Selective vulnerability to neurodegenerative disease: The curious case of Prion Protein

DMM Disease Models and Mechanisms

Volumn 7, Issue 1, 2014, Pages 21-29

  Jackson, Walker S ^a  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Huntington's disease; Knock in mice; Neurodegeneration; Neuropathology; Prion diseases; Spinocerebellar ataxia

Indexed keywords

METAL; PRION PROTEIN;

BRAIN REGION; DEGENERATIVE DISEASE; GENE MUTATION; HUMAN; HUNTINGTON CHOREA; MICROENVIRONMENT; NEUROPATHOLOGY; PARKINSON DISEASE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SPINOCEREBELLAR DEGENERATION;

HUNTINGTON'S DISEASE; KNOCK-IN MICE; NEURODEGENERATION; NEUROPATHOLOGY; PRION DISEASES; SPINOCEREBELLAR ATAXIA;

ALZHEIMER DISEASE; ANIMALS; BRAIN; HUMANS; METALS; MICE; MOLECULAR CHAPERONES; MUTATION; NEURODEGENERATIVE DISEASES; PARKINSON DISEASE; PRION DISEASES; PRIONS; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN FOLDING; RIBOSOMES;

EID: 84892430377     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.012146     Document Type: Review

References (112)

1. Aguzzi, A. and Rajendran, L. (2009). The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64, 783-790.
2. Aguzzi, A., Barres, B. A. and Bennett, M. L. (2013). Microglia: scapegoat, saboteur, or something else? Science 339, 156-161.
3. Aidt, F. H., Hasholt, L. F., Christiansen, M. and Laursen, H. (2013). Localization of A11-reactive oligomeric species in prion diseases. Histopathology 62, 994-1001.
4. Alais, S., Simoes, S., Baas, D., Lehmann, S., Raposo, G., Darlix, J. L. and Leblanc, P. (2008). Mouse neuroblastoma cells release prion infectivity associated with exosomal vesicles. Biol. Cell 100, 603-618.
5. Apetri, A. C., Surewicz, K. and Surewicz, W. K. (2004). The effect of diseaseassociated mutations on the folding pathway of human prion protein. J. Biol. Chem. 279, 18008-18014.
6. Arcelli, P., Frassoni, C., Regondi, M. C., De Biasi, S. and Spreafico, R. (1997). GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Res. Bull. 42, 27-37.
7. Ashok, A. and Hegde, R. S. (2009). Selective processing and metabolism of diseasecausing mutant prion proteins. PLoS Pathog. 5, e1000479.
8. Asuni, A. A., Pankiewicz, J. E. and Sadowski, M. J. (2013). Differential molecular chaperone response associated with various mouse adapted scrapie strains. Neurosci. Lett. 538, 26-31.
9. Bolmont, T., Clavaguera, F., Meyer-Luehmann, M., Herzig, M. C., Radde, R., Staufenbiel, M., Lewis, J., Hutton, M., Tolnay, M. and Jucker, M. (2007). Induction of tau pathology by intracerebral infusion of amyloid-beta -containing brain extract and by amyloid-beta deposition in APP x Tau transgenic mice. Am. J. Pathol. 171, 2012-2020.
10. Borchelt, D. R., Davis, J., Fischer, M., Lee, M. K., Slunt, H. H., Ratovitsky, T., Regard, J., Copeland, N. G., Jenkins, N. A., Sisodia, S. S. et al. (1996). A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet. Anal. 13, 159-163.
11. Braak, H. and Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239-259.
12. Bremer, J., Baumann, F., Tiberi, C., Wessig, C., Fischer, H., Schwarz, P., Steele, A. D., Toyka, K. V., Nave, K. A., Weis, J. et al. (2010). Axonal prion protein is required for peripheral myelin maintenance. Nat. Neurosci. 13, 310-318.
13. Brown, L. R. and Harris, D. A. (2003). Copper and zinc cause delivery of the prion protein from the plasma membrane to a subset of early endosomes and the Golgi. J. Neurochem. 87, 353-363.
