Therapeutic redistribution of metal ions to treat Alzheimer's disease

Accounts of Chemical Research

Volumn 45, Issue 9, 2012, Pages 1604-1611

  Crouch, Peter J ^a   Barnham, Kevin J ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; GLYOXALBIS(N(4) METHYLTHIOSEMICARBAZONATO)COPPER(II); GLYOXALBIS(N(4)-METHYLTHIOSEMICARBAZONATO)COPPER(II); ION; ORGANOMETALLIC COMPOUND;

ALZHEIMER DISEASE; ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; DISEASE MODEL; MOUSE; PATHOLOGY;

ALZHEIMER DISEASE; ANIMALS; COPPER; DISEASE MODELS, ANIMAL; IONS; MICE; MOLECULAR STRUCTURE; ORGANOMETALLIC COMPOUNDS;

EID: 84866432813     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar300074t     Document Type: Article

References (56)

1. Crouch, P. J.; Harding, S. M.; White, A. R.; Camakaris, J.; Bush, A. I.; Masters, C. L. Mechanisms of Aβ Mediated Neurodegeneration in Alzheimer's Disease. Int. J. Biochem. Cell Biol. 2008, 40, 181-198
2. Glenner, G. G.; Wong, C. W. Alzheimer's Disease: Initial Report of the Purification and Characterization of a Novel Cerebrovascular Amyloid Protein Biochem. Biophys. Res. Commun. 1984, 120, 885-890
3. Masters, C. L.; Simms, G.; Weinman, N. A.; Multhaup, G.; McDonald, B. L.; Beyreuther, K. Amyloid Plaque Core Protein in Alzheimer Disease and Down Syndrome Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 4245-4249
4. Selkoe, D. J.; Abraham, C. R.; Podlisny, M. B.; Duffy, L. K. Isolation of Low-Molecular-Weight Proteins from Amyloid Plaque Fibers in Alzheimer's Disease J. Neurochem. 1986, 46, 1820-1834
5. Citron, M. Alzheimer's Disease: Strategies for Disease Modification Nat. Rev. Drug Discovery 2010, 9, 387-398
6. Atwood, C. S.; Moir, R. D.; Huang, X.; Scarpa, R. C.; Bacarra, N. M. E.; Romano, D. M.; Hartshorn, M. A.; Tanzi, R. E.; Bush, A. I. Dramatic Aggregation of Alzheimer Ab by Cu(II) is Induced by Conditions Representing Physiological Acidosis J. Biol. Chem. 1998, 273, 12817-12826
7. Bush, A. I.; Pettingall, W. H.; Multhaup, G.; Paradis, M.; Vonsattel, J.-P.; Gusella, J. F.; Beyreuther, K.; Masters, C. L.; Tanzi, R. E. Rapid Induction of Alzheimer Aβ Amyloid Formation by Zinc Science 1994, 265, 1464-1467
8. Huang, X.; Atwood, C. S.; Moir, R. D.; Hartshorn, M. A.; Vonsattel, J. P.; Tanzi, R. E.; Bush, A. I. Zinc-Induced Alzheimer's Abeta1-40 Aggregation Is Mediated by Conformational Factors J. Biol. Chem. 1997, 272, 26464-26470
9. 1-42 J. Neurosci. 2005, 25, 672-679
10. Curtain, C. C.; Ali, F.; Volitakis, I.; Cherny, R. A.; Norton, R. S.; Beyreuther, K.; Barrow, C. J.; Masters, C. L.; Bush, A. I.; Barnham, K. J. 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. 2001, 276, 20466-20473
11. Huang, X.; Atwood, C. S.; Hartshorn, M. A.; Multhaup, G.; Goldstein, L. E.; Scarpa, R. C.; Cuajungco, M. P.; Gray, D. N.; Lim, J.; Moir, R. D.; Tanzi, R. E.; Bush, A. I. The Aβ Peptide of Alzheimer's Disease Directly Produces Hydrogen Peroxide through Metal Ion Reduction Biochemistry 1999, 38, 7609-7616
