Selective presynaptic degeneration in the synaptopathy associated with ME7-induced hippocampal pathology

Neurobiology of Disease

Volumn 35, Issue 1, 2009, Pages 63-74

  Gray, Bryony C ^a   Siskova, Zuzana ^a   Perry, V Hugh ^a   O'Connor, Vincent ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Chronic neurodegeneration; Electron microscopy; ME7 scrapie; Synapse

Indexed keywords

PRION PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN HOMOGENATE; CELL COUNT; CONTROLLED STUDY; DISEASE ASSOCIATION; ELECTRON MICROSCOPY; IN VIVO STUDY; INOCULATION; MOUSE; NERVE DEGENERATION; NEUROPATHY; NONHUMAN; PRESYNAPTIC NERVE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; SCRAPIE AGENT; SYNAPTOPATHY;

ANIMALS; CELL COUNT; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE TISSUE PROTEINS; PHOSPHOPYRUVATE HYDRATASE; PRESYNAPTIC TERMINALS; PRION DISEASES; PRIONS; SCRAPIE; SYNAPSES; TIME FACTORS;

EID: 67349280983     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.04.001     Document Type: Article

References (51)

1. Amaral D., and Lavenex P. Hippocampal neuroanatomy. In: Morris R., Amaral D., Bliss T., and O'Keefe J. (Eds). Hippocampus (2006), Oxford UP
2. Anderson M., Bocharova O.V., Makarava N., Breydo L., Salnikov V.V., and Baskakov I.V. Polymorphism and ultrastructural organization of prion protein amyloid fibrils: an insight from high resolution atomic force microscopy. J. Mol. Biol. 358 (2006) 580-596
3. Belichenko P.V., Brown D., Jeffrey M., and Fraser J.R. Dendritic and synaptic alterations of hippocampal pyramidal neurones in scrapie-infected mice. Neuropathol. Appl. Neurobiol. 26 (2000) 143-149
4. Betmouni S., Perry V.H., and Gordon J.L. Evidence for an early inflammatory response in the central nervous system of mice with scrapie. Neuroscience 74 (1996) 1-5
5. Betmouni S., Clements J.P., and Perry V.H. Vacuolation in murine prion disease: an informative artefact. Curr. Biol. 9 (1999) R677-R679
6. Brown D.R. Mayhem of the multiple mechanisms: modelling neurodegeneration in prion disease. J. Neurochem. 82 (2002) 209-215
7. Burke M.A., Mobley W.C., Cho J., Wiegand S.J., Lindsay R.M., Mufson E.J., and Kordower J.H. Loss of developing cholinergic basal forebrain neurons following excitotoxic lesions of the hippocampus: rescue by neurotrophins. Exp. Neurol. 130 (1994) 178-195
8. Chandra S., Gallardo G., Fernández-Chacón R., Schlüter O.M., and Südhof T.C. Alpha-synuclein co-operates with CSPalpha in preventing neurodegeneration. Cell 123 (2005) 383-396
9. Chiesa R.P., Piccardo P., Dossena S., Nowoslawski L., Roth K.A., Ghetti B., and Harris D.A. Bax deletion prevents neuronal loss but not neurological symptoms in a transgenic model of inherited prion disease. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 238-243
10. Chiti Z., Knutsen O.M., Betmouni S., and Greene J.R. An integrated, temporal study of the behavioural, electrophysiological and neuropathological consequences of murine prion disease. Neurobiol. Dis. 22 (2006) 363-373
11. Collinge J., and Clarke A.R. A general model of prion strains and their pathogenicity. Science 318 (2007) 930-936
12. Cunningham C., Deacon R., Wells H., Boche D., Waters S., Diniz C.P., Scott H., Rawlins J.N., and Perry V.H. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur. J. Neurosci. 17 (2003) 2147-2155
13. Diez M., Groth D., DeArmond S.J., Prusiner S.B., and Hökfelt T. Changes in neuropeptide expression in mice infected with prions. Neurobiol. Aging 28 (2007) 748-765
14. Dron M., Bailly Y., Beringue V., Haeberlé A.M., Griffond B., Risold P.Y., Tovey M.G., Laude H., and Dandoy-Dron F. SCRG1, a potential marker of autophagy in transmissible spongiform encephalopathies. Autophagy 2 (2006) 58-60
