A theoretical investigation of the functional role of the axial methionine ligand of the CuA site in cytochrome c oxidase

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 10, 2011, Pages 1314-1327

  Kang, Jiyoung ^a   Kino, Hiori ^b   Tateno, Masaru ^c  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^c UNIVERSITY OF HYOGO   (Japan)

Author keywords

Electron transfer; Electronic structure; Hybrid QM MM calculation; Redox potential; Structural modeling; Transition metal binding protein

Indexed keywords

AMINO ACID; AXIAL METHIONINE LIGAND; COPPER ION; CYTOCHROME C OXIDASE; METHIONINE; PROTON PUMP; UNCLASSIFIED DRUG;

CONFERENCE PAPER; ELECTRON TRANSPORT; ENERGY METABOLISM; ENZYME ACTIVITY; HYBRIDIZATION; MOLECULAR MECHANICS; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN STRUCTURE; QUANTUM MECHANICS; REGULATORY MECHANISM;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATTLE; COMPUTATIONAL BIOLOGY; COPPER; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; LIGANDS; METHIONINE; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; OXIDATION-REDUCTION; PROTEIN STRUCTURE, TERTIARY; QUANTUM THEORY; SEQUENCE HOMOLOGY, AMINO ACID; THERMODYNAMICS;

BOVINAE;

EID: 80051600211     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.06.014     Document Type: Conference Paper

References (64)

