Possible role for Ca2+ in the pathophysiology of the prion protein?

BioFactors

Volumn 37, Issue 3, 2011, Pages 241-249

  Peggion, Caterina ^a   Bertoli, Alessandro ^a   Sorgato, M Catia ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Alzheimer's disease; Ca2+ homeostasis; Prion disease; PrPC

Indexed keywords

CALCIUM ION; PRION PROTEIN; CALCIUM;

ALZHEIMER DISEASE; CALCIUM HOMEOSTASIS; HUMAN; NERVE DEGENERATION; NONHUMAN; PATHOPHYSIOLOGY; PRION DISEASE; PRIORITY JOURNAL; REVIEW; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PRION;

ALZHEIMER DISEASE; ANIMALS; CALCIUM; HUMANS; MODELS, BIOLOGICAL; PRION DISEASES; PRIONS;

EID: 79959519400     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.161     Document Type: Review

References (101)

1. Aguzzi, A. and Calella, A. M. (2009) Prions: protein aggregation and infectious diseases. Physiol. Rev. 89, 1105-1152.
2. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144.
3. Wüthrich, K. and Riek, R. (2001) Three-dimensional structures of prion proteins. Adv. Protein Chem. 57, 55-82.
4. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. USA 95, 13363-13383.
5. Büeler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H. P., DeArmond, S. J., Prusiner, S. B., Aguet, M., and Weissmann, C. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582.
6. Manson, J. C., Clarke, A. R., Hooper, M. L., Aitchison, L., McConnell, I., and Hope, J. (1994) 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 8, 121-127.
7. Mallucci, G. R., Ratte, S., Asante, E. A., Linehan, J., Gowland, I., Jefferys, J. G., and Collinge, J. (2002) Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21, 202-210.
8. Büeler, H., Aguzzi, A., Sailer, A., Greiner, R. A., Autenried, P., Aguet, M., and Weissmann, C. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347.
9. Criado, J. R., Sanchez-Alavez, M., Conti, B., Giacchino, J. L., Wills, D. N., Henriksen, S. J., Race, R., Manson, J. C., Chesebro, B., and Oldstone, M. B. (2005) Mice devoid of prion protein have cognitive deficits that are rescued by reconstitution of PrP in neurons. Neurobiol. Dis. 19, 255-265.
10. Nazor, K. E., Seward, T., and Telling, G. C. (2007) Motor behavioral and neuropathological deficits in mice deficient for normal prion protein expression. Biochim. Biophys. Acta 1772, 645-653.
11. Zhang, C. C., Steele, A. D., Lindquist, S., and Lodish, H. F. (2006) Prion protein is expressed on long-term repopulating hematopoietic stem cells and is important for their self-renewal. Proc. Natl. Acad. Sci. USA 103, 2184-2189.
12. Stella, R., Massimino, M. L., Sandri, M., Sorgato, M. C., and Bertoli, A. (2010) Cellular prion protein promotes regeneration of adult muscle tissue. Mol. Cell. Biol. 30, 4864-4876.
13. Aguzzi, A., Baumann, F., and Bremer, J. (2008) The prion's elusive reason for being. Annu. Rev. Neurosci. 31, 439-477.
14. 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.
15. Sorgato, M. C., Peggion, C., and Bertoli, A. (2009) Is, indeed, the prion protein a Harlequin servant of "many" masters? Prion 3, 202-205.
16. Mattson, M. P. (2007) Calcium and neurodegeneration. Aging Cell 6, 337-350.
17. Kristensson, K., Feuerstein, B., Taraboulos, A., Hyun, W. C., Prusiner, S. B., and DeArmond, S. J. (1993) Scrapie prions alter receptor-mediated calcium responses in cultured cells. Neurology 43, 2335-2341.
