Spectroscopic investigation of stellacyanin mutants: Axial ligand interactions at the blue copper site

Journal of the American Chemical Society

Volumn 125, Issue 37, 2003, Pages 11314-11328

  George, Serena DeBeer ^a,b   Basumallick, Lipika ^a   Szilagyi, Robert K ^a   Randall, David W ^a   Hill, Michael G ^c   Nersissian, Aram M ^d   Valentine, Joan S ^d   Hedman, Britt ^a,b   Hodgson, Keith O ^a,b   Solomon, Edward I ^a  

^a STANFORD UNIVERSITY   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^c OCCIDENTAL COLLEGE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRONIC STRUCTURE; PARAMAGNETIC RESONANCE; SPECTROSCOPIC ANALYSIS;

STELLACYANIN MUTANTS;

COPPER;

CYANINE DYE; LIGAND; STELLACYANINE; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CHEMICAL BOND; CHEMICAL STRUCTURE; COVALENT BOND; ELECTRON SPIN RESONANCE; LIGAND BINDING; MOLECULAR INTERACTION; MUTANT; OXIDATION REDUCTION REACTION; SPECTROSCOPY; STRUCTURE ANALYSIS;

BINDING SITES; COPPER; CUCUMIS SATIVUS; LIGANDS; METALLOPROTEINS; MOLECULAR STRUCTURE; MUTATION; OXYGEN; PLANT PROTEINS; SPECTRUM ANALYSIS;

EID: 0041691318     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja035802j     Document Type: Article

References (100)

