Soluble amyloid β1-28-copper(I)/copper(II)/iron(II) complexes are potent antioxidants in cell-free systems

Biochemistry

Volumn 47, Issue 30, 2008, Pages 7796-7806

  Baruch Suchodolsky, Rozena ^a   Fischer, Bilha ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; GLYCOPROTEINS; IRON; METAL IONS; METALS; MODULATION; ZINC;

ALZHEIMER'S DISEASE (AD); METAL-ION COMPLEXES; OXIDATIVE DAMAGE;

IONS;

AMYLOID BETA PROTEIN; ANTIOXIDANT; COPPER COMPLEX; HYDROGEN PEROXIDE; IRON COMPLEX; METAL ION; COPPER; IRON;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL FREE SYSTEM; CHELATION; CONTROLLED STUDY; DECOMPOSITION; ELECTRON SPIN RESONANCE; MOLECULAR MECHANICS; MOLECULAR MODEL; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; SOLUBILITY; SPIN TRAPPING; CHEMISTRY; HUMAN; METABOLISM; PATHOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANTIOXIDANTS; CELL-FREE SYSTEM; COPPER; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; HYDROGEN PEROXIDE; IRON; MICROSCOPY, ELECTRON, TRANSMISSION;

EID: 48249117506     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800114g     Document Type: Article

References (88)