18. Wong, K., Qiu, Y., Hyun, W., Nixon, R., VanCleff, J., Sanchez-Salazar, J., Prusiner, S. B., and DeArmond, S. J. (1996) Decreased receptor-mediated calcium response in prion-infected cells correlates with decreased membrane fluidity and IP3 release. Neurology 47, 741-750.
19. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O., and Tagliavini, F. (1993) Neurotoxicity of a prion protein fragment. Nature 362, 543-546.
20. Florio, T., Thellung, S., Amico, C., Robello, M., Salmona, M., Bugiani, O., Tagliavini, F., Forloni, G., and Schettini, G. (1998) Prion protein fragment 106-126 induces apoptotic cell death and impairment of L-type voltage-sensitive calcium channel activity in the GH3 cell line. J. Neurosci. Res. 54, 341-352.
21. Thellung, S., Florio, T., Villa, V., Corsaro, A., Arena, S., Amico, C., Robello, M., Salmona, M., Forloni, G., Bugiani, O., Tagliavini, F., and Schettini, G. (2000) Apoptotic cell death and impairment of L-type voltage-sensitive calcium channel activity in rat cerebellar granule cells treated with the prion protein fragment 106-126. Neurobiol. Dis. 7, 299-309.
22. Thellung, S., Florio, T., Corsaro, A., Arena, S., Merlino, M., Salmona, M., Tagliavini, F., Bugiani, O., Forloni, G., and Schettini, G. (2000) Intracellular mechanisms mediating the neuronal death and astrogliosis induced by the prion protein fragment 106-126. Int. J. Dev. Neurosci. 18, 481-492.
23. Sandberg, M. K., Wallén, P., Wikström, M. A., and Kristensson, K. (2004) Scrapie-infected GT1-1 cells show impaired function of voltage-gated N-type calcium channels (Ca(v) 2.2) which is ameliorated by quinacrine treatment. Neurobiol. Dis. 15, 143-151.
24. Johnston, A. R., Black, C., Fraser, J., and MacLeod, N. (1997) Scrapie infection alters the membrane and synaptic properties of mouse hippocampal CA1 pyramidal neurons. J. Physiol. 500, 1-15.
25. Johnston, A. R., Fraser, J. R., Jeffrey, M., and MacLeod, N. (1998) Alterations in potassium currents may trigger neurodegeneration in murine scrapie. Exp. Neurol. 151, 326-333.
26. Johnston, A. R., Fraser, J. R., Jeffrey, M., and MacLeod, N. (1998) Synaptic plasticity in the CA1 area of the hippocampus of scrapie-infected mice. Neurobiol. Dis. 5, 188-195.
27. Barrow, P. A., Holmgren, C. D., Tapper, A. J., and Jefferys, J. G. (1999) Intrinsic physiological and morphological properties of principal cells of the hippocampus and neocortex in hamsters infected with scrapie. Neurobiol. Dis. 6, 406-423.
28. Cunningham, C., Deacon, R., Wells, H., Boche, D., Waters, S., Diniz, C. P., Scott, H., Rawlins, J. N., and Perry, V. H. (2003) Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur. J. Neurosci. 17, 2147-2155.
29. Chiti, Z., Knutsen, O. M., Betmouni, S., and Greene, J. R. (2006) An integrated, temporal study of the behavioural, electrophysiological and neuropathological consequences of murine prion disease. Neurobiol. Dis. 22, 363-373.
30. Mallucci, G. R., White, M. D., Farmer, M., Dickinson, A., Khatun, H., Powell, A. D., Brandner, S., Jefferys, J. G., and Collinge, J. (2007) Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 53, 325-335.
31. Kourie, J. I., Culverson, A. L., Farrelly, P. V., Henry, C. L., and Laohachai, K. N. (2002) Heterogeneous amyloid-formed ion channels as a common cytotoxic mechanism: implications for therapeutic strategies against amyloidosis. Cell Biochem. Biophys. 36, 191-207.
