The Rapid Exchange of Zinc2 + Enables Trace Levels to Profoundly Influence Amyloid-β Misfolding and Dominates Assembly Outcomes in Cu2 +/Zn2 + Mixtures

Journal of Molecular Biology

Volumn 428, Issue 14, 2016, Pages 2832-2846

  Matheou, Christian J ^a   Younan, Nadine D ^a   Viles, John H ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

aggregation; Alzheimer's disease; A ; copper; zinc

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; COPPER ION; ZINC ION; COPPER; ION; PROTEIN AGGREGATE; ZINC;

ARTICLE; BINDING AFFINITY; BIOACCUMULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GROWTH CURVE; ION EXCHANGE; METAL BINDING; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN MISFOLDING; RAPID EXCHANGE; TRANSMISSION ELECTRON MICROSCOPY; ALZHEIMER DISEASE; HUMAN; KINETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; COPPER; HUMANS; IONS; KINETICS; PROTEIN AGGREGATES; PROTEIN FOLDING; ZINC;

EID: 84977546465     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.05.017     Document Type: Article

References (77)

1. [1] Prince, M., Jackson, J., Ferri, C.P., Sousa, R., Albanese, E., Ribeiro, W.S., et al. Alzheimer's disease international world Alzheimer report. International AsD, 2009, 1–96.
2. [2] Hardy, J.A., Higgins, G.A., Alzheimer's disease: the amyloid cascade hypothesis. Science 256 (1992), 184–185.
3. [3] Lambert, M.P., Barlow, A.K., Chromy, B.A., Edwards, C., Freed, R., Liosatos, M., et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 6448–6453.
4. [4] Walsh, D.M., Klyubin, I., Fadeeva, J.V., Cullen, W.K., Anwyl, R., Wolfe, M.S., et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 (2002), 535–539.
5. [5] Ballard, C., Gauthier, S., Corbett, A., Brayne, C., Aarsland, D., Jones, E., Alzheimer's disease. Lancet 377 (2011), 1019–1031.
6. [6] Hardy, J., Selkoe, D.J., The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002), 353–356.
7. [7] Bush, A.I., Pettingell, W.H., Multhaup, G., Paradis, M.d., Vonsattel, J.P., Gusella, J.F., et al. Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 265 (1994), 1464–1467.
8. [8] Lovell, M.A., Robertson, J.D., Teesdale, W.J., Campbell, J.L., Markesbery, W.R., Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci. 18 (1998), 47–52.
9. [9] Fukada, T., Yamasaki, S., Nishida, K., Murakami, M., Hirano, T., Zinc homeostasis and signaling in health and diseases: zinc signaling. J. Biol. Inorg. Chem. 16 (2011), 1123–1134.
10. [10] Ceccom, J., Halley, H., Daumas, S., Lassalle, J.M., A specific role for hippocampal mossy fiber's zinc in rapid storage of emotional memories. Learn. Mem. 21 (2014), 287–297.
11. [11] Lin, D.D., Cohen, A.S., Coulter, D.A., Zinc-induced augmentation of excitatory synaptic currents and glutamate receptor responses in hippocampal CA3 neurons. J. Neurophysiol. 85 (2001), 1185–1196.
12. [12] Howell, G.A., Welch, M.G., Frederickson, C.J., Stimulation-induced uptake and release of zinc in hippocampal slices. Nature 308 (1984), 736–738.
13. [13] Assaf, S.Y., Chung, S.H., Release of endogenous Zn2 + from brain tissue during activity. Nature 308 (1984), 734–736.