15. Ferguson R.E., Carroll H.P., Harris A., Maher E.R., Selby P.J., and Banks R.E. Housekeeping proteins: a preliminary study illustrating some limitations as useful references in protein expression studies. Proteomics 5 (2005) 566-571
16. Fernández-Alfonso T., and Ryan T.A. The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol. 16 (2006) 413-420
17. Fernández-Chacón R., Wölfel M., Nishimune H., Tabares L., Schmitz F., Castellano-Muñoz M., Rosenmund C., Montesinos M.L., Sanes J.R., Schneggenburger R., and Südhof T.C. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 42 (2004) 237-251
18. Ferrer I. Synaptic pathology and cell death in the cerebellum in Creutzfeldt-Jakob disease. Cerebellum 1 (2002) 213-222
19. Frazer H. Diversity in the neuropathology of scrapie-like diseases in animals. Br. Med. Bull. 49 (1993) 792-809
20. Fuhrmann M., Mitteregger G., Kretzschmar H., and Herms J. Dendritic pathology in prion disease starts at the synaptic spine. J. Neurosci. 27 (2007) 6224-6233
21. Gray B.C., Skipp P., O'Connor V., and Perry V.H. Increased expression of glial fibrillary acidic protein fragments and mu-calpain activation within the hippocampus of prion-infected mice. Biochem. Soc. Trans. 34 (2006) 51-54
22. Guenther K., Deacon R.M., Perry V.H., and Rawlins J.N. Early behavioural changes in scrapie-affected mice and the influence of dapsone. Eur. J. Neurosci. 14 (2001) 401-409
23. He L., Lu X.Y., Jolly A.F., Eldridge A.G., Watson S.J., Jackson P.K., Barsh G.S., and Gunn T.M. Spongiform degeneration in mahoganoid mutant mice. Science 299 (2003) 710-712
24. Heynen A.J., Quinian E.M., Bae D.C., and Bear M.F. Bi-directional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron 28 (2000) 527-536
25. Jeffrey M., Fraser J.R., Halliday W.G., Fowler N., Goodsir C.M., and Brown D.A. Early unsuspected neuron and axon terminal loss in scrapie-infected mice revealed by morphometry and immunocytochemistry. Neuropathol. Appl. Neurobiol. 21 (1995) 41-49
26. 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. Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol. Appl. Neurobiol. 26 (2000) 41-54
27. Johnston A.R., Fraser J.R., Jeffrey M., and MacLeod N. Synaptic plasticity in the CA1 area of the hippocampus of scrapie-infected mice. Neurobiol. Dis. 5 (1998) 188-195
28. Leuba G., Savioz A., Vernay A., Carnal B., Kraftsik R., Tardif E., Riederer I., and Riederer B.M. Differential changes in synaptic proteins in the Alzheimer frontal cortex with marked increase in PSD-95 postsynaptic protein. J. Alzheimer's Dis. 15 (2008) 139-151
29. Liberski P.P., Sikorska B., Bratosiewicz-Wasik J., Gajdusek D.C., and Brown P. Neuronal cell death in transmissible spongiform encephalopathies (prion diseases) revisited: from apoptosis to autophagy. Int. J. Biochem. Cell Biol. 36 (2004) 2473-2490
30. Mack T.G., Reiner M., Beirowski B., Mi W., Emanuelli M., Wagner D., Thomson D., Gillingwater T., Court F., Conforti L., Fernando F.S., Tariton A., Andressen C., Addicks K., Magni G., Ribchester R.R., Perry V.H., and Coleman M.P. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4 (2001) 1199-1206
31. Magalhães A.C., Baron G.S., Lee K.S., Steele-Mortimer O., Dorward D., Prado M.A., and Caughey B. Uptake and neuritic transport of scrapie prion protein coincident with infection of neuronal cells. J. Neurosci. 25 (2005) 5207-5211
32. Mallucci G.R., White M.D., Farmer M., Dickinson A., Khatun H., Powell A.D., Brandner S., Jefferys J.G., and Collinge J. Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 53 (2007) 325-335
