Prion protein deposition and abnormal synaptic protein expression in the cerebellum in Creutzfeldt-Jakob disease

Neuroscience

Volumn 97, Issue 4, 2000, Pages 715-726

  Ferrer, I ^a   Puig, B ^a   Blanco, R ^a   Martii E ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Creutzfeldt Jakob disease; PrP; Rab3a; SNAP 25; Synapsin 1; Synaptophysin

Indexed keywords

PRION PROTEIN; SYNAPSIN I; SYNAPTOPHYSIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN;

ARTICLE; CELL FRACTIONATION; CEREBELLUM; CONTROLLED STUDY; CREUTZFELDT JAKOB DISEASE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; NEUROTRANSMISSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL;

AGED; ANTIGENS, SURFACE; CEREBELLAR CORTEX; CEREBELLUM; CREUTZFELDT-JAKOB SYNDROME; FEMALE; HUMANS; MALE; MIDDLE AGED; NERVE TISSUE PROTEINS; NEURONS; PRIONS; PRPC PROTEINS; RAB3A GTP-BINDING PROTEIN; SYNAPSES; SYNAPSINS; SYNTAXIN 1;

EID: 0034109081     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00045-2     Document Type: Article

References (68)

1. Beck E. and Daniel P. M. (1987) Neuropathology of transmissible spongiform encephalopathies. In Prions: Novel Infectious Pathogens Causing Scrapie and Creutzfeldt-Jakob Disease (eds Prusiner S. B. and McKinley M. P.), pp. 3105-3108. Academic, Orlando, FL.
2. Bell J.E., Ironside J.W. Neuropathology of spongiform encephalopathies in humans. Br. med. Bull. 49:1993;738-777.
3. Bennett M.K., Calakos N., Scheller R.H. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science. 257:1992;255-259.
4. Bennett M.K., García-Arrarás J.E., Elferink L.A., Peterson K., Fleming A.M., Hazuka C.D., Scheller R.H. The syntaxin family of vesicular transport receptors. Cell. 74:1993;863-873.
5. Berciano J., Berciano M.T., Polo J.M., Figols J., Ciudad J., Lafarga M. Creutzfeldt-Jakob disease with severe involvement of cerebral white matter and cerebellum. Virchows Arch. A, Pathol. Anat. 417:1990;533-538.
6. Borchelt D.R., Koliatsos V.E., Guarnieri M., Pardo C.A., Sisodia S.S., Price D.L. Rapid anterograde transport of the cellular prion glycoprotein in the peripheral and central nervous system. J. biol. Chem. 269:1994;14711-14714.
7. Brownell B., Oppenheimer D.R. An ataxic form of subacute presenile polioencephalopathy (Creutzfeldt-Jakob disease). J. Neurol. Neurosurg. Psychiat. 28:1965;350-361.
8. Bruce M.E., McBride P.A., Farquhar C.F. Precise targeting of the pathology of the sialoglycoprotein PrP and vacuolar degeneration in mouse scrapie. Neurosci. Lett. 102:1989;1-6.
9. Büeler H., Aguzzi A., Sailer A., Greiner R.A., Autenreid P., Aguet M., Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell. 73:1993;1339-1347.
10. Büeler H., Fisher M., Lanfg Y., Blurthmann H., Lipp H.P., DeArmond S.J., Prusiner S.B., Aguet M., Weissmann C. Normal development and behavior of mice lacking the neuronal surface PrP protein. Nature. 365:1992;577-582.
11. Catsicas S., Larhammar D., Blomquist A., Sanna P.P., Milner R.J., Wilson M.C. Expression of a conserved cell-type-specific protein in nerve terminals coincides with synaptogenesis. Proc. natn. Acad. Sci. U.S.A. 88:1991;785-789.
12. Chou S.M., Payne W.N., Gibbs C.J., Gajdusek D.C. Transmission and scanning electron microscopy of spongiform change in Creutzfeldt-Jakob disease. Brain. 103:1980;885-904.
