119
Views
30
CrossRef citations to date
0
Altmetric
Review

Metal homeostasis in Alzheimer’s disease

, &
Pages 711-722 | Published online: 10 Jan 2014

References

  • Cummings JL, Vinters HV, Cole GM, Khachaturian ZS. Alzheimer's disease: etiologies, pathophysiology, cognitive reserve, and treatment opportunities. Neurology51, S2–S17 (1998).
  • Glenner GG, Wong CW. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun.120, 885–890 (1984).
  • Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl Acad. Sci. USA82, 4245–4249 (1985).
  • Kang J, Lemaire HG, Unterbeck A et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature325, 733–736 (1987).
  • Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev.81, 741–766 (2001).
  • Sherrington R, Rogaev EI, Liang Y et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease.Nature375, 754–760 (1995).
  • Lemere CA, Blusztajn JK, Yamaguchi H, Wisniewski T, Saido TC, Selkoe DJ. Sequence of deposition of heterogeneous amyloid β-peptides and Apo E in Down syndrome: implications for initial events in amyloid plaque formation. Neurobiol. Dis.3, 16–32 (1996).
  • Bush AI, Pettingell WH, Multhaup G et al. Rapid induction of Alzheimer A β amyloid formation by zinc. Science265, 1464–1467 (1994).
  • Huang X, Atwood CS, Moir RD et al. Zinc-induced Alzheimer's Aβ1–40 aggregation is mediated by conformational factors. J. Biol. Chem.272, 26464–26470 (1997).
  • Atwood CS, Scarpa RC, Huang X et al. 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 (2000).
  • Cuajungco MP, Faget KY, Huang X, Tanzi RE, Bush AI. Metal chelation as a potential therapy for Alzheimer's disease. Ann. NY Acad. Sci.920, 292–304 (2000).
  • Sano M, Ernesto C, Thomas RG et al. A controlled trial of selegiline, α-tocopherol, or both as treatment for Alzheimer's disease. The Alzheimer's Disease Cooperative Study. N. Engl. J. Med.336, 1216–1222 (1997).
  • Frederickson CJ. Neurobiology of zinc and zinc-containing neurons. Int. Rev. Neurobiol.31, 145–238 (1989).
  • Kardos J, Kovacs I, Hajos F, Kalman M, Simonyi M. Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability. Neurosci. Lett.103, 139–144 (1989).
  • Massie HR, Aiello VR, Iodice AA. Changes with age in copper and superoxide dismutase levels in brains of C57BL/6J mice. Mech. Ageing Dev.10, 93–99 (1979).
  • Morita A, Kimura M, Itokawa Y. The effect of aging on the mineral status of female mice. Biol. Trace Elem. Res.42, 165–177 (1994).
  • Maynard CJ, Cappai R, Volitakis I et al. Overexpression of Alzheimer's disease amyloid-β opposes the age-dependent elevations of brain copper and iron. J. Biol. Chem.277, 44670–44676 (2002).
  • Zecca L, Gallorini M, Schunemann V et al. Iron, neuromelanin and ferritin content in the substantia nigra of normal subjects at different ages: consequences for iron storage and neurodegenerative processes.J. Neurochem.76, 1766–1773 (2001).
  • Deibel MA, Ehmann WD, Markesbery WR. Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer's disease: possible relation to oxidative stress. J. Neurol. Sci.143, 137–142 (1996).
  • Cuajungco MP, Lees GJ. Zinc metabolism in the brain: relevance to human neurodegenerative disorders. Neurobiol. Dis.4, 137–169 (1997).
  • Atwood CS, Huang X, Moir RD, Tanzi RE, Bush AI. Role of free radicals and metal ions in the pathogenesis of Alzheimer's disease. Met. Ions Biol. Syst.36, 309–364 (1999).
  • Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR. Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci.158, 47–52 (1998).
  • Pajonk FG, Kessler H, Supprian T et al. Cognitive decline correlates with low plasma concentrations of copper in patients with mild to moderate Alzheimer's disease. J. Alzheimers Dis.8, 23–27 (2005).
  • Maynard CJ, Bush AI, Masters CL, Cappai R, Li QX. Metals and amyloid-β in Alzheimer's disease. Int. J. Exp. Pathol.86, 147–159 (2005).