14. Brown, D. R., Qin, K., Herms, J. W., Madlung, A., Manson, J., Strome, R., Fraser, P. E., Kruck, T., von Bohlen, A., Schulz-Schaeffer, W. et al. (1997). The cellular prion protein binds copper in vivo. Nature 390, 684-687.
15. Brundin, P., Melki, R. and Kopito, R. (2010). Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat. Rev. Mol. Cell Biol. 11, 301-307.
16. Bugiani, O., Giaccone, G., Piccardo, P., Morbin, M., Tagliavini, F. and Ghetti, B. (2000). Neuropathology of Gerstmann-Sträussler-Scheinker disease. Microsc. Res. Tech. 50, 10-15.
17. Calella, A. M., Farinelli, M., Nuvolone, M., Mirante, O., Moos, R., Falsig, J., Mansuy, I. M. and Aguzzi, A. (2010). Prion protein and Abeta-related synaptic toxicity impairment. EMBO Mol Med 2, 306-314.
18. Canello, T., Friedman-Levi, Y., Mizrahi, M., Binyamin, O., Cohen, E., Frid, K. and Gabizon, R. (2012). Copper is toxic to PrP-ablated mice and exacerbates disease in a mouse model of E200K genetic prion disease. Neurobiol. Dis. 45, 1010-1017.
19. Capellari, S., Parchi, P., Russo, C. M., Sanford, J., Sy, M. S., Gambetti, P. and Petersen, R. B. (2000a). Effect of the E200K mutation on prion protein metabolism. Comparative study of a cell model and human brain. Am. J. Pathol. 157, 613-622.
20. Capellari, S., Zaidi, S. I., Long, A. C., Kwon, E. E. and Petersen, R. B. (2000b). The Thr183Ala Mutation, not the loss of the first glycosylation site, alters the physical properties of the prion protein. J. Alzheimers Dis. 2, 27-35.
21. Capellari, S., Strammiello, R., Saverioni, D., Kretzschmar, H. and Parchi, P. (2011). Genetic Creutzfeldt-Jakob disease and fatal familial insomnia: insights into phenotypic variability and disease pathogenesis. Acta Neuropathol. 121, 21-37.
22. Chan, C. S., Guzman, J. N., Ilijic, E., Mercer, J. N., Rick, C., Tkatch, T., Meredith, G. E. and Surmeier, D. J. (2007). 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447, 1081-1086.
23. Chiesa, R., Piccardo, P., Biasini, E., Ghetti, B. and Harris, D. A. (2008). Aggregated, wild-type prion protein causes neurological dysfunction and synaptic abnormalities. J. Neurosci. 28, 13258-13267.
24. Costanzo, M., Abounit, S., Marzo, L., Danckaert, A., Chamoun, Z., Roux, P. and Zurzolo, C. (2013). Transfer of polyglutamine aggregates in neuronal cells occurs in tunneling nanotubes. J. Cell Sci. 126, 3678-3685.
25. Cushman, M., Johnson, B. S., King, O. D., Gitler, A. D. and Shorter, J. (2010). Prion-like disorders: blurring the divide between transmissibility and infectivity. J. Cell Sci. 123, 1191-1201.
26. Danzer, K. M., Kranich, L. R., Ruf, W. P., Cagsal-Getkin, O., Winslow, A. R., Zhu, L., Vanderburg, C. R. and McLean, P. J. (2012). Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol. Neurodegener. 7, 42.
27. Dossena, S., Imeri, L., Mangieri, M., Garofoli, A., Ferrari, L., Senatore, A., Restelli, E., Balducci, C., Fiordaliso, F., Salio, M. et al. (2008). Mutant prion protein expression causes motor and memory deficits and abnormal sleep patterns in a transgenic mouse model. Neuron 60, 598-609.
28. Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S. D., Ntzouni, M., Margaritis, L. H., Stefanis, L. and Vekrellis, K. (2010). Cell-produced alphasynuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 30, 6838-6851.