1. Case, F. (2005) Metal for the mind. Chem. World 2, 28-32.
2. Qureshi, G. A., Memon, S. A., Memon, A. B., Ghouri, R. A., Memon, J. M., and Parvez, S. H. (2005) The emerging role of iron, zinc, copper, magnesium and selenium and oxidative stress in health and diseases. Biog. Amines 19, 147-169.
3. Uriu-Adams, J. Y., and Keen, C. L. (2005) Copper, oxidative stress, and human health. Mol. Aspects Med. 26, 268-298.
4. Korycka, D., Malgorzata, B., and Richardson, T. (1978) Activated oxygen species and oxidation of food constituents. Crit. Rev. Food Sci. Nutr. 10, 209-241.
5. Halliwell, B. (1997) Antioxidants and human disease: a general introduction. Nutr. Rev. 55, S44-S49; discussion S49-S52.
6. Fenton, H. J. H. (1894) J. Chem. Soc. 65, 899.
7. Halliwell, B., Gutteridge, J. M. C., and Aruoma, O. I. (1987) The deoxyribose method: a simple "test-tube" assay for determination of rate constants for reactions of hydroxyl radicals. Anal. Biochem. 165, 215-219.
8. 2 mixtures: effects of metal ion chelation and the search for high-valent metal-oxygen intermediates. Arch. Biochem. Biophys. 323, 63-70.
9. Haber, F., and Weiss, J. (1934) The catalytic decomposition of hydrogen peroxide by iron salts. Proc. R. Soc. London A147, 332-351.
10. Weiss, J. (1935) Electron transition processes in the mechanism of oxidation and reduction reactions in solutions. Naturwissenschaften 23, 64-69.
11. Barb, W. G., Baxendale, J. H., George, P., and Hargrave, K. R. (1951) Reactions of ferrous and ferric ions with hydrogen peroxide. I. Ferrous-ion reaction. Trans. Faraday Soc. 47, 462-500.
12. Pecci, L., Montefoschi, G., and Cavallini, D. (1997) Some new details of the copper-hydrogen peroxide interaction. Biochem. Biophys. Res. Commun. 235, 264-267.
13. Gutteridge, J. M. C., and Wilkins, S. (1983) Copper salt-dependent hydroxyl radical formation. Damage to proteins acting as antioxidants. Biochim. Biophys. Acta 759, 38-41.
14. Behl, C., Davis, J. B., Lesley, R., and Schubert, D. (1994) Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77, 817-827.
15. Tomiyama, T., Shoji, A., Kataoka, K.-i., Suwa, Y., Asano, S., Kaneko, H., and Endo, N. (1996) Inhibition of amyloid β protein aggregation and neurotoxicity by rifampicin. Its possible function as a hydroxyl radical scavenger. J. Biol. Chem. 271, 6839-6844.
16. Huang, X., Moir, R. D., Tanzi, R. E., Bush, A. I., and Rogers, J. T. (2004) Redox-active metals, oxidative stress, and Alzheimer's disease pathology. Ann. N.Y. Acad. Sci. 1012, 153-163.
17. Glenner, G. G., and Wong, C. W. (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885-890.
18. Masters, C. L., Simms, G., Weinman, N. A., Multhaup, G., McDonald, B. L., and Beyreuther, K. (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. U.S.A. 82, 4245-4249.
19. Selkoe, D. J. (1991) The molecular pathology of Alzheimer's disease. Neuron 6, 487-498.
20. Atwood, C. S., Huang, X., Moir, R. D., Tanzi, R. E., and Bush, A. I. (1999) Role of free radicals and metal ions in the pathogenesis of Alzheimer's disease. Metal Ions Biol. Sys. 36, 309-364.
21. Lovell, M. A., Robertson, J. D., Teesdale, W. J., Campbell, J. L., and Markesbery, W. R. (1998) Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci. 158, 47-52.
22. Atwood, C. S., Scarpa, R. C., Huang, X., Moir, R. D., Jones, W. D., Fairlie, D. P., Tanzi, R. E., and Bush, A. I. (2000) Characterization of copper interactions with Alzheimer amyloid β peptides: identification of an attomolar-affinity copper binding site on amyloid β1-42. J. Neurochem. 75, 1219-1233.
23. Guilloreau, L., Damian, L., Coppel, Y., Mazarguil, H., Winterhalter, M., and Faller, P. (2006) Structural and thermodynamical properties of CuII amyloid-β16/28 complexes associated with Alzheimer's disease. J. Biol. Inorg. Chem. 11, 1024-1038.
24. Dong, J., Atwood, C. S., Anderson, V. E., Siedlak, S. L., Smith, M. A., Perry, G., and Carey, P. R. (2003) Metal binding and oxidation of amyloid-β within isolated senile plaque cores: Raman microscopic evidence. Biochemistry 42, 2768-2773.
