Lipid rafts: Linking prion protein to zinc transport and amyloid-β toxicity in Alzheimer's disease

Frontiers in Cell and Developmental Biology

Volumn 2, Issue AUG, 2014, Pages

  Watt, Nicole T ^a   Griffiths, Heledd H ^b   Hooper, Nigel M ^b  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Alzheimer's disease; AMPA receptor; Amyloid; Cholesterol; Prion protein; Zinc

Indexed keywords

EID: 84964562485     PISSN: None     EISSN: 2296634X     Source Type: Journal    
DOI: 10.3389/fcell.2014.00041     Document Type: Article

References (69)

1. 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
2. Barry, A. E., Klyubin, I., McDonald, J. M., Mably, A. J., Farrell, M. A., Scott, M., et al. (2011). Alzheimer's disease brain-derived amyloid-β-mediated inhibition of LTP in vivo is prevented by immunotargeting cellular prion protein. J. Neurosci. 31, 7259-7263. doi: 10.1523/JNEUROSCI.6500-10.2011
3. Beyersmann, D., and Haase, H. (2001). Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals 14, 331-341. doi: 10.1023/A:1012905406548
4. Brautigan, D. L., Bornstein, P., and Gallis, B. (1981). Phosphotyrosyl-protein phosphatase. Specific inhibition by Zn. J. Biol. Chem. 256, 6519-6522
5. Bush, A. I., Pettingell, W. H., Multhaup, G., d Paradis, M., Vonsattel, J. P., Gusella, J. F., et al. (1994). Rapid induction of Alzheimer Aβ amyloid formation by zinc. Science 265, 1464-1467. doi: 10.1126/science.8073293
6. Calella, A. M., Farinelli, M., Nuvolone, M., Mirante, O., Moos, R., Falsig, J., et al. (2010). Prion protein and Aβ-related synaptic toxicity impairment. EMBO Mol. Med. 2, 306-314. doi: 10.1002/emmm.201000082
7. Chung, E., Ji, Y., Sun, Y., Kascsak, R. J., Kascsak, R. B., Mehta, P. D., et al. (2010). Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer's disease model mouse. BMC Neurosci. 11:130. doi: 10.1186/1471-2202-11-130
8. Cisse, M., and Mucke, L. (2009). Alzheimer's disease: a prion protein connection. Nature 457, 1090-1091. doi: 10.1038/4571090a
9. Cousins, R. J., Liuzzi, J. P., and Lichten, L. A. (2006). Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. 281, 24085-24089. doi: 10.1074/jbc.R600011200
10. Deshpande, A., Kawai, H., Metherate, R., Glabe, C. G., and Busciglio, J. (2009). A role for synaptic zinc in activity-dependent Aβ oligomer formation and accumulation at excitatory synapses. J. Neurosci. 29, 4004-4015. doi: 10.1523/JNEUROSCI.5980-08.2009
11. Di Paolo, G., and Kim, T.-W. (2011). Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat. Rev. Neurosci. 12, 284-296. doi: 10.1038/nrn3012
12. Dong, J., Atwood, C. S., Anderson, V. E., Siedlak, S. L., Smith, M. A., Perry, G., et al. (2003). Metal binding and oxidation of amyloid-β within isolated senile plaque cores: Raman microscopic evidence. Biochemistry 42, 2768-2773. doi: 10.1021/bi0272151
13. Ehsani, S., Salehzadeh, A., Huo, H., Reginold, W., Pocanschi, C. L., Ren, H., et al. (2012). LIV-1 ZIP ectodomain shedding in prion-infected mice resembles cellular response to transition metal starvation. J. Mol. Biol. 422, 556-574. doi: 10.1016/j.jmb.2012.06.003
14. Esler, W. P., Stimson, E. R., Jennings, J. M., Ghilardi, J. R., Mantyh, P. W., and Maggio, J. E. (1996). Zinc-induced aggregation of human and rat β-amyloid peptides in vitro. J. Neurochem. 66, 723-732. doi: 10.1046/j.1471-4159.1996.66020723.x
15. Frederickson, C. J., Koh, J. Y., and Bush, A. I. (2005). The neurobiology of zinc in health and disease. Nat. Rev. Neurosci. 6, 449-462. doi: 10.1038/nrn1671
16. Freir, D. B., Nicoll, A. J., Klyubin, I., Panico, S., McDonald, J. M., Risse, E., et al. (2011). Interaction between prion protein and toxic amyloid β assemblies can be therapeutically targeted at multiple sites. Nat. Commun. 2, 336. doi: 10.1038/ncomms1341