12. Smith, D. P.; Smith, D. G.; Curtain, C. C.; Boas, J. F.; Pilbrow, J. R.; Ciccotosto, G. D.; Lau, T. L.; Tew, D. J.; Perez, K.; Wade, J. D.; Bush, A. I.; Drew, S. C.; Separovic, F.; Masters, C. L.; Cappai, R.; Barnham, K. J. Copper Mediated Amyloid-Beta Toxicity Is Associated with an Intermolecular Histidine Bridge J. Biol. Chem. 2006, 281, 15145-15154
13. Deshpande, A.; Kawai, H.; Metherate, R.; Glabe, C. G.; Busciglio, J. A Role for Synaptic Zinc in Activity-Dependent Aβ Oligomer Formation and Accumulation at Excitatory Synapses J. Neurosci. 2009, 29, 4004-4015
14. 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. 2002, 99, 7705-7710
15. 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. 1998, 158, 47-52
16. Cherny, R. A.; Atwood, C. S.; Xilinas, M. E.; Gray, D. N.; Jones, W. D.; McLean, C. A.; Barnham, K. J.; Volitakis, I.; Fraser, F. W.; Kim, Y.; Huang, X.; Goldstein, L. E.; Moir, R. D.; Lim, J. T.; Beyreuther, K.; Zheng, H.; Tanzi, R. E.; Masters, C. L.; Bush, A. I. Treatment with a Copper-Zinc Chelator Markedly and Rapidly Inhibits Beta-Amyloid Accumulation in Alzheimer's Disease Transgenic Mice Neuron 2001, 30, 665-676
17. Hsiao, K.; Chapman, P.; Nilsen, S.; Eckman, C.; Harigaya, Y.; Younkin, S.; Yang, F.; Cole, G. Correlative Memory Deficits, Aβ Elevation, and Amyloid Plaques in Transgenic Mice Science 1996, 274, 99-102
18. Padmanabhan, G.; Becue, I.; Smith, J. A. In Analytical Profiles of Drug Substances; Klauss, E.; Florey, E., Eds.; Academic Press: New York, 1989; pp 57-90.
19. Hartley, D. M.; Walsh, D. M.; Ye, C. P.; Diehl, T.; Vasquez, S.; Vassilev, P. M.; Teplow, D. B.; Selkoe, D. J. Protofibrillar Intermediates of Amyloid β-Protein Induce Acute Electrophysiological Changes and Progressive Neurotoxicity in Cortical Neurons J. Neurosci. 1999, 19, 8876-8884
20. McLean, C. A.; Cherny, R. A.; Fraser, F. W.; Fuller, S. J.; Smith, M. J.; Beyreuther, K.; Bush, A. I.; Masters, C. L. Soluble Pool of Aβ Amyloid as a Determinant of Severity of Neurodegeneration in Alzheimer's Disease Ann. Neurol. 1999, 46, 860-866
21. Crouch, P. J.; Tew, D. J.; Du, T.; Nguyen, D. N.; Caragounis, A.; Filiz, G.; Blake, R. E.; Trounce, I. A.; Soon, C. P.; Laughton, K.; Perez, K. A.; Li, Q. X.; Cherny, R. A.; Masters, C. L.; Barnham, K. J.; White, A. R. Restored Degradation of the Alzheimer's Amyloid-β Peptide by Targeting Amyloid Formation J. Neurochem. 2009, 108, 1198-1207
22. Ritchie, C. W.; Bush, A. I.; Mackinnon, A.; Macfarlane, S.; Mastwyk, M.; MacGregor, L.; Kiers, L.; Cherny, R.; Li, Q. X.; Tammer, A.; Carrington, D.; Mavros, C.; Volitakis, I.; Xilinas, M.; Ames, D.; Davis, S.; Beyreuther, K.; Tanzi, R. E.; Masters, C. L. Metal-Protein Attenuation with Iodochlorhydroxyquin (Clioquinol) Targeting Aβ Amyloid Deposition and Toxicity in Alzheimer Disease: A Pilot Phase 2 Clinical Trial Arch. Neurol. 2003, 60, 1685-1691
23. Treiber, C.; Simons, A.; Strauss, M.; Hafner, M.; Cappai, R.; Bayer, T. A.; Multhaup, G. Clioquinol Mediates Copper Uptake and Counteracts Copper Efflux Activities of the Amyloid Precursor Protein of Alzheimer's Disease J. Biol. Chem. 2004, 279, 51958-51964
