Determination of the magnetic axes of cobalt(II) and nickel(II) azurins from 1H NMR data: Influence of the metal and axial ligands on the origin of magnetic anisotropy in blue copper proteins

Biochemistry

Volumn 37, Issue 24, 1998, Pages 8659-8673

  Donaire, Antonio ^a   Salgado, Jesús ^b   Moratal, José María ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AZURIN;

ARTICLE; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; LIGAND BINDING; MAGNETISM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; STRUCTURE ACTIVITY RELATION;

ANISOTROPY; AZURIN; COBALT; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; NICKEL; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 0032537548     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi971974f     Document Type: Article

References (112)

1. Holm, R. H., Kennepohl, P., and Solomon, E. I. (1996) Chem. Rev. 96, 2239-2314.
2. Gray, H. B., and Winkler, J. R. (1996) Annu. Rev. Biochem. 65, 537-561.
3. Solomon, E. I., Penfield, K. W., Geweirth, A. A., Lowery, M. D., Shadle, S. E., Guckert, G. A., and LaCroix, L. B. (1996) Inorg. Chim. Acta 243, 67-78.
4. Solomon, E. I., Baldwin, M. J., and Lowery, M. D. (1992) Chem. Rev. 92, 521-542.
5. Sykes, A. G. (1991) in Advances in Inorganic Chemistry (Sykes, A. G., Ed.) pp 377-408, Academic Press, New York.
6. Williams, G., Moore, G. R., Porteous, R., Robinson, M. N., Soffe, N., and Williams, R. J. P. (1985) J. Mol. Biol. 183, 409-428.
7. Williams, G., Moore, G. R., and Williams, R. J. P. (1985) Comments Inorg. Chem. 4, 55-98.
8. Scheek, R. M., van Gunsteren, W. F., and Kaptein, R. (1989) Methods Enzymol. 177, 204-218.
9. Detlefsen, D. J., Thanabal, V., Pecoraro, V. L., and Wagner, G. (1991) Biochemistry 30, 9040-9046.
10. La Mar, G. N. and de Ropp, J. S. (1993) in Biological Magnetic Resonance (Berliner, L. J., and Reuben, J., Eds.) Vol. 12, pp 1-78, Plenum Press, New York.
11. Bertini, I., Turano, P., and Vila, A. J. (1993) Chem. Rev. 93, 2833-2932.
12. La Mar, G. N. (1995) in NMR of Paramagnetic Macromolecules (La Mar, G. N., Ed.) NATO ASI Series, Dordrecht, The Netherlands.
13. Bertini, I., and Luchinat, C. (1996) NMR of paramagnetic substances, in Coordination Chemistry Reviews (Lever, A. B. P., Ed.) Vol. 150, Elsevier, Amsterdam.
14. Turner, D. L., Salgueiro, C. A., Schenkels, P., LeGall, J., and Xavier, A. V. (1995) Biochim. Biophys. Acta 1246, 24-28.
15. Coutinho, I., and Xavier, A. V. (1994) Methods Enzymol. 243, 119-140.
16. Palma, P. N., Moura, I., LeGall, J., van Beeumen, J., Wampler, J. E., and Moura, J. J. G. (1994) Biochemistry 33, 6394-6407.
17. Clark, K., Dugad, L. B., Bartsch, R. G., Cusanovich, M. A., and La Mar, G. N. (1996) J. Am. Chem. Soc. 118, 4654-4664.
18. Chen, Z. G., de Ropp, J. S., Hernandez, G., and La Mar, G. N. (1994) J. Am. Chem. Soc. 116, 8772-8783.
19. Turner, D. L. (1995) Eur. J. Biochem. 227, 829-837.
20. Banci, L., Bertini, I., Marconi, S., Pierattelli, R., and Sligar, S. G. (1994) J. Am. Chem. Soc. 116, 4866-4873.
21. Banci, L., Bertini, I., Bruschi, M., Sompornpisut, P., and Turano, P. (1996) Proc. Natl. Acad. Sci. U.S.A. 93, 14396-14400.
22. Calzolai, L., Gorst, C. M., Zhao, Z. H., Teng, Q., Adams, M. W. W., and La Mar, G. N. (1995) Biochemistry 34, 11373-11384.
23. Gorst, C. M., Yeh, Y.-H., Teng, Q., Calzolai, L., Zhou, Z.-H., Adams, M. W. W., and La Mar, G. N. (1995) Biochemistry 34, 600-610.