17. Friedlich, A. L., Lee, J. Y., van Groen, T., Cherny, R. A., Volitakis, I., Cole, T. B., et al. (2004). Neuronal zinc exchange with the blood vessel wall promotes cerebral amyloid angiopathy in an animal model of Alzheimer's disease. J. Neurosci. 24, 3453-3459. doi: 10.1523/JNEUROSCI.0297-04.2004
18. Fuentealba, R. A., Liu, Q., Zhang, J., Kanekiyo, T., Hu, X., Lee, J. M., et al. (2010). Low-density lipoprotein receptor-related protein 1 (LRP1) mediates neuronal Aβ 42 uptake and lysosomal trafficking. PLoS ONE 5:e11884. doi: 10.1371/journal.pone.0011884
19. Gaudreault, S. B., Dea, D., and Poirier, J. (2004). Increased caveolin-1 expression in Alzheimer's disease brain. Neurobiol. Aging 25, 753-759. doi: 10.1016/j.neurobiolaging.2003.07.004
20. Gimbel, D. A., Nygaard, H. B., Coffey, E. E., Gunther, E. C., Lauren, J., Gimbel, Z. A., et al. (2010). Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J. Neurosci. 30, 6367-6374. doi: 10.1523/JNEUROSCI.0395-10.2010
21. Grabrucker, A. M., Knight, M. J., Proepper, C., Bockmann, J., Joubert, M., Rowan, M., et al. (2011). Concerted action of zinc and ProSAP/Shank in synaptogenesis and synapse maturation. EMBO J. 30, 569-581. doi: 10.1038/emboj.2010.336
22. Guirland, C., and Zheng, J. Q. (2007). Membrane lipid rafts and their role in axon guidance. Adv. Exp. Med. Biol. 621, 144-155. doi: 10.1007/978-0-387-76715-4_11
23. Head, B. P., Peart, J. N., Panneerselvam, M., Yokoyama, T., Pearn, M. L., Niesman, I. R., et al. (2010). Loss of caveolin-1 accelerates neurodegeneration and aging. PloS ONE 5:e15697. doi: 10.1371/journal.pone.0015697
24. Hering, H., Lin, C. C., and Sheng, M. (2003). Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262-3271
25. Hu, N.-W., Nicoll, A. J., Zhang, D., Mably, A. J., O'Malley, T., Purro, S. A., et al. (2014). mGlu5 receptors and cellular prion protein mediate amyloid-β-facilitated synaptic long-term depression in vivo. Nat. Commun. 5:3374. doi: 10.1038/ncomms4374
26. Kanekiyo, T., Zhang, J., Liu, Q., Liu, C.-C., Zhang, L., and Bu, G. (2011). Heparan sulphate proteoglycan and the low-density lipoprotein receptor-related protein 1 constitute major pathways for neuronal amyloid-β uptake. J. Neurosci. 31, 1644-1651. doi: 10.1523/JNEUROSCI.5491-10.2011
27. Kessels, H. W., Nguyen, L. N., Nabavi, S., and Malinow, R. (2010). The prion protein as a receptor for amyloid-β. Nature 466, E3-E4; discussion: E4-E5. doi: 10.1038/nature09217
28. Khan, G. M., Tong, M., Jhun, M., Arora, K., and Nichols, R. A. (2010). β-Amyloid activates presynaptic a7 nicotinic acetylcholine receptors reconstituted into a model nerve cell system: involvement of lipid rafts. Eur. J. Neurosci. 31, 788-796. doi: 10.1111/j.1460-9568.2010.07116.x
29. Kozlowski, H., Luczkowski, M., and Remelli, M. (2010). Prion proteins and copper ions. Biological and chemical controversies. Dalton Trans. 39, 6371-6385. doi: 10.1039/c001267j
30. Lai, A. Y., and McLaurin, J. (2010). Mechanisms of amyloid-β peptide uptake by neurons: the role of lipid rafts and lipid raft-associated proteins. Int. J. Alzheimers Dis. 2011:548380. doi: 10.4061/2011/548380
31. Larson, M., Sherman, M. A., Amar, F., Nuvolone, M., Schneider, J. A., Bennett, D. A., et al. (2012). The complex PrPc-Fyn couples human oligomeric Aβ with pathological Tau changes in Alzheimer's disease. J. Neurosci. 32, 16857-16871. doi: 10.1523/JNEUROSCI.1858-12.2012
32. Lauren, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., and Strittmatter, S. M. (2009). Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers. Nature 457, 1128-1132. doi: 10.1038/nature07761
33. Lee, J. Y., Cole, T. B., Palmiter, R. D., Suh, S. W., and Koh, J. Y. (2002). 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, 7705-7710. doi: 10.1073/pnas.092034699
34. Linden, R., Martins, V. R., Prado, M. A., Cammarota, M., Izquierdo, I., and Brentani, R. R. (2008). Physiology of the prion protein. Physiol. Rev. 88, 673-728. doi: 10.1152/physrev.00007.2007