1. A. Namslauer, and P. Brzezinski Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase FEBS Lett. 567 2004 103 110 (Pubitemid 38686431)
2. S. Papa, N. Capitanio, and G. Capitanio A cooperative model for proton pumping in cytochrome c oxidase Biochim. Biophys. Acta 1655 2004 353 364 (Pubitemid 38526199)
3. V.R.I. Kaila, M.I. Verkhovsky, and M. Wikström Proton-coupled electron transfer in cytochrome oxidase Chem. Rev. 110 2010 7062 7081
4. J.J. Regan, B.E. Ramirez, J.R. Winkler, H.B. Gray, and B.G. Malmstrom Pathways for electron tunneling in cytochrome c oxidase J. Bioenerg. Biomembr. 30 1998 35 39 (Pubitemid 28262405)
5. M.L. Tan, I. Balabin, and J.N. Onuchic Dynamics of electron transfer pathways in cytochrome c oxidase Biophys. J. 86 2004 1813 1819 (Pubitemid 38295614)
6. C.C. Moser, C.C. Page, and P.L. Dutton Darwin at the molecular scale: selection and variance in electron tunnelling proteins including cytochrome c oxidase Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 2006 1295 1305 (Pubitemid 44338490)
7. A to heme a electron transfer in Paracoccus denitrificans cytochrome c oxidase Biophys. J. 90 2006 2131 2137
8. T. Tsukihara, H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono, and S. Yoshikawa The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A Science 272 1996 1136 1144
9. C. Ostermeier, A. Harrenga, U. Ermler, and H. Michel Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment Proc. Natl. Acad. Sci. U. S. A. 94 1997 10547 10553
10. 3-cytochrome c oxidase from Thermus thermophilus EMBO J. 19 2000 1766 1776 (Pubitemid 30204388)
11. M. Svensson-Ek, J. Abramson, G. Larsson, S. Tornroth, P. Brzezinski, and S. Iwata The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides J. Mol. Biol. 321 2002 329 339
12. A centers and their biosynthetic models in azurin J. Biol. Inorg. Chem. 15 2010 461 483
13. S. Iwata, C. Ostermeier, B. Ludwig, and H. Michel Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans Nature 376 1995 660 669
14. P.M. Kroneck, W.A. Antholine, J. Riester, and W.G. Zumft The cupric site in nitrous oxide reductase contains a mixed-valence [Cu(II), Cu(I)] binuclear center: a multifrequency electron paramagnetic resonance investigation FEBS Lett. 242 1988 70 74 (Pubitemid 19012251)
15. A in cytochrome c oxidase FEBS Lett. 248 1989 212 213
16. A-type centers: ligand-field control of ground-state properties related to electron transfer J. Am. Chem. Soc. 120 1998 5246 5263 (Pubitemid 28328888)
17. S. DeBeer George, M. Metz, R.K. Szilagyi, H. Wang, S.P. Cramer, Y. Lu, W.B. Tolman, B. Hedman, K.O. Hodgson, and E.I. Solomon A quantitative description of the ground-state wave function of Cu(A) by X-ray absorption spectroscopy: comparison to plastocyanin and relevance to electron transfer J. Am. Chem. Soc. 123 2001 5757 5767 (Pubitemid 32904711)
18. A-binding site in cytochrome c oxidase FEBS Lett. 268 1990 5 7 (Pubitemid 20233816)
19. S.M. Berry, M. Ralle, D.W. Low, N.J. Blackburn, and Y. Lu Probing the role of axial methionine in the blue copper center of azurin with unnatural amino acids J. Am. Chem. Soc. 125 2003 8760 8768 (Pubitemid 36896121)
20. D.K. Garner, M.D. Vaughan, H.J. Hwang, M.G. Savelieff, S.M. Berry, J.F. Honek, and Y. Lu Reduction potential tuning of the blue copper center in Pseudomonas aeruginosa azurin by the axial methionine as probed by unnatural amino acids J. Am. Chem. Soc. 128 2006 15608 15617 (Pubitemid 44894099)
21. A domain of cyanobacterial cytochrome c oxidase J. Biol. Chem. 279 2004 10293 10303 (Pubitemid 38372636)
22. A center than in a blue copper center J. Am. Chem. Soc. 127 2005 7274 7275 (Pubitemid 40753581)
23. A center Biochemistry 38 1999 5677 5683 (Pubitemid 29220587)
24. A site in cytochrome c oxidase of Rhodobacter sphaeroides: II. Rapid kinetic analysis of electron transfer Biochemistry 41 2002 2298 2304 (Pubitemid 34160891)
