ESEEM analysis of multi-histidine Cu(II)-coordination in model complexes, peptides, and amyloid-β

Journal of Physical Chemistry B

Volumn 118, Issue 30, 2014, Pages 8935-8944

  Silva, K Ishara ^a   Michael, Brian C ^a   Geib, Steven J ^a   Saxena, Sunil ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COPPER COMPOUNDS; GLYCOPROTEINS; METAL IONS; NEURODEGENERATIVE DISEASES; PEPTIDES; PH; ZINC; ZINC COMPOUNDS;

ALZHEIMERS DISEASE; COORDINATION MODES; EQUATORIAL LIGANDS; HISTIDINE RESIDUES; METAL-ION COORDINATION; MODEL COMPLEXES; MOLECULAR LEVELS; PHYSIOLOGICAL PH;

COORDINATION REACTIONS;

AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-16); COPPER; HISTIDINE; IMIDAZOLE DERIVATIVE; NITROGEN; PEPTIDE; PEPTIDE FRAGMENT; ZINC;

CHEMICAL STRUCTURE; CHEMISTRY; PROCEDURES; SPECTROSCOPY; VALIDATION STUDY; X RAY DIFFRACTION;

AMYLOID BETA-PEPTIDES; COPPER; HISTIDINE; IMIDAZOLES; MODELS, MOLECULAR; NITROGEN; PEPTIDE FRAGMENTS; PEPTIDES; SPECTRUM ANALYSIS; X-RAY DIFFRACTION; ZINC;

EID: 84905393641     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp500767n     Document Type: Article

References (72)

