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Expert Review of Neurotherapeutics Volume 9, 2009 - Issue 5
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Review

Calcium dyshomeostasis and neurotoxicity of Alzheimer’s β-amyloid protein

Masahiro Kawahara Department of Analytical Chemistry, School of Pharmaceutical Sciences, Kyushu University of Health and Welfare, 1714-1 Yoshino-cho, Nobeoka-shi, Miyazaki 882-8508, Japan. [email protected]
,
Midori Negishi-Kato Institute of Industrial Science (IIS), The University of Tokyo, 4-6-1 Komaba, Meguro-ku, Tokyo 153-8904, Japan
&
Yutaka Sadakane Department of Analytical Chemistry, School of Pharmaceutical Sciences, Kyushu University of Health and Welfare, 1714-1 Yoshino-cho, Nobeoka-shi, Miyazaki 882-8508, Japan
Pages 681-693 | Published online: 09 Jan 2014

References

  • Selkoe DJ. The molecular pathology of Alzheimer disease. Neuron6, 487–498 (1991).
  • Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science297, 353–356 (2002).
  • Wirths O, Multhaup G, Bayer TA. A modified β-amyloid hypothesis: intraneuronal accumulation of the β-amyloid peptide – the first step of a fatal cascade. J. Neurochem.91, 513–520 (2004).
  • Selkoe DJ. Soluble oligomers of the amyloid β-protein impair synaptic plasticity and behavior. Behav. Brain Res.192, 106–113 (2008).
  • Green KN, LaFerla FM. Linking calcium to Aβ and Alzheimer’s disease. Neuron59, 190–194 (2008).
  • Mattson MP, Chan SL. Neuronal and glial calcium signaling in Alzheimer’s disease. Cell Calcium.34, 385–397 (2003).
  • Arispe N, Diaz JC, Simakova O. Aβ ion channels. Prospects for treating Alzheimer’s disease with Aβ channel blockers. Biochim. Biophys. Acta.1768, 1952–1965 (2007).
  • Kawahara M. Disruption of calcium homeostasis in the pathogenesis of Alzheimer’s disease and other conformational diseases. Curr. Alzheimer Res.1, 87–95 (2004).
  • Lal R, Lin H, Quist AP. Amyloid β ion channel: 3D structure and relevance to amyloid channel paradigm. Biochim. Biophys. Acta.1768, 1966–1975 (2007).
  • Goate A, Chartier-Harlin MC, Mullan M, et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer’s disease. Nature349, 704–706 (1991).
  • 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).
  • Selkoe DJ, Wolfe MS. Presenilin: running with scissors in the membrane. Cell131, 215–221 (2007).
  • Yankner BA, Duffy LK, Kirschner DA. Neurotropic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides. Nature250, 279–282 (1990).
  • Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW. In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res.563, 311–314 (1991).
  • Simmons LK, May PC, Tomaselli KJ et al. Secondary structure of amyloid β peptide correlates with neurotoxic activity in vitro. Mol. Pharmacol.45, 373–379 (1994).
  • Jarrett JT, Lansbury PT Jr. Seeding “one-dimensional crystallization” of amyloid: a pathogenic mechanism in Alzheimer’s disease and scrapie? Cell73, 1055–1058 (1993).
  • Scheuner D, Eckman C, Jensen M et al. Secreted amyloid β-protein similar to that in the senile plaques of Alzheimer’s disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer’s disease. Nat. Med.2, 864–870 (1996).
  • Dickson DW, Crystal HA, Bevona C, Honer W, Vincent I, Davies P. Correlations of synaptic and pathological markers with cognition of the elderly. Neurobiol. Aging16, 285–298 (1995).
  • Terry RD, Masliah E, Salmon DP et al. Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol.30, 572–580 (1991).
  • Fukuyama R, Mizuno T, Mori S, Nakajima K, Fushiki S, Yanagisawa K. Age-dependent change in the levels of Aβ40 and Aβ42 in cerebrospinal fluid from control subjects, and a decrease in the ratio of Aβ42 to Aβ40 level in cerebrospinal fluid from Alzheimer’s disease patients. Eur. Neurol.43, 155–160 (2000).
  • Shirotani K, Tsubuki S, Iwata N et al. Neprilysin degrades both amyloid β peptides 1–40 and 1–42 most rapidly and efficiently among thiorphan- and phosphoramidon-sensitive endopeptidases. J. Biol. Chem.276, 21895–21901 (2001).
