Identification of ubiquinol binding motifs at the QoSite of the cytochrome bc 1 complex

Journal of Physical Chemistry B

Volumn 119, Issue 2, 2015, Pages 433-447

  Barragan, Angela M ^a,b   Crofts, Antony R ^c   Schulten, Klaus ^a,b   Solov'Yov, Ilia A ^d,e  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e IOFFE INSTITUTE   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; ELECTRON TRANSITIONS; ENZYMES; HYDROGEN BONDS; MOLECULAR DYNAMICS; QUANTUM CHEMISTRY; REACTION KINETICS; SYNTHESIS (CHEMICAL);

AMINO ACID RESIDUES; ELECTRON ACCEPTOR; ELECTRON TRANSFER; IRON-SULFUR CLUSTERS; PROTON COUPLED ELECTRON TRANSFERS; PROTON-MOTIVE FORCES; QUANTUM CHEMICAL CALCULATIONS; RHODOBACTER CAPSULATUS;

ELECTRONS;

PROTEIN BINDING; UBIQUINOL; UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE; WATER;

ANALOGS AND DERIVATIVES; CHEMISTRY; ELECTRON TRANSPORT; ENZYMOLOGY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN MOTIF; QUANTUM THEORY; RHODOBACTER CAPSULATUS;

AMINO ACID MOTIFS; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX III; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; QUANTUM THEORY; RHODOBACTER CAPSULATUS; UBIQUINONE; WATER;

EID: 84921282815     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp510022w     Document Type: Article

References (91)