25. Atwood, C. S., Moir, R. D., Huang, X., Scarpa, R. C., Bacarra, N. M. E., Romano, D. M., Hartshorn, M. A., Tanzi, R. E., and Bush, A. I. (1998) Dramatic aggregation of Alzheimer Aβ by Cu(II) is induced by conditions representing physiological acidosis. J. Biol. Chem. 273, 12817-12826.
26. Curtain, C. C., Ali, F., Volitakis, I., Cherny, R. A., Norton, R. S., Beyreuther, K., Barrow, C. J., Masters, C. L., Bush, A. I., and Barnham, K. J. (2001) Alzheimer's disease amyloid-β binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits. J. Biol. Chem. 276, 20466-20473.
27. Malouf, A. T. (1992) Effect of beta amyloid peptides on neurons in hippocampal slice cultures. Neurobiol. Aging 13, 543-551.
28. Pike, C. J., Walencewicz, A. J., Glabe, C. G., and Cotman, C. W. (1991) Aggregation-related toxicity of synthetic β-amyloid protein in hippocampal cultures. Eur. J. Pharmacol. 207, 367-368.
29. Pike, C. J., Burdick, D., Walencewicz, A. J., Glabe, C. G., and Cotman, C. W. (1993) Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13, 1676-1687.
30. Lambert, M. P., Barlow, A. K., Chromy, B. A., Edwards, C., Freed, R., Liosatos, M., Morgan, T. E., Rozovsky, I., Trommer, B., Viola, K. L., Wals, P., Zhang, C., Finch, C. E., Krafft, G. A., and Klein, W. L. (1998) Diffusible, nonfibrillar ligands derived from Abeta1 - 42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453.
31. Huang, X., Cuajungco, M. P., Atwood, C. S., Hartshorn, M. A., Tyndall, J. D. A., Hanson, G. R., Stokes, K. C., Leopold, M., Multhaup, G., Goldstein, L. E., Scarpa, R. C., Saunders, A. J., Lim, J., Moir, R. D., Glahe, C., Bowden, E. F., Masters, C. L., Fairlie, D. P., Tanzi, R. E., and Bush, A. I. (1999) Cu(II) potentiation of Alzheimer Aβ neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction. J. Biol. Chem. 274, 37111-37116.
32. Whitson, J. S., Glabe, C. G., Shintani, E., Abcar, A., and Cotman, C. W. (1990) β-Amyloid protein promotes neuritic branching in hippocampal cultures. Neurosci. Lett. 110, 319-324.
33. Rottkamp, C. A., Raina, A. K., Zhu, X., Gaier, E., Bush, A. I., Atwood, C. S., Chevion, M., Perry, G., and Smith, M. A. (2001) Redox-active iron mediates amyloid-β toxicity. Free Radical Biol. Med. 30, 447-450.
34. Schubert, D., and Chevion, M. (1995) The role of iron in beta amyloid toxicity. Biochem. Biophys. Res. Commun. 216, 702-707.
35. Barrow, C. J., Yasuda, A., Kenny, P. T. M., and Zagorski, M. G. (1992) Solution conformations and aggregational properties of synthetic amyloid β-peptides of Alzheimer's disease. Analysis of circular dichroism spectra. J. Mol. Biol. 225, 1075-1093.
36. Zagorski, M. G., and Barrow, C. J. (1992) NMR studies of amyloid β-peptides: proton assignments, secondary structure, and mechanism of an α-helix → β-sheet conversion for a homologous, 28-residue, N-terminal fragment. Biochemistry 31, 5621-5631.
37. Huang, X., Atwood, C. S., Hartshorn, M. A., Multhaup, G., Goldstein, L. E., Scarpa, R. C., Cuajungco, M. P., Gray, D. N., Lim, J., Moir, R. D., Tanzi, R. E., and Bush, A. I. (1999) The Aβ peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry 38, 7609-7616.
38. Bush, A. I., Masters, C. L., and Tanzi, R. E. (2003) Copper, β-amyloid, and Alzheimer's disease: Tapping a sensitive connection. Proc. Natl. Acad. Sci. U.S.A. 100, 11193-11194.
39. Irie, K., Murakami, K., Masuda, Y., Morimoto, A., Ohigashi, H., Ohashi, R., Takegoshi, K., Nagao, M., Shimizu, T., and Shirasawa, T. (2005) Structure of β-amyloid fibrils and its relevance to their neurotoxicity. Implications for the pathogenesis of Alzheimer's disease. J. Biosci. Bioeng. 99, 437-447.
40. Smith, M. A., Nunomura, A., Zhu, X., Takeda, A., and Perry, G. (2000) Metabolic, metallic, and mitotic sources of oxidative stress in Alzheimer disease. Antiox. Redox Signal. 2, 413-420.
41. Smith, M. A., Joseph, J. A., and Perry, G. (2000) Arson. Tracking the culprit in Alzheimer's disease. Ann. N.Y. Acad. Sci. 924, 35-38.
42. Shigenaga, M. K., Hagen, T. M., and Ames, B. N. (1994) Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U.S.A. 91, 10771-10778.
43. Atwood, C. S., Obrenovich, M. E., Liu, T., Chan, H., Perry, G., Smith, M. A., and Martins, R. N. (2003) Amyloid-β: a chameleon walking in two worlds: a review of the trophic and toxic properties of amyloid-β. Brain Res. Rev. 43, 1-16.