33. Manson, J.C., Jamieson, E., Baybutt, H., Tuzi, N.L., Barron, R., McConnell, I., Somerville, R., Ironside, J., Will, R., Sy, M.S., Melton, D.W., Hope, J., Bostock, C., 1999. A single amino acid alteration (101L) introduced into murine PrP dramatically alters incubation time of transmissible spongiform encephalopathy. 18:6855-6864.
34. Morris R.J., Parkyn C.J., and Jen A. Traffic of prion protein between different compartments on the neuronal surface, and the propagation of prion disease. FEBS Lett. 580 (2006) 5565-5571
35. Pan K.-M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., Melhorn I., Huang Z., Fletterick R.J., Cohen F.E., and Prusiner S.B. Conversion of α-helices into β-sheet features in the formation of the scrapie prion proteins. Proc. Nat. Acad. Sci. U. S. A. 90 (1993) 10962-10966
36. Pearson H.E., and Thompson T.P. Atrophy and degeneration of ganglion cells in central retina following loss of postsynaptic target neurons in the dorsal lateral geniculate nucleus of the adult cat. Exp. Neurol. 119 (1993) 113-119
37. c on the road: trafficking of the cellular prion protein. J. Neurochem. 88 (2004) 769-781
38. Prusiner S.B. Molecular biology of prion diseases. Science 252 (1991) 1515-1522
39. Reynolds E.S. The use of lead citrate at high pH an electron opaque stain in electron microscopy. J. Cell Biol. 17 (1963) 208-212
40. Rockenstein E., Crews L., and Masliah E. Transgenic animal models of neurodegenerative diseases and their application to treatment development. Adv. Drug Deliv. Rev. 59 (2007) 1093-1102
41. Safroniew M.V., Cooper J.D., Svendsen C.N., Crossman P., Ip N.Y., Lindsay R.M., Zafra F., and Lindholm D. Atrophy but not death of adult cholinergic neurons after ablation of target capacity to produce mRNAs for NGF, BDNF and NT3. J. Neurosci. 13 (1993) 5263-5276
42. Saxena S., and Caroni P. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 83 (2007) 174-191
43. Silveira J.R., Raymond G.J., Hughson A.G., Race R.E., Sim V.L., Hayes S.F., and Caughey B. The most infectious prion protein particles. Nature 437 (2005) 257-261
44. Sikorska B. Mechanisms of neuronal death in transmissible spongiform encephalopathies. Folia Neuropathol. 42 Suppl B (2004) 89-95
45. Sisó S., Puig B., Varea R., Vidal E., Acín C., Prinz M., Montrasio F., Badiola J., Aguzzi A., Pumarola M., and Ferrer I. Abnormal synaptic protein expression and cell death in murine scrapie. Acta Neuropathol. 103 (2002) 615-626
46. Small S.A., Wu E.X., Bartsch D., Perera G.M., Lacefield C.O., DeLaPaz R., Mayeux R., Stern Y., and Kandel E.R. Imaging physiologic dysfunction of individual hippocampal subregions in humans and genetically modified mice. Neuron 28 (2000) 653-664
47. Steele A.D., King O.D., Jackson W.S., Hetz C.A., Borkowski A.W., Thielen P., Wollmann R., and Lindquist S. Diminishing apoptosis by deletion of Bax or overexpression of Bcl-2 does not protect against infectious prion toxicity in vivo. J. Neurosci. 27 (2007) 13022-13027
48. Sunyach C., Jen A., Deng J., Fitzgerald K.T., Frobert Y., Grassi J., McCaffrey M.W., and Morris R. The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. EMBO J. 22 (2003) 3591-3601
49. Williams A., Lucassen P.J., Ritchie D., and Bruce M. PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie. Exp. Neurol. 144 (1997) 433-438
50. Wishart T.M., Parson S.H., and Gillingwater T.H. Synaptic vulnerability in neurodegenerative disease. J. Neuropathol. Exp. Neurol. 65 (2006) 733-739
51. Yi J.J., and Ehlers M.D. Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol. Rev. 59 (2007) 14-39