32. Kagan, B. L., Azimov, R., and Azimova, R. (2004) Amyloid peptide channels. J. Membr. Biol. 202, 1-10.
33. Demuro, A., Mina, E., Kayed, R., Milton, S. C., Parker, I., and Glabe, C. G. (2005) Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 280, 17294-17300.
34. Lin, M. C., Mirzabekov, T., and Kagan, B. L. (1997) Channel formation by a neurotoxic prion protein fragment. J. Biol. Chem. 272, 44-47.
35. Kawahara, M., Kuroda, Y., Arispe, N., and Rojas, E. (2000) Alzheimer's beta-amyloid, human islet amylin, and prion protein fragment evoke intracellular free calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell line. J. Biol. Chem. 275, 14077-14083.
36. Kourie, J. I. and Culverson, A. (2000) Prion peptide fragment PrP[106-126] forms distinct cation channel types. J. Neurosci. Res. 62, 120-133.
37. Bahadi, R., Farrelly, P. V., Kenna, B. L., Kourie, J. I., Tagliavini, F., Forloni, G., and Salmona, M. (2003) Channels formed with a mutant prion protein PrP(82-146) homologous to a 7-kDa fragment in diseased brain of GSS patients. Am. J. Physiol. Cell Physiol. 285, C862-C872.
38. Alier, K., Li, Z., Mactavish, D., Westaway, D., and Jhamandas, J. H. (2010) Ionic mechanisms of action of prion protein fragment PrP(106-126) in rat basal forebrain neurons. J. Neurosci. Res. 88, 2217-2227.
39. Zou, W. Q. and Gambetti, P. (2007) Prion: the chameleon protein. Cell. Mol. Life Sci. 64, 3266-3270.
40. Malenka, R. C. and Bear, M. F. (2004) LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
41. Jin, J. K., Choi, J. K., Lee, H. G., Kim, Y. S., Carp, R. I., and Choi, E. K. (1999) Increased expression of CaM kinase II alpha in the brains of scrapie-infected mice. Neurosci. Lett. 273, 37-40.
42. Khosravani, H., Zhang, Y., Tsutsui, S., Hameed, S., Altier, C., Hamid, J., Chen, L., Villemaire, M., Ali, Z., Jirik, F. R., and Zamponi, G. W. (2008) Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. J. Cell Biol. 181, 551-565.
43. Hetz, C., Russelakis-Carneiro, M., Maundrell, K., Castilla, J., and Soto, C. (2003) Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J. 22, 5435-5445.
44. Ferreiro, E., Resende, R., Costa, R., Oliveira, C. R., and Pereira, C. M. (2006) An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-beta peptides neurotoxicity. Neurobiol. Dis. 23, 669-678.
45. Ferreiro, E., Costa, R., Marques, S., Cardoso, S. M., Oliveira, C. R., and Pereira, C. M. (2008) Involvement of mitochondria in endoplasmic reticulum stress-induced apoptotic cell death pathway triggered by the prion peptide PrP(106-126). J. Neurochem. 104, 766-776.
46. Ferreiro, E., Oliveira, C. R., and Pereira, C. M. (2008) The release of calcium from the endoplasmic reticulum induced by amyloid-beta and prion peptides activates the mitochondrial apoptotic pathway. Neurobiol. Dis. 30, 331-342.
47. Torres, M., Castillo, K., Armisén, R., Stutzin, A., Soto, C., and Hetz, C. (2010) Prion protein misfolding affects calcium homeostasis and sensitizes cells to endoplasmic reticulum stress. PLoS One 5, e15658.
48. Mukherjee, A., Morales-Scheihing, D., Gonzalez-Romero, D., Green, K., Taglialatela, G., and Soto, C. (2010) Calcineurin inhibition at the clinical phase of prion disease reduces neurodegeneration, improves behavioral alterations and increases animal survival. PLoS Pathog. 6, e1001138.
49. Jeffrey, M., Halliday, W. G., Bell, J., Johnston, A. R., MacLeod, N. K., Ingham, C., Sayers, A. R., Brown, D. A., and Fraser, J. R. (2000) Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol. Appl. Neurobiol. 26, 41-54.
