25. Yang, L.; Song, G.; Jernigan, R. L. Protein Elastic Network Models and the Ranges of Cooperativity Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 12347-12352
26. Yang, S. C.; Park, S.; Makowski, L.; Roux, B. A Rapid Coarse Residue-Based Computational Method for X-Ray Solution Scattering Characterization of Protein Folds and Multiple Conformational States of Large Protein Complexes Biophys. J. 2009, 96, 4449-4463
27. Skliros, A.; Zimmermann, M. T.; Chakraborty, D.; Saraswathi, S.; Katebi, A. R.; Leelananda, S. P.; Kloczkowski, A.; Jernigan, R. L. The importance of slow motions for protein functional loops Phys. Biol. 2012, 9 014001
28. Agarwal, P. K.; Alam, S. R. Biomolecular simulations on petascale: Promises and challenges J. Phys. Conf. Ser. 2006, 46, 327-333
29. Dror, R. O.; Dirks, R. M.; Grossman, J. P.; Xu, H. F.; Shaw, D. E. Biomolecular Simulation: A Computational Microscope for Molecular Biology Annu. Rev. Biophys. 2012, 41, 429-452
30. Kastner, J.; Senn, H. M.; Thiel, S.; Otte, N.; Thiel, W. QM/MM Free-Energy Perturbation Compared to Thermodynamic Integration and Umbrella Sampling: Application to an Enzymatic Reaction J. Chem. Theory Comput. 2006, 2, 452-461
31. Agarwal, P. K.; Geist, A.; Gorin, A. Protein Dynamics and Enzymatic Catalysis: Investigating the Peptidyl-Prolyl Cis-Trans Isomerization Activity of Cyclophilin A Biochemistry 2004, 43, 10605-10618
32. Leone, V.; Marinelli, F.; Carloni, P.; Parrinello, M. Targeting Biomolecular Flexibility with Metadynamics Curr. Opin. Struc. Biol. 2010, 20, 148-154
33. Leone, V.; Lattanzi, G.; Molteni, C.; Carloni, P. Mechanism of Action of Cyclophilin A Explored by Metadynamics Simulations PLoS Comput. Biol. 2009, 5 e1000309
34. Lange, O. F.; Grubmuller, H. Full Correlation Analysis of Conformational Protein Dynamics Proteins 2008, 70, 1294-1312
35. Romo, T. D.; Grossfield, A.; Pitman, M. C. Concerted Interconversion between Ionic Lock Substates of the beta(2) Adrenergic Receptor Revealed by Microsecond Timescale Molecular Dynamics Biophys. J. 2010, 98, 76-84
36. Bucher, D.; Grant, B. J.; Markwick, P. R.; McCammon, J. A. Accessing a Hidden Conformation of the Maltose Binding Protein Using Accelerated Molecular Dynamics PLoS Comput. Biol. 2011, 7 e1002034
37. Mincer, J. S.; Schwartz, S. D. Rate-Promoting Vibrations and Coupled Hydrogen-Electron Transfer Reactions in the Condensed Phase: A Model for Enzymatic Catalysis J. Chem. Phys. 2004, 120, 7755-7760
38. Davarifar, A.; Antoniou, D.; Schwartz, S. D. The Promoting Vibration in Human Heart Lactate Dehydrogenase Is a Preferred Vibrational Channel J. Phys. Chem. B 2011, 115, 15439-15444
39. Camilloni, C.; Robustelli, P.; De Simone, A.; Cavalli, A.; Vendruscolo, M. Characterization of the Conformational Equilibrium between the Two Major Substates of RNase A Using NMR Chemical Shifts J. Am. Chem. Soc. 2012, 134, 3968-3971
40. Tantillo, D. J.; Chen, J. G.; Houk, K. N. Theozymes and Compuzymes: Theoretical Models for Biological Catalysis Curr. Opin. Chem. Biol. 1998, 2, 743-750
