Investigating metal-binding in proteins by nuclear magnetic resonance

Cellular and Molecular Life Sciences

Volumn 64, Issue 9, 2007, Pages 1085-1104

  Jensen, M Ringkjøbing ^a   Hass, M A S ^a   Hansen, D F ^a,b   Led, J J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Backbone dynamics; Calmodulin; Chemical shift mapping; NMR; Paramagnetic NMR; Plastocyanin; Prion protein; Zinc finger

Indexed keywords

ALPHA SYNUCLEIN; COPPER PROTEIN; ISOENZYME; METAL ION; PLASTOCYANIN; PRION PROTEIN; THIOREDOXIN; ZINC FINGER PROTEIN;

BINDING AFFINITY; BINDING SITE; ELECTRON SPIN RESONANCE; METAL BINDING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW;

ANIMALS; BINDING SITES; IRON; MAGNETIC RESONANCE SPECTROSCOPY; METALLOPROTEINS; METALS; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 34247617799     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-6447-x     Document Type: Review

References (182)

1. Lu, Y. and Valentine, J. S. (1997) Engineering metal-binding sites in proteins. Curr. Opin. Struct. Biol. 7, 495-500.
2. Gross, E. L. (1993) Plastocyanin: structure and function. Photosyn. Res. 37, 103-116.
3. Gray, H. B., Malmström, B. G. and Williams, R. J. P. (2000) Copper coordination in blue proteins. J. Biol. Inorg. Chem. 5, 551-559.
4. De Rienzo, F., Gabdoulline, R. R., Wade, R. C., Sola, M. and Menziani, M. C. (2004) Computational approaches to structural and functional analysis of plastocyanin and other blue copper proteins. Cell. Mol. Life Sci. 61, 1123-1142.
5. Solomon, E. I., Szilagyi, R. K., George, S. D. B. and Basumallick, L. (2004) Electronic structures of metal sites in proteins and models: contribution to function in blue copper proteins. Chem. Rev. 104, 419-458.
6. P-árraga, G., Horvath, S. J., Eisen, A., Taylor, W. E., Hood, L., Young, E. T. and Klevit, R. E. (1988) Zinc-dependent structure of a single-finger domain of yeast ADR1. Science 241, 1489-1492.
7. Wilson, C. J., Apiyo, D. and Wittung-Stafshede, P. (2004) Role of cofactors in metalloprotein folding. Q. Rev. Biophys. 37, 285-314.
8. Shriver, D. F., Atkins, P. W., Overton, T. L., Rourke, J. P., Weller, M. T. and Armstrong, F. A. (2006) Inorganic Chemistry, 4th edition, p. 715, Oxford University Press.
9. Capozzi, F., Casadei, F. and Luchinat, C. (2006) EF-hand protein dynamics and evolution of calcium signal transduction: an NMR view. J. Biol. Inorg. Chem. 11, 949-962.
10. 2+ binding, J. Biol. Chem. 277, 20694-20701.
11. Zhang, C.-M., Perona, J. J. and Hou, Y.-M. (2003) Amino acid discrimination by a highly differentiated metal center of an aminoacyl-tRNA synthetase. Biochemistry 42, 10931-10937.
12. Gaggelli, E., Kozlowski, H., Valensin, D. and Valensin, G. (2006) Copper homeostasis and neurodegenerative disorders (Alzheimers, prion, and parkinsons diseases and amyotrophic lateral sclerosis). Chem. Rev. 106, 1995-2044.
13. Blundell, T. L., Dodson, G. G., Hodgkin, D. M. C. and Mercola, D. A. (1972) Insulin: the structure in crystal and its reflection in chemistry and biology. Adv. Protein Chem. 26, 279-402.
14. Cunningham, B. C., Mulkerrin, M. G. and Wells, J. A. (1991) Dimerization of human growth hormone by zinc. Science 253, 545-548.
15. Cavanagh, J., Fairbrother, W. J., Palmer III, A. G. and Skelton, N. J. (1996) Protein NMR Spectroscopy. Principles and Practice, pp. 478-518, Academic Press, San Diego.
16. 2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc.Natl. Acad. Sci. USA. 94, 12366-12371.
17. Shuker, S. B., Hajduk, P. J., Meadows, R. P. and Fesik, S. W. (1996) Discovering high-affinity ligands for proteins: SAR by NMR. Science 274, 1531-1534.
18. Pellecchia, M., Montgomery, D. L., Stevens, S. Y., Kooi, C.W. V., Feng, H. P., Gierasch, L. M. and Zuiderweg, E. R. (2000) Structural insights into substrate binding by the molecular chaperone DnaK. Nat. Struct. Biol. 7, 298-303.