50. Collinge, J., Whittington, M. A., Sidle, K. C., Smith, C. J., Palmer, M. S., Clarke, A. R., and Jefferys, J. G. (1994) Prion protein is necessary for normal synaptic function. Nature 370, 295-297.
51. Whittington, M. A., Sidle, K. C., Gowland, I., Meads, J., Hill, A. F., Palmer, M. S., Jefferys, J. G., and Collinge, J. (1995) Rescue of neurophysiological phenotype seen in PrP null mice by transgene encoding human prion protein. Nat. Genet. 9, 197-201.
52. Manson, J. C., Hope, J., Clarke, A. R., Johnston, A., Black, C., and MacLeod, N. (1995) PrP gene dosage and long term potentiation. Neurodegeneration 4, 113-115.
53. Lledo, P. M., Tremblay, P., DeArmond, S. J., Prusiner, S. B., and Nicoll, R. A. (1996) Mice deficient for prion protein exhibit normal neuronal excitability and synaptic transmission in the hippocampus. Proc. Natl. Acad. Sci. USA 93, 2403-2407.
54. Herms, J. W., Kretzchmar, H. A., Titz, S., and Keller, B.U (1995) Patch-clamp analysis of synaptic transmission to cerebellar purkinje cells of prion protein knockout mice. Eur. J. Neurosci. 7, 2508-2512.
55. Nguyen, P. V., Duffy, S. N., and Young, J. Z. (2000) Differential maintenance and frequency-dependent tuning of LTP at hippocampal synapses of specific strains of inbred mice. J. Neurophysiol. 84 2484-2493.
56. Steele, A. D., Lindquist, S., and Aguzzi, A. (2007) The prion protein knockout mouse: a phenotype under challenge. Prion 1, 83-93.
57. Curtis, J., Errington, M., Bliss, T., Voss, K., and MacLeod, N. (2003) Age-dependent loss of PTP and LTP in the hippocampus of PrP-null mice. Neurobiol. Dis. 13, 55-62.
58. Prestori, F., Rossi, P., Bearzatto, B., Lainé, J., Necchi, D., Diwakar, S., Schiffmann, S. N., Axelrad, H., and D'Angelo, E. (2008) Altered neuron excitability and synaptic plasticity in the cerebellar granular layer of juvenile prion protein knock-out mice with impaired motor control. J. Neurosci. 28, 7091-7103.
59. Colling, S. B., Collinge, J., and Jefferys, J. G. (1996) Hippocampal slices from prion protein null mice: disrupted Ca(2+)-activated K+ currents. Neurosci. Lett. 209, 49-52.
60. Asante, E. A., Li, Y. G., Gowland, I., Jefferys, J. G., and Collinge, J. (2004) Pathogenic human prion protein rescues PrP null phenotype in transgenic mice. Neurosci. Lett. 360, 33-36.
61. 2+ homeostasis in hippocampal CA1 neurons. J. Neurochem. 98, 1876-1885.
62. 2+-buffering in prion-null mice: association with reduced afterhyperpolarizations in CA1 hippocampal neurons. J. Neurosci. 28, 3877-3886.
63. Sah, P. and Davies, P. (2000) Calcium-activated potassium currents in mammalian neurons. Clin. Exp. Pharmacol. Physiol. 27, 657-663.
64. 2+-activated K+ currents in cerebellar purkinje cells. Neurobiol. Dis. 8, 324-330.
65. Zamponi, G. W. and Stys, P. K. (2009) Role of prions in neuroprotection and neurodegeneration: a mechanism involving glutamate receptors? Prion 3, 187-189.
66. Rangel, A., Burgaya, F., Gavín, R., Soriano, E., Aguzzi, A., and Del Río, J. A. (2007) Enhanced susceptibility of Prnp-deficient mice to kainate-induced seizures, neuronal apoptosis, and death: role of AMPA/kainate receptors. J. Neurosci. Res. 85, 2741-2755.
