Role of metal ions in the cognitive decline of down syndrome

Frontiers in Aging Neuroscience

Volumn 6, Issue JUN, 2014, Pages

  Malakooti, Nakisa ^a   Pritchard, Melanie A ^b   Adlard, Paul A ^a   Finkelstein, David I ^a  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Alzheimer disease; Calcium; Copper; Down syndrome; Iron; Zinc

Indexed keywords

ADAPTOR PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; CALCINEURIN; CALCIUM; CALCIUM CHANNEL L TYPE; CLATHRIN; COPPER; FERRITIN; GAMMA SECRETASE; GLUTAMATE RECEPTOR; INTERSECTIN; INTERSECTIN 1; IRON; IRON REGULATORY FACTOR; METAL ION; TAU PROTEIN; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER;

AGE; CHROMOSOME 21; DOWN SYNDROME; HOMEOSTASIS; HUMAN; IMMUNOREACTIVITY; IRON STORAGE; IRON TRANSPORT; MEMORY CONSOLIDATION; MENTAL DETERIORATION; METAL BINDING; NERVE CELL PLASTICITY; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NONHUMAN; PHENOTYPE; REVIEW; SECRETORY PATHWAY; UPREGULATION;

EID: 84904543316     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00136     Document Type: Review

References (64)