1. Malmström, B. G.; Leckner, J. The Chemical Biology of Copper Curr. Opin. Chem. Biol. 1998, 2, 286-292
2. Deschampsa, P.; Kulkarnia, P. P.; Gautam-Basakb, M.; Sarkar, B. The Saga of Copper(II)- l -Histidine Coord. Chem. Rev. 2005, 249, 895-909
3. Viles, J. H. Metal Ions and Amyloid Fiber Formation in Neurodegenerative Diseases. Copper, Zinc and Iron in Alzheimers, Parkinsons and Prion Diseases Coord. Chem. Rev. 2012, 256, 2271-2284
4. Faller, P.; Hureau, C. Bioinorganic Chemistry of Copper and Zinc Ions Coordinated to Amyloid-β Peptide Dalton Trans. 2009, 1080-1094
5. Binolfi, A. S.; Lamberto, G. R.; Duran, R.; Quintanar, L.; Bertoncini, C. W.; Souza, J. M.; Cerveñansky, C.; Zweckstetter, M.; Griesinger, C.; Fernández, C. O. Site-Specific Interactions of Cu(II) with α and β-Synuclein: Bridging the Molecular Gap between Metal Binding and Aggregation J. Am. Chem. Soc. 2008, 130, 11801-11812
6. Binolfi, A.; Rodriguez, E. E.; Valensin, D.; DAmelio, N.; Ippoliti, E.; Obal, G.; Duran, R.; Magistrato, A.; Pritsch, O.; Zweckstetter, M. Bioinorganic Chemistry of Parkinsons Disease: Structural Determinants for the Copper-Mediated Amyloid Formation of Alpha-Synuclein Inorg. Chem. 2010, 49, 10668-10679
7. 2+ Binding Modes of Recombinant α-Synuclein: Insights from EPR Spectroscopy J. Am. Chem. Soc. 2008, 130, 7766-7773
8. Bortolus, M.; Bisaglia, M.; Zoleo, A.; Fittipaldi, M.; Benfatto, M.; Bubacco, L.; Maniero, A. L. Structural Characterization of a High Affinity Mononuclear Site in the Copper(II)-α-Synuclein Complex J. Am. Chem. Soc. 2010, 132, 18057-18066
9. 2+ Site in the α-Synuclein Protein of Parkinsons Disease Biochemistry 2011, 50, 1771-1777
10. Binolfia, A.; Quintanarb, L.; Bertoncinic, C. W.; Griesingerd, C.; Fernández, C. O. Bioinorganic Chemistry of Copper Coordination to Alpha-Synuclein: Relevance to Parkinsons Disease Coord. Chem. Rev. 2012, 256, 2188-2201
11. Rasia, R. M.; Bertoncini, C. W.; Marsh, D.; Hoyer, W.; Cherny, D.; Zweckstetter, M.; Griesinger, C.; Jovin, T. M.; Fernández, C. O. Structural Characterization of Copper(II) Binding to α-Synuclein: Insights into the Bioinorganic Chemistry of Parkinsons Disease Proc. Natl. Acad. Sci. 2005, 102, 4294-4299
12. 2+ Binding Sites in the N-Terminal Domain of the Prion Protein by Epr and Cd Spectroscopy Biochemistry 2000, 39, 13760-13771
13. Burns, C. S.; Aronoff-Spencer, E.; Legname, G.; Prusiner, S. B.; Antholine, W. E.; Gerfen, G. J.; Peisach, J.; Millhauser, G. L. Copper Coordination in the Full-Length, Recombinant Prion Protein Biochemistry 2003, 42, 6794-6803
14. 2+ Binding Modes of Full-Length Prion Protein J. Biol. Chem. 2007, 283, 1870-1881
15. Millhauser, G. L. Copper and the Prion Protein: Methods, Structures, Function,and Disease Annu. Rev. Phys. Chem. 2007, 58, 299-320
16. 2+ Coordination Modes J. Am. Chem. Soc. 2007, 129, 15440-15441
17. Chattopadhyay, M.; Walter, E. D.; Newell, D. J.; Jackson, P. J.; Aronoff-Spencer, E.; Peisach, J.; Gerfen, G. J.; Bennett, B.; Antholine, W. E.; Millhauser, G. L. The Octarepeat Domain of the Prion Protein Binds Cu(II) with Three Distinct Coordination Modes at pH 7.4 J. Am. Chem. Soc. 2005, 127, 12647-12656
18. Jackson, G. S.; Murray, I.; Hosszu, L. L. P.; Gibbs, N.; Waltho, J. P.; Clarke, A. R.; Collinge, J. Location and Properties of Metal-Binding Sites on the Human Prion Protein Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 8531-8535
19. 2+ Ions at Physiological Concentrations J. Mol. Biol. 2005, 346, 1393-1407
20. Stellato, F.; Spevacek, A.; Proux, O.; Minicozzi, V.; Millhauser, G.; Morante, S. Zinc Modulates Copper Coordination Mode in Prion Protein Octa-Repeat Subdomains Eur. Biophys J. 2011, 40, 1259-1270