19. Zuiderweg, E. R. P. (2002) Mapping protein-protein interactions in solution by NMR spectroscopy. Biochemistry 41, 1-7.
20. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, pp. 93-114. Wiley, New York.
21. Badsberg, U., Jørgensen, A. M. M., Gesmar, H., Led, J. J., Hammerstad, J. M., Jespersen, L.-L. and Ulstrup, J. (1996) Solution structure of reduced plastocyanin from the bluegreen alga Anabaena variabilis. Biochemistry 35, 7021-7031.
22. Öz, G., Pountney, D. L. and Armitage, I. M. (1998) NMR spectroscopic studies of I=1/2 metal ions in biological systems, Biochem. Cell Biol. 76, 223-234.
23. Akke, M. and Chazin, W. J. (2001) An open and shut case. Nat. Struct. Biol. 8, 910-912.
24. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28, 8972-8979.
25. Ishima, R. and Torchia, D. A. (2000) Protein dynamics from NMR. Nat. Struct. Biol. 7, 740-743.
26. Palmer, A. G. (2004) NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104, 3623-3640.
27. Mandel, A. M., Akke, M. and Palmer, A. G. (1995) Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163.
28. Kay, L. E. (2005) NMR studies of protein dynamics. J. Magn. Reson. 173, 193-207.
29. Boehr, D. D., Dyson, H. J. and Wright, P. E. (2006) An NMR perspective on enzyme dynamics. Chem. Rev. 106, 3055-3079.
30. Lipari, G. and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104, 4546-4559.
31. Lipari, G. and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104, 4559-4570.
32. Carr, H. Y. and Purcell, E. M. (1954) Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys. Rev. 94, 630-638.
33. Meiboom, S. and Gill, D. (1958) Modified spin-echo method for measuring nuclear relaxation times. Rev. Sci. Instrum. 29, 688-691.
34. Palmer, A. G., Kroenke, C. D. and Loria, J. P. (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 339, 204-238.
35. 15N NMR relaxation and chemical shift: conformational exchange in plastocyanin induced by histidine protonations. J. Am. Chem. Soc. 126, 753-765.
36. Mandel, A. M., Akke, M. and Palmer, A.G. (1996) Dynamics of ribonuclease H: temperature dependence of motions on multiple time scales. Biochemistry 35, 16009-16023.
37. Kurland, R. J. and McGarvey, B. R. (1970) Isotropic NMR shifts in transition metal complexes: the calculation of the fermi contact and pseudocontact terms. J. Magn. Reson. 2, 286-301.
38. Arnesano, F., Banci, L. and Piccioli, M. (2005) NMR structures of paramagnetic metalloproteins. Q. Rev. Biophys. 38, 167-219.
39. Bertini, I., Luchinat, C., Parigi, G. and Pierattelli, R. (2005) NMR spectroscopy of paramagnetic metalloproteins. ChemBioChem 6, 1536-1549.
40. Donaldson, L. W., Skrynnikov, N. R., Choy, W.-Y., Muhandiram, D. R., Sarkar, B., Forman-Kay, J. D. and Kay, L. E. (2001) Structural characterization of proteins with an attached ATCUN motif by paramagnetic relaxation enhancement NMR spectroscopy. J. Am. Chem. Soc. 123, 9843-9847.
41. Gaponenko, V., Dvoretsky, A., Walsby, C., Hoffman, B. M. and Rosevear, P. R. (2000) Calculation of z-coordinates and orientational restraints using a metal binding tag. Biochemistry 39, 15217-15224.
42. Feeney, J., Birdsall, B., Bradbury, A. F., Biekofsky, R. R. and Bayley, P. M. (2001) Calmodulin tagging provides a general method of using lanthanide induced magnetic field orientation to observe residual dipolar couplings in proteins in solution. J. Biomol. NMR 21, 41-48.
43. Dvoretsky, A., Gaponenko, V. and Rosevear, P. R. (2002) Derivation of structural restraints using a thiol-reactive chelator. FEBS Lett. 528, 189-192.
44. Gaponenko, V., Altieri, A. S., Li, J. and Byrd, R. A. (2002) Breaking symmetry in the structure determination of (large) symmetric protein dimers. J. Biomol. NMR 24, 143-148.
45. Iwahara, J., Anderson, D. E., Murphy, E. C. and Clore, G. M. (2003) EDTA-derivatized deoxythymidine as a tool for rapid determination of protein binding polarity to DNA by intermolecular paramagnetic relaxation enhancement. J. Am. Chem. Soc. 125, 6634-6635.