1. Mitchell, P. D. Nobel Lectures in Chemistry 1971-1980; World Scientific Publishing Co.: Hackensack, NJ, 1993.
2. Nicholls, D. G.; Ferguson, S. Bioenergetics; Academic Press: New York, NY, 2013.
3. Wikstrom, M.; Krab, K.; Saraste, M. Proton-Translocating Cytochrome Complexes Annu. Rev. Biochem. 1981, 50, 623-655
4. 1 Nature 1998, 392, 677-684
5. 1 Complex of Mitochondria and Photosynthetic Bacteria Curr. Opin. Struct. Biol. 1998, 8, 501-509
6. 1 Complex: Reaction Mechanism and Prevention of Short-circuiting Biochim. Biophys. Acta, Bioenerg. 2005, 1709, 5-34
7. Cramer, W. A.; Hasan, S. S.; Yamashita, E. The Q-cycle of Cytochrome bc Complexes: A Structure Perspective Biochim. Biophys. Acta, Bioenerg. 2011, 1807, 788-802
8. 1 Complex from Bovine Heart Mitochondria Science 1997, 277, 60-66
9. 1 Complex with its Bound Substrate Cytochrome c Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 2800-2805
10. 1: Comparison with its Mitochondrial and Chloroplast Counterparts Photosynth. Res. 2004, 81, 251-275
11. Mitchell, P. Possible Molecular Mechanisms of the Protonmotive Function of Cytochrome Systems J. Theor. Biol. 1976, 62, 327-367
12. 1 Complex of Rhodobacter Capsulatus Biochemistry 1992, 31, 11864-11873
13. 1 Complex Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 10021-10026
14. 1 Complex: Effects on the Biophysical Properties of the Rieske Iron-Sulfur Protein and on the Kinetics of the Complex J. Biol. Chem. 2010, 285, 9233-9248
15. 1 with Bound Substrate and Inhibitors at the Qi Site Biochemistry 2003, 42, 9067-9080
16. 1 Complex from the Yeast Saccharomyces Cerevisiae Co-crystallized with an Antibody Fv Fragment Structure 2000, 8, 669-684
17. Ark, G. V.; Berden, J. A. Binding of HQNO to Beef-Heart Sub-mitochondrial Particles Biochim. Biophys. Acta, Bioenerg. 1977, 459, 119-137
18. Grimard, V.; Lensink, M.; Debailleul, F.; Ruysschaert, J.-M.; Govaerts, C. Bacterial Membranes: Structural and Molecular Biology; Horizon Scientific Press: Wymondham, UK, 2014; Chapter 6.
19. 1 Complex Biophys. J. 1999, 77, 1753-1768
20. 1 Complex: Different Domains of the Quinol Binding Pocket and Their Role in the Mechanism and Binding of Inhibitors Biochemistry 1999, 38, 15807-15826
21. 1 Complex Predicted by Atomistic Molecular Dynamics Simulations Biochim. Biophys. Acta, Bioenerg. 2013, 1827, 761-768
22. Ullmann, M. G.; Noodleman, L.; Case, D. A. Density Functional Calculation of pKa Values and Redox Potentials in the Bovine Rieske Iron-Sulfur Protein J. Biol. Inorg. Chem. 2002, 7, 632-639
23. 1: Comparison with its Mitochondrial and Chloroplast Counterparts Photosynth. Res. 2004, 81, 251-275
24. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
25. Mackerell, A. D.; Feig, M.; Brooks, C. L. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
26. 1 Complex for Atomistic Molecular Dynamics Simulations Theor. Chem. Acc. 2013, 132, 1-13
27. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A. Gaussian 09, Revision D.01; Gaussian Inc.: Wallingford, CT, 2009.
28. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38
29. Yang, X.; Trumpower, B. Purification of a Three-Subunit Ubiquinol-Cytochrome c Oxidoreductase Complex from Paracoccus Denitrificans J. Biol. Chem. 1986, 261, 12282-12289
30. 1 from the Photosynthetic Bacterium Rhodobacter sphaeroides J. Biol. Chem. 2008, 283, 2846-2857
31. Aguayo, D.; González-Nilo, F. D.; Chipot, C. Insight into the Properties of Cardiolipin Containing Bilayers from Molecular Dynamics Simulations, Using a Hybrid All-Atom/United-Atom Force Field J. Chem. Theory Comput. 2012, 8, 1765-1773
32. Feller, S. E.; Yin, D.; Pastor, R. W.; MacKerell, A. Molecular Dynamics Simulation of Unsaturated Lipid Bilayers at Low Hydration: Parameterization and Comparison with Diffraction Studies Biophys. J. 1997, 73, 2269-2279
33. Becke, A. D. Density-Functional Thermochemistry. III. The Role of Exact Exchange J. Chem. Phys. 1993, 98, 5648-5652
34. Bayly, C. I.; Cieplak, P.; Cornell, W.; Kollman, P. A. A Well-Behaved Electrostatic Potential Based Method Using Charge Restraints for Deriving Atomic Charges: the RESP Model J. Phys. Chem. 1993, 97, 10269-10280
35. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An Nlog(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
36. Feller, S. E.; Zhang, Y.; Pastor, R. W.; Brooks, B. R. Constant Pressure Molecular Dynamics Simulation: the Langevin Piston Method J. Chem. Phys. 1995, 103, 4613-4621