24. Donaire, A., Gorst, C. M., Zhou, Z. H., Adams, M. W. W., and La Mar, G. N. (1994) J. Am. Chem. Soc. 116, 6841-6849.
25. Aono, S., Bertini, I., Cowan, J. A., Luchinat, C., Rosato, A., and Viezzoli, M. S. (1996) J. Biol. Inorg. Chem. 1, 523-528.
26. Bertini, I., Dikiy, A., Luchinat, C., Macinai, R., Viezzoli, M. S., and Vincenzini, M. (1997) Biochemistry 36, 3570-3579.
27. Bertini, I., Capozzi, F., Luchinat, C., Piccioli, M., and Vila, A. J. (1994) J. Am. Chem. Soc. 116, 651-660.
28. Bertini, I., Donaire, A., Felli, I. C., Luchinat, C., and Rosato, A. (1997) Inorg. Chem. 36, 4798-4803.
29. Bertini, I., Bren, K. L., Clemente, A., Fee, J. A., Gray, H. B., Luchinat. C., Malmström, B. G., Richards, J. H., Sanders, D., and Slutter, C. E. (1996) J. Am. Chem. Soc. 46, 11658-11659.
30. Dennison, C., Berg, A., de Vries, S., and Canters, G. W. (1996) FEBS Lett. 394, 340-344.
31. Murthy, N. N., Karlin, K. D., Bertini, I., and Luchinat, C. (1997) J. Am. Chem. Soc. 119, 2156-2162.
32. Donaire, A., Salgado, J., Jimenez, H. R., and Moratal, J. M. (1995) in Nuclear Magnetic Resonance of Paramagnetic Macromolecules (La Mar, G. N., Ed.) pp 213-244, Kluwer Academic Publishers, Dordrecht, The Netherlands.
33. Banci, L., and Piccioli, M. (1996) in Encyclopedia of Magnetic Resonance (Grant, D. M., and Harris, R. K., Eds.) pp 1365-1373, Wiley, Chichester, U.K.
34. Bertini, I., & Luchinat, C. (1986) in NMR of paramagnetic molecules in biological systems, Benjamin/Cummings, Menlo Park, CA.
35. Rajarathnam, K., La Mar, G. N., Chiu, M. L., and Sligar, S. G. (1992) J. Am. Chem. Soc. 114, 9048-9058.
36. La Mar, G. N., Chen, Z. G., Vyas, K., and McPherson, A. D. (1995) J. Am. Chem. Soc. 117, 411-419.
37. Banci, L., Bertini, I., Pierattelli, R., Tien, M., and Vila, A. J. (1995) J. Am. Chem. Soc. 117, 8659-8667.
38. Gochin, M., and Roder, H. (1995) Bull. Magn. Reson. 17, 1-4.
39. Banci, L., Bertini, I., Bren, K. L., Cremonini, M. A., Gray, H. B., Luchinat, C., and Turano, P. (1996) J. Biol. Inorg. Chem. 1, 117-126.
40. Guiles, R. D., Sarma, S., DiGate, R. J., Banville, D., Basus, V. J., Kuntz, I. D., and Waskell, L. (1996) Nat. Struct. Biol. 3, 333-339.
41. Banci, L., Bertini, I., Gori Savellini, G., Romagnoli, A., Turano, P., Cremonini, M. A., Luchinat, C., and Gray, H. B. (1997) Proteins: Struct. Funct., Genet. 29, 68-76.
42. Banci, L., Dugad, L. B., La Mar, G. N., Keating K. A., Luchinat, C., and Pierattelli, R. (1992) Biophys. J. 63, 530-543.
43. Bertini, I., Jonsson, B.-H., Luchinat, C., Pierattelli, R., and Vila, A. J. (1994) J. Magn. Reson., Ser. B 104, 230-239.
44. Bertini, I., Luchinat, C., Piccioli, M., Vicens Oliver, M., and Viezzoli, M. S. (1991) Eur. Biophys. J. 20, 269-279.
45. Blaszak, J. A., Ulrich, E. L., Markley, J. L., and McMillin, D. R. (1982) Biochemistry 21, 6253-6258.
46. Bertini, I., Viezzoli, M. S., Luchinat, C., Stafford, E., Cardin, A. D. Behnke, W. D., Bhattacharyya, L., and Brewer, C. (1987) J. Biol. Chem. 262, 16984-16994.
47. Ming, L. J., Banci, L., Luchinat, C., Bertini, I., and Valentine, J. S. (1988) Inorg. Chem. 27, 4458-4463.
48. Zannoni, D. (1989) Bichim. Biophys. Acta 975, 299.
49. Baker, E. N. (1988) J. Mol. Biol. 203, 1071.
50. Nar, H., Messerschmidt, A., Huber, R., van de Kamp, M., and Canters, G. W. (1991) J. Mol. Biol. 218, 427.