14. [14] Qian, J., Noebels, J.L., Exocytosis of vesicular zinc reveals persistent depression of neurotransmitter release during metabotropic glutamate receptor long-term depression at the hippocampal CA3-CA1 synapse. J. Neurosci. 26 (2006), 6089–6095.
15. [15] Nydegger, I., Rumschik, S.M., Kay, A.R., Zinc is externalized rather than released during synaptic transmission. ACS Chem. Neurosci. 1 (2010), 728–736.
16. [16] Paoletti, P., Vergnano, A.M., Barbour, B., Casado, M., Zinc at glutamatergic synapses. Neuroscience 158 (2009), 126–136.
17. [17] Faller, P., Hureau, C., Bioinorganic chemistry of copper and zinc ions coordinated to amyloid-beta peptide. Dalton Trans., 1080-1094, 2009.
18. [18] Danielsson, J., Pierattelli, R., Banci, L., Gräslund, A., High-resolution NMR studies of the zinc-binding site of the Alzheimer's amyloid beta-peptide. FEBS J. 274 (2007), 46–59.
19. [19] Talmard, C., Bouzan, A., Faller, P., Zinc binding to amyloid-beta: isothermal titration calorimetry and Zn competition experiments with Zn sensors. Biochemistry 46 (2007), 13,658–13,666.
20. [20] Vogt, K., Mellor, J., Tong, G., Nicoll, R., The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26 (2000), 187–196.
21. [21] Molnar, P., Nadler, J.V., Synaptically-released zinc inhibits N-methyl-D-aspartate receptor activation at recurrent mossy fiber synapses. Brain Res. 910 (2001), 205–207.
22. [22] Frederickson, C.J., Neurobiology of zinc and zinc-containing neurons. Int. Rev. Neurobiol. 31 (1989), 145–238.
23. [23] Noy, D., Solomonov, I., Sinkevich, O., Arad, T., Kjaer, K., Sagi, I., Zinc–amyloid beta interactions on a millisecond time-scale stabilize non-fibrillar Alzheimer-related species. J. Am. Chem. Soc. 130 (2008), 1376–1383.
24. [24] Adlard, P.A., Cherny, R.A., Finkelstein, D.I., Gautier, E., Robb, E., Cortes, M., et al. Rapid restoration of cognition in Alzheimer's transgenic mice with 8-hydroxy quinoline analogs is associated with decreased interstitial Abeta. Neuron 59 (2008), 43–55.
25. [25] Linkous, D.H., Adlard, P.A., Wanschura, P.B., Conko, K.M., Flinn, J.M., The effects of enhanced zinc on spatial memory and plaque formation in transgenic mice. J. Alzheimers Dis. 18 (2009), 565–579.
26. [26] Hua, H., Munter, L., Harmeier, A., Georgiev, O., Multhaup, G., Schaffner, W., Toxicity of Alzheimer's disease-associated Abeta peptide is ameliorated in a Drosophila model by tight control of zinc and copper availability. Biol. Chem. 392 (2011), 919–926.
27. [27] Corona, C., Masciopinto, F., Silvestri, E., Viscovo, A.D., Lattanzio, R., Sorda, R.L., et al. Dietary zinc supplementation of 3xTg-AD mice increases BDNF levels and prevents cognitive deficits as well as mitochondrial dysfunction. Cell Death Dis., 1, 2010, e91.
28. [28] Lee, J.Y., Cole, T.B., Palmiter, R.D., Suh, S.W., Koh, J.Y., Contribution by synaptic zinc to the gender-disparate plaque formation in human Swedish mutant APP transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 7705–7710.
29. [29] Adlard, P.A., Parncutt, J.M., Finkelstein, D.I., Bush, A.I., Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimer's disease?. J. Neurosci. 30 (2010), 1631–1636.
30. [30] Syme, C.D., Viles, J.H., Solution 1H NMR investigation of Zn2 + and Cd2 + binding to amyloid-beta peptide (Abeta) of Alzheimer's disease. Biochim. Biophys. Acta 2006 (1764), 246–256.