24. White, A. R.; Du, T.; Laughton, K. M.; Volitakis, I.; Sharples, R. A.; Xilinas, M. E.; Hoke, D. E.; Holsinger, R. M.; Evin, G.; Cherny, R. A.; Hill, A. F.; Barnham, K. J.; Li, Q. X.; Bush, A. I.; Masters, C. L. Degradation of the Alzheimer Disease Amyloid Beta-Peptide by Metal-Dependent up-Regulation of Metalloprotease Activity J. Biol. Chem. 2006, 281, 17670-17680
25. Hanger, D. P.; Hughes, K.; Woodgett, J. R.; Brion, J. P.; Anderton, B. H. Glycogen Synthase Kinase-3 Induces Alzheimer's Disease-Like Phosphorylation of Tau: Generation of Paired Helical Filament Epitopes and Neuronal Localisation of the Kinase Neurosci. Lett. 1992, 147, 58-62
26. Mandelkow, E. M.; Drewes, G.; Biernat, J.; Gustke, N.; Van Lint, J.; Vandenheede, J. R.; Mandelkow, E. Glycogen Synthase Kinase-3 and the Alzheimer-Like State of Microtubule-Associated Protein Tau FEBS Lett. 1992, 314, 315-321
27. Hooper, C.; Killick, R.; Lovestone, S. The GSK3 Hypothesis of Alzheimer's Disease J. Neurochem. 2008, 104, 1433-1439
28. Beraldo, H.; Gambino, D. The Wide Pharmacological Versatility of Semicarbazones, Thiosemicarbazones and Their Metal Complexes Mini-Rev. Med. Chem. 2004, 4, 31-39
29. Green, M. A.; Klippenstein, D. L.; Tennison, J. R. Copper(II) Bis(Thiosemicarbazone) Complexes as Potential Tracers for Evaluation of Cerebral and Myocardial Blood Flow with PET J. Nucl. Med. 1988, 29, 1549-1557
30. Lewis, J. S.; Sharp, T. L.; Laforest, R.; Fujibayashi, Y.; Welch, M. J. Tumor Uptake of Copper-Diacetyl-Bis(N(4)-Methylthiosemicarbazone): Effect of Changes in Tissue Oxygenation J. Nucl. Med. 2001, 42, 655-661
31. West, D. X.; Liberta, A. E.; Padhye, S. B.; Chikate, R. C.; Sonawane, P. B.; Kumbhar, A. S.; Yerande, R. G. Thiosemicarbazone Complexes of Copper(II): Structural and Biological Studies Coord. Chem. Rev. 1993, 123, 49-71
32. Xiao, Z.; Donnelly, P. S.; Zimmermann, M.; Wedd, A. G. Transfer of Copper between Bis(Thiosemicarbazone) Ligands and Intracellular Copper-Binding Proteins. Insights into Mechanisms of Copper Uptake and Hypoxia Selectivity Inorg. Chem. 2008, 47, 4338-4347
33. Petering, D. H. Concerning the Role of Zinc in the Antitumor Activity of 3-Ethoxy-2-Oxobutyraldehyde Bis(Thiosemicarbazonato) Zinc(II) and Related Chelates Biochem. Pharmacol. 1974, 23, 567-576
34. Fodero-Tavoletti, M. T.; Villemagne, V. L.; Paterson, B. M.; White, A. R.; Li, Q. X.; Camakaris, J.; O'Keefe, G.; Cappai, R.; Barnham, K. J.; Donnelly, P. S. Concerning the Role of Zinc in the Antitumor Activity of 3-Ethoxy-2-Oxobutyraldehyde Bis(Thiosemicarbazonato) Zinc(II) and Related Chelates J. Alzheimer's Dis. 2010, 20, 49-55
35. Dearling, J. L.; Blower, P. J. Redox-Active Metal Complexes for Imaging Hypoxic Tissues: Structure Activity Relationships in Copper(II) Bis(Thiosemicarbazone) Complexes Chem. Commun. 1998, 2531-2532
