Spectroscopic and electronic structure studies of the trinuclear Cu cluster active site of the multicopper oxidase laccase: Nature of its coordination unsaturation

Journal of the American Chemical Society

Volumn 127, Issue 40, 2005, Pages 13832-13845

  Quintanar, Liliana ^a   Yoon, Jungjoo ^a   Aznar, Constantino P ^b   Palmer, Amy E ^a   Andersson, K Kristoffer ^c   Britt, R David ^b   Solomon, Edward I ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER COMPOUNDS; CRYSTALLOGRAPHY; DISCRETE FOURIER TRANSFORMS; ELECTRONIC STRUCTURE; HYDROGEN; HYDROGEN BONDS; PH EFFECTS; POSITIVE IONS; PROTEINS; SPECTROSCOPIC ANALYSIS;

MULTICOPPER OXIDASE LACCASE; NEGATIVE PROTEIN POCKETS; TRINUCLEAR CUPRIC CLUSTERS; UNSATURATION;

ENZYMES;

COPPER; LACCASE;

ANALYTIC METHOD; ARTICLE; CHEMICAL STRUCTURE; CLUSTER ANALYSIS; CRYSTALLOGRAPHY; HYDROGEN BOND; LIGAND BINDING; SPECTROSCOPY; STRUCTURE ANALYSIS;

COPPER; DEUTERIUM; ELECTRON SPIN RESONANCE SPECTROSCOPY; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; LACCASE; LIGANDS; MODELS, CHEMICAL; MODELS, MOLECULAR; NITROGEN; ORGANOMETALLIC COMPOUNDS; PROTEIN CONFORMATION; REFERENCE STANDARDS; THERMODYNAMICS;

EID: 26444463761     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja0421405     Document Type: Article

References (77)