35. Lu, T., Aron, L., Zullo, J., Pan, Y., Kim, H., Chen, Y., et al. (2014). REST and stress resistance in ageing and Alzheimer's disease. Nature 507, 448-454. doi: 10.1038/nature13163
36. Mocchegiani, E., Bertoni-Freddari, C., Marcellini, F., and Malavolta, M. (2005). Brain, aging and neurodegeneration: role of zinc ion availability. Prog. Neurobiol. 75, 367-390. doi: 10.1016/j.pneurobio.2005.04.005
37. Nykjaer, A., and Willnow, T. E. (2002). The low-density lipoprotein receptor gene family: a cellular Swiss army knife? Trends Cell Biol. 12, 273-280. doi: 10.1016/S0962-8924(02)02282-1
38. Ohno-Iwashita, Y., Shimada, Y., Hayashi, M., and Inomata, M. (2010). Plasma membrane microdomains in aging and disease. Geriatr. Gerontol. Int. 10 Suppl. 1, S41-S52. doi: 10.1111/j.1447-0594.2010.00600.x
39. Parkin, E. T., Tan, F., Skidgel, R. A., Turner, A. J., and Hooper, N. M. (2003). The ectodomain shedding of angiotensin-converting enzyme is independent of its localisation in lipid rafts. J. Cell Sci. 116, 3079-3087. doi: 10.1242/jcs.00626
40. Plum, L. M., Rink, L., and Haase, H. (2010). The essential toxin: impact of zinc on human health. Int. J. Environ. Res. Public health 7, 1342-1365. doi: 10.3390/ijerph7041342
41. Pushie, M. J., Pickering, I. J., Martin, G. R., Tsutsui, S., Jirik, F. R., and George, G. N. (2011). Prion protein expression level alters regional copper, iron and zinc content in the mouse brain. Metallomics 3, 206-214. doi: 10.1039/c0mt00037j
42. Renner, M., Lacor, P. N., Velasco, P. T., Xu, J., Contractor, A., Klein, W. L., et al. (2010). Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron 66, 739-754. doi: 10.1016/j.neuron.2010.04.029
43. Rushworth, J. V., Griffiths, H. H., Watt, N. T., and Hooper, N. M. (2013). Prion protein-mediated toxicity of amyloid-β oligomers requires lipid rafts and the transmembrane LRP1. J. Biol. Chem. 288, 8935-8951. doi: 10.1074/jbc.M112.400358
44. Rushworth, J. V., and Hooper, N. M. (2010). Lipid rafts: linking Alzheimer's amyloid-β production, aggregation, and toxicity at neuronal membranes. Int. J. Alzheimers Dis. 2011, 603052. doi: 10.4061/2011/603052
45. Saito, T., Takahashi, K., Nakagawa, N., Hosokawa, T., Kurasaki, M., Yamanoshita, O., et al. (2000). Deficiencies of hippocampal Zn and ZnT3 accelerate brain aging of Rat. Biochem. Biophys. Res. Commun. 279, 505-511. doi: 10.1006/bbrc.2000.3946
46. Sales, N., Rodolfo, K., Hassig, R., Faucheux, B., Di Giamberardino, L., and Moya, K. L. (1998). Cellular prion protein localization in rodent and primate brain. Eur. J. Neurosci. 10, 2464-2471. doi: 10.1046/j.1460-9568.1998.00258.x
47. Schmitt-Ulms, G., Ehsani, S., Watts, J. C., Westaway, D., and Wille, H. (2009). Evolutionary descent of prion genes from the ZIP family of metal ion transporters. PLoS ONE 4:e7208. doi: 10.1371/journal.pone.0007208
48. Sensi, S. L., Paoletti, P., Bush, A. I., and Sekler, I. (2009). Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 10, 780-791. doi: 10.1038/nrn2734
49. Singh, N., Haldar, S., Tripathi, A. K., McElwee, M. K., Horback, K., and Beserra, A. (2014). Iron in neurodegenerative disorders of protein misfolding: a case of prion disorders and Parkinson's disease. Antioxid. Redox Signal. 21, 471-484. doi: 10.1089/ars.2014.5874
50. Solis, G. P., Malaga-Trillo, E., Plattner, H., and Stuermer, C. A. (2010). Cellular roles of the prion protein in association with reggie/flotillin microdomains. Front. Biosci. 15, 1075-1085. doi: 10.2741/3662
51. Stellato, F., Spevacek, A., Proux, O., Minicozzi, V., Millhauser, G., and Morante, S. (2011). Zinc modulates copper coordination mode in prion protein octa-repeat subdomains. Eur. Biophys. J. 40, 1259-1270. doi: 10.1007/s00249-011-0713-4