36. Donnelly, P. S.; Caragounis, A.; Du, T.; Laughton, K. M.; Volitakis, I.; Cherny, R. A.; Sharples, R. A.; Hill, A. F.; Li, Q. X.; Masters, C. L.; Barnham, K. J.; White, A. R. Selective Intracellular Release of Copper and Zinc Ions from Bis(Thiosemicarbazonato) Complexes Reduces Levels of Alzheimer Disease Amyloid-β Peptide J. Biol. Chem. 2008, 283, 4568-4577
37. Crouch, P. J.; Hung, L. W.; Adlard, P. A.; Cortes, M.; Lal, V.; Filiz, G.; Perez, K. A.; Nurjono, M.; Caragounis, A.; Du, T.; Laughton, K.; Volitakis, I.; Bush, A. I.; Li, Q. X.; Masters, C. L.; Cappai, R.; Cherny, R. A.; Donnelly, P. S.; White, A. R.; Barnham, K. J. Increasing Cu Bioavailability Inhibits Aβ Oligomers and Tau Phosphorylation Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 381-386
38. Adlard, P. A.; Cherny, R. A.; Finkelstein, D. I.; Gautier, E.; Robb, E.; Cortes, M.; Volitakis, I.; Liu, X.; Smith, J. P.; Perez, K.; Laughton, K.; Li, Q. X.; Charman, S. A.; Nicolazzo, J. A.; Wilkins, S.; Deleva, K.; Lynch, T.; Kok, G.; Ritchie, C. W.; Tanzi, R. E.; Cappai, R.; Masters, C. L.; Barnham, K. J.; Bush, A. I. Rapid Restoration of Cognition in Alzheimer's Transgenic Mice with 8-Hydroxy Quinoline Analogs is Associated with Decreased Interstitial Aβ Neuron 2008, 59, 43-55
39. Malm, T. M.; Iivonen, H.; Goldsteins, G.; Keksa-Goldsteine, V.; Ahtoniemi, T.; Kanninen, K.; Salminen, A.; Auriola, S.; Van Groen, T.; Tanila, H.; Koistinaho, J. Pyrrolidine Dithiocarbamate Activates Akt and Improves Spatial Learning in APP/PS1 Mice without Affecting β-Amyloid Burden J. Neurosci. 2007, 27, 3712-3721
40. Lee, J. Y.; Friedman, J. E.; Angel, I.; Kozak, A.; Koh, J. Y. The Lipophilic Metal Chelator DP-109 Reduces Amyloid Pathology in Brains of Human β-Amyloid Precursor Protein Transgenic Mice Neurobiol. Aging 2004, 25, 1315-1321
41. Lannfelt, L.; Blennow, K.; Zetterberg, H.; Bâtsman, S.; Ames, D.; Harrison, J.; Masters, C. L.; Targum, S.; Bush, A. I.; Murdoch, R.; Wilson, J.; Ritchie, C. W. Safety, Efficacy, and Biomarker Findings of PBT2 in Targeting Aβ as a Modifying Therapy for Alzheimer's Disease: A Phase IIa, Double-Blind, Randomised, Placebo-Controlled Trial Lancet Neurol. 2008, 7, 779-786
42. Faux, N. G.; Ritchie, C. W.; Gunn, A.; Rembach, A.; Tsatsanis, A.; Bedo, J.; Harrison, J.; Lannfelt, L.; Blennow, K.; Zetterberg, H.; Ingelsson, M.; Masters, C. L.; Tanzi, R. E.; Cummings, J. L.; Herd, C. M.; Bush, A. I. PBT2 Rapidly Improves Cognition in Alzheimer's Disease: Additional Phase II Analyses J. Alzheimer's Dis. 2010, 20, 509-516
43. Lannfelt, L.; Blennow, K.; Zetterberg, H.; Bâtsman, S.; Ames, D.; Harrison, J.; Masters, C. L.; Targum, S.; Bush, A. I.; Murdoch, R.; Wilson, J.; Ritchie, C. W. Safety, Efficacy, and Biomarker Findings of PBT2 in Targeting Aβ as a Modifying Therapy for Alzheimer's Disease: A Phase IIa, Double-Blind, Randomised, Placebo-Controlled Trial-Erratum Lancet Neurol. 2009, 8, 981
44. Adlard, P. A.; Bica, L.; White, A. R.; Nurjono, M.; Filiz, G.; Crouch, P. J.; Donnelly, P. S.; Cappai, R.; Finkelstein, D. I.; Bush, A. I. Metal Ionophore Treatment Restores Dendritic Spine Density and Synaptic Protein Levels in a Mouse Model of Alzheimer's Disease PloS One 2011, 6 e17669
