Advertisement

BioMetals

, Volume 27, Issue 2, pp 371–388 | Cite as

Heavy metals toxicity: effect of cadmium ions on amyloid beta protein 1–42. Possible implications for Alzheimer’s disease

  • Gabriella Notarachille
  • Fabio Arnesano
  • Vincenza Calò
  • Daniela MeleleoEmail author
Article

Abstract

Cadmium (Cd) is an environmental contaminant, highly toxic to humans. This biologically non-essential element accumulates in the body, especially in the kidney, liver, lung and brain and can induce several toxic effects, depending on the concentration and the exposure time. Cd has been linked to Alzheimer’s disease (AD) as a probable risk factor, as it shows higher concentrations in brain tissues of AD patients than in healthy people, its implication in the formation of neurofibrillary tangles and in the aggregation process of amyloid beta peptides (AβPs). AβPs seem to have toxic properties, particularly in their aggregated state; insoluble AβP forms, such as small and large aggregates, protofibrils and fibrils, appear to be implicated in the pathogenesis of AD. In our study, we have evaluated the effect of Cd, at different concentrations, both on the AβP1–42 ion channel incorporated in a planar lipid membrane made up of phosphatidylcholine containing 30 % cholesterol and on the secondary structure of AβP1–42 in aqueous environment. Cadmium is able to interact with the AβP1–42 peptide by acting on the channel incorporated into the membrane as well as on the peptide in solution, both decreasing AβP1–42 channel frequency and in solution forming large and amorphous aggregates prone to precipitate. These experimental observations suggesting a toxic role for Cd strengthen the hypothesis that Cd may interact directly with AβPs and may be a risk factor in AD.

Keywords

Cadmium AβP Aggregation Ion channel Membranes 

Notes

Acknowledgments

This work was supported by a grant from the Fondazione Cassa di Risparmio di Puglia. The authors acknowledge Anthony Green for proofreading and providing linguistic advice.

