alpha-Synuclein (alpha S) is the main protein component of Lewy bodies, characterizing the pathogenesis of Parkinson's disease. alpha S is unstructured in solution but adopts a helical structure in its extended N-terminal segment upon association with membranes. In vitro the protein binds avidly Cu-II, but in vivo the protein is N-acetylated, and Cu-II binding is lost. We have now clarified the binding characteristics of the Cu-I complex with the truncated alpha S peptide 1-15, both in N-acetylated and free amine forms, in a membrane mimetic environment and found that complexation occurs with a 1:2 Cu-I-alpha S stoichiometry, where Cu-I is bound to Met1 and Met5 residues of two helical peptide chains. The resulting tetrahedral Cu-I center is redox-stable, does not form reactive oxygen species, and is unreactive against dopamine in the presence of O-2. This suggests that, unlike cytosolic Cu-I-alpha S, which retains the capacity to activate O-2 and promote oxidative reactions, membrane-bound Cu-I-alpha S may serve as a sink for unreactive copper.