41. Kiss, G.; Celebi-Olcum, N.; Moretti, R.; Baker, D.; Houk, K. N. Computational Enzyme Design Angew. Chem., Int. Ed. 2013, 52, 5700-5725
42. Bhabha, G.; Lee, J.; Ekiert, D. C.; Gam, J.; Wilson, I. A.; Dyson, H. J.; Benkovic, S. J.; Wright, P. E. A Dynamic Knockout Reveals That Conformational Fluctuations Influence the Chemical Step of Enzyme Catalysis Science 2011, 332, 234-238
43. Fan, Y.; Cembran, A.; Ma, S. H.; Gao, J. L. Connecting Protein Conformational Dynamics with Catalytic Function As Illustrated in Dihydrofolate Reductase Biochemistry 2013, 52, 2036-2049
44. Loveridge, E. J.; Behiry, E. M.; Guo, J. N.; Allemann, R. K. Evidence That a 'Dynamic Knockout' in Escherichia coli Dihydrofolate Reductase Does Not Affect the Chemical Step of Catalysis Nat. Chem. 2012, 4, 292-297
45. Eisenmesser, E. Z.; Millet, O.; Labeikovsky, W.; Korzhnev, D. M.; Wolf-Watz, M.; Bosco, D. A.; Skalicky, J. J.; Kay, L. E.; Kern, D. Intrinsic Dynamics of an Enzyme Underlies Catalysis Nature 2005, 438, 117-121
46. Hardy, J. A.; Lam, J.; Nguyen, J. T.; O'Brien, T.; Wells, J. A. Discovery of an Allosteric Site in the Caspases Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 12461-12466
47. Erlanson, D. A.; Wells, J. A.; Braisted, A. C. Tethering: Fragment-Based Drug Discovery Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 199-223
48. Wang, N. K.; Majmudar, C. Y.; Pomerantz, W. C.; Gagnon, J. K.; Sadowsky, J. D.; Meagher, J. L.; Johnson, T. K.; Stuckey, J. A.; Brooks, C. L.; Wells, J. A.; Mapp, A. K. Ordering a Dynamic Protein Via a Small-Molecule Stabilizer J. Am. Chem. Soc. 2013, 135, 3363-3366
49. Pieper, U.; Webb, B. M.; Barkan, D. T.; Schneidman-Duhovny, D.; Schlessinger, A.; Braberg, H.; Yang, Z.; Meng, E. C.; Pettersen, E. F.; Huang, C. C.; Datta, R. S.; Sampathkumar, P.; Madhusudhan, M. S.; Sjolander, K.; Ferrin, T. E.; Burley, S. K.; Sali, A. ModBase, a Database of Annotated Comparative Protein Structure Models, And Associated Resources Nucleic Acids. Res. 2011, 39, D465-D474
50. Muller, M. M.; Allison, J. R.; Hongdilokkul, N.; Gaillon, L.; Kast, P.; van Gunsteren, W. F.; Marliere, P.; Hilvert, D. Directed Evolution of a Model Primordial Enzyme Provides Insights into the Development of the Genetic Code PLoS Genet. 2013, 9 e1003187
51. Yang, S. C.; Blachowicz, L.; Makowski, L.; Roux, B. Multidomain Assembled States of Hck Tyrosine Kinase in Solution Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 15757-15762
52. Furnham, N.; Blundell, T. L.; DePristo, M. A.; Terwilliger, T. C. Is One Solution Good Enough? Nat. Struct. Mol. Biol. 2006, 13, 184-5
53. Sinko, W.; de Oliveira, C.; Williams, S.; Van Wynsberghe, A.; Durrant, J. D.; Cao, R.; Oldfield, E.; McCammon, J. A. Applying Molecular Dynamics Simulations to Identify Rarely Sampled Ligand-Bound Conformational States of Undecaprenyl Pyrophosphate Synthase, an Antibacterial Target Chem. Biol. Drug Des. 2011, 77, 412-420
54. Agarwal, P. K.; Schultz, C.; Kalivretenos, A.; Ghosh, B.; Broedel, S. E. Engineering a Hyper-catalytic Enzyme by Photoactivated Conformation Modulation J. Phys. Chem. Lett. 2012, 3, 1142-1146