1. Acevedo, K. M., Opazo, C. M., Norrish, D., Challis, L. M., Li, Q.-X., White, A. R., et al. (2014). Phosphorylation of amyloid precursor protein at threonine-668 is essential for its copper-responsive trafficking in SH-SY5Y neuroblastoma cells. J. Biol. Chem. 289, 11007-11019. doi: 10.1074/jbc.m113.538710
2. Adlard, P. A., and Bush, A. I. (2006). Metals and Alzheimer's disease. J. Alzheimers Dis. 10, 145-163.
3. Adlard, P. A., Parncutt, J. M., Finkelstein, D. I., and Bush, A. I. (2010). Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimer's disease? J. Neurosci. 30, 1631-1636. doi: 10.1523/JNEUROSCI.5255-09.2010
4. Alzheimer, A., Stelzmann, R., Schnitzlein, H. N., and Murtagh, F. R. (1995). An English translation of Alzheimer's 1907 paper, "Uber eine eigenartige Erkankung der Hirnrinde". Clin. Anat. 8, 429-431. doi: 10.1002/ca.980080612
5. Anekonda, T. S., Quinn, J. F., Harris, C., Frahler, K., Wadsworth, T. L., and Woltjer, R. L. (2011). L-type voltage-gated calcium channel blockade with isradipine as a therapeutic strategy for Alzheimer's disease. Neurobiol. Dis. 41, 62-70. doi: 10.1016/j.nbd.2010.08.020
6. Barnham, K. J., Mckinstry, W. J., Multhaup, G., Galatis, D., Morton, C. J., Curtain, C. C., et al. (2003). Structure of the Alzheimer's disease amyloid precursor protein copper binding domain a regulator of neuronal copper homeostasis. J. Biol. Chem. 278, 17401-17407. doi: 10.1074/jbc.m300629200
7. Bonda, D. J., Lee, H.-G., Blair, J. A., Zhu, X., Perry, G., and Smith, M. A. (2011). Role of metal dyshomeostasis in Alzheimer's disease. Metallomics 3, 267-270. doi: 10.1039/c0mt00074d
8. Burch, P., and Milunsky, A. (1969). Early-onset diabetes mellitus in the general and Down's syndrome populations: genetics, aetiology and pathogenesis. Lancet 293, 554-558. doi: 10.1016/s0140-6736(69)91961-8
9. Bush, A. I. (2013). The metal theory of Alzheimer's disease. J. Alzheimers Dis. 33, S277-S281. doi: 10.3233/JAD-2012-129011
10. Bush, A. I., Pettingell, W., Paradis, M., and Tanzi, R. E. (1994). Modulation of a beta adhesiveness and secretase site cleavage by zinc. J. Biol. Chem. 269, 12152-12158.
11. Cataldo, A. M., Petanceska, S., Peterhoff, C. M., Terio, N. B., Epstein, C. J., Villar, A., et al. (2003). App gene dosage modulates endosomal abnormalities of Alzheimer's disease in a segmental trisomy 16 mouse model of down syndrome. J. Neurosci. 23, 6788-6792.
12. Cataldo, A. M., Peterhoff, C. M., Troncoso, J. C., Gomez-Isla, T., Hyman, B. T., and Nixon, R. A. (2000). Endocytic pathway abnormalities precede amyloid ß deposition in sporadic Alzheimer's disease and down syndrome: differential effects of apoe genotype and presenilin mutations. Am. J. Pathol. 157, 277-286. doi: 10.1016/s0002-9440(10)64538-5
13. Cater, M., Mcinnes, K., Li, Q., Volitakis, I., La Fontaine, S., Mercer, J., et al. (2008). Intracellular copper deficiency increases amyloid-beta secretion by diverse mechanisms. Biochem. J. 412, 141-152. doi: 10.1042/BJ20080103
14. Cheon, M. S., Dierssen, M., Kim, S. H., and Lubec, G. (2008). Protein expression of BACE1, BACE2 and APP in Down syndrome brains. Amino Acids 35, 339-343. doi: 10.1007/s00726-007-0618-9
15. Cole, T. B., Wenzel, H. J., Kafer, K. E., Schwatzkorin, P. A., and Palmiter, R. D. (1999). Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc. Natl. Acad. Sci. U S A 96, 1716-1721. doi: 10.1073/pnas.96.4.1716
16. Contestabile, A., Benfenati, F., and Gasparini, L. (2010). Communication breaks-down: from neurodevelopment defects to cognitive disabilities in down syndrome. Prog. Neurobiol. 91, 1-22. doi: 10.1016/j.pneurobio.2010.01.003
17. Dahms, S. O., Könnig, I., Roeser, D., Gührs, K.-H., Mayer, M. C., Kaden, D., et al. (2012). Metal binding dictates conformation and function of the amyloid precursor protein (APP) E2 domain. J. Mol. Biol. 416, 438-452. doi: 10.1016/j.jmb.2011.12.057
18. De Felice, F. G., Velasco, P. T., Lambert, M. P., Viola, K., Fernandez, S. J., Ferreira, S. T., et al. (2007). Aß 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, 11590-11601. doi: 10.1074/jbc.M607483200
19. Duce, J. A., Tsatsanis, A., Cater, M. A., James, S. A., Robb, E., Wikhe, K., et al. (2010). Iron-export ferroxidase activity of ß-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 142, 857-867. doi: 10.1016/j.cell.2010.08.014
20. Epstein, C. J. (1995). "The metabolic and molecular bases of inherited disease," in Down Syndrome (Trisomy 21), eds C. Scriver, A. L. Beaudet, W. S. Sly and D. Vale (New York: McGraw-Hill, Inc.), 749-794.
21. Ermak, G., Morgan, T. E., and Davies, K. J. (2001). Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer's disease. J. Biol. Chem. 276, 38787-38794. doi: 10.1074/jbc.m102829200