25. A site in cytochrome c oxidase of Rhodobacter sphaeroides: I. Spectral and functional properties Biochemistry 41 2002 2288 2297 (Pubitemid 34160890)
26. A sites J. Am. Chem. Soc. 129 2007 11884 11885 (Pubitemid 47512003)
27. T. Ohta, Y. Hagiwara, J. Kang, K. Nishikawa, T. Yamamoto, H. Nagao, and M. Tateno Evaluation of electronic and geometrical properties of the blue copper site in fully solvated azurin by QM/MM hybrid calculations using a new interface program connecting QM and MM engines J. Comput. Theor. Nanosci. 6 2009 2648 2655
28. A site: factors that influence delocalization and their contributions to electron transfer J. Am. Chem. Soc. 130 2008 5194 5205 (Pubitemid 351537080)
29. 2O reductase J. Am. Chem. Soc. 128 2006 16452 16453 (Pubitemid 46032695)
30. A redox site in cytochrome c oxidase into a mononuclear copper center Biochemistry 36 1997 3232 3236 (Pubitemid 27142395)
31. A azurin Inorg. Chem. 45 2006 102 107
32. K. Muramoto, K. Hirata, K. Shinzawa-Itoh, S. Yoko-o, E. Yamashita, H. Aoyama, T. Tsukihara, and S. Yoshikawa A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 104 2007 7881 7886 (Pubitemid 47185845)
33. D.A. Case, T.A. Darden, T.E.C. III, C.L. Simmerling, R.E.D.J. Wang, K.M.M.R. Luo, D.A. Pearlman, M. Crowley, R.C. Walker, W. Zhang, B. Wang, S. Hayik, A. Roitberg, G. Seabra, K.F. Wong, F. Paesani, X. Wu, S. Brozell, V. Tsui, H. Gohlke, L. Yang, C. Tan, J. Mongan, V. Hornak, G. Cui, P. Beroza, D.H. Mathews, C. Schafmeister, W.S. Ross, and P.A. Kollman AMBER9 2006
34. C.I. Bayly, P. Cieplak, W. Cornell, and P.A. Kollman A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model J. Phys. Chem. 97 1993 10269 10280
35. A.D. Becke Density-functional thermochemistry. III. The role of exact exchange J. Chem. Phys. 98 1993 5648 5652
36. M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, J.A.M. Jr., T. Vreven, K.N. Kudin, J.C. Burant, J.M. Millam, S.S. Iyengar, J. Tomasi, V. Barone, B. Mennucci, M. Cossi, G. Scalmani, N. Rega, G.A. Petersson, H. Nakatsuji, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, M. Klene, X. Li, J.E. Knox, H.P. Hratchian, J.B. Cross, V. Bakken, C. Adamo, J. Jaramillo, R. Gomperts, R.E. Stratmann, O. Yazyev, A.J. Austin, R. Cammi, C. Pomelli, J.W. Ochterski, P.Y. Ayala, K. Morokuma, G.A. Voth, P. Salvador, J.J. Dannenberg, V.G. Zakrzewski, S. Dapprich, A.D. Daniels, M.C. Strain, O. Farkas, D.K. Malick, A.D. Rabuck, K. Raghavachari, J.B. Foresman, J.V. Ortiz, Q. Cui, A.G. Baboul, S. Clifford, J. Cioslowski, B.B. Stefanov, A.L.G. Liu, P. Piskorz, I. Komaromi, R.L. Martin, D.J. Fox, T. Keith, M.A. Al-Laham, C.Y. Peng, A. Nanayakkara, M. Challacombe, P.M.W. Gill, B. Johnson, W. Chen, M.W. Wong, C. Gonzalez, and J.A. Pople 2004 Gaussian, Inc. Wallingford CT
37. A. Schafer, C. Huber, and R. Ahlrichs Fully optimized contracted Gaussian basis sets of triple zeta valence quality for atoms Li to Kr J. Chem. Phys. 100 1994 5829 5835
38. V.A. Rassolov, J.A. Pople, M.A. Ratner, and T.L. Windus 6-31G basis set for atoms K through Zn J. Chem. Phys. 109 1998 1223 1229 (Pubitemid 128678537)
39. A. Oda, N. Yamaotsu, and S. Hirono New AMBER force field parameters of heme iron for cytochrome P450s determined by quantum chemical calculations of simplified models J. Comput. Chem. 26 2005 818 826 (Pubitemid 40751576)
40. 2 docking J. Phys. Chem. B 108 2004 20376 20387 (Pubitemid 40079159)
41. J. Wang, R.M. Wolf, J.W. Caldwell, P.A. Kollman, and D.A. Case Development and testing of a general amber force field J. Comput. Chem. 25 2004 1157 1174
42. Y. Hagiwara, T. Ohta, and M. Tateno QM/MM hybrid calculation of biological macromolecules using a new interface program connecting QM and MM engines J. Phys.: Condens. Matt. 21 2009 (064234)
43. S.M. Cybulski, and C.E. Seversen Critical examination of the supermolecule density functional theory calculations of intermolecular interactions J. Chem. Phys. 122 2005 014117 014119