References

  1. Abramov AY, Ionov M, Pavlov E, Duchen MR (2011) Membrane cholesterol content plays a key role in the neurotoxicity of β-amyloid: implications for Alzheimer’s disease. Aging Cell 10:595–603PubMedGoogle Scholar
  2. Alberdi E, Sánchez-Gómez MV, Cavaliere F, Pérez-Samartín A, Zugaza JL, Trullas R, Domercq M, Matute C (2010) Amyloid beta oligomers induce Ca2+ dysregulation and neuronal death through activation of ionotropic glutamate receptors. Cell Calcium 47:264–272PubMedGoogle Scholar
  3. Arispe N, Pollard H, Rojas E (1993a) Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein [A beta P-(1-40)] in bilayer membranes. Proc Natl Acad Sci USA 90:10573–10577PubMedCentralPubMedGoogle Scholar
  4. Arispe N, Rojas E, Pollard H (1993b) Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc Natl Acad Sci USA 90:567–571PubMedCentralPubMedGoogle Scholar
  5. Arispe N, Pollard H, Rojas E (1996) Zn2+ interaction with Alzheimer amyloid beta protein calcium channels. Proc Natl Acad Sci USA 93:1710–1715PubMedCentralPubMedGoogle Scholar
  6. Ashley R, Harroun T, Hauss T, Breen K, Bradshaw J (2006) Autoinsertion of soluble oligomers of Alzheimer’s Abeta(1-42) peptide into cholesterol-containing membranes is accompanied by relocation of the sterol towards the bilayer surface. BMC Struct Biol 6:21PubMedCentralPubMedGoogle Scholar
  7. Basun H, Forssell L, Wetterberg L, Winblad B (1991) Metals and trace elements in plasma and cerebrospinal fluid in normal aging and Alzheimer’s disease. J Neural Transm Park Dis Dement Sect 3:231–258PubMedGoogle Scholar
  8. Bitan G, Fradinger EA, Spring SM, Teplow DB (2005) Neurotoxic protein oligomers—what you see is not always what you get. Amyloid 12:88–95PubMedGoogle Scholar
  9. Bocharova OV, Breydo L, Salnikov VV, Baskakov IV (2005) Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44:6776–6787PubMedGoogle Scholar
  10. Bolognin S, Messori L, Drago D, Gabbiani C, Cendron L, Zatta P (2011) Aluminum, copper, iron and zinc differentially alter amyloid-Aβ(1-42) aggregation and toxicity. Int J Biochem Cell Biol 43:877–885PubMedGoogle Scholar
  11. Bravard A, Vacher M, Gouget B, Coutant A, de Boisferon FH, Marsin S, Chevillard S, Radicella JP (2006) Redox regulation of human OGG1 activity in response to cellular oxidative stress. Mol Cell Biol 26:7430–7436PubMedCentralPubMedGoogle Scholar
  12. Bush A (2000) Metals and neuroscience. Curr Opin Chem Biol 4:184–191PubMedGoogle Scholar
  13. Bush A (2003) The metallobiology of Alzheimer’s disease. Trends Neurosci 26:207–214PubMedGoogle Scholar
  14. Caughey B, Lansbury PT (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 26:267–298PubMedGoogle Scholar
  15. Chauhan V, Chauhan A (2006) Oxidative stress in Alzheimer’s disease. Pathophysiology 13:195–208PubMedGoogle Scholar
  16. Chen WT, Liao YH, Yu HM, Cheng IH, Chen YR (2011) Distinct effects of Zn2+, Cu2+, Fe3+, and Al3+ on amyloid-beta stability, oligomerization, and aggregation: amyloid-beta destabilization promotes annular protofibril formation. J Biol Chem 286:9646–9656PubMedCentralPubMedGoogle Scholar
  17. Davis CH, Berkowitz ML (2010) A molecular dynamics study of the early stages of amyloid-beta(1-42) oligomerization: the role of lipid membranes. Proteins 78:2533–2545PubMedCentralPubMedGoogle Scholar
  18. De Felice FG, Velasco PT, Lambert MP, Viola K, Fernandez SJ, Ferreira ST, Klein WL (2007) Abeta oligomers induce neuronal oxidative stress through an N-methyl-d-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J Biol Chem 282:11590–11601PubMedGoogle Scholar