21. Morante, S.; González-Iglesias, R.; Potrich, C.; Meneghini, C.; Meyer-Klaucke, W.; Menestrina, G.; Gasset, M. Inter- and Intra-Octarepeat Cu(II) Site Geometries in the Prion Protein Implications in Cu(II) Binding Cooperativity and Cu(II)-Mediated Assemblies J. Biol. Chem. 2004, 279, 11753-11759
22. Furlan, S.; Penna, G. L.; Guerrieri, F.; Morante, S.; Rossi, G. C. Ab Initio Simulations of Cu Binding Sites on the N-Terminal Region of Prion Protein J. Biol. Inorg. Chem. 2007, 12, 571-583
23. Guerrieri, F.; Minicozzi, V.; Morante, S.; Rossi, G.; Furlan, S.; Penna, G. L. Modeling the Interplay of Glycine Protonation and Multiple Histidine Binding of Copper in the Prion Protein Octarepeat Subdomains J. Biol. Inorg. Chem. 2009, 14, 361-374
24. Quintanar, L.; Rivillas-Acevedo, L.; Grande-Aztatzi, R.; Gómez-Castro, C. Z.; Arcos-López, T.; Vela, A. Copper Coordination to the Prion Protein: Insights from Theoretical Studies Coord. Chem. Rev. 2013, 257, 429-444
25. Syme, C. D.; Nadal, R. C.; Rigby, S. E.; Viles, J. H. Copper Binding to the Amyloid-β (Aβ) Peptide Associated with Alzheimers Disease: Folding, Coordination Geometry, pH Dependence, Stoichiometry, and Affinity of Aβ-(1-28): Insights from a Range of Complementary Spectroscopic Techniques J. Biol. Chem. 2004, 279, 18169-18177
26. Guilloreau, L.; Damian, L.; Coppel, Y.; Mazarguil, H.; Winterhalter, M.; Faller, P. Structural and Thermodynamical Properties of Cuii Amyloid-β16/28 Complexes Associated with Alzheimers Disease J. Biol. Inorg. Chem. 2006, 11, 1024-1038
27. Shin, B.-K.; Saxena, S. Direct Evidence That All Three Histidine Residues Coordinate to Cu(II) in Amyloid-β(1-16) Biochemistry 2008, 47, 9117-9123
28. Morante, S. The Role of Metals in β-Amyloid Peptide Aggregation: X-Ray Spectroscopy and Numerical Simulations Curr. Alzheimers Res. 2008, 5, 508-524
29. Faller, P.; Hureau, C. Impact of Metallic Ions in Alzheimers Disease: Insights from XAS Spectroscopy Actual. Chim. 2011, 356-357
30. Youssef, E. K.; Pierre, D.; Peter, F.; Petra, H. New Insights into the Coordination of Cu(II) by the Amyloid-β 16 Peptide from Fourier Transform Ir Spectroscopy and Isotopic Labeling J. Phys. Chem. B 2011, 115, 14812-14821
31. Hureau, C.; Coppel, Y.; Dorlet, P.; Solari, P. L.; Sayen, S.; Guillon, E.; Sabater, L.; Faller, P. Deprotonation of the Asp1-Ala2 Peptide Bond Induces Modification of the Dynamic Copper(II) Environment in the Amyloid-β Peptide near Physiological pH Angew. Chem., Int. Ed. 2009, 48, 9522-9525
32. Kowalik-Jankowska, T.; Ruta, M.; Wisniewska, K.; ankiewicz, L. Coordination Abilities of the 1-16 and 1-28 Fragments of B-Amyloid Peptide Towards Copper(II) Ions: A Combined Potentiometric and Spectroscopic Study J. Inorg. Biochem. 2003, 95, 270-282
33. Lu, Y.; Prudent, M.; Qiao, L.; Mendeza, M. A.; Girault, H. H. Copper(I) and Copper(II) Binding to β-Amyloid 16 (Aβ16) Studied by Electrospray Ionization Mass Spectrometry Metallomics 2010, 2, 474-479
34. Raffa, D. F.; Gómez-Balderas, R.; Brunelle, P.; Rickard, G. A.; Rauk, A. Ab Initio Model Studies of Copper Binding to Peptides Containing a His-His Sequence: Relevance to the β-Amyloid Peptide of Alzheimers Disease J. Biol. Inorg. Chem. 2005, 10, 887-902
35. Rauk, A. Why Is the Amyloid Beta Peptide of Alzheimers Disease Neurotoxic? Dalton Trans. 2008, 1273-1282
36. Drew, S. C.; Noble, C. J.; Masters, C. L.; Hanson, G. R.; Barnham, K. J. Pleomorphic Copper Coordination by Alzheimers Disease Amyloid-β Peptide J. Am. Chem. Soc. 2009, 131, 1195-1207