13. Clinton J., Forsyth C., Royston M.C., Roberts G.W. Synaptic degeneration is the primary neuropathological feature in prion disease: a preliminary study. NeuroReport. 4:1993;65-68.
14. Collinge J., Whittington M.A., Sidle K.C.L., Smith J., Palmer M.S., Clarke A.R., Jeffreys J.G.R. Prion protein is necessary for normal synaptic function. Nature. 370:1994;295-297.
15. DeArmond S.J., Mobley W.C., De Mott D.L., Barry R.A., Beckstead J.H., Prusiner S.B. Changes in the localization of brain prion proteins during scrapie infection. Neurology. 37:1987;1271-1280.
16. DeArmond S.J., Prusiner S.B. Etiology and pathogenesis of prion diseases. Am. J. Path. 146:1995;785-811.
17. DeArmond S. J. and Prusiner S. B. (1997) Prion diseases. In Greenfield's Neuropathology (eds Graham D. I. and Lantos P. L.), Vol. 2, pp. 122-128. Arnold, London.
18. DeCamilli P., Benfenatti P., Valtorta F., Greengard P. The synapsins. A. Rev. cell. Biol. 6:1990;433-460.
19. Edelmann L., Hanson P.I., Chapman E.R., Jahn R. Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic machine. Eur. molec. Biol. Org. J. 4:1995;224-231.
20. Ferrer I., Costa F., Grau Veciana J.M. Creutzfeldt-Jakob disease: a Golgi study. Neuropath. appl. Neurobiol. 7:1981;237-242.
21. Ferrer I., Kulisewski J., Vázquez J., González A., Pineda M. Purkinje cells in degenerative diseases of the cerebellum and its connections: a Golgi study. Clin. Neuropath. 7:1988;237-242.
22. Ferrer I., Rivera R., Blanco R., Martí E. Expression of proteins linked to exocytosis and neurotransmission in Creutzfeldt-Jakob disease. Neurobiol. Dis. 6:1999;92-100.
23. Fischer von Mollard G.F., Mignery G.A., Baumert M., Perin M.S., Hanson T.J., Burger P.M., Jahn R., Südhof T.C. Rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc. natn. Acad. Sci. U.S.A. 87:1990;1988-1992.
24. Fischer von Mollard G.F., Stahl B., Li C., Südhof T.C., Jahn R. Rab proteins in regulated exocytosis. Trends biol. Sci. 19:1994;164-168.
25. Fischer von Mollard G.F., Südhof T.C., Jahn R. A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature. 349:1991;79-81.
26. C) in synaptic boutons of normal hamster hippocampus. C. r. hebd Séanc. Acad. Sci., Paris III. 318:1995;339-344.
27. Fraser H., Dickinson A.G. Targeting of scrapie lesions and spread of the agent via the retino-tectal projection. Brain Res. 346:1985;32-38.
28. Geppert M., Bolshakov A., Siegelbaum S.A., Takei K., De Camilli P., Hammer R.E., Südhof T.C. The role of Rab3a in neurotransmitter release. Nature. 369:1994;493-497.
29. Gomori A.J., Partnow M.J., Horoupian D.S., Hirano A. The ataxic form of Creutzfeldt-Jakob disease. Archs Neurol. 29:1973;318-323.
30. Haraguchi T., Fisher S., Olofson S., Endo T., Groth D., Tarentino A., et al. Asparagine-linked glycosylation of the scrapie and cellular prion proteins. Archs Biochem. Biophys. 274:1989;1-13.
31. Herms J.W., Kretzchmar H.A., Tilz S., Keller B.U. Patch-clamp analysis of synaptic transmission to cerebellar Purkinje cells of prion protein knockout mice. Eur. J. Neurosci. 12:1995;2508-2512.
32. Herms J.W., Tings T., Gall S., Madlung A., Giese A., Siebert H., Schürmann P., Windl O., Brose N., Kreutzschmar H. Evidence of presynaptic location and function of the prion protein. J. Neurosci. 15:1999;8866-8875.