44. M.W. Schmidt, K.K. Baldridge, J.A. Boatz, S.T. Elbert, M.S. Gordon, J.H. Jensen, S. Koseki, N. Matsunaga, K.A. Nguyen, S. Su, T.L. Windus, M. Dupuis, and J.A. Montgomery General atomic and molecular electronic structure system J. Comput. Chem. 14 1993 1347 1363
45. V. Tipmanee, H. Oberhofer, M. Park, K.S. Kim, and J. Blumberger Prediction of reorganization free energies for biological electron transfer: a comparative study of Ru-modified cytochromes and a 4-helix bundle protein J. Am. Chem. Soc. 132 2010 17032 17040
46. J. Blumberger Free energies for biological electron transfer from QM/MM calculation: method, application and critical assessment Phys. Chem. Chem. Phys. 10 2008 5651
47. J. Blumberger, and M.L. Klein Reorganization free energies for long-range electron transfer in a porphyrin-binding four-helix bundle protein J. Am. Chem. Soc. 128 2006 13854 13867 (Pubitemid 44632865)
48. V.R. Kaila, M.P. Johansson, D. Sundholm, and M. Wikstrom Interheme electron tunneling in cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 107 2010 21470 21475
49. C.C. Moser, J.M. Keske, K. Warncke, R.S. Farid, and P.L. Dutton Nature of biological electron transfer Nature 355 1992 796 802
50. R.A. Marcus, and N. Sutin Electron transfers in chemistry and biology Biochim. Biophys. Acta 811 1985 265 322 (Pubitemid 15246565)
51. A.M. Kelterer, S. Landgraf, and G. Grampp Quantum mechanical investigation of the inner-sphere reorganization energy of cyclooctatetraene/ cyclooctatetraene radical anion. Part I Spectrochim. Acta A Mol. Biomol. Spectrosc. 57 2001 1959 1969
52. Molecular Operating Environment (MOE) version 2003.02 2003 Chemical Computing Group Quebec, Canada
53. L.M. Hunsicker-Wang, R.L. Pacoma, Y. Chen, J.A. Fee, and C.D. Stout A novel cryoprotection scheme for enhancing the diffraction of crystals of recombinant cytochrome ba3 oxidase from Thermus thermophilus Acta Crystallogr. D Biol. Crystallogr. 61 2005 340 343 (Pubitemid 43965375)
54. T. Fechteler, U. Dengler, and D. Schomburg Prediction of protein three-dimensional structures in insertion and deletion regions: a procedure for searching data bases of representative protein fragments using geometric scoring criteria J. Mol. Biol. 253 1995 114 131
55. M. Levitt Accurate modeling of protein conformation by automatic segment matching J. Mol. Biol. 226 1992 507 533
56. D.M. Ferguson, and D.J. Raber A new approach to probing conformational space with molecular mechanics: random incremental pulse search J. Am. Chem. Soc. 111 1989 4371 4378
57. A binding site in subunit II of cytochrome c oxidase J. Biol. Chem. 270 1995 25363 25369
58. M. Hay, J.H. Richards, and Y. Lu Construction and characterization of an azurin analog for the purple copper site in cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 93 1996 461 464 (Pubitemid 26038177)
59. A site by NMR spectroscopy J. Am. Chem. Soc. 131 2009 1939 1946
60. S. Corni, F. De Rienzo, R. Di Felice, and E. Molinari Role of the electronic properties of azurin active site in the electron-transfer process Int. J. Quantum Chem. 102 2005 328 342 (Pubitemid 40437004)
61. D.K. Garner, M.D. Vaughan, H.J. Hwang, M.G. Savelieff, S.M. Berry, J.F. Honek, and Y. Lu Reduction potential tuning of the blue copper center in Pseudomonas aeruginosa azurin by the axial methionine as probed by unnatural amino acids J. Am. Chem. Soc. 128 2006 15608 15617 (Pubitemid 44894099)
62. C. Dennison The role of ligand-containing loops at copper sites in proteins Nat. Prod. Rep. 25 2008 15 24 (Pubitemid 351207545)
63. D.G.T. Hai Lin QM/MM: what have we learned, where are we, and where do we go from here? Theor. Chem. Acc. 117 2007 185 199
64. C.O. Fernandez, J.A. Cricco, C.E. Slutter, J.H. Richards, H.B. Gray, and A.J. Vila Axial ligand modulation of the electronic structures of binuclear copper sites: analysis of paramagnetic 1H NMR spectra of Met160Gln Cu(A) J. Am. Chem. Soc. 123 2001 11678 11685 (Pubitemid 33121789)