22. Ermak, G., Pritchard, M. A., Dronjak, S., Niu, B., and Davies, K. J. (2011). Do RCAN1 proteins link chronic stress with neurodegeneration? FASEB J. 25, 3306-3311. doi: 10.1096/fj.11-185728
23. Farrar, G., Altmann, P., Welch, S., Wychrij, O., Ghose, B., Lejeune, J., et al. (1990). Defective gallium-transferrin binding in Alzheimer disease and down syndrome: possible mechanism for accumulation of aluminium in brain. Lancet 335, 747-750. doi: 10.1016/0140-6736(90)90868-6
24. Finefrock, A. E., Bush, A. I., and Doraiswamy, P. M. (2003). Current status of metals as therapeutic targets in Alzheimer's disease. J. Am. Geriatr. Soc. 51, 1143-1148. doi: 10.1046/j.1532-5415.2003.51368.x
25. Frederickson, C. J., Klitenick, M. A., Manton, W. I., and Kirkpatrick, J. B. (1983). Cytoarchitectonic distribution of zinc in the hippocampus of man and the rat. Brain Res. 273, 335-339. doi: 10.1016/0006-8993(83)90858-2
26. Frederickson, C. J., Suh, S. W., Silva, D., Frederickson, C. J., and Thompson, R. B. (2000). Importance of zinc in the central nervous system: the zinc-containing neuron. J. Nutr. 130, 1471S-1483S.
27. Fuentes, J. J., Genesca, L., Kingsbury, T. J., Cunningham, K. W., Perez-Riba, M., Estivill, X., et al. (2000). DSCR1, overexpressed in down syndrome, is an inhibitor of calcineurin-mediated signaling pathways. Hum. Mol. Genet. 9, 1681-1690. doi: 10.1093/hmg/9.11.1681
28. Galdzicki, Z., Coan, E., Rapoport, S., and Stoll, J. (1998). Increased expression of voltage-activated calcium channels in cultured hippocampal neurons from mouse trisomy 16, a model for Down syndrome. Brain Res. Mol. Brain Res. 56, 200-206. doi: 10.1016/s0169-328x(98)00046-1
29. Gerlach, M., Ben-Shachar, D., Riederer, P., and Youdim, M. (1994). Altered brain metabolism of iron as a cause of neurodegenerative diseases? J. Neurochem. 63, 793-807. doi: 10.1046/j.1471-4159.1994.63030793.x
30. Greenberg, S., Bacskai, B., and Hyman, B. (2003). Alzheimer disease's double-edged vaccine. Nat. Med. 9, 389-390. doi: 10.1038/nm847
31. Hattori, M., Fujiyama, A., Taylor, T., Watanabe, H., Yada, T., Park, H.-S., et al. (2000). The DNA sequence of human chromosome 21. Nature 405, 311-319. doi: 10.1038/35012518
32. Huang, X., Atwood, C. S., Hartshorn, M. A., Multhaup, G., Scarpa, R. C., Cuajungco, M. P., et al. (1999). The Aβ peptide of Alzheimer's disease directlyproduces hydrogen peroxide through metal ion reduction. Biochemistry 38, 7609-7616. doi: 10.1021/bi990438f
33. Hyman, B. T., Van Hoesen, G. W., Kromer, L. J., and Damasio, A. R. (1986). Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann. Neurol. 20, 472-481. doi: 10.1002/ana.410200406
34. Ikeda, S., Yanagisawa, N., Allsop, D., and Glenner, G. G. (1989). Evidence of amyloid beta-protein immunoreactive early plaque lesions in Down's syndrome brains. Lab. Invest. 61, 133-137.
35. Jang, H., Arce, F. T., Ramachandran, S., Capone, R., Azimova, R., Kagan, B. L., et al. (2010). Truncated beta-amyloid peptide channels provide an alternative mechanism for Alzheimer's disease and down syndrome. Proc. Natl. Acad. Sci. U S A 107, 6538-6543. doi: 10.1073/pnas.0914251107
36. Kardos, J., Kovács, I., Hajós, F., Kálmán, M., and Simonyi, M. (1989). Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability. Neurosci. Lett. 103, 139-144. doi: 10.1016/0304-3940(89)90565-x
37. Klomp, L., Farhangrazi, Z. S., Dugan, L. L., and Gitlin, J. D. (1996). Ceruloplasmin gene expression in the murine central nervous system. J. Clin. Invest. 98, 207-215. doi: 10.1172/jci118768
38. Lei, P., Ayton, S., Finkelstein, D. I., Spoerri, L., Ciccotosto, G. D., Wright, D. K., et al. (2012). Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export. Nat. Med. 18, 291-295. doi: 10.1038/nm.2613
39. Lemere, C., Blusztajn, J., Yamaguchi, H., Wisniewski, T., Saido, T., and Selkoe, D. (1996). Sequence of deposition of heterogeneous amyloid ß-peptides and APO E in Down syndrome: implications for initial events in amyloid plaque formation. Neurobiol. Dis. 3, 16-32. doi: 10.1006/nbdi.1996.0003
40. Leveugle, B., Spik, G., Perl, D. P., Bouras, C., Fillit, H. M., and Hof, P. R. (1994). The iron-binding protein lactotransferrin is present in pathologic lesions in a variety of neurodegenerative disorders: a comparative immunohistochemical analysis. Brain Res. 650, 20-31. doi: 10.1016/0006-8993(94)90202-x
41. Loeffler, D., Connor, J., Juneau, P., Snyder, B., Kanaley, L., Demaggio, A., et al. (1995). Transferrin and iron in normal, Alzheimer's disease and Parkinson's disease brain regions. J. Neurochem. 65, 710-716. doi: 10.1046/j.1471-4159.1995.65020710.x
42. Lyubartseva, G., Smith, J. L., Markesbery, W. R., and Lovell, M. A. (2010). Alterations of zinc transporter proteins ZnT-1, ZnT-4 and ZnT-6 in preclinical Alzheimer's disease brain. Brain Pathol. 20, 343-350. doi: 10.1111/j.1750-3639.2009.00283.x