33. Hess D.T., Slater T.M., Wilson M.C., Skene J.H.P. The 25kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS. J. Neurosci. 12:1992;4634-4641.
34. Hogan R.N., Baringer J.R., Prusiner S.B. Scrapie infection diminishes spines and increases varicosities of dendrites in hamsters: a quantitative Golgi study. J. Neuropath. exp. Neurol. 46:1987;461-473.
35. Ironside J.W. Review: Creutzfeldt-Jakob disease. Brain Path. 6:1996;379-388.
36. Ironside J. W. and Bell J. E. (1997) Pathology of prion diseases. In Prion Diseases (eds Collinge J. and Palmer M. S.), p. 1996. Oxford University Press, Oxford.
37. Jahn R., Südhof T.C. Synaptic vesicles and exocytosis. A. Rev. Neurosci. 17:1994;219-246.
38. Jeffrey M., Fraser J.R., Halliday W.G., Fowler N., Goodsir C.M., Brown D.A. Early unsuspected neuron and axon terminal loss in scrapie-infected mice revealed by morphometry and immunohistochemistry. Neuropath. appl. Neurobiol. 21:1995;41-49.
39. Jeffrey M., Goodsir C.M., Bruce M.E., McBride P.A., Scott J.R., Halliday W.G. Infection scrapie prion protein (PrP) accumulates on neuronal plasmalemma in scrapie infected mice. Neurosci. Lett. 147:1992;106-109.
40. Jeffrey M., Goodsir C.M., Bruce M.E., McBride P.A., Farquhar C. Morphogenesis of amyloid plaques in 87V murine scrapie. Neuropath. appl. Neurobiol. 20:1994;535-542.
41. Jeffrey M., Halliday W.G. Numbers of neurons in vacuolated and nonvacuolated neuroanatomical nuclei in bovine spongiform encephalopathy-affected brains. J. comp. Path. 110:1994;287-294.
42. Jellinger K., Heiss W.D., Deisenhammer E. The ataxic (cerebellar) form of Creutzfeldt-Jakob disease. J. Neurol. 207:1974;289-305.
43. Jendroska K., Heinzel F.P., Torchia M., Stowring L., Kretzschmar H.A., Kon A., Stern A., Prusiner S.B., DeArmond S.J. Proteinase-resistant prion protein accumulation in Syrian Hamster brain correlates with regional pathology and scrapie infectivity. Neurology. 41:1991;1482-1490.
44. Kitamoto T., Don-ura K., Muramoto T., Niyazono M., Tateishi J. The primary structure of the prion protein influences the distribution of abnormal prion protein. Am. J. Path. 141:1992;271-272.
45. Kitamoto T., Shin R.W., Don-ura K., Tonokane N., Miyazono N., Muramoto T., Tateishi J. Abnormal isoform of prion protein accumulates in the synaptic structures of the central nervous system in patients with Creutzfeldt-Jakob disease. Am. J. Path. 140:1992;1285-1294.
46. Landis D.N.M.D., Williams R.S., Masters C.L. Golgi and electron microscopic studies of spongiform encephalopathies. Neurology. 31:1981;538-549.
47. Lantos P.L. From slow virus to prions: a review of transmissible spongiform encephalopathies. Histopathology. 20:1992;1-11.
48. Li L., Chin L.S., Shupliakov O., Brodin L., Sihra T.S., Hvalby O., Jensen V., Zheng D., McNamara J.O., Greengard P., Andersen P. Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin 1-deficient mice. Proc. natn. Acad. Sci. U.S.A. 92:1995;9235-9239.
49. Liberski P., Yanigahira R., Asher D.M., Gibbs C.J., Gajdusek D.C. Reevaluation of the ultrastructural pathology of experimental Creutzfeldt-Jakob disease. Brain. 113:1990;121-137.