37. Dorlet, P.; Gambarelli, S.; Faller, P.; Hureau, C. Pulse EPR Spectroscopy Reveals the Coordination Sphere of Copper(II) Ions in the 1-16 Amyloid-β Peptide: A Key Role of the First Two N-Terminus Residues Angew. Chem., Int. Ed. 2009, 48, 9273-9276
38. Shin, B.-K.; Saxena, S. Substantial Contribution of the Two Imidazole Rings of the His13-His14 Dyad to Cu(II) Binding in Amyloid-β(1-16) at Physiological pH and Its Significance J. Phys. Chem. A 2011, 115, 9590-9602
39. Silva, K. I.; Saxena, S. Zn(II) Ions Substantially Perturb Cu(II) Ion Coordination in Amyloid-β at Physiological pH J. Phys. Chem. B 2013, 117, 9386-9394
40. Drew, S. C.; Noble, C. J.; Masters, C. L.; Hanson, G. R.; Barnham, K. J. Pleomorphic Copper Coordination by Alzheimers Disease Amyloid-β Peptide J. Am. Chem. Soc. 2009, 131, 1195-1207
41. 2+ Binding in Fibrillar Amyloid-β [Aβ(1-40)] Protein J. Am. Chem. Soc. 2012, 134, 18330-18337
42. Hureau, C. Coordination of Redox Active Metal Ions to the Amyloid Precursor Protein and to Amyloid-β Peptides Involved in Alzheimer Disease. Part 1: An Overview Coord. Chem. Rev. 2012, 256, 2164-2174
43. Dorlet, P.; Gambarelli, S.; Faller, P.; Hureau, C. Pulse EPR Spectroscopy Reveals the Coordination Sphere of Copper(II) Ions in the 1-16 Amyloid-β Peptide: A Key Role of the First Two N-Terminus Residues Angew. Chem., Int. Ed. 2009, 48, 9273-9276
44. Jun, S.; Gillespie, J. R.; Shin, B. K.; Saxena, S. The Second Cu(II)-Binding Site in a Proton-Rich Environment Interferes with the Aggregation of Amyloid-Beta(1-40) into Amyloid Fibrils Biochemistry 2009, 48, 10724-10732
45. Alies, B.; Sasaki, I.; Sayen, S.; Guillon, E.; Faller, P.; Hureau, C. Zn Impacts Cu Coordination to Amyloid-β, the Alzheimers Peptide, but Not the Ros Production and the Associated Cell Toxicity Chem. Commun. 2013, 49, 2130-2132
46. Lovell, M. A.; Robertsona, J. D.; Teesdaleb, W. J.; Campbell, J. L.; Markesbery, W. R. Copper, Iron and Zinc in Alzheimers Disease Senile Plaques J. Neurol. Sci. 1998, 158, 47-52
47. McCracken, J.; Desai, P. R.; Papadopoulos, N. J.; Villafranca, J. J.; Peisach, J. Electron Spin-Echo Studies of the Copper(II) Binding Sites in Dopamine β-Hydroxylase Biochemistry 1988, 27, 4133-4137
48. Goldfarb, D.; Fauth, J.-M.; Tor, Y.; Shanzer, A. Study of Cu(II) Binding to Chiral Tripodal Ligands by Electron Spin Echo Spectroscopy J. Am. Chem. Soc. 1991, 113, 1941-1948
49. 4 Acta Chem. Scand. 1972, 26, 3969-3976
50. Abuhijleh, A. L.; Woods, C.; Ahmed, I. Y. Synthesis and Molecular Structure of Monomeric Copper(II) Acetates with 2-Methylimidazole and 1,2-Dimethylimidazole Inorg. Chim. Acta 1990, 190, 11-17
51. Sato, M.; Nagae, S.; Ohmae, K.; Nakaya, J.-I. Preparation and Crystal Structure of an Imidazolate: Bridged Polynuclear Complex [{Cu(Im)(Dien)}N][ClO4] N (Dien = Diethylenetriamine), and Its Properties in Dimethyl Sulfoxide Solution J. Chem. Soc., Dalton Trans. 1986, 1949
52. Merrifield, R. B. Solid Phase Peptide Synthesis. I. The Synthesis of a Tetrapeptide J. Am. Chem. Soc. 1963, 85, 2149-2154
53. Fields, G. B.; Noble, R. L. Solid Phase Peptide Synthesis Utilizing 9-Fluorenylmethoxycarbonyl Amino Acids Int. J. Pept. Protein Res. 1990, 35, 161-214
54. Fauth, J. M.; Schweiger, A.; Braunschweiler, L.; Forrer, J.; Ernst, R. R. Elimination of Unwanted Echoes and Reduction of Deadtime in Three-Pulse Electron Spin-Echo Spectroscopy J. Magn. Reson. 1986, 66, 74
55. Gemperle, C.; Aebli, G.; Schweiger, A.; Ernst, R. R. Phase Cycling in Pulse EPR J. Magn. Reson. 1990, 88, 241