46. Wöhnert, J., Franz, K. J., Nitz, M., Imperiali, B. and Schwalbe, H. (2003) Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. J. Am. Chem. Soc. 125, 13338-13339.
47. Gaponenko, V., Sarma, S. P., Altieri, A. S., Horita, D. A., Li, J. and Byrd, R. A. (2004) Improving the accuracy of NMR structures of large proteins using pseuducontact shifts as long-range restraints. J. Biomol. NMR 28, 205-212.
48. Ikegami, T., Verdier, L., Sakhaii, P., Grimme, S., Pescatore, B., Saxena, K., Fiebig, K.M. and Griesinger, C. (2004) Novel techniques for weak alignment of proteins in solution using chemical tags coordinating lanthanide ions. J. Biomol. NMR 29, 339-349.
49. Pintacuda, G., Moshref, A., Leonchiks, A., Sharipo, A. and Otting, G. (2004) Site-specific labelling with a metal chelator for protein-structure refinement. J. Biomol. NMR 29, 351-361.
50. Prudêncio, M., Rohovec, J., Peters, J. A., Tocheva, E., Boulanger, M. J., Murphy, M. E. P., Hupkes, H.-J., Kosters, W., Impagliazzo, A. and Ubbink, M. (2004) A caged lanthanide complex as a paramagnetic shift agent for protein NMR. Chem. Eur. J. 10, 3252-3260.
51. Solomon, I. (1955) Relaxation processes in a system of two spins. Phys. Rev. 99, 559-565.
52. Mispelter, J., Momenteau, M. and Lhoste, J.-M. (1993) Heteronuclear magnetic resonance: applications to biological and related paramagnetic molecules. Biol. Magn. Res. 12, 299-355.
53. Jensen, M. R. and Led, J. J. (2004) Determination of the electron relaxation rates in paramagnetic metal complexes: applicability of available NMR methods. J.Magn. Reson. 167, 169-177.
54. Bertini, I., Lee, Y.-M., Luchinat, C., Piccioli, M. and Poggi, L. (2001) Locating the metal ion in calcium-binding proteins by using cerium(III) as a probe. ChemBioChem 2, 550-558.
55. Babini, E., Bertini, I., Capozzi, F., Felli, I. C., Lelli, M. and Luchinat, C. (2004) Direct carbon detection in paramagnetic metalloproteins to further exploit pseudocontact shift restraints. J. Am. Chem. Soc. 126, 10496-10497.
56. 13C direct detected nmr increases the detectability of residual dipolar couplings. J. Am. Chem. Soc. 128, 15042-15043.
57. 13C-detected heteronuclear NMR spectroscopy. J. Biomol. NMR 36, 111-122.
58. Ubbink, M., Worrall, J. A. R., Canters, G. W., Groenen, E. J. J. and Huber, M. (2002) Paramagnetic resonance of biological metal centers. Annu. Rev. Biophys. Struct. 31, 393-422.
59. Goldfarb, D. and Arieli, D. (2004) Spin distribution and the location of protons in paramagnetic proteins. Annu. Rev. Biophys. Biomol. Struct. 33, 441-468.
60. McLaughlin, A. C. and Leigh, J. S. (1973) Relaxation times in systems with chemical exchange: approximate solutions for the nondilute case. J. Magn. Res. 9, 296-304.
61. Aime, S., D'Amelio, N., Fragai, M., Lee, Y.-M., Luchinat, C., Terreno, E. and Valensin, G. (2002) A paramagnetic probe to localize residues next to carboxylates on protein surfaces. J. Biol. Inorg. Chem. 7, 617-622.
62. Jensen, M. R., Petersen, G., Lauritzen, C., Pedersen, J. and Led, J. J. (2005) Metal binding sites in proteins: identification and characterization by paramagnetic NMR relaxation. Biochemistry 44, 11014-11023.
63. Bertini, I., Luchinat, C. and Parigi, G. (2001) Solution NMR of Paramagnetic Molecules. Applications to Metallobiomolecules and Models, p. 84-85. Elsevier, Amsterdam.
64. 15N labeled biomolecules characterized through cross-correlation rates: applications to paramagnetic proteins. J. Biomol. NMR 12, 509-521.
65. Bertini, I., Bryant, D. A., Ciurli, S., Dikiy, A., Fern-ndez, C. O., Luchinat, C., Safarov, N., Vila, A. J. and Zhao, J. (2001) Backbone dynamics of plastocyanin in both oxidation states: solution structure of the reduced form and comparison with the oxidized state. J. Biol. Chem. 276, 47217-47226.