43. Ma, H., Xiong, H., Liu, T., Zhang, L., Godzik, A., and Zhang, Z. (2004). Aggregate formation and synaptic abnormality induced by DSCR1. J. Neurochem. 88, 1485-1496. doi: 10.1046/j.1471-4159.2003.02294.x
44. Mann, D. (1988). The pathological association between Down syndrome and Alzheimer disease. Mech. Ageing Dev. 43, 99-136. doi: 10.1016/0047-6374(88)90041-3
45. Mann, D. M., Jones, D., Prinja, D., and Purkiss, M. S. (1990). The prevalance of amyloid (A4) protein depositis within the cereblar and cerebellar cortex in Down's syndrome and Alzheimer's dosease. Acta Neuropathol. 80, 318-327. doi: 10.1007/bf00294651
46. Mattson, M. P., Barger, S. W., Cheng, B., Lieberburg, I., Smith-Swintosky, V. L., and Rydel, R. E. (1993a). beta-Amyloid precursor protein metabolites and loss of neuronal Ca2+ homeostasis in Alzheimer's disease. Trends Neurosci. 16, 409-414. doi: 10.1016/0166-2236(93)90009-b
47. Mattson, M. P., Tomaselli, K. J., and Rydel, R. E. (1993b). Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res. 621, 35-49. doi: 10.1016/0006-8993(93)90295-x
48. Maynard, C. J., Cappai, R., Volitakis, I., Cherny, R. A., White, A. R., Beyreuther, K., et al. (2002). Overexpression of Alzheimer's disease amyloid-ß opposes the age-dependent elevations of brain copper and iron. J. Biol. Chem. 277, 44670-44676. doi: 10.1074/jbc.m204379200
49. Mok, K. Y., Jones, E. L., Hanney, M., Harold, D., Sims, R., Williams, J., et al. (2014). Polymorphisms in BACE2 may affect the age of onset Alzheimer's dementia in Down syndrome. Neurobiol. Aging 35, 1513.e1-1513.e5. doi: 10.1016/j.neurobiolaging.2013.12.022
50. Nalbandyan, R. (1983). Copper in brain. Neurochem. Res. 8, 1211-1232. doi: 10.1007/bf00963993
51. Peiris, H., Raghupathi, R., Jessup, C. F., Zanin, M. P., Mohanasundaram, D., Mackenzie, K. D., et al. (2012). Increased expression of the glucose-responsive gene, RCAN1, causes hypoinsulinemia, β-cell dysfunction and diabetes. Endocrinology 153, 5212-5221. doi: 10.1210/en.2011-2149
52. Perluigi, M., di Domenico, F., Fiorini, A., Cocciolo, A., Giorgi, A., Foppoli, C., et al. (2011). Oxidative stress occurs early in Down syndrome pregnancy: a redox proteomics analysis of amniotic fluid. Proteomics Clin. Appl. 5, 167-178. doi: 10.1002/prca.201000121
53. Pike, C. J., Overman, M. J., and Cotman, C. W. (1995). Amino-terminal deletions enhance aggregation of ß-amyloid peptides in vitro. J. Biol. Chem. 270, 23895-23898. doi: 10.1074/jbc.270.41.23895
54. Piñero, D. J., and Connor, J. R. (2000). Iron in the brain: an important contributor in normal and diseased states. Neuroscientist 6, 435-453. doi: 10.1177/107385840000600607
55. Prasher, V. P., Farrer, M. J., Kessling, A. M., Fisher, E. M. C., West, R. J., Barber, P. C., et al. (1998). Molecular mapping of alzheimer-type dementia in Down's syndrome. Ann. Neurol. 43, 380-383. doi: 10.1002/ana.410430316
56. Sayre, L. M., Perry, G., Harris, P. L., Liu, Y., Schubert, K. A., and Smith, M. A. (2000). In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer's disease. J. Neurochem. 74, 270-279. doi: 10.1046/j.1471-4159.2000.0740270.x
57. Schupf, N., and Sergievsky, G. H. (2002). Genetic and host factors for dementia in Down's syndrome. Br. J. Psychiatry 180, 405-410. doi: 10.1192/bjp.180.5.405
58. Sensi, S. L., Paoletti, P., Koh, J.-Y., Aizenman, E., Bush, A. I., and Hershfinkel, M. (2011). The neurophysiology and pathology of brain zinc. J. Neurosci. 31, 16076-16085. doi: 10.1523/jneurosci.3454-11.2011
59. Sindreu, C., and Storm, D. R. (2011). Modulation of neuronal signal transduction and memory formation by synaptic zinc. Front. Behav. Neurosci. 5:68. doi: 10.3389/fnbeh.2011.00068
60. Smith, M. A., Wehr, K., Harris, P. L., Siedlak, S. L., Connor, J. R., and Perry, G. (1998). Abnormal localization of iron regulatory protein in Alzheimer's disease. Brain Res. 788, 232-236. doi: 10.1016/s0006-8993(98)00002-x
61. Stark, M. J. R. (1996). Yeast protein serine/threonine phosphatases: multiple roles and diverse regulation. Yeast 12, 1647-1675. doi: 10.1002/(SICI)1097-0061(199612)12:16<1647::AID-YEA71>3.0.CO;2-Q
62. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S., Mendiaz, E. A., Denis, P., et al. (1999). [Beta]-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741. doi: 10.1126/science.286.5440.735
63. White, A. R., Reyes, R., Mercer, J. F., Camakaris, J., Zheng, H., Bush, A. I., et al. (1999). Copper levels are increased in the cerebral cortex and liver of APP and APLP2 knockout mice. Brain Res. 842, 439-444. doi: 10.1016/s0006-8993(99)01861-2
64. Wilcock, D. M., and Griffin, W. S. (2013). Down's syndrome, neuroinflammation and Alzheimer neuropathogenesis. J. Neuroinflammation 10:84. doi: 10.1186/1742-2094-10-84