Electronic structure of the peroxy intermediate and its correlation to the native intermediate in the multicopper oxidases: Insights into the reductive cleavage of the O-O bond

Journal of the American Chemical Society

Volumn 129, Issue 43, 2007, Pages 13127-13136

  Yoon, Jungjoo ^a   Solomon, Edward I ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MULTICOPPER OXIDASES; PEROXIDE BRIDGES; PEROXY INTERMEDIATE; REDUCTIVE CLEAVAGE;

CHARGE TRANSFER; COPPER OXIDES; DENSITY FUNCTIONAL THEORY; DIAMAGNETIC MATERIALS; GROUND STATE; MOLECULAR ORBITALS; POTENTIAL ENERGY; SPECTROSCOPIC ANALYSIS;

ELECTRONIC STRUCTURE;

COPPER DERIVATIVE; COPPER OXIDASE; OXYGEN; PEROXY RADICAL; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHEMICAL BINDING; CHEMICAL STRUCTURE; DENSITY FUNCTIONAL THEORY; ELECTRON TRANSPORT; MOLECULAR DYNAMICS; MOLECULAR STABILITY; OXIDATION; REDUCTION; THERMODYNAMICS;

CERULOPLASMIN; COMPUTER SIMULATION; ELECTRONS; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXYGEN; PEROXIDES; PROTEIN STRUCTURE, TERTIARY; PROTONS;

EID: 35848965478     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja073947a     Document Type: Article

References (68)