1. Solomon, E. I.; Sundaram, U. M.; Machonkin, T. E. Chem. Rev. 1996, 96, 2563-2605.
2. Morie-Bebel, M. M.; Morris, M. C.; Menzie, J. L.; McMillin, D. R. J. Am. Chem. Soc. 1984, 106, 3677-3678.
3. Allendorf, M. D.; Spira, D. J.; Solomon, E. I. Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 3063.
4. Spira-Solomon, D. J.; Allendorf, M. D.; Solomon, E. I. J. Am. Chem. Soc. 1986, 108, 5318.
5. Cole, J. L.; Tan, G. O.; Yang, E. K.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1990, 112, 2243-2249.
6. Messerschmidt, A.; Ladenstein, R.; Huber, R.; Bolognesi, M.; Avigliano, L.; Petruzzelli, R.; Rossi, A.; Finazzi-Agro, A. J. Mol. Biol. 1992, 224, 179-205.
7. Zaitseva, I.; Zaitsev, V.; Card, G.; Moshov, 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. Roberts, S.; Weichsel, A.; Grass, G.; Thakali, K.; Hazzard, J.; Tollin, G.; Rensing, C.; Montfort, W. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 2766-2771.
11. Hakulinen, N.; Kiiskinen, L.; Kruus, K.; Saloheimo, M.; Paananen, A.; Koivula, A.; Rouvinen, J. Nat. Struct. Biol. 2002, 9, 601-605.
12. Enguita, F.; Martins, L.; Henriques, A.; Carrondo, M. J. Biol. Chem. 2003, 278, 19416-19425.
13. Morie-Bebel, M. M.; McMillin, D. R.; Antholine, W. E. Biochem. J. 1986, 235, 415-420.
14. Fraterrigo, T. L.; Miller, C.; Reinhammar, B.; McMillin, D. R. J. Biol. Inorg. Chem. 1999, 4, 183-187.
15. Li, J.; McMillin, D. R.; Antholine, W. E. J. Am. Chem. Soc. 1992, 114, 725-727.
16. Bonomo, R. P.; Castronovo, B. M. G.; Santoro, A. M. Dalton Trans. 2004, 1, 104-112.
17. Cole, J. L.; Clark, P. A.; Solomon, E. I. J. Am. Chem. Soc. 1990, 112, 9534-9548.
18. Sundaram, U. M.; Zhang, H. H.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1997, 119, 12525-12540.
19. Messerschmidt, A.; Luecke, H.; Huber, R. J. Mol. Biol. 1993, 230, 997-1014.
20. Zaitsev, V. N.; Zaitseva, I.; Papiz, M.; Lindley, P. F. J. Biol. Inorg. Chem. 1999, 4, 579-587.
21. Brändén, R.; Malmstrom, B. G.; Vänngard, T. Eur. J. Biochem. 1973, 36, 195-200.
22. Reinhammar, B. Biochim. Biophys. Acta 1970, 205, 35-47.
23. Reinhammar, B. R. M. Biochim. Biophys. Acta 1972, 275, 245-259.
24. Morie-Bebel, M. M.; Menzie, J. L.; McMillin, D. R. In Conference on Copper Coordination Chemistry: Karlin, K. D., Zubieta, J., Eds.; Adenine Press: Guilderland, NY, 1984; Vol. 1, pp 89 ff.
25. Severns, J. C.; McMillin, D. R. Biochemistry 1990, 29, 8592-8597.
26. Felsenfeld, G. Arch. Biochem. Biophys. 1960, 87, 247-251.
27. Carithers, R. P.; Palmer, G. J. Biol. Chem. 1981, 256, 7967-7976.
28. Sturgeon, B. E.; Britt, R. D. Rev. Sci. Instrum. 1992, 63, 2186-2192.
29. Mims, W. B. J. Magn. Reson. 1984, 59, 291-306.
30. Mims, W. B. Proc. R. Soc. London 1965, 283, 452.
31. Davies, E. R. Phys. Lett. 1974, 47A, 1-2.
32. Frisch, M. J.; et al. Gaussian 98, revision A.11.3: Gaussian, Inc.: Pittsburgh, PA, 1998.
33. Schaftenaar, G.; Noordik, J. H. J. Comput. Aided Mol. Des. 2000, 14, 123-124.
34. Gorelsky, S. I. AOMix program, revision 5.83; http://www.sg-chem.net/.
35. Gorelsky, S. I.; Lever, A. B. P. J. Organomet. Chem. 2001, 635, 187-196.
36. Noodleman, L. J. Chem. Phys. 1981, 74, 5737-5743.
37. Tuczek, F.; Solomon, E. I. J. Am. Chem. Soc. 1994, 116, 6916-6924.
38. Becke, A. D. J. Chem. Phys. 1993, 98, 5648-5652.
39. Dunning, T. H. J.; Hay, P. J. In Modern Theoretical Chemistry; Schaefer, H. F., III, Ed.; Plenum: New York, 1976; Vol. 3, p 1.
40. Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 270-283.
41. Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 299-310.
42. Wadt, W. R.; Hay, P. J. J. Chem. Phys. 1985, 82, 284-298.