31. [31] Mekmouche, Y., Coppel, Y., Hochgrafe, K., Guilloreau, L., Tallmard, C., Mazarguil, H., et al. Characterization of the Zn-II binding to the peptide amyloid-beta(1-16) linked to Alzheimer's disease. Chembiochem 6 (2005), 1663–1671.
32. [32] Minicozzi, V., Stellato, F., Comai, M., Dalla Serra, M., Potrich, C., Meyer-Klaucke, W., et al. Identifying the minimal copper- and zinc-binding site sequence in amyloid-beta peptides. J. Biol. Chem. 283 (2008), 10,784–10,792.
33. [33] Viles, J.H., Metal ions and amyloid fiber formation in neurodegenerative diseases. Copper, zinc and iron in Alzheimer's, Parkinson's and prion diseases. Coord. Chem. Rev. 256 (2012), 2271–2284.
34. [34] Yoshiike, Y., Tanemura, K., Murayama, O., Akagi, T., Murayama, M., Sato, S., et al. New insights on how metals disrupt amyloid beta-aggregation and their effects on amyloid-beta cytotoxicity. J. Biol. Chem. 276 (2001), 32,293–32,299.
35. [35] Ha, C., Ryu, J., Park, C.B., Metal ions differentially influence the aggregation and deposition of Alzheimer's beta-amyloid on a solid template. Biochemistry 46 (2007), 6118–6125.
36. [36] Raman, B., Ban, T., Yamaguchi, K., Sakai, M., Kawai, T., Naiki, H., et al. Metal ion-dependent effects of clioquinol on the fibril growth of an amyloid {beta} peptide. J. Biol. Chem. 280 (2005), 16,157–16,162.
37. [37] House, E., Collingwood, J., Khan, A., Korchazkina, O., Berthon, G., Exley, C., Aluminium, iron, zinc and copper influence the in vitro formation of amyloid fibrils of Abeta42 in a manner which may have consequences for metal chelation therapy in Alzheimer's disease. J. Alzheimers Dis. 6 (2004), 291–301.
38. [38] Tougu, V., Karafin, A., Zovo, K., Chung, R.S., Howells, C., West, A.K., et al. Zn(II)- and Cu(II)-induced non-fibrillar aggregates of amyloid-beta (1-42) peptide are transformed to amyloid fibrils, both spontaneously and under the influence of metal chelators. J. Neurochem. 110 (2009), 1784–1795.
39. [39] Sharma, A.K., Pavlova, S.T., Kim, J., Kim, J., Mirica, L.M., The effect of Cu2 + and Zn2 + on the A beta(42) peptide aggregation and cellular toxicity. Metallomics 5 (2013), 1529–1536.
40. [40] Chen, W.T., Liao, Y.H., Yu, H.M., Cheng, I.H., Chen, Y.R., 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 (2011), 9646–9656.
41. [41] Chen, W.T., Hong, C.J., Lin, Y.T., Chang, W.H., Huang, H.T., Liao, J.Y., et al. Amyloid-beta (Aβ) D7H mutation increases oligomeric Aβ42 and alters properties of Aβ-zinc/copper assemblies. PLoS ONE, 7, 2012, e35807.
42. [42] Solomonov, I., Korkotian, E., Born, B., Feldman, Y., Bitler, A., Rahimi, F., et al. Zn2 + − Abeta40 complexes form metastable quasi-spherical oligomers that are cytotoxic to cultured hippocampal neurons. J. Biol. Chem. 287 (2012), 20,555–20,564.
43. [43] Abelein, A., Graslund, A., Danielsson, J., Zinc as chaperone-mimicking agent for retardation of amyloid beta peptide fibril formation. Proc. Natl. Acad. Sci. U. S. A., 2015.
44. [44] Garai, K., Sahoo, B., Kaushalya, S.K., Desai, R., Maiti, S., Zinc lowers amyloid-beta toxicity by selectively precipitating aggregation intermediates. Biochemistry 46 (2007), 10,655–10,663.
