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Originally published In Press as doi:10.1074/jbc.M100175200 on March 27, 2001

J. Biol. Chem., Vol. 276, Issue 23, 20466-20473, June 8, 2001
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Alzheimer's Disease Amyloid-beta Binds Copper and Zinc to Generate an Allosterically Ordered Membrane-penetrating Structure Containing Superoxide Dismutase-like Subunits*

Cyril C. CurtainDagger §, Feda Ali, Irene Volitakis||, Robert A. Cherny||, Raymond S. NortonDagger , Konrad Beyreuther**, Colin J. Barrow, Colin L. Masters||, Ashley I. Bush||Dagger Dagger , and Kevin J. BarnhamDagger §§

From the Dagger  Biomolecular Research Institute, 343 Royal Parade, Parkville, Victoria 3052, Australia, the § Department of Physics, Monash University, Clayton, Victoria 3168, Australia, the  School of Chemistry, University of Melbourne, Parkville, Victoria 3010, Australia, the || Department of Pathology, University of Melbourne and the Mental Health Research Institute of Victoria, Parkville, Victoria 3052, Australia, the ** Center for Molecular Biology, University of Heidelberg, Im Neuenheimer Feld 282, 69120 Heidelberg, Germany, and the Dagger Dagger  Laboratory for Oxidation Biology, Genetics and Aging Unit and the Department of Psychiatry, Harvard Medical School, Massachusetts General Hospital East, Charlestown, Massachusetts 02129

Amyloid beta  peptide (Abeta ) is the major constituent of extracellular plaques and perivascular amyloid deposits, the pathognomonic neuropathological lesions of Alzheimer's disease. Cu2+ and Zn2+ bind Abeta , inducing aggregation and giving rise to reactive oxygen species. These reactions may play a deleterious role in the disease state, because high concentrations of iron, copper, and zinc have been located in amyloid in diseased brains. Here we show that coordination of metal ions to Abeta is the same in both aqueous solution and lipid environments, with His6, His13, and His14 all involved. At Cu2+/peptide molar ratios >0.3, Abeta coordinated a second Cu2+ atom in a highly cooperative manner. This effect was abolished if the histidine residues were methylated at Nepsilon 2, indicating the presence of bridging histidine residues, as found in the active site of superoxide dismutase. Addition of Cu2+ or Zn2+ to Abeta in a negatively charged lipid environment caused a conformational change from beta -sheet to alpha -helix, accompanied by peptide oligomerization and membrane penetration. These results suggest that metal binding to Abeta generated an allosterically ordered membrane-penetrating oligomer linked by superoxide dismutase-like bridging histidine residues.

* This work was supported in part by grants from the NH&MRC, NIA (to A. I. B.), and Prana Biotechnology Ltd.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§§ To whom correspondence should be addressed. Fax: 61-3-99039655; E-mail: kevin.barnham@bioresi.com.au.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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