  19. Di Carlo M (2010) Beta amyloid peptide: from different aggregation forms to the activation of different biochemical pathways. Eur Biophys J 39:877–888PubMedGoogle Scholar
  20. Di Paolo G, Kim TW (2011) Linking lipids to Alzheimer’s disease: cholesterol and beyond. Nat Rev Neurosci 12:284–296PubMedCentralPubMedGoogle Scholar
  21. Drago D, Bettella M, Bolognin S, Cendron L, Scancar J, Milacic R, Ricchelli F, Casini A, Messori L, Tognon G et al (2008) Potential pathogenic role of beta-amyloid(1-42)-aluminum complex in Alzheimer’s disease. Int J Biochem Cell Biol 40:731–746PubMedGoogle Scholar
  22. Durell S, Guy H, Arispe N, Rojas E, Pollard H (1994) Theoretical models of the ion channel structure of amyloid beta-protein. Biophys J 67:2137–2145PubMedCentralPubMedGoogle Scholar
  23. Fahim MA, Nemmar A, Dhanasekaran S, Singh S, Shafiullah M, Yasin J, Zia S, Hasan MY (2012) Acute cadmium exposure causes systemic and thromboembolic events in mice. Physiol Res 61:73–80PubMedGoogle Scholar
  24. Gallucci E, Meleleo D, Micelli S, Picciarelli V (2003) Magainin 2 channel formation in planar lipid membranes: the role of lipid polar groups and ergosterol. Eur Biophys J 32:22–32PubMedGoogle Scholar
  25. Gennis RB (1989) Biomembranes: molecular structure and function. Springer, New YorkGoogle Scholar
  26. Glabe CG (2006) Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol Aging 27:570–575PubMedGoogle Scholar
  27. Gonçalves JF, Fiorenza AM, Spanevello RM, Mazzanti CM, Bochi GV, Antes FG, Stefanello N, Rubin MA, Dressler VL, Morsch VM et al (2010) N-acetylcysteine prevents memory deficits, the decrease in acetylcholinesterase activity and oxidative stress in rats exposed to cadmium. Chem Biol Interact 186:53–60PubMedGoogle Scholar
  28. Gonçalves JF, Nicoloso FT, da Costa P, Farias JG, Carvalho FB, da Rosa MM, Gutierres JM, Abdalla FH, Pereira JS, Dias GR et al (2012) Behavior and brain enzymatic changes after long-term intoxication with cadmium salt or contaminated potatoes. Food Chem Toxicol 50:3709–3718PubMedGoogle Scholar
  29. Ha C, Ryu J, Park CB (2007) Metal ions differentially influence the aggregation and deposition of Alzheimer’s beta-amyloid on a solid template. Biochemistry 46:6118–6125PubMedGoogle Scholar
  30. Haass C, Selkoe DJ (1993) Cellular processing of beta-amyloid precursor protein and the genesis of amyloid beta-peptide. Cell 75:1039–1042PubMedGoogle Scholar
  31. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297:353–356PubMedGoogle Scholar
  32. Hertel C, Terzi E, Hauser N, Jakob-Rotne R, Seelig J, Kemp JA (1997) Inhibition of the electrostatic interaction between beta-amyloid peptide and membranes prevents beta-amyloid-induced toxicity. Proc Natl Acad Sci USA 94:9412–9416PubMedCentralPubMedGoogle Scholar
  33. Hirakura Y, Lin M, Kagan B (1999) Alzheimer amyloid abeta1-42 channels: effects of solvent, pH, and Congo Red. J Neurosci Res 57:458–466PubMedGoogle Scholar
  34. Hotz P, Buchet JP, Bernard A, Lison D, Lauwerys R (1999) Renal effects of low-level environmental cadmium exposure: 5-year follow-up of a subcohort from the Cadmibel study. Lancet 354:1508–1513PubMedGoogle Scholar
  35. Im JY, Paik SG, Han PL (2006) Cadmium-induced astroglial death proceeds via glutathione depletion. J Neurosci Res 83:301–308PubMedGoogle Scholar
  36. Iwatsubo T, Odaka A, Suzuki N, Mizusawa H, Nukina N, Ihara Y (1994) Visualization of A beta 42(43) and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43). Neuron 13:45–53PubMedGoogle Scholar
