New evidence that the Alzheimer β-amyloid peptide does not spontaneously form free radicals: An ESR study using a series of spin-traps

Free Radical Biology and Medicine

Volumn 30, Issue 10, 2001, Pages 1154-1162

  Turnbull, Stuart ^a   Tabner, Brian J ^a   El Agnaf, Omar M A ^b   Twyman, Lance J ^c   Allsop, David ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

amyloid; Alzheimer's disease; ESR spectroscopy; Free radicals; Hydrogen peroxide; Oxidative stress; Spin trapping

Indexed keywords

2 METHYL 2 NITROSOPROPANE; 3,5 DIBROMO 4 NITROSOBENZENESULFONIC ACID; 5,5 DIMETHYL 1 PYRROLINE 1 OXIDE; AMYLOID BETA PROTEIN; FREE RADICAL; HYDROGEN PEROXIDE; N TERT BUTYL ALPHA (4 PYRIDYL 1 OXIDE) NITRONE; N TERT BUTYL ALPHA PHENYLNITRONE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CATALYSIS; CONTROLLED STUDY; DECOMPOSITION; ELECTRON SPIN RESONANCE; HUMAN; HUMAN CELL; HYDROLYSIS; NEUROTOXICITY; OXIDATIVE STRESS; PEPTIDE ANALYSIS; PRIORITY JOURNAL; SPIN TRAPPING;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; COPPER; DARKNESS; ELECTRON SPIN RESONANCE SPECTROSCOPY; FREE RADICALS; HUMANS; HYDROGEN PEROXIDE; IRON; LIGHT; SPIN LABELS; SPIN TRAPPING;

EID: 0035874024     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(01)00510-X     Document Type: Article

References (44)