37. Shoji, M.; Koizumi, K.; Kitagawa, Y.; Yamanaka, S.; Okumura, M.; Yamaguchi, K. Theory of Chemical Bonds in Metalloenzymes IV: Hybrid-DFT Study of Rieske-type [2Fe-2S] Clusters Int. J. Quantum Chem. 2007, 107, 609-627
38. Bassan, A.; Blomberg, M. R.; Borowski, T.; Siegbahn, P. E. Oxygen Activation by Rieske Non-heme Iron Oxygenases, a Theoretical Insight J. Phys. Chem. B 2004, 108, 13031-13041
39. Salomon, O.; Reiher, M.; Hess, B. A. Assertion and Validation of the Performance of the B3LYP Functional for the First Transition Metal Row and the G2 Test Set J. Chem. Phys. 2002, 117, 4729-4737
40. Niu, S.; Nichols, J. A.; Ichiye, T. Optimization of Spin-Unrestricted Density Functional Theory for Redox Properties of Rubredoxin Redox Site Analogues J. Chem. Theory Comput. 2009, 5, 1361-1368
41. Sigfridsson, E.; Olsson, M. H.; Ryde, U. A Comparison of the Inner-Sphere Reorganization Energies of Cytochromes, Iron-Sulfur Clusters, and Blue Copper Proteins J. Phys. Chem. B 2001, 105, 5546-5552
42. 15N NMR Chemical Shifts in Iron-Sulfur Proteins as Determined by Comparison of Experimental Data with Hybrid Density Functional Calculations J. Am. Chem. Soc. 1998, 120, 4806-4814
43. Sigfridsson, E.; Olsson, M. H.; Ryde, U. Inner-Sphere Reorganization Energy of Iron-Sulfur Clusters Studied with Theoretical Methods Inorg. Chem. 2001, 40, 2509-2519
44. Szilagyi, R. K.; Winslow, M. A. On the Accuracy of Density Functional Theory for Iron-Sulfur Clusters J. Comput. Chem. 2006, 27, 1385-1397
45. Berry, E. A.; Guergova-Kuras, M.; Huang, L. S.; Crofts, A. R. Structure and function of Cytochrome bc Complexes Annu. Rev. Biochem. 2000, 69, 1005-1075
46. 1 Complex in Rhodobacter Sphaeroides J. Biol. Chem. 1999, 274, 33931-33944
47. 1 Complex Biochemistry 2000, 39, 7436-7444
48. Zu, Y.; Couture, M. M.-J.; Kolling, D. R.; Crofts, A. R.; Eltis, L. D.; Fee, J. A.; Hirst, J. Reduction Potentials of Rieske Clusters: Importance of the Coupling Between Oxidation State and Histidine Protonation State Biochemistry 2003, 42, 12400-12408
49. Kolling, D. J.; Brunzelle, J. S.; Lhee, S.; Crofts, A. R.; Nair, S. K. Atomic Resolution Structures of Rieske Iron-Sulfur Protein: Role of Hydrogen Bonds in Tuning the Redox Potential of Iron-Sulfur Clusters Structure 2007, 15, 29-38
50. Kolling, D. R.; Samoilova, R. I.; Shubin, A. A.; Crofts, A. R.; Dikanov, S. A. Proton Environment of Reduced Rieske Iron-Sulfur Cluster Probed by Two-Dimensional ESEEM Spectroscopy J. Phys. Chem. A 2008, 113, 653-667
51. Hsueh, K.-L.; Westler, W. M.; Markley, J. L. NMR Investigations of the Rieske Protein from Thermus Thermophilus Support a Coupled Proton and Electron Transfer Mechanism J. Am. Chem. Soc. 2010, 132, 7908-7918
52. 15N NMR Titration Study Demonstrates the Role of Iron-Ligated Histidines in the pH Dependence of the Reduction Potential J. Am. Chem. Soc. 2006, 128, 10672-10673
53. 1 Complex J. Phys. Chem. Lett. 2013, 4, 3602-3606
54. 1 Complex Biochemistry 1995, 34, 16004-16012
55. Hammes-Schiffer, S. Current Theoretical Challenges in Proton-Coupled Electron Transfer: Electron-Proton Nonadiabaticity, Proton Relays, and Ultrafast Dynamics J. Phys. Chem. Lett. 2011, 2, 1410-1416
56. Hammes-Schiffer, S. Catalytic Efficiency of Enzymes: A Theoretical Analysis Biochemistry 2013, 52, 2012-2020
57. Solov'yov, I. A.; Domratcheva, T.; Moughal Shahi, A. R.; Schulten, K. Decrypting Cryptochrome: Revealing the Molecular Identity of the Photoactivation Reaction J. Am. Chem. Soc. 2012, 134, 18046-18052
58. Moughal Shahi, A. R.; Domratcheva, T. Challenges in Computing Electron-Transfer Energies of DNA Repair Using Hybrid QM/MM Models J. Chem. Theory Comput. 2013, 9, 4644-4652
59. Solov'yov, I. A.; Domratcheva, T.; Schulten, K. Separation of Photoinduced Radical Pair in Cryptochrome to a Functionally Critical Distance Sci. Rep. 2014, 4, 1-8
60. Dittrich, M.; Freddolino, P. L.; Schulten, K. J. When Light Falls in LOV: A Quantum Mechanical/Molecular Mechanical Study of Photoexcitation in Phot-LOV1 of Chlamydomonas reinhardtii J. Phys. Chem. B 2005, 109, 13006-13013
61. Zou, X.; Ma, W.; Solov'yov, I. A.; Chipot, C.; Schulten, K. Recognition of Methylated DNA Through Methyl-CpG Binding Domain Proteins Nucleic Acids Res. 2012, 40, 2747-2758