  • Walsh DM, Tseng BP, Rydel RE, Podlisny MB, Selkoe DJ. The oligomerization of amyloid β-protein begins intracellularly in cells derived from human brain. Biochemistry39, 10831–10839 (2000).
  • Lambert MP, Barlow AK, Chromy BA et al. Diffusible, nonfibrillar ligands derived from Aβ1–42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA95, 6448–6453 (1998).
  • Gellermann GP, Byrnes H, Striebinger A et al. Aβ-globulomers are formed independently of the fibril pathway. Neurobiol. Dis.30, 212–220 (2008).
  • Harper JD, Wong SS, Lieber CM, Lansbury PT. Observation of metastable Aβ amyloid protofibrils by atomic force microscopy. Chem. Biol.4, 119–125 (1997).
  • Roychaudhuri R, Yang M, Hoshi MM, Teplow DB. Amyloid β-protein assembly and Alzheimer disease. J. Biol. Chem.284, 4749–4753 (2009).
  • Hartley DM, Walsh DM, Ye CP et al. Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci.19, 8876–8884 (1999).
  • Chromy BA, Nowak RJ, Lambert MP et al. Self-assembly of Aβ1–42 into globular neurotoxins. Biochemistry42, 12749–12760 (2003).
  • Lassmann H, Fischer P, Jellinger K. Synaptic pathology of Alzheimer’s disease. Ann. NY Acad. Sci.695, 59–64 (1993).
  • Walsh DM, Klyubin I, Fadeeva JV et al. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature416, 483–484 (2002).
  • Walsh DM, Selkoe DJ. Aβ oligomers – a decade of discovery. J. Neurochem.101, 1172–1184 (2007).
  • Lacor PN, Buniel MC, Chang L et al. Synaptic targeting by Alzheimer’s-related amyloid β oligomers. J. Neurosci.24, 10191–10200 (2004).
  • Lacor PN, Buniel MC, Furlow PW et al. Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer’s disease. J. Neurosci.27, 796–807 (2007).
  • Ishibashi K, Tomiyama T, Nishitsuji K, Hara M, Mori H. Absence of synaptophysin near cortical neurons containing oligomer Aβ in Alzheimer’s disease brain. J. Neurosci. Res.84, 632–636 (2006).
  • Tomiyama T, Nagata T, Shimada H et al. A new amyloid b variant favoring oligomerization in Alzheimer’s-type dementia. Ann. Neurol.63, 377–387 (2008).
  • Small DH, Mok SS, Bornstein JC. Alzheimer’s disease and Aβ toxicity: from top to bottom. Nat. Rev. Neurosci.2, 595–598 (2001).
  • Zipfel GJ, Babcock DJ, Lee JM, Choi DW. Neuronal apoptosis after CNS injury: the roles of glutamate and calcium. J. Neurotrauma.17, 857–869 (2000).
  • Raynaud F, Marcilhac A. Implication of calpain in neuronal apoptosis. A possible regulation of Alzheimer’s disease. FEBS J.273, 3437–3443 (2006).
  • Gordon-Krajcer W, Gajkowska B.Excitotoxicity-induced expression of amyloid precursor protein (β-APP) in the hippocampus and cortex of rat brain. an electron-microscopy and biochemical study. Folia Neuropathol.39, 163–173 (2001).
  • Gasparini L, Racchi M, Binetti G et al. Peripheral markers in testing pathophysiological hypotheses and diagnosing Alzheimer’s disease. FASEB J.12, 17–34 (1998).
  • Herms J, Schneider I, Dewachter I, Caluwaerts N, Kretzschmar H, Van Leuven F. Capacitive calcium entry is directly attenuated by mutant presenilin-1, independent of the expression of the amyloid precursor protein. J. Biol. Chem.278, 2484–2489 (2003).
  • Mattson MP, Guo Q, Furukawa K, Pedersen WA. Presenilins, the endoplasmic reticulum, and neuronal apoptosis in Alzheimer’s disease. J. Neurochem.70, 1–14 (1998).
  • Green KN, Demuro A, Akbari Y et al. SERCA pump activity is physiologically regulated by presenilin and regulates amyloid β production. J. Cell Biol.181, 1107–1116 (2008).
  • Mattson MP, Barger SW, Cheng B, Lieberburg I, Smith-Swintosky VL, Rydel RE. β-amyloid precursor protein metabolites and loss of neuronal Ca2+ homeostasis in Alzheimer’s disease. Trends Neurosci.16, 409–414 (1993).
  • Hartmann H, Eckert A, Müller WE. Disturbances of the neuronal calcium homeostasis in the aging nervous system. Life Sci.55, 2011–2018 (1994).