66. Head, J. F., Inouye, S., Teranishi, K. and Shimomura, O. (2000) The crystal structure of the photoprotein aequorin at 2.3 Ångström resolution. Nature 405, 372-376.
67. 2+-binding photoprotein. J. Biochem. 138, 613-620.
68. Crivici, A. and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin. Annu. Rev. Biophys. Biomol. Struct. 24, 85-116.
69. Ikura, M. (1996) Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21, 14-17.
70. Barbato, G., Ikura, M., Kay, L. E., Pastor, R. W. and Bax, A. (1992) Backbone dynamics of calmodulin studied by N-15 relaxation using inverse detected two-dimensional NMR spectroscopy - the central helix is flexible. Biochemistry 31, 5269-5278.
71. Strynadka, N. C. J. and James, M. N. G. (1989) Crystal structures of the helix-loop-helix calcium binding proteins. Annu. Rev. Biochem. 58, 951-998.
72. Babu, Y. S., Sack, J. S. and Greenhough, T. J. and Bugg, C. E., Means, A. R. and Cook, W. J. (1985) Three-Dimensional structure of calmodulin. Nature 315, 37-40.
73. Kretsinger, R. H., Rudnick, S. E. and Weissman, L. J. (1986) Crystal structure of calmodulin. J. Inorg. Biochem. 28, 289-302.
74. Babu, Y. S., Bugg, C. E. and Cook, W. J. (1988) Structure of calmodulin refined at 2.2 Å resolution. J. Mol. Biol. 204, 191-204.
75. Zhang, M., Tanaka, T. and Ikura, M. (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2, 758-767.
76. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C. B. and Bax, A. (1995) Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2, 768-776.
77. Finn, B. E., Evenäs, J., Drakenberg, T., Waltho, J. P., Thulin, E. and Forsén, S. (1995) Calcium-induced structural changes and domain autonomy in calmodulin. Nat. Struct. Biol. 2, 777-783.
78. Evenäs, J., Forsén, S., Malmendal, A. and Akke, M. (1999) Backbone dynamics and energetics of a calmodulin domain mutant exchanging between closed and open conformations. J. Mol. Biol. 289, 603-617.
79. Malmendal, A., Evenäs, J., Forsén, S. and Akke, M. (1999) Structural dynamics in the C-terminal domain of calmodulin at low calcium levels. J. Mol. Biol. 293, 883-899.
80. Evenäs, J., Malmendal, A. and Akke, M. (2001) Dynamics of the transition between open and closed conformations in a calmodulin C-terminal domain mutant. Structure 9, 185-195.
81. Linse, S., Helmersson, A. and Forsén, S. (1991) Calcium-binding to calmodulin and its globular domains. J. Biol. Chem. 266, 8050-8054.
82. 2+-saturated state. Biochemistry 36, 3448-3457.
83. 2+ binding and conformational changes in a calmodulin domain. Biochemistry 37, 13744-13754.
84. 15N NMR relaxation measurements. Eur. J. Biochem. 230, 1014-1024.
85. Malmendal, A., Linse, S., Evenäs, J., Forsén, S. and Drakenberg, T. (1999) Battle for the EF-hands: magnesium-calcium interference in calmodulin. Biochemistry 38, 11844-11850.
86. Malmendal, A., Evenäs, J., Thulin, E., Gippert, G. P., Drakenberg, T. and Forsén, S. (1998) When size is important: accommodation of magnesium in a calcium binding regulatory domain. J. Biol. Chem. 273, 28994-29001.
87. Wittung-Stafshede, P. (2004) Role of cofactors in folding of the blue-copper protein azurin. Inorg. Chem. 43, 7926-7933.
88. Miller, J., McLachlan, A. D. and Klug, A. (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 4, 1609-1614.
89. Berg, J. M. and Godwin, H. A. (1997) Lessons from zinc-binding peptides. Annu. Rev. Biophys. Biomol. Struct. 26, 357-371.
90. Cox, E. H. and McLendon, G. L. (2000) Zinc-dependent protein folding. Curr. Opin. Chem. Biol. 4, 162-165.
91. Diakun, G. P., Fairall, L. and Klug, A. (1986) EXAFS study of the zinc-binding sites in the protein transcription factor IIIA. Nature 324, 698-699.
92. Lee, M. S., Gippert, G. P., Soman, K. V., Case, D. A. and Wright, P. E. (1989) Three-dimensional solution structure of a single zinc finger DNA-binding domain. Science 245, 635-637.