62. Mitchell, P. The Protonmotive Q-cycle: A General Formulation FEBS Lett. 1975, 59, 137-139
63. Brandt, U.; Okun, J. G. Role of Deprotonation Events in Ubihydroquinone: Cytochrome c Oxidoreductase from Bovine Heart and Yeast Mitochondria Biochemistry 1997, 36, 11234-11240
64. 1 Complex by Blocking a Protonatable Group J. Biol. Chem. 1995, 270, 25001-25006
65. 1 Complex in Paracoccus Denitrificans Eur. J. Biochem. 1998, 255, 100-106
66. 1 Complexes Containing Site-Directed Mutants of the Rieske Iron-Sulfur Protein Biochim. Biophys. Acta, Bioenerg. 1998, 1365, 125-134
67. 1 Complex Controls the Rate of Ubihydroquinone Oxidation Biochim. Biophys. Acta, Bioenerg. 2004, 1655, 77-92
68. Link, T. A. Two pK Values of the Oxidised Rieske [2Fe-2S] Cluster Observed by CD Spectroscopy Biochim. Biophys. Acta, Bioenerg. 1994, 1185, 81-84
69. Leggate, E. J.; Hirst, J. Roles of the Disulfide Bond and Adjacent Residues in Determining the Reduction Potentials and Stabilities of Respiratory-type Rieske Clusters Biochemistry 2005, 44, 7048-7058
70. 1 Complex Determined by MAD Phasing at 1.5 Å Resolution Structure 1996, 4, 567-579
71. Colbert, C. L.; Couture, M. M.-J.; Eltis, L. D.; Bolin, J. T. A Cluster Exposed: Structure of the Rieske Ferredoxin From Biphenyl Dioxygenase and the Redox Properties of Rieske Fe-S proteins Structure 2000, 8, 1267-1278
72. Hunsicker-Wang, L. M.; Heine, A.; Chen, Y.; Luna, E. P.; Todaro, T.; Zhang, Y. M.; Williams, P. A.; McRee, D. E.; Hirst, J.; Stout, C. D. A Cluster Exposed: Structure of the Rieske Ferredoxin From Biphenyl Dioxygenase and the Redox Properties of Rieske Fe-S Proteins Biochemistry 2003, 42, 7303-731
73. Dikanov, S. A.; Kolling, D. R.; Endeward, B.; Samoilova, R. I.; Prisner, T. F.; Nair, S. K.; Crofts, A. R. Identification of Hydrogen Bonds to the Rieske Cluster Through the Weakly Coupled Nitrogens Detected by Electron Spin Echo Envelope Modulation Spectroscopy J. Biol. Chem. 2006, 281, 27416-27425
74. 1 Complex by ATR-FTIR Spectroscopy Biochemistry 2005, 44, 4230-4237
75. Boveris, A. Determination of the Production of Superoxide Radicals and Hydrogen Peroxide in Mitochondria Methods Enzymol. 1984, 105, 429-435
76. Muller, F. The Nature and Mechanism of Superoxide Production by the Electron Transport Chain: its Relevance to Aging J. Am. Aging Assoc. 2000, 23, 227-253
77. Turrens, J. F.; Alexandre, A.; Lehninger, A. L. Ubisemiquinone is the Electron Donor for Superoxide Formation by Complex III of Heart Mitochondria Arch. Biochem. Biophys. 1985, 237, 408-414
78. Beckman, K. B.; Ames, B. N. The Free Radical Theory of Aging Matures Physiol. Rev. 1998, 78, 547-581
79. Harman, D. Free Radical Theory of Aging Mutat. Res. 1992, 275, 257-266
80. Muller, F. L.; Lustgarten, M. S.; Jang, Y.; Richardson, A.; Van Remmen, H. Trends in Oxidative Aging Theories Free Radical Biol. Med. 2007, 43, 477-503
81. 1 Complex Biochim. Biophys. Acta, Bioenerg. 2013, 1827, 1362-1377
82. LeBard, D. N.; Matyushov, D. V. Protein-Water Electrostatics and Principles of Bioenergetics Phys. Chem. Chem. Phys. 2010, 12, 15335-15348
83. 1 Complex Biochim. Biophys. Acta, Bioenerg. 2013, 1827, 365-386
84. Hammes-Schiffer, S.; Soudackov, A. V. Proton-Coupled Electron Transfer in Solution, Proteins, and Electrochemistry J. Phys. Chem. B 2008, 112, 14108-14123
85. 1 Complex: Importance for the Q-cycle and Superoxide Production Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 7887-7892
86. o Semiquinone Radical Biochim. Biophys. Acta, Bioenerg. 2007, 1767, 883-887
87. Cammack, R.; MacMillan, F. Metals in Biology; Springer: Secaucus, NJ, 2010; pp 11-44.
88. Vennam, P. R.; Fisher, N.; Krzyaniak, M. D.; Kramer, D. M.; Bowman, M. K. A caged, destabilized free radical intermediate in the Q-Cycle Chem. Biochem. 2013, 14, 1745-1753
89. Eriksen, J.; Sauer, S.; Mikkelsen, K.; Jensen, H.; Kongsted, J. On the Importance of Excited State Dynamic Response Electron Correlation in Polarizable Embedding Methods J. Comput. Chem. 2012, 33, 2012-2022
90. Knecht, S.; Marian, C.; Kongsted, J.; Mennucci, B. On the Photophysics of Carotenoids: A Multireference DFT Study of Peridinin J. Phys. Chem. B 2013, 117, 13808-13815
91. Beerepoot, M.; Steindal, A.; Kongsted, J.; Brandsdal, B.; Frediani, L.; Ruud, K.; Olsen, J. A Polarizable Embedding DFT Study of One-Photon Absorption in Fluorescent Proteins Phys. Chem. Chem. Phys. 2013, 15, 4735-4743