45. [45] Syme, C.D., Nadal, R.C., Rigby, S.E.J., Viles, J.H., Copper binding to the amyloid-beta (Ab) peptide associated with Alzheimer's disease. J. Biol. Chem. 279 (2004), 18169–18177.
46. [46] Kardos, J., Kovács, I., Hajós, F., Kálmán, M., Simonyi, M., Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability. Neurosci. Lett. 103 (1989), 139–144.
47. [47] Sarell, C.J., Syme, C.D., Rigby, S.E., Viles, J.H., Copper(II) binding to amyloid-beta fibrils of Alzheimer's disease reveals a picomolar affinity: stoichiometry and coordination geometry are independent of Abeta oligomeric form. Biochemistry 48 (2009), 4388–4402.
48. [48] Sarell, C.J., Wilkinson, S.R., Viles, J.H., Substoichiometric levels of Cu2 + ions accelerate the kinetics of fiber formation and promote cell toxicity of amyloid-{beta} from Alzheimer disease. J. Biol. Chem. 285 (2010), 41,533–41,540.
49. [49] Matheou, C.J., Younan, N.D., Viles, J.H., Cu2 + accentuates distinct misfolding of Abeta(1-40) and Abeta(1-42) peptides, and potentiates membrane disruption. Biochem. J. 466 (2015), 233–242.
50. [50] Alies, B., Sasaki, I., Proux, O., Sayen, S., Guillon, E., Faller, P., et al. Zn impacts Cu coordination to amyloid-beta, the Alzheimer's peptide, but not the ROS production and the associated cell toxicity. Chem. Commun. (Camb.) 49 (2013), 1214–1216.
51. [51] Silva, K.I., Saxena, S., Zn(II) ions substantially perturb Cu(II) ion coordination in amyloid-beta at physiological pH. J. Phys. Chem. B 117 (2013), 9386–9394.
52. [52] Roychaudhuri, R., Yang, M., Hoshi, M.M., Teplow, D.B., Amyloid beta-protein assembly and Alzheimer disease. J. Biol. Chem. 284 (2009), 4749–4753.
53. [53] Jarrett, J.T., Lansbury, P.T. Jr., Seeding “one-dimensional crystallization” of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie?. Cell 73 (1993), 1055–1058.
54. [54] Barria, M.A., Gonzalez-Romero, D., Soto, C., Cyclic amplification of prion protein misfolding. Methods Mol. Biol. 849 (2012), 199–212.
55. [55] Faller, P., Hureau, C., Berthoumieu, O., Role of metal ions in the self-assembly of the Alzheimer's amyloid-beta peptide. Inorg. Chem. 52 (2013), 12,193–12,206.
56. [56] Hartter, D.E., Barnea, A., Evidence for release of copper in the brain: depolarization-induced release of newly taken-up 67copper. Synapse 2 (1988), 412–415.
57. [57] Srabasti Acharya, L.J.L., Reconfiguration of the Alzheimer's peptide kinetically controls aggregation in Alzheimer's disease. Biophys. J. 108 (2015), 65a–66a.
58. [58] Yang, M., Teplow, D.B., Amyloid beta-protein monomer folding: free-energy surfaces reveal alloform-specific differences. J. Mol. Biol. 384 (2008), 450–464.
59. [59] Sgourakis, N.G., Yan, Y., McCallum, S.A., Wang, C., Garcia, A.E., The Alzheimer's peptides Abeta40 and 42 adopt distinct conformations in water: a combined MD / NMR study. J. Mol. Biol. 368 (2007), 1448–1457.
60. [60] Heller, G.T., Sormanni, P., Vendruscolo, M., Targeting disordered proteins with small molecules using entropy. Trends Biochem. Sci. 40 (2015), 491–496.
61. [61] Bitan, G., Kirkitadze, M.D., Lomakin, A., Vollers, S.S., Benedek, G.B., Teplow, D.B., Amyloid beta -protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 330–335.
