"strange kinetics" in the Temperature Dependence of Methionine ligand rebinding dynamics in cytochrome c

Journal of Physical Chemistry B

Volumn 117, Issue 24, 2013, Pages 7190-7202

  Zhang, Ping ^a   Ahn, Steven Wooseok ^a   Straub, John E ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; GLASS TRANSITION; LIGANDS; MOLECULAR DYNAMICS; PROTEINS; TEMPERATURE DISTRIBUTION;

CLASSICAL MOLECULAR DYNAMICS; DYNAMIC HETEROGENEITY; LIGAND DISSOCIATION; LOWER TEMPERATURES; PROTEIN ENERGY LANDSCAPE; PROTEIN STRUCTURES; STRUCTURAL ARRANGEMENT; TEMPERATURE DEPENDENCE;

DYNAMICS;

EID: 84879361819     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp400481m     Document Type: Article

References (58)

1. Negrerie, M.; Kruglik, S. G.; Lambry, J. C.; Vos, M. H.; Martin, J. L.; Franzen, S. Role of Heme Iron Coordination and Protein Structure in the Dynamics and Geminate Rebinding of Nitric Oxide to the H93G Myoglobin Mutant: Implication for Nitric Oxide Sensors J. Biol. Chem. 2006, 281, 10389-10398
2. Walther, M.; Raicu, V.; Ogilvie, J. P.; Phillips, R.; Kluger, R.; Miller, R. J. Determination of the Fe-CO Bond Energy in Myoglobin Using Heterodyne-Detected Transient Thermal Phase Grating Spectroscopy J. Phys. Chem. B 2005, 109, 20605-20611
3. Silkstone, G.; Jasaitis, A.; Wilson, M. T.; Vos, M. H. Ligand Dynamics in an Electron Transfer Protein. Picosecond Geminate Recombination of Carbon Monoxide to Heme in Mutant Forms of Cytochrome c J. Biol. Chem. 2007, 282, 1638-1649
4. Mizutani, Y.; Kitagawa, T. Ultrafast Dynamics of Myoglobin Probed by Time-Resolved Resonance Raman Spectroscopy Chem. Rec. 2001, 1, 258-275
5. McMahon, B. H.; Stojkovic, B. P.; Hay, P. J.; Martin, R. L.; Garcia, A. E. Microscopic Model of Carbon Monoxide Binding to Myoglobin J. Chem. Phys. 2000, 113, 6831-6850
6. Margulis, C. J.; Guallar, V.; Sim, E.; Friesner, R. A.; Berne, B. J. A New Semiempirical Approach to Study Ground and Excited States of Metal Complexes in Biological Systems J. Phys. Chem. B 2002, 106, 8038-8046
7. Yamashita, T.; Bouzhir-Sima, L.; Lambry, J. C.; Liebl, U.; Vos, M. H. Ligand Dynamics and Early Signaling Events in the Heme Domain of the Sensor Protein Dos from Escherichia coli J. Biol. Chem. 2008, 283, 2344-2352
8. Agmon, N.; Hopfield, J. J. CO Binding to Heme Proteins: A Model for Barrier Height Distributions and Slow Conformational Changes J. Chem. Phys. 1983, 79, 2042-2053
9. Nutt, D. R.; Karplus, M.; Meuwly, M. Potenial Energy Surfaces and Molecular Dynamics of MbNO: Existence of an Unsuspected FeON Minimum J. Phys. Chem. B 2005, 109, 21118-21125
10. Berlina, Y. A.; Fischer, S. F.; Chekunaevb, N. I.; Goldanskii, V. I. Non-Exponential Non-Arrhenius Relaxation in the Course of CO Rebinding to Heme Proteins Chem. Phys. 1995, 200, 369-385
11. Meuwly, M.; Becker, O. M.; Stote, R.; Karplus, M. NO Rebinding to Myoglobin: A Reactive Molecular Dynamics Study Biophys. Chem. 2002, 98, 183-207
12. Banushkina, P.; Meuwly, M. Free-Energy Barrier in MbCO Rebinding J. Phys. Chem. B 2005, 109, 16911-16917
13. Nutt, D. R.; Meuwly, M. Studying Reactive Processes with Classical Dynamics: Rebinding Dynamics in MbNO Biophys. J. 2006, 90, 1191-1201
14. Straub, J. E.; Karplus, M. Molecular Dynamics Study of the Photodissociation of Carbon Monoxide from Myoglobin: Ligand Dynamics in the First 10ps Chem. Phys. 1991, 158, 221-248
15. Petrich, J. W.; Lambry, J. C.; Kuczera, K.; Karplus, M.; Poyart, C.; Martin, J. L. Ligand Binding and Protein Relaxation in Heme Proteins: A Room Temperature Analysis of NO Geminate Recombination Biochemistry 1991, 30, 3975-3987