29. Faas, H., Jackson, W. S., Borkowski, A. W., Wang, X., Ma, J., Lindquist, S. and Jasanoff, A. (2010). Context-dependent perturbation of neural systems in transgenic mice expressing a cytosolic prion protein. Neuroimage 49, 2607-2617.
30. Francis, P. T., Palmer, A. M., Snape, M. and Wilcock, G. K. (1999). The cholinergic hypothesis of Alzheimer's disease: a review of progress. J. Neurol. Neurosurg. Psychiatry 66, 137-147.
31. Friedman-Levi, Y., Meiner, Z., Canello, T., Frid, K., Kovacs, G. G., Budka, H., Avrahami, D. and Gabizon, R. (2011). Fatal prion disease in a mouse model of genetic E200K Creutzfeldt-Jakob disease. PLoS Pathog. 7, e1002350.
32. Frost, B. and Diamond, M. I. (2010). Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 11, 155-159.
33. Gambetti, P., Parchi, P., Petersen, R. B., Chen, S. G. and Lugaresi, E. (1995). Fatal familial insomnia and familial Creutzfeldt-Jakob disease: clinical, pathological and molecular features. Brain Pathol. 5, 43-51.
34. Gambetti, P., Kong, Q., Zou, W., Parchi, P. and Chen, S. G. (2003). Sporadic and familial CJD: classification and characterisation. Br. Med. Bull. 66, 213-239.
35. Ghetti, B., Tagliavini, F., Giaccone, G., Bugiani, O., Frangione, B., Farlow, M. R. and Dlouhy, S. R. (1994). Familial Gerstmann-Sträussler- Scheinker disease with neurofibrillary tangles. Mol. Neurobiol. 8, 41-48.
36. Glabe, C. G. (2006). Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol. Aging 27, 570-575.
37. Goh, A. X., Li, C., Sy, M. S. and Wong, B. S. (2007). Altered prion protein glycosylation in the aging mouse brain. J. Neurochem. 100, 841-854.
38. Gousset, K. and Zurzolo, C. (2009). Tunnelling nanotubes: a highway for prion spreading? Prion 3, 94-98.
39. Gousset, K., Schiff, E., Langevin, C., Marijanovic, Z., Caputo, A., Browman, D. T., Chenouard, N., de Chaumont, F., Martino, A., Enninga, J. et al. (2009). Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 11, 328-336.
40. Grad, L. I., Guest, W. C., Yanai, A., Pokrishevsky, E., O'Neill, M. A., Gibbs, E., Semenchenko, V., Yousefi, M., Wishart, D. S., Plotkin, S. S. et al. (2011). Intermolecular transmission of superoxide dismutase 1 misfolding in living cells. Proc. Natl. Acad. Sci. USA 108, 16398-16403.
41. Graveland, G. A., Williams, R. S. and DiFiglia, M. (1985). Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science 227, 770-773.
42. Guest, W. C., Silverman, J. M., Pokrishevsky, E., O'Neill, M. A., Grad, L. I. and Cashman, N. R. (2011). Generalization of the prion hypothesis to other neurodegenerative diseases: an imperfect fit. J. Toxicol. Environ. Health A 74, 1433-1459.
43. Haigh, C. L., Lewis, V. A., Vella, L. J., Masters, C. L., Hill, A. F., Lawson, V. A. and Collins, S. J. (2009). PrPC-related signal transduction is influenced by copper, membrane integrity and the alpha cleavage site. Cell Res. 19, 1062-1078.
44. Haraguchi, T., Fisher, S., Olofsson, S., Endo, T., Groth, D., Tarentino, A., Borchelt, D. R., Teplow, D., Hood, L., Burlingame, A. et al. (1989). Asparagine-linked glycosylation of the scrapie and cellular prion proteins. Arch. Biochem. Biophys. 274, 1-13.
45. Harris, J. A., Devidze, N., Verret, L., Ho, K., Halabisky, B., Thwin, M. T., Kim, D., Hamto, P., Lo, I., Yu, G. Q. et al. (2010). Transsynaptic progression of amyloid-β- induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 68, 428-441.