44. Behl, C., Davis, J., Cole, G. M., and Schubert, D. (1992) Vitamin E protects nerve cells from amyloid β protein toxicity. Biochem. Biophys. Res. Commun. 186, 944-950.
45. Kontush, A., Berndt, C., Weber, W., Akopyan, V., Arlt, S., Schippling, S., and Beisiegel, U. (2001) Amyloid-β is an antioxidant for lipoproteins in cerebrospinal fluid and plasma. Free Radical Biol. Med. 30, 119-128.
46. Zou, K., Gong, J.-S., Yanagisawa, K., and Michikawa, M. (2002) A novel function of monomelic amyloid β-protein serving as an antioxidant molecule against metal-induced oxidative damage. J. Neurosci. 22, 4833-4841.
47. Andorn, A. C., and Kalaria, R. N. (2000) Factors affecting pro-and anti-oxidant properties of fragments of the β-protein precursor (bPP): Implication for Alzheimer's disease. J. Alzheimer's Dis. 2, 69-78.
48. Gibson, G. E., Zhang, H., Sheu, K. F. R., and Park, L. C. H. (2000) Differential alterations in antioxidant capacity in cells from Alzheimer patients. Biochim. Biophys. Acta, Mol. Basis Dis. 1502, 319-329.
49. Kontush, A., Donarski, N., and Beisiegel, U. (2001) Resistance of human cerebrospinal fluid to in vitro oxidation is directly related to its amyloid-β content. Free Radical Res. 35, 507-517.
50. Bush, A. I. (2000) Metals and neuroscience. Curr. Opin. Chem. Biol. 4, 184-191.
51. Varadarajan, S., Yatin, S., Aksenova, M., and Butterfield, D. A. (2000) Review: Alzheimer's amyloid β-peptide-associated free radical oxidative stress and neurotoxicity. J. Struct. Biol. 130, 184-208.
52. Markesbery, W. R. (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radical Biol. Med. 23, 134-147.
53. Syme, C. D., Nadal, R. C., Rigby, S. E. J., and Viles, J. H. (2004) Copper binding to the amyloid-β (Aβ) peptide associated with Alzheimer's disease: Folding, coordination geometry, pH dependence, stoichiometry, and affinity of Aβ-(1-28): Insights from a range of complementary spectroscopic techniques. J. Biol. Chem. 279, 18169-18177.
54. Talafous, J., Marcinowski, K. J., Klopman, G., and Zagorski, M. G. (1994) Solution structure of residues 1-28 of the amyloid β-peptide. Biochemistry 33, 7788-7796.
55. Shen, C. L., Scott, G. L., Merchant, F., and Murphy, R. M. (1993) Light scattering analysis of fibril growth from the amino-terminal β(1-28) of β-amyloid peptide. Biophys. J. 65, 2383-2395.
56. Brenner, A. J., and Harris, E. D. (1995) A quantitative test for copper using bicinchoninic acid. Anal. Biochem. 226, 80-84.
57. Kalyanaraman, B. (1982) Detection of toxic free radicals in biology and medicine. Rev. Biochem. Toxicol. 4, 73-139.
58. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
59. Mira, H., Vilar, M., Esteve, V., Martinell, M., Kogan Marcelo, J., Giralt, E., Salom, D., Mingarro, I., Penarrubia, L., and Perez-Paya, E. (2004) Ionic self-complementarity induces amyloid-like fibril formation in an isolated domain of a plant copper metallochaperone protein. BMC Struct. Biol. 4, 7.
60. 2+ inhibits the aggregation of amyloid β-peptide (1-42) in vitro. Angew. Chem., Int. Ed. 40, 2274-2277.
61. Klunk, W. E., Pettegrew, J. W., and Abraham, D. J. (1989) Quantitative evaluation of Congo red binding to amyloid-like proteins with a beta-pleated sheet conformation. J. Histochem. Cytochem. 37, 1273-1281.
62. Ali, F. E., Separovic, F., Barrow, C. J., Yao, S., and Barnham, K. J. (2006) Copper and zinc mediated oligomerization of Aβ peptides. Int. J. Pept. Res. Therapeut. 12, 153-164.
63. Jiang, D., Men, L., Wang, J., Zhang, Y., Chickenyen, S., Wang, Y., and Zhou, F. (2007) Redox reactions of copper complexes formed with different β-amyloid peptides and their neuropathalogical relevance. Biochemistry 46, 9270-9282.
64. Ciccotosto, G. D., Barnham, K. J., Cherny, R. A., Masters, C. L., Bush, A. I., Curtain, C. C., Cappai, R., and Tew, D. (2004) Methionine oxidation: Implications for the mechanism of toxicity of the β-amyloid peptide from Alzheimer's disease. Lett. Pept. Sci. 10, 413-417.