93. Nolte, R. T., Conlin, R. M., Harrison, S. C. and Brown, R. S. (1998) Differing roles for zinc fingers in DNA recognition: structure of a six-finger transcription factor IIIA complex. Proc. Natl. Acad. Sci. USA 95, 2938-2943.
94. Laity, J. H., Lee, B. M. and Wright, P. E. (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11, 39-46.
95. Andreini, C., Banci, L. and Bertini, I. and Rosato, A. (2006) Counting the zinc-proteins encoded in the human genome. J. Proteome Res. 5, 196-201.
96. Klug, A. and Schwabe, J. W. R. (1995) Zinc fingers. FASEB J. 9, 597-604.
97. Frankel, A. D., Berg, J. M. and Pabo, C. O. (1987) Metal-dependent folding of a single zinc finger from transcription factor IIIA. Proc. Natl. Acad. Sci. USA 84, 4841-4845.
98. Miura, T., Satoh, T. and Takeuchi, H. (1998) Role of metal-ligand coordination in the folding pathway of zinc finger peptides. Biochim. Biophys. Acta 1384, 171-179.
99. 2+ binding effects on the zinc-ribbon of human general transcription factor TFIIB. Biochem. J. 378, 317-324.
100. Giedroc, D. P., Chen, X., Pennella, M. A. and LiWang, A. C. (2001) Conformational heterogeneity in the C-terminal zinc fingers of human MTF-1. J. Biol. Chem. 276, 42322-42332.
101. Potter, B. M., Feng, L. S., Parasuram, P. P., Matskevich, V. A., Wilson, J. A., Andrews, G. K. and Laity, J. H. (2005) The six zinc fingers of metal-responsive element binding transcription factor-1 form stable and quasi-ordered structures with relatively small differences in zinc affinities. J. Biol. Chem. 280, 28529-28540.
102. Wu, X., Bishopric, N. H., Discher, D. J., Murphy, B. J. and Webster, K. A. (1996) Physical and functional sensitivity of zinc finger transcription factors to redox change. Mol. Cell. Biol. 16, 1035-1046.
103. Baldwin, M. A. and Benz, C. C. (2002) Redox control of zinc finger proteins. Methods Enzymol. 353, 54-69.
104. Witkiewicz-Kucharczyk, A. and Bal, W. (2006) Damage of zinc fingers in DNA repair proteins: a novel molecular mechanism in carcinogenesis. Toxicology Lett. 162, 29-42.
105. Solomon, E. I. and Lowery, M. D. (1993) Electronic structure contributions to function in bioinorganic chemistry. Science 259, 1575-1581.
106. Randall, D. W., Gamelin, D. R., LaCroix, L. B. and Solomon, E. I. (2000) Electronic structure contributions to electron transfer in blue Cu and Cu-A. J. Biol. Inorg. Chem. 5, 16-29.
107. Solomon, E. I. (2006) Spectroscopic methods in bioinorganic chemistry: blue to green to red copper sites. Inorg. Chem. 45, 8012-8025.
108. De Kerpel, J. O. A. and Ryde, U. (1999) Protein strain in blue copper proteins studied by free energy pertubation. Proteins: Structure, Function, and Genetics 36, 157-174.
109. Ryde, U., Olsson, M. H. M., Roos, B. O., De Kerpel, J. O. A. and Pierloot, K. (2000) On the role of strain in blue copper proteins, J. Biol. Inorg. Chem. 5, 565-574.
110. George, S. J., Lowery, M. D., Solomon, E. I. and Cramer, S. P. (1993) Copper L-edge spectral studies: a direct experimental probe of the ground-state covalency in the blue copper site in plastocyanin. J. Am. Chem. Soc. 115, 2968-2969.
111. Shadle, S. E., Penner-Hahn, J. E., Schugar, H. J., Hedman, B., Hodgson, K. O. and Solomon, E. I. (1993) X-ray absorption spectroscopic studies of the blue copper site:metal and ligand K-edge studies to probe the origin of the EPR hyperfine splitting in plastocyanin. J. Am. Chem. Soc. 115, 767-776.
112. 14N ENDOR spectroscopy. J. Am. Chem. Soc. 113, 1533-1538.
113. Bertini, I., Ciurli, S., Dikiy, A., Gasanov, R., Luchinat, C., Martini, G. and Safarov, N. (1999) High-field NMR studies of oxidized blue copper proteins: the case of spinach plastocyanin. J. Am. Chem. Soc. 121, 2037-2046.
114. Hansen, D. F. and Led, J. J. (2004) Mapping the electronic structure of the blue copper site in plastocyanin by NMR relaxation. J. Am. Chem. Soc. 126, 1247-1252.