  • Kato-Negishi M, Muramoto K, Kawahara M, Hosoda R, Kuroda Y, Ichikawa M. Bicuculline induces synapse formation on primary cultured accessory olfactory bulb neurons. Eur. J. Neurosci.18, 1343–1352 (2003).
  • Sabo SL, Ikin AF, Buxbaum JD, Greengard P. The amyloid precursor protein and its regulatory protein, FE65, in growth cones and synapses in vitro and in vivo. J. Neurosci.23, 5407–5415 (2003).
  • Chin JH, Tse FW, Harris K, Jhamandas JH. β-amyloid enhances intracellular calcium rises mediated by repeated activation of intracellular calcium stores and nicotinic receptors in acutely dissociated rat basal forebrain neurons. Brain Cell Biol.35, 173–186 (2006).
  • Arispe N, Rojas E, Pollard HB. Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl Acad. Sci. USA90, 567–571 (1993).
  • Arispe N, Rojas E, Pollard HB. Giant multilevel cation channels formed by Alzheimer disease amyloid β protein [AβP-1–40] in bilayer membranes. Proc. Natl Acad. Sci. USA90, 10573–10577 (1993).
  • Arispe N, Pollard HB, Rojas E. Zn2+ interactions with Alzheimer’s amyloid β protein calcium channels. Proc. Natl Acad. Sci. USA93, 1710–1715 (1996).
  • Arispe N, Diaz JC, Flora M. Efficiency of histidine-associating compounds for blocking the alzheimer’s Aβ channel activity and cytotoxicity. Biophys J.95, 4879–4889 (2008).
  • Mirzabekov T, Lin MC, Yuan WL et al. Channel formation in planar lipid bilayers by a neurotoxic fragment of the β-amyloid peptide. Biochem. Biophys. Res. Commun.202, 1142–1148 (1994).
  • Hirakura Y, Lin MC, Kagan BL. Alzheimer amyloid Aβ1–42 channels: effects of solvent, pH, and Congo Red. J. Neurosci. Res.57, 458–466 (1999).
  • Fraser SP, Suh YH, Chong YH, Djamgoz MB. Membrane currents induced in Xenopus oocytes by the C-terminal fragment of the β-amyloid precursor protein. J. Neurochem.66, 2034–2040 (1996).
  • Mattson MP, Begley JG, Mark RJ, Furukawa K. Aβ25–35 induces rapid lysis of red blood cells: contrast with Aβ1–42 and examination of underlying mechanisms. Brain Res.771, 147–153 (1997).
  • McLaurin J, Chakrabartty A. Membrane disruption by Alzheimer β-amyloid peptides mediated through specific binding to either phospholipids or gangliosides. Implications for neurotoxicity. J. Biol. Chem.271, 26482–26489 (1996).
  • Blanc EM, Toborek M, Mark RJ, Hennig B, Mattson MP. Amyloid β-peptide induces cell monolayer albumin permeability, impairs glucose transport, and induces apoptosis in vascular endothelial cells. J. Neurochem.68, 1870–1881 (1997).
  • Müller WE, Eckert GP, Scheuer K, Cairns NJ, Maras A, Gattaz WF. Effects of β-amyloid peptides on the fluidity of membranes from frontal and parietal lobes of human brain. High potencies of Aβ1–42 and Aβ1–43. Amyloid5, 10–15 (1998).
  • Valincius G, Heinrich F, Budvytyte R et al. Soluble amyloid β-oligomers affect dielectric membrane properties by bilayer insertion and domain formation: implications for cell toxicity. Biophys. J.95, 4845–4861 (2008).
  • Kayed R, Sokolov Y, Edmonds B et al. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem.279, 46363–46366 (2004).
  • Rhee SK, Quist AP, Lal R. amyloid β protein-1–42 forms calcium-permeable, Zn2+-sensitive channel. J. Biol. Chem.273, 13379–13382 (1998).
  • Durell SR, Guy HR, Arispe N, Rojas E, Pollard HB. Theoretical models of the ion channel structure of amyloid β-protein. Biophys. J.67, 2137–2145 (1994).
  • Mellon PL, Windle JJ, Goldsmith PC, Padula JL, Weiner RI. Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron5, 1–10 (1990).
  • Kawahara M, Arispe N, Kuroda Y, Rojas E. Alzheimer’s disease amyloid β-protein forms Zn2+-sensitive, cation-selective channels across excised membrane patches from hypothalamic neurons. Biophys. J.73, 67–75 (1997).