67. Walz, R., Amaral, O. B., Rockenbach, I. C., Roesler, R., Izquierdo, I., Cavalheiro, E. A., Martins, V. R., and Brentani, R. R. (1999) Increased sensitivity to seizures in mice lacking cellular prion protein. Epilepsia 40, 1679-1682.
68. Spudich, A., Frigg, R., Kilic, E., Kilic, U., Oesch, B., Raeber, A., Bassetti, C. L., and Hermann, D. M. (2005) Aggravation of ischemic brain injury by prion protein deficiency: role of ERK-1/-2 and STAT-1. Neurobiol. Dis. 20, 442-449.
69. 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.
70. Mattson, M. P., LaFerla, F. M., Chan, S. L., Leissring, M. A., Shepel, P. N., and Geiger, J. D. (2000) Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23, 222-229.
71. Brini, M. (2003) Ca(2+) signalling in mitochondria: mechanism and role in physiology and pathology. Cell Calcium 34, 399-405.
72. Jouaville, L. S., Pinton, P., Bastianutto, C., Rutter, G. A., and Rizzuto, R. (1999) Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. USA 96, 13807-13812.
73. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.
74. Bernardi, P. (1999) Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 79, 1127-1155.
75. Brini, M., Miuzzo, M., Pierobon, N., Negro, A., and Sorgato, M. C. (2005) The prion protein and its paralogue Doppel affect calcium signaling in Chinese hamster ovary cells. Mol. Biol. Cell 16, 2799-2808.
76. 2+ movements in cerebellar granule neurons. J. Neurochem. 116, 881-890.
77. Beraldo, F. H., Arantes, C. P., Santos, T. G., Machado, C. F., Roffe, M., Hajj, G. N., Lee, K. S., Magalhães, A. C., Caetano, F. A., Mancini, G. L., Lopes, M. H., Américo, T. A., Magdesian, M. H., Ferguson, S. S., Linden, R., Prado, M. A., and Martins, V. R. (2011) Metabotropic glutamate receptors transduce signals for neurite outgrowth after binding of the prion protein to laminin γ1 chain. FASEB J. 25, 265-279.
78. Zanata, S. M., Lopes, M. H., Mercadante, A. F., Hajj, G. N., Chiarini, L. B., Nomizo, R., Freitas, A. R., Cabral, A. L., Lee, K. S., Juliano, M. A., de Oliveira, E., Jachieri, S. G., Burlingame, A., Huang, L., Linden, R., Brentani, R. R., and Martins, V. R. (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21, 3307-3316.
79. Lopes, M. H., Hajj, G. N., Muras, A. G., Mancini, G. L., Castro, R. M., Ribeiro, K. C., Brentani, R. R., Linden, R., and Martins, V. R. (2005) Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J. Neurosci. 25, 11330-11339.
80. Beraldo, F.H., Arantes, C. P., Santos, T. G., Queiroz, N. G., Young, K., Rylett, R. J., Markus, R. P., Prado, M. A., and Martins, V. R. (2010) Role of alpha7 nicotinic acetylcholine receptor in calcium signaling induced by prion protein interaction with stress-inducible protein 1. J. Biol. Chem. 285, 36542-36550.
81. Ramljak, S., Asif, A. R., Armstrong, V. W., Wrede, A., Groschup, M. H., Buschmann, A., Schulz-Schaeffer, W., Bodemer, W., and Zerr, I. (2008) Physiological role of the cellular prion protein (PrPc): protein profiling study in two cell culture systems. J. Proteome Res. 2008 7, 2681-2695.
82. Weiss, E., Ramljak, S., Asif, A. R., Ciesielczyk, B., Schmitz, M., Gawinecka, J., Schulz-Schaeffer, W., Behrens, C., and Zerr, I. (2010) Cellular prion protein overexpression disturbs cellular homeostasis in SH-SY5Y neuroblastoma cells but does not alter p53 expression: a proteomic study. Neuroscience 169, 1640-1650.