115. Hansen, D. F., Gorelsky, S. I., Sarangi, R., Hodgson, K. O., Hedman, B., Christensen, H. E. M., Solomon, E. I. and Led, J. J. (2006) Reinvestigation of the method used to map the electronic structure of blue copper proteins by NMR relaxation. J. Biol. Inorg. Chem. 11, 277-285.
116. Penfield, K. W., Gewirth, A. A. and Solomon, E. I. (1985) Electronic structure and bonding of the blue copper site in plastocyanin. J. Am. Chem. Soc. 107, 4519-4529.
117. Pierloot, K., De Kerpel, J. O. A., Ryde, U. and Roos, B. O. (1997) Theoretical study of the electronic spectrum of plastocyanin. J. Am. Chem. Soc. 119, 218-226.
118. Pierloot, K., De Kerpel, J. O. A., Ryde, U., Olsson, M. H. M. and Roos, B. O. (1998) Relation between the structure and spectroscopic properties of blue copper proteins. J. Am. Chem. Soc. 120, 13156-13166.
119. van Gastel, M., Coremans, J. W. A., Sommerdijk, H., van Hemert, M. C. and Groenen, E. J. J. (2002) An ab initio quantum-chemical study of the blue-copper site of azurin. J. Am. Chem. Soc. 124, 2035-2041.
120. Guss, J. M., Bartunik, H. D. and Freeman, H. C. (1992) Accuracy and precision in protein structure analysis: restrained least squares refinement of the structure of poplar plastocyanin at 1.33 Å resolution. Acta Cryst. B 48, 790-811.
121. Cheung, K.-C., Strange, R. W. and Hasnain, S. S. (2000) 3D EXAFS refinement of the Cu site of azurin sheds light on the nature of structural change at the metal centre in an oxidation-reduction process: an integrated approach combining EXAFS and crystallography. Acta. Cryst. D 56, 697-704.
122. Hansen, D. F. and Led, J. J. (2006) Determination of the geometric structure of the metal site in a blue copper protein by paramagnetic NMR. Proc. Natl. Acad. Sci. USA 103, 1738-1743.
123. Hansen, D. F. and Led, J. J. (2001) Measuring the longitudinal NMR relaxation rates of fast relaxing nuclei using a signal eliminating relaxation filter. J. Magn. Reson. 151, 339-346.
124. Bertini, I., Fernández, C. O., Karlsson, B. G., Leckner, J., Luchinat, C., Malmström, B. G., Nersissian, A. M., Pierattelli, R., Shipp, E., Valentine, J. S. and Vila, A. J. (2000) Structural information through NMR hyperfine shifts in blue copper proteins. J. Am. Chem. Soc. 122, 3701-3707.
125. 1H NMR spectroscopy. Biochemistry 35, 3085-3092.
126. 1H NMR spectroscopy: Cu(II)-pseudoazurin and Cu(II)-rusticyanin. J. Am. Chem. Soc. 124, 13698-13708.
127. 1H NMR NOE study on Co(II) stellacyanin: some clues about the structure of the metal site. FEBS Lett. 355, 15-18.
128. 1H NMR spectrum of the cobalt(II) derivative of spinach plastocyanin. Inorg. Chem. 43, 1502-1510.
129. 1H NMR study. Biochemistry 35, 1810-1819.
130. Salgado, J., Kalverda, A. P., Diederix, R. E. M., Canters, G. W., Moratal, J. M., Lawler, A. T. and Dennison, C. (1999) Paramagnetic NMR investigations of Co(II) and Ni(II) amicyanin. J. Biol. Inorg. Chem. 4, 457-467.
131. 1H NMR study of Co(II)-pseudoazurin. J. Biol. Inorg. Chem. 8, 75-82.
132. Dennison, C. and Harrison, M. D. (2004) The active-site structure of umecyanin, the stellacyanin from horseradish roots. J. Am. Chem. Soc. 126, 2481-2489.
133. Taylor, J. P., Hardy, J. and Fischbeck, K. H. (2002) Toxic proteins in neurodegenerative disease. Science 296, 1991-1995.
134. Lee, J. C., Langen, R., Hummel, P. A., Gray, H. B. and Winkler, J. R. (2004) α-Synuclein structures from fluorescence energy-transfer kinetics: implications for the role of the protein in parkinson's disease. Proc. Natl. Acad. Sci. USA 101, 16466-16471.
135. Bernado, P., Bertoncini, C. W., Griesinger, C., Zweckstetter, M. and Blackledge, M. (2005) Defining long-range order and local disorder in native alpha-synuclein using residual dipolar couplings. J. Am. Chem. Soc. 127, 17968-17969.