1. Solomon, E. I.; Chen, P.; Metz, M.; Lee, S. K.; Palmer, A. E. Angew. Chem., Int. Ed. 2001, 40, 4570-4590.
2. Solomon, E. I.; Sundaram, U. M.; Machonkin, T. E. Chem. Rev. 1996, 96, 2563-2605.
3. Cole, J. L.; Tan, G. O.; Yang, E. K.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1990, 112, 2243-2249.
4. Spira-Solomon, D. J.; Allendorf, M. D.; Solomon, E. I. J. Am. Chem. Soc. 1986, 108, 5318-5328.
5. Messerschmidt, A.; Ladenstein, R.; Huber, R.; Bolognesi, M.; Avigliano, L.; Petruzzelli, R.; Rossi, A.; Finazzi-Agró, A. J. Mol. Biol. 1992, 224, 179-205.
6. Ducros, V.; Brzozowski, A. M.; Wilson, K. S.; Brown, S. H.; Østergaard, P.; Schneider, P.; Yaver, D. S.; Pedersen, A. H.; Davies, G. J. Nat. Struct. Biol. 1998, 5, 310-316.
7. Zaitseva, I.; Zaitsev, V.; Card, G.; Moshkov, K.; Bax, B.; Ralph, A.; Lindley, P. J. Biol. Inorg. Chem. 1996, 1, 15-23.
8. Bertrand, T.; Jolivalt, C.; Briozzo, P.; Caminade, E.; Joly, N.; Madzak, C.; Mougin, C. Biochemistry 2002, 41, 7325-7333.
9. Piontek, K.; Antorini, M.; Choinowski, T. J. Biol. Chem. 2002, 277, 37663-37669.
10. Hakulinen, N.; Kiiskinen, L. L.; Kraus, K.; Saloheimo, M.; Paananen, A.; Koivula, A.; Rouvinen, J. Nat. Struct. Biol. 2002, 9, 601-605.
11. Roberts, S. A.; Weichsel, A.; Grass, G.; Thakali, K.; Hazzard, J. T.; Tollin, G.; Rensing, C.; Montfort, W. R. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 2766-2771.
12. Enguita, F. J.; Marcal, D.; Martins, L. O.; Grenha, R.; Henriques, A. O.; Lindley, P. F.; Carrondo, M. A. J. Biol. Chem. 2004, 279, 23472-23476.
13. Smith, A. W.; Camara-Artigas, A.; Wang, M. T.; Allen, J. P.; Francisco, W. A. Biochemistry 2006, 45, 4378-4387.
14. Taylor, A. B.; Stoj, C. S.; Ziegler, L.; Kosman, D. J.; Hart, P. J. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 15459-15464.
15. Garavaglia, S.; Cambria, M. T.; Miglio, M.; Ragusa, S.; Iacobazzi, V.; Palmieri, F.; D'Ambrosio, C.; Scaloni, A.; Rizzi, M. J. Mol. Biol. 2004, 342, 1519-1531.
16. Messerschmidt, A.; Luecke, H.; Huber, R. J. Mol. Biol. 1993, 230, 997-1014.
17. Bento, I.; Martins, L. O.; Lopes, G. G.; Carrondo, M. A.; Lindley, P. F. Dalton Trans. 2005, 3507-3513.
18. Lee, S. K.; George, S. D.; Antholine, W. E.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 2002, 124, 6180-6193.
19. Brändén, R.; Deinum, J. Biochim. Biophys. Acta 1978, 524, 297-304.
20. Aasa, R.; Brändén, R.; Deinum, J.; Malmström, B. G.; Reinhammar, B.; Vänngård, T. FEBS Lett. 1976, 61, 115-119.
21. Manabe, T.; Manabe, N.; Hiromi, K.; Hatano, H. FEBS Lett. 1972, 23, 268-270.
22. Machonkin, T. E.; Solomon, E. I. J. Am. Chem. Soc. 2000, 122, 12547-12560.
23. Palmer, A. E.; Lee, S. K.; Solomon, E. I. J. Am. Chem. Soc. 2001, 123, 6591-6599.
24. Yoon, J.; Mirica, L. M.; Stack, T. D. P.; Solomon, E. I. J. Am. Chem. Soc. 2004, 126, 12586-12595.
25. Yoon, J.; Mirica, L. M.; Stack, T. D. P.; Solomon, E. I. J. Am. Chem. Soc. 2005, 127, 13680-13693.
26. Yoon, J.; Solomon, E. I. Inorg. Chem. 2005, 44, 8076-8086.
27. Yoon, J.; Solomon, E. I. Coord. Chem. Rev. 2007, 251, 379-400.
28. Yoon, J.; Liboiron, B. D.; Sarangi, R.; Hodgson, K. O.; Hedman, B.; Solomon, E. I. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 13609-13614.
29. Rulíšek, L.; Solomon, E. I.; Ryde, U. Inorg. Chem. 2005, 44, 5612-5628.
30. Morie-Bebel, M. M.; Morris, M. C.; Menzie, J. L.; McMillin, D. R. J. Am. Chem. Soc. 1984, 106, 3677-3678.
31. Shin, W.; Sundaram, U. M.; Cole, J. L.; Zhang, H. H.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1996, 118, 3202-3215.
32. Hassett, R. F.; Yuan, D. S.; Kosman, D. J. J. Biol. Chem. 1998, 273, 23274-23282.
33. Blackburn, N. J.; Ralle, M.; Hassett, R.; Kosman, D. J. Biochemistry 2000, 39, 2316-2324.
34. Palmer, A. E.; Quintanar, L.; Severance, S.; Wang T. P.; Kosman, D. J.; Solomon, E. I. Biochemistry 2002, 41, 6438-6448.
35. Quintanar, L.; Stoj, C.; Wang, T. P.; Kosman, D. J.; Solomon, E. J. Biochemistry 2005, 44, 6081-6091.
36. Cole, J. L.; Ballou, D. P.; Solomon, E. I. J. Am. Chem. Soc. 1991, 113, 8544-8546.
37. Augustine, A. J.; Quintanar, L.; Stoj, C. S.; Kosman, D. J.; Solomon, E. I. J. Am. Chem. Soc. 2007, 129, 13118-13126.
38. Magnus, K. A.; Hazes, B.; Tonthat, H.; Bonaventura, C.; Bonaventura, J.; Hol, W. G. J. Proteins 1994, 19, 302-309.