  • Maurer I, Zierz S, Moller HJ. A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients. Neurobiol. Aging.21, 455–462 (2000).
  • Cottrell DA, Blakely EL, Johnson MA, Ince PG, Turnbull DM. Mitochondrial enzyme-deficient hippocampal neurons and choroidal cells in AD. Neurology57, 260–264 (2001).
  • McGeer EG, McGeer PL, Harrop R, Akiyama H, Kamo H. Correlations of regional postmortem enzyme activities with premortem local glucose metabolic rates in Alzheimer's disease. J. Neurosci. Res.27, 612–619 (1990).
  • Connor JR, Tucker P, Johnson M, Snyder B. Ceruloplasmin levels in the human superior temporal gyrus in aging and Alzheimer's disease. Neurosci. Lett.159, 88–90 (1993).
  • Bayer TA, Schafer S, Simons A et al. Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid Aβ production in APP23 transgenic mice. Proc. Natl Acad. Sci. USA100, 14187–14192 (2003).
  • Valko M, Morris H, Cronin MT. Metals, toxicity and oxidative stress. Curr. Med. Chem.12, 1161–1208 (2005).
  • Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science284, 805–808 (1999).
  • Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA. 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease.J. Neurochem.68, 2092–2097 (1997).
  • Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G. Widespread peroxynitrite-mediated damage in Alzheimer's disease. J. Neurosci.17, 2653–2657 (1997).
  • Smith MA, Richey PL, Taneda S et al. Advanced Maillard reaction end products, free radicals, and protein oxidation in Alzheimer's disease. Ann. NY Acad. Sci.738, 447–454 (1994).
  • Smith MA, Harris PL, Sayre LM, Perry G. Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc. Natl Acad. Sci. USA94, 9866–9868 (1997).
  • Smith CD, Carney JM, Starke-Reed PE et al. Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc. Natl Acad. Sci. USA88, 10540–10543 (1991).
  • Perry G, Taddeo MA, Petersen RB et al. Adventiously-bound redox active iron and copper are at the center of oxidative damage in Alzheimer disease. Biometals16, 77–81 (2003).
  • Curtain CC, Ali F, Volitakis I et al. 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 (2001).
  • Atwood CS, Moir RD, Huang X et al. Dramatic aggregation of Alzheimer Aβ by Cu(II) is induced by conditions representing physiological acidosis. J. Biol. Chem.273, 12817–12826 (1998).
  • Atwood CS, Huang X, Khatri A et al. Copper catalyzed oxidation of Alzheimer Aβ. Cell Mol. Biol.46, 777–783 (2000).
  • Dong J, Atwood CS, Anderson VE et al. Metal binding and oxidation of amyloid-β within isolated senile plaque cores: Raman microscopic evidence. Biochemistry42, 2768–2773 (2003).
  • Behl C, Davis JB, Lesley R, Schubert D. Hydrogen peroxide mediates amyloid β protein toxicity. Cell77, 817–827 (1994).
  • Huang X, Atwood CS, Hartshorn MA et al. The Aβ peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry38, 7609–7616 (1999).
  • Galeazzi L, Ronchi P, Franceschi C, Giunta S. In vitro peroxidase oxidation induces stable dimers of β-amyloid (1–42) through dityrosine bridge formation. Amyloid6, 7–13 (1999).
  • Barnham KJ, Haeffner F, Ciccotosto GD et al. Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer's disease β-amyloid. FASEB J.18, 1427–1429 (2004).
  • Atwood CS, Perry G, Zeng H et al. Copper mediates dityrosine cross-linking of Alzheimer's amyloid-b. Biochemistry43, 560–568 (2004).
  • Perry G, Cash AD, Smith MA. Alzheimer disease and oxidative stress. J. Biomed. Biotechnol.2, 120–123 (2002).
  • Kuo YM, Webster S, Emmerling MR, De Lima N, Roher AE. Irreversible dimerization/tetramerization and post-translational modifications inhibit proteolytic degradation of A β peptides of Alzheimer's disease. Biochim. Biophys. Acta1406, 291–298 (1998).
  • Barnham KJ, Ciccotosto GD, Tickler AK et al. Neurotoxic, redox-competent Alzheimer's β-amyloid is released from lipid membrane by methionine oxidation. J. Biol. Chem.278, 42959–42965 (2003).