46. Hesketh, S., Sassoon, J., Knight, R. and Brown, D. R. (2008). Elevated manganese levels in blood and CNS in human prion disease. Mol. Cell. Neurosci. 37, 590-598.
47. Hofmann, J. P., Denner, P., Nussbaum-Krammer, C., Kuhn, P. H., Suhre, M. H., Scheibel, T., Lichtenthaler, S. F., Schätzl, H. M., Bano, D. and Vorberg, I. M. (2013). Cell-to-cell propagation of infectious cytosolic protein aggregates. Proc. Natl. Acad. Sci. USA 110, 5951-5956.
48. Hsiao, K. K., Scott, M., Foster, D., Groth, D. F., DeArmond, S. J. and Prusiner, S. B. (1990). Spontaneous neurodegeneration in transgenic mice with mutant prion protein. Science 250, 1587-1590.
49. Hyman, B. T., Van Hoesen, G. W., Damasio, A. R. and Barnes, C. L. (1984). Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225, 1168-1170.
50. Ivanova, L., Barmada, S., Kummer, T. and Harris, D. A. (2001). Mutant prion proteins are partially retained in the endoplasmic reticulum. J. Biol. Chem. 276, 42409-42421.
51. Jackson, W. S., Borkowski, A. W., Faas, H., Steele, A. D., King, O. D., Watson, N., Jasanoff, A. and Lindquist, S. (2009). Spontaneous generation of prion infectivity in fatal familial insomnia knockin mice. Neuron 63, 438-450.
52. Jackson, W. S., Borkowski, A. W., Watson, N. E., King, O. D., Faas, H., Jasanoff, A. and Lindquist, S. (2013). Profoundly different prion diseases in knock-in mice carrying single PrP codon substitutions associated with human diseases. Proc. Natl. Acad. Sci. USA 110, 14759-14764.
53. Jucker, M. and Walker, L. C. (2011). Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann. Neurol. 70, 532-540.
54. Kane, M. D., Lipinski, W. J., Callahan, M. J., Bian, F., Durham, R. A., Schwarz, R. D., Roher, A. E. and Walker, L. C. (2000). Evidence for seeding of beta -amyloid by intracerebral infusion of Alzheimer brain extracts in beta-amyloid precursor proteintransgenic mice. J. Neurosci. 20, 3606-3611.
55. Karapetyan, Y. E., Saá, P., Mahal, S. P., Sferrazza, G. F., Sherman, A., Salès, N., Weissmann, C. and Lasmézas, C. I. (2009). Prion strain discrimination based on rapid in vivo amplification and analysis by the cell panel assay. PLoS ONE 4, e5730.
56. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W. and Glabe, C. G. (2003). Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489.
57. Khosravani, H., Zhang, Y., Tsutsui, S., Hameed, S., Altier, C., Hamid, J., Chen, L., Villemaire, M., Ali, Z., Jirik, F. R. et al. (2008). Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. J. Cell Biol. 181, 551-565.
58. Kondrashov, N., Pusic, A., Stumpf, C. R., Shimizu, K., Hsieh, A. C., Xue, S., Ishijima, J., Shiroishi, T. and Barna, M. (2011). Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145, 383-397.
59. Kovács, G. G., Trabattoni, G., Hainfellner, J. A., Ironside, J. W., Knight, R. S. and Budka, H. (2002). Mutations of the prion protein gene phenotypic spectrum. J. Neurol. 249, 1567-1582.
60. Kralovicova, S., Fontaine, S. N., Alderton, A., Alderman, J., Ragnarsdottir, K. V., Collins, S. J. and Brown, D. R. (2009). The effects of prion protein expression on metal metabolism. Mol. Cell. Neurosci. 41, 135-147.
61. Kuczius, T. and Kelsch, R. (2013). The effect of copper and zinc binding on the solubility and resistance to proteolysis of physiological prion protein PrP depends on the tissue source and the PrP glycotypes. J. Cell. Biochem. 114, 2690-2698.