83. Liang, J., Luo, G., Ning, X., Shi, Y., Zhai, H., Sun, S., Jin, H., Liu, Z., Zhang, F., Lu, Y., Zhao, Y., Chen, X., Zhang, H., Guo, X., Wu, K., and Fan, D. (2007) Differential expression of calcium-related genes in gastric cancer cells transfected with cellular prion protein. Biochem. Cell Biol. 85, 375-383.
84. Lesné, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., Gallagher, M., and Ashe, K. H. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 16, 352-357.
85. Cheng, I. H., Scearce-Levie, K., Legleiter, J., Palop, J. J., Gerstein, H., Bien-Ly, N., Puoliväli, J., Lesné, S., Ashe, K. H., Muchowski, P. J., and Mucke, L. (2007) Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J. Biol. Chem. 17, 23818-23828.
86. Zheng, H. and Koo, E. H. (2006) The amyloid precursor protein: beyond amyloid. Mol. Neurodegener. 3, 1-5.
87. Walsh, D. M. and Selkoe, D. J. (2007) Abeta oligomers-a decade of discovery. J. Neurochem. 101, 1172-1184.
88. Kim, J. H., Anwyl, R., Suh, Y. H., Djamgoz, M. B., and Rowan, M. J. (2001) Use-dependent effects of amyloidogenic fragments of (beta)-amyloid precursor protein on synaptic plasticity in rat hippocampus in vivo. J. Neurosci. 15, 1327-1333.
89. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 4, 535-539.
90. Wang, H. W., Pasternak, J. F., Kuo, H., Ristic, H., Lambert, M. P., Chromy, B., Viola, K. L., Klein, W. L., Stine, W. B., Krafft, G. A., and Trommer, B. L. (2002) Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res. 11, 133-140.
91. Oddo, S., Caccamo, A., Shepherd, J. D., Murphy, M. P., Golde, T. E., Kayed, R., Metherate, R., Mattson, M. P., Akbari, Y., and LaFerla, F. M. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 31, 409-421
92. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842.
93. Li, S., Hong, S., Shepardson, N. E., Walsh, D. M., Shankar, G. M., and Selkoe, D. (2009) Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 25, 788-801.
94. Berridge, M. J. (2010) Calcium hypothesis of Alzheimer's disease. Pflugers Arch. 459, 441-449.
95. Voigtländer, T., Klöppel, S., Birner, P., Jarius, C., Flicker, H., Verghese-Nikolakaki, S., Sklaviadis, T., Guentchev, M., and Budka, H. (2001) Marked increase of neuronal prion protein immunoreactivity in Alzheimer's disease and human prion diseases. Acta Neuropathol. 101, 417-423.
96. Riemenschneider, M., Klopp, N., Xiang, W., Wagenpfeil, S., Vollmert, C., Müller, U., Förstl, H., Illig, T., Kretzschmar, H., and Kurz, A. (2004) Prion protein codon 129 polymorphism and risk of Alzheimer disease. Neurology 27, 364-366.
97. 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 amyloid-beta oligomers. Nature 26, 1128-1132.
98. Gimbel, D. A., Nygaard, H. B., Coffey, E. E., Gunther, E. C., Laurén, J., Gimbel, Z. A., and Strittmatter, S. M. (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J. Neurosci. 5, 6367-6374.
99. Balducci, C., Beeg, M., Stravalaci, M., Bastone, A., Sclip, A., Biasini, E., Tapella, L., Colombo, L., Manzoni, C., Borsello, T., Chiesa, R., Gobbi, M., Salmona, M., and Forloni, G. (2010) Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc. Natl. Acad. Sci. USA 2, 2295-2300.
100. 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.
101. Kessels, H. W., Nguyen, L. N., Nabavi, S., and Malinow, R. (2010) The prion protein as a receptor for amyloid-beta. Nature 12, E3-E4.