1. Gray, H. B.; Solomon, E. I. In Copper Proteins; Spiro, T. G., Ed.; Wiley: New York, 1981: pp 1-39.
2. Adman, E. T. Adv. Protein Chem. 1991, 42, 145-197.
3. Adman, E. T. In Topics in Molecular and Structural Biology: Metalloproteins; Harrisson, P., Ed.; Macmillan: New York, 1985; Vol. 1, pp 1-42.
4. Sykes, A. G. 1991. 107, 377-408.
5. Messerschmidt, A. Struct. Bonding 1998, 90, 37-68.
6. Randall, D. W.; Gamelin, D. R.; LaCroix, L. B.; Solomon, E. I. J. Biol. Inorg. Chem. 2000, 5, 16-29.
7. Nersissian, A. M.; Shipp, E. L. Adv. Protein Chem. 2002. 60, 271-340.
8. Penfield, K. W.; Gewirth, A. A.; Solomon. E. I. J. Am. Chem. Soc. 1985, 107, 4519-4529.
9. Solomon, E. I.; Baldwin, M. I.; Lowery, M. D. Chem. Rev. 1992, 92, 521-542.
10. Guckert, J. A.; Lowery, M. D.; Solomon, E. I. J. Am. Chem. Soc. 1995, 117, 2817-2844.
11. Shadle, S. E.; Penner-Hahn, J. E.; Schugar, H. J.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1993, 115, 767-776.
12. Lowery, M. D.; Guckert, J. A.; Gebhard, M. S.; Solomon E. I. J. Am. Chem. Soc. 1993, 115, 3012-3013.
13. LaCroix. L. B.; Shadle. S. E.; Wang. Y. N.; Averill, B. A.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1996, 118, 7755-7768.
14. LaCroix, L. B.; Randall, D. W.; Nersissian, A. M.; Hoitink, C. W. G.; Canters, G. W.; Valentine, J. S.; Solomon, E. I. J. Am. Chem. Soc. 1998, 120, 9621-9631.
15. Adman, E. T.; Godden, J. W.; Turley, S. J. Biol. Chem. 1995, 270, 27458-27474.
16. Guss, J. M.; Merritt, E. A.; Phizackerley, R. P.; Phizackericy, R. P.; freeman, h. c. J. Mol. Biol. 1996, 259, 686-705.
17. Hart, P. J.; Nersissian, A. M.; Herrmann, R. G.; Nalbandyan, R. M.; Valentine, J. S.; Eisenberg, D. Protein Sci. 1996, 5, 2175-2183.
18. Xu, F.; Shin, W.; Brown, S. H.; Wahleithner, J.; Sundaram, U. M.; Solomon, E. I. Biochim. Biophys. Acta 1996, 1292, 303-311.
19. Messerschmidt, A. In Multicopper Oxidases; Messerschmidt, A., Ed.; World Scientific: Singapore, 1997; pp 23-80.
20. Germann, U. A.; Müller, G.; Hunziker, P. E.; Lerch, K. J. Biol. Chem. 1988, 263, 885-896.
21. DeBeer, S.; Randall, D. W.; Nersissian, A. M.; Valentine, J. S.; Hedman, B.; Hodgson, K. O.; Solomon. E. I. J. Phys. Chem. B 2000, 104, 10814-10819.
22. Palmer, A. E.; Randall, D. W.; Xu, F.; Solomon, E. I. J. Am. Chem. Soc. 1999, 121, 7138-7149.
23. Pierloot, K.; DeKerpel, J. O. A.; Ryde, U.; Olsson, M. H. M.; Roos, B. O. J. Am. Chem. Soc. 1998, 120, 13156-13166.
24. Ryde, U.; Olsson, M. H. M. Int. Z Quantum Chem. 2001, 81, 335-347.
25. Nersissian, A. M.; Mehrabian, Z. B.; Nalbandyan, R. M.; Hart, P. J.; Fraczkiewicz, G.; Czernuszewicz, R. S.; Bender, C. J.; Peisach, J.; Herrmann R. G.; Valentine, J. S. Protein Sci. 1996, 5, 2184-2192.
26. Nersissian, A. M.; Immoos, C.; Hill, M. G.; Hart, P. J.; Williams, G.; Herrmann, R. G.; Valentine, J. S. Protein Sci. 1998, 7, 1915-1929.
27. Karlsson, B. G.; Pascher, T.; Nordling, M.; Arvidsson, R. H. A.; Lundberg, L. G. FEBS Lett. 1989, 246, 211-217.
28. Hedman, B.; Frank, P.; Gheller, S. F.; Roe. A. L.; Newton, W. E.; Hodgson, K. O. J. Am. Chem. Soc. 1988, 110, 3798-3805.
29. Lytle, F. W.; Greegor, R. B.; Sandstrom, D. R.; Marques, E. C.; Wong, J. ; Spiro, C. L.; Huffman, G. P.; Huggins, F. E. Nucl. Instrum. Method. 1984, 226, 542-548.
30. Stern, E. A.; Heald, S. M. Rev. Sci. Instrum. 1979, 50, 1579-1582.