51. Nar, H., Messerschimdt, A., Huber, R., van de Kamp, M., and Canters, G. W. (1991) J. Mol. Biol. 221, 765-772.
52. Romero, A., Hoitink, C. W. G., Nar, H., Huber, R., Messerschmidt, A., and Canters, G. W. (1993) J. Mol. Biol. 229, 1007-1021.
53. Murphy, L. M. M., Strange, R. W., Karlsson, G. B., Lundberg, L. G., Pascher, T., Reinhammar, B., and Hasnain, S. (1993) Biochemistry 32, 1965-1975.
54. Karlson, B. G., Tsai, L. C., Nar, H., Sanders-Loehr, J., Bonander, N., Langer, V., and Sjolin, L. (1997) Biochemistry 36, 4089-4095.
55. Guss, J. M., and Freeman, H. C. (1983) J. Mol. Biol. 169, 521-563.
56. Guss, J. M., Harrowell, P. R., Murata, M., Norris, V. A., and Freeman, H. C. (1986) J. Mol. Biol. 192, 361-387.
57. Hart, P. J., Nersissian, A. M., Herrmann, R. G., Nalbandyan, R. M., Valentine, J. S., and Eisenberg, D. (1996) Protein Sci. 5, 2175-2183.
58. Kalverda, A. P., Wymenga, S. S., Lommen, A., van de Ven, F. J. M., Cees, W. H., and Canters, G. W. (1994) J. Mol. Biol. 240, 358-371.
59. Coremans, J. W. A., Poluektov, O. G., Groenen, E. J. J., Canters, G. W., Nar, H., and Messerschmidt, A. (1994) J. Am. Chem. Soc. 116, 3097-3101.
60. Salgado, J., Jimenez, H. R., Donaire, A., and Moratal, J. M. (1995) Eur. J. Biochem. 231, 358-369.
61. Moratal Mascarell, J. M., Salgado, J., Donaire, A., Jimenez, H. R., and Castells, J. (1993) Inorg. Chem. 32, 3587-3588.
62. Moratal Mascarell, J. M., Salgado, J., Donaire, A., Jimenez, H. R., Castells, J., and Martinez Ferrer, M.-J. (1993) Magn. Reson. Chem. 31, S41-S46.
63. Moratal Mascarell, J. M., Salgado, J., Donaire, A., Jimenez, H. R., and Castells, J. (1993) J. Chem. Soc. , Chem. Commun., 110-112.
64. Salgado, J., Jimenez, H. R., Moratal, J. M., Kroes, S. J., Warmerdam, G. C. M., and Canters, G. W. (1996) Biochemistry 35, 1810-1819.
65. Jimenez, H. R., Salgado, J., Moratal, J. M., and Morgenstern-Badarau, I. (1996) Inorg. Chem. 35, 2737-2741.
66. Moratal, J. M., Romero, A., Salgado, J., Perales-Alarcon, A., and Jimenez, H. R. (1995) Eur. J. Biochem. 228, 653-657.
67. Bonander, N., Vanngard, T., Tsai, L. C., Langer, V., Nar, H., and Sjolin, L. (1997) Proteins: Struct., Funct., Genet. 27, 385-394.
68. Piccioli, M., Luchinat, C., Mizoguchi, T. J., Ramirez, B. E., Gray, H. B., and Richards, J. H. (1995) Inorg. Chem. 34, 737-742.
69. Parr, S. R., Barber, D., Greenwood, C., Phillips, B. W., and Melling, J. (1976) Biochem. J. 157, 423-430.
70. Rance, M., Sörensen, O. W., Bodenhausen, G., Wagner, G., Ernst, R. R., and Wüthrich, K. (1983) Biochem. Biophys. Res. Commun. 117, 479.
71. Bax, A., Griffey, R. H., and Hawkins, B. L. (1983) J. Magn. Reson. 55, 301-315.
72. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) J. Chem. Phys. 77, 4546-4553.
73. Griesinger, C., Otting, G., Wüthrich, K., and Ernst, R. R. (1988) J. Am. Chem. Soc. 110, 7870-7872.
74. Cavanagh, J., and Rance, M. (1990) J. Magn. Reson. 88, 72-85.
75. Bax, A., and Davis, D. G. (1985) J. Magn. Reson. 65, 355-360.
76. Marion, D., and Wüthrich, K. (1983) Biochem. Biophys. Res. Commun. 113, 967-974.
77. van de Kamp, M., Canters, G. W., Wijmenga, S. S., Lommen, A., Hilbers, C. W., Nar, H., and Messerschmidt, A. (1992) Biochemistry 31, 10194-10207.
78. Oh, B.-H., and Markley, J. L. (1990) Biochemistry 29, 3993-4004.
79. Oh, B.-H., Mooberry, E. S., and Markley, J. L. (1990) Biochemistry 29, 4004-4011.
80. Oh, B.-H., and Markley, J. L. (1990) Biochemistry 29, 4012-4017.