45. Crouch, P. J.; Savva, M. S.; Hung, L. W.; Donnelly, P. S.; Mot, A. I.; Parker, S. J.; Greenough, M. A.; Volitakis, I.; Adlard, P. A.; Cherny, R. A.; Masters, C. L.; Bush, A. I.; Barnham, K. J.; White, A. R. The Alzheimer's Therapeutic PBT2 Promotes Amyloid-β Degradation and GSK3 Phosphorylation Via a Metal Chaperone Activity J. Neurochem. 2011, 119, 220-230
46. Diaz, N.; Suarez, D. Molecular Dynamics Simulations of Matrix Metalloproteinase 2: Role of the Structural Metal Ions Biochemistry 2007, 46, 8943-8952
47. Caragounis, A.; Du, T.; Filiz, G.; Laughton, K. M.; Volitakis, I.; Sharples, R. A.; Cherny, R. A.; Masters, C. L.; Drew, S. C.; Hill, A. F.; Li, Q. X.; Crouch, P. J.; Barnham, K. J.; White, A. R. Differential Modulation of Alzheimer's Disease Amyloid Beta Peptide Accumulation by Diverse Classes of Metal Ligands Biochem. J. 2007, 407, 435-450
48. Donnelly, P. S.; Liddell, J. R.; Lim, S.; Paterson, B. M.; Cater, M. A.; Savva, M. S.; Mot, A. I.; James, J. L.; Trounce, I. A.; White, A. R.; Crouch, P. J. An Impaired Mitochondrial Electron Transport Chain Increases Retention of the Hypoxia Imaging Agent Diacetylbis(4-Methylthiosemicarbazonato)CopperII Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 47-52
49. Materia, S.; Cater, M. A.; Klomp, L. W.; Mercer, J. F.; La Fontaine, S. Clusterin (Apolipoprotein J), a Molecular Chaperone That Facilitates Degradation of the Copper-ATPases ATP7a and ATP7b J. Biol. Chem. 2011, 286, 10073-10083
50. van den Berghe, P. V.; Folmer, D. E.; Malingre, H. E.; van Beurden, E.; Klomp, A. E.; van de Sluis, B.; Merkx, M.; Berger, R.; Klomp, L. W. Human Copper Transporter 2 is Localized in Late Endosomes and Lysosomes and Facilitates Cellular Copper Uptake Biochem. J. 2007, 407, 49-59
51. Price, K. A.; Caragounis, A.; Paterson, B. M.; Filiz, G.; Volitakis, I.; Masters, C. L.; Barnham, K. J.; Donnelly, P. S.; Crouch, P. J.; White, A. R. Sustained Activation of Glial Cell Epidermal Growth Factor Receptor by Bis(Thiosemicarbazonato) Metal Complexes is Associated with Inhibition of Protein Tyrosine Phosphatase Activity J. Med. Chem. 2009, 52, 6606-6620
52. Price, K. A.; Filiz, G.; Caragounis, A.; Du, T.; Laughton, K. M.; Masters, C. L.; Sharples, R. A.; Hill, A. F.; Li, Q. X.; Donnelly, P. S.; Barnham, K. J.; Crouch, P. J.; White, A. R. Activation of Epidermal Growth Factor Receptor by Metal-Ligand Complexes Decreases Levels of Extracellular Amyloid Beta Peptide Int. J. Biochem. Cell Biol. 2008, 40, 1901-1917
53. Perez, L. R.; Franz, K. J. Minding Metals: Tailoring Multifunctional Chelating Agents for Neurodegenerative Disease Dalton Trans. 2010, 39, 2177-2187
54. Scott, L. E.; Orvig, C. Medicinal Inorganic Chemistry Approaches to Passivation and Removal of Aberrant Metal Ions in Disease Chem. Rev. 2009, 109, 4885-4910
55. Tamano, H.; Takeda, A. Dynamic Action of Neurometals at the Synapse Metallomics 2011, 3, 656-661
56. Bush, A. I. The Metallobiology of Alzheimer's Disease Trends Neurosci. 2003, 26, 207-214