1. Allsop D. Introduction to Alzheimer's disease. Hooper N. Alzheimer's disease methods and protocols . 2000;1-21 Humana Press, Totawa, NJ.
2. Hardy J., Allsop D. Amyloid deposition as the central event in the etiology of Alzheimer's disease. Trends Pharmacol. Sci. 12:1991;383-388.
3. Selkoe D.J. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature. 399:(Suppl.):1999;A23-A31.
4. Teplow D.B. Structural and kinetic features of amyloid β-protein fibrillogenesis. Int. J. Exp. Clin. Invest. 5:1998;121-142.
5. Iversen L.L., Mortishire-Smith R.J., Pollack S.J., Shearman M.S. The toxicity in vitro of β-amyloid protein. Biochem. J. 311:1995;1-16.
6. Dobson C.M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 24:1999;329-332.
7. Kakizuka A. Protein precipitation a common etiology in neurodegenerative disorders? Trends Genet. 14:1998;396-402.
8. Koo E.H., Lansbury P.T., Kelly J.W. Amyloid diseases abnormal protein aggregation in neurodegeneration . Proc. Natl. Acad. Sci. USA. 96:1999;3342-3344.
9. Yan S.D., Chen X.F.-J., Chen M., Zhu H., Roher A., Slattery T., Zhao L., Nagashima M., Morser J., Migheli A., Nawroth P., Stern D., Schmidt A.M. RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature. 382:1996;685-691.
10. Roher A.E., Chaney M.O., Kuo Y.M., Webster S.D., Stine W.B., Haverkamp L.J., Woods A.S., Cotter R.J., Tuohy J.M., Krafft G.A., Bonnell B.S., Emmerling M.R. Morphology and toxicity of Aβ-(1-42)-dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease. J. Biol. Chem. 271:1996;20631-20635.
11. 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., Klein W.L. Diffusible, nonfibrillar ligands derived from Aβ (1-42) are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA. 95:1998;6448-6453.
12. Walsh D.M., Lomakin A., Benedek G.B., Condron M.M., Teplow D.B. Amyloid β-protein fibrillogenesis detection of a protofibrillar intermediate . J. Biol. Chem. 272:1997;22364-22372.
13. Walsh D.M., Hartley D.M., Kusumoto Y., Fezoui Y., Condron M.M., Lomakin A., Benedek G.B., Selkoe D.J., Teplow D.B. Amyloid β-protein fibrillogenesis structure and biological activity of protofibrillar intermediates . J. Biol. Chem. 274:1999;25945-25952.
14. Hartley D.M., Walsh D.M., Ye C.P., Diehl T., Vasquez S., Vassilev P.M., Teplow D.B., Selkoe D.J. Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci. 19:1999;8876-8884.
15. Harper J.D., Wong S.S., Lieber C.M., Lansbury P.T. Assembly of Aβ amyloid protofibrils an in vitro model for a possible early event in Alzheimer's disease . Biochemistry. 38:1999;8972-8980.
16. Howlett D.R., Ward R.V., Bresciani L., Jennings K.H., Christie G., Allsop D., Gray C.W., Karran E.H. Biological activity associated with a high molecular weight form of β-amyloid. Alzheimer's Rep. 2:1999;171-177.
17. Hensley K., Carney J.M., Mattson M.P., Aksenova M., Harris M., Wu J.F., Floyd R.A., Butterfield D.A. A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide relevance to Alzheimer's disease . Proc. Natl. Acad. Sci. USA. 91:1994;3270-3274.
18. Hensley K., Butterfield D.A., Mattson M., Aksenova M., Harris M., Wu J.F., Floyd R., Carney J. A model for beta-amyloid aggregation and neurotoxicity based on the free radical generating capacity of the peptide implications of "molecular shrapnel" for Alzheimer's disease . Proc. West Pharmacol. Soc. 38:1995;113-120.
19. Yatin S.M., Varadarajan S., Link C.D., Butterfield D.A. In vitro and in vivo oxidative stress associated with Alzheimer's amyloid β-peptide (1-42). Neurobiol. Aging. 20:1999;325-330.
20. Varadarajan S., Yatin S., Kanski J., Jahanshahi F., Butterfield D.A. Methionine residue 35 is important in amyloid β-peptide-associated free radical oxidative stress. Brain Res. Bull. 50:1999;133-141.
21. Tomiyama T., Shoji A., Kataoka K., Suwa Y., Asano S., Kaneko H., Endo N. Inhibition of amyloid β protein aggregation and neurotoxicity by rifampicin. Its possible function as a hydroxyl radical scavenger. J. Biol. Chem. 271:1996;6839-6844.
22. Dikalov S.I., Vitek M.P., Maples K.R., Mason R.P. Amyloid β peptides do not form peptide-derived free radicals spontaneously, but can enhance metal-catalyzed oxidation of hydroxylamines to nitroxides. J. Biol. Chem. 274:1999;9392-9399.
23. 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., Bush A.I. The Aβ peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry. 38:1999;7609-7616.
24. Bush A.I., Huang X., Fairlie D.P. The possible origin of free radicals from amyloid β peptides in Alzheimer's disease. Neurobiol. Aging. 20:1999;335-337.
25. 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., Glabe C., Bowden E.F., Masters C.L., Fairlie D.P., Tanzi R.E., Bush A.I. Cu(II) potentiation of Alzheimer Aβ neurotoxicity. J. Biol. Chem. 274:1999;37111-37116.
26. El-Agnaf O.M.A., Goodwin H., Sheridan J.M., Frears E.R., Austen B.M. Improved solid-phase syntheses of amyloid proteins associated with neurodegenerative diseases. Protein and Peptide Letts. 7:2000;1-8.
27. Duling D.R. Simulation of multiple isotropic spin-trap EPR-spectra. J. Magn. Reson. B. 104:1994;105-110.
28. Forrester A. Landolt-Börnstein - Numerical data and functional relationships in science and technology. Fischer H. Magnetic properties of free radicals. 1989;8-16 Springer, Berlin.
29. Windle J.J. Hyperfine coupling constants for nitroxide spin probes in water and carbon tetrachloride. J. Magn. Reson. 45:1981;432-439.
30. Janzen E.G., Haire D.L. Two decades of spin-trapping. Tanner D.D. Advances in free radical chemistry. vol. 1:1990;253-295 JAI Press, Greenwich, CT.
31. Kalyanaraman K., Perez-Reyes E., Mason R.P. The reduction of nitroso spin-traps in chemical and biological systems. A cautionary note. Tetrahedron Lett. 20:1979;4809-4812.
32. Kotake Y., Janzen E.G. Decay and fate of the hydroxyl radical adduct of α-phenyl-N-tert-butylnitrone in aqueous media. J. Am. Chem. Soc. 113:1991;9503-9506.
33. 13C for three-parameter scatter plots. J. Org. Chem. 53:1988;4532-4542.
34. Mekarbane P.G., Tabner B.J. ESR spin-trap study of radicals present during the thermolysis of some di-tert-alkyl peroxides. Magn. Reson. Chem. 36:1998;826-832.
35. Trousson P., Lion Y. Fourier transform numerical analysis of the long-range proton hyperfine coupling in nitroxide radicals. J. Phys. Chem. 89:1985;1954-1958.
36. Bush A.I. Metals and neuroscience. Curr. Opin. Chem. Biol. 2:2000;184-191.
37. Turnbull S., Tabner B.J., El-Agnaf O.M.A., Moore S., Davies Y., Allsop D. α-Synuclein implicated in Parkinson's disease catalyses the formation of hydrogen peroxide in vitro. Free Rad. Biol. Med. 30:2001;1163-1170.
38. Hensley K., Pye Q.N., Maidt M.L., Stewart C.A., Robinson K.A., Jaffrey F., Floyd R.A. Interaction of α-phenyl-N-tert-butyl nitrone and alternative electron acceptors with complex 1 indicates a substrate reduction site upstream from the rotenone binding site. J. Neurochem. 71:1998;2549-2557.
39. Chamulitrat W., Parker C.E., Tomer K.B., Mason R.P. Phenyl N-tert-butyl nitrone forms nitric oxide as a result of its Fe(III) catalysed hydrolysis or hydroxyl radical adduct formation. Free Radic. Res. 23:1995;1-14.
40. Britigan B.E., Pou S., Rosen G.M., Lilleg D.M., Buettner G.R. Hydroxyl radical is not a product of the reaction of xanthine-oxidase - the confounding problem of adventitous iron bound to xanthine-oxidase. J. Biol. Chem. 265:1990;17533-17538.
41. Atamna H., Paler-Martinez A., Ames B.N.X. N-t-butyl hydroxylamine, a hydrolysis product of α-phenyl-N-t-butyl nitrone, is more potent in delaying senescence in human lung fibroblasts. J. Biol. Chem. 275:2000;6741-6748.
42. Makino K., Hagiwara T., Hagi A., Nishi M., Murakami A. Cautionary note for DMPO spin trapping in the presence of iron ion. Biochem. Biophys. Res. Commun. 172:1990;1073-1080.
43. Varadarajan S., Yatin S., Aksenova M., Butterfield D.A. Review: Alzheimer's amyloid β-peptide-associated free radical oxidative stress and neurotoxicity. J. Struct. Biol. 130:2000;184-208.
44. Kay C.J. Mechanical mechanism for the peptidyl free radical generation by amyloid fibrils. FEBS Lett. 403:1997;230-235.