31. It should be noted that all samples were run both before and after the addition of excess oxidant. For all samples, the S K-edge data remained very similar, except for an increase in the pre-edge intensity of Q99L stellacyanin, consistent with the presence of some reduced copper. Similarly, the overall Cu K-edge shape remained very similar after addition of oxidant. except for the decreased intensity of a feature at ∼8983 eV in Q99L corresponding to the presence of some reduced copper. EPR spectra before and after the addition of oxidant gave equivalent parameters.
32. George, G. N. EDG_FIT; Stanford Synchrotron Radiation Laboratory, Stanford Linear Accelerator Center. Stanford University, Stanford, CA 94309.
33. DeWitt, J. G.; Bentsen, J. G.; Rosenzweig, A. C.; Hedman, B.; Green, J.; Pilkington, S.; Papaefthymiou, G. C.; Dalton, H.; Hodgson, K. O.; Lippard, S. J. J. Am. Chem. Soc. 1991, 113, 9219-9235.
34. Kau, L.-S.; Spira-Solomon, D. J.; Penner-Hah, J. E.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1987, 109, 6433-6442.
35. Rehr, J. J.; Mustre de Leon, J.; Zabinsky, S. I.; Albers, R. C. J. Am. Chem. Soc. 1991, 113, 5135-5140.
36. Mustre de Leon, J.; Rehr, J. J.; Zabinsky, S. I.; Albers, R. C. Phys. Rev. B 1991, 44, 4146-4156.
37. George, G. N. EXAFSPAK; Stanford Synchrotron Radiation Laboratory, Stanford Linear Accelerator Center, Stanford University, Stanford, CA 94309.
38. Allendorf, M. D.; Spira, D. J.; Solomon, E. I. Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 3063-3067.
39. Browett, W. R.; Fucaloro, A. F.; Morgan, T. V.; Stephens, P. J. J. Am. Chem. Soc. 1983, 105. 1868-1872.
40. Carithers, R. P.; Palmer, G. J. J. Biol. Chem. 1981, 256, 7967-7976.
41. Felsenfeld, G. Arch. Biochem. Biophys. 1960, 87, 247-251.
42. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Zakrzewski, V. G.; Montgomery, J. A. J.; Stratmann, R. E. ; Burant, J. C.; Dapprich, S.; Millam, J. M.; Daniels, A. D.; Kudin, K. N.; Strain, M. C.; Farkas, O.; Tomasi, J.; Barone, V.; Cossi, M.; Cammi, R.; Mennucci, B.; Pomelli, C.; Adamo, C.; Clifford, S.; Ochterski, J.; Petersson, G. A.; Ayala, P. Y.; Cui, Q.; Morokuma, K.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Cioslowski, J.; Ortiz, J. V.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Gomperts, R.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Gonzalez, C.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Andres, J. L.; Head-Gordon, M.; Replogle, E. S.; Pople, J. A. Gaussian 98, revision A.ll; Gaussian, Inc.: Pittsburgh, PA, 1998.
43. Becke, A. D. Phys. Rev. A: Gen. Phys. 1988, 38, 3098-3100.
44. Perdew, J. P. Phys. Rev. B: Condens. Mater. 1986, 33, 8822-8824.
45. Vosko, S. H.; Wilk, L.; Nusair, M. Can. J. Phys. 1980, 58, 1200-1211.
46. Schaefer, A.; Horn, H.; Ahlrichs, R. J. Chem. Phys. 1992, 97, 2571-2577.
47. (a) Hariharan, P. C.; Pople, J. A. Theor. Chim. Acta 1973, 28, 213-222.
48. (b) Francl, M. M.; Pietro, W. J.; Hehre, W. J.; Binkley, J. S.; Gordon, M. S.; DeFrees, D. J.; Pople, J. A. J. Chem. Phys. 1982, 77, 3654-3665.
49. (c) Rassolov, V. A.; Pople, J. A.; Ratner, M. A.; Windus, T. L. J. Chem. Phys. 1998, 109, 1223-1229.
50. (a) Siegbahn, P. E. M.; Blomberg, M. R. A. Chem. Rev. 2000, 100, 421-437.
51. (b) Ryde, U.; Olsson, M. H. M.; Pierloot, K. Theor. Comput. Chem. 2001, 9, 1-55.
52. (c) Szilagyi, R. K.; Metz, M.; Solomon, E. I. J. Phys. Chem. A 2002, 106, 2994-3007.
53. (a) Foster, J. P.; Weinhold, F. J. Am. Chem. Soc. 1980, 102, 7211-7218.