39. Matoba, Y.; Kumagai, T.; Yamamoto, A.; Yoshitsu, H.; Sugiyama, M. J. Biol. Chem. 2006, 281, 8981-8990.
40. Cuff, M. E.; Miller, K. I.; van Holde, K. E.; Hendrickson, W. A. J. Mol. Biol. 1998, 278, 855-870.
41. Sundaram, U. M.; Zhang, H. H.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1997, 119, 12525-12540.
42. Frisch, M. J.; et al. Gaussian 03, revision C.01; Gaussian, Inc.: Pittsburgh, PA, 2004.
43. Noodleman, L. J. Chem. Phys. 1981, 74, 5737-5743.
44. Becke, A. D. J. Chem. Phys. 1993, 98, 5648-5652.
45. Tenderholt, A. PyMOlyze, ver. 1.5; Stanford University: Stanford, CA, 2006.
46. Chalupský, J.; Neese, F.; Solomon, E. I.; Ryde, U.; Rulíšek, L. Inorg. Chem. 2006, 45, 11051-11059.
47. 2--bridged PI structure was performed with a larger basis set, with triple-ζ 6-311G* on Cu and coordinated N/O atoms and 6-31G* on the rest, to verify that the structures obtained in this study with the double-ζ quality basis set, with 6-31G* on Cu and coordinated N/O atoms and 3-21G* on the rest, are sound. As a result, it is found that the overall structure of PI remains the same and the geometric parameters are very similar to those obtained with the double-ζ basis set, as indicated in Table 1.
48. Mirica, L. M.; Ottenwaelder, X.; Stack, T. D. P. Chem. Rev. 2004, 104, 1013-1045.
49. These energies are based on calculations using B3LYP functional with 6-3IG* basis set on Cu and coordinated N/O atoms and 3-21G* basis set on the rest.
50. Eickman, N. C.; Himmelwright, R. S.; Solomon, E. I. Proc. Natl. Acad. Sci. U.S.A. 1979, 76, 2094-2098.
51. Quintanar, L.; Yoon, J.; Aznar, C. P.; Palmer, A. E.; Andersson, K. K.; Britt, R. D.; Solomon, E. I. J. Am. Chem. Soc. 2005, 127, 13832-13845.
52. Lubien, C. D.; Winkler, M. E.; Thamann, T. J.; Scott, R. A.; Co, M. S.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1981, 103, 7014-7016.
53. Penner-Hahn, J. E.; Hedman, B.; Hodgson, K. O.; Spira, D. J.; Solomon, E. I. Biochem. Biophys. Res. Commun. 1984, 119, 567-574.
54. Spira-Solomon, D. J.; Solomon, E. I. J. Am. Chem. Soc. 1987, 109, 6421-6432.
55. -1).
56. -1) quenches the fluorescence in this region, allowing the resonance Raman spectrum to be obtained.
57. Unpublished results.
58. To compare the energy difference between the direct proton transfer from a proton donor to a proton acceptor and the indirect proton transfer via a water molecule, we have modeled the proton-transfer process between a formate ion and a formic acid at the B3LYP/6-31++G** level. As a result, energy barriers for the proton-transfer process directly between a formate and a formic acid and that mediated by a water molecule were estimated with relatively similar values of ∼7.9 and ∼12.0 kcal/mol, respectively. (The distance between O atoms accepting and donating the proton was fixed at 2.80 Å. See Figures S2, S3 and figure legends for details of the calculations.)
59. 28 Thus, while the |βαα) spin configuration contributes significantly in me early stage of O-O bond cleavage (which includes the transition state, vide infra), the other two spin configurations become equally important as all three Cu centers in the trinuclear cluster become oxidized.
60. As indicated in footnote 58, the energy barrier in the proton-transfer process is estimated to be higher when it is mediated by a water molecule. However, the relative stability of PI+e+H, compared to that of PI+e, can provide enough thermodynamic driving force to make the energy barrier in the proton-transfer process still small relative to the overall transition-state energy.
61. Hazes, B.; Magnus, K. A.; Bonaventura, C.; Bonaventura, J.; Dauter, Z.; Kalk, K. H.; Hol, W. G. J. Protein Sci. 1993, 2, 597-619.
62. Sawyer, D. T. Oxygen Chemistry; Oxford University Press: New York, 1991.
63. Aasa, R.; Brändén, R.; Deinum, J.; Malmström, B. G.; Reinhammar, B.; Vänngård, T. Biochem. Biophys. Res. Commun. 1976, 70, 1204-1209.
64. Andréasson, L. E.; Brändén, R.; Reinhammar, B. Biochim. Biophys. Acta 1976, 438, 370-379.
65. Huang, H.-W.; Zoppellaro, G.; Sakurai, T. J. Biol. Chem. 1999, 274, 32718-32724.
66. Blomberg, M. R. A.; Siegbahn, P. E. M. Biochim. Biophys. Acta 2006, 1757, 969-980.
67. Blomberg, M. R. A.; Siegbahn, P. E. M. J. Comput. Chem. 2006, 27, 1373-1384.
68. Blomberg, M. R. A.; Siegbahn, P. E. M.; Wikstrom, M. Inorg. Chem. 2003, 42, 5231-5243.