81. Xia, B., Westler, W. M., Cheng, H., Meyer, J., Moulis, J.-M., and Markley, J. L. (1995) J. Am. Chem. Soc. 117, 5347-5350.
82. La Mar, G. N. (1973) in NMR of Paramagnetic Molecules (La Mar, G. N., Horrocks, W. D. W., and Holm, R. H., Eds.) Academic Press, New York.
83. Banci, L., Bertini, I., Luchinat, C., Donaire, A., Martinez, M.-J., and Moratal Mascarell, J. M. (1990) Comments Inorg. Chem. 9, 245-261.
84. Karplus, M., (1963) J. Am. Chem. Soc. 85, 2870-2871.
85. Ho, F. F.-L., and Reilley, C. N. (1969) Anal. Chem. 41, 1835-1841.
86. Pratt, L., and Smith, B. B. (1968) Trans. Faraday Soc. 65, 915-927.
87. Bertini, I., Donaire, A., Feinberg, B. A., Luchinat, C., Piccioli, M., and Yuan, H. (1995) Eur. J. Biochem. 232, 192-205.
88. Huber, J. G., Gaillard, J., and Moulis, J.-M. (1995) Biochemistry 34, 194-205.
89. Wang, P. L., Donaire, A., Zhou, Z. H., Adams, M. W. W., and La Mar, G. N. (1996) Biochemistry 35, 11319-11328.
90. Sheppard, S. K., Eaton, G. R., and Eaton, S. S. (1989) Inorg. Chem. 28, 4496-4499.
91. Eaton, D. R., Josey, A. D., Phillips, W. D., and Benson, R. E. (1962) J. Chem. Phys. 37, 347-360.
92. Eaton, D. R., Josey, A. D., Benson, R. E., Phillips, W. D., and Cairns, T. L. (1962) J. Am. Chem. Soc. 84, 4100-4106.
93. Happe, J. A., and Ward, R. L. (1963) J. Chem. Phys. 39, 1211-1218.
94. Kluiber, R. W., and Horrocks, W. D., Jr. (1965) J. Am. Chem. Soc. 87, 5350-5356.
95. Kluiber, R. W., and Horrocks, W. D., Jr. (1967) Inorg. Chem. 6, 166.
96. Holm, R. H., Everett, G. W., and Horrocks, W. D., Jr. (1966) J. Am. Chem. Soc. 88, 1071.
97. Wu, F.-J., and Kurtz, D. M., Jr. (1989) J. Am. Chem. Soc. 111, 6563-6572.
98. Langen, R., Jensen, G. M., Jacob, U., Stephen, P. J., and Warshel, A. (1992) J. Biol. Chem. 267, 25625-25627.
99. Huang, J., Ostrander, R. L., Rheingold, A. L., Leung, Y., and Walters, M. A. (1994) J. Am. Chem. Soc. 116, 6769-6776.
100. Moore, G. R., Pettigrew, G. W., and Rogers, N. K. (1986) Proc. Natl. Acad. Sci. U.S.A. 83, 4998-4999.
101. SKjeldahl, L., Westler, W. M., Oh, B.-H., Krezel, A. M., Holden, H. M., Jacobson, B. L., Rayment, I., and Markley, J. L. (1991) Biochemistry 30, 7363-7368.
102. Mouesca, J. M., Rius, G. J., and Lamotte, B. (1993) J. Am. Chem. Soc. 115, 4714-4731.
103. Rius, G. J., and Lamotte, B. (1989) J. Am. Chem. Soc. 111, 2464-2469.
104. Doan, P. E., Fan, C., and Hoffman, B. M. (1994) J. Am. Chem. Soc. 116, 1033-1041.
105. Penfield, K. W., Gay, R. R., Himmelwright, R. S., Eickman, N. C., Norris, V. A., Freeman, H. C., and Solomon, E. I. (1981) J. Am. Chem. Soc. 103, 4382-4388.
106. Mizoguchi, T. J., Di Bilio, A. J., Gray, H. B., and Richards, J. H. (1992) J. Am. Chem. Soc. 114, 10076-10078.
107. Han, J., Loehr, T. M., Valentine, J. S., Averill, B. A., and Sanders-Loehr, J. (1993) J. Am. Chem. Soc. 115, 4256-4263.
108. Coremans, J. W. A., Poluektov, O. G., Groenen, E. J. J., Canters, G. W., Nar, H., and Messerschmidt, A. (1997) J. Am. Chem. Soc. 119, 4726-4731.
109. Penfield, K. W., Gewirth, A. A., and Solomon, E. I. (1985) J. Am. Chem. Soc. 107, 4519-4529.
110. Salgado, J. (1995) Ph.D. Dissertation, University of Valencia, Valencia, Spain.
111. Vila, A. J. and Fernandez, C. O. (1996) J. Am. Chem. Soc. 118, 7291-7298.
112. Ubbink, M., Lian, L. Y., Modi, S., Evans, P. A., and Bendall, D. S. (1996) Eur. J. Biochem. 242, 132-147.