  • Tickler AK, Smith DG, Ciccotosto GD et al. Methylation of the imidazole side chains of the Alzheimer disease amyloid-β peptide results in abolition of superoxide dismutase-like structures and inhibition of neurotoxicity, J. Biol. Chem.280, 13355–13363 (2005).
  • Ciccotosto GD, Tew DJ, Curtain CC et al. Enhanced toxicity and cellular binding of a modified amyloid β peptide with a methionine to valine substitution, J. Biol. Chem.279, 42528–42534 (2004).
  • Kanski J, Varadarajan S, Aksenova M, Butterfield DA. Role of glycine-33 and methionine-35 in Alzheimer's amyloid β-peptide 1–42-associated oxidative stress and neurotoxicity. Biochim. Biophys. Acta1586, 190–198 (2002).
  • Opazo C, Huang X, Cherny RA et al. Metalloenzyme-like activity of Alzheimer's disease β-amyloid. Cu-dependent catalytic conversion of dopamine, cholesterol, and biological reducing agents to neurotoxic H(2)O(2). J. Biol. Chem.277, 40302–40308 (2002).
  • Crouch PJ, Blake R, Duce JA et al. Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-β1–42. J. Neurosci.25, 672–679 (2005).
  • White AR, Bush AI, Beyreuther K, Masters CL, Cappai R. Exacerbation of copper toxicity in primary neuronal cultures depleted of cellular glutathione.J. Neurochem.72, 2092–2098 (1999).
  • Irizarry MC, Gurol ME, Raju S et al. Association of homocysteine with plasma amyloid β protein in aging and neurodegenerative disease. Neurology65, 1402–1408 (2005).
  • White AR, Huang X, Jobling MF et al. Homocysteine potentiates copper- and amyloid b peptide-mediated toxicity in primary neuronal cultures: possible risk factors in the Alzheimer's-type neurodegenerative pathways.J. Neurochem.76, 1509–1520 (2001).
  • Puglielli L, Friedlich AL, Setchell KD et al. Alzheimer disease β-amyloid activity mimics cholesterol oxidase. J. Clin. Invest.115, 2556–2563 (2005).
  • Murray IV, Sindoni ME, Axelsen PH. Promotion of oxidative lipid membrane damage by amyloid β proteins, Biochemistry44, 12606–12613 (2005).
  • Wasco W, Bupp K, Magendantz M, Gusella JF, Tanzi RE, Solomon F. Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer disease-associated amyloid β protein precursor. Proc. Natl Acad. Sci. USA89, 10758–10762 (1992).
  • Bayer TA, Cappai R, Masters CL, Beyreuther K, Multhaup G. It all sticks together--the APP-related family of proteins and Alzheimer's disease. Mol. Psychiatry4, 524–528 (1999).
  • Barnham KJ, McKinstry WJ, Multhaup G et al. Structure of the Alzheimer's disease amyloid precursor protein copper binding domain. A regulator of neuronal copper homeostasis. J. Biol. Chem.278, 17401–17407 (2003).
  • White AR, Multhaup G, Galatis D et al. Contrasting, species-dependent modulation of copper-mediated neurotoxicity by the Alzheimer's disease amyloid precursor protein. J. Neurosci.22, 365–376 (2002).
  • White AR, Multhaup G, Maher F et al. The Alzheimer's disease amyloid precursor protein modulates copper-induced toxicity and oxidative stress in primary neuronal cultures. J. Neurosci.19, 9170–9179 (1999).
  • Hsiao K, Chapman P, Nilsen S et al. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science274, 99–102 (1996).
  • White AR, Reyes R, Mercer JF et al. Copper levels are increased in the cerebral cortex and liver of APP and APLP2 knockout mice. Brain Res.842, 439–444 (1999).
  • Bellingham SA, Ciccotosto GD, Needham BE et al. Gene knockout of amyloid precursor protein and amyloid precursor-like protein-2 increases cellular copper levels in primary mouse cortical neurons and embryonic fibroblasts.J. Neurochem.91, 423–428 (2004).
  • Hassett R, Kosman DJ. Evidence for Cu(II) reduction as a component of copper uptake bySaccharomyces cerevisiae. J. Biol. Chem.270, 128–134 (1995).