54. (b) Reed, A. E.; Curtiss, L. A.; Weinhold, F. Chem. Rev. 1988, 88, 899-926.
55. (c) Carpenter, J. E.; Weinhold, F. J. Mol. Struct. (THEOCHEM) 1988, 169, 41-62.
56. (a) Csaszar, P.; Pulay, P. J. Mol. Struct. (THEOCHEM) 1984, 114, 31-34.
57. (b) Farkas, O.; Schlegel, H. B. J. Chem. Phys. 1998, 109, 7100-7104.
58. (c) Farkas, O.; Schlegel H. B. J. Chem. Phys. 1999, 111, 10806-10814.
59. There are 6 sulfurs (3 Met and 3 Cys) in WT stellacyanin, 7 sulfurs (4 Met and 3 Cys) in the Q99M mutant, 6 sulfurs (3 Met and 3 Cys) in the Q99L mutant, and 9 sulfurs (3 Cys and 6 Met) in azurin. For all four proteins, all of the sulfurs will contribute to the edge, while only one Cys thiolate contributes to the pre-edge.
60. The shifts in rising edge background are attributed to both a different total number of sulfurs in the proteins and to differences in copper loading. Fits to the pre-edge region account for the differences in the rising edge background.
61. It should be noted that both Q99M stellacyanin and azurin have an apparent higher covalency value than plastocyanin.11 All Q99M stellacyanin and azurin samples were fully oxidized and spin quantitated to determine copper loading; thus. these data most likely reflect a more accurate covalency estimate for a classic blue copper site.
62. It should be noted that for azurin a distant (∼3 Å) Cu-O interaction to a backbone amide carbonyl, trans to the thioether, is sometime discussed, which is not present in the Q99M mutant. However. at this distance, little covalent bonding interaction is present between the Cu and the compact O 2p orbitals, ref 6.
63. Kosugi, N.; Yokoyama, T.; Asakura, K.; Kuroda, H. Chem. Phys. 1984. 91, 249-256.
64. Bair, R. A.; Goddard, W. A., III. Phys. Rev. B 1980, 22, 2767-2776.
65. On the basis of the EPR parameters, the additional tightly bound Cu(II) site is significantly less covalent than a TI copper site and thus should have a much less intense shakedown feature. Hence, it is likely that the shakedown feature for the Q99L TI site is even more intense than that of Q99M. This trend is consistent with S K-edge results. It should also be noted that the feature at ∼8983 eV in the Q99L Cu K-edge spectrum corresponds to the presence of a small amount of reduced copper.
66. The Cu K-edge data indicate a small amount of Cu(I) in oxidized Q99L stellacyanin. This would have only a small effect on the Cu-S distance of Q99L and would if anything make the Cu-S distance slightly longer.
67. Guss, J. M.; Bartunik, H. D.; Freeman, H. C. Acta Crystallogr. 1992, B48, 790-811.
68. Nar, H.; Messerschmidt, A.; Canters, G. W. J. Mol. Biol. 1991, 221, 765-772.
69. -1) for comparison to Q99L stellacyanin fits. Fits over the shorter data range did not change the Cu-S or Cu-N distances.
70. It should be noted that the presence of an additional tightty bound four-coordinate copper in Q99L stellacyanin would tend to decrease the intensity of the ∼8984 eV feature, and thus the intensity of this feature should be even greater.
71. Blair, D. F.; Campbell, G. W.; Schoonover, J. R.; Chan, S. I.; Gray, H. B.; Malmström, B. G.; Pecht, I.; Swanson, B. I.; Woodruff, W. H.; Cho, W. K.; English, A. M.; Fry, H. A.; Lum, V.; Norton, K. A. J. Am. Chem. Soc. 1985, 107, 5755-5766.
72. Han, J.; Adman, E. T.; Beppu, T.; Codd, R.; Freeman, H. C.; Huq, L.; Loehr, T. M.; Sanders-Loehr, J. Biochemistry 1991, 30, 10904-10913.