136. Lee, J. C., Gray, H. B. and Winkler, J. R. (2005) Tertiary contact formation in α-synuclein probed by electron transfer. J. Am. Chem. Soc. 127, 16388-16389.
137. Paik, S. R., Shin, H.-J., Lee, J.-H., Chang, C.-S. and Kim, J. (1999) Copper(II)-induced self-oligomerization of α-synuclein. Biochem. J. 340, 821-828.
138. Uversky, V. N., Li, J. and Fink, A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human α-synuclein, J. Biol. Chem. 276, 44284-44296.
139. Binolfi, A., Rasia, R. M., Bertoncini, C. W., Ceolin, M., Zweckstetter, M., Griesinger, C., Jovin, T. M. and Fernandez, C. O. (2006) Interaction of α-synuclein with divalent metal ions reveals key differences: a link between structure, binding specificity and fibrillation enhancement. J. Am. Chem. Soc. 128, 9893-9901.
140. Rasia, R. M., Bertoncini, C. W., Marsh, D., Hoyer, W., Cherny, D., Zweckstetter, M., Griesinger, C., Jovin, T. M. and Fernandez, C. O. (2005) Structural characterization of copper(II) binding to α-synuclein: insights into the bioinorganic chemistry of parkinson's disease. Proc. Natl. Acad. Sci. USA 102, 4294-4299.
141. Sung, Y., Rospigliosi, C. and Eliezer, D. (2006) NMR mapping of copper binding sites in alpha-synuclein. Biochim. Biophys. Acta 1764, 5-12.
142. Giasson, B. I., Murray, I. V. J., Trojanowski, J. Q. and Lee, V. M.-Y. (2001) A hydrophobic stretch of 12 amino acid residues in the middle of α-synuclein is essential for filament assembly. J. Biol. Chem. 276, 2380-2386.
143. Bertoncini, C. W., Jung, Y.-S., Fernandez, C. O., Hoyer, W., Griesinger, C., Jovin, T. M. and Zweckstetter, M. (2005) Release of long-range tertiary interactions potentiates aggregation of natively unstructured α-synuclein. Proc. Natl. Acad. Sci. USA 102, 1430-1435.
144. Prusiner, S. B. (1991) Molecular biology of prion diseases. Science 252, 1515-1522.
145. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D., Hayes, S. F. and Caughey, W. S. (1991) Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30, 7672-7680.
146. Pan, K.-M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., Cohen, F. E. and Prusiner, S. B. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA 90, 10962-10966.
147. Brown, D. R., Wong, B.-S., Hafiz, F., Clive, C., Haswell, S. J. and Jones, I. M. (1999) Normal prion protein has an activity like that of superoxide dismutase. Biochem. J. 344, 1-5.
148. Brown, D. R., Clive, C. and Haswell, S. J. (2001) Antioxidant activity related to copper binding of native prion protein. J. Neurochem. 76, 69-76.
149. Wong, B. S., Pan, T., Liu, T., Li, R., Petersen, R. B., Jones, I. M., Gambetti, P., Brown, D. R. and Sy, M. S. (2000) Breakthroughs and views - prion disease: a loss of antioxidant function? Biochem. Biophys. Res. Commun. 275, 249-252.
150. Shiraishi, N., Ohta, Y. and Nishikimi, M. (2000) The octapeptide repeat region of prion protein binds Cu(II) in the redox-inactive state. Biochem. Biophys. Res. Commun. 267, 398-402.
151. Whittal, R. M., Ball, H. L., Cohen, F. E., Burlingame, A. L., Prusiner, S. B. and Baldwin, M. A. (2000) Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci. 9, 332-343.
152. Lehmann, S. (2002) Metal ions and prion diseases. Curr. Opin. Chem. Biol. 6, 187-192.
153. Brown, D. R. (2001) Prion and prejudice normal protein and the synapse. TRENDS in Neurosci. 24, 85-90.
154. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R. and Wüthrich, K. (1996) NMR structure of the mouse prion protein domain PrP (121-231). Nature 382, 180-182.
155. James, T. L., Liu, H., Ulyanov, N.B., Farr-Jones, S., Zhang, H., Donne, D. G., Kaneko, K., Groth, D., Mehlhorn, I., Prusiner, S. B. and Cohen, F. E. (1997) Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc. Natl. Acad. Sci. USA 94, 10086-10091.
156. Donne, D. G., Viles, J. H., Groth, D., Mehlhorn, I., James, T. L., Cohen, F. E., Prusiner, S. B., Wright, P. E. and Dyson, H. J. (1997) Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc. Natl. Acad. Sci. USA 94, 13452-13457.