56. Guilloreau, L.; Combalbert, S.; Sournia-Saquet, A.; Mazarguil, H.; Faller, P. Redox Chemistry of Copper-Amyloid-β: Thegeneration of Hydroxyl Radical in the Presenceof Ascorbate Is Linked to Redox-Potentials and Aggregation State ChemBioChem 2007, 8, 1317-1325
57. Burns, C. S.; Aronoff-Spencer, E.; Dunham, C. M.; Lario, P.; Avdiech, N. I.; Antholine, W. E.; Olmstead, M. M.; Vrielink, A.; Gerfen, G. J.; Peisach, J. Molecular Features of the Copper Binding Sites in the Octarepeat Domain of the Prion Protein Biochemistry 2002, 41, 3991-4001
58. Deligiannakis, Y.; Louloudib, M.; Hadjiliadis, N. Electron Spin Echo Envelope Modulation (ESEEM) Spectroscopy as a Tool to Investigate the Coordination Environment of Metal Centers Coord. Chem. Rev. 2000, 201, 1-112
59. Peisach, J.; Blumberg, W. E. Structural Implications Derived from the Analysis of EPR Spectra of Natural and Artificial Copper Proteins Arch. Biochem. Biophys. 1974, 165, 691-708
60. Hernández-Guzmán, J.; Sun, L.; Mehta, A. K.; Dong, J.; Lynn, D. G.; Warncke, K. Copper(II)-Bis-Histidine Coordination Structure in a Fibrillar Amyloid β-Peptide Fragment and Model Complexes Revealed by Electron Spin Echo Envelope Modulation Spectroscopy ChemBioChem 2013, 14, 1762-1771
61. McCracken, J.; Pember, S.; Benkovic, S. J.; Villafranca, J. J.; Miller, R. J.; Peisach, J. Electron Spin-Echo Studies of the Copper Binding Site in Phenylalanine Hydroxylase from Chromobacterium Violaceum J. Am. Chem. Soc. 1988, 110, 1069-1074
62. Burns, C. S.; Aronoff-Spencer, E.; Dunham, C. M.; Lario, P.; Avdievich, N. I.; Antholine, W. E.; Olmstead, M. M.; Vrielink, A.; Gerfen, G. J.; Peisach Molecular Features of the Copper Binding Sites in the Octarepeat Domain of the Prion Protein Biochemistry 2002, 41, 3991-4001
63. Shin, B.-K.; Saxena, S. Insight into Potential Cu(II)-Binding Motifs in the Four Pseudorepeats of Tau Protein J. Phys. Chem. B 2011, 115, 15067-15078
64. McCracken, J.; Peisach, J.; Cote, C. E.; McGuirl, M. A.; Dooley, D. M. Pulsed EPR Studies of the Semiquinone State of Copper-Containing Amine Oxidases J. Am. Chem. Soc. 1992, 114, 3715-3720
65. Mims, W. B. Envelope Modulation in Spin-Echo Experiments Phys. Rev. B 1972, 5, 2409-2419
66. Lai, A.; Flanagan, H. L.; Singel, D. J. Multifrequency Electron Spin Echo Envelope Modulation in S = 1/2, I = 1/2 Systems: Analysis of the Spectral Amplitudes, Line Shapes, and Linewidths J. Chem. Phys. 1988, 89, 7161-7166
67. Tang, X. S.; Diner, B. A.; Larsen, B. S.; Gilchrist, M. L., Jr.; Lorigan, G. A.; Britt, R. D. Identification of Histidine at the Catalytic Site of the Photosynthetic Oxygen-Evolving Complex Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 704-708
68. Singh, V.; Zhu, Z.; Davidson, V. L.; McCracken, J. Characterization of the Tryptophan Tryptophyl-Semiquinone Catalytic Intermediate of Methylamine Dehydrogenase by Electron Spin-Echo Envelope Modulation Spectroscopy J. Am. Chem. Soc. 2000, 122, 931-938
69. Stoll, S.; Calle, C.; Mitrikas, G.; Schweiger, A. Peak Suppression in Eseem Spectra of Multinuclear Spin Systems J. Magn. Reson. 2005, 177, 93-101
70. a Measurements of the β-Peptide and Mechanism of pH-Induced Amyloid Formation J. Am. Chem. Soc. 1999, 121, 8698-8706
71. Zhang, X.; Tian, Y.; Li, Z.; Tian, X.; Sun, H.; Liu, H.; Moore, A.; Ran, C. Design and Synthesis of Curcumin Analogues for in Vivo Fluorescence Imaging and Inhibiting Copper-Induced Cross-Linking of Amyloid Beta Species in Alzheimers Disease J. Am. Chem. Soc. 2013, 135, 16397-16409
72. 2+ Coordination of Alzheimers Disease Amyloid-B Peptide: Relevance to N-Terminally Truncated Forms J. Am. Chem. Soc. 2009, 131, 8760-8761