  • Borchardt T, Camakaris J, Cappai R, Masters CL, Beyreuther K, Multhaup G. Copper inhibits β-amyloid production and stimulates the non-amyloidogenic pathway of amyloid-precursor-protein secretion. Biochem. J.344(Pt 2), 461–467 (1999).
  • Phinney AL, Drisaldi B, Schmidt SD et al. In vivo reduction of amyloid-β by a mutant copper transporter. Proc. Natl Acad. Sci. USA100, 14193–14198 (2003).
  • Takeda A. Movement of zinc and its functional significance in the brain. Brain Res. Brain Res. Rev.34, 137–148 (2000).
  • Weiss JH, Sensi SL, Koh JY. Zn(2+): a novel ionic mediator of neural injury in brain disease. Trends Pharmacol. Sci.21, 395–401 (2000).
  • Frederickson CJ, Suh SW, Silva D, Frederickson CJ, Thompson RB. Importance of zinc in the central nervous system: the zinc-containing neuron. J. Nutr.130, S1471–S1483 (2000).
  • Miller LM, Wang Q, Telivala TP, Smith RJ, Lanzirotti A, Miklossy J. Synchrotron-based infrared and X-ray imaging shows focalized accumulation of Cu and Zn co-localized with β-amyloid deposits in Alzheimer's disease. J. Struct. Biol. (2005) (Epub ahead of print).
  • Lee JY, Mook-Jung I, Koh JY. Histochemically reactive zinc in plaques of the Swedish mutant β-amyloid precursor protein transgenic mice. J. Neurosci.19, RC10 (1999).
  • Bush AI. The metallobiology of Alzheimer's disease. Trends Neurosci.26, 207–214 (2003).
  • Liu ST, Howlett G, Barrow CJ. Histidine-13 is a crucial residue in the zinc ion-induced aggregation of the Aβ peptide of Alzheimer's disease. Biochemistry38, 9373–9378 (1999).
  • Lee JY, Cole TB, Palmiter RD, Suh SW, Koh JY. Contribution by synaptic zinc to the gender-disparate plaque formation in human Swedish mutant APP transgenic mice. Proc. Natl Acad. Sci. USA99, 7705–7710 (2002).
  • Friedlich AL, Lee JY, van Groen T et al. Neuronal zinc exchange with the blood vessel wall promotes cerebral amyloid angiopathy in an animal model of Alzheimer's disease. J. Neurosci.24, 3453–3459 (2004).
  • Cuajungco MP, Goldstein LE, Nunomura A et al. Evidence that the β-amyloid plaques of Alzheimer's disease represent the redox-silencing and entombment of Aβ by zinc. J. Biol. Chem.275, 19439–19442 (2000).
  • McLean CA, Cherny RA, Fraser FW et al. Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol.46, 860–866 (1999).
  • Suzuki K, Miura T, Takeuchi H. Inhibitory effect of copper(II) on zinc(II)-induced aggregation of amyloid β-peptide. Biochem. Biophys. Res. Commun.285, 991–996 (2001).
  • Sottrup-Jensen LSO, Kristensen L, Fey GH. The α-macroglobulin bait region. Sequence diversity and localization of cleavage sites for proteinases in five mammalian α-macroglobulins. J. Biol. Chem.264, 15781–15789 (1989).
  • Du Y, Bales KR, Dodel RC et al. α2-macroglobulin attenuates β-amyloid peptide 1–40 fibril formation and associated neurotoxicity of cultured fetal rat cortical neurons. J. Neurochem.70, 1182–1188 (1998).
  • Du Y, Ni B, Glinn M et al. α2-macroglobulin as a β-amyloid peptide-binding plasma protein.J. Neurochem.69, 299–305 (1997).
  • Yu WH, Lukiw WJ, Bergeron C, Niznik HB, Fraser PE. Metallothionein III is reduced in Alzheimer's disease. Brain Res.894, 37–45 (2001).
  • Zambenedetti P, Giordano R, Zatta P. Metallothioneins are highly expressed in astrocytes and microcapillaries in Alzheimer's disease. J. Chem. Neuroanat.15, 21–26 (1998).
  • Carson JA, Turner AJ. β-amyloid catabolism: roles for neprilysin (NEP) and other metallopeptidases?J. Neurochem.81, 1–8 (2002).
  • Das S, Mandal M, Chakraborti T, Mandal A, Chakraborti S. Structure and evolutionary aspects of matrix metalloproteinases: a brief overview. Mol. Cell Biochem.253, 31–40 (2003).
  • Sipe JC, Lee P, Beutler E. Brain iron metabolism and neurodegenerative disorders. Dev. Neurosci.24, 188–196 (2002).
  • White AR, Du T, Laughton KM et al. Masters CL degradation of the Alzhemeimer’s disease amyloid β peptide by metal dependent upregulation of metalloproteases. J. Biol. Chem. (2006) (In press).
  • Connor JR, Menzies SL, Burdo JR, Boyer PJ. Iron and iron management proteins in neurobiology. Pediatr. Neurol.25, 118–129 (2001).
  • Sayre LM, Perry G, Harris PL, Liu Y, Schubert KA, Smith MA. In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer's disease: a central role for bound transition metals.J. Neurochem.74, 270–279 (2000).
  • Beard JL, Connor JR, Jones BC. Iron in the brain. Nutr. Rev.51, 157–170 (1993).
  • Schipper HM. Heme oxygenase-1: role in brain aging and neurodegeneration. Exp. Gerontol.35, 821–830 (2000).
  • Dobson J. On the structural form of iron in ferritin cores associated with progressive supranuclear palsy and Alzheimer's disease. Cell Mol. Biol.47, OL49–OL50 (2001).
  • Kuroda Y, Kawahara M. Aggregation of amyloid β-protein and its neurotoxicity: enhancement by aluminum and other metals. Tohoku J. Exp. Med.174, 263–268 (1994).
  • Rottkamp CA, Raina AK, Zhu X et al. Redox-active iron mediates amyloid-β toxicity. Free Radic. Biol. Med.30, 447–450 (2001).
  • Rogers JT, Randall JD, Cahill CM et al. An iron-responsive element type II in the 5'-untranslated region of the Alzheimer's amyloid precursor protein transcript. J. Biol. Chem.277, 45518–45528 (2002).
  • Cherny RA, Atwood CS, Xilinas ME et al. Treatment with a copper-zinc chelator markedly and rapidly inhibits β-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron.30, 665–676 (2001).
  • Ritchie CW, Bush AI, Mackinnon A et al. Metal-protein attenuation with iodochlorhydroxyquin (clioquinol) targeting Aβ amyloid deposition and toxicity in Alzheimer disease: a pilot Phase 2 clinical trial. Arch. Neurol.60, 1685–1691 (2003).
  • Ritchie CW, Bush AI, Masters CL. Metal-protein attenuating compounds and Alzheimer's disease. Expert Opin. Investig. Drugs13, 1585–1592 (2004).
  • Gaeta A, Hider RC. The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy.Br. J. Pharmacol.146, 1041–1059 (2005).
  • Huang X, Cuajungco MP, Atwood CS et al. Cu(II) potentiation of alzheimer Aβ neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction. J. Biol. Chem.274, 37111–37116 (1999).
  • Cherny RA, Legg JT, McLean CA et al. Aqueous dissolution of Alzheimer's disease Aβ amyloid deposits by biometal depletion. J. Biol. Chem.274, 23223–23228 (1999).
  • Lee JY, Friedman JE, Angel I, Kozak A, Koh JY. The lipophilic metal chelator DP-109 reduces amyloid pathology in brains of human β-amyloid precursor protein transgenic mice. Neurobiol. Aging25, 1315–1321 (2004).
  • Dominguez DI, De Strooper B. Novel therapeutic strategies provide the real test for the amyloid hypothesis of Alzheimer's disease. Trends Pharmacol. Sci.23, 324–330 (2002).
  • Crapper McLachlan DR, Dalton AJ, Kruck TP et al. Intramuscular desferrioxamine in patients with Alzheimer's disease. Lancet337, 1304–1308 (1991).
  • Liu G, Garrett MR, Men P, Zhu X, Perry G, Smith MA. Nanoparticle and other metal chelation therapeutics in Alzheimer disease. Biochim. Biophys. Acta.1741, 246–252 (2005).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.