157. Riek, R., Hornemann, S., Wider, G., Glockshuber, R. and Wüthrich, K. (1997) NMR characterization of the full-length recombinantmurine prion protein, mPrP(23-231), FEBS Lett 413, 282-288.
158. Viles, J. H., Cohen, F. E., Prusiner, S. B., Goodin, D. B., Wright, P. E. and Dyson, H. J. (1999) Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc. Natl. Acad. Sci. USA 96, 2042-2047.
159. Garnett, A. P. and Viles, J. H. (2003) Copper binding to the octarepeats of the prion protein. J. Biol. Chem. 278, 6795-6802.
160. Thompsett, A. R., Abdelraheim, S. R., Daniels, M. and Brown, D. R. (2005) High affinity binding between copper and full-length prion protein identified by two different techniques. J. Biol. Chem. 280, 42750-42758.
161. Hornshaw, M. P., McDermott, J. R., Candy, J. M. and Lakey, J. H. (1995) Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem. Biophys. Res. Commun. 207, 621-629.
162. Hornshaw, M. P., McDermott, J. R., Candy, J. M. and Lakey, J. H. (1995) Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides. Biochem. Biophys. Res. Commun. 214, 993-999.
163. Brown, D. R., Qin, K., Herms, J. W., Madlung, A., Manson, J., Strome, R., Fraser, P. E., Kruck, T., Bohlen, A., Schulz-Schaeffer, W., Giese, A., Westaway, D. and Kretzschmar, H. (1997) The cellular prion protein binds copper in vivo. Nature 390, 684-687.
164. Stöckel, J., Safar, J., Wallace, A.C., Cohen, F. E. and Prusiner, S. B. (1998) Prion protein selectively binds copper(II) ions. Biochemistry 37, 7185-7193.
165. 2+ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy. Biochemistry 39, 13760-13771.
166. Jackson, G. S., Murray, I., Hosszu, L. L. P., Gibbs, N., Waltho, J. P., Clarke, A. R. and Collinge, J. (2001) Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. USA 98, 8531-8535.
167. Gaggelli, E., Bernardi, F., Molteni, E., Pogni, R., Valensin, D., Valensin, G., Remelli, M., Luczkowski, M. and Kozlowski, H. (2005) Interaction of the human prion PrP(106-126) sequence with copper(II), manganese(II), and zinc(II): NMR and EPR studies. J. Am. Chem. Soc. 127, 996-1006.
168. Bocharova, O. V., Breydo, L., Salnikov, V. V. and Baskakov, I. V. (2005) Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44, 6776-6787.
169. Weissmann, C. (2004) The state of the prion. Nat. Rev. Microbiol. 2, 861-871.
170. Baskakov, I. V. and Bocharova, O. V. (2005) In vitro conversion of mammalian prion protein into amyloid fibrils displays unusual features. Biochemistry 44, 2339-2348.
171. Pan, K.-M., Stahl, N. and Prusiner, S. B. (1992) Purification and properties of the cellular prion protein from syrian hamster brain. Protein Sci. 1, 1343-1352.
172. Wadsworth, J. D. F., Hill, A. F., Joiner, S., Jackson, G. S., Clarke, A. R. and Collinge, J. (1999) Strain-specific prion-protein conformation determined by metal ions. Nat. Cell Biol. 1, 55-59.
173. Brown, D. R., Hafiz, F., Glasssmith, L. L., Wong, B.-S., Jones, I. M., Clive, C. and Haswell, S. J. (2000) Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J. 19, 1180-1186.
174. 2+ ions at physiological concentrations. J. Mol. Biol. 346, 1393-1407.
175. Treiber, C., Simons, A. and Multhaup, G. (2006) Effect of copper and manganese on the de novo generation of protease-resistant prion protein in yeast cells. Biochemistry 45, 6674-6680.
176. Tsenkova, R. N., Iordanova, I. K., Toyoda, K. and Brown, D. R. (2004) Prion protein fate governed by metal binding. Biochem. Biophys. Res. Commun. 325, 1005-1012.
177. 2+-IDA complex localization on protein surface and its application to elucidate long distance information. FEBS Lett. 566, 157-161.
178. 2+-induced pseudocontact shifts in a native nonmetalloprotein. Biochemistry 45, 8782-8787.
179. Holmgren, A. (1985) Thioredoxin. Annu. Rev. Biochem. 54, 237-271.
180. 180 van Holde, M. (1990) Biochemistry, p. 140. Benjamin/Cummings, Mento Park.
181. DeLano, W. L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos.
182. Koradi, R., Billeter, M. and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.