62. Larson, M., Sherman, M. A., Amar, F., Nuvolone, M., Schneider, J. A., Bennett, D. A., Aguzzi, A. and Lesné, S. E. (2012). The complex PrP(c)-Fyn couples human oligomeric Aβ with pathological tau changes in Alzheimer's disease. J. Neurosci. 32, 16857-16871.
63. Laurén, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W. and Strittmatter, S. M. (2009). Cellular prion protein mediates impairment of synaptic plasticity by amyloidbeta oligomers. Nature 457, 1128-1132.
64. Lee, S., Kim, W., Li, Z. and Hall, G. F. (2012). Accumulation of vesicle-associated human tau in distal dendrites drives degeneration and tau secretion in an in situ cellular tauopathy model. Int. J. Alzheimers Dis. 2012, 172837.
65. Li, J. Y., Englund, E., Holton, J. L., Soulet, D., Hagell, P., Lees, A. J., Lashley, T., Quinn, N. P., Rehncrona, S., Björklund, A. et al. (2008). Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat. Med. 14, 501-503.
66. Lin, C. H., Tallaksen-Greene, S., Chien, W. M., Cearley, J. A., Jackson, W. S., Crouse, A. B., Ren, S., Li, X. J., Albin, R. L. and Detloff, P. J. (2001). Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum. Mol. Genet. 10, 137-144.
67. Luk, K. C., Kehm, V. M., Zhang, B., O'Brien, P., Trojanowski, J. Q. and Lee, V. M. (2012). Intracerebral inoculation of pathological α-synuclein initiates a rapidly progressive neurodegenerative α-synucleinopathy in mice. J. Exp. Med. 209, 975-986.
68. Marzo, L., Gousset, K. and Zurzolo, C. (2012). Multifaceted roles of tunneling nanotubes in intercellular communication. Front Physiol 3, 72.
69. Meyer-Luehmann, M., Stalder, M., Herzig, M. C., Kaeser, S. A., Kohler, E., Pfeifer, M., Boncristiano, S., Mathews, P. M., Mercken, M., Abramowski, D. et al. (2003). Extracellular amyloid formation and associated pathology in neural grafts. Nat. Neurosci. 6, 370-377.
70. Meyer-Luehmann, M., Coomaraswamy, J., Bolmont, T., Kaeser, S., Schaefer, C., Kilger, E., Neuenschwander, A., Abramowski, D., Frey, P., Jaton, A. L. et al. (2006). Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 313, 1781-1784.
71. Moleres, F. J. and Velayos, J. L. (2007). The neurochemical nature of PrP(c)- containing cells in the rat brain. Brain Res. 1174, 143-151.
72. Moreno, J. A., Radford, H., Peretti, D., Steinert, J. R., Verity, N., Martin, M. G., Halliday, M., Morgan, J., Dinsdale, D., Ortori, C. A. et al. (2012). Sustained translational repression by eIF2α-P mediates prion neurodegeneration. Nature 485, 507-511.
73. Petersen, R. B., Parchi, P., Richardson, S. L., Urig, C. B. and Gambetti, P. (1996). Effect of the D178N mutation and the codon 129 polymorphism on the metabolism of the prion protein. J. Biol. Chem. 271, 12661-12668.
74. Piccardo, P., Dlouhy, S. R., Lievens, P. M., Young, K., Bird, T. D., Nochlin, D., Dickson, D. W., Vinters, H. V., Zimmerman, T. R., Mackenzie, I. R. et al. (1998). Phenotypic variability of Gerstmann-Sträussler-Scheinker disease is associated with prion protein heterogeneity. J. Neuropathol. Exp. Neurol. 57, 979-988.
75. Piccardo, P., Manson, J. C., King, D., Ghetti, B. and Barron, R. M. (2007). Accumulation of prion protein in the brain that is not associated with transmissible disease. Proc. Natl. Acad. Sci. USA 104, 4712-4717.