16. Schaad, O.; Zhou, H. X.; Szabo, A.; Eaton, W. A.; Henry, E. R. Simulation of the Kinetics of Ligand Binding to a Protein by Molecular Dynamics: Germinate Rebinding of Nitric Oxide to Myoglobin Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 9547-9551
17. Li, H.; Elber, R.; Straub, J. E. Molecular Dynamics Simulation of NO Recombination to Myoglobin Mutants J. Biol. Chem. 1993, 268, 17908-17916
18. Ma, J.; Huo, S.; Straub, J. E. Molecular Dynamics Simulation Study of the B-States of Solvated Carbon Monoxymyoglobin J. Am. Chem. Soc. 1997, 119, 2541-2551
19. Sagnella, D. E.; Straub, J. E. Directed Energy "Funneling" Mechanism for Heme Cooling Following Ligand Photolysis or Direct Excitation in Solvated Carbonmonoxy Myoglobin J. Phys. Chem. B 2001, 105, 7057-7063
20. Jensen, K. P.; Ryde, U. How O2 Binds to Heme J. Biol. Chem. 2004, 279, 14561-14569
21. Dunietz, B. D.; Dreuw, A.; Head-Gordon, M. Initial Steps of the Photodissociation of the CO Ligated Heme Group J. Phys. Chem. B 2003, 107, 5623-5629
22. Dreuw, A.; Dunietz, B. D.; Head-Gordon, M. Characterization of the Relevant Excited States in the Photodissociation of CO-Ligated Hemoglobin and Myoglobin J. Am. Chem. Soc. 2002, 124, 12070-12071
23. Harvey, J. N. DFT Computation of the Intrinsic Barrier to CO Germinate Recombination with Heme Compounds J. Am. Chem. Soc. 2000, 122, 12401-12402
24. Frauenfelder, H.; Sligar, S. G.; Wolynes, P. G. The Energy Landscapes and Motions of Proteins Science 1991, 254, 1598-1603
25. Gibson, Q. H.; Edelstein, J. S. Oxygen Binding and Subunit Interaction of Hemoglobin in Relation to the Two State Model J. Biol. Chem. 1987, 262, 516-519
26. Olson, J. S.; Rohlfs, R. J.; Gibson, Q. H. Ligand Recombination to the α and β Subunits of Human Hemoglobin J. Biol. Chem. 1987, 262, 12930-12938
27. Gibson, Q. H.; Regan, R.; Elber, R.; Olson, J. S.; Carver, T. E. Distal Pocket Residues Affect Picosecond Ligand Recombination in Myoglobin J. Biol. Chem. 1992, 267, 22022-22034
28. Carlson, M. L.; Regan, R.; Elber, R.; Li, H.; Phillips, G. N.; Olson, J. S.; Gibson, Q. H. NO Recombination to Double Mutants of Myoglobin: Role of Ligand Diffusion in a Fluctuating Heme Pocket Biochemistry 1994, 33, 10597-10606
29. Jongeward, K. A.; Magde, D.; Taube, D. J.; Traylor, T. G. Picosecond Kinetics of Cytochromes b5 and C* J. Biol. Chem. 1988, 263, 6027-6030
30. Agmon, N.; Sastry, G. M. Temperature-Dependent Effecitve Potential Explains CO Rebinding to Myoglobin Chem. Phys. 1996, 212, 207-219
31. Agmon, N.; Doster, W.; Post, F. The Transition from Inhomogeneous to Homogeneous Kinetics in CO Binding to Myoglobin Biophys. J. 1994, 66, 1612-1622
32. Austin, R.; Beeson, K.; Eisenstein, L.; Frauenfelder, H. Dynamics of Ligand Binding to Myoglobin Biochemistry 1975, 14, 5355-5373
33. Nienhaus, G. U.; Mourant, J. R.; FRauenfelder, H. Spectroscopic Evidence for Conformational Relaxation in Myoglobin Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 2902-2906
34. Ionascu, D.; Gruia, F.; Ye, X.; Yu, A.; Rosca, F.; Beck, C.; Demidov, A.; Olson, J. S.; Champion, P. M. Temperature-Dependent Studies of NO Recombination to Heme and Heme Proteins J. Am. Chem. Soc. 2005, 127, 16921-16934
35. Ye, X.; Ionascu, D.; Gruia, F.; Yu, A.; Benabbas, A.; Champion, P. M. Temperature-Dependent Heme Kinetics with Nonexponential Binding and Barrier Relaxation in the Absence of Protein Conformational Substates Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 14682-14687