65. Guilloreau, L., Combalbert, S., Sournia-Saquet, A., Mazarguil, H., and Faller, P. (2007) Redox chemistry of copper-amyloid-b: the generation of hydroxyl radical in the presence of ascorbate is linked to redox-potentials and aggregation state. ChemBioChem 8, 1317-1325.
66. Hou, L., and Zagorski, M. G. (2006) NMR reveals anomalous copper(II) binding to the amyloid Aβ peptide of Alzheimer's disease. J. Am. Chem. Soc. 128, 9260-9261.
67. Ueda, J.-i., Saito, N., and Ozawa, T. (1996) Detection of free radicals produced from reactions of lipid hydroperoxide model compounds with Cu(II) complexes by ESR spectroscopy. Arch. Biochem. Biophys. 325, 65-76.
68. Kim, Y. S., and Han, S. (2000) Nitric oxide protects Cu,Zn-superoxide dismutase from hydrogen peroxide-induced inactivation. FEBS Lett. 479, 25-28.
69. Rae, T. D., Schmidt, P. J., Pufahl, R. A., Culotta, V. C., and O'Halloran, T. V. (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284, 805-808.
70. Hicks, M., and Gebicki, J. M. (1986) Rate constants for reaction of hydroxyl radicals with Tris, Tricine and Hepes buffers. FEBS Lett. 199, 92-94.
71. Gelvan, D., and Saltman, P. (1990) Different cellular targets for copper- and iron-catalyzed oxidation observed using a copper-compatible thiobarbituric acid assay. Biochim. Biophys. Acta, Gen. Subj. 1035, 353-360.
72. Hanna, P. M., Chamulitrat, W., and Mason, R. P. (1992) When are metal ion-dependent hydroxyl and alkoxyl radical adducts of 5,5-dimethyl-1-pyrroline N-oxide artifacts? Arch. Biochem. Biophys. 296, 640-644.
73. Baruch, R., and Fischer, B. (2007) Can nucleotides prevent Cu-induced oxidative damage?, J. Inorg. Biochem. (in press).
74. Richter, Y., and Fischer, B. (2006) Nucleotides and inorganic phosphates as potential antioxidants. J. Biol. Inorg. Chem. 11, 1063-1074.
75. Lovell, M. A., Gabbita, S. P., and Markesbery, W. R. (1999) Increased DNA oxidation and decreased levels of repair products in Alzheimer's disease ventricular CSF. J. Neurochem. 72, 771-776.
76. Wang, J., Markesbery, W. R., and Lovell, M. A. (2006) Increased oxidative damage in nuclear and mitochondrial DNA in mild cognitive impairment. J. Neurochem. 96, 825-832.
77. Atwood, C. S., Huang, X., Khatri, A., Scarpa, R. C., Kim, Y.-S., Moir, R. D., Tanzi, R. E., Roher, A. E., and Bush, A. I. (2000) Copper catalyzed oxidation of Alzheimer Aβ. Cell. Mol. Biol. 46, 777-783.
78. Zhao, F., Ghezzo-Schoneich, E., Aced, G. I., Hong, J., Milby, T., and Schoneich, C. (1997) Metal-catalyzed oxidation of histidine in human growth hormone. Mechanism, isotope effects, and inhibition by a mild denaturing alcohol. J. Biol. Chem. 272, 9019-9029.
79. Uchida, K., and Kawakishi, S. (1994) Identification of oxidized histidine generated at the active site of Cu,Zn-superoxide dismutase exposed to H2O2. Selective generation of 2-oxo-histidine at the histidine 118. J. Biol. Chem. 269, 2405-2410.
80. Berlett, B. S., and Stadtman, E. R. (1997) Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20313-20316.
81. Platis, I. E., Ermacora, M. R., and Fox, R. O. (1993) Oxidative polypeptide cleavage mediated by EDTA-iron covalently linked to cysteine residues. Biochemistry 32, 12761-12767.
82. 2+) ions accompanies the E1P→E2P conformational change. Proc. Natl. Acad. Sci. U.S.A. 97, 11954-11959.
83. Murray, I. V. J., Sindoni, M. E., and Axelsen, P. H. (2005) Promotion of oxidative lipid membrane damage by amyloid β proteins. Biochemistry 44, 12606-12613.
84. 2+ in a mononuclear metal ion binding site. J. Am. Chem. Soc. 126, 13534-13538.
85. +2 and sheet breakers on aggregation of amyloid peptides. Protein Pept. Lett. 12, 197-202.
86. Gorman, P. M., and Chakrabartty, A. (2001) Alzheimer β-amyloid peptides: structures of amyloid fibrils and alternate aggregation products. Biopolymers 60, 381-394.
87. Walsh, D. M., Hartley, D. M., Kusumoto, Y., Fezoui, Y., Condron, M. M., Lomakin, A., Benedek, G. B., Selkoe, D. J., and Teplow, D. B. (1999) Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274, 25945-25952.
88. Kuo, Y.-M., Emmerling, M. R., Vigo-Pelfrey, C., Kasumic, T. C., Kirkpatrick, J. B., Murdoch, G. H., Ball, M. J., and Roher, A. E. (1996) Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem. 271, 4077-4081.