76. Porto-Carreiro, I., Février, B., Paquet, S., Vilette, D. and Raposo, G. (2005). Prions and exosomes: from PrPc trafficking to PrPsc propagation. Blood Cells Mol. Dis. 35, 143-148.
77. Prusiner, S. B. (1998). Prions. Proc. Natl. Acad. Sci. USA 95, 13363-13383.
78. 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.
79. Resenberger, U. K., Harmeier, A., Woerner, A. C., Goodman, J. L., Müller, V., Krishnan, R., Vabulas, R. M., Kretzschmar, H. A., Lindquist, S., Hartl, F. U. et al. (2011). The cellular prion protein mediates neurotoxic signalling of β-sheet-rich conformers independent of prion replication. EMBO J. 30, 2057-2070.
80. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R. and Wüthrich, K. (1996). NMR structure of the mouse prion protein domain PrP(121-231). Nature 382, 180-182.
81. Riek, R., Hornemann, S., Wider, G., Glockshuber, R. and Wüthrich, K. (1997). NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett. 413, 282-288.
82. Riesner, D. (2003). Biochemistry and structure of PrP(C) and PrP(Sc). Br. Med. Bull. 66, 21-33.
83. Rossetti, G., Cong, X., Caliandro, R., Legname, G. and Carloni, P. (2011). Common structural traits across pathogenic mutants of the human prion protein and their implications for familial prion diseases. J. Mol. Biol. 411, 700-712.
84. Saman, S., Kim, W., Raya, M., Visnick, Y., Miro, S., Saman, S., Jackson, B., McKee, A. C., Alvarez, V. E., Lee, N. C. et al. (2012). Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J. Biol. Chem. 287, 3842-3849.
85. Shen, L. and Ji, H. F. (2011). Mutation directional selection sheds light on prion pathogenesis. Biochem. Biophys. Res. Commun. 410, 159-163.
86. Sofroniew, M. V. and Vinters, H. V. (2010). Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
87. Somogyi, P. and Klausberger, T. (2005). Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 562, 9-26.
88. Sperling, R. A., Laviolette, P. S., O'Keefe, K., O'Brien, J., Rentz, D. M., Pihlajamaki, M., Marshall, G., Hyman, B. T., Selkoe, D. J., Hedden, T. et al. (2009). Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63, 178-188.
89. Spevacek, A. R., Evans, E. G., Miller, J. L., Meyer, H. C., Pelton, J. G. and Millhauser, G. L. (2013). Zinc drives a tertiary fold in the prion protein with familial disease mutation sites at the interface. Structure 21, 236-246.
90. Stahl, N., Borchelt, D. R., Hsiao, K. and Prusiner, S. B. (1987). Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51, 229-240.
91. Steele, A. D., Emsley, J. G., Ozdinler, P. H., Lindquist, S. and Macklis, J. D. (2006). Prion protein (PrPc) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis. Proc. Natl. Acad. Sci. USA 103, 3416-3421.
92. Sulzer, D. and Surmeier, D. J. (2013). Neuronal vulnerability, pathogenesis, and Parkinson's disease. Mov. Disord. 28, 41-50.
93. Taraboulos, A., Raeber, A. J., Borchelt, D. R., Serban, D. and Prusiner, S. B. (1992). Synthesis and trafficking of prion proteins in cultured cells. Mol. Biol. Cell 3, 851-863.
94. Tateishi, J. and Kitamoto, T. (1995). Inherited prion diseases and transmission to rodents. Brain Pathol. 5, 53-59.
95. Tateishi, J., Brown, P., Kitamoto, T., Hoque, Z. M., Roos, R., Wollman, R., Cervenáková, L. and Gajdusek, D. C. (1995). First experimental transmission of fatal familial insomnia. Nature 376, 434-435.
96. Tateishi, J., Kitamoto, T., Hoque, M. Z. and Furukawa, H. (1996). Experimental transmission of Creutzfeldt-Jakob disease and related diseases to rodents. Neurology 46, 532-537.