43. Szilagyi, R. K.; Metz, M.; Solomon, E. I. J. Phys. Chem. A 2002, 106, 2994-3007.
44. Schäfer, A.; Horn, H.; Ahlrichs, R. J. Chem. Phys. 1992, 97, 2571-2577.
45. McGarvey, B. R. In Transition Metal Chemistry; Carlin, B. L., Ed.; Marcel Dekker: New York, 1966; Vol. 3, pp 89-201.
46. Gewirth, A. A.; Cohen, S. L.; Schugar, H. J.; Solomon, E. I. Inorg. Chem. 1987, 26, 1133-1146.
47. Doan, P. E.; Fan, C.; Davoust, C. E.; Hoffman, B. M. J. Magn. Reson. 1991, 95, 196-200.
48. van Camp, H. L.; Sands, R. H.; Fee, J. A. J. Chem. Phys. 1981, 75, 2098-2107.
49. Roberts, J. E.; Cline, J. F.; Lum, V.; Freeman, H.; Gray, H. B.; Peisach, J.; Reinhammar, B.; Hoffman, B. M. J. Am. Chem. Soc. 1984, 106, 5324-5330.
50. Werst, M. M.; Davoust, C. E.; Hoffman, B. M. J. Am. Chem. Soc. 1991, 113, 1533-1538.
51. Goodman, B. A.; Raynor, J. B. Adv. Inorg. Chem. Radiochem. 1970, 13, 135-362.
52. Weil, J. A.; Bolton, J. R.; Wertz, J. E. Electron Paramagnetic Resonance: Elementary Theory and Practical Applications; Wiley-Interscience: New York, 1994.
53. Mims, W. B.; Peisach, J. J. Chem. Phys. 1978, 69, 4921-4930.
54. Lu, J.; Bender, C. J.; McCracken, J.; Peisach, J.; Severns, J. C.; McMillin, D. R. Biochemistry 1992, 31, 6265-6272.
55. To fully describe the number of protons and their hyperfine coupling parameters, data acquisition at g parallel with smaller τ is required.
56. Deinum, J. S.; Vanngard, T. FEBS Lett. 1975, 58, 62-65.
57. Bernanducci, E. E.; Schwindinger, W. F.; Hughey, J. L.; Krogh-Jespersen, K.; Schugar, H. J. J. Am. Chem. Soc. 1981, 103, 1686-1691.
58. Fawcett, T. G.; Bernanducci, E. E.; Krogh-Jespersen, K.; Schugar, H. J. J. Am. Chem. Soc. 1980, 102, 2598-2604.
59. Gamelin, D. R.; Randall, D. W.; Hay, M. T.; Houser, R. P.; Mulder, T. C.; Canters, G. W.; de Vries, S.; Tolman, W. B.; Lu, Y.; Solomon, E. I. J. Am. Chem. Soc. 1998, 120, 5246-5263.
60. 61
61. Chen, P.; Fujisawa, K.; Solomon, E. I. J. Am. Chem. Soc. 2000, 122, 10177-10193.
62. It should be noted that this pH effect is independent of the buffer used; MES, potassium phosphate, and potassium phthalate buffers yield similar results.
63. Sillen, L. G.; Martell, A. E. Stabilin Constants of Metal-Ion Complexes; The Chemical Society: London, 1974.
64. Groves, J. T.; Chambers, J. R. R. J. Am. Chem. Soc. 1984, 106, 630-638.
65. Groves, J. T.; Olson, J. R. Inorg. Chem. 1985, 24, 2715-2717.
66. Nitta, K.; Kataoka, K.; Sakurai, T. J. Inorg. Biochem. 2002, 91, 125-131.
67. Randall, D. W.: DeBeer-George, S.; Hedman, B.; Hodgson, K. O.; Fujisawa, K.; Solomon, E. I. J. Am. Chem. Soc. 2000, 122, 11620-11631.
68. Experimental results are best matched by B38HFP86/VTZ*+6- 31G*. Other methods, such as B3LYP, gave much more covalent descriptions of the Cu-O bond in T2, with Cu characters <50%.
69. Charges on the atoms in the T2T3 site were taken from either Mulliken population analysis or natural population analysis (NPA) in the DFT calculations, and the four Asp/Glu residues were treated as point -1e charges (ε = 5).
70. Eisenstadt, M.; Friedman, H. L. J. Chem. Phys. 1968, 48, 4445-4458.
71. Winkler, M. E.; Spira, D. J.; LuBien, C. D.; Thamann, T. J.; Solomon, E. I. Biochem. Biophys. Rex. Commun. 1982, 107, 727-734.
72. 3 substituted for the histidine ligands.
73. -).
74. 75
75. Quintanar, L.; Stoj, C.; Wang, T.-P.; Kosman, D. J.; Solomon, E. I. Biochemistry 2005, 44, 6081-6091.
76. (a) 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.
77. (b) Yoon, J.; Mirica, L. M.; Stack, T. D. P.; Solomon, E. I. J. Am. Chem. Soc. 2005, in press.