  37. Jarrett JT, Berger EP, Lansbury PT (1993) The C-terminus of the beta protein is critical in amyloidogenesis. Ann N Y Acad Sci 695:144–148PubMedGoogle Scholar
  38. Jiang LF, Yao TM, Zhu ZL, Wang C, Ji LN (2007) Impacts of Cd(II) on the conformation and self-aggregation of Alzheimer’s tau fragment corresponding to the third repeat of microtubule-binding domain. Biochim Biophys Acta 1774:1414–1421PubMedGoogle Scholar
  39. Jin T, Lu J, Nordberg M (1998) Toxicokinetics and biochemistry of cadmium with special emphasis on the role of metallothionein. Neurotoxicology 19:529–535PubMedGoogle Scholar
  40. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87PubMedGoogle Scholar
  41. Jones MM, Cherian MG (1990) The search for chelate antagonists for chronic cadmium intoxication. Toxicology 62:1–25PubMedGoogle Scholar
  42. Kakio A, Nishimoto S, Kozutsumi Y, Matsuzaki K (2003) Formation of a membrane-active form of amyloid beta-protein in raft-like model membranes. Biochem Biophys Res Commun 303:514–518PubMedGoogle Scholar
  43. Kataranovski M, Janković S, Kataranovski D, Stosić J, Bogojević D (2009) Gender differences in acute cadmium-induced systemic inflammation in rats. Biomed Environ Sci 22:1–7PubMedGoogle Scholar
  44. Karimi MM, Jafari Sani M, Mahmudabadi AZ, Jafari Sani A, and Kathibi, RS (2012) Effect of acute toxicity of cadmium in mice kidney cells. Iran J Toxicol 6Google Scholar
  45. Kayed R, Head E, Thompson J, McIntire T, Milton S, Cotman C, Glabe C (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486–489PubMedGoogle Scholar
  46. Kayed R, Sokolov Y, Edmonds B, McIntire T, Milton S, Hall J, Glabe C (2004) Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J Biol Chem 279:46363–46366PubMedGoogle Scholar
  47. Kirkitadze MD, Condron MM, Teplow DB (2001) Identification and characterization of key kinetic intermediates in amyloid beta-protein fibrillogenesis. J Mol Biol 312:1103–1119PubMedGoogle Scholar
  48. Klement K, Wieligmann K, Meinhardt J, Hortschansky P, Richter W, Fändrich M (2007) Effect of different salt ions on the propensity of aggregation and on the structure of Alzheimer’s abeta(1-40) amyloid fibrils. J Mol Biol 373:1321–1333PubMedGoogle Scholar
  49. Kuperstein I, Broersen K, Benilova I, Rozenski J, Jonckheere W, Debulpaep M, Vandersteen A, Segers-Nolten I, Van Der Werf K, Subramaniam V et al (2010) Neurotoxicity of Alzheimer’s disease Aβ peptides is induced by small changes in the Aβ42 to Aβ40 ratio. EMBO J 29:3408–3420PubMedCentralPubMedGoogle Scholar
  50. Lafuente A, Esquifino AI (1999) Cadmium effects on hypothalamic activity and pituitary hormone secretion in the male. Toxicol Lett 110:209–218PubMedGoogle Scholar
  51. Lesné S, Koh M, Kotilinek L, Kayed R, Glabe C, Yang A, Gallagher M, Ashe K (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352–357PubMedGoogle Scholar
  52. Lesné S, Kotilinek L, Ashe KH (2008) Plaque-bearing mice with reduced levels of oligomeric amyloid-beta assemblies have intact memory function. Neuroscience 151:745–749PubMedCentralPubMedGoogle Scholar
  53. Li X, Lv Y, Yu S, Zhao H, Yao L (2012) The effect of cadmium on Aβ levels in APP/PS1 transgenic mice. Exp Ther Med 4:125–130PubMedCentralPubMedGoogle Scholar
  54. Lin H, Bhatia R, Lal R (2001) Amyloid beta protein forms ion channels: implications for Alzheimer’s disease pathophysiology. FASEB J 15:2433–2444PubMedGoogle Scholar