52. Stys, P. K., You, H., and Zamponi, G. W. (2012). Copper-dependent regulation of NMDA receptors by cellular prion protein: implications for neurodegenerative disorders. J. Physiol. 590, 1357-1368. doi: 10.1113/jphysiol.2011.225276
53. Szewczyk, B. (2013). Zinc homeostasis and neurodegenerative disorders. Front. Aging Neurosci. 5:33. doi: 10.3389/fnagi.2013.00033
54. Taylor, D. R., and Hooper, N. M. (2007). The low-density lipoprotein receptor-related protein 1 (LRP1) mediates the endocytosis of the cellular prion protein. Biochem. J. 402, 17-23. doi: 10.1042/BJ20061736
55. Taylor, D. R., Watt, N. T., Perera, W. S., and Hooper, N. M. (2005). Assigning functions to distinct regions of the N-terminus of the prion protein that are involved in its copper-stimulated, clathrin-dependent endocytosis. J. Cell Sci. 118, 5141-5153. doi: 10.1242/jcs.02627
56. Toth, K. (2011). Zinc in neurotransmission. Annu. Rev. Nutr. 31, 139-153. doi: 10.1146/annurev-nutr-072610-145218
57. Um, J. W., Kaufman, A. C., Kostylev, M., Heiss, J. K., Stagi, M., Takahashi, H., et al. (2013). Metabotropic glutamate receptor 5 is a coreceptor for Alzheimer Aβ oligomer bound to cellular prion protein. Neuron 79, 887-902. doi: 10.1016/j.neuron.2013.06.036
58. Um, J. W., Nygaard, H. B., Heiss, J. K., Kostylev, M. A., Stagi, M., Vortmeyer, A., et al. (2012). Alzheimer amyloid-β oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat. Neurosci. 15, 1227-1235. doi: 10.1038/nn.3178
59. Wang, F., Dufner-Beattie, J., Kim, B. E., Petris, M. J., Andrews, G., and Eide, D. J. (2004). Zinc-stimulated endocytosis controls activity of the mouse ZIP1 and ZIP3 zinc uptake transporters. J. Biol. Chem. 279, 24631-24639. doi: 10.1074/jbc.M400680200
60. Watt, N. T., Griffiths, H. H., and Hooper, N. M. (2013). Neuronal zinc regulation and the prion protein. Prion 7, 203-208. doi: 10.4161/pri.24503
61. Watt, N. T., Taylor, D. R., Kerrigan, T. L., Griffiths, H. H., Rushworth, J. V., Whitehouse, I. J., et al. (2012). Prion protein facilitates uptake of zinc into neuronal cells. Nat. Commun. 3, 1134. doi: 10.1038/ncomms2135
62. Watt, N. T., Whitehouse, I. J., and Hooper, N. M. (2010). The role of zinc in Alzheimer's disease. Int. J. Alzheimers Dis. 2011:971021. doi: 10.4061/2011/971021
63. Whitehouse, I. J., Jackson, C. D., Turner, A. J., and Hooper, N. M. (2010). Prion protein is reduced in aging and in sporadic but not in familial Alzheimer's disease. J. Alzheimers Dis. 22, 1023-1031. doi: 10.3233/JAD-2010-101071
64. Whitehouse, I. J., Miners, J. S., Glennon, E. B., Kehoe, P. G., Love, S., Kellett, K. A., et al. (2013). Prion protein is decreased in Alzheimer's brain and inversely correlates with BACE1 activity, amyloid-β levels and Braak stage. PLoS ONE 8:e59554. doi: 10.1371/journal.pone.0059554
65. Williamson, R., Usardi, A., Hanger, D. P., and Anderton, B. H. (2008). Membrane-bound β-amyloid oligomers are recruited into lipid rafts by a Fyn-dependent mechanism. FASEB J. 22, 1552-1559. doi: 10.1096/fj.07-9766com
66. Willmann, R., Pun, S., Stallmach, L., Sadasivam, G., Santos, A. F., Caroni, P., et al. (2006). Cholesterol and lipid microdomains stabilize the postsynapse at the neuromuscular junction. EMBO J. 25, 4050-4060. doi: 10.1038/sj.emboj.7601288
67. Wilson, M., Hogstrand, C., and Maret, W. (2012). Picomolar concentrations of free zinc(II) ions regulate receptor protein-tyrosine phosphatase β activity. J. Biol. Chem. 287, 9322-9326. doi: 10.1074/jbc.C111.320796
68. Wong, B. X., Hung, Y. H., Bush, A. I., and Duce, J. A. (2014). Metals and cholesterol: two sides of the same coin in Alzheimer's disease pathology. Front. Aging Neurosci. 6:91. doi: 10.3389/fnagi.2014.00091
69. Wong, C. P., Magnusson, K. R., and Ho, E. (2013). Increased inflammatory response in aged mice is associated with age-related zinc deficiency and zinc transporter dysregulation. J. Nutr. Biochem. 24, 353-359. doi: 10.1016/j.jnutbio.2012.07.005