62. [62] Chen, Y.R., Glabe, C.G., Distinct early folding and aggregation properties of Alzheimer amyloid-beta peptides Abeta40 and Abeta42: stable trimer or tetramer formation by Abeta42. J. Biol. Chem. 281 (2006), 24,414–24,422.
63. [63] Xiao, Y., Ma, B., McElheny, D., Parthasarathy, S., Long, F., Hoshi, M., et al. Abeta(1-42) fibril structure illuminates self-recognition and replication of amyloid in Alzheimer's disease. Nat. Struct. Mol. Biol. 22 (2015), 499–505.
64. [64] Mithu, V.S., Sarkar, B., Bhowmik, D., Chandrakesan, M., Maiti, S., Madhu, P.K., Zn(++) binding disrupts the asp(23)-Lys(28) salt bridge without altering the hairpin-shaped cross-beta structure of Abeta(42) amyloid aggregates. Biophys. J. 101 (2011), 2825–2832.
65. [65] Dawson, R.M.C., Elliot, D.C., Elliot, W.H., Jones, K.M., Data for Biochemical Research. 1986, Claredon Press, Oxford UK.
66. [66] Sparks, D.L., Schreurs, B.G., Trace amounts of copper in water induce beta-amyloid plaques and learning deficits in a rabbit model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 11,065–11,069.
67. [67] Singh, S.K., Sinha, P., Mishra, L., Srikrishna, S., Neuroprotective role of a novel copper chelator against Abeta 42 induced neurotoxicity. Int. J. Alzheimers Dis., 2013, 2013, 567,128.
68. [68] Sanokawa-Akakura, R., Cao, W., Allan, K., Patel, K., Ganesh, A., Heiman, G., et al. Control of Alzheimer's amyloid beta toxicity by the high molecular weight immunophilin FKBP52 and copper homeostasis in Drosophila. PLoS ONE, 5, 2010, e8626.
69. [69] Faller, P., Hureau, C., La Penna G, G., Metal ions and intrinsically disordered proteins and peptides: from Cu/Zn amyloid-β to general principles. Acc. Chem. Res. 47 (2014), 2252–2259.
70. [70] Barritt, J.D., Viles, J.H., Truncated amyloid-beta(11-40/42) from Alzheimer disease binds Cu2 + with a femtomolar affinity and influences fiber assembly. J. Biol. Chem. 290 (2015), 27,791–27,802.
71. [71] Takeda, A., Nakamura, M., Fujii, H., Tamano, H., Synaptic Zn(2 +) homeostasis and its significance. Metallomics 5 (2013), 417–423.
72. [72] Brown, C.E., Dyck, R.H., Distribution of zincergic neurons in the mouse forebrain. J. Comp. Neurol. 479 (2004), 156–167.
73. [73] Matlack, K.E., Tardiff, D.F., Narayan, P., Hamamichi, S., Caldwell, K.A., Caldwell, G.A., et al. Clioquinol promotes the degradation of metal-dependent amyloid-beta (Abeta) oligomers to restore endocytosis and ameliorate Abeta toxicity. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 4013–4018.
74. [74] Cherny, R.A., Atwood, C.S., Xilinas, M.E., Gray, D.N., Jones, W.D., McLean, C.A., et al. Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 30 (2001), 665–676.
75. [75] Fezoui, Y., Hartley, D.M., Harper, J.D., Khurana, R., Walsh, D.M., Condron, M.M., et al. An improved method of preparing the amyloid beta-protein for fibrillogenesis and neurotoxicity experiments. Amyloid 7 (2000), 166–178.
76. [76] Younan, N.D., Viles, J.H., A comparison of three fluorophores for the detection of amyloid fibers and prefibrillar oligomeric assemblies. ThT (thioflavin T); ANS (1-Anilinonaphthalene-8-sulfonic acid); and bisANS (4,4'-Dianilino-1,1'-binaphthyl-5,5'-disulfonic acid). Biochemistry 54 (2015), 4297–4306.
77. [77] Uversky, V.N., Li, J., Fink, A.L., Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276 (2001), 44,284–44,296.