  55. López E, Arce C, Oset-Gasque MJ, Cañadas S, González MP (2006) Cadmium induces reactive oxygen species generation and lipid peroxidation in cortical neurons in culture. Free Radic Biol Med 40:940–951PubMedGoogle Scholar
  56. Lovell M, Robertson J, Teesdale W, Campbell J, Markesbery W (1998) Copper, iron and zinc in Alzheimer’s disease senile plaques. J Neurol Sci 158:47–52PubMedGoogle Scholar
  57. Lue L, Kuo Y, Roher A, Brachova L, Shen Y, Sue L, Beach T, Kurth J, Rydel R, Rogers J (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer’s disease. Am J Pathol 155:853–862PubMedCentralPubMedGoogle Scholar
  58. Lui E, Fisman M, Wong C, Diaz F (1990) Metals and the liver in Alzheimer’s disease. An investigation of hepatic zinc, copper, cadmium, and metallothionein. J Am Geriatr Soc 38:633–639PubMedGoogle Scholar
  59. Lukawski K, Nieradko B, Sieklucka-Dziuba M (2005) Effects of cadmium on memory processes in mice exposed to transient cerebral oligemia. Neurotoxicol Teratol 27:575–584PubMedGoogle Scholar
  60. Mason RP, Jacob RF, Walter MF, Mason PE, Avdulov NA, Chochina SV, Igbavboa U, Wood WG (1999) Distribution and fluidizing action of soluble and aggregated amyloid beta-peptide in rat synaptic plasma membranes. J Biol Chem 274:18801–18807PubMedGoogle Scholar
  61. McLean C, Cherny R, Fraser F, Fuller S, Smith M, Beyreuther K, Bush A, Masters C (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer’s disease. Ann Neurol 46:860–866PubMedGoogle Scholar
  62. Meleleo D, Galliani A, Notarachille G (2013) AβP1-42 incorporation and channel formation in planar lipid membranes: the role of cholesterol and its oxidation products. J Bioenerg Biomembr 45:369–381PubMedGoogle Scholar
  63. Micelli S, Gallucci E, Meleleo D, Stipani V, Picciarelli V (2002) Mitochondrial porin incorporation into black lipid membranes: ionic and gating contribution to the total current. Bioelectrochemistry 57:97–106PubMedGoogle Scholar
  64. Micelli S, Meleleo D, Picciarelli V, Gallucci E (2004) Effect of sterols on beta-amyloid peptide (AbetaP 1-40) channel formation and their properties in planar lipid membranes. Biophys J 86:2231–2237PubMedCentralPubMedGoogle Scholar
  65. Minami A, Takeda A, Nishibaba D, Takefuta S, Oku N (2001) Cadmium toxicity in synaptic neurotransmission in the brain. Brain Res 894:336–339PubMedGoogle Scholar
  66. Miyashita N, Straub JE, Thirumalai D (2009) Structures of beta-amyloid peptide 1-40, 1-42, and 1-55-the 672-726 fragment of APP-in a membrane environment with implications for interactions with gamma-secretase. J Am Chem Soc 131:17843–17852PubMedCentralPubMedGoogle Scholar
  67. Moschou M, Papaefthimiou C, Kagiava A, Antonopoulou E, Theophilidis G (2008) In vitro assessment of the effects of cadmium and zinc on mammalian nerve fibres. Chemosphere 71:1996–2002PubMedGoogle Scholar
  68. Müller P, Rudin D, Tien T, Weacott W (1962) Reconstitution of cell membrane structure in vitro and its trasformation into an excitable system. Nature 194:979–980Google Scholar
  69. Nishimura Y, Yamaguchi JY, Kanada A, Horimoto K, Kanemaru K, Satoh M, Oyama Y (2006) Increase in intracellular Cd(2 +) concentration of rat cerebellar granule neurons incubated with cadmium chloride: cadmium cytotoxicity under external Ca(2 +)-free condition. Toxicol In Vitro 20:211–216PubMedGoogle Scholar
  70. Panayi A, Spyrou N, Iversen B, White M, Part P (2002) Determination of cadmium and zinc in Alzheimer’s brain tissue using inductively coupled plasma mass spectrometry. J Neurol Sci 195:1–10PubMedGoogle Scholar