97. Tebbenkamp, A. T. and Borchelt, D. R. (2010). Analysis of chaperone mRNA expression in the adult mouse brain by meta analysis of the Allen Brain Atlas. PLoS ONE 5, e13675.
98. Thackray, A. M., Knight, R., Haswell, S. J., Bujdoso, R. and Brown, D. R. (2002). Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem. J. 362, 253-258.
99. Turk, E., Teplow, D. B., Hood, L. E. and Prusiner, S. B. (1988). Purification and properties of the cellular and scrapie hamster prion proteins. Eur. J. Biochem. 176, 21-30.
100. van der Kamp, M. W. and Daggett, V. (2009). The consequences of pathogenic mutations to the human prion protein. Protein Eng. Des. Sel. 22, 461-468.
101. Vella, L. J., Sharples, R. A., Lawson, V. A., Masters, C. L., Cappai, R. and Hill, A. F. (2007). Packaging of prions into exosomes is associated with a novel pathway of PrP processing. J. Pathol. 211, 582-590.
102. Verret, L., Mann, E. O., Hang, G. B., Barth, A. M., Cobos, I., Ho, K., Devidze, N., Masliah, E., Kreitzer, A. C., Mody, I. et al. (2012). Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149, 708-721.
103. Watase, K., Weeber, E. J., Xu, B., Antalffy, B., Yuva-Paylor, L., Hashimoto, K., Kano, M., Atkinson, R., Sun, Y., Armstrong, D. L. et al. (2002). A long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 34, 905-919.
104. Watt, N. T., Taylor, D. R., Kerrigan, T. L., Griffiths, H. H., Rushworth, J. V., Whitehouse, I. J. and Hooper, N. M. (2012). Prion protein facilitates uptake of zinc into neuronal cells. Nat Commun 3, 1134.
105. Watts, J. C., Giles, K., Stöhr, J., Oehler, A., Bhardwaj, S., Grillo, S. K., Patel, S., DeArmond, S. J. and Prusiner, S. B. (2012). Spontaneous generation of rapidly transmissible prions in transgenic mice expressing wild-type bank vole prion protein. Proc. Natl. Acad. Sci. USA 109, 3498-3503.
106. Weise, J., Sandau, R., Schwarting, S., Crome, O., Wrede, A., Schulz-Schaeffer, W., Zerr, I. and Bähr, M. (2006). Deletion of cellular prion protein results in reduced Akt activation, enhanced postischemic caspase-3 activation, and exacerbation of ischemic brain injury. Stroke 37, 1296-1300.
107. Westaway, D., DeArmond, S. J., Cayetano-Canlas, J., Groth, D., Foster, D., Yang, S. L., Torchia, M., Carlson, G. A. and Prusiner, S. B. (1994). Degeneration of skeletal muscle, peripheral nerves, and the central nervous system in transgenic mice overexpressing wild-type prion proteins. Cell 76, 117-129.
108. Wolfe, M. S. (2009). Tau mutations in neurodegenerative diseases. J. Biol. Chem. 284, 6021-6025.
109. Yang, W., Cook, J., Rassbach, B., Lemus, A., DeArmond, S. J. and Mastrianni, J. A. (2009). A New Transgenic Mouse Model of Gerstmann-Straussler- Scheinker Syndrome Caused by the A117V Mutation of PRNP. J. Neurosci. 29, 10072-10080.
110. You, H., Tsutsui, S., Hameed, S., Kannanayakal, T. J., Chen, L., Xia, P., Engbers, J. D., Lipton, S. A., Stys, P. K. and Zamponi, G. W. (2012). Aβ neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. USA 109, 1737-1742.
111. Zoghbi, H. Y. (2000). Spinocerebellar ataxias. Neurobiol. Dis. 7, 523-527.
112. Zou, R. S., Fujioka, H., Guo, J. P., Xiao, X., Shimoji, M., Kong, C., Chen, C., Tasnadi, M., Voma, C., Yuan, J. et al. (2011). Characterization of spontaneously generated prion-like conformers in cultured cells. Aging (Albany, NY Online) 3, 968-984.