73. (a) Badger, R. M. J. Chem. Phys. 1934, 2, 128.
74. (b) Herschbach, D. R.; Laurie, V. W. J. Chem. Phys. 1961, 35, 458-463.
75. Piepho, S. B.; Schatz, P. N. In Group Theory in Spectroscopy - With Applications to Magnetic Circular Dichroism; Piepho, S. B., Schatz, P. N., Eds. ; John Wiley and Sons: New York, 1983.
76. Gerstman, B. S.; Brill, A. S. J. Chem. Phvs. 1985, 82, 1212-1230.
77. Gewirth, A. A.; Solomon, E. I. J. Am. Chem. Soc. 1988, 110, 3811-3819.
78. McGarvey, B. R. In Transition Metal Chemistry; Carlin, B. L., Ed.; M. Dekker: New York, 1966 pp 89-201.
79. Randall, D. W.; George, S. D.; Holland, P. L.; Hedman, B.; Hodgson, K. O.; Tolman, W. B.; Solomon, E. I. J. Am. Chem. Soc. 2000, 122, 11632-11648.
80. Marcus, R. A.; Sutin, N. Biochim. Biophys. Acta 1985, 811, 265-322.
81. Newton, M. D. Chem. Rev. 1991, 91, 767-792.
82. Beratan, D. N.; Betts, J. N.; Onuchic, J. N. Science 1991, 252, 1285-1288.
83. Beratan, D. N.; Hopfield, J. J. J. Am. Chem. Soc. 1984, 106, 6, 1584-1594.
84. Beratan, D. N.; Onuchic, J. N.; Hopfield, J. J. J. Chem. Phys. 1987, 86, 4488-4498.
85. Machonkin, T. E.; Solomon, E. I. J. Am. Chem. Soc. 2000, 122, 12547-12560.
86. George. S. D.; Metz, M.; Szilagyi, R. K.; Wang, H. X.; Cramer, S. P.; Lu, Y.; Tolman, W. B.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 2001, 123, 5757-5767.
87. Regan, J. J.; DiBilio, A. J.; Langen, R.; Skov, L. K.; Winkler, J. R.; Gray, H. B.; Onuchic, J. N. Chem. Biol. 1995, 2, 489-496.
88. Cu-S(reduced) is assumed to be the same for WT, Q99M, and Q99L stellacyanin.
89. (a) Fraga, E.; Webb, M. A.; Loppnow, G. R. J. Phys. Chem. 1996, 100, 3278-3287.
90. (b) Webb, M. A.; Kwong, C. M.; Loppnow, G. R. J. Phys. Chem. B 1997, 101, 5062-5069.
91. Nersissian, A. M.; Hart, J. P.; Valentine, J. S. In Handbook of Metalloproteins; Messerschmidt, A., Huber, R., Poulos, T., Wieghardt. K.. Eds.; John Wiley and Sons: Chichester, 2001; pp 1219-1234.
92. Campos-Vallette, M.; Figueroa, K.; LaTorre, R. O.; Diaz Fleming, G.; Costamagna, J.; Canales, J. C.; Rey-Lafon, M.; Derouault, J. Vib. Spectrosc. 1993, 6, 25-35.
93. Experimentally, the total reorganization energy for stellacyanin is 1.4 times greater than that of plastocyanin. However, this has been attributed to the more exposed nature of the site, which increases the outer sphere contribution to λ (Farver, O.; Pecht, I. Inorg. Chem. 1990, 29, 4855-4858).
94. Malmström, B. G.; Leckner, J. Curr. Opin. Chem. Biol. 1998, 2, 286-292.
95. Malmström, B. G.; Reinhammer, B.; Vänngård, T. I. Eur. J. Biochem. 1971, 18, 463-468.
96. Diederix, R. E.; Canters, G. W.; Dennison, C. Biochemistry 2000, 39, 9551-9560.
97. Ingeledew, W. J.; Cobley, J. G. Biochim. Biophys. Acta 1980, 590, 141-158.
98. Kennepohl, P.; Solomon, E. I. Inorg. Chem. 2003, 42, 689-695.
99. Rose, K.; Shadle, S. E.; Glaser, T.; de Vries, S.; Cherepanov, A.; Canters, G. W.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1999, 121, 2353-2363.
100. -1 in energy. The trigonally distorted tetrahedral structure is similar to the structures on the plateau of the constrained optimization (Figure 10, red line, steps 17-30) with nonequal Cu-N distances. Their tetragonal structure does not compare directly with any point of the optimization pathways discussed here, because the arrangement of the ligands are different.