36. Srajer, V.; Champion, P. M. Investigations of Optical Line Shapes and Kinetic Hole Burning in Myoglobin Biochemistry 1991, 30, 7390-7402
37. Srajer, V.; Schomacker, K.; Champion, P. Spectral Broadening in Biomolecules Phys. Rev. Lett. 1986, 57, 1267-1270
38. Zhang, P.; Malolepsza, E.; Straub, J. E. Dynamics of Methionine Ligand Rebinding in Cytochrome c J. Phys. Chem. B 2012, 116, 6980-6990
39. Wang, W.; Ye, X.; Demidov, A. A.; Rosca, F.; Sjodin, T.; Cao, W.; Sheeran, M.; Champion, P. M. Femtosecond Multicolor Pump-Probe Spectroscopy of Ferrous Cytochrome c J. Phys. Chem. B 2000, 104, 10789-10801
40. Negrerie, M.; Cianetti, S.; Vos, M. H.; Martin, J. L.; Kruglik, S. G. Ultrafast Heme Dynamics in Ferrous Versus Ferric Cytochrome c Studied by Time-Resolved Resonance Raman and Transient Absorption Spectroscopy J. Phys. Chem. B 2006, 110, 12766-12781
41. Vos, M. H.; Battistoni, A.; Lechauve, C.; Marden, M. C.; Kiger, L.; Desbois, A.; Pilet, E.; de Rosny, E.; Liebl, U. Ultrafast Heme Residue Bond Formation in Six-Coordinate Heme Proteins: Implications for Functional Ligand Exchange Biochemistry 2008, 47, 5718-5723
42. Zang, C.; Stevens, J. A.; Link, J. J.; Guo, L.; Wang, L.; Zhong, D. Ultrafast Proteinquake Dynamics in Cytochrome c J. Am. Chem. Soc. 2009, 131, 2846-2852
43. Jorgensen, W.; Chandrasekhar, J.; Madura, J.; Impey, R.; Klein, M. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935
44. Verlet, L. Computer Experiments on Classical Fluids. I. Thermodynamical Properties of Lennard-Jones Molecules Phys. Rev. 1967, 1, 98-103
45. MacKerell, A. D.; Bashford, D.; Bellott, M.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
46. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. 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
47. Amadei, A.; Linssen, A.; Berendsen, H. Essential Dyanmics of Proteins Proteins 1993, 17, 412-425
48. Fischer, S.; Karplus, M. Conjugate Peak Refinement: an Algorithm for Finding Reaction Paths and Accurate Transition States in Systems with Many Degrees of Freedom Chem. Phys. Lett. 1992, 194, 252-261
49. Frauenfelder, H.; Wolynes, P. G. Rate Theories and Puzzles of Hemeprotein Kinetics Science 1985, 229, 337-345
50. Straub, J.; Berne, B. A Statistical Theory for the Effect of Nonadiabatic Transition on Activated Processes J. Chem. Phys. 1987, 87, 6111-6116
51. Berne, B.; Borkovec, M.; Straub, J. Classical and Modern Methods in Reaction Rate Theory J. Phys. Chem. 1988, 92, 3711-3725
52. Biroli, G.; Garrahan, J. P. Perspective: The Glass Transition J. Chem. Phys. 2013, 138, 12A301
53. Chandler, D.; Garrahan, J. Dynamics on the Way to Forming Glass: Bubbles in Space-Time Annu. Rev. Phys. Chem. 2010, 61, 191-217
54. Agmon, N.; Rabinovich, S. Diffusive Dynamics on Potential Energy Surfaces: Nonequilibrium CO Binding to Heme Proteins J. Chem. Phys. 1992, 97, 7270-7286
55. Elber, R.; Karplus, M. Multiple Conformational States of Proteins: A Molecular Dynamics Analysis of Myoglobin Science 1987, 235, 318-321
56. Friedman, M.; Rousseau, D. L.; Ondrias, M. R.; Stepnoski, R. A. Transient Raman Study of Hemoglobin:Structural Dependence of the Iron-Histidine Linkage Science 1982, 218, 1244-1246
57. Gerstman, B. S. CO Binding to Hemoglobin: Spin-Tunneling Temperature, Fe Electronic States, and Electronic Effects on Nonadiabatic Dynamics J. Chem. Phys. 1988, 88, 6228-6232
58. Sabelko, J.; Ervin, J.; Gruebele, M. Observation of Strange Kinetics in Protein Folding Proc. Nat. Acad. Sci. USA 1999, 96, 6031-6036