  71. Pollard HB, Rojas E, Arispe N (1993) A new hypothesis for the mechanism of amyloid toxicity, based on the calcium channel activity of amyloid beta protein (A beta P) in phospholipid bilayer membranes. Ann N Y Acad Sci 695:165–168PubMedGoogle Scholar
  72. Quist A, Doudevski I, Lin H, Azimova R, Ng D, Frangione B, Kagan B, Ghiso J, Lal R (2005) Amyloid ion channels: a common structural link for protein-misfolding disease. Proc Natl Acad Sci USA 102:10427–10432PubMedCentralPubMedGoogle Scholar
  73. Raghunathan G, Seetharamulu P, Brooks BR, Guy HR (1990) Models of delta-hemolysin membrane channels and crystal structures. Proteins 8:213–225PubMedGoogle Scholar
  74. Ragunathan N, Dairou J, Sanfins E, Busi F, Noll C, Janel N, Dupret JM, Rodrigues-Lima F (2010) Cadmium alters the biotransformation of carcinogenic aromatic amines by arylamine N-acetyltransferase xenobiotic-metabolizing enzymes: molecular, cellular, and in vivo studies. Environ Health Perspect 118:1685–1691PubMedCentralPubMedGoogle Scholar
  75. Ricchelli F, Drago D, Filippi B, Tognon G, Zatta P (2005) Aluminum-triggered structural modifications and aggregation of beta-amyloids. Cell Mol Life Sci 62:1724–1733PubMedGoogle Scholar
  76. Roychaudhuri R, Yang M, Hoshi MM, Teplow DB (2009) Amyloid beta-protein assembly and Alzheimer disease. J Biol Chem 284:4749–4753PubMedCentralPubMedGoogle Scholar
  77. Sanderson KL, Butler L, Ingram VM (1997) Aggregates of a beta-amyloid peptide are required to induce calcium currents in neuron-like human teratocarcinoma cells: relation to Alzheimer’s disease. Brain Res 744:7–14PubMedGoogle Scholar
  78. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, Bird TD, Hardy J, Hutton M, Kukull W et al (1996) Secreted amyloid beta-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 2:864–870PubMedGoogle Scholar
  79. Selkoe D (2001a) Alzheimer’s disease: genes, proteins, and therapy. Physiol Rev 81:741–766PubMedGoogle Scholar
  80. Selkoe D (2001b) Clearing the brain’s amyloid cobwebs. Neuron 32:177–180PubMedGoogle Scholar
  81. Selkoe D (2004) Cell biology of protein misfolding: the examples of Alzheimer’s and Parkinson’s diseases. Nat Cell Biol 6:1054–1061PubMedGoogle Scholar
  82. Seubert P, Vigo-Pelfrey C, Esch F, Lee M, Dovey H, Davis D, Sinha S, Schlossmacher M, Whaley J, Swindlehurst C (1992) Isolation and quantification of soluble Alzheimer’s beta-peptide from biological fluids. Nature 359:325–327PubMedGoogle Scholar
  83. Shafrir Y, Durell S, Arispe N, Guy HR (2010) Models of membrane-bound Alzheimer’s Abeta peptide assemblies. Proteins 78:3473–3487PubMedCentralPubMedGoogle Scholar
  84. Shirwany NA, Payette D, Xie J, Guo Q (2007) The amyloid beta ion channel hypothesis of Alzheimer’s disease. Neuropsychiatr Dis Treat 3:597–612PubMedCentralPubMedGoogle Scholar
  85. Simmons MA, Schneider CR (1993) Amyloid beta peptides act directly on single neurons. Neurosci Lett 150:133–136PubMedGoogle Scholar
  86. Smart OS, Breed J, Smith GR, Sansom MS (1997) A novel method for structure-based prediction of ion channel conductance properties. Biophys J 72:1109–1126PubMedCentralPubMedGoogle Scholar
  87. Smith DG, Cappai R, Barnham KJ (2007) The redox chemistry of the Alzheimer’s disease amyloid beta peptide. Biochim Biophys Acta 1768:1976–1990PubMedGoogle Scholar
  88. Sokolov Y, Kozak J, Kayed R, Chanturiya A, Glabe C, Hall J (2006) Soluble amyloid oligomers increase bilayer conductance by altering dielectric structure. J Gen Physiol 128:637–647PubMedCentralPubMedGoogle Scholar