  • Kawahara M, Arispe N, Kuroda Y, Rojas E. Alzheimer’s β-amyloid, human islet amylin and prion protein fragment evoke intracellular free-calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell-line. J. Biol. Chem.275, 14077–14083 (2000).
  • Kawahara M, Kuroda Y. Molecular mechanism of neurodegeneration induced by Alzheimer’s β-amyloid protein: channel formation and disruption of calcium homeostasis. Brain Res. Bull.53, 389–397 (2000).
  • Kawahara M, Kuroda Y. Intracellular calcium changes in neuronal cells induced by Alzheimer’s β-amyloid protein are blocked by estradiol and cholesterol. Cell. Mol. Neurobio.21, 1–13 (2001).
  • Kato-Negishi M, Kawahara M. Neurosteroids block the increase in intracellular calcium level induced by Alzheimer’s β-amyloid protein in long-term cultured rat hippocampal neurons. Neuropsy. Dis. Treat.4, 209–218 (2008).
  • Bechinger B. Structure and functions of channel-forming peptides: magainins, cecropins, melittin and alamethicin. J. Membr. Biol.156, 197–211 (1997).
  • Tomita T, Watanabe M, Yasuda T. Influence of membrane fluidity on the assembly of Staphylococcus aureus α-toxin, a channel-forming protein, in liposome membrane. J. Biol. Chem.267, 13391–13397 (1992).
  • Eckert GP, Cairns NJ, Maras A, Gattaz WF, Muller WE. Cholesterol modulates the membrane-disordering effects of β-amyloid peptides in the hippocampus: specific changes in Alzheimer’s disease. Dement. Geriatr. Cogn. Disord.11, 181–186 (2000).
  • Bhakdi S, Tranum-Jensen J. α-toxin of Staphylococcus aureus. Microbiol. Rev.55, 733–751 (1991).
  • Imura Y, Choda N, Matsuzaki K. Magainin 2 in action: distinct modes of membrane permeabilization in living bacterial and mammalian cell. Biophys. J.95(12), 5757–5765 (2008).
  • Carrell RW, Lomas DA. Conformational disease. Lancet350, 134–138 (1997).
  • Prusiner SB. Prions. Proc. Natl Acad. Sci. USA95, 13363–13383 (1998).
  • Forloni G, Angeretti N, Chiesa R et al. Neurotoxicity of a prion protein fragment. Nature362, 543–546 (1993).
  • Ikeda H, Yamaguchi M, Sugai S, Aze Y, Narumiya S, Kakizuka A. Expanded polyglutamine in the Machado-Joseph disease protein induces cell death in vitro and in vivo. Nat. Genet.13, 196–202 (1996).
  • Kaplan B, Ratner V, Haas E. α-synuclein: its biological function and role in neurodegenerative diseases. J. Mol. Neurosci.20, 83–92 (2003).
  • el-Agnaf OM, Irvine GB. Aggregation and neurotoxicity of α-synuclein and related peptides. Biochem. Soc. Trans.30, 559–565 (2002).
  • Srinivasan R, Marchant RE, Zagorski MG. ABri peptide associated with familial British dementia forms annular and ring-like protofibrillar structures. Amyloid11, 10–13 (2004).
  • Lin MC, Mirzabekov T, Kagan BL. Channel formation by a neurotoxic prion protein fragment. J. Biol. Chem.272, 44–47 (1997).
  • Kourie JI, Culverson A. Prion peptide fragment PrP[106–126] forms distinct cation channel types. J. Neurosci. Res.62, 120–133 (2000).
  • Hirakura Y, Azimov R, Azimova R, Kagan BL. Polyglutamine-induced ion channels: a possible mechanism for the neurotoxicity of Huntington and other CAG repeat diseases. J. Neurosci. Res.60, 490–494 (2000).
  • Lashuel HA, Hartley D, Petre BM, Walz T, Lansbury PT Jr. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature418, 291 (2002).
  • May PC, Boggs LN, Fuson KS. Neurotoxicity of human amylin in rat primary hippocampal cultures: similarity to Alzheimer’s disease Amyloid-β neurotoxicity. J. Neurochem.61, 2330–2333 (1993).
  • Mirzabekov TA, Lin MC, Kagan BL. Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem.271, 1988–1992 (1996).
  • Quist A, Doudevski I, Lin H et al. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc. Natl Acad. Sci. USA102, 10427–10432 (2005).
  • Danzer KM, Haasen D, Karow AR et al. Different species of α-synuclein oligomers induce calcium influx and seeding. J. Neurosci.27, 9220–9232 (2007).