50. Lledó P.M., Johannes L., Vernier P., Zorec R., Darchen F., Vincent J.D., Henry J.P., Mason W.T. Rab3 proteins: key players in the control of exocytosis. Trends Neurosci. 17:1994;426-432.
51. Lledó P.M., Tremblay P., DeArmond S.J., Prusiner S.B., Nicoll R.A. Mice deficient for prion protein exhibit normal neuronal excitability and synaptic transmission in the hippocampus. Proc. natn. Acad. Sci. U.S.A. 93:1996;2403-2407.
52. Masters C. L. and Gajdusek D. C. (1982) The spectrum of Creutzfeldt-Jakob disease and the virus-induced subacute spongiform encephalopathies. In Advances in Neuropathology (eds Thomas Smith W. and Cavanagh J. B.), Vol. 2, pp. 139-143. Churchill Livingstone, Edinburgh.
53. McMahon H.T., Bolshakov V.Y., Janz R., Hammer R.E., Siegelbaum S.A., Südhof T.C. Synaptophysin, a major synaptic protein, is not essential for neurotrasmitter release. Proc. natn. Acad. Sci. U.S.A. 93:1996;4760-4764.
54. Niemann H., Blasi J., Jahn R. Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol. 4:1994;179-185.
55. Oyler G.A., Higgins G.A., Hart R.A., Battenberg E., Billingsley M., Bloom F.E., Wilson M.C. The identification of a novel synaptosomal-associated protein SNAP-25 differentially expressed by neuronal subpopulations. J. Cell Biol. 109:1989;3039-3052.
56. Palay S.L., Chan-Palay V. Cerebellar Cortex: Cytology and Organization. 1974;Springer, Berlin.
57. Parchi P., Castellani R., Capellari S., Ghetti B., Young K., Chen S.G., Farlow M., Dickson D.W., Sima A.A.F., Trojanowski J.Q., Petersen R.B., Gambetti P. Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann. Neurol. 39:1996;767-778.
58. Pfeffer S.R. Rab GTPases: master regulators of membrane trafficking. Curr. Opin. Cell Biol. 6:1994;522-526.
59. Prusiner S. B. (1997) Cell biology and transgenic models of prion diseases. In Prion Diseases (eds Collinge J. and Palmer M. S.), pp. 130-162. Oxford University Press, Oxford.
60. Prusiner S.B., Groth D., Serban A., Koehler R., Foster D., Torchia M., Burton D., Yang S.L., DeArmond S.J. Ablation of the prion protein (PrP) gene in mice prevents scrapie and facilitates production of anti-PrP antibodies. Proc. natn. Acad. Sci. U.S.A. 90:1993;10608-10612.
61. Rosahl T.W., Gepert M., Spillane D., Herz J., Hammer R.E., Malenka R.C., Südhof T.C. Short-term synaptic plasticity is altered in mice lacking synapsin 1. Cell. 75:1993;661-670.
62. Rosahl T.W., Spillane D., Missler M., Hertz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., Südhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature. 375:1995;488-493.
63. Simons K., Zerial M. Rab proteins and the road maps for intracellular transport. Neuron. 11:1993;789-799.
64. Söllner T., Rothman J.E. Neurotransmission: harnessing fusion machinery at the synapse. Trends Neurosci. 17:1994;344-347.
65. Südhof T.C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 375:1995;645-653.
66. Tobler I., Gaus S.E., Deboer T., Achermann P., Fisher M., Rülicke T., Moser M., Oesh B., McBride P.A., Manson J.C. Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature. 380:1996;639-642.
67. Valtorta F., Benfenatti F., Greengard P. Structure and function of synapsins. J. Cell Biol. 267:1992;7195-7198.
68. Volknandt W. The synaptic vesicles and its targets. Neuroscience. 64:1995;277-300.