  89. Sowa B, Steibert E (1985) Effect of oral cadmium administration to female rats during pregnancy on zinc, copper, and iron content in placenta, foetal liver, kidney, intestine, and brain. Arch Toxicol 56:256–262PubMedGoogle Scholar
  90. Stellato F, Menestrina G, Serra MD, Potrich C, Tomazzolli R, Meyer-Klaucke W, Morante S (2006) Metal binding in amyloid beta-peptides shows intra- and inter-peptide coordination modes. Eur Biophys J 35:340–351PubMedGoogle Scholar
  91. Stipani V, Gallucci E, Micelli S, Picciarelli V, Benz R (2001) Channel formation by salmon and human calcitonin in black lipid membranes. Biophys J 81:3332–3338PubMedCentralPubMedGoogle Scholar
  92. Syme CD, Viles JH (2006) Solution 1H NMR investigation of Zn2+ and Cd22+ binding to amyloid-beta peptide (Abeta) of Alzheimer’s disease. Biochim Biophys Acta 1764:246–256PubMedGoogle Scholar
  93. Tien TH (1974) Bilayer Lipid Membrane: theory and practice. Marcel Dekker, New YorkGoogle Scholar
  94. Tien TH, Mountz JD, and Martinosi AN (1977) Protein-lipid interaction in bilayer lipid membranes (BLM). In: The enzyme of biological membranes, vol 1. Plenum, NY, pp 139–170Google Scholar
  95. Valincius G, Heinrich F, Budvytyte R, Vanderah D, McGillivray D, Sokolov Y, Hall J, Lösche M (2008) Soluble amyloid beta-oligomers affect dielectric membrane properties by bilayer insertion and domain formation: implications for cell toxicity. Biophys J 95:4845–4861PubMedCentralPubMedGoogle Scholar
  96. Vargas J, Alarcón J, Rojas E (2000) Displacement currents associated with the insertion of Alzheimer disease amyloid beta-peptide into planar bilayer membranes. Biophys J 79:934–944PubMedCentralPubMedGoogle Scholar
  97. Walsh D, Klyubin I, Fadeeva J, Cullen W, Anwyl R, Wolfe M, Rowan M, Selkoe D (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535–539PubMedGoogle Scholar
  98. Walsh DM, Townsend M, Podlisny MB, Shankar GM, Fadeeva JV, El Agnaf O, Hartley DM, Selkoe DJ (2005) Certain inhibitors of synthetic amyloid beta-peptide (Abeta) fibrillogenesis block oligomerization of natural Abeta and thereby rescue long-term potentiation. J Neurosci 25:2455–2462PubMedGoogle Scholar
  99. Wang B, Du Y (2013) Cadmium and its neurotoxic effects. Oxid Med Cell Longev 2013:898034PubMedCentralPubMedGoogle Scholar
  100. Wang HY, Lee DH, Davis CB, Shank RP (2000) Amyloid peptide Abeta(1-42) binds selectively and with picomolar affinity to alpha7 nicotinic acetylcholine receptors. J Neurochem 75:1155–1161PubMedGoogle Scholar
  101. Weiner H, Frenkel D (2006) Immunology and immunotherapy of Alzheimer’s disease. Nat Rev Immunol 6:404–416PubMedGoogle Scholar
  102. Yano K, Hirosawa N, Sakamoto Y, Katayama H, Moriguchi T (2003) Aggregations of amyloid beta-proteins in the presence of metal ions. Toxicol Lett 144:s134Google Scholar
  103. Yuan Y, Bian JC, Liu XZ, Zhang Y, Sun Y, Liu ZP (2012) Oxidative stress and apoptotic changes of rat cerebral cortical neurons exposed to cadmium in vitro. Biomed Environ Sci 25:172–181Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Gabriella Notarachille
    • 1
  • Fabio Arnesano
    • 2
  • Vincenza Calò
    • 2
  • Daniela Meleleo
    • 1
    Email author
  1. 1.Department of Biosciences, Biotechnologies and BiopharmaceuticsUniversity of Bari “Aldo Moro”BariItaly
  2. 2.Department of ChemistryUniversity of Bari “Aldo Moro”BariItaly

Personalised recommendations