  • Tomiyama T, Asano S, Suwa Y et al. Rifampicin prevents the aggregation and neurotoxicity of amyloid β protein in vitro. Biochem. Biophys. Res. Commun.204, 76–83 (1994).
  • Ono K, Hasegawa K, Naiki H, Yamada M. Curcumin has potent anti-amyloidogenic effects for Alzheimer’s β-amyloid fibrils in vitro. J. Neurosci. Res.75(6), 742–750 (2004).
  • Thomas T, Nadackal TG, Thomas K. Aspirin and non-steroidal anti-inflammatory drugs inhibit Amyloid-β aggregation. Neuroreport12, 3263–3267 (2001).
  • Kawahara M. Effects of aluminum on the nervous system and its possible link with neurodegenerative diseases. J. Alzheimer Dis.8, 171–182 (2005).
  • Bush AI. Copper, zinc, and the metallobiology of Alzheimer disease. Alzheimer Dis. Assoc. Disord.17(3), 147–150 (2003).
  • Cuajungco MP, Fagét 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).
  • Bolognin S, Zatta P, Drago D, Parnigotto PP, Ricchelli F, Tognon G. Mutual stimulation of β-amyloid fibrillogenesis by clioquinol and divalent metals. Neuromolecular Med.10, 322–332 (2008).
  • Schäfer S, Pajonk FG, Multhaup G, Bayer TA. Copper and clioquinol treatment in young APP transgenic and wild-type mice: effects on life expectancy, body weight, and metal-ion levels. J. Mol. Med.85, 405–413 (2007).
  • Kawahara M, Konoha K, Sadakane Y. Neurotoxicity of zinc: the involvement of calcium homeostasis and carnosine. Biomed. Res. Trace Elements18, 26–34 (2007).
  • Wisniewski T, Konietzko U. Amyloid-β immunisation for Alzheimer’s disease. Lancet Neurol.7(9), 805–811 (2008).
  • 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(5S Suppl.), 1471S–1483S (2000).
  • Hertel C, Terzi E, Hauser N, Jakob-Rotne R, Seelig J, Kemp JA. Inhibition of the electrostatic interaction between β-amyloid peptide and membranes prevents β-amyloid-induced toxicity. Proc. Natl Acad. Sci. USA94, 9412–9416 (1997).
  • Seelig J, Lehrmann R, Terzi E. Domain formation induced by lipid–ion and lipid–peptide interactions. Mol. Membr. Biol.12, 51–57 (1995).
  • Hartmann H, Eckert A, Muller WE. Apolipoprotein E and cholesterol affect neuronal calcium signalling: the possible relationship to β-amyloid neurotoxicity. Biochem. Biophys. Res. Commun.200, 1185–1192 (1994).
  • Corder EH, Saunders AM, Strittmatter WJ et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science261, 921–923 (1993).
  • Schwartz Z, Gates PA, Nasatzky E, et al. Effect of 17β-estradiol on chondrocyte membrane fluidity and phospholipid metabolism is membrane-specific, sex-specific, and cell maturation-dependent. Biochim. Biophys. Acta.1282, 1–10 (1996).
  • Arispe N, Doh M. Plasma membrane cholesterol controls the cytotoxicity of Alzheimer’s disease AβP1–40 and 1–42 peptides. FASEB J.16, 1526–1536 (2002).
  • Nilsen J, Chen S, Irwin RW, Iwamoto S, Brinton RD. Estrogen protects neuronal cells from amyloid β-induced apoptosis via regulation of mitochondrial proteins and function. BMC Neurosci.7, 74–85 (2006).
  • Tsutsui K, Ukena K, Usui M, et al. Novel brain function: biosynthesis and actions of neurosteroids in neurons. Neurosci. Res.36, 261–273 (2000).
  • Charalampopoulos I, Alexaki VI, Tsatsanis C et al. Neurosteroids as endogenous inhibitors of neuronal cell apoptosis in aging. Ann. NY Acad. Sci.1088, 139–152 (2006).
  • Hillen T, Lun A, Reischies FM, et al. DHEA-S plasma levels and incidence of Alzheimer’s disease. Biol. Psychiatry47, 161–163 (2000).
  • Huppert FA, Van Niekerk JK, Herbert J. Dehydroepiandrosterone (DHEA) supplementation for cognition and well-being. Cochrane. Database Syst. Rev.2, CD000304 (2000).
  • Markou A, Duka T, Prelevic GM.Estrogens and brain function